Role of Bisphenol-A Induced Oxidative Stress in Spermatogenesis of Wistar Albino Rats

Authors

  • Raksha Sharma Research Scholar, Department of Zoology, Reproductive Physiology Lab, University of Rajasthan, Jaipur, Rajasthan 302004, India.
  • Manish Kumar Sharma Assistant Professor, Department of Zoology, Raj Rishi Autonomous College, Alwar, Rajasthan 301001, India.
  • Seema Srivastava Professor and Head, Department of Zoology, Reproductive Physiology Lab, University of Rajasthan, Jaipur, Rajasthan 302004, India.

DOI:

https://doi.org/10.48165/

Keywords:

Antioxidants, Bisphenol-A, Spermatogenesis, Stereological evaluation

Abstract

Bisphenol-A is a known endocrine disruptor and  reproductive toxicant. It has been associated with epigenetic  modification, autophagy, oxidative stress and apoptosis.  Many studies have indicated interferences in  spermatogenesis due to Bisphenol-A exposure. Since  oxidative stress plays important role in regulation of various  stages of spermatogenesis, therefore, excessive generation of  Reactive Oxygen Species can also have effects on  spermatogenesis that may reach beyond hormonal  regulations. Three doses of Bisphenol-A (10, 50, and 100  mg/kg body weight) were investigated for its effect on  testicular antioxidant status (Catalase, Glutathione,  Glutathione S Transferase, , Glutathione Peroxidase and  Glutathione disulphide). Stereological estimation of germ  cells (spermatogonia, spermatocytes, spermatids) and  Sertoli cells was carried out to spermatogenic interferences  in the histological architecture. Cause and effect analysis  was tested to elucidate association between oxidative stress  and numeric spermatogenesis. This study indicated severe  decline (30-70%) in the activities of major antioxidant  enzymes in response to Bisphenol-A exposure. Higher doses  (50 and 100 mg Bisphenol-A) induced maximum damage in  histological architecture of testis. Seminiferous tubules  indicated loss of germ cells and consequently sperms in the  lumen. The histological evaluation went in accordance with  stereological evaluation of germ cells. A pattern in  disorientation of germ cells was intercepted through  morphometric assessment that corresponded to activity of  antioxidants. Bisphenol-A induced oxidative stress plays  important role in regulation of spermatogenesis. There was  a clear parallel between number of germ cell and Sertoli cell  decline and loss of activity of major antioxidants. BPA  induced oxidative stress had differential effect on germ  cells, where spermatogonia and spermatids appeared to  have low toleration than spermatocytes. 

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References

Global Industry Analysts. Inc. (2015). Bisphenol A Market Trends. Retrieved from

https://www.strategyr.com/MarketResea rch/Bisphenol_A_Market_Trends.asp. 2. Experts, I. (2016). Bisphenol-A-a global market overview. Columbus, OH: Hexion Inc.

Statista (2020): Chemicals & Resources Chemical Industry. U.S. bisphenol A production volume 1990-2019. 2020. Published by Lucía Fernández, Aug 5, 2021. Retrieved from https://www.statista.com/statistics/9747

/us-bisphenol-a-production-volume/. 4. Almeida, S., Raposo, A., Almeida‐González, M., & Carrascosa, C. (2018). Bisphenol A: Food exposure and impact on human health. Comprehensive reviews in food science and food safety, 17(6), 1503-1517.

Vandenberg, L. N., Hauser, R., Marcus, M., Olea, N., & Welshons, W. V. (2007). Human exposure to bisphenol A (BPA). Reproductive toxicology, 24(2), 139- 177.

Kang, J. H., Kondo, F., & Katayama, Y. (2006). Human exposure to bisphenol A. Toxicology, 226(2-3), 79-89.

