Prenatal Exposure to the Phytoestrogen Daidzein Resulted in Persistent Changes in Ovarian Surface Epithelial Cell Height, Folliculogenesis, and Estrus Phase Length in Adult Sprague-Dawley Rat Offspring

REFERENCES

• Adlercreutz, H., Hockerstedt, K., Bannwart, C., Bloigu, S., Hamalainen, E., Fotsis, T., and Ollus, A. 1987. Effect of dietary components, including lignans and phytoestrogens, on enterohepatic circulation and liver metabolism of estrogens and on sex hormone binding globulin (SHBG). J. Steroid. Biochem. 27: 1135–1144.
   PubMedGoogle Scholar
• An, J., Tzagarakis-Foster, C., Scharschmidt, T.C., Lomri, N., and Leitman, D. C. 2001. Estrogen receptor beta-selective transcriptional activity and recruitment of coregulators by phytoestrogens. J. Biol. Chem. 276: 17808–17814.
   PubMed Web of Science ®Google Scholar
• Andres, S., Abraham, K., Appel, K. E., and Lampen, A. 2011. Risks and benefits of dietary isoflavones for cancer. Crit. Rev. Toxicol. 41: 463–506.
   PubMed Web of Science ®Google Scholar
• Auersperg, N., Wong, A. S., Choi, K. C., Kang, S. K., and Leung, P. C. 2001. Ovarian surface epithelium: Biology, endocrinology, and pathology. Endocr. Rev. 22: 255–288.
   PubMed Web of Science ®Google Scholar
• Bai, W., Oliveros-Saunders, B., Wang, Q., Acevedo-Duncan, M. E., and Nicosia, S. V. 2000. Estrogen stimulation of ovarian surface epithelial cell proliferation. In Vitro Cell Dev. Biol. Anim. 36: 657–666.
   PubMed Web of Science ®Google Scholar
• Barkhem, T., Carlsson, B., Nilsson, Y., Enmark, E., Gustafsson, J., and Nilsson, S. 1998. Differential response of estrogen receptor alpha and estrogen receptor beta to partial estrogen agonists/antagonists. Mol. Pharmacol. 54: 105–112.
   PubMed Web of Science ®Google Scholar
• Bolt, H. M., Janning, P., Michna, H., and Degen, G. H. 2001. Comparative assessment of endocrine modulators with oestrogenic activity: I. Definition of a hygiene-based margin of safety (HBMOS) for xeno-oestrogens against the background of European developments. Arch. Toxicol. 74: 649–662.
   PubMed Web of Science ®Google Scholar
• Borgeest, C., Symonds, D., Mayer, L. P., Hoyer, P. B., and Flaws, J. A. 2002. Methoxychlor may cause ovarian follicular atresia and proliferation of the ovarian epithelium in the mouse. Toxicol. Sci. 68: 473–478.
   PubMed Web of Science ®Google Scholar
• Casanova, M., You, L., Gaido, K. W., Archibeque-Engle, S., Janszen, D. B., and Heck, H. A. 1999. Developmental effects of dietary phytoestrogens in Sprague-Dawley rats and interactions of genistein and daidzein with rat estrogen receptors alpha and beta in vitro. Toxicol. Sci. 51: 236–244.
   PubMed Web of Science ®Google Scholar
• Chandrareddy, A., Muneyyirci-Delale, O., McFarlane, S. I., and Murad, O. M. 2008. Adverse effects of phytoestrogens on reproductive health: a report of three cases. Complement Ther. Clin. Pract. 14: 132–135.
   PubMedGoogle Scholar
• Ch’Ang, T. S. 1958. Reproductive disturbances of Romney ewe lambs grazed on red clover (Trifolium pratense) pastures. Nature 182: 1175.
   PubMed Web of Science ®Google Scholar
• Choi, K. C., Kang, S. K., Tai, C. J., Auersperg, N., and Leung, P. C. 2001. Estradiol up-regulates antiapoptotic Bcl-2 messenger ribonucleic acid and protein in tumorigenic ovarian surface epithelium cells. Endocrinology 142: 2351–2360.
