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September 2012

September 2012

Authors:

Kalpa Wishvajith Samarakoon

General Sir John Kotelawala Defence University

You-Jin Jeon

Jeju National University

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Review

Bio-functionalities of proteins derived from marine algae —A review

Kalpa Samarakoon

, You-Jin Jeon

a,b,

⁎

School of Marine Biomedical Sciences, Jeju National University, Jeju 690-756, Republic of Korea

Marine and Environmental Research Institute, Jeju National University, Hamdok, Jeju 695-814, Republic of Korea

abstractarticle info

Article history:

Received 17 January 2012

Accepted 18 March 2012

Keywords:

Proteolytic enzymes

Enzymatic extractions

Bioactive peptides

Health effects

Marine algae are a diverse group of organisms that have been targeted to ﬁgure out their secondary

metabolites and broad spectrum of natural bioactivities for beneﬁcial health effects in many decades.

Recently, increasing attention has been paid on the pronouncement of bio-functional proteins and some

peptides from marine macro and microalgae. Interestingly, many marine algal peptides possess speciﬁc

biological properties due to these potential components having health-promoting effects. Therefore, this

review will provide an overview on the protein-based research literatures from marine algae with the

conditions of gaining access to peptides from parent proteins by proteolytic enzymes or fermentations.

Moreover, this covers most of the proteins and protein derivatives including peptides with the range from di-

peptides to poly-peptides. Speciﬁc bioactivities, including antioxidative, antihypertensive, anticoagulative,

antitumor and immune-stimulative properties are also discussed. In this review, identiﬁed bioactivities and

potentialities of marine algal protein sources will be discussed for future pharmaceutical, nutraceutical and

cosmeceutical applications.

Contents

1. Introduction .............................................................. 948

2. Isolation and puriﬁcation of bioactive peptides from marine algae proteins ................................. 949

3. Pharmacological values of algal proteins and applications ......................................... 950

3.1. Antioxidative activity ...................................................... 950

3.2. Antihypertensive activity ..................................................... 953

3.3. Anticoagulant activity ...................................................... 954

3.4. Antiproliferation activity ..................................................... 955

3.5. Immune-stimulant activity .................................................... 956

4. Nutritional values of algal proteins and applications ........................................... 956

5. Cosmeceutical values of algal proteins and applications .......................................... 957

6. Conclusion ............................................................... 958

References ................................................................. 958

1. Introduction

Nowadays, there is a huge interest on natural products obtained

from marine organisms that can promote the state of health and well-

being for humans and other animals. Thus, the large and structurally

diverse array of marine-derived natural resources exist in the ocean

(Aneiros & Garateix, 2004), and they can be described as the largest

remained reservoir of secondary metabolites to evaluate for the

future therapeutic needs. In fact, macro and microalgae are a diverse

group of photosynthetic marine organisms that have adapted to

survive in highly complex and competitive environments, including

extreme salinity levels, temperature variations, low light intensities

and nutrient deﬁcient habitats (Plaza, Cifuentes, & Ibanez, 2008).

Interestingly, marine algae play a major role by being primary

producers in the ocean, since other marine organisms might be

relying on algae to acquire their energy requirements along the food

web. Therefore, it is logical to consider that algae could be a key,

bearing rich source of secondary metabolites, including functional

Food Research International 48 (2012) 948–960

⁎Corresponding author at: School of Marine Biomedical Sciences, Jeju National

University, Jeju 690-756, Republic of Korea. Tel.: +82 64 754 3475; fax: + 82 64 756

3493.

E-mail addresses: kalpa_samarakoon@yahoo.com (K. Samarakoon),

youjinj@jejunu.ac.kr (Y.-J. Jeon).

doi:10.1016/j.foodres.2012.03.013

Contents lists available at SciVerse ScienceDirect

Food Research International

journal homepage: www.elsevier.com/locate/foodres

nutrients and associated bioactive peptides, than other marine

organisms. Indeed, algae could be a natural source with prominent

biological activities, and it is gaining an interest for many scientists.

Besides, a great deal of attraction also has risen when chasing along

the novel bioactive peptides with respect to their health effects (Kim

& Wijesekara, 2010). Taken together, a vast array of exploration has

been focused on marine algae to ﬁnd new functional ingredients.

Macroalgae or “seaweeds,”which are multicellular organisms

with a great diversity of forms and sizes, and can be classiﬁed into three

broad groups based on their pigmentation, such as brown seaweed

(Phaeophyceae), red seaweed (Rhodophyceae) and green seaweed

(Chlorophyceae). In contrast to macroalgae, microalgae are microscopic

organisms and can be classiﬁed into blue-green algae (Cyanobateria),

diatoms (Bacillariophyta) and dinoﬂagellates (Dinophyceae). More-

over, these fascinating species are commonly identiﬁed as phytoplank-

ton in the ocean water, and also being identiﬁed as primary producers

(Garson, 1989). Furthermore, microalgae have been recognized as

particular marine sources that bear some interesting and untapped

bioactive constituents.

Bio-functionalities or bioactivities of peptides have been described

as mimic hormones, or showing drug like activities. In addition, they

could alter the physiological functions or raise a positive impact

through binding to speciﬁc receptors and interact on target cells or

inhibition by enzyme actions (FitzGerald & Murray, 2007; Kitts &

Weiler, 2003). Some algae species have induced biological activities,

which are associated with proteins, protein hydrolysates or peptides,

that can affect their standing beyond their nutritional values as

antioxidant (Karavita et al., 2007; Kim et al., 2006), antihypertensive

(FitzGerald & Murray, 2007), immune-modulatory (Morris et al.,

2007), anticancer (Sheih, Fang, Wu, & Lin, 2010), hepeto-protective

(Hwang, Kim, & Nam, 2008; Kang, Qian, Ryu, Kim, & Kim, 2012) and

anticoagulant (Athukorala & Jeon, 2005). These bioactivities would be

an added advantage to gain access to their multifunctional applica-

tions, including functional foods or nutraceuticals (Chacón-Lee &

Gonzalez-Mảriño, 2010; Guil-Guerrero, Navaro-Juarez, Lopez-

Martinez, Campara-Madrid, & Rebolloso-Fuentes, 2004; Mohamed,

Hashim, & Rahman, 2012), pharmaceuticals (Dominic & Danquah,

2011), and cosmeceuticals (Sekar & Chandramohan, 2008; Stolz &

Obermayer, 2005).

Therefore, this review discusses the overview of recent trends in

isolation and characterization of functional proteins, bioactive

peptides, signiﬁcant amino acids and amino acid-like components

from marine macro and microalgae. Moreover, comprehensive

analyses of algal protein hydrolysates and bioactive peptides have

been taking part in recent pharmacological, nutraceutical and

comeceutical aspects. However, there is a challenge to ﬁnd out a

platform for the future therapeutic needs from bioactive peptides,

and a need to make a better improvement by establishing a new

generation of therapeutic agents (Pauline, Joannis-Cassan, Elie, &

Arsene, 2006). Furthermore, these would serve humanity and

prospective organisms for its comprehensive health beneﬁts.

2. Isolation and puriﬁcation of bioactive peptides from marine

algae proteins

Recently, endogenous marine peptides have opened new scenario

in advance to develop pharmaceutical agents (Kim & Wijesekara,

2010). Therefore, there has been a growing demand to isolate new

functional proteins or bioactive peptides from marine algae (Harnedy

& FitzGerald, 2011). Over the years, biological activities of enzymatic

extracts from marine algae were considered signiﬁcantly. Bioactivities

of the proteolytic enzyme extracts are based on their inherent amino

acid compositions and sequences, and it may vary from two to twenty

amino acid constituents, accordingly (Meisel & FitzGerald, 2003).

Besides, some particular interests have been seen on the marine algal

peptides due to its speciﬁchealthbeneﬁts (Harnedy & FitzGerald,

2011). To explore the potentiality of bioactive resources and the nature

of the chemical constituents, method of separation, isolation and

characterization techniques have been determined. However, the

isolation of biological active components from the enzymatic extracts

was given high yield and much purity compared to the organic solvent

extractions. Therefore, high yields and enormous bioactivities from

enzyme-assisted extractions (EAEs) have received more attention than

the organic extracts and its counterparts (Heo, Park, Lee, & Jeon, 2005).

Recently, a few studies have been reported respect to the organic

solvent extractions due to the experience of remaining toxic residues

with the target compounds.

Therefore, explorations of potential bioactive peptides by acces-

sing algae proteins are described by the initiation of proteolytic

enzyme-assisted extractions (PEAEs) (see Fig. 1). Access into the

inner cellular materials of the marine algae is facilitated by cell wall

broken down enzymes (Cellulase), considered as a worthy and a

highly sophisticated technique. On the other hand, the use of

mechanical techniques such as ultra sound sonication and pulverizing

the lyophilized materials by grinding might also be helpful. Basically,

bioactive peptides can be obtained from inner food-protein sources

by three ways, (i) hydrolysis by digestive enzymes from animals

(ii) hydrolysis by proteolytic enzymes, harvested by microorganisms

or plants and (iii) hydrolysis by proteolytic microorganisms during

fermentation (Korhonen & Pihlanto, 2006). Moreover, Table 1 shows

that gastrointestinal enzymes, including pepsin, trypsin and α-

chymotrypsin, have been used more commonly in PEAEs (Heo &

Jeon, 2008; Heo, Jeon, Lee, Kim, & Lee, 2003; Heo, Park, Lee, & Jeon,

2005; Je et al., 2009; Kang, Qian, Ryu, & Kim, 2011). Importantly, the

encrypted bioactive peptides range in sizes from 2 to 20 amino acid

constituents and can be harvested either by each of proteolytic

hydrolysation or serially a combination of them together (Kim &

Wijesekara, 2010).

Moreover, adjusting the physico-chemical conditions for proteo-

lytic enzymes such as optimum temperatures and respective pHs in

the protein solutions would be the key factors when hydrolyzing in

vitro (Table 1). Besides, protein hydrolysates may employ further to

fractionate for different distributions of molecular weights by using

ultra-ﬁltration (UF) membranes with the different pore sizes. The

selections of cut-off molecular masses (3 kDa, 5 kDa, 10 kDa and

30 kDa) are determined with the guidance of sodium dodecyl sulfate-

polyacrylamide gel electrophoresis (SDS-PAGE) proﬁle for desired

protein hydrolysates accordingly. In addition, the sequential chro-

matographic techniques (i.e., ion-exchange, gel ﬁltration chromatog-

raphy and reverse-phase high performance liquid chromatography

(RP-HPLC)) also can be utilized for further isolations or puriﬁcations

up to the optimum level (Chabeaud et al., 2009). Furthermore, the

spectrophotometric methodologies such as liquid chromatography–

mass spectrophotometry (LC–MS) and mass–mass spectrophotome-

try (MS–MS) are frequently used to characterize the molecular

structures and molecular masses of bioactive peptides along the

chromatographic steps. Therefore, these systematic approaches are

worthy and limitless while employing serially combined enzymatic

hydrolysis with the microbial fermentations to obtain number of

bioactive peptides from desired protein sources (Dominic & Danquah,

2011). However, the commercialization of bioactive peptides would

become an interesting view for the pharmaceutical industries as new

chemical-entities for lead-compounds or innovative drugs from

marine algae. Therefore, in recent years, the pharmaceutical ﬁrms

have been looking towards the investigation and utilization of new

isolation methodologies under optimized conditions, which are costly

but time efﬁcient rather than the laboratory-scale. The technological

advances in industrial-scale (i.e. combining conventional membrane

ﬁltration with electrophoresis on separating highly charge bioactive

peptides) might be the faster way of separation than chromatography

(Bargeman et al., 2002). In addition, peptide Quantitative Structure–

Activity Relationship (QSAR) modeling information can be used to

949K. Samarakoon, Y.-J. Jeon / Food Research International 48 (2012) 948–960

predict the peptide structures with the ability to cross membrane

barriers in the speciﬁc target sites (Jimsheena & Gowada, 2010).

Furthermore, the improvement of the structures, stabilities and

capacities of the bioactive peptides to binding sites of human model

systems with the incorporation of synthetic peptides needs to be

discussed further.

