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Natural Product Research
Formerly Natural Product Letters
ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/gnpl20
Phytochemical composition, biological activity and
anti-inflammatory potential of acetone extract
from the lichen Platismatia glauca (L.) W.L. Culb. &
C.F. Culb
Marijana Kosanić, Branislav Ranković, Tatjana Stanojković, Perica Vasiljević,
Aleksandar Kočović, Anja Manojlović, Marijana Anđić, Jovana Bradić,
Vladimir Jakovljević & Nedeljko Manojlović
To cite this article: Marijana Kosanić, Branislav Ranković, Tatjana Stanojković, Perica Vasiljević,
Aleksandar Kočović, Anja Manojlović, Marijana Anđić, Jovana Bradić, Vladimir Jakovljević &
Nedeljko Manojlović (15 Dec 2023): Phytochemical composition, biological activity and anti-
inflammatory potential of acetone extract from the lichen Platismatia glauca (L.) W.L. Culb. &
C.F. Culb, Natural Product Research, DOI: 10.1080/14786419.2023.2294479
To link to this article: https://doi.org/10.1080/14786419.2023.2294479
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NATURAL PRODUCT RESEARCH
Phytochemical composition, biological activity and
anti-inammatory potential of acetone extract from the
lichen Platismatia glauca (L.) W.L. Culb. & C.F. Culb
Marijana Kosanića, Branislav Rankovića, Tatjana Stanojkovićb,
Perica Vasiljevićc, Aleksandar Kočovićd,e , Anja Manojlovićd, Marijana Anđićd,e,
Jovana Bradićd,e, Vladimir Jakovljevićd,e,f and Nedeljko Manojlovićd
aDepartment of Biology, Faculty of Science, University of Kragujevac, Kragujevac, Serbia; bInstitute of
Oncology and Radiology of Serbia, Belgrade, Serbia; cFaculty of Science, University of Niš, Niš, Serbia;
dDepartment of Pharmacy, Faculty of Medical Sciences, University of Kragujevac, Kragujevac, Serbia;
eCenter of Excellence for Redox Balance Research in Cardiovascular and Metabolic Disorders, Kragujevac,
Serbia; fDepartment of Human Pathology, IM Sechenov First Moscow State Medical University (Sechenov
University), Moscow, Russia
ABSTRACT
This investigation examined the antioxidant, antimicrobial, cyto-
toxic, and anti-inflammatory activities of the acetone extract of the
lichen Platismatia glauca (L.) W.L. Culb. & C.F. Culb. (PGAE). The phy-
tochemical study of PGAE showed presence of seven compounds:
salazinic acid, β-orcinol carboxylic acid, 3-hydroxyphysodalic acid,
physodalic acid, physodic acid, atranorin, and chloroatranorin. The
antimicrobial potential was determined by microdilution which
showed that S. aureus was most sensitive to the effect of PGAE
with MIC value 0.312 mg/ml. Antioxidant activity was evaluated by
using DPPH method. The obtained IC50 value for PGAE was
194.30 ± 3.32 µg/ml. The cytotoxic effect of the extract was evalu-
ated by MTT test and the strongest activity was towards human
epithelial carcinoma cells with IC50 value of 59.10 ± 0.46 µg/ml. The
findings revealed that the application of lichen extracts decreased
the paw edoema in a dose-dependent manner at 1, 2, 3, and 4 h
following carrageenan administration.
© 2023 Informa UK Limited, trading as Taylor & Francis Group
CONTACT Nedeljko Manojlović mtnedeljko@gmail.com
Supplemental data for this article can be accessed online at https://doi.org/10.1080/14786419.2023.2294479.
https://doi.org/10.1080/14786419.2023.2294479
ARTICLE HISTORY
Received 5 May 2023
Accepted 6 December
2023
KEYWORDS
Platismatia glauca (L.)
