Therapeutic effects of thymoquinone or capsaicin on acrylamide-induced reproductive toxicity in rats mediated by their effect on oxidative stress, inflammation, and tight junction integrity

References

• Abd-Ellah, M., et al., 2016. Quercetin attenuates di-(2-ethylhexyl) phthalate-induced testicular toxicity in adult rats. Human & Experimental Toxicology, 35 (3), 232–243.
   PubMed Web of Science ®Google Scholar
• Abdel-Daim, M.M., et al., 2020. Protective effects of thymoquinone against acrylamide-induced liver, kidney and brain oxidative damage in rats. Environmental Science and Pollution Research, 27 (30), 37709–37717.
   PubMed Web of Science ®Google Scholar
• Alyoussef, A., and Al-Gayyar, M.M., 2016. Thymoquinone ameliorated elevated inflammatory cytokines in testicular tissue and sex hormones imbalance induced by oral chronic toxicity with sodium nitrite. Cytokine, 83, 64–74.
   PubMed Web of Science ®Google Scholar
• Aras, D., et al., 2017. In Vivo acrylamide exposure may cause severe toxicity to mouse oocytes through its metabolite glycidamide. PLoS One, 12 (2), e0172026.
   PubMed Web of Science ®Google Scholar
• Aggarwal, B., et al., 2011. Identification of novel anti-inflammatory agents from Ayurvedic medicine for prevention of chronic diseases: "reverse pharmacology" and "bedside to bench" approach. Current Drug Targets, 12 (11), 1595–1653.
   PubMed Web of Science ®Google Scholar
• Atta, M.S., et al., 2018. Thymoquinone attenuates cardiomyopathy in streptozotocin-treated diabetic rats. Oxidative Medicine and Cellular Longevity, 2018, 1–10.
   Web of Science ®Google Scholar
• Bancroft, J.D., Stevens, A., and Turner, D. R., 1996. Theory and practice of histological techniques. 4th ed. New York, NY: Churchill Livingstone, 766.
   Google Scholar
• Besaratinia, A., and Pfeifer, G.P., 2007. A review of mechanisms of acrylamide carcinogenicity. Carcinogenesis, 28 (3), 519–528.
   PubMed Web of Science ®Google Scholar
• Bratthauer, G. L., 2010. The avidin–biotin complex (ABC) method and other avidin–biotin binding methods. Immunocytochemical methods and protocols. Springer, 257–270.
   Google Scholar
• Bungau, S., et al., 2019. Health benefits of polyphenols and carotenoids in age-related eye diseases. Oxidative Medicine and Cellular Longevity, 2019, 1–22. 2019.
   Web of Science ®Google Scholar
• Cheever, K.L., et al., 1985. Testicular effects of bis (2-methoxyethyl) ether in the adult male rat. Toxicology and Industrial Health, 5 (6), 1099–1109.
   Google Scholar
• Clermont, Y., Leblond, C., and Messier, B., 1959. Duration of the cycle of the seminal epithelium of the rat. Archives D'anatomie Microscopique et de Morphologie Experimentale, 48, 37–55.
   PubMedGoogle Scholar
• Dang, Y., et al., 2018. Protective effect of apigenin on acrylonitrile-induced inflammation and apoptosis in testicular cells via the NF-κB pathway in rats. Inflammation, 41 (4), 1448–1459.
   PubMed Web of Science ®Google Scholar
• Dearfield, K.L., et al., 1988. Acrylamide: its metabolism, developmental and reproductive effects, genotoxicity, and carcinogenicity. Mutation Research/Reviews in Genetic Toxicology, 195 (1), 45–77.
   Google Scholar
• Delfino, F., and Walker, W.H., 1998. Stage-specific nuclear expression of NF-kappaB in mammalian testis . Molecular Endocrinology (Baltimore, Md.), 12 (11), 1696–1707.
   PubMedGoogle Scholar
• Erdemli, Z., et al., 2019. The effects of acrylamide and Vitamin E administration during pregnancy on adult rats testis. Andrologia, e13292.
   PubMed Web of Science ®Google Scholar
• Ellman, G.L., 1959. Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics, 82 (1), 70–77.
