DOI QR코드

DOI QR Code

Understanding the molecular mechanisms of bisphenol A action in spermatozoa

  • Rahman, Md Saidur (Department of Animal Science and Technology and BET Research Institute, Chung-Ang University) ;
  • Pang, Myung-Geol (Department of Animal Science and Technology and BET Research Institute, Chung-Ang University)
  • Received : 2019.05.13
  • Accepted : 2019.07.25
  • Published : 2019.09.30

Abstract

Bisphenol A (BPA) is an endocrine-disrupting chemical that is capable of interfering with the normal function of the endocrine system in the body. Exposure to this chemical from BPA-containing materials and the environment is associated with deleterious health effects, including male reproductive abnormalities. A search of the literature demonstrated that BPA, as a toxicant, directly affects the cellular oxidative stress response machinery. Because of its hormone-like properties, it can also bind with specific receptors in target cells. Therefore, the tissue-specific effects of BPA mostly depend on its endocrine-disrupting capabilities and the expression of those particular receptors in target cells. Although studies have shown the possible mechanisms of BPA action in various cell types, a clear consensus has yet to be established. In this review, we summarize the mechanisms of BPA action in spermatozoa by compiling existing information in the literature.

Keywords

Acknowledgement

Supported by : National Research Foundation of Korea (NRF)

