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Aluminum Chloride–Induced Reproductive Toxicity in Rats: the Protective Role of Zinc Oxide Nanoparticles

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Maha S Lokman at Helwan University
Maha S Lokman
Eman Ashraf
Eman Ashraf
Eman Ashraf
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Rami Kassab at Helwan University
Rami Kassab
Ahmed E Abdel Moneim at Helwan University
Ahmed E Abdel Moneim
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Abstract and Figures

Reproductive toxicity is a major challenge associated with aluminum (Al) exposure. Therefore, this study aimed to investigate the effects of zinc oxide nanoparticle (ZnONP) treatment on Al-induced reproductive toxicity in rats. Thirty-two adult male albino rats were allocated into four equal groups as follows: control, AlCl3 orally administered group (100 mg/kg bwt), ZnONPs injected intraperitoneally (i.p.) group (4 mg/kg bwt), and ZnONPs + AlCl3–treated group. The treatment was daily extended for 42 consecutive days. Oral administration of AlCl3 showed an oxidative damage confirmed by an increase in malondialdehyde and nitric oxide levels and superoxide dismutase activity and accompanied by a decrease in glutathione content and catalase activity. Also, AlCl3 administration increased the pro-inflammatory mediator tumor necrosis factor-alpha. Furthermore, significant declines in the levels of serum male reproductive hormones testosterone, luteinizing hormone, and follicle-stimulating hormone in AlCl3-intoxicated rats were noticed. In parallel, severe histopathological alterations were observed in testis tissues. Additionally, the immunohistochemical analysis showed that AlCl3 administration potentiates cell death in the testicular tissue by elevating the immunostaining intensity signal for the pro-apoptotic protein, cysteinyl aspartate specific protease-3 (caspase-3) and a marked depletion in the cell proliferation expression marker, Ki-67, in germinal cells of AlCl3-treated group. On the other hand, the daily i.p. injection to rats with ZnONPs before AlCl3 was found to ameliorate the reproductive toxicity induced by Al administration through reducing the testicular oxidative stress and improving the inflammatory, apoptotic, and reproductive markers as well as histopathological alterations in the testis. These results suggest that ZnONPs could be used as an alternative agent to minimize the reproductive toxicity associated with Al exposure through its antioxidant, anti-inflammatory, anti-apoptotic, and reproductive modulatory activities.
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https://doi.org/10.1007/s12011-021-03010-8
Aluminum Chloride–Induced Reproductive Toxicity inRats:
theProtective Role ofZinc Oxide Nanoparticles
MahaLokman1,2· EmanAshraf2· RamiB.Kassab2,3· AhmedE.AbdelMoneim2· NabilA.El‑Yamany2
Received: 1 October 2021 / Accepted: 31 October 2021
© The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2021
Abstract
Reproductive toxicity is a major challenge associated with aluminum (Al) exposure. Therefore, this study aimed to investi-
gate the effects of zinc oxide nanoparticle (ZnONP) treatment on Al-induced reproductive toxicity in rats. Thirty-two adult
male albino rats were allocated into four equal groups as follows: control, AlCl3 orally administered group (100mg/kg bwt),
ZnONPs injected intraperitoneally (i.p.) group (4mg/kg bwt), and ZnONPs + AlCl3–treated group. The treatment was daily
extended for 42 consecutive days. Oral administration of AlCl3 showed an oxidative damage confirmed by an increase in
malondialdehyde and nitric oxide levels and superoxide dismutase activity and accompanied by a decrease in glutathione
content and catalase activity. Also, AlCl3 administration increased the pro-inflammatory mediator tumor necrosis factor-alpha.
Furthermore, significant declines in the levels of serum male reproductive hormones testosterone, luteinizing hormone, and
follicle-stimulating hormone in AlCl3-intoxicated rats were noticed. In parallel, severe histopathological alterations were
observed in testis tissues. Additionally, the immunohistochemical analysis showed that AlCl3 administration potentiates cell
death in the testicular tissue by elevating the immunostaining intensity signal for the pro-apoptotic protein, cysteinyl aspartate
specific protease-3 (caspase-3) and a marked depletion in the cell proliferation expression marker, Ki-67, in germinal cells
of AlCl3-treated group. On the other hand, the daily i.p. injection to rats with ZnONPs before AlCl3 was found to ameliorate
the reproductive toxicity induced by Al administration through reducing the testicular oxidative stress and improving the
inflammatory, apoptotic, and reproductive markers as well as histopathological alterations in the testis. These results sug-
gest that ZnONPs could be used as an alternative agent to minimize the reproductive toxicity associated with Al exposure
through its antioxidant, anti-inflammatory, anti-apoptotic, and reproductive modulatory activities.