3. Pharmacological values of algal proteins and applications

3.1. Antioxidative activity

Antioxidants play an important role in the human body by

reducing oxidative reactions. Especially, endogenous antioxidant

enzymes such as superoxide dismutase, catalase, glutathione peroxi-

dase and non-enzymatic antioxidants such as vitamin C, α-tocopherol

and selenium protect internal organs and tissues from oxidative

damage by various toxic reactive oxygen and nitrogen species (Ahn,

Jeon, Kang, Shin, & Jung, 2004). However, imbalances between the

endogenous antioxidants and reactive oxygen species (ROS) lead to

cause serious health issues and disorders such as cancer, cardiovascular

disease, hypertension, diabetes mellitus, inﬂammatory diseases, neu-

rodegenerative diseases and aging (Valko et al., 2007). These disorders

are increasing due to certain conditions such as environment pollutions,

chemicals of smoke, alcohol and high-fat diet.Therefore, researchers are

continually seeking for a good source with potent antioxidant ability as

an alternative for the dietary supplements. In fact, among the marine

fauna and ﬂora, marine algae have considered as a rich source of natural

antioxidants (Ngo, Wijesekara, Vo, Ta, & Kim, 2011). This ﬁnding

strongly suggests that susceptibility of extraordinary environmental

changes in the ocean with low light intensities and high oxygen

concentrations. Especially, rising up of the dissolved oxygen level in the

sea water with intense UV radiations might be possible during the

summer season. In fact, oxygen level can ﬂuctuate in the ocean due to

temperature variations, salinity or nutrient levels and light intensities,

seasonally. However, natural oxygenated environment leads to form

free radicals and other ROS in cells. Thus, marine algae could quench

these effects and protect themselves without having serious photo-

oxidative damages (Guedes, Helena, Amaro, & Malcata, 2011). There-

fore, there might be a potent antioxidative mechanism with necessary

facilitating metabolites for their self-protection. In the past few decades

this has been targeted to screen and isolate a broad spectrum of

secondary metabolites with antioxidant effect. This fact has been

revealed in many marine macro and microalgae research literatures

(Heo, Cha, Lee, Cho, & Jeon, 2005; Heo, Cha, Lee, Lee, & Jeon, 2006; Heo,

Park, Park, Kim, & Jeon, 2005; Karavita et al., 2007; Kim et al., 2006).

Recently, some of the related research works have focused on

antioxidant protein hydrolysates or peptides than the extractions of

organic solvents from marine algae. Moreover, certain sequences of

amino acidswith covalent bonds and associated thermal stabilities have

gained effective antioxidant properties (Sheih, Wu, & Fang, 2009). Even

though, few of studies have carried out to target on bioactive peptides

and some more remaining until being explored (Table 2).

The antioxidant activities of marine macro and microalgae have

been investigated by various in vitro assays, such as DPPH (1,1-

diphenyl-2-pricrylhydrazyl), hydroxyl radical, hydrogen peroxide

and superoxide anion scavenging methods, which have determined

by electron spin resonance (ESR) spectrophotometry method (Ngo et

al., 2011). One of the ﬁrst pronounced antioxidative effects was

revealed from water-soluble, protease enzymatic extracts of seven

species of marine edible brown seaweeds, including Ecklonia cava,

Scytosiphon lomentaria,Ishige okamurae,Sargassum fullvelum,Sargasum

horneri and Sargassum thunbergii around Jeju-Do coasts in South Korea

(Heo, Lee, Song, & Jeon, 2003). Enzymatic extracts of E. cava have

scavenged DPPH free radicals more effectively than other algal extracts.

Marine algae

Cell wall disruption

Mechanical method

e.g. Sonication

Enzymatic method

e.g. Carbohydrase

Dry powder

Freeze drying and pulverization

Expose inner cell material

Hydrolysis by digestive

enzymes from animals

Hydrolysis by Proteolytic enzymes

derived from microorganisms or

plants

Hydrolysis by Proteolytic

microorganisms during

fermentation

Protein hydrolysates

Isolation of target Peptides

Ultra membrane filtration / Ion exchange or

Gel filtration chromatography

Bioactivity guided isolation

Purification

Reverse Phase-HPLC

Determination of amino acid sequence and molecular mass

MS-ESI

Proteolytic hydrolysation

Fig. 1. Schematic diagram for the recovery of bioactive peptides from proteolytic enzyme-assisted extractions (PEAEs) of marine algae (RP-HPLC: reverse-phase high performance

liquid chromatography; MS-ESI: mass spectrometry-electrospray ionization).

950 K. Samarakoon, Y.-J. Jeon / Food Research International 48 (2012) 948–960

Table 1

Proteolytic hydrolysation of marine algae by using various enzymes and their characteristics with optimum conditions.

Enzyme Type of protease Target place of the polypeptides Source of origin Optimum

conditions

Marine algae and potent bioactivities

respect to the each enzyme

References

pH Temperature

(°C)

Pepsin Digestive, acid protease and

endo-peptidase

Cleavage for hydrophobic aromatic

amino acid residues, phenylalanine,

leucine and tyrosine

Porcine gastric mucosa 2 37 Chlorella vulgaris —antioxidative Sheih, Wu, and Fang

(2009)

Navicula incerta —antioxidative Kang et al. (2011)

Spirulina platensis —ACE-I inhibitory activity Suetsuna and Chen

(2001)

Trypsin Digestive, Serine protease

and endo-peptidase

Cleavage for C-terminal side of

lysine and arginine

Bovine, porcine or human

pancreas

537 Chlorella vulgaris —antioxidative Sheih, Wu, and Fang

(2009)

α-

Chymotrypsin

Digestive, Serine protease and

endo-peptidase

Cleavage for C-terminal side of tyrosin,

phenylalanine, tryptophan and leucine

Bovine pancrease 8 37 Chlorella vulgaris —antioxidative Sheih, Wu, and Fang

(2009)

Neutrase Bacterial protease,

metallo-endo-protinase (Zn)

Bacillus amyloliquefaciens 850 Scytosiphon lomentaria —lipid peroxidation

inhibitory activity

Heo, Lee, Song, and

Jeon (2003)

Alcalase Serin endo-protease Bacillus licheniformis 750 Ecklonia cava —lipid peroxidation

inhibitory activity

Heo, Lee, Song, and

Jeon (2003)

Porphyr yezoensis —ACE-I inhibitory activity Qu et al. (2010)

Papain Cysteine protease, endo-

peptidase

Cleavage for basic amino acids,leucine, glycine.

Hydrolysis esters and amides

Carica papaya (papaya

latex)

637 Navicula incerta —hepatic ﬁbrosis inhibitory Kang (2011)

Chlorella vulgaris —nutritional value Morris et al. (2007)

Protamex Endo-exo-peptidase Bacillus sp. 6 40 Spirulina platensis—ACE-I inhibitory activity He et al. (2007)

Kojizyme Amino and carboxy peptidase Selected Basillus and

Aspergillus strains

640 Ishige okamurae —cytoprotective effect against

induced DNA damage

Heo and Jeon (2008)

Flavourzyme Endo-exo-peptidase Aspergillus oryzae 750 Ecklonia cava —ACE-I inhibitory activity Athukorala and Jeon

(2005)

Protease S Serin endo-protease Bacillus stearothermophilus 790 Undaria pinnatiﬁda Sato et al. (2002)

Optimum hydrolysation conditions were employed according to the citation (Heo, Lee, Song, & Jeon, 2003).

951K. Samarakoon, Y.-J. Jeon / Food Research International 48 (2012) 948–960

Table 2

Bioactive peptides and possible bioactivities with the IC

values from protein hydrolysates of the marine algae.

Marine algae Possible bioactivity Proteolytic enzymes, fermenting

micro-organisms or others

Bioactive amino acids or peptide sequences IC

values

References Country

Navicula incerta Anti-oxidative:

DPPH Pepsin Acidic amino acids; Glu-, Asp-, Lys-, Arg- 196 μg/mL

Hydroxyl α-chymotrypsin 102 μg/mL Kang et al. (2011) South Korea

Superoxide Neutrase 196 μg/mL

Navicula incerta Hepatic ﬁbrosis

inhibitory effect

Papain Pro-Gly-Trp-Asn-Gln-Trp-Phe-Leu Val-Glu-Val-Leu-Pro-Pro-Ala-Glu-Leu Kang (2011) South Korea

Chlorella vulgaris Anti-oxidative:

superoxide radical

Pepsin Val-Glu-Cys-Iyr-Gly-Pro-Asn-Arg-Pro-Glu-Phe 7.5 μMSheih, Wu, and Fang (2009) Taiwan, ROC

Chlorella vulgaris ACE inhibitory Pepsin Val-Glu-Cys-Iyr-Gly-Pro-Asn-Arg-Pro-Glu-Phe 29.6 μMSheih, Fang, and Wu (2009) Taiwan, ROC

Chlorella vulgaris Anti-proliferartion Pepsin Val-Glu-Cys-Iyr-Gly-Pro-Asn-Arg-Pro-Glu-Phe 70.7 μMSheih et al. (2010) Taiwan, ROC

Chlorella vulgaris ACE-I inhibitory Pepsin Ile-Val-Val-Glu 315.3 μMSuetsuna and Chen (2001) Japan

Ala-Phe-Leu 63.8 μM

Phe-Ala-Leu 26.3 μM

Ala-Glu-Leu 57.1 μM

Val-Val-Pro-Pro-Ala 79.5 μM

Spirulina platensis ACE-I inhibitory Pepsin Ile-Ala-Glu 34.7 μMSuetsuna and Chen (2001) Japan

Phe-Ala-Leu 26.2 μM

Ala-Glu-Leu 57.1 μM

Ile-Ala-Pro-Gly 11.4 μM

Val-Ala-Phe 35.8 μM

Undaria pinnatiﬁda Antihypertensive Pepsin Ala-Ile-Tyr-Lys 213 μMSuetsuna and Nakano (2000) Japan

Tyr-Lys-Tyr-Tyr 64.2 μM

Lys-Phe-Tyr-Gly 90.5 μM

Tyr-Asn-Lys-Leu 21 μM

Undaria pinnatiﬁda Antihypertensive Protease S Val-Tyr 35.2 μMSato et al. (2002) Japan

Ile-Tyr 6.1 μM

Ala-Trp 18.8 μM

Phe-Tyr 42.3 μM

Val-Trp 3.3 μM

Ile-Trp 1.5 μM

Leu-Trp 23.6 μM

Undaria pinnatiﬁda Antihypertensive Hot-water extract Tyr-His 5.1 μMSuetsuna et al. (2004) Japan

Lys-Trp 10.8 μM

Lys-Tyr 7.7 μM

Lys-Phe 28.3 μM

Phe-Tyr 3.7 μM

Val-Trp 10.8 μM

Val-Phe 43.7 μM

Ile-Tyr 2.7 μM

Ile-Trp 12.4 μM

Val-Tyr 11.3 μM

Porphyra yezoensis ACE-I inhibitory Pepsin Ile-Tyr 2.69 μMSuetsuna (1998) Japan

Met-Lys-Tyr 7.26 μM

Ala-Lys-Tyr-Ser-Tyr 1.52 μM

Leu-Arg-Tyr 5.06 μM

Porphyra yezoensis Antihypertensive Pepsin Ala-Lys-Tyr-Ser-Tyr Saito and Hiroshi (2005) Japan

Pavlova lutheri Myoﬁbroblast differentiation Candida rugopelliculosa Met-Pro-Gly-Pro-Leu-Ser-Pro-Leu Ryu (2011) South Korea

value: the concentration of peptide required to inhibit 50% of the activity.

952 K. Samarakoon, Y.-J. Jeon / Food Research International 48 (2012) 948–960

The highest inhibitory capacity of lipid peroxidation in linoleic acid was

observed in Alcalase and Neutrase extracts of E. cava and of

S. lomentaria,respectively(Heo, Lee, Song, & Jeon, 2003). Besides,

these enzymatic hydrolysates of E. cava have shown antioxidant

properties with thermal stability, which exerted the activity even by

heating at 100 °C temperature up to 8 h (Heo, Jeon, Lee, Kim, & Lee,

2003). Furthermore, enzymatic extracts exhibited more prominent

effects on hydrogen peroxide scavenging activity of approximately 90%,

comparing to commercial antioxidants (Heo, Park, Lee, & Jeon, 2005).

Heo and Jeon (2008) have shown that a strong hydrogen peroxide

scavenging effect against protease enzymatic extracts from a brown

macro alga, I. okamurae than carbohydrase extracts. Moreover, the

concentration of protease extracts (140 μg/mL) including Alcalase,

Flavourzyme, Kojizyme and Protamex was shown with remarkably

high scavenging activities of 91.62, 93.41, 96.27 and 93.71%, against

hydrogen peroxide respectively. Interestingly, the Kojizyme extract

possessed thermal stability and retained its original activity of

approximately 70% after 24 h of heating at 100 °C. Moreover, Kojizyme

extract of I. okamurae showed a prominent cytoprotective effect against

-induced DNA damage on human lymphocytes in the dose-

dependent manner. Besides, prominent H

-scavenging activities

were shown by Protamex, Flavourzyme and Alcalase extracts of

S. fullvelum,S. thunbergii and S. horneri, respectively. In another study,

a brown seaweed S. lomentaria was shown strong ROS scavenging

activities after being hydrolysed by proteases (Ahn et al., 2004).

EAEs from red algae Palmaria palmate have exhibited the greatest

scavenging activities against DPPH and peroxyl radicals when treated

with proteases than carbohydrases. Moreover, liberating small

molecular mass peptides or amino acids by enzymatic hydrolysis by

proteases might be contributed to enhancement of their scavenging

activities of ROS (Wang et al., 2010). In another work, EAEs of Undaria

pinnatiﬁda prepared by using proteases exhibited strong scavenging

activities on DPPH and hydroxyl radicals (Je et al., 2009). In addition,

a marine macroalgae, Ulva fasciata has showed the detoxiﬁcation

effect against reactive oxygen species induced oxidative stress by UV-

B radiation. In this study, it has been suggested that involving

ascorbate–glutathione cycle with inherent simulative enzymes as an

antioxidant defense system (Shiu & Lee, 2005).

