Neonatal exposure of male rats to Bisphenol A impairs fertility and expression of sertoli cell junctional proteins in the testis

Toxicology

Volumn 265, Issue 1-2, 2009, Pages 56-67

  Salian, Smita ^a   Doshi, Tanvi ^a   Vanage, Geeta ^a  

^a NATIONAL INSTITUTE FOR RESEARCH IN REPRODUCTIVE HEALTH   (India)

Author keywords

Bisphenol A; Endocrine disrupters; Fertility; Neonatal exposure; Sertoli cell junctional proteins

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CELL PROTEIN; CONNEXIN 43; DIETHYLSTILBESTROL; NERVE CELL ADHESION MOLECULE; PROTEIN ZO1; SERTOLI CELL JUNCTIONAL PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL JUNCTION; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; LITTER SIZE; MALE; MALE INFERTILITY; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SERTOLI CELL; SPERMATOGENESIS; SPERMATOZOON COUNT; TESTIS; TESTIS DEVELOPMENT;

ANIMALS; ANIMALS, NEWBORN; CADHERINS; CONNEXIN 43; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCRINE DISRUPTORS; EPIDIDYMIS; FEMALE; FERTILITY; HORMONES; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; INTERCELLULAR JUNCTIONS; LITTER SIZE; MALE; MEMBRANE PROTEINS; PHENOLS; PHOSPHOPROTEINS; PREGNANCY; RATS; SEMINIFEROUS TUBULES; SERTOLI CELLS; SPERM COUNT; SPERM MOTILITY; TESTIS;

ANIMALIA; RATTUS;

EID: 70349984500     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2009.09.012     Document Type: Article

References (46)