   PubMed Web of Science ®Google Scholar
• FAO, et al., 2002. Health implications of acrylamide in food: report of a Joint FAO/WHO consultation, WHO headquarters, Geneva, Switzerland, 25–27 June 2002. World Health Organization.
   Google Scholar
• Faul, F., et al., 2007. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39 (2), 175–191.
   PubMed Web of Science ®Google Scholar
• Foster, P.M., et al., 1986. Testicular toxicity of 2-methoxyacetaldehyde, a possible metabolite of ethylene glycol monomethyl ether, in the rat. Toxicology Letters, 32 (1-2), 73–80.
   PubMed Web of Science ®Google Scholar
• Friedman, M.A., Dulak, L.H., and Stedham, M.A., 1995. A lifetime oncogenicity study in rats with acrylamide. Fundamental and Applied Toxicology, 27 (1), 95–105.
   PubMedGoogle Scholar
• Fouad, A. A., Albuali, W. H., and Jresat, I., 2014. Protective effect of thymoquinone against arsenic-induced testicular toxicity in rats. ed. Kuala Lumpur, Malaysia: International Conference on Pharmacology and Pharmaceutical Medicine (ICPPM),
   Google Scholar
• Greenwald, R., 1985. CRC Handbook of Methods for Oxygen Radical. by Thornalley PJ, Bannister JV, CRC Press, New York, 133–136.
   Google Scholar
• Gürler, H., et al., 2016. Effects of cryopreservation on sperm viability, synthesis of reactive oxygen species, and DNA damage of bovine sperm. Theriogenology, 86 (2), 562–571.
   PubMed Web of Science ®Google Scholar
• He, Y., et al., 2017. Effect of epigallocatechin-3-gallate on acrylamide-induced oxidative stress and apoptosis in PC12 cells. Human & Experimental Toxicology, 36 (10), 1087–1099.
   PubMed Web of Science ®Google Scholar
• Hoppe, P.C., and Pitts, S., 1973. Fertilization in vitro and development of mouse ova. Biology of Reproduction, 8 (4), 420–426.
   PubMed Web of Science ®Google Scholar
• Javdan, N., et al., 2018. FOXO 1 targeting by capsaicin reduces tissue damage after testicular torsion. Andrologia, 50 (4), e12987.
   Web of Science ®Google Scholar
• Jiang, X.-H., et al., 2014. Blood-testis barrier and spermatogenesis: lessons from genetically-modified mice. Asian Journal of Andrology, 16 (4), 572–580.
   PubMed Web of Science ®Google Scholar
• Kangasniemi, M., et al., 1990. Cellular regulation of follicle‐stimulating hormone (FSH) binding in rat seminiferous tubules. Journal of Andrology, 11 (4), 336–343.
   PubMedGoogle Scholar
• Katen, A.L., et al., 2016. Chronic acrylamide exposure in male mice results in elevated DNA damage in the germline and heritable induction of CYP2E1 in the testes. Biology of Reproduction, 95 (4), 15–86. 86,
   PubMed Web of Science ®Google Scholar
• Kumar, J., Das, S., and Teoh, S.L., 2018. Dietary acrylamide and the risks of developing cancer: facts to ponder. Frontiers in Nutrition, 5, 14.
   PubMed Web of Science ®Google Scholar
• Lorenzo, J.M., et al., 2018. Bioactive peptides as natural antioxidants in food products–a review. Trends in Food Science & Technology, 79, 136–147.
   Web of Science ®Google Scholar
• Mabrouk, A., and Ben Cheikh, H., 2016. Thymoquinone supplementation ameliorates lead-induced testis function impairment in adult rats. Toxicology and Industrial Health, 32 (6), 1114–1121.
   PubMed Web of Science ®Google Scholar
• Markkula, M., et al., 1995. The follicle-stimulating hormone (FSH) beta- and common alpha-subunits are expressed in mouse testis, as determined in wild-type mice and those transgenic for the FSH beta-subunit/herpes simplex virus thymidine kinase fusion gene. Endocrinology, 136 (11), 4769–4775.
   PubMed Web of Science ®Google Scholar
• Marklund, S.L., 1985. Product of extracellular-superoxide dismutase catalysis. FEBS Letters, 184 (2), 237–239.