W.L. Culb. & C.F. Culb;
Parmeliaceae;
phytochemical analysis;
antimicrobial activity;
antioxidant activity;
cytotoxic activity
2 M. KOSANIĆ ETAL.
1. Introduction
Lichens are symbiotic organisms consisting of a fungus and a photosynthetic organ-
ism, either an alga or Cyanobacteria. Until now, more than 20000 species of lichens
have been identified (He and Naganuma 2022). Lichens can live in conditions where
neither the alga nor the fungus can live independently (Mallen-Cooper et al. 2022).
They commonly grow on rock surfaces or as epiphytes on trees and shrubs (Park
et al. 2023). A specific characteristic of lichens is that they produce a large number
of secondary metabolites with different chemical structures (Goga et al. 2020). New
studies have revealed that lichens and their secondary metabolites exert a wide variety
of biological actions including antimicrobial, antioxidant, anti-inflammatory, analgesic,
antipyretic, and cytotoxic activities (Ranković and Kosanić 2021).
Platismatia glauca (L.) W.L. Culb. & C.F. Culb (P. glauca) is a large, foliose species,
widespread and often very common on acidic bark and twigs. It is a diverse lichen
with a loosely attached thallus and broad lobes growing upward. It may have simple
or coralloid isidia, granular soredia, and a nearly fruticulose and coralloid morphology.
The upper surface has a smooth texture, while the lower surface has a paler tone
(Kuznetsova et al. 2021). This lichen has been traditionally used as a spice in India
and the Middle East (Abdallah 2019; Šeklić and Jovanović 2022). Recent studies have
shown that P. glauca exerts significant suppressive effects on the migration and inva-
siveness of colorectal cancer cells (HCT-116 and SW-480) (Šeklić and Jovanović 2022).
Previous investigations have confirmed the presence of different secondary metabolites
(atranorin, chloroatranorin, atraric acid, and caperatic acid) in this lichen (Culberson
1969; Mitrovic et al. 2014).
There is constant progress in the field of understanding the pathophysiological
basis and novel therapeutic approaches to diseases such as infectious diseases
(Serra-Burriel et al. 2020), oncological diseases (Debela et al. 2021), and diseases
caused by oxidative stress (Forman and Zhang 2021), and there is a constant need
for new bioactive compounds that can be used in their treatment, where lichens
represent a rich source of such compounds.
The aim of this study is to conduct detailed chemical analysis and investigate
antimicrobial, antioxidant, and cytotoxic activities and potential anti-inflammatory
activity of the acetone extract of the lichen P. glauca in order to find an easily acces-
sible source of natural biological agents that could be used in the pharmaceutical
industry and for the treatment of various diseases.
2. Results and discussion
2.1. Phytochemical analysis
The HPLC analysis was used to identify the secondary metabolites present in the
acetone extract of the lichen P. glauca (PGAE) growing in Serbia. The HPLC chromato-
grams of the standards and identified components of PGAE recorded at 254 nm are
given in Figure S1. Identification of the lichen metabolites was achieved by comparison
of their retention time values and UV spectra with the standard substance previously
isolated from lichens. UV spectra of salazinic acid and atranorin with spectral range
NATURAL PRODUCT RESEARCH 3
200–400 nm are given in Figure S2. Detailed data on the retention time, absorption
maxima, and content of the identified secondary metabolites are presented in Table S1.
The solvent system used for HPLC chromatography allowed excellent separation of
the peaks. Seven metabolites with the most intense peaks in the chromatogram are
salazinic acid, β-orcinol carboxylic acid, 3-hydroxyphysodalic acid, physodalic acid,
physodic acid, atranorin, and chloroatranorin. The structures of the detected com-
pounds are shown in Figure 1. Three small peaks on retention times 4.57 ± 0.01,
4.98 ± 0.02, and 6.99 ± 0.01 remained unidentified. Based on the chromatogram, it can
be seen that salazinic acid (3-formyl-2,4-dihydroxy-6-methylbenzoic acid) exhibited
the most intense peak in the HPLC chromatogram of the PGAE. This acid belongs to
depsidones and is very important because it possesses a wide range of biological
activities, such as antioxidant, antimicrobial, and cytotoxic activities (Manojlović etal.