1. Aikawa H., Koyama S., Matsuda M., Nakahashi K., Akazome Y., and Mori T. Relief effect of vitamin A on the decreased motility of sperm and the increased incidence of malformed sperm in mice exposed neonatally to Bisphenol A. Cell Tissue Res. 315 (2004) 119-124
2. Al-Hiyasat A., Darmani H., and Elbetieha A. Effects of Bisphenol A on adult male mouse fertility. Eur. J. Oral Sci. 110 (2002) 163-167. http://0-toxsci.oxfordjournals.org.library.uchsc.edu/cgi/external_ref http://0-toxsci.oxfordjournals.org.library.uchsc.edu/cgi/external_ref? access_num = 10.1034%2Fj.1600-0722.2002.11201.x&link_type = DOI
3. Anahara R., Yoshida M., Toyama Y., Maekawa M., Kai M., Ishino F., Toshimori K., and Mori C. Estrogen agonists, 17 beta-estradiol, Bisphenol A, and diethylstilbestrol decrease cortactin expression in the mouse testis. Arch. Histol. Cytol. 69 (2006) 101-107
4. Batias C., Defamie N., Lablack A., Thepot D., Fenichel P., Segretain D., and Pointis G. Modified expression of testicular gap-junction connexin 43 during normal spermatogenic cycle and in altered spermatogenesis. Cell Tissue Res. 298 (1999) 113-121
5. Batias C., Siffroi J., Fénichel P., Pointis G., and Segretain D. Connexin43 gene expression and regulation in the rodent seminiferous epithelium. J. Histochem. Cytochem. 48 (2000) 793-805
6. Bremner W., Millar M., Sharpe R., and Saunders P. Immunohistochemical localization of androgen receptors in the rat testes: evidence for stage-dependent expression and regulation by androgens. Endocrinology 135 (1994) 1227-1234
7. Brotons J., Olea-Serrano M., Villalobos M., Pedraza V., and Olea N. Xenoestrogens released from lacquer coatings in food cans. Environ. Health Perspect. 103 (1995) 608-612
8. Cheng C., and Mruk D. Cell junction dynamics in the testis: sertoli-germ cell interactions and male contraceptive development. Physiol. Rev. 82 (2002) 825-874
9. D'Souza R., Gill-Sharma M., Pathak S., Kedia N., Kumar R., and Balasinor N. Effect of high intratesticular estrogen on the seminiferous epithelium in adult male rats. Mol. Cell. Endocrinol. 241 (2005) 41-48
10. Ema M., Fujii S., Furukawa M., Kiguchi M., Ikka A., and Harazono A. Rat two-generation reproductive toxicity study of Bisphenol A. Reprod. Toxicol. 15 (2001) 505-523
11. European food safety authority (EFSA), 2008. Scientific opinion of the panel on food additives, flavourings, processing aids and materials in contact with food (AFC). EFSA J. 759, 1-10.
12. European union risk assessment report, 2003. 4,4′-isopropylidenediphenol (Bisphenol A) risk assessment (EINECS no. 201-245-8).
13. Fink C., Weigel R., Hembes T., Lauke-Wettwer H., Kliesch S., Bergmann M., and Brehm R. Altered expression of ZO-1 and ZO-2 in Sertoli cells and loss of blood-testis barrier integrity in testicular carcinoma in situ. Neoplasia 12 (2006) 1019-1027
14. Fiorini C., Tilloy-Ellul A., Chevalier S., Charuel C., and Pointis G. Sertoli cell junctional proteins as early targets for different classes of reproductive toxicants. Reprod. Toxicol. 18 (2004) 413-421
15. Goyal H., Robateau A., Braden T., Williams C., Srivastava K., and Ali K. Neonatal estrogen exposure of male rats alters reproductive functions at adulthood. Biol. Reprod. 68 (2003) 2081-2091
16. Gray T., and Beamand J. Effect of some phthalate esters and other testicular toxins on primary cultures of testicular cells. Food Chem. Toxicol. 22 (1984) 123-131
17. Hess R. Quantitative and qualitative characteristics of the stages and transitions in the cycle of the rat seminiferous epithelium: light microscopic observations of perfusion-fixed and plastic embedded testes. Biol. Reprod. 43 (1990) 525-542
18. Iida H., Môri T., Kaneko T., Urasoko A., Yamada F., and Shibata Y. Disturbed spermatogenesis in mice prenatally exposed to an endocrine disruptor Bisphenol A. Mammal Study 27 (2002) 73-82
19. Johnson K., Patel S., and Boekelheide K. Multiple cadherin superfamily members with unique expression profiles are produced in rat testis. Endocrinology 141 (2000) 675-683
20. Kato H., Furuhashi T., Tanaka M., Katsu Y., Watanabe H., Ohta Y., and Iguchi T. Effects of Bisphenol A given neonatally on reproductive functions of male rats. Reprod. Toxicol. 22 (2006) 20-29. http://0-toxsci.oxfordjournals.org.library.uchsc.edu/cgi/external_ref http://0-toxsci.oxfordjournals.org.library.uchsc.edu/cgi/external_ref? access_num=10.1016%2Fj.reprotox.2005.10.003&link_type=DOI
21. Kuiper G., Lemmen J., Carlsson B., Corton J., Safe S., van der Saag P., van der Burg B., and Gustafsson J. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139 (1998) 4252-4263
22. Lanning L., Creasy D., Chapin R., Mann P., Barlow N., Regan K., and Goodman D. Recommended approaches for the evaluation of testicular and epididymal toxicity. Toxicol. Pathol. 30 (2002) 507-520
23. NTP, 2001. National Toxicology Program's Report of the Endocrine Disruptors Low Dose Peer Review. National Toxicology Program, Research Triangle Park, NC.
24. NTP, 2008. NTP-CERHR Monograph on the Potential Human Reproductive and Developmental Effects of Bisphenol A. NTP-08-5994. Research Triangle Park, NC.