   PubMed Web of Science ®Google Scholar
• Miller, M., Carter, D., and Sipes, I., 1982. Pharmacokinetics of acrylamide in Fisher-334 rats. Toxicology and Applied Pharmacology, 63 (1), 36–44.
   PubMed Web of Science ®Google Scholar
• Mizrak, S.C., et al., 2008. Spermatogonial stem cell sensitivity to capsaicin: an in vitro study. Reproductive Biology and Endocrinology, 6 (1), 1–9.
   PubMed Web of Science ®Google Scholar
• Morrow, C.M., et al., 2010. Claudin and occludin expression and function in the seminiferous epithelium. Philosophical Transactions of the Royal Society B: Biological Sciences, 365 (1546), 1679–1696.
   PubMed Web of Science ®Google Scholar
• Mortimer, D., Shu, M., and Tan, R., 1986. Standardization and quality control of sperm concentration and sperm motility counts in semen analysis. Human Reproduction (Oxford, England), 1 (5), 299–303.
   PubMed Web of Science ®Google Scholar
• O'Neill, J., et al., 2012. Unravelling the mystery of capsaicin: a tool to understand and treat pain. Pharmacological Reviews, 64 (4), 939–971.
   PubMed Web of Science ®Google Scholar
• Odell, I.D., and Cook, D., 2013. Immunofluorescence techniques. The Journal of Investigative Dermatology, 133 (1), e4.
   PubMed Web of Science ®Google Scholar
• Odet, F., et al., 2011. Lactate dehydrogenase C and energy metabolism in mouse sperm. Biology of Reproduction, 85 (3), 556–564.
   PubMed Web of Science ®Google Scholar
• Pakarainen, T., et al., 2007. Extragonadal LH/hCG action—not yet time to rewrite textbooks. Molecular and Cellular Endocrinology, 269 (1–2), 9–16.
   PubMed Web of Science ®Google Scholar
• Park, S., et al., 2017. Capsaicin attenuates spermatogenic cell death induced by scrotal hyperthermia through its antioxidative and anti‐apoptotic activities. Andrologia, 49 (5), e12656.
   Web of Science ®Google Scholar
• Parzefall, W., 2008. Minireview on the toxicity of dietary acrylamide. Food and Chemical Toxicology, 46 (4), 1360–1364.
   PubMed Web of Science ®Google Scholar
• Percie du Sert, N., et al., 2020. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. Journal of Cerebral Blood Flow and Metabolism, 40 (9), 1769–1777.
   PubMed Web of Science ®Google Scholar
• Pourentezari, M., et al., 2014. Effects of acrylamide on sperm parameters, chromatin quality, and the level of blood testosterone in mice. Iranian Journal of Reproductive Medicine, 12 (5), 335.
   PubMedGoogle Scholar
• Pyun, C.W., et al., 2014. In vivo protective effects of dietary curcumin and capsaicin against alcohol-induced oxidative stress. BioFactors, 40 (5), 494–500.
   PubMed Web of Science ®Google Scholar
• Rachow, S., et al., 2013. Occludin is involved in adhesion, apoptosis, differentiation and Ca2+-homeostasis of human keratinocytes: implications for tumorigenesis. PLoS One, 8 (2), e55116.
   PubMed Web of Science ®Google Scholar
• Rao, R., 2009. Occludin phosphorylation in regulation of epithelial tight junctions. Annals of the New York Academy of Sciences, 1165, 62–68.
   PubMed Web of Science ®Google Scholar
• Regueira, M., et al., 2015. FSH and bFGF regulate the expression of genes involved in Sertoli cell energetic metabolism. General and Comparative Endocrinology, 222, 124–133.
   PubMed Web of Science ®Google Scholar
• Riboldi, B.P., Vinhas, Á.M., and Moreira, J.D., 2014. Risks of dietary acrylamide exposure: a systematic review. Food Chemistry, 157, 310–322.
   PubMed Web of Science ®Google Scholar
• Rosli, F.D., et al., 2019. Ameliorative effects of thymoquinone on sperm parameters and testosterone level of nicotine-treated Sprague Dawley rats. Brazilian Archives of Biology and Technology, 62:e19180039, 1–11.