Several studies also conﬁrmed that low molecular weight

hydrolysates have more potency to possess ROS scavenging activities

than high molecular weight hydrolysates (Chang, Wu, & Chiang,

2007). In addition, Sheih, Wu, and Fang (2009) showed that potent

antioxidative activity of pepsin hydrolysate from Chlorella vulgaris

protein waste, generated during production of essence. Further, the

isolated and puriﬁed peptide (VECYGPNRPQF) with a low molecular

mass (1309 Da) was exhibited signiﬁcant tolerance effect against

gastrointestinal enzymes. Furthermore, the puriﬁed peptide from

algal protein has shown higher ABTS radical scavenging (IC

9.8±

0.5 μM) and superoxide radical scavenging (IC

7.5±0.12 μM)

activities by comparing with the standard antioxidants. Besides,

moderate antioxidative and scavenging effects were reported against

DPPH radicals (IC

value 58.0±1.2 μM). A benthic diatom Navicula

incerta has been subjected to hydrolysis by various proteases, and

pronounced detectable antioxidant activity was observed (Kang et al.,

2011). Further, enzymatic hydrolysates were tested by electron spin-

trapping techniques for free radical scavenging effects on DPPH,

hydroxyl and superoxide radicals, while the highest IC

values were

recorded as 196 μg/mL (pepsin), 102.0 μg/mL (α-chymotrypsin) and

196.0 μg/mL (neutrase), respectively. Furthermore, majorities of

amino acid constituents were negatively charge, including glutamic

acid and aspartic acid in the hydrolysates (Kang et al., 2011).

C-Phycocyanin, a type of water-soluble protein pigment from

Spirulina plantensis has showed the inhibitory effect against CCl

induced lipid peroxidation in the rat liver in vivo. Furthermore, radical

scavenging activity (IC

value 5.0 μM) of C-phycocyanin was

detected against peroxyl radical scavenger in vitro as well. Taken

together, the involvement of the chromophore (bilin group) in

phycocyanin can be facilitated to scavenge reactive oxygen radicals

(Bhat & Madyastha, 2000). Besides, antioxidative peptides are

associated in 5–11 amino acid residues including, proline, histidine,

tyrosine or tryptophan and hydrophobic amino acids in the milk

protein (Pihlanto, 2006). In addition, two antioxidant peptides,

carnosine and glutathione also have been found in macroalgae.

However, these peptides are present in high concentrations in animal

muscles. Thus, the red seaweed Ancanthophora delilei has been

described as a source of carnosine (β-alanyl-L-histidine), a histidyl

peptide with an antioxidant activity as well as is associated the ability

of chelate transition metals (Fleurence, 2004). Consequently, anti-

oxidative protein hydrolysates, peptides or amino acids from marine

algae are thought as potential sources to control various oxidative

processes. Nevertheless, it is difﬁcult to compare these results from

various studies with diversities of in vitro assay systems and an

inconsistency in the conditions used to evaluate their antioxidative

capacity (Samaranayaka & Li-Chan, 2011).

3.2. Antihypertensive activity

Cardiovascular diseases (CVDs) claim a high risk for many lives in

the world population and frequently challenge to health problems

(Kearney, Whelton, Reynolds, Muntner, & He, 2005). CVDs have been

identiﬁed as the leading risk factor for mortality and are associated

with high blood pressure or hypertension. In addition, the estimated

total number of adults with hypertension over 25% in 2000 was 972

million in both economically developed and developing countries.

Further, it was predicted to increase in 2025 by about 60% to a total

1.56 billion adult suffering with the burden of hypertension (Kearney

et al., 2005). Besides, hypertension leads to other cardiovascular

diseases, including arteriosclerosis, stroke, myocardial infarctions

(MI) and renal disease in later stage as well (Kearney et al., 2005).

Diet therapy and lifestyle modiﬁcations are the most desirable tool

that effectively reduces the blood pressure. Therefore, natural sources

of ACE-I inhibitors raise the possibilities that could be formulated

with dietary intake (Wilson, Hayes, & Carney, 2011).

Renin–angiotensin–aldosterone system (RAAS) plays an impor-

tant role in regulating blood volume and responsible for the control of

blood pressure and ﬂuid balance in humans (Fitzgerald, Gallagher,

Tasdemir, & Hayes, 2011). Angiotensin-I-converting enzyme (ACE-I)

is a monomeric, membrane-bound zinc metalloprotease, which

catalyzes the conversion of decapeptide angiotensin-I to the octa-

peptide angiotensin-II by removing a carboxyl-terminal dipeptide

(Zhao & Xu, 2008). Angiotensin-II is known as a potent vasoconstric-

tive molecule. Thus, ACE-I have long been revealed as a key part of the

rennin–angiotensin system (RAS), which regulates the blood pres-

sure. Therefore, ACE-I inhibitory factor is the way for the treatment of

hypertension (Riordan, 2003). Verdecchia, Angeli, Mazzotta, Gentile,

and Reboldi (2008) have stated that RAS can be inhibited by two

ways, inhibition of angiotensin-I generation from angiotensinogen as

directly inhibit by rennin, and blocking the conversion of angiotensin-

II from angiotensin-I by ACE-I. Thus, renin is also considered as mono

speciﬁc enzyme and displays a remarkable speciﬁcity on angiotensi-

nogen and renin catalyzes as the ﬁrst and limiting step of the RAS

(Fitzgerald et al., 2011). Therefore, renin inhibitors have a positive

effect that offers for blocking this complex hormonal system by initial

point of activation (Michel, Randy, Juerg, & Norman, 2006). However,

a novel direct renin inhibitor, known as aliskiren has been progressed

recently (Tabassum, 2011). Gradman et al. (2005) have shown that

aliskiren is orally effective a non-peptide with low molecular weight,

once-daily treatment lowers the blood pressure effectively in patients

with mild to moderate hypertension. Moreover, synthesized chemical

drugs such as Captopril®, Enalapril®, Alacepril® and Lisinopril® have

been used very much in the treatment and prevention of hyperten-

sion (Atkinson & Robertson, 1979). Nevertheless, these synthesized

953K. Samarakoon, Y.-J. Jeon / Food Research International 48 (2012) 948–960

ACE inhibitors lead to cause undesirable side effects such as lost of

taste, chronic dry cough, renal impairment and angioneurotic edema

(Kim & Wijesekara, 2010). Recently, there has been a great interest to

search novel ACE inhibitors from marine algae as alternatives for

synthetic drugs (Kim & Wijesekara, 2010). Therefore, bioactive

peptides from marine macro and microalgae could be the major

sources for this instance with least or no side effects, since ACE-I

inhibited potency have been highlighted based on protein hydroly-

sates in many researches (Suetsuna & Chen, 2001; Suetsuna &

Nakano, 2000).

ACE inhibitory activities of enzymatic hydrolysates from seven

brown algae species namely E. cava,I. okamurae,S. fulvellum,

S. horneri,S. coreanum,S. thunbergii and S. lomentaria have been

reported (Athukorala & Jeon, 2005). In their experiment, ﬁve

commercial proteases including Kojizyme, Flavourzyme, Neutrase,

Alcalase and Protamex were employed to obtain respective hydroly-

sates from the selected seaweeds. Thus, E. cava was exhibited the

most potent ACE inhibitory effect among the species tested.

Flavourzyme digested E. cava showed the IC

value of 0.3 μg/mL.

Meanwhile, a commercial drug captopril has shown an IC

value of

0.05 μg/mL. Furthermore, > 30 kDa of ﬂavourzyme digest fraction

(protein content 27%) separated from an ultraﬁltration membrane

was observed positive effect on ACE-I inhibitory assay. In another

work, Cha et al. (2006) have been testing further on a brown seaweed

E. cava for ACE-I inhibitory activity using proteolytic digests at 70 °C.

In fact, Flavourzyme hydrolysate showed the highest inhibitory

activity approximately 90%. Moreover, IC

values of anti-ACE activity

of ﬁve different enzymatic digests were ranged from 2.33 to 3.56 μg/mL.

Potent ACE-I inhibitory effect was observed from C. vulgaris, after

hydrolyzed by pepsin on the protein waste of C. vulgaris industrial by-

product (Sheih, Fang, & Wu, 2009). Furthermore, the isolated amino

acid sequence, a hendeca-peptide (Val-Glu-Cys-Tyr-Gly-Pro-Asn-

Arg-Pro-Gln-Phe) was revealed with ACE-I inhibitory activity (IC

value of 29.6 μM). Interestingly, puriﬁed hendeca-peptide showed

signiﬁcant heat (at 40–100 °C temperature range) and pH (2–10 pH

range) stability against gastrointestinal enzymes (Sheih, Fang, & Wu,

2009). In another study, C. vulgaris and Spirulina platensis have been

subjected to separate a few of peptidic fractions from pepsin

digestion. Further, following peptides Ile-Ala-Glu, Ile-Ala-Pro-Gly

and Val-Ala-Phe have been obtained from S. platensis pepsin

hydrolysates and exhibited ACE-I inhibitory activities IC

values

34.7, 11.4 and 35.8 μM, respectively (Suetsuna & Chen, 2001). In

addition, C. vulgaris has been led to report ACE-I inhibitory activities

with IC

values of 315.3, 63.8, 26.3, 57.1 and 79.5 μM in the following

peptides Ile-Val-Val-Glu, Ala-Phe-Leu, Phe-Ala-Leu, Ala-Glu-Leu, and

Val-Val-Pro-Pro-Ala, respectively (See Table 2).

On the other hand, peptidic digests of wakame (U. pinnatiﬁda)

exhibited ACE-I inhibitory activities (IC

values of 213, 64.2, 90.5 and

21 μM) against amino acid sequences Ala-Ile-Tyr-Lys, Tyr-Lys-Tyr-

Tyr, Lys-Phe-Tyr-Gly, and Tyr-Asn-Lys-Leu, respectively (Suetsuna &

Nakano, 2000). Moreover, another seven kinds of ACE-I inhibitory

peptides were isolated from wakame by using protease S ‘Amano’

enzyme (Sato et al., 2002). According to the literature, the isolated

dipeptides as Val-Tyr, Ile-Tyr, Ala-Trp, Phe-Tyr, Val-Trp, Ile-Trp, and

Leu-Trp were reported to have IC

values of 35.2, 6.1, 18.8, 42.3, 3.3,

1.5 and 23.6 μM, respectively. Among these peptides, Val-Tyr, Ile-Tyr,

Phe-Tyr and Ile-Trp signiﬁcantly reduced the blood pressures when

treated with a single oral administration dose (1 mg/kg mouse)

against spontaneously hypertensive rats (SHRs). In another experi-

ment, a hot water extract of U. pinnatiﬁda was subjected to isolate ten

kind of dipeptides, including Tyr-His, Lys-Trp, Lys-Tyr, Lys- Phe, Phe-

Tyr, Val-Trp, Val-Phe, Ile-Tyr, Ile-Trp and Val-Tyr. These also

decreased the blood pressure in SHR (Suetsuna, Maekawa, & Chen,

2004). An edible red algae species, Porphyra yezoensis has been

hydrolyzed by seven commercial proteolytic enzymes and then

Alcalase was selected as the effective hydrolysate among them.

Furthermore, glutelin was isolated as the major protein (77.1%) from

P. yezoensis as high extraction yield (28.3%) than other reported

proteins such as albumin and gliadan (Qu et al., 2010). In another

work, Suetsuna (1998) showed that P. yezoensis has potent ACE-I

inhibitory activity against spontaneously hypertensive rats (SHR).

Further, the pepsin hydrolaysate of P. yezoensis could be separated

into several peptides including Ile-Tyr, Met-Lys-Tyr, Ala-Lys-Ser-Tyr

and Leu-Arg-Tyr with ACE inhibitory IC

values 2.69, 7.26, 1.52 and

5.06 μM, respectively. Besides, another oligopeptide Ala-Lys-Tyr-Ser-

Tyr has also been reported from P. yezoensis against the pepsin

hydrolysate (Saito & Hiroshi, 2005). In addition, He et al. (2007) have

shown that protein hydrolysates of red seaweed Polysiphonia

urceolata and microalga S. platensis possessed ACE-I inhibitory

activities with an IC

value less than 1.0 mg/mL. According to the

results, IC

values 0.17 and 0.22 mg/mL were reported by the

S.platensis hydrolysates after digested Protamex and SM98011,

respectively. Moreover, the high content of branched and aromatic,

amino acids such as Ile, Val, Phe and Tyr were reported to be

responsible in marine proteins for the ACE-I inhibitory activities. In

another suggestion, branched amino acid residues at N-terminal

positions and aromatic amino acid residues at C-terminal positions in

the substrates or competitive inhibitors could be preferred for anti-

ACE activity as well (He et al., 2007).