European Food Safety Authority (EFSA). (2004). Opinion of the Scientific Panel on food additives, flavourings, processing

aids and materials in contact with food (AFC) related to 2, 2‐bis (4‐hydroxyphenyl) propane bis (2, 3‐epoxypropyl) ether (Bisphenol A diglycidyl ether, BADGE). REF. No 13510 and 39700. EFSA Journal, 2(7), 86.

Chapin, R. E., Adams, J., Boekelheide, K., Gray Jr, L. E., Hayward, S. W., Lees, P. S., ... & Woskie, S. R. (2008). NTP‐CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A. Birth Defects Research Part B: Developmental and Reproductive Toxicology, 83(3), 157-395.

Vandenberg, L. N., Ehrlich, S., Belcher, S. M., Ben-Jonathan, N., Dolinoy, D. C., Hugo, E. R., ...& vomSaal, F. S. (2013). Low dose effects of bisphenol A: An integrated review of in vitro, laboratory animal, and epidemiology studies. Endocrine disruptors, 1(1), e26490.

World Health Organization. (2011). Joint FAO/WHO expert meeting to review toxicological and health aspects of bisphenol A: final report, including report of stakeholder meeting on bisphenol A, 1- 5 November 2010, Ottawa, Canada.

Shelby, M. D. (2008). NTP-CERHR monograph on the potential human reproductive and developmental effects of bisphenol A. Ntpcerhrmon, (22), v-vii.

Geens, T., Goeyens, L., Kannan, K., Neels, H., & Covaci, A. (2012). Levels of bisphenol-A in thermal paper receipts from Belgium and estimation of human exposure. Science of the total environment, 435, 30-33.

Thayer, K. A., Doerge, D. R., Hunt, D., Schurman, S. H., Twaddle, N. C., Churchwell, M. I., ... & Birnbaum, L. S. (2015). Pharmacokinetics of bisphenol A in humans following a single oral administration. Environment

international, 83, 107-115.

Völkel, W., Colnot, T., Csanády, G. A., Filser, J. G., & Dekant, W. (2002). Metabolism and kinetics of bisphenol A in humans at low doses following oral administration. Chemical research in toxicology, 15(10), 1281-1287.

Calafat, A. M., Ye, X., Wong, L. Y., Reidy, J. A., & Needham, L. L. (2008). Exposure of the US population to bisphenol A and 4- tertiary-octylphenol: 2003– 2004. Environmental health perspectives, 116(1), 39-44.

European Food Safety Authority (EFSA). (2015). Scientific Opinion on the Risks to Public Health Related to the Presence of Bisphenol A (BPA) in Foodstuffs: Executive Summary, 1st ed. Parma: European Food Safety Authority.

Dodson, R. E., Nishioka, M., Standley, L. J., Perovich, L. J., Brody, J. G., &Rudel, R. A. (2012). Endocrine disruptors and asthma-associated chemicals in consumer products. Environmental health perspectives, 120(7), 935-943.

Pottenger, L. H., Domoradzki, J. Y., Markham, D. A., Hansen, S. C., Cagen, S. Z., &WaechterJr, J. M. (2000). The relative bioavailability and metabolism of bisphenolA in rats is dependent upon the route of administration. Toxicological Sciences, 54(1), 3-18.

Negishi, T., Tominaga, T., Ishii, Y., Kyuwa, S., Hayasaka, I., Kuroda, Y., & Yoshikawa, Y. (2004). Comparative study on toxicokinetics of bisphenol A in F344 rats, monkeys (Macacafascicularis), and chimpanzees (Pan troglodytes). Experimental animals, 53(4), 391-394.

Tominaga, T., Negishi, T., Hirooka, H., Miyachi, A., Inoue, A., Hayasaka, I., & Yoshikawa, Y. (2006). Toxicokinetics of bisphenol A in rats, monkeys and chimpanzees by the LC–MS/MS method. Toxicology, 226(2-3), 208-217.

Lv, Y., Lu, S., Dai, Y., Rui, C., Wang, Y., Zhou, Y., ...& Fan, R. (2017). Higher dermal exposure of cashiers to BPA and its association with DNA oxidative damage. Environment international, 98, 69- 74.