Keywords Aluminum· Zinc nanoparticles· Oxidative stress· Inflammation· Apoptosis· Reproductive toxicity
Introduction
Aluminum (Al) is an environmental and industrial pollutant
that induces a broad spectrum of toxicity [1]. Male infer-
tility, as the most difficult form of infertility, is governed
by a variety of causative factors, including environmental
disruptors, genetic defects, physiological and endocrine fail-
ure, and testis pathologies. Al exposure is one of the impor-
tant pathogeneses for male infertility [2].
Aluminum toxicity causes severe imbalances in the oxi-
dant–antioxidant system and, as a consequence, generates
the reactive oxygen species (ROS), which are highly reac-
tive and can cause damage to the nucleic acid, lipids, and
proteins [3]. High concentrations of this metal cause degen-
eration of seminiferous tubules, presence of edema in the
intertubular compartment of the testis, presence of immature
spermatocytes in the epididymal lumen, and reduction in
serum testosterone. Sperm motility and concentration were
altered in rats exposed to Al as well. Furthermore, epithelial
cells from the epididymis might change their structure and
function after Al exposure. Al-induced toxicity may affect
reproductive organ functions via oxidative stress and nitric
oxide overproduction [4].
* Ahmed E. Abdel Moneim
aest1977@hotmail.com;
ahmed_abdelmoneim@science.helwan.edu.eg
1 Biology Department, College ofScience andHumanities,
Prince Sattam bin Abdul Aziz University, Alkharj,
SaudiArabia
2 Department ofZoology andEntomology, Faculty ofScience,
Helwan University, Cairo, Egypt
3 Department ofBiology, Faculty ofScience andArts,
Al-Baha University, Almakhwah, Al-Baha, SaudiArabia
/ Published online: 6 November 2021
Biological Trace Element Research (2022) 200:4035–4044
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Similar to our findings, ZnO-NPs were found to be efficient in decreasing MDA and increasing reduced glutathione in diabetic rats' testes [31]. Moreover, treating rats with ZnO-NPs for 6 weeks succeeded to defend against aluminum (Al)-induced oxidative stress in the testes [32]. On the other side, Ziamajidi et al. [33] showed that ZnO-NPs at 200 mg/kg induced oxidative stress in the testes. ...
... All histopathological Zn deficiency has been linked to a malfunction in the normal development of Leydig cells as well as impairment in LH receptors, both of which have a negative impact on testosterone biosynthesis [40]. In addition, the favorable effects of cZnO and ZnO-NPs on testosterone and sperm quality may potentially be attributable to their antioxidant activity, which protects testicular tissues from BPA-induced oxidative damage [32], which confirmed our findings. More notably, ZnO-NPs outperformed cZnO in terms of testosterone production, which could be attributed to ZnO-NPs' stronger antioxidant activity than the conventional version [20]. ...
... Zn was a promising treatment to protect thyroid gland against potassium dichromate thyrotoxicity [45]. Additionally, the beneficial effects on thyroid hormones may be due to the high antioxidant activity of cZnO or ZnO-NPs [32], which may protect the thyroid tissue from oxidative damage. ...
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... In this study, the increase in serum and testes MDA levels following exposure to AlCl3 can be attributed to an increased burden of oxidative stress. This is likely due to the production of reactive oxygen species (ROS), which in turn induce lipid and protein oxidation, as previously mentioned by recent studies [27][28][29]. Additionally, there was a reduction in TAC activity and sperm count. ...
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Full-text available
  • May 2019
Aluminum is recognized as a public health concern because of its potential toxic effects on human health. Therefore, the present experiment was undertaken to determine the effectiveness of curcumin (CUR) in reducing the hepatotoxicity induced by aluminum chloride (AlCl3) in animals. In this experimental study, forty male rats were allocated to five groups (N = 8), viz. no treatment (control), solvent (DMSO or distilled water), CUR (10 mg/kg B.W.), AlCl3 (10 mg/kg B.W.), and CUR+AlCl3 (each with 10 mg/kg B.W.). Treatments were performed by intra-peritoneal injections for 28 days. On the final day, animals were sacrificed, and liver function markers in blood plasma, hepatic antioxidants, and lipid peroxidation index in liver homogenate were estimated. AlCl3 treatment resulted in a significant increase in plasma AST, ALT, ALP and LDH activities with decreased total protein compared to control. AlCl3 significantly reduced superoxide dismutase (SOD), catalase (CAT) and glutathione (GSH) levels but increased malondialdehyde (MDA) level in the liver compared to control. AlCl3 also caused various histopathological changes in the livers of rats. Curcumin could normalize nearly all these parameters. CUR improved levels of changes in different parameters when was combined with AlCl3. It is concluded that CUR has beneficial effects being able to antagonize AlCl3 toxicity.