Taken together, structure–activity correlations have further

conﬁrmed that among the different peptide inhibitors of ACE may

inﬂuence strongly when binding to substrates with C-terminal

tripeptide sequences. However, the intensities of ACE activity were

also affected by the adjacent amino acid of the C-terminal proline

residue in a particular peptide (Li, Le, Shi, & Shrestha, 2004). Even for

the potent activities, this should be a change with the hydrophobic

amino acids. Hence, this might be the possible mechanism for

evaluating the ACE-I inhibitory activities and antihypertensive effects.

Despite the fact, most of the anti ACE-I activities of peptides from food

derived-proteins were measured in vitro (Li et al., 2004). Therefore, it

is needed to explore the blood pressure lowering activities or

hypertensive activities with respect to algal peptides in vivo.

According to the facts, a little research work was carried out up to

long-term efﬁcacy and safety as considering the therapeutic purpose.

Therefore, it is needed to discuss more about the bioactive algal

peptides for the uses as nutraceutical and pharmaceutical potentials

with effects of both prevention and treatment of hypertension.

3.3. Anticoagulant activity

Blood coagulation is the complex process and an important part of

homeostasis. Association of blood coagulation factors is involve in

order to stop bleeding and to repair the place of damaged wall of a

blood vessel. However, coagulation processes get interfered by the

anticoagulants, which can extendedly exist or stop blood coagulation

due to endogenous and exogenous factors (Jung, Je, Kim, & Kim,

2002). These anticoagulants are considered as a convenient tool for

exploration of the mechanism of the blood coagulation cascade

system. The blood coagulation pathway has associated with at least

13 or more plasma serine proteases. These were known as blood

coagulating factors and involve in the clotting mechanism by

consisting with intrinsic and extrinsic pathways to a ﬁnal common

pathway (David & Thomas, 2007). The identiﬁed factors, including FII,

FVII, FIX and FX, each with γ-carboxyglutamic acid form a calcium-

mediated formation of phospholipid-factors complex as intrinsic

factor tenase. In order to accomplish the clotting process, the extrinsic

factor tenase and the prothrombinase complexes are used (Blostein,

Furie, Rajotte, & Furie, 2003).

A few of commercial anticoagulants have been identiﬁed and used

for many years. Especially, anticoagulants are being used in

medication for thrombotic disorders as well as for medical equip-

ments such as blood transfusions, test tubes and renal dialysis.

954 K. Samarakoon, Y.-J. Jeon / Food Research International 48 (2012) 948–960

Moreover, heparin, coumarine and warfarin are used as the most

common commercial anticoagulants for the therapeutic purposes.

However, several side effects have been reported as development of

thrombocytopenia and hemorrhagic effect (Hylek, Molina, Shea,

Henault, & Regan, 2007). Therefore, there is an increasing interest

for the natural anticoagulants that are appropriately safe for future

therapeutic uses. However, anticoagulant activities from marine algal

bioactive peptides have been reported much rarely. Conversely,

marine macro and microalgae species were considered so far, and

potent anticoagulant activities were observed on the other functional

metabolites such as proteoglycan (Athukorala, Lee, Kim, & Jeon,

2007).

The anticoagulant potentialities have been evaluated by the hot-

water extracts from 22 species of green and brown seaweeds around

Jeju coastal area in South Korea (Athukorala et al., 2007). Further,

considerably high anticoagulant activities were reported from Codium

fragile and Sargassum horneri against activated partial thromboplastin

time (APTT) and prothrombin time (PT) assays. According to the

results, high molecular weight polysaccharides (>30 kDa fraction)

were the major component than the protein in both algal species.

Therefore, anticoagulant effects were considered to be associated

with complex form of carbohydrates and protein (proteoglycan). The

anticoagulant activity of marine green algae, Codium pugniformis, was

assessed by studying the APTT, PT and thrombin time (TT) using

normal human plasma, comparing with the commercial anticoagu-

lant heparin (Matsubara, Matsuura, Hori, & Miyazawa, 2000). In this

study, the anticoagulant activity has been shown due to proteoglycan

including sulfated polysaccharide (326 μg/mg) and protein polysac-

charide (52.0 μg/mg). However, anticoagulant marine peptides have

been concisely isolated from marine organisms, including blood ark

shell, Scapharca broughtonii (Jung et al., 2002), yellow ﬁn sole,

Limanda aspera (Rajapakse, Jung, Mendis, Moon, & Kim, 2005), and

granulated ark, Tegillarca granosa (Jung et al., 2007), and blue mussel,

Mytilus edulis (Jung & Kim, 2009). Therefore, anticoagulants are most

commonly used in medications, where related compounds increase

the action of anti-thrombin upon thrombin and target them to

activate factor Xa for clot formation. Therefore, a direct thrombin

inhibitor or interference to particular coagulant factors associated

with enzymatic targets would be used for development of novel

anticoagulants. Moreover, there has been no research recently

touching on proteins or bioactive peptides with effects of anticoagulant

activities from marine algae. Therefore, this review affords to explore

novel bioactive protein hydrolysates or peptides from the proteins of

marine phycological sources, in order to supply anticoagulant activities

with enough satisfaction for the future pharmacological needs.

3.4. Antiproliferation activity

Cancer is globally the ﬁrst-leading cause of death in economically

developed countries and the second-leading cause of death in

developing countries (Ezzati, Lopez, Rodgers, Hoorn, & Murray,

2002). Cancer is a continually increasing threat for the global

population, and considered to be raised with aging and adaptation

to cancer-causing behaviors. Based on GLOBOCAN 2008 estimates,

about 12.7 million cancer cases have been reported and 7.6 million of

deaths are estimated to have occurred in 2008 (Jemal et al., 2011).

Furthermore, 64% of deaths have reported in developing countries

among 56% reported cancer cases. Besides, 14% cancer deaths out of

23% of total breast cancer-cases in females and 23% of cancer deaths

out of 17% total lung cancer cases in males have been reported.

Despite the fact, cancer causes can be controllable. From reported

cancer cases 5–10% were caused by genetic defects and the remaining

90–95% of cases were attributed to environment and lifestyle factors,

including tobacco smoke (25–30%), diet (30–35%), infections

(15–20%), obesity (10–20%), alcohols (4–6%), physical inactivity and

environment pollutants (Anand et al., 2008). Therefore, awareness of

the cancer-causing factors and early diagnosis with implementing the

treatments are beneﬁcial for prevention.

Chemotherapy is a main promising approach to prevent and cure

cancers, which has aimed to reduce morbidity and mortality of cancer

by delaying the process of carcinogenesis (Sheih et al., 2010).

However, the development of resistance is being frequently occurred

against chemotherapeutic consequences. In this regard, the bioactive

functional secondary metabolites have triggered from natural

sources. Therefore, marine algae facilitate a fruitful source of

functional ingredients and are to be used in cancer chemotherapy.

Recently, C. vulgaris derived peptide has been shown to inhibit solar

ultraviolet B (UVB) induced matrix metalloproteinase-1(MMP-1)

level in skin ﬁbroblast cells (Chen, Liou, Chen, & Shih, 2011). UVB

radiation is considered as an agent of inducing the expressions of

MMP-1, MMP-3 and MMP-9 in human normal epidermis. Meanwhile,

MMP-1 was thought as to involve in collagen degradation and lead to

affect on photoaging. According to these studies, 10 or 5 mg/mL of

C. vulgaris peptides has diminished the UVB induced level of MMP-1

and cysteine-rich 61 (CYR61) mRNA expression along the monocyte

chemoattractant protein-1 (MCP-1) production. Furthermore, c-fos

and c-jun expressions were also down regulated by peptides from

C. vulgaris. In fact, the actions of transcription factor-1 (AP-1), CYR61

and MCP-1 gene expressions also were suppressed and led to

evaluate the protective effect of microalgae derived peptides on

UVB induced human skin ﬁbroblasts (Chen et al., 2011). In addition,

Hasegawa et al. (2002) showed that hot-water extracted a puriﬁed

glycoprotein (ARS-2) with an amino acid sequence of DVGEAFPTVV-

DALVA from C. vulgaris which was expressed by the toll-like receptor

(TLR-2) against the antitumor activities. Moreover, ARS-2 stimulated

spleen-adherent cells of mice produced interleukin-12 (IL-12) p40 as

TLR-2 dependent manner but not for TLR-4. Furthermore, the isolated

hendeca-peptide (VECYGPNRPQF) of pepsin hydrolysate from

C. vulgaris protein waste exhibited a strong antiproliferation in the

dose-dependent manner and induced the post-G1 cell cycle arrest in

the AGS cells (Sheih et al., 2010). According to the results, the growth

inhibition activities of puriﬁed peptide and pepsin hydrolysate with

values of 70.7 ±1.2 μg/mL and 1.74± 0.3 mg/mL were reported

against the AGS cell line, respectively. In fact, cytotoxicity was also

not observed against WI-38 lung ﬁbroblast cells in vitro (Sheih et al.,

2010). In another study, Sulaiman, Shamaan, Ngah, and Yusof (2006)

have shown the effect of antioxidant enzyme status in hot-water

extracts from C. vulgaris on liver cancer induced rats. Moreover, all

doses (50, 150 and 300 mg/kg body weight) reduced the level of

superoxide dismutase (SOD) during all the weeks (0, 4, 8 and 12)

while experimenting against the liver cancer induced groups (choline

deﬁcient diet +0.1% ethionine in drinking water; CDE) and

comparing them to the control groups. Therefore, a protective role

has been assigned in the liver cancer induced rats by replacing or

compensating the endogenous antioxidant enzyme.

C-Phycocyanin, a major biliprotein isolated from S. platensis with

high purity (>95%) has been tested on the growth and multiplication

of human chronic myeloid leukemia cell line (K562) (Subhashini et

al., 2004). Thus, 50 μM of C-phycocyanin treated up to 48 h against

K562 cells signiﬁcantly diminished (49%) their proliferation. Besides,

cells treated with 25 and 50 μM of C-phycocyanin during 48 h showed

14.11 and 20.93% cells by ﬂow cytometric analysis in sub-G0/G1

phase, respectively. In fact, apoptotic body formation due to inducing

C-phycocyanin on K562 cells has been conﬁrmed by releasing

cytochrome cfrom the mitochondria into the cytosol. (Subhashini et

al., 2004). In another study, the isolated C-phycocyanin from

S. platensis treated on human hepatocarcinoma cell line (HepG2)

has revealed a down regulation of the expression of multidrug

resistance protein-1 (MDR-1). Further, it was noted that the ROS and

cyclooxygenase-2 (COX-2) mediated pathways are involved in the

NF- B and AP-1 (Nishanth et al., 2010). In addition, Minkova et al.

(2011) showed that the high-purity B-phycoerythrin isolated from

955K. Samarakoon, Y.-J. Jeon / Food Research International 48 (2012) 948–960

Porphyridium cruentum was responsible for the inhibition of tumor

cell proliferation on Grafﬁmyeloid tumor cells in the dose-dependent

manner in vitro. Moreover, about 50 and 63% of the growth inhibition

was recorded against 50 and 100 μg/mL of B-phycoerythrin, respec-

tively. Further, it has been proved that the effect of apoptosis is

caused by changing the cellular morphology such as, cell shrinkage,

membrane bleeding and DNA fragmentations. Therefore, biliproteins,

including C-phycocyanin and B-phycoerythrin exerted anti-proliferation

and antitumor activities in algae pigments through in vitro assays.

Taken together, these ﬁndings indicate that protein hydrolysates or

peptides from C. vulgaris and phycobiliproteins from some marine algae

can be used for the development of pharmaceuticals against cancers.

3.5. Immune-stimulant activity

The health beneﬁts primarily attribute from many functional

ingredients of macro and microalgae. Therefore, proteins and

peptides have gained an increasing demand not only as nutrition

but also as its potential for its health-promoting effects. In recent

years, in vitro and in vivo studies have revealed that bioactive

secondary metabolites may induce and promote the human health

factors. Further explorations on the bioactive proteins or protein-

derived peptides from the marine algae can be distinguished by ex

vivo assays through enzymatic hydrolysis. Besides, most of the

peptides are encrypted in the parent proteins in the algae and

maybe release and processed during gastrointestinal digestion (Kim

& Wijesekara, 2010). Therefore, protein hydrolysates have been

widely used for speciﬁc formulations in order to enhance the

nutritional and functional values of the food (Becker, 2007). In

addition, it is noteworthy to ﬁnd out the induction and stimulation of

the immune system by bioactive peptides from the marine algae for

the human health effects.

A green micro alga, C. vulgaris has been hydrolyzed by the

pancreatic enzyme with an enzyme/substrate ratio of 20 AU/g with

the conditions of pH 7.5 and temperature at 45 °C for 4 h (Morris et

al., 2007). According to the studies, it has achieved both innate and

speciﬁc immune responses after using undernourished Balb/c mice.