   Web of Science ®Google Scholar
• Sarioglu-Buke, A., et al., 2001. Capsaicin effectively prevents apoptosis in the contralateral testis after ipsilateral testicular torsion. BJU International, 88 (7), 787–789.
   PubMed Web of Science ®Google Scholar
• Sayed, M.M., Hassanein, K.M., and Senosy, W., 2014. Protective effects of thymoquinone and l-cysteine on cadmium-induced reproductive toxicity in rats. Toxicology Reports, 1, 612–620.
   PubMedGoogle Scholar
• Shimeda, Y., et al., 2005. Protective effects of capsaicin against cisplatin-induced nephrotoxicity in rats. Biological & Pharmaceutical Bulletin, 28 (9), 1635–1638.
   PubMed Web of Science ®Google Scholar
• Singh, S., Natarajan, K., and Aggarwal, B.B., 1996. Capsaicin (8-methyl-N-vanillyl-6-nonenamide) is a potent inhibitor of nuclear transcription factor-kappa B activation by diverse agents. Journal of Immunology (Baltimore, Md. : 1950), 157 (10), 4412–4420.
   PubMed Web of Science ®Google Scholar
• Spiridonov, V., et al., 2017. The role of capsaicin-sensitive nerves in regulating blood dehydroepiandrosterone sulfate levels in rats in normal conditions and in metabolic syndrome. Neuroscience and Behavioral Physiology, 47 (1), 33–39.
   Google Scholar
• Sumner, S.C., et al., 1999. Role of cytochrome P450 2E1 in the metabolism of acrylamide and acrylonitrile in mice. Chemical Research in Toxicology, 12 (11), 1110–1116.
   PubMed Web of Science ®Google Scholar
• Sun, J., et al., 2018. Protection of cyanidin-3-O-glucoside against acrylamide- and glycidamide-induced reproductive toxicity in leydig cells. Food and Chemical Toxicology, 119, 268–274.
   PubMed Web of Science ®Google Scholar
• Tanrıkulu-Küçük, S., et al., 2019. Dietary curcumin and capsaicin: relationship with hepatic oxidative stress and apoptosis in rats fed a high fat diet. Advances in Clinical and Experimental Medicine, 28 (8), 1013–1020.
   PubMed Web of Science ®Google Scholar
• Tareke, E., et al., 2002. Analysis of acrylamide, a carcinogen formed in heated foodstuffs. Journal of Agricultural and Food Chemistry, 50 (17), 4998–5006.
   PubMed Web of Science ®Google Scholar
• Tavakkoli, A., et al., 2017. Black seed (Nigella sativa) and its constituent thymoquinone as an antidote or a protective agent against natural or chemical toxicities. Iranian Journal of Pharmaceutical Research: IJPR, 16 (Suppl), 2.
   PubMed Web of Science ®Google Scholar
• Tietz, N., 1986. Text book of clinical chemistry (NW Tietz, eds.). Philadelphia, London, Toronto: WB Saunders Company.
   Google Scholar
• Tüfek, N.H., et al., 2015. Effects of thymoquinone on testicular structure and sperm production in male obese rats. Systems Biology in Reproductive Medicine, 61 (4), 194–204.
   PubMed Web of Science ®Google Scholar
• Uchiyama, M., and Mihara, M., 1978. Determination of malonaldehyde precursor in tisss by thiobarbituric acid test. Analytical Biochemistry, 86 (1), 271–278.
   PubMed Web of Science ®Google Scholar
• Wachtel, M., et al., 2001. Down-regulation of occludin expression in astrocytes by tumour necrosis factor (TNF) is mediated via TNF type-1 receptor and nuclear factor-kappaB activation. Journal of Neurochemistry, 78 (1), 155–162.
   PubMed Web of Science ®Google Scholar
• Wang, H., et al., 2010. Reproductive toxicity of acrylamide-treated male rats. Reproductive Toxicology, 29 (2), 225–230.
   PubMed Web of Science ®Google Scholar
• Wyrobek, A.J., et al., 1983. An evaluation of the mouse sperm morphology test and other sperm tests in nonhuman mammals: a report of the US Environmental Protection Agency Gene-Tox Program. Mutation Research/Reviews in Genetic Toxicology, 115 (1), 1–72.
   Google Scholar