2012; White et al. 2014; Ureña-Vacas et al. 2022). Previous studies have shown that
lichen P. glauca contains atranorin and caperatic acid (Culberson and Culberson 1968;
Huneck and Yoshimura 1996). Based on the GC/MS and NMR analysis, Mitrovic et al.
(2014) have shown the presence of caperatic acid, atraric acid, atranorin, and chlo-
roatranorin as the predominant compounds in P. glauca. They found some methylated
compounds (for example, atraric acid and methyl-β-orcinolcarboxylic acid) because
used derivatized (methylated) extract of P. glauca for analysis. Atraric acid (methyl-β-or-
cinolcarboxylate or methyl-2,4-dihydroxy-3,6-dimethylbenzoate) is a methylated deri-
vate of β-orcinolcarboxylic acid, the compound that we identified in the extract.
HPLC-UV method is better than GC/MS because we identified the authentic compounds
in the form in which they are present in the lichen. In addition, we found salazinic
acid, 3-hydroxyphysodalic acid, physodalic acid, and physodic acid, which have not
been identified by the GC/MS method (Mitrovic et al. 2014). This is the first identifi-
cation of these compounds in this species. Although this is the first study in which
these compounds were detected in P. glauca their presence is not unusual for other
lichens from the Parmeliaceae family (Gómez-Serranillos etal. 2014). These compounds
have previously been identified from lichen Hypogymnia physodes (L.) Nyl., Parmelia
saxatilis (L.) Ach., and Parmelia sulcata Taylor (Gómez-Serranillos etal. 2014; Ranković
et al. 2014).
2.2. Antioxidant activity
The results of antioxidant assays of the PGAE are presented in Table S2. The IC50 value
for the DPPH assay was 194.30 μg/mL. As shown in Table S2, the reducing power was
concentration-dependent. Absorbance values in reducing power assay varied from
0.0972 to 0.2894. The analyses of these various antioxidant activities revealed that
there was a statistically significant difference between the extract and the control
(p < 0.05).
Lichens synthesise numerous secondary metabolites, primarily phenols, and anti-
oxidant activity is most frequently associated with their presence (Elečko etal. 2022).
Lichen phenolics are mainly depsides, depsidones, dibenzofurans, and pulvinic acid
derivatives (Goga et al. 2020). Relatively strong antioxidant effects were previously
found for polyphenolics that constitute P. glauca (salazinic acid, physodic acid, atra-
norin) by many researchers, (Manojlović et al. 2012; Kosanić et al. 2013; 2014) who
NATURAL PRODUCT RESEARCH 5
found varying antioxidant success in free radical scavenging, superoxide anion radical
scavenging, and reducing power, so that these components are probably responsible
for the detected antioxidant activity in PGAE.
Before our research, Mitrovic etal. (2014) studied the antioxidant properties of P.
glauca. In this study, in addition to acetone, other solvents (ethyl acetate and meth-
anol) were used, but it was confirmed that there is an antioxidant potential and that
there are compounds in P. glauca. that exhibit an antioxidant effect. Studzińska-Sroka
et al. (2022), also showed the antioxidant potential of P. glauca, but other methods
of measurement were used (ABTS method) to estimate the antioxidant potential.
Therefore, we are not able to directly compare the results, but it was confirmed that
the acetone extract of lichen P. glauca exhibits an antioxidant effect to a certain extent.
2.3. Antimicrobial activity
The antimicrobial effect of the PGAE on the tested microorganisms is shown in Table S3.