Moreover, oral administration of protein hydrolysate (500 mg/kg)

was experimented during 8 days after 3 days of fasting period and a

marked increase up to 128% of the lymphocyte pool was reported by

comparing it to the control group of mice (p b0.01). Therefore, the

hemopoiesis was judged by the recovery of the bone marrow

cellularity and the leukocyte count in the peripheral blood. Further-

more, the functional activities of macrophages were also greatly

increased. In fact, mononuclear phagocytic system and both humoral

and cell mediated immune functions were also stimulated including,

T-dependent antibody responses and reconstitution of delayed-type

hypersensitivity (DTH) responses (Morris et al., 2007). A potent

stimulator (ONC-107 Responding™) of the mouse B cell proliferation

and an activator of macrophages have been boosted by water

extraction of Chlorella pyrenoidosa selectively. Further, the molecular

mass of polysaccharide/protein complex was revealed as larger than

100 kDa with immune-stimulatory effect against inﬂuenza virus

(Kralovec et al., 2007).

Protease enzyme extract, E. cava has shown the immune-

stimulant effect on murine splenocytes in vitro. As reported, once

after treated E. cava hydrolysate on ICR mice has dramatically

enhanced the proliferation effect of splenocytes, including lympho-

cytes, monocytes and granulocytes. Furthermore, number of CD4

cells, CD8

T cells and CD45R/B220

B cells were increased markedly

compared to the untreated controls. Besides, the mRNA expressions

and production level of Th-1 type cytokines, including TNF-αand

IFN-γwere down regulated. Thus, Th-2 type cytokines, including IL-4

and IL-10 were up regulated (Ahn et al., 2008). Taken together, these

facts are concerned with the immune-modulatory and therapeutic

roles of bioactive proteins or protein complexes obtained from the

marine algae sources.

4. Nutritional values of algal proteins and applications

There is a long tradition behind the consumption of seaweeds in

the East and Paciﬁc Asian countries due to their well-known

nutritional impact as rich sources of polysaccharides, proteins, lipids,

minerals, vitamins and dietary ﬁbers (Burtin, 2003; Gupta & Abu-

Ghannam, 2011; Mohamed et al., 2012; Paul, Christoper, Brooks,

Campbell, & Rowland, 2007). However, seaweeds have gained

another value in European countries as a major source for thickening

and gelling agents, including alginate, carrageenan and agar, the so-

called phycocolloids. These primary constituents were extracted from

red and brown algal cell walls and have considered as use for animal

foods or other industrial applications (Burtin, 2003). Generally, the

protein content of the seaweeds is low comparing it to microalgae.

Moreover, it might be varied according to species and seasonal

conditions. According to the facts, brown algae have shown less

protein content (3–15% of the dry weight) with respect to the green

and red seaweeds (10–47% of the dry weight) (Fleurence, 1999). The

reason of low content of protein in brown seaweeds is due to the

available high phenolic content, whereas red and green seaweeds

might have low-level phenol lead to have a high content of protein.

Burtin (2003) has shown that some red seaweeds, such as Palmaria

palmate and Porphyra tenera posses high-protein contents up to 35

and 47% of the dry weight, respectively. In contrast, the protein

content of Ulva spp. (belong to green seaweed) is in the range of

15–20% of the dry matter. Some of the brown seaweeds, including

Laminaria digitata,Ascophyllum nodosum,Fucus vesiculosus and

Himanthalia elongate have shown low protein content (b15% of the

dry matter).

Edible microalgae, Spirulina and Aphanizomenon species have been

used as food for thousands of years (Jensen, Ginsberg, & Drapeau,

2001). Essential nutrients also have exhibited in some microalgae

biomasses (Becker, 2007). In addition, Tokuşoglu and Ünal (2003)

have shown that edible microalgae, including C. vulgaris,S. platensis

and Isochrisis galbana have been potential for food supplements and

food additives after being cultured. From their nutritional composi-

tions, a very high-protein content (avg. 63.0%) (p b0.01) was reported

respect to S. platensis. In fact, I. galbana showed the high source of

total lipid content 17.16% (p b0.01) including polyunsaturated fatty

acids (PUFA), eicosapentaenoic acid (EPA), docosahexaenoic acid

(DHA) and dense of minerals as well. Therefore, microalgae are

composed of an unusual breadth of nutritional quality compared to

macroalgae as well as conventional plants in our diet.

It is well-known that chains of amino acids are used to build up

proteins. In addition, essential amino acids are acquired from the food

sources or dietary supplements, since humans cannot synthesis them.

Therefore, amino acids are important nutrients that are required for

essential physiological and biological functions for humans, including

bile-acid conjugation, osmoregulation, retinal and neurological

development, immune functions and maintenance of the calcium

level as well (Shao & Hathcock, 2008). Hence, amino acids intimately

play a key role with the above functions in humans and other animals.

In terms of amino acid composition, the marine algae make a sense of

their nutritional value. Besides, nutritional quality of protein is

determined signiﬁcantly by amino acid content, proportion and

bioavailability (Becker, 2007). In addition, Rashida (1991) has

detected 17 amino acids of the protein hydrolysates among the

eighteen species of seaweeds. Interestingly, an appreciate amount of

the amino acid lysine, which is usually deﬁcient in terrestrial plants,

has been reported. Furthermore, the distribution pattern of these

amino acids revealed some pronouncement of variations among

seaweeds like Rhodophyceae, Chlorophyceae and Phaeophyceae. In

addition, other studies indicated that both aspartic and glutamic acids

956 K. Samarakoon, Y.-J. Jeon / Food Research International 48 (2012) 948–960

constitute a large amino acid fraction of seaweeds, compared to foods

such as soybeans and eggs (Fleurence, 1999, 2004). Moreover, the

functional properties of defatted microalgae biomasses, including

Porphyridium cruentum,Nannochloropsis spp., and Phaeodactylum

tricornutum have been comparatively studied with soybean ﬂour

(Guil-Guerrero et al., 2004). According to the facts, Nannochloropsis

spp. and P. tricornutum showed high compositions of hydrophobic

and hydrophilic amino acids than soybean ﬂour at 41.6% and 22.9%,

and 40.7% and 21%, respectively. However, the protein biomass was

higher in soybean ﬂour (45%) than reported in Nannochloropsis spp.

(28.8%) and P. tricornutum (36.4%), respectively. In addition, these

algal bio masses can be described as potential sources of formulation

of acidic foods such as milk analog products and protein-rich

carbonated beverages with facilitating essential constituents to

humans and animals (Guil-Guerrero et al., 2004). Besides, Becker

(2004) has conﬁrmed that investigation of amino acid proﬁles and

pattern of various algae are favorably equal or sometimes even

superior compared to the conventional plant proteins. Moreover,

noodles, breads, biscuits, ice cream and other common foods along

with liquid foods such as health drinks, soft drinks, tea, beer and

spirits consist of nutritive health values (Liang, Xueming, Chen, &

Chen, 2004).

Furthermore, S. platensis has been taken a special attention as one

of the most analyzed species among the microalgae. In fact, high

qualities and quantities of protein (60%–70% of dry weight),

consisting of the high rate of amino acids with the greatest

bioavailability, make a huge demand (Babadzhanov et al., 2004).

Further, Morist, Montesinos, Cusido, and Godia (2001) have shown

that high quantities of lysine (Lys) were found in S. platensis about

50–55 mg/g proteins. In addition, methionine and cysteine (Met+ Cys)

together (15–20 mg/g protein) and threonine (45–50 mg/g of proteins)

have been reported as processed amino acids from S. platensis

compared to other amino acids. Indeed, these values were contrasted

to FAO and WHO recommendations and would be higher than that of

‘ideal protein’. Furthermore, phycobiliproteins as major photosynthetic

accessory pigments, including phycoerythrin, phycocyanin, allophyco-

cyanin and phycoerythrocyanin, have been reported in marine algae

(Niu, Wang, & Tseng, 2006). Besides, Synechococcus spp. (blue-green

algae) (Viskari & Colyer, 2003)andPorphyridium cruentum (red algae)

can be described as interesting species among the marine algae that

used to extract phycobiliproteins. Interestingly, these particular groups

of proteinshave been used as natural colorants in foods such as chewing

gums, dairy products, ice sherbaths and gellies (Bermejo, Alvarez-Pez,

Acien Fernandez, & Molina, 2002). Therefore, a variety of health

products such as tablets, capsules, powder or extracted bioactive

ingredients including beta-carotene and phycocyanin have been

marketed recently (Guil-Guerrero et al., 2004).

Taurine is another simple protein or as a peptide which was found

in the free form and showed a numerous biological and functional

requirement (Houstan, 2005). Recently, taurine has become a popular

ingredient in the functional foods, beverages and dietary supple-

ments. Besides, Dawczynski, Schubert, and Jahireis (2007) have

reported that red macroalgae contained high amount of taurine

compared to green and brown algae species. Further, signiﬁcant taurine

contents were seen from Gelidium subcostatum and Grateloupia elliptic

(belong to red algae) at 998.7 and 198.2 nmol/g wet weight,

respectively. In addition, glycoproteins (lectins) were also considered

as a type of interesting proteins in marine seaweeds which can be

extracted with carbohydrate moiety. In a group of researches, Hwang,

Kwon, Kim, and Nam (2008) and Hwang, Kim, and Nam (2008) have

reported that they could have extracted the bioactive glycoproteins

from brown alga (Hizikia fusiformis) and red alga (P. yezoensis). In fact,

chemoprotective effect was revealed against acetaminophen (AAP)-

induced liver damage rats in vivo and in vitro.Inanotherstudy,anew

lectin has been isolated from marine green algae, Ulva pertusa (Wang et

al., 2003). Due to the chemical properties of lectins, a great deal of

attraction has been paved for the ﬁeld of immunology, cell biology,

cancer research and genetic engineering. Therefore, many types of

seaweed have shown their medicinal and nutritional value comprised

in proteins or glycoproteins. Over the many years, this has been proven

by many populations with the expectation of quality life and well-being

with their delicacy on marine algae. On the other hand, consumption of

some cyanobacteria can be associated with health risk. Hence, a number

of hepatotoxins and neurotoxins produced belong to mycrocystin that

are the well-known toxins found in cyanobactria (Miroslav & Zorica,

2008). Further, Cox, Banack, and Murch (2003) have stated that β-N-

methylamino-L-alanine (BMAA) as a non protein amino acid showed

neurotoxic activities of toxin products from cyanobacterial culture.

However, the protein quality and the digestibility were inﬂuenced

by the species of marine macro and microalgae with seasonal periods

and contents of anti-nutritional factors such as phenolic and poly-

saccharides (Fleurence, 1999). Taken together, consumption of macro

or microalgae would be an added advantage for the daily life and it is

gaining a nutraceutical value with health-promoting effects. There-

fore, the associated functional ingredients from edible marine macro

and microalgae might serve for the fulﬁllments of future needs as

functional food.

5. Cosmeceutical values of algal proteins and applications

Cosmeceutical applications are derived as ‘cosmetics’with poten-

tial of ‘pharmaceutical’or drug like beneﬁts for the human skin, and

they can enhance its protection, appearance and anti-aging properties

(Kim, Ravichandran, Khan, & Kim, 2008). Along with the innovation

of biotechnological aspects, cosmeceuticals have gained much

interest with the marine algal natural products (Raja, Hemaiswarys,

Kumar, Sridhar, & Rengasamy, 2008). Over the past few decades, a

noticeable dinning habit of marine algae was pronounced due to their

enriched key ingredients and responsible for desirable health effects.

However, in recent years, algae were not only taken as a delicacy, but

also been proposed to be used as the products with effective

physiological applications. In fact, cosmeceutical preparations were

gained much attention from the marine algae, and have become a

major counterpart for the utilization of external applications on to the

skin (Spolaore, Joannis-Cassan, Duran, & Isambert, 2006). Uses of

algal proteins or derivatives are important in conferring moisture

retention on hair and skin. On the other hand, algal proteins show a

strong afﬁnity with hair or skin to improve their nourishments.

Moreover, rich protein contents and biologically dynamic growth

factors in many of the algae can facilitate for the preparation of

cosmeceuticals. Furthermore, cosmeceutcals are supposed to be

involved in healing and repairing damaged skin with moisturizing

and maintaining the nourishment as well. Major components in

physiological activities, particularly peptides or protein hydrolysates

derived from Porphyra spp. and wakame seaweeds under appropriate

conditions, can be applied cosmoceutically (Hagino & Masanobu,

2003).