25. Olea N., Pulgar R., Pérez P., Olea-Serrano F., Rivas A., Novillo-Fertrell A., Pedraza V., Soto A., and Sonnenshein C. Estrogenicity of resin-based composites and sealants used in dentistry. Environ. Health Perspect. 104 (1996) 298-305
26. Plum A., Hallas G., Magin T., Dombrowski F., Hagendorff A., Schumacher B., Wolpert C., Kim J., Lamers W., Evert M., Meda P., Traub O., and Willecke K. Unique and shared functions of different connexins in mice. Curr. Biol. 10 (2000) 1083-1091
27. Ramos J., Varayoud J., Kass L., Rodriguez H., Costabel L., Munoz-de-Toro M., and Luque E. Bisphenol A induces both transient and permanent histofunctional alterations of the hypothalamic-pituitary-gonadal axis in prenatally exposed male rats. Endocrinology 144 (2003) 3206-3215
28. Richburg J., and Boekelheide K. Mono-(2-ethylhexyl) phthalate rapidly alters both Sertoli cell vimentin filaments and germ cell apoptosis in young rat testes. Toxicol. Appl. Pharmacol. 137 (1996) 42-50
29. Richter C., Birnbaum L., Farabollini F., Newbold R., Rubin B., Talsness C., Vandenbergh J., Walser-Kuntz D., and vom Saal F. In vivo effects of Bisphenol A in laboratory rodent studies. Reprod. Toxicol. 24 (2007) 199-224
30. Risley M., Tan I., Roy C., and Sáez J. Cell-, age- and stage-dependent distribution of connexin43 gap junctions in testes. J. Cell Sci. 103 (1992) 81-96
31. Sakaue M., Ohsako S., Ishimura R., Kurosawa S., Kurohmaru M., Hayashi Y., Aoki Y., Yonemoto J., and Tohyama C. Bisphenol-A affects spermatogenesis in the adult rat even at a low dose. J. Occup. Health 43 (2001) 185-190
32. Sharpe R., Atanassova N., McKinnell C., Parte P., Turner K., Fisher J., Kerr J., Groome N., Macpherson S., Millar M., and Saunders P. Abnormalities in functional development of the Sertoli cells in rats treated neonatally with diethylstilbestrol: a possible role for estrogens in Sertoli cell development. Biol. Reprod. 59 (1998) 1084-1094
33. Sinha N., Adhikari N., Narayan R., and Saxena D. Cytotoxic effect of endosulfan on rat Sertoli-germ coculture. Reprod. Toxicol. 13 (1999) 291-294
34. Sobarzo C., Lustig L., Ponzio R., and Denduchis B. Effect of di-(2-ethylhexyl) phthalate on N-cadherin and catenin protein expression in rat testis. Reprod. Toxicol. 22 (2006) 77-86
35. Sridharan S., Brehm R., Bergmann M., and Cooke P. Role of connexin 43 in Sertoli cells of testis. Ann. N. Y. Acad. Sci. 1120 (2007) 131-143
36. Takahashi O., and Oishi S. Testicular toxicity of dietary 2,2-Bis (4-hydroxyphenyl) propane (Bisphenol A) in F344 rats. Arch. Toxicol. 75 (2001) 42-51
37. Toyama Y., Suzuki-Toyota F., Maekawa M., Ito C., and Toshimori K. Adverse effect of Bisphenol A to spermiogenesis in mice and rats. Arch. Histol. Cytol. 67 (2004) 373-381
38. Toyama Y., and Yuasa S. Effects of neonatal administration of 17β-estradiol, β-estradiol 3-benzoate or Bisphenol A on mouse and rat spermatogenesis. Reprod. Toxicol. 19 (2004) 181-188
39. Tsutsumi O. Assesment of human contamination of estrogenic endocrine disrupting chemicals and their risk for human reproduction. J. Steroid Biochem. Mol. Biol. 93 (2005) 325-330
40. Tyl R., Myers C., Marr M., Thomas B., Keimowitz A., Brine D., Veselica M., Fail P., Chang T., Seely J., Joiner R., Butala J., Dimond S., Cagen Z., Shiotsuka R., Stropp G., and Waechter J. Three-generation reproductive toxicity study of dietary Bisphenol A in CD Sprague-Dawley rats. Toxicol. Sci. 681 (2002) 21-146
41. Vandenberg L., Hauser R., Marcus M., Olea N., and Welshons W. Human exposure to Bisphenol A (BPA). Reprod. Toxicol. 24 (2007) 139-177
42. vom Saal F., Cooke P., Buchanan D., Palanza P., Thayer K., Nagel S., Parmigiani S., and Welshons W. A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicol. Ind. Health. 14 (1998) 239-260
43. vom Saal F., and Hughes C. An extensive new literature concerning low-dose effects of Bisphenol A shows the need for a new risk assessment. Environ. Health Perspect. 113 (2005) 926-933
44. vom Saal F., Nagel S., Timms B., and Welshons W. Implications for human health of the extensive Bisphenol A literature showing adverse effects at low doses: a response to attempts to mislead the public. Toxicology 212 (2005) 244-245
45. vom Saal F., Akingbemi B., Belcher S., Birnbaum L., Crain D., Eriksen M., Farabollini F., Guillette L., Hauser R., Heindel J., Ho S., Hunt P., Iguchi T., Jobling S., Kanno J., Keri R., Knudsen K., Laufer H., LeBlanc G., Marcus M., McLachlan J., Myers J., Nadal A., Newbold R., Olea N., Prins G., Richter C., Rubin B., Sonnenschein C., Soto A., Talsness C., Vandenbergh J., Vandenberg L., Walser-Kuntz D., Watson C., Welshons W., Wetherill Y., and Zoeller R. Chapel Hill Bisphenol A expert panel consensus statement: integration of mechanisms, effects in animals and potential to impact human health at current levels of exposure. Reprod. Toxicol. 24 (2007) 131-180
46. Wong C., Mruk D., Lui W., and Cheng C. Regulation of blood-testis barrier dynamics: an in vivo study. J. Cell Sci. 117 (2004) 783-798