The MIC values varied from 0.312 to 10 mg/mL for bacteria and from 2.5 to 20 mg/mL
for fungi. The most susceptible bacteria were S. aureus (ATCC 25923) and B. subtilis
(ATCC 6633) while the most susceptible fungi were F. oxysporum (ATCC 62506), C. albi-
cans (ATCC 10231), and A. alternate (ATCC 11680). The most resistant microorganisms
were A. flavus (ATCC 9170) and A. niger (ATCC 16888) with MIC value of 20 mg/mL. The
antimicrobial activity of the PGAE was compared to standard antimicrobial agents,
streptomycin (for bacteria) and ketoconazole (for fungi). DMSO was used as the negative
control and it showed no effect on the tested microorganisms.
The level of antimicrobial activity of PGAE depends on test microbes and the con-
centration of extract. Fungi were more resistant to PGAE than bacteria due to the more
complex structure of the fungal cell wall which is in accordance with many other studies
(Heleno etal. 2015; Rosenberger etal. 2018) which have demonstrated that the structure
and the permeability of the cell wall are the main reasons for different sensitivities in
bacteria and fungi. Similar to our research, P. glauca methanol extract was evaluated
for its antimicrobial potential by Gulluce et al. (Gulluce et al. 2006) and it showed
activity against four Gram-positive bacterial strains (two strains of Bacillus subtilis, Bacillus
macerans, and Clavibacter michiganense), where the MIC value for the corresponding
Bacillus subtilis (ATCC 6633) strain is 20 times lower than in our research (MIC values
31.25 and 625 µg/mL respectively). It cannot be concluded what the difference in the
antimicrobial effect of these two extracts originates from since the phytochemical
analysis of the methanol extract was not performed, but there is the possibility that
methanol extracted some additional compounds that could exhibit antimicrobial activity.
Çobanoğlu et al. (2010) also found the activity of acetone and chloroform extracts of
P. glauca against Gram-negative bacteria (Pseudomonas aeruginosa, Escherichia coli, and
Acinetobacter sp.) Although the antimicrobial activity was not tested by the microdilution
method but by the disc diffusion method, it can be observed that the acetone extract
has a more pronounced antimicrobial effect compared to the chloroform extract, i.e.
that the zone of inhibition in the acetone extract has a larger diameter than the zone
of inhibition in the chloroform extract (inhibition zone diameter 10.1 mm and 8 mm
respectively). This indicates that acetone extracted substances with a slightly more
pronounced antimicrobial effect, but unfortunately a detailed chemical analysis is not
6 M. KOSANIĆ ETAL.
available. In the study Abdallah (2019), it was shown that methanol extract of lichen
P. glauca has antifungal activity to Candida albicans (ATCC 10231), but it is weaker
compared to the PGAE used in our research against the same fungal strain (MIC values
6250 and 2500 µg/mL respectively). The phytochemical composition was not examined
in this study, so we are not able to say why there is a difference in activities. Our
research revealed that P. glauca contains atranorin, salazinic, and physodic acids which
have been shown to exhibit powerful antimicrobial activity against numerous bacteria
and fungi (Manojlović et al. 2012; Kosanić et al. 2013) so that type of activity for P.
glauca was expected.
2.4. Cytotoxic activity
The obtained data for the cytotoxic effect of PGAE showed that the IC50 against HeLa,
A549, and LS174, cell lines were 59.10, 78.38, and 87.63 μg/mL, respectively (Table S4).
The tested extract possesses weaker activity compared with cis-DDP. PGAE expressed
relatively strong cytotoxic potential on the used cancer cells, among which HeLa cells
were the most sensitive.