According to the revealed facts, we can rely on utilizing of marine

algae in cosmeceutical industry, since they possess beneﬁcial prop-

erties to human health such as antioxidant, anti-aging, immune-

stimulant, anti-inﬂammatory and anti-irritant effects (Morist et al.,

2001). The extracts from Arthrospira and Chlorella species are well-

known in the skin care market (Stolz & Obermayer, 2005). B-

Phycoerythrin is a major light harvesting type of protein, which is

found in many algae species, including blue-green algae (Bermejo et

al., 2002; Kim et al., 2008). This showed the tremendous bioactivities,

including antioxidant, anti-inﬂammatory, neuroprotective, antiviral,

antitumor, hepetoprotective, serum lipid reducing and liver protect-

ing activities (Sekar & Chandramohan, 2008). In addition, B-

phycoerythrin has shown effects of heat stability and pH tolerant

characteristics, which have been applied as the natural pink and

purple colorants for lipsticks, eyeliner and also formulations for

957K. Samarakoon, Y.-J. Jeon / Food Research International 48 (2012) 948–960

cosmetic products (Viskari & Colyer, 2003). Furthermore, mycosporines

and mycosporines like amino acids have exhibited ultra violet (UV)

radiation absorption properties in the range of 310–365 nm wave-

lengths (Oren & Gunde-Cimerman, 2007). Low molecular weight,

water-soluble compounds have been isolated from the marine red algae

Gracilaria cornea (Arad & Yaron, 1992) and reported to be used in body

lotions due to its skin protective effect. Therefore, these can act as

sunscreen compounds against UV radiations (Sinha, Klisch, Groniger, &

Hader, 2000). The skin matrix has known to be responsible for the skin's

mechanical properties. Therefore, the increment of collagen production

and inhibition of MMP-1 activities would be expected from cosmeceu-

ticals in order to reduce the natural aging process. Moreover, the

extracts from C. vulgaris havebeen used for tissue regeneration and also

for wrinkle reduction by the stimulation of collagen synthesis in the

skin (Spolaore et al., 2006). Furthermore, antioxidative marine algal

peptides might be an interesting source of primary ingredients for the

formulation of future cosmeceuticals due to its protective effect from

ROS damaging activities. Therefore, algal peptides and protein de-

rivatives are of concern to be good candidates for functional cosmetics.

6. Conclusion

Marine algae have long been identiﬁed as excellent reservoirs of

extract proteins and its derivatives with potent functional bioactivities.

However, these studies were rarely being discussed by researchers.

Therefore, this endeavor led to give an overview of the proteins, protein

derivatives, peptides, peptide derivatives, amino acids and amino acid-

like compounds from marine algae, based on published researches in

the past few years. Furthermore, these components have been targeted

to discuss the effects and their respective functional bioactivities along

with their recent pharmacological needs. Interestingly, bioactive

peptides and amino acids may act as alternative molecules to small

molecular drugs. Moreover, these have shown a great advantage over

the conventional drugs with high bioavailability and bio-speciﬁcity to

the targets. Consequently, the properties of low toxicity, structural

diversity and least or no accumulations of these molecules in the body

tissues were given wide interest by many scientists to be used due to its

therapeutic purposes. Taken together, this evidence suggested that

valuable biological functions associated with marine algal proteins and

peptides might be used in future potentialities, including, pharmaceu-

ticals, cosmeceuticals and functional foods. Over the years, most of the

research studies on the marine algae have been focused on in vitro or

mouse model systems. Therefore, in order to commercialize the

bioactive peptides, the performances of research studies using human

models or clinical trials are a necessity in the future.

References

Ahn, G., Hwang, I., Park, E. J., Kim, J. H., Jeon, Y. J., Lee, J. H., et al. (2008).

Immunomodulatory effects of an enzymatic extracts from Ecklonia cava on murine

splenocytes. Marine Biotechnology,10, 278–289.

Ahn, C. B., Jeon, Y. J., Kang, D. S., Shin, T. S., & Jung, B. M. (2004). Free radical scavenging

activity of enzymatic extracts from a brown seaweed Scytosiphon lomentaria by

electron spin resonance spectrometry. Food Research International,37, 253–258.

Anand, P., Kunnumakara, A. B., Sundaram, C., Harikumar, K. B., Tharakan, S. T., Lai, O. S.,

et al. (2008). Cancer is a preventable disease that requires major lifestyle changes.

Pharmaceutical Research,25, 2097–2116.

Aneiros, A., & Garateix, A. (2004). Bioactive peptides from marine sources:

pharmacological properties and isolation procedures. Journal of Chromatography

B,803,41–53.

Arad, S., & Yaron, A. (1992). Natural pigments from red microalgae for use in foods and

cosmetics. Trends in Food Science and Technology,3,92–97.

Athukorala, Y., & Jeon, Y. J. (2005). Screening for angiotensin-1-converting enzyme

inhibitory activity of Ecklonia cava.Journal of Food Science and Nutrition,10,

134–139.

Athukorala, Y., Lee, K. W., Kim, S. K., & Jeon, Y. J. (2007). Anticoagulant activity of

marine green and brown algae collected from Jeju Island in Korea. Bioresource

Technology,98, 1711–1716.

Atkinson, A. B., & Robertson, J. I. S. (1979). Captopril in the treatment of clinical

hypertension and cardiac failure. The Lancet,314, 836–839.

Babadzhanov, A. S., Abdusamatova, N., Yusupova, F. M., Faizullaeva,N., Mezhlumyan, L. G.,

& Malikova, M.Kh. (2004). Chemical composition of Spirulina plantensis cultivated in

Uzbekistan. Chemistry of Natural Compounds,40,276–279.

Bargeman, G., Koopsb, G. H., Houwing, J., Breebaartb, I., van der Horsta, H. C., &

Wesslingb, M. (2002). The development of electro-membrane ﬁltration for the

isolation of bioactive peptides: The effect of membrane selection and operating

parameters on the transport rate. Desalination,149, 369–374.

Becker, E. W. (2004). Handbook of microalgae culture. In A. Richmond (Ed.), Microalgae

in human and animal nutrition (pp. 312–351). Oxford: Blackwell Publishing.

Becker, E. W. (2007). Micro algae as a source of protein. Biotechnology Advances,25,

207–210.

Bermejo, R. R., Alvarez-Pez, J. M., Acien Fernandez, F. G., & Molina, G. E. (2002).

Recovery of pure B-phycoerythrin from the microalga Porphyridium cruentum.

Journal of Biotechnology,93,73–85.

Bhat, B. V., & Madyastha, K. M. (2000). C-Phycocyanin: A potent peroxyl radical

scavenger in vivo and in vitro.Biochemical and Biophysical Research Communica-

tions,275,20–25.

Blostein, M. D., Furie, B. C., Rajotte, I., & Furie, B. (2003). The Gla domain of factor IXa

binds to factor VIIIa in the tenase complex. The Journal of Biological Chemistry,278,

31297–31302.

Burtin, P. (2003). Nutritional value of seaweeds. EJEAFChe,4, 498–503.

Cha, S. H., Ahn, G. N., Heo, S. J., Kim, K. N., Lee, K. W., Song, C. B., et al. (2006). Screening

of extracts from marine green and brown algae in Jeju for potential marine

angiotensin-I converting enzyme (ACE) inhibitory activity. Journal of the Korean

Society of Food Science and Nutrition,35, 307–314.

Chabeaud, A., Vandanjon, L., Bourseau, P., Jaouen, P., Chaplain-Derouiniot, M., &

Guerard, F. (2009). Performances of ultraﬁltration membranes for fractionating a

ﬁsh protein hydrolysate: Application to the reﬁning of bioactive peptic fractions.

Separation and Puriﬁcation Technology,66, 463–471.

Chacón-Lee, T. L., & Gonzalez-Mảriño, G. E. (2010). Microalgae for “health”foods —

Possibilities and challenges. Comprehensive reviews in Food Science and Food Safety,

9, 655–675.

Chang, C. Y., Wu, K. C., & Chiang, S. H. (2007). Antioxidant properties and protein

compositions of porcine haemoglobin hydrolysates. Food Chemistry,100,

1537–1543.

Chen, C. L., Liou, S. F., Chen, S. J., & Shih, M. F. (2011). Protective effects of

chlorella-derived peptide on UVB-induced production of MMP-1 and degradation

of procollagen genes in human skin ﬁbroblasts. Regulatory Toxicology and

Pharmacology,60, 112–119.

Cox, P. A., Banack, S. A., & Murch, S. J. (2003). Biomagniﬁcation of cyanobacterial

neurotoxins and neurodegenerative disease among the Chamarro people of Guam.

Proceedings of the National Academy of Sciences of the United States of America,100,

13380–13383.

David, G., & Thomas, R. (2007). Intrinsic pathway of coagulation and arterial

thrombosis. Arteriosclerosis, Thrombosis, and Vascular Biology,27, 2507–2513.

Dawczynski, C., Schubert, R., & Jahireis, G. (2007). Amino acids, fatty acids, and dietary

ﬁbre in edible seaweed products. Food Chemistry,103, 891–899.

Dominic, A., & Danquah, M. K. (2011). Industrial-scale manufacturing of

pharmaceutical-grade bioactive peptides. Biotechnology Advances,29, 272–277.

Ezzati, M., Lopez, A. D., Rodgers, A., Hoorn, S. V., & Murray, C. J. L. (2002). Selected major

risk factors and global and regional burden of disease. The Lancet,360, 1347–1360.

Fitzgerald, C., Gallagher, E., Tasdemir, D., & Hayes, M. (2011). Heart health peptides

from macroalgae and their potential use in functional foods. Journal of Agricultural

and Food Chemistry,59, 6829–6836.

FitzGerald, J. R., & Murray, A. B. (2007). Bioactive peptides and lactic fermentations.

International Journal Diary Technology,59, 118–125.

Fleurence, J. (1999). Seaweed proteins: Biochemical, nutritional aspects and potential

uses. Trends in Food Science and Technology,10,25–28.

Fleurence, J. (2004). Seaweed proteins. In R. Y. Yada (Ed.), Proteins in food processing

(pp. 197–213). Cambridge, UK: Woodhead publishing limited.

Garson, J. M. (1989). Biosynthetic studies on marine natural products. Natural Product

Reports,6, 143–170.

Gradman, A. H., Schmieder, R. E., Lins, R. L., Nussberger, J., Yanntong, C., & Bedigian, P.

(2005). Aliskiren, a novel orally effective rennin inhibitor, provides

dose-dependent antihypertensive efﬁcacy and placebo-like tolerability in hyper-

tensive patients. Circulation,11, 1012–1018.

Guedes, A. C., Amaro, Helena M., & Malcata, X. F. (2011). Microalgae as source of high

added-value compounds —A brief review of recent work. Biotechnology Progress,

27, 597–613.

Guil-Guerrero, J. L., Navaro-Juarez, R., Lopez-Martinez, J. C., Campara-Madrid, P., &

Rebolloso-Fuentes, M. M. (2004). Functional properties of the biomass of three

microalgal species. Journal of Food Engineering,65, 511–517.

Gupta, S., & Abu-Ghannam, N. (2011). Bio active potential and possible health effects of

edible brown seaweeds. Trends in Food Science and Technology,22, 315–326.

Hagino, H., & Masanobu, S. (2003). Use of algal proteins in cosmetics. European Patent

1 433 463 B1, Dec. 18.

Harnedy, P. A., & FitzGerald, R. J. (2011). Bioactive proteins, peptides, and amino acids

from macroalgae. Journal of Phycology,47, 218–232.

Hasegawa, T., Matsuguchi, T., Noda, K., Tanaka, K., Kumamoto, S., Shoyama, Y., et al.

(2002). Toll-like receptor 2 is at least partly involved in the antitumor activity of

glycoprotein from Chlorella vulgaris.International Immunopharmacology,2,

579–589.

He, H. L., Chen, X. L., Wu, H., Sun, C. Y., Zhang, Y. Z., & Zhou, B. C. (2007). High

throughput and rapid screening of marine protein hydrolysates enriched in

peptides with angiotensin-I-converting enzyme inhibitory activity by capillary

electrophoresis. Bioresource Technology,98, 3499–3505.

958 K. Samarakoon, Y.-J. Jeon / Food Research International 48 (2012) 948–960

Heo, S. J., Cha, S. H., Lee, K. W., Cho, S. K., & Jeon, Y. J. (2005). Antioxidant activities of

Chlorophyta and Phaeophyta from Jeju Island. Algae,20, 251–260.

Heo, S. J., Cha, S. H., Lee, K. W., Lee, K. W., & Jeon, Y. J. (2006). Antioxidant activities of

red algae from Jeju Island. Algae,21, 149–156.

Heo, S. J., & Jeon, Y. J. (2008). Radical scavenging capacity and cytoprotective effect of

enzymatic digests of Ishige okumurae.Journal of Applied Phycology,20, 1087–1095.

Heo, S. J., Jeon, Y. J., Lee, J., Kim, H. T., & Lee, W. K. (2003). Antioxidant effect of

enzymatic hydrolyzate from a kelp, Ecklonia cava.Algae,18, 341–347.

Heo, S. J., Lee, K. W., Song, C. B., & Jeon, Y. J. (2003). Antioxidant activity of enzymatic

extracts from brown seaweeds. Algae,18(1), 71–81.

Heo, S. J., Park, E. J., Lee, K. W., & Jeon, Y. J. (2005). Antioxidant activities of enzymatic

extracts from brown seaweeds. Bioresource Technology,96, 1613–1623.

Heo, S. J., Park, P. J., Park, E. J., Kim, S. K., & Jeon, Y. J. (2005). Antioxidant activity of

enzymatic extracts from a brown seaweed Ecklonia cava by electron spin

resonance spectrometry and comet assay. European Food Research and Technology,

221,41–47.