References

  1. Rahman MS, Kwon WS, Karmakar PC, Yoon SJ, Ryu BY, Pang MG. Gestational exposure to bisphenol A affects the function and proteome profile of F1 spermatozoa in adult mice. Environ Health Perspect 2017;125:238-45. https://doi.org/10.1289/EHP378
  2. Rahman MS, Kwon WS, Ryu DY, Khatun A, Karmakar PC, Ryu BY, et al. Functional and proteomic alterations of F1 capacitated spermatozoa of adult mice following gestational exposure to bisphenol A. J Proteome Res 2018;17:524-35. https://doi.org/10.1021/acs.jproteome.7b00668
  3. Erler C, Novak J. Bisphenol a exposure: human risk and health policy. J Pediatr Nurs 2010;25:400-7. https://doi.org/10.1016/j.pedn.2009.05.006
  4. Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev 2009;30:75-95. https://doi.org/10.1210/er.2008-0021
  5. Rahman MS, Kwon WS, Lee JS, Yoon SJ, Ryu BY, Pang MG. Bisphenol- A affects male fertility via fertility-related proteins in spermatozoa. Sci Rep 2015;5:9169. https://doi.org/10.1038/srep09169
  6. Rahman MS, Kwon WS, Yoon SJ, Park YJ, Ryu BY, Pang MG. A novel approach to assessing bisphenol-A hazards using an in vitro model system. BMC Genomics 2016;17:577. https://doi.org/10.1186/s12864-016-2979-5
  7. Rochester JR. Bisphenol A and human health: a review of the literature. Reprod Toxicol 2013;42:132-55. https://doi.org/10.1016/j.reprotox.2013.08.008
  8. Heindel JJ, Newbold RR, Bucher JR, Camacho L, Delclos KB, Lewis SM, et al. NIEHS/FDA CLARITY-BPA research program update. Reprod Toxicol 2015;58:33-44. https://doi.org/10.1016/j.reprotox.2015.07.075
  9. Ryu DY, Rahman MS, Pang MG. Determination of highly sensitive biological cell model systems to screen BPA-related health hazards using Pathway Studio. Int J Mol Sci 2017;18:E1909. https://doi.org/10.3390/ijms18091909
  10. Flint S, Markle T, Thompson S, Wallace E. Bisphenol A exposure, effects, and policy: a wildlife perspective. J Environ Manage 2012;104:19-34. https://doi.org/10.1016/j.jenvman.2012.03.021
  11. Faheem M, Khaliq S, Lone KP. Disruption of the reproductive axis in freshwater fish, catla, after bisphenol-A exposure. Zoolog Sci 2017;34:438-44. https://doi.org/10.2108/zs170009
  12. de Lamirande E, Gagnon C. Impact of reactive oxygen species on spermatozoa: a balancing act between beneficial and detrimental effects. Hum Reprod 1995;10 Suppl 1:15-21. https://doi.org/10.1093/humrep/10.suppl_1.15
  13. Rahman MS, Kwon WS, Lee JS, Kim J, Yoon SJ, Park YJ, et al. Sodium nitroprusside suppresses male fertility in vitro. Andrology 2014;2:899-909. https://doi.org/10.1111/j.2047-2927.2014.00273.x
  14. Agarwal A, Sharma RK, Nallella KP, Thomas AJ Jr, Alvarez JG, Sikka SC. Reactive oxygen species as an independent marker of male factor infertility. Fertil Steril 2006;86:878-85. https://doi.org/10.1016/j.fertnstert.2006.02.111
  15. Aitken RJ, Paterson M, Fisher H, Buckingham DW, van Duin M. Redox regulation of tyrosine phosphorylation in human spermatozoa and its role in the control of human sperm function. J Cell Sci 1995;108(Pt 5):2017-25. https://doi.org/10.1242/jcs.108.5.2017
  16. Gassman NR. Induction of oxidative stress by bisphenol A and its pleiotropic effects. Environ Mol Mutagen 2017;58:60-71. https://doi.org/10.1002/em.22072
  17. Takayanagi S, Tokunaga T, Liu X, Okada H, Matsushima A, Shimohigashi Y. Endocrine disruptor bisphenol A strongly binds to human estrogen-related receptor gamma (ERRgamma) with high constitutive activity. Toxicol Lett 2006;167:95-105. https://doi.org/10.1016/j.toxlet.2006.08.012
  18. Nadal A, Ropero AB, Laribi O, Maillet M, Fuentes E, Soria B. Nongenomic actions of estrogens and xenoestrogens by binding at a plasma membrane receptor unrelated to estrogen receptor alpha and estrogen receptor beta. Proc Natl Acad Sci U S A 2000;97:11603-8. https://doi.org/10.1073/pnas.97.21.11603
  19. Bonefeld-Jorgensen EC, Long M, Hofmeister MV, Vinggaard AM. Endocrine-disrupting potential of bisphenol A, bisphenol A dimethacrylate, 4-n-nonylphenol, and 4-n-octylphenol in vitro: new data and a brief review. Environ Health Perspect 2007;115 Suppl 1:69-76. https://doi.org/10.1289/ehp.9368
  20. Zoeller RT, Bansal R, Parris C. Bisphenol-A, an environmental contaminant that acts as a thyroid hormone receptor antagonist in vitro, increases serum thyroxine, and alters RC3/neurogranin expression in the developing rat brain. Endocrinology 2005;146:607-12. https://doi.org/10.1210/en.2004-1018
  21. Naz RK, Sellamuthu R. Receptors in spermatozoa: are they real? J Androl 2006;27:627-36. https://doi.org/10.2164/jandrol.106.000620
  22. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev 2007;87:905-31. https://doi.org/10.1152/physrev.00026.2006
  23. Ptak A, Gregoraszczuk EL. Bisphenol A induces leptin receptor expression, creating more binding sites for leptin, and activates the JAK/Stat, MAPK/ERK and PI3K/Akt signalling pathways in human ovarian cancer cell. Toxicol Lett 2012;210:332-7. https://doi.org/10.1016/j.toxlet.2012.02.003
  24. Ptak A, Rak-Mardyla A, Gregoraszczuk EL. Cooperation of bisphenol A and leptin in inhibition of caspase-3 expression and activity in OVCAR-3 ovarian cancer cells. Toxicol In Vitro 2013;27:1937-43. https://doi.org/10.1016/j.tiv.2013.06.017
  25. Wan X, Ru Y, Chu C, Ni Z, Zhou Y, Wang S, et al. Bisphenol A accelerates capacitation-associated protein tyrosine phosphorylation of rat sperm by activating protein kinase A. Acta Biochim Biophys Sin (Shanghai) 2016;48:573-80. https://doi.org/10.1093/abbs/gmw039
  26. Smith TB, Dun MD, Smith ND, Curry BJ, Connaughton HS, Aitken RJ. The presence of a truncated base excision repair pathway in human spermatozoa that is mediated by OGG1. J Cell Sci 2013;126(Pt 6):1488-97. https://doi.org/10.1242/jcs.121657