Lee, I., Kim, S., Kim, K. T., Kim, S., Park, S., Lee, H., ...& Choi, K. (2018). Bisphenol A exposure through receipt handling and its association with insulin resistance among female cashiers. Environment international, 117, 268-275.

Akingbemi, B. T., Sottas, C. M., Koulova, A. I., Klinefelter, G. R., & Hardy, M. P. (2004). Inhibition of testicular steroidogenesis by the xenoestrogenbisphenol A is associated with reduced pituitary luteinizing hormone secretion and decreased steroidogenic enzyme gene expression in rat Leydig cells. Endocrinology, 145(2), 592- 603.

Nanjappa, M. K., Simon, L., & Akingbemi, B. T. (2012). The industrial chemical bisphenol A (BPA) interferes with proliferative activity and development of steroidogenic capacity in rat Leydig cells. Biology of reproduction, 86(5), 135-1.

Olukole, S. G., Ola-Davies, E. O., Lanipekun, D. O., &Oke, B. O. (2020). Chronic exposure of adult male Wistar rats to bisphenol A causes testicular oxidative stress: Role of gallic acid. Endocrine regulations, 54(1), 14-21.

Celino, F. T., Yamaguchi, S., Miura, C., Ohta, T., Tozawa, Y., Iwai, T., & Miura, T. (2011). Tolerance of spermatogonia to oxidative stress is due to high levels of Zn and Cu/Zn superoxide dismutase. Plos one, 6(2), e16938.

Kaur, S., Saluja, M., & Bansal, M. P. (2018). Bisphenol A induced oxidative stress and apoptosis in mice testes: Modulation by selenium. Andrologia, 50(3), e12834.

CPCSEA.(2010) Guidelines on the regulation of scientific experiments on animals. New Delhi: Ministry of Environment and Forests, CPCSEA Standard Operating Procedures for Institutional Animals Ethics Committee (IAEC).

Aebi, H. (1974). Catalase. In Methods of enzymatic analysis (pp. 673-684). Academic press.

Wood, J. L. (1970). In Metabolic Conjugation and Metabolic hydrolysis (Fishman, WH ed.,). Academic press, Newyork, 2, 261-299.

Hissin, P. J., & Hilf, R. (1976). A fluorometric method for determination of oxidized and reduced glutathione in tissues. Analytical biochemistry, 74(1), 214- 226.

Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. Journal of biological Chemistry, 249(22), 7130-7139.

Zhengwei, Y., Wreford, N. G., Schlatt, S., Weinbauer, G. F., Nieschlag, E., & McLachlan, R. I. (1998). Acute and specific impairment of spermatogonial development by GnRH antagonist induced gonadotrophin withdrawal in the adult macaque (Macacafascicularis). Reproduction, 112(1), 139-147.

Wreford, N. G. (1995). Theory and practice of stereological techniques applied to the estimation of cell number and nuclear volume in the testis. Microscopy research and technique, 32(5), 423-436.

Gundersen, H. J., & Jensen, E. B. (1987). The efficiency of systematic sampling in stereology and its prediction. Journal of microscopy, 147(3), 229-263.

deKretser, D. M., Loveland, K. L., Meinhardt, A., Simorangkir, D., &Wreford, N. (1998). Spermatogenesis. Human

reproduction, 13(suppl_1), 1-8.

Huleihel, M., &Lunenfeld, E. (2004). Regulation of spermatogenesis by paracrine/autocrine testicular factors. Asian Journal of Andrology, 6(3), 259-268.

Nishimura, H., & L’Hernault, S. W. (2017). Spermatogenesis. Current Biology, 27(18), R988-R994.

Maiorino, M., & Ursini, F. (2002). Oxidative stress, spermatogenesis and fertility.

Aitken, R. J., & Clarkson, J. S. (1987). Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. Reproduction, 81(2), 459-469.