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The influence of melatonin supplementation against aluminum-induced toxicity in brains of male rats
Article
Full-text available
  • Feb 2019
Aluminum (Al), an ubiquitous element in nature, enters the body primarily through gastrointestinal tract, respiratory system and skin. Being a powerful neurotoxin for human brain, Al was reported to be involved in the etiology of Alzheimer's disease due to its easy access and accumulation in the central nervous system. Melatonin (Mel) is a tryptophan-derived neurohormone in animals and plants, and produced in the pineal gland of all mammalian species. The present study examines the effects of Mel on Al-induced oxidative stress, inflammation, tissue factor production and brain damage in rat brain. Wistar albino rats were divided into four groups. Group I: control animals; Group II: rats injected with 10 mg/kg Mel; Group III: rats injected with 5 mg/kg Al 2 (SO 4 ) 3 ; and Group IV: rats injected combination of Al and Mel (5 mg/kg Al 2 (SO 4 ) 3 and 10 mg/kg Mel). Animals were injected three times a week for one month. At the end of the month, rats were sacrificed, their brains were removed. It was found that lipid peroxidation, protein carbonyl, advanced oxidation protein products, hydroxyproline levels, tissue factor, catalase, superoxide dismutase, glutathione peroxidase, glutathione reductase, myeloperoxidase, acetylcholine esterase, alkaline phosphatase, acid phosphatase and glucose-6-phosphate dehydrogenase activities were increased, while paraoxonase, arylesterase, sodium potassium ATPase activities and glutathione levels were decreased in the Al-treated group. Mel treatment reversed these changes by demonstrating significant antioxidant effects. Results indicated that Mel has potential therapeutic value against Al-induced oxidative stress in the rat brain tissue and these effects may be related to its antioxidant activities.
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Potential toxicity of aluminum and fluoride on some biochemical aspects of male rat's offspring
Article
Full-text available
  • Mar 2019
Background: This work was designed to evaluate the potential hazards of sodium fluoride (NaF) and aluminum chloride (AlCl 3) given separately or in conjugation throughout the prenatal and up to weaning time or till the postnatal 70th day. The levels of the following parameters were then assessed; vitamin C (ascorbic acid), glutathione (GSH) and oxidized glutathione (GSSH), malondialdehyde (MDA), total protein, albumin, total calcium, ionized calcium, creatinine, urea, uric acid, and bilirubin. In addition, the activities of alanine aminotransferase (ALT) and aspartate aminotransferase (AST) were determined. In this study, female pregnant rats were allocated into four groups. The first received the drinking deionized water and served as a normal group, the second was given a daily dose of NaF (0.15 g/L) dissolved in deionized water from day 6 of gestation till the end of the weaning period, and the third was given a daily dose of AlCl 3 (500 mg/L) for the same period of time. The fourth group was given drinking water containing combined doses of NaF + AlCl 3 for a similar length of time. Each group was further divided into two subgroups; the first continued to be treated with the same pollutants in drinking deionized water at the same dose level until the age of 70 days, whereas the second group was supplied with pure deionized water free from the intoxicating substances for the same period of time.
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Ameliorative Effect of Zinc Oxide Nanoparticles on Nicotine Induced Testicular Dysfunction; Biochemical and Histological Study
Article
  • Jun 2019
Objective The aim of this study was to evaluate potential impact of zinc oxide nanoparticle on the possible testicular toxicity induced by nicotine. Methods 24 adult male albino rats were divided into four groups; negative control group, zinc oxide nanoparticle group: rats were received 5 mg/kg/day zinc oxide nanoparticles orally, nicotine treated group: rats were administered nicotine (1 mg/kg/day) intraperitoneally and nicotine with zinc oxide nanoparticles: rats were treated with nicotine and zinc oxide nanoparticles daily for 28 days. Serum testosterone level, testicular malondialdehyde, SOD and catalase activities were measured. Testes were examined by light and electron microscopes as well. Results Significant decreases of serum testosterone level, testicular SOD and catalase activity and significant increase of testicular MDA in nicotine treated group when compared with control group were detected. Zinc oxide nanoparticles administration reversed these changes. Conclusion Zinc oxide nanoparticles ameliorated nicotine induced testicular dysfunction.
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