  27. Kwon WS, Rahman MS, Lee JS, Kim J, Yoon SJ, Park YJ, et al. A comprehensive proteomic approach to identifying capacitation related proteins in boar spermatozoa. BMC Genomics 2014;15:897. https://doi.org/10.1186/1471-2164-15-897
  28. Rahman MS, Kwon WS, Pang MG. Prediction of male fertility using capacitation-associated proteins in spermatozoa. Mol Reprod Dev 2017;84:749-59. https://doi.org/10.1002/mrd.22810
  29. Brohi RD, Huo LJ. Posttranslational modifications in spermatozoa and effects on male fertility and sperm viability. OMICS 2017;21:245-56. https://doi.org/10.1089/omi.2016.0173
  30. Wang H, Ding Z, Shi QM, Ge X, Wang HX, Li MX, et al. Anti-androgenic mechanisms of Bisphenol A involve androgen receptor signaling pathway. Toxicology 2017;387:10-6. https://doi.org/10.1016/j.tox.2017.06.007
  31. Holdcraft RW, Braun RE. Hormonal regulation of spermatogenesis. Int J Androl 2004;27:335-42. https://doi.org/10.1111/j.1365-2605.2004.00502.x
  32. McLachlan RI, Wreford NG, Robertson DM, de Kretser DM. Hormonal control of spermatogenesis. Trends Endocrinol Metab 1995;6:95-101. https://doi.org/10.1016/1043-2760(94)00215-P
  33. Liang H, Xu W, Chen J, Shi H, Zhu J, Liu X, et al. The association between exposure to environmental bisphenol A and gonadotropic hormone levels among men. PLoS One 2017;12:e0169217. https://doi.org/10.1371/journal.pone.0169217
  34. Romano ME, Webster GM, Vuong AM, Thomas Zoeller R, Chen A, Hoofnagle AN, et al. Gestational urinary bisphenol A and maternal and newborn thyroid hormone concentrations: the HOME Study. Environ Res 2015;138:453-60. https://doi.org/10.1016/j.envres.2015.03.003
  35. Krajewska-Kulak E, Sengupta P. Thyroid function in male infertility. Front Endocrinol (Lausanne) 2013;4:174. https://doi.org/10.3389/fendo.2013.00174
  36. Manfo FP, Jubendradass R, Nantia EA, Moundipa PF, Mathur PP. Adverse effects of bisphenol A on male reproductive function. Rev Environ Contam Toxicol 2014;228:57-82. https://doi.org/10.1007/978-3-319-01619-1_3
  37. Liu C, Duan W, Li R, Xu S, Zhang L, Chen C, et al. Exposure to bisphenol A disrupts meiotic progression during spermatogenesis in adult rats through estrogen-like activity. Cell Death Dis 2013;4:e676. https://doi.org/10.1038/cddis.2013.203
  38. D'Souza R, Gill-Sharma MK, Pathak S, Kedia N, Kumar R, Balasinor N. Effect of high intratesticular estrogen on the seminiferous epithelium in adult male rats. Mol Cell Endocrinol 2005;241:41-8. https://doi.org/10.1016/j.mce.2005.04.011
  39. Hatef A, Alavi SM, Abdulfatah A, Fontaine P, Rodina M, Linhart O. Adverse effects of bisphenol A on reproductive physiology in male goldfish at environmentally relevant concentrations. Ecotoxicol Environ Saf 2012;76:56-62. https://doi.org/10.1016/j.ecoenv.2011.09.021
  40. Hatef A, Zare A, Alavi SM, Habibi HR, Linhart O. Modulations in androgen and estrogen mediating genes and testicular response in male goldfish exposed to bisphenol A. Environ Toxicol Chem 2012;31:2069-77. https://doi.org/10.1002/etc.1919
  41. Williams C, Bondesson M, Krementsov DN, Teuscher C. Gestational bisphenol A exposure and testis development. Endocr Disruptors (Austin) 2014;2:e29088. https://doi.org/10.4161/endo.29088
  42. Delbes G, Levacher C, Habert R. Estrogen effects on fetal and neonatal testicular development. Reproduction 2006;132:527-38. https://doi.org/10.1530/rep.1.01231
  43. Jefferson WN, Couse JF, Banks EP, Korach KS, Newbold RR. Expression of estrogen receptor beta is developmentally regulated in reproductive tissues of male and female mice. Biol Reprod 2000;62:310-7. https://doi.org/10.1095/biolreprod62.2.310
  44. Asadi N, Bahmani M, Kheradmand A, Rafieian-Kopaei M. The impact of oxidative stress on testicular function and the role of antioxidants in improving it: a review. J Clin Diagn Res 2017;11:IE01-5.
  45. Kaur S, Saluja M, Bansal MP. Bisphenol A induced oxidative stress and apoptosis in mice testes: modulation by selenium. Andrologia 2018;50.
  46. El-Beshbishy HA, Aly HA, El-Shafey M. Lipoic acid mitigates bisphenol A-induced testicular mitochondrial toxicity in rats. Toxicol Ind Health 2013;29:875-87. https://doi.org/10.1177/0748233712446728
  47. Packer L, Witt EH, Tritschler HJ. Alpha-lipoic acid as a biological antioxidant. Free Radic Biol Med 1995;19:227-50. https://doi.org/10.1016/0891-5849(95)00017-R
  48. Agarwal A, Virk G, Ong C, du Plessis SS. Effect of oxidative stress on male reproduction. World J Mens Health 2014;32:1-17. https://doi.org/10.5534/wjmh.2014.32.1.1
  49. Rando OJ. Daddy issues: paternal effects on phenotype. Cell 2012;151:702-8. https://doi.org/10.1016/j.cell.2012.10.020
  50. Skinner MK. Metabolic disorders: fathers' nutritional legacy. Nature 2010;467:922-3. https://doi.org/10.1038/467922a
  51. Donkin I, Barres R. Sperm epigenetics and influence of environmental factors. Mol Metab 2018;14:1-11. https://doi.org/10.1016/j.molmet.2018.02.006
  52. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner MK. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLoS One 2013;8:e55387. https://doi.org/10.1371/journal.pone.0055387
  53. Manikkam M, Guerrero-Bosagna C, Tracey R, Haque MM, Skinner MK. Transgenerational actions of environmental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures. PLoS One 2012;7:e31901. https://doi.org/10.1371/journal.pone.0031901
  54. Leung YK, Govindarajah V, Cheong A, Veevers J, Song D, Gear R, et al. Gestational high-fat diet and bisphenol A exposure heightens mammary cancer risk. Endocr Relat Cancer 2017;24:365-78. https://doi.org/10.1530/ERC-17-0006
  55. Palmer NO, Bakos HW, Fullston T, Lane M. Impact of obesity on male fertility, sperm function and molecular composition. Spermatogenesis 2012;2:253-63. https://doi.org/10.4161/spmg.21362