Houstan, M. C. (2005). Neutraceuticals, vitamins, antioxidants, and minerals in the

prevention and treatment of hypertension. Progress in Cardiovascular Diseases,47,

396–449.

Hwang, H. J., Kim, I. H., & Nam, T. J. (2008). Effect of a glycoprotein from Hizikia

fusiformis on acetaminophen-induced liver injury. Food and Chemical Toxicology,

46, 3475–3481.

Hwang, H. J., Kwon, M. J., Kim, I. H., & Nam, T. J. (2008). Chemopreventive effect of a

protein from the red algae Porphyra yezoensis on acetaminophen induced liver

injury in rats. Phytotherapy Research,22, 1149–1153.

Hylek, E. M., Molina, C. E., Shea, C., Henault, L. E., & Regan, S. (2007). Major hemorrhage

and tolerability of warfarin in the ﬁrst year of therapy among elderly patients with

atrial ﬁbrillation. Circulation,115, 2689–2696.

Je, J. Y., Park, P. J., Kim, E. K., Park, J. S., Yoon, H. D., Kim, K. R., et al. (2009). Antioxidant

activity of enzymatic extracts from the brown seaweed Undaria pinnatiﬁda by

electron spin resonance spectroscopy. LWT-Food Science and Technology,42,

874–878.

Jemal, A., Bray, F., Center, M. M., Ferlay, J., Ward, E., & Forman, D. (2011). Global cancer

statistics. CA. Cancer Journal for Clinicians,61,69–90.

Jensen, G. S., Ginsberg, D. I., & Drapeau, M. S. (2001). Blue green algae as an

immune-enhancer and biomodulator. Journal of the American Nutraceutical

Association,3,24–30.

Jimsheena, V. K., & Gowada, L. R. (2010). Arachin derived peptides as selective

angiotensin I-converting enzyme (ACE) inhibitors: Structure–activity relationship.

Peptides,31, 1165–1176.

Jung, W. K., Je, J. Y., Kim, H. J., & Kim, S. K. (2002). A novel anticoagulant protein from

Scapharca broughtonii.Journal of Biochemistry and Molecular Biology,5, 199–205.

Jung, W. K., Jo, H. Y., Qian, Z. J., Jeong, Y. J., Park, S. G., Choi, W. L., et al. (2007). A novel

anticoagulant protein with high afﬁnity to blood coagulation factor Va from

Tegillarca granosa.Journal of Biochemistry and Molecular Biology,40, 832–838.

Jung, W. K., & Kim, S. K. (2009). Isolation and characterization of an anticoagulant

oligopeptide from blue mussel, Mytilus edulis.Food Chemistry,117, 687–692.

Kang, K. H. (2011). Hepatocyte injury and hepatic ﬁbrosis inhibitory effect of peptides

isolated from microalgae, Navicula incerta. Ph.D thesis, Department of Chemistry,

Pukyoung National University, Busan, South Korea.

Kang, K. H., Qian, Z. J., Ryu, B., & Kim, S. K. (2011). Characterization of growth and

protein contents from microalgae Navicula incerta with the investigation of

antioxidant activity of enzymatic hydrolysates. Food Science and Biotechnology,

20(1), 183–191.

Kang, K. H., Qian, Z. J., Ryu, B. M., Kim, D., & Kim, S. K. (2012). Protective effects of

protein hydrolysate from marine microalgae Navicular incerta on ethanol-induced

toxicity in HepG2/CYP2E1 cells. Food Chemistry,132, 677–685.

Karavita, R., Senevirathne, M., Athukorala, Y., Affan, A., Lee, Y. J., Kim, S. K., et al. (2007).

Protective effect of enzymatic extracts from microalgae against DNA damage

induced by H

.Marine Biotechnology,9, 479–490.

Kearney, P. M., Whelton, M., Reynolds, K., Muntner, P., & He, J. (2005). Global burden of

hypertension: Analysis of worldwide data. The Lancet,365, 217–223.

Kim, K. N., Heo, S. J., Song, C. B., Lee, J., Heo, M. S., Yeo, I. K., et al. (2006). Protective

effect of Ecklonia cava enzymatic extracts on hydrogen peroxide-induced cell

damage. Process Biochemistry,41, 2393–2401.

Kim, S. K., Ravichandran, Y. D., Khan, S. B., & Kim, Y. T. (2008). Prospective of the

cosmeceuticals derived from marine organisms. Biotechnology and Bioprocess

Engineering,13, 511–523.

Kim, S. K., & Wijesekara, I. (2010). Development and biological activities of

marine-derived bioactive peptides: A review. Journal of Functional foods,2,1–9.

Kitts, D. D., & Weiler, K. (2003). Bioactive proteins and peptides from food sources.

Applications of bioprocesses used in isolation and recovery. Current Pharmaceutical

Design,9, 1309–1323.

Korhonen, H., & Pihlanto, A. (2006). Bioactive peptides: Production and functionality.

International Dairy Journal,16, 945–960.

Kralovec, J. A., Metera, K. L., Kumar, J. R., Watson, L. V., Girouard, G. S., Guan, Y., et al.

(2007). Immunostimulatory principles from Chlorella pyrenoidosa—Part 1: Isola-

tion and biological assessment in vitro.Phytomedicine,14,57–64.

Li, H. G., Le, G. W., Shi, Y. H., & Shrestha, S. (2004). Angiotensin-I-converting enzyme

inhibitory peptides derived from food proteins and their physiological and

pharmacological effects. Nutrition Research,24, 469–486.

Liang, S., Xueming, L., Chen, F., & Chen, Z. (2004). Current microalgal health food R & D

activities in China. Hydrobiologia,512,45–48.

Matsubara, K., Matsuura, Y., Hori, K., & Miyazawa, K. (2000). An anticoagulant

proteoglycan from the marine green alga, Codium pugniformis.Journal of Applied

Phycology,12,9–14.

Meisel, H., & FitzGerald, R. J. (2003). Biofunctional peptides from milk proteins:

Mineral binding and cytomodulatory effects. Current Pharmaceutical Design,9,

1289–1295.

Michel, A., Randy, W., Juerg, N., & Norman, K. H. (2006). Renin inhibition with aliskiren:

Where are we now and where are we going? Journal of Hypertension,24, 243–256.

Minkova, M. K., Toshkova, R. A., Gardeva, E. G., Tchorbadjieva, M. I., Ivanova, N. J.,

Yossifova, L. S., et al. (2011). Antitumor activity of B-phycoerythrin from

Porphyridium cruentum.Journal of Pharmacy Research,4, 1480–1482.

Miroslav, G., & Zorica, S. (2008). Microalgae and cyanobacteria: Food for thought.

Journal of Phycology,44, 260–268.

Mohamed, S., Hashim, S. N., & Rahman, H. A. (2012). Seaweeds: A sustainable

functional food for complementary and alternative therapy. Trends in Food Science

and Technology,23,83–96.

Morist, A., Montesinos, J. L., Cusido, J. A., & Godia, F. (2001). Recovery and treatment of

Spirulina platensis cells cultured in a continous photbioreactor to be used as food.

Process Biochemistry,37, 535–547.

Morris, H. J., Carrillo, O., Almarales, A., Berm'udez, R. C., Lebeque, Y., Fontaine, R., et al.

(2007). Immunostimulant activity of an enzymatic protein hydrolysate from green

microalga Chlorella vulgaris on undernourished mice. Enzyme and Microbial

Technology,40, 456–460.

Ngo, D. H., Wijesekara, I., Vo, T. S., Ta, Q. V., & Kim, S. K. (2011). Marine food-derived

functional ingredients as potential antioxidants in the food industry: An overview.

Food Research International,44, 523–529.

Nishanth, R. P., Ramakrishna, B. S., Jyotsna, R. G., Roy, K. R., Reddy, G. V., Reddy, P. K.,

et al. (2010). C-Phycocyanin inhibits MDR1 through reactive oxygen species and

cyclooxygenase-2. Europian Journal of Pharmacology,649,74–83.

Niu, J. F., Wang, G. C., & Tseng, C. K. (2006). Method of large-scale isolation and

puriﬁcation of R-phycoerythrin from red algae Polysiphonia urceolata Grev. Protein

Expression and Puriﬁcation,49,23–31.

Oren, A., & Gunde-Cimerman, N. (2007). Mycosporines and mycosporine- like amino

acids: UV protectants of multipurpose secondary metabolites? FEMS Microbiology

Letters,269,1–10.

Paul, M. A., Christoper, I. R. G., Brooks, M., Campbell, R., & Rowland, I. R. (2007).

Nutritional value of edible seaweeds. Nutrition Reviews,65, 535–543.

Pauline, S., Joannis-Cassan, C., Elie, D., & Arsene, I. (2006). Commercial application of

microalgae. Journal of Bioscience and Bioengineering,2,87–96.

Pihlanto, A. (2006). Antioxidative peptides derived from milk proteins. International

Dairy Journal,16, 1306–1314.

Plaza, M., Cifuentes, A., & Ibanez, E. (2008). In the search of new functional food

ingredients from algae. Trends in Food Science and Technology,19,31–39.

Qu, W., Ma, H., Pan,Z., Luo, L., Wang, Z., & He, R. (2010). Preparation of antihypertensive

activity of peptides from Porphyra yezoensis.Food Chemistry,123,14–20.

Raja, R., Hemaiswarys, S., Kumar, N. A., Sridhar, S., & Rengasamy, R. (2008). A

prospective on the biotechnological potential of microalgae. Critical Reviews in

Microbiology,34,77–88.

Rajapakse, N., Jung, W. K., Mendis, E., Moon, S. H., & Kim, S. K. (2005). Anticoagulant

derived from ﬁsh protein hydrolysate inhibits factor Xlla and platelet aggregation.

Life Sciences,76, 2607–2619.

Rashida, Q. (1991). Amino acid composition of some common seaweeds. Pakistan

Journal of Pharmaceutical Sciences,4(1), 49–54.

Riordan, J. F. (2003). Angiotensin-I-converting enzyme and its relatives. Genome

Biology,4, 225.

Ryu, B. M. (2011). A peptide derived from microalga, Pavlova lutheri, fermented by

Candida rugopelliculosa induces myoﬁbroblasts differentiation in human dermal

ﬁbroblasts. Ph.D thesis, Department of Chemistry, Pukyoung National University,

Busan, South Korea.

Saito, M., & Hiroshi, H. (2005). Antihypertensive effect of oligopeptides derived from

nori (Porphyra yezoensis) and Ala-Lys-Tyr-Ser-Tyr in rats. Journal of Japanese

Society of Nutrition and Food Science,58, 177–184.

Samaranayaka, A. G. P., & Li-Chan, E. C. Y. (2011). Food-derived peptidic antioxidants: A

review of their production, assessment, and potential applications. Journal of

Functional Foods,3, 229–254.

Sato, M., Hosokawa, T., Yamaguchi, T., Nakano, T., Muramoto, K., Kahara, T., et al. (2002).

Angiotensin I-converting enzyme inhibitorypeptides derived from wakame (Undaria

pinnatiﬁda) and their antihypertensive effects in spontaneously hypertensive rats.

Journal of Agricultural and Food Chemistry,50,6245–6252.

Sekar, S., & Chandramohan, M. (2008). Phycobiliprotein as commodity: Trends in

applied research, patents and commercialization. Journal of Applied Phycology,20,

113–136.

Shao, A., & Hathcock, J. N. (2008). Risk assessment for the amino acids taurine,

L-glutamine and L-arginine. Regulatory Toxicology and Pharmacology,50, 376–399.

Sheih, I. C., Fang, T. J., & Wu, T. K. (2009). Isolation and characterization of a novel

angiotensin-I converting enzyme (ACE) inhibitory peptide from the algae protein

waste. Food Chemistry,115, 279–284.

Sheih, I. C., Fang, T. J., Wu, T. K., & Lin, P. H. (2010). Anticancer and antioxidant activities

of the peptide fraction from algae protein in waste. Journal of Agriculture and Food

Chemistry,58, 1202–1207.

Sheih, I. C., Wu, T. K., & Fang, T. J. (2009). Antioxidant properties of a new antioxidative

peptide from algae protein hydrolysate in different oxidation systems. Bioresource

Technology,100, 3419–3425.

Shiu, C. T., & Lee, T. M. (2005). Ultraviolet-B-induced oxidative stress and responses of

the ascorbate–glutathione cycle in a marine macroalgae Ulva fasciata.Journal of

Experimental Botany,56, 2851–2865.

Sinha, R. P., Klisch, M., Groniger, A., & Hader, D. P. (2000). Mycosporine-like amino

acids in the marine red alga Gracilaria cornea —Effects of UV and heat.

Environmental and Experimental Botany,43,33–43.

959K. Samarakoon, Y.-J. Jeon / Food Research International 48 (2012) 948–960

Spolaore, P., Joannis-Cassan, C., Duran, E., & Isambert, A. (2006). Commercial applications

of microalgae. Journal of Bioscience and Bioengineering,101,87–96.