There are only a few studies on the cytotoxic potential of P. glauca. The extract
of P. glauca with n-hexane used as a solvent showed significant cytotoxic effects
on L1210 (murine leukaemia), 3LL (murine Lewis lung carcinoma), and U251 (human
glioblastoma) cells (Bézivin et al. 2003). Similarly, it was found that methanol,
acetone, and ethyl acetate extracts of P. glauca have cytotoxic effects on colorectal
cancer (HCT-116, SW-480) cell lines (Šeklić et al. 2018). Data on the biological
activity of lichen P. glauca in the literature are limited, but it was confirmed that
compounds contained in this species such as salazinic acid, physodic acid, physo-
dalic acid, and atranorin can be active against some cancer cells including human
melanoma Fem-x and human colon carcinoma LS174 cell line, monocytic leukaemia
cell lines (U937 and HL-60) (Toledo Marante et al. 2003; Manojlović et al. 2012;
Kosanić et al. 2014; Ureña-Vacas et al. 2022). Physodalic acid and physodic acid
show a cytotoxic effect towards rat thymocytes which is probably induced by
oxidative stress. It is believed that the specific depsidone structure of these com-
pounds is responsible for this biological effect (Pavlovic et al. 2013). In previous
studies, it was shown that physodic acid and salazinic acid exert a more pronounced
cytotoxic effect against the LS174 cell line compared to PGAE. IC50 values are
17.89 μg/mL for physodic acid (Manojlović etal. 2012), 5.67 μg/mL for salazinic acid
(Kosanić et al. 2013), and 87.63 μg/mL for PGAE. In this context, this depsidone
structure lichen acids show 5 to 13 times stronger activity compared to PGAE itself.
This phenomenon can be explained by the different content of these compounds
in the extract itself, as well as the potential antagonistic effect among the sub-
stances present in the extract. Also physodic acid and physodalic acid reduce the
viability of HeLa cell lines after 72 h from the application of the extract at IC50
values of 63 μg/mL for physodic acid and 283 μg/mL for physodalic acid (Stojanović
et al. 2014), which is higher compared to PGAE (IC50=59.1 μg/mL). There is a pos-
sibility that HeLa cell lines are more sensitive to the synergistic effect of substances
present in PGAE than is the case with the LS174 cell line. Additional research is
NATURAL PRODUCT RESEARCH 7
needed to reveal the possible mechanisms of action of both individual substances
and their combined effect in the extract.
2.5. Acute oral toxicity
The study found that the administration of PGAE at a dose of 2000 mg/kg did not
cause toxic symptoms or mortality in any animals. During 14 consecutive days of
continuous observation, no behavioural changes were observed. Histopathological
findings were normal, and no drug-related morbidity or mortality occurred. Therefore,
the PGAE is considered non-toxic and safe for further biological activity screening.
2.6. Anti-inammatory activity
The carrageenan-induced inflammation was manifested by swelling and quantified
by determination of the paw edoema increase. A rise in paw edoema depended on
the time from carrageenan injection (1, 2, 3, and 4 h) and the applied dose of the
lichen extract (50, 100, and 200 mg/kg), and the results are shown in Table S5.
PGAE in all doses was able to reduce rat paw edoema compared to the Ctrl group,
with the greatest edoema inhibition observed after three and four hours of carra-
geenan injection. In the third and fourth hour, the PGAE in the lowest dose showed
a percentage of inhibition of 36.84 and 30.53 respectively, while the dose of 100 mg/
kg led to a percentage inhibition of 33.84 in the third and 36.48 in the fourth hour.
Additionally, the most prominent effect was achieved after administration of PGAE in
the highest dose of 200 mg/kg in the third and fourth hour after carrageenan injection
in comparison to Ctrl with the percentage inhibition of paw edoema of 47.37 and
46.12 respectively. The anti-inflammatory activity was still the greatest after the appli-
cation of indomethacin in comparison to all applied doses of PGAE. Interestingly the
highest dose of PGAE in the third hour exerted a similar effect as the standard drug.
In our research, an experimentally carrageenan-induced inflammation model was
chosen since it is considered in the literature as convenient for testing the potential
of different agents to reduce local edoema (William Carey etal. 2010; Morales et al.