Jin, P., Wang, X., Chang, F., Bai, Y., Li, Y., Zhou, R., & Chen, L. (2013). Low dose bisphenol A impairs spermatogenesis by suppressing reproductive hormone production and promoting germ cell apoptosis in adult rats. Journal of biomedical research, 27(2), 135.

Santiago, J., Silva, J. V., Santos, M. A., & Fardilha, M. (2021). Fighting Bisphenol A Induced Male Infertility: The Power of Antioxidants. Antioxidants, 10(2), 289.

Hu, W., Dong, T., Wang, L., Guan, Q., Song, L., Chen, D., ...& Wang, X. (2017). Obesity aggravates toxic effect of BPA on spermatogenesis. Environment international, 105, 56-65.

Khalaf, A. A., Ahmed, W. M. S., Moselhy, W. A., Abdel-Halim, B. R., & Ibrahim, M. A. (2019). Protective effects of selenium and nano-selenium on bisphenol-induced reproductive toxicity in male rats. Human & experimental toxicology, 38(4), 398-408.

***********************************************

Traverso, N., Ricciarelli, R., Nitti, M., Marengo, B., Furfaro, A. L., Pronzato, M. A., ...& Domenicotti, C. (2013). Role of glutathione in cancer progression and chemoresistance. Oxidative Med Cell Longev 2013: 972913.

Koster, J. F., Slee, R. G., Rutten-Van Beysterveld, C. C. M., & Montfoort, A. (1983). The effect of (13 OOH) linoleic acid on human erythrocytes and on erythrocyte ghosts. Biochimicaet Biophysica Acta (BBA)- Lipids and Lipid Metabolism, 754(3), 238-242.

Spector, A., Huang, R. R. C., & Wang, G. M. (1985). The effect of H2O2 on lens epithelial cell glutathione. Current eye research, 4(12), 1289-1295.

Jongkind, J. F., Verkerk, A., & Baggen, R. G. (1989). Glutathione metabolism of human vascular endothelial cells under peroxidative stress. Free Radical Biology and Medicine, 7(5), 507-512.

González-Rojo, S., Lombó, M., Fernández Díez, C., & Herráez, M. P. (2019). Male exposure to bisphenola impairs spermatogenesis and triggers histone hyperacetylation in zebrafish testes. Environmental Pollution, 248, 368-

Ge, L. C., Chen, Z. J., Liu, H., Zhang, K. S., Su, Q., Ma, X. Y., ... & Wang, H. S. (2014). Signaling related with biphasic effects of bisphenol A (BPA) on Sertoli cell proliferation: a comparative proteomic analysis. BiochimicaetBiophysicaActa (BBA)- General Subjects, 1840(9), 2663-2673.

Munir, B., Qadir, A., & Tahir, M. (2017). Negative effects of bisphenol A on testicular functions in albino rats and their abolitions with Tribulusterristeris L. Brazilian journal of pharmaceutical Sciences, 53.

Almansa-Ordonez, A., Bellido, R., Vassena, R., Barragan, M., & Zambelli, F. (2020). Oxidative stress in reproduction: a mitochondrial perspective. Biology, 9(9), 269.

Fujiwara, Y., Miyazaki, W., Koibuchi, N., &Katoh, T. (2018). The effects of low-dose Bisphenol A and Bisphenol F on neural differentiation of a fetal brain-derived neural progenitor cell line. Frontiers in Endocrinology, 9, 24.

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Published

2022-06-15

Issue

Vol. 41 No. 1 (2022): Bulletin of Pure and Applied Sciences-Zoology (Jan-Jun) 2022

Section

Articles

How to Cite

Role of Bisphenol-A Induced Oxidative Stress in Spermatogenesis of Wistar Albino Rats . (2022). Bulletin of Pure & Applied Sciences- Zoology , 41(1), 131–142. https://doi.org/10.48165/