Cited by

  1. Bisphenols Threaten Male Reproductive Health via Testicular Cells vol.11, 2019, https://doi.org/10.3389/fendo.2020.00624
  2. The Importance of Oxidative Stress in Determining the Functionality of Mammalian Spermatozoa: A Two-Edged Sword vol.9, pp.2, 2019, https://doi.org/10.3390/antiox9020111
  3. Oxidative Stress and BPA Toxicity: An Antioxidant Approach for Male and Female Reproductive Dysfunction vol.9, pp.5, 2020, https://doi.org/10.3390/antiox9050405
  4. Multigenerational and transgenerational impact of paternal bisphenol A exposure on male fertility in a mouse model vol.35, pp.8, 2019, https://doi.org/10.1093/humrep/deaa139
  5. Mitochondrial Reactive Oxygen Species (ROS) Production Alters Sperm Quality vol.10, pp.1, 2019, https://doi.org/10.3390/antiox10010092
  6. Environmental Factors-Induced Oxidative Stress: Hormonal and Molecular Pathway Disruptions in Hypogonadism and Erectile Dysfunction vol.10, pp.6, 2019, https://doi.org/10.3390/antiox10060837
  7. Bisphenol A and Its Analogues Deteriorate the Hormones Physiological Function of the Male Reproductive System: A Mini-Review vol.9, pp.11, 2019, https://doi.org/10.3390/biomedicines9111744