Stolz, P., & Obermayer, B. (2005). Manufacturing microalgae for skin care. Cosmetics

Toiletries,120,99–106.

Subhashini, J., Mahipal,S. V. K., Reddy, M. C., Reddy, M. M., Rachamallu, A., & Reddanna, P.

(2004). Molecular mechanisms in C-Phycocyanin induce apoptosis in human chronic

myeloid leukemia cell line-K562. Biochemical Pharmacology,68,453–462.

Suetsuna, K. (1998). Puriﬁcation and identiﬁcation of angiotensin I-converting enzyme

inhibitors from the red alga Porphyra yezoensis.Journal of Marine Biotechnology,6,

163–167.

Suetsuna, K., & Chen, J. R. (2001). Identiﬁcation of antihypertensive peptides from

peptic digests of two microalgae, Chlorella vulgaris and Spirulina platensis.Marine

Biotechnology,3, 305–309.

Suetsuna, K., Maekawa, K., & Chen, J. R. (2004). Antihypertensive effects of Undaria

pinnatiﬁda (wakame) peptide on blood pressure in spontaneously hypertensive

rats. The Journal of Nutritional Biochemistry,15, 267–272.

Suetsuna, K., & Nakano, T. (2000). Identiﬁcation of antihypertensive peptides from

peptidic digest of wakame (Undaria pinnatiﬁda). The Journal of Nutritional

Biochemistry,11, 450–454.

Sulaiman, S., Shamaan, N. A., Ngah, W. Z. W., & Yusof, Y. A. M. (2006). Chemopreventi ve

effect of Chlorella vulgaris in choline deﬁcient diet and ethionine induced liver

carcinogenesis in rats. International Journal of Cancer Research,2, 234–241.

Tabassum, N. (2011). Aliskiren: A new renin inhibitor as anti-hypertensive. Journal of

Applied Pharmaceutical Science,01,30–33.

Tokuşoglu, Ö., & Ünal, M. K. (2003). Biomass nutrient proﬁles of three microalgae:

Spirilina platensis,Chlorella vulgaris, and Isochrisis galbana.Food chemistry and

Toxicology,68, 1144–1148.

Valko, M., Leibfritz, D., Mancol, J., Cronin, M. T. D., Mazur, M., & Telser, J. (2007). Free

radicals and antioxidants in normal physiological functions and human disease.

The International Journal of Biochemistry & Cell Biology,39,44–84.

Verdecchia, P., Angeli, F., Mazzotta, G., Gentile, G., & Reboldi, G. (2008). The rennin

angiotensin system in the development of cardiovascular disease: Role of aliskiren

in risk reduction. Vascular Health and Risk Management,4, 971–981.

Viskari, P. J., & Colyer, C. L. (2003). Rapid extraction of phycobiliproteins from cultures

cyanobacteria samples. Analytical Biochemistry,319, 263–271.

Wang, T., Jonsdottir, R., Kristinsson, H. G., Hreggvidsson, G. O., Jonsson, J. O.,

Thorkelsson, G., et al. (2010). Enzyme-enhanced extraction of antioxidant

ingredients from red algae Palmaria palmate.LWT-Food Science and Technology,

43, 1387–1397.

Wang, S., Zhong, F. D., Zhang, Y. J., Wu, Z. J., Lin, Q. Y., & Xie, L. H. (2003). Molecular

characterization of a new lectins from the green algae Ulva pertusa.Acta Biochemica

et Biophysica Sinica,36, 111–117.

Wilson, J., Hayes, M., & Carney, B. (2011). Angiotensin-1-converting enzyme and prolyl

endopeptidase inhibitory peptides from natural sources with a foucs on marine

processing by-products. Food Chemistry,129, 235–244.

Zhao, Y., & Xu, C. (2008). Structure and function of angiotensin converting enzyme and

its inhibitors. Chinese Journal of Biotechnology,24, 171–176.

960 K. Samarakoon, Y.-J. Jeon / Food Research International 48 (2012) 948–960

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Blue-green algae as an immuno-enhancer and biomodulator

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Jan 2001

Antioxidant Activities of Red Algae from Jeju Island

Article

Full-text available

Mar 2006

The aim of the present study was to evaluate the antioxidant activity of red algae in Jeju Island. The algal extracts were obtained with MeOH and fresh water at 20 and 70?C, and screened for antioxidant activities using hydroxyl radical (HO?), superoxide anion (O2?), hydrogen peroxide (H2O2) and DPPH free radical scavenging assays. Among them, Gracilaria verrucosa methanolic extract at 20?C (20ME, 96.85%), G. textorii aqueous extract at 20?C (20AE, 88.01%), Grateloupia filicina 20AE (85.35%), and Polysiphonia japonica 20ME (94.92%) exhibited the highest scavenging activities against HO?, O2?, H2O2, and DPPH free radicals, respectively. Moreover, P. japonica (20ME and 70ME) is correlated between DPPH free radical scavenging activity and polyphenolic contents. These results indicate that some red algae in Jeju Island could be potential candidates for development of antioxidants.

Screening of Extracts from Marine Green and Brown Algae in Jeju for Potential Marine Angiotensin-I Converting Enzyme (ACE) Inhibitory Activity

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Full-text available

Mar 2006

This study was conducted to screen in vitro angiotensin converting enzyme (ACE) inhibitory activities of methanol (MeOH) and aqueous extracts which were prepared by four different extractions-80% methanol extracts(ME) at , respectively and aqueous extracts (AE) at both temperatures with the residue of the MEs-of ten marine green algae and nineteen brown algae collected along Jeju coast of Korea. Most marine brown algae extracts showed higher capacities than those of marine green algae in ACE inhibitory activity. Particularly, MeOH extract (70ME) of Hizikia fusiforme showed the strongest inhibition activity (about 87%) among all the extracts. Also, 70 MEs of Enteromorpha linza, Ishige sinicola, Laminaria ochotensis, Petrospongium rugosum, Sagrassum horneri, Undaria pinnatifida and MeOH extracts (20ME) of Myagropsis myagroides, Petrospongium rugosum, aqueous extracts (20AE) of Codium contractum, Enteromorpha compressa, and aqueous extracts (70AE) of Ecklonia cava, Petrospongium rugosum showed moderate ACE inhibitory activities more than 50% and the other extracts exhibited weak activities. On tile other hand, E. cava had the best ACE inhibitory activity among 70AEs. This indicates that 70AE of E. cava contains potential anti-ACE macromolecular. We tried to proteolytic digest 70AE of E. cava to induce production of anti-ACE peptides from E. cava 70AE. The enzymes used are five pretenses including Kojizyme, Flavourzyme, Neutrase, Alcalase, and Protamex, which are food grade-commercial enzymes from Novo Co. Flavourzyme-digest of E. cava 70AE showed the highest inhibitory activity about 90%. And the five different enzymatic digests of the E. cava 70AE ranged from 2.33 to 3.56 , respectively in values of anti-ACE activity.

Screening for Angiotensin 1-Converting Enzyme Inhibitory Activity of Ecklonia cava

Article

Jun 2005

Seven brown algal species (Ecklonia cava, Ishige okamurae, Sargassum fulvellum, Sargassum horneri, Sargassum coreanum, Sargassum thunbergii and Scytosiphon lomentaria) were hydrolyzed using five proteases (Protamex, Kojizyme, Neutrase, Flavourzyme and Alcalase) and screened for angiotensin 1-converting enzyme (ACE) inhibitory activities. Most algal species examined showed good ACE inhibitory activities after the enzymatic hydrolysis. However, E. cava was the most potent ACE inhibitor of the seven species. Flavourzyme digest of E. cava exhibited an IC_{50} of around 0.3\;?g/mL for ACE; captopril has an IC_{50} of \~0.05\;?g/mL. The Flavourzyme digest was separated to three fractions by an ultrafiltration membrane (5, 10, 30 kDa MWCO) system according to the molecular weights. The active components were mainly concentrated in >30 kD fraction which are composed of the highest protein content (27\%) and phenolic content (261 mg/100 mL) compared to the other two smaller molecular weight fractions. Therefore, the active compounds appear to be relatively high molecular weight complex molecules associated with protein (glycoprotein) and polyphenols. Therefore, E. cave is a potential source of antihypertensive compound.

Manufacturing microalgae for skin care

Article

Jan 2003

Chemopreventive Effect of Chlorella vulgaris in Choline Deficient Diet and Ethionine Induced Liver Carcinogenesis in Rats

Article

Mar 2006

Chlorella vulgaris (CV), a unicellular green micro alga, has been widely used as a food supplement and credited with chemopreventive potential against several cancers. CV is reported to have a massive amount of antioxidant such as carotenoids, vitamin E, minerals and enzymes. However its antioxidant effect has not yet been explored in great detail. The aim of this study is to determine the effect of Chlorella vulgaris on the antioxidant enzyme status in liver cancer induced rats. Male Wistar rats (200-250 g) were divided into 8 groups in terms of diet given: control group (normal rat chow), liver cancer induced group (choline deficient diet + 0.1% ethionine in drinking water (CDE)), CV group with three different doses (50, 150 and 300 mg kg-1 body weight) and liver cancer group treated with CV at different concentrations (CDE + CV at 50, 150 and 300 mg kg-1 body weight). Blood sample was taken from rats via orbital sinus at 0, 4, 8 and 12 weeks for the determination of endogenous antioxidant enzymes [superoxide dismutase, (SOD), catalase and glutathione peroxidase, (GPx)] and lipid peroxidation active metabolite, malondialdehyde (MDA). Levels of SOD increased significantly (p<0.05) in CDE group when compared to the control group (normal rat chow) at 8 and 12 weeks of experiment. CV at all doses managed to reduce SOD activity at all weeks of experiment. There was no significant change of catalase level between the control and CDE group at the respective weeks of experiment but CV was able to reduce catalase activity (p<0.05) in CDE rats. There was a significant increase (p<0.05) of GPx activity in the CDE group compared to the control group at week 12. However, CV did not have the same effect on GPx as for SOD and catalase activities whereby GPx activity increased further (p<0.05) in CDE rats when treated with CV. The level of MDA increased significantly (p<0.05) in CDE rats when compared to the control group at week 12. CV at 150 and 300 mg kg-1 body weight managed to reduce MDA level in CDE rats. In conclusion, Chlorella vulgaris may have a protective role in liver cancer induced rats by replacing or compensating the activities of endogenous antioxidant enzymes and by reducing lipid peroxidation.

Antihypertensive Effect of Oligopeptides Derived from Nori (Porphyra yezoensis) and Ala-Lys-Tyr-Ser-Tyr in Rats

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Antioxidant Effect of Enzymatic Hydrolyzate from a Kelp, Ecklonia cava

Article

Dec 2003

The potential antioxidative activity of water-soluble enzymatic hydrolyzates from a kelp, Ecklonia cava was evaluated by free radical scavenging and lipid peroxidation assays. To prepare water-soluble hydrolyzates from E. cava the seaweed was enzymatically hydrolyzed by five carbohydrases (Viscozyme, Celluclast, AMG, Termamyl and Ultraflo) and five proteases (Protamex, Kojizyme, Neutrase, Flavourzyme and Alcalase). Among all the hydrolyzates, Celluclast hydrolyzate effectively scavenged free radicals released from DPPH (1,1-diphenyl-2- pricrylhydrazyl) and recorded around 73% scavenging activity at the concentration of 4 mg . This hydrolyzate was thermally stable and DPPH radical scavenging activity remained 80% or higher at heating temperatures of 40 and 60 up to 12 h and around 80% at 100 up to 8 h. AMG and Ultraflo hydrolyzate inhibited the lipid peroxidation of fish oil as that of -tocopherol. These results suggested that an enzymatic extraction will be an effective way for the production of a potential antioxidant from seaweeds.

Biosynthetic studies on marine natural products

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Jan 1989
NAT PROD REP

Mary J. Garson

Submitted to the Faculty of Graduate Studies and Research in partial fulfilment of the requirements for the degree of Doctor of Philosophy, Department of Chemistry. Thesis (Ph.D.)--University of Alberta, 1991.

Bioactive potential and possible health effects of edible brown seaweeds (Review)

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Jun 2011
TRENDS FOOD SCI TECH

Marine macroalgae (seaweeds) are rich in bioactive compounds that could potentially be exploited as functional ingredients for both human and animal health applications. Despite the intensive efforts that are being made to isolate and identify new compounds with potential medicinal, health or pharmaceutical activities, very few compounds with real potency are available. Bioactive compounds that are most extensively researched include sulfated polysaccharides, phlorotannins and diterpenes. These compounds have been reported to possess strong anti-viral, anti-tumor and anti-cancer properties. At the same time, the prebiotic health potential of the polysaccharides from seaweeds is also increasingly being studied either by feeding whole seaweeds or purified polysaccharides to laboratory and farm animals. The present review discusses the pharmaceutical, health and research potential of different bioactive compounds present in brown seaweeds.

Bio-functionalities of proteins derived from marine algae–A review

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Kalpa Wishvajith Samarakoon · You-Jin Jeon

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