2014). Our findings revealed that the application of PGAE decreased the paw edoema
in a dose-dependent manner at 1, 2, 3, and 4h following carrageenan administration.
Percentage of edoema inhibition suggested that PGAE at doses 50, 100, and 200 mg/
kg can inhibit an acute inflammatory process as verified by significant inhibition of
paw edoema in rats 3 and 4 h after carrageenan injection. PGAE in the highest dose
was the most efficient in the third and fourth hour following carrageenan-induced
inflammation. Literature data indicate that acute inflammatory response involves two
phases, the initial and the latter (Mićović etal. 2022). The initial phase occurs approx-
imately 1–2 h after carrageenan administration and includes the production of hista-
mine and serotonin by mast cells, while prostaglandin and various cytokines are
implicated in the later phase (Karim et al. 2019). NSAIDs exhibit anti-inflammatory
activity during the second phase of carrageenan-induced inflammation through cyclo-
oxygenase inhibition and suppression of prostaglandin biosynthesis by inhibiting the
enzyme cyclooxygenase (COX) (Ju et al. 2022). The anti-inflammatory potential of
8 M. KOSANIĆ ETAL.
depsidone salazinic acid and physodic acid has been demonstrated in in vitro studies
(Studzińska-Sroka and Dubino 2018) but has never been investigated in vivo in a
model of carrageenan-induced paw edoema. The potential for the anti-inflammatory
activity of both individual secondary metabolites and extracts containing them is
evident, but it is up to future research to reveal the exact molecular mechanism of
the anti-inflammatory effect of lichen secondary metabolites. Given the fact that PGAE
exerted the most intensive effect during the second phase of carrageenan-induced
inflammation, we may assume that the potential mechanism of action at least partially
involves influence on prostaglandin synthesis. Considering the similar course of paw
edoema reduction in given time intervals, we can assume that PGAE acts by a similar
mechanism as indomethacin, but additional research is necessary to examine in detail
the mechanism of anti-inflammatory action of both PGAE and individual components.
3. Experimental
The experimental part is available in Supplemental Material.
4. Conclusions
The phytochemical analysis of the PGAE revealed the presence of seven secondary
metabolites, including salazinic acid, β-orcinol carboxylic acid, 3-hydroxyphysodalic
acid, physodalic acid, physodic acid, atranorin, and chloroatranorin. This is the first
identification of salazinic acid, 3-hydroxyphysodalic acid, physodalic acid, and physodic
acid in this species. The extract exhibited significant antioxidant activity, attributed
to the presence of phenolic compounds like salazinic acid, physodic acid, and atra-
norin. PGAE also demonstrated antimicrobial activity against both bacteria and fungi,
with S. aureus, B. subtilis, F. oxysporum, C. albicans, and A. alternata being the most
susceptible microorganisms. Additionally, PGAE showed promising cytotoxic potential
against HeLa, A549, and LS174 cell lines. Moreover, PGAE exhibited anti-inflammatory
effects in a dose-dependent manner in a carrageenan-induced inflammation model,
with the highest dose (200 mg/kg) showing the most significant reduction in paw
edoema, comparable to the standard drug indomethacin. Overall, the results suggest
that PGAE contains a diverse array of bioactive compounds with potential applications
in pharmaceutical and medicinal fields. Further research is warranted to elucidate the
underlying mechanisms of its biological activities and to isolate and characterise
specific active compounds for future drug development and therapeutic applications.
Disclosure statement
The authors declare no conict of interest.
Funding
This study was funded by the Ministry of Education, Science and Technology Development of
the Republic of Serbia (Agreement No 451-03-68/2022-14/200122, 451-03-47/2023-01/200111)
and the Science Fund of the Republic of Serbia, The Program Ideas, project NES:7743504.
NATURAL PRODUCT RESEARCH 9
ORCID
Aleksandar Kočović http://orcid.org/0000-0001-9906-436X
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