   PubMed Web of Science ®Google Scholar
• Degen, G. H., Janning, P., Diel, P., Michna H., and Bolt, H. M. 2002. Transplacental transfer of the phytoestrogen daidzein in DA/Han rats. Arch. Toxicol. 76, 23–29.
   PubMed Web of Science ®Google Scholar
• Delclos, K. B., Constance C. Weis, C. C., Bucci, T. J., Olson, G., Mellick, P., Natalya Sadovova, N., Latendresse, J. R., Brett Thorn, B., and Newbold, R. R. 2009. Overlapping but distinct effects of genistein and ethinyl estradiol (EE2) in female Sprague-Dawley rats in multigenerational reproductive and chronic toxicity studies. Reprod. Toxicol. 27: 117–132.
   PubMed Web of Science ®Google Scholar
• Devine, P. J., Payne, C. M., McCuskey, M. K., and Hoyer, P. B. 2000. Ultrastructural evaluation of oocytes during atresia in rat ovarian follicles. Biol. Reprod. 63: 1245–1252.
   PubMed Web of Science ®Google Scholar
• Foster, W. G., Chan, S., Platt, L., and Hughes, C. L., Jr., 2002. Detection of phytoestrogens in samples of second trimester human amniotic fluid. Toxicol. Lett. 129: 199–205.
   PubMed Web of Science ®Google Scholar
• Fowler, P. A., Anderson, R. A., Saunders, P.T., Kinnell, H., Mason, J. I., Evans, D. B., Bhattacharya, S., Flannigan, S., Franks, S., Monteiro, A., and O’Shaughnessy, P. J., 2011. Development of steroid signaling pathways during primordial follicle formation in the human fetal ovary. J. Clin. Endocrinol. Metab. 96: 1754–1762.
   PubMed Web of Science ®Google Scholar
• Gaido, K. W., Leonard, L. S., Maness, S. C., Hall, J. M., McDonnell, D. P., Saville, B., and Safe, S. 1999. Differential interaction of the methoxychlor metabolite 2,2-bis-(p-hydroxyphenyl)-1,1,1-trichloroethane with estrogen receptors alpha and beta. Endocrinology 140: 5746–5753.
   PubMed Web of Science ®Google Scholar
• Greco, T. L., and Payne, A. H. 1994. Ontogeny of expression of the genes for steroidogenic enzymes P450 side-chain cleavage, 3 beta-hydroxysteroid dehydrogenase, P450 17 alpha-hydroxylase/C17-20 lyase, and P450 aromatase in fetal mouse gonads. Endocrinology 135: 262–268.
   PubMed Web of Science ®Google Scholar
• Gulliver, L. S., and Hurst, P. R. 2011. Novel approaches to quantify estradiol-induced loss of ERbeta1 protein in older mouse ovarian surface epithelium: New tools to assess the role of ER protein subtypes in predisposing to ovarian epithelial cancer? Horm. Cancer 2: 204–13.
   PubMedGoogle Scholar
• Hedelin, M., Löf, M., Andersson, T. M., Adlercreutz, H., and Weiderpass, E. 2011. Dietary phytoestrogens and the risk of ovarian cancer in the women’s lifestyle and health cohort study. Cancer Epidemiol. Biomarkers Prev. 20: 308–317.
   PubMed Web of Science ®Google Scholar
• Hirshfield, A. N, and DeSanti, A. M. 1995. Patterns of ovarian cell proliferation in rats during the embryonic period and the first three weeks postpartum. Biol. Reprod. 53: 1208–1221.
   PubMed Web of Science ®Google Scholar
• Hunn, J., and Rodriguez, G. C. 2012. Ovarian cancer: Etiology, risk factors, and epidemiology. Clin. Obstet. Gynecol. 55: 3–23.
   PubMed Web of Science ®Google Scholar
• Kaludjerovic J., Chen J., and Ward W. E. 2012. Early life exposure to genistein and daidzein disrupts structural development of reproductive organs in female mice. J. Toxicol. Environ. Health A 75: 649–660.
   PubMed Web of Science ®Google Scholar
• King, S. M., and Burdette, J. E. 2011. Evaluating the progenitor cells of ovarian cancer: Analysis of current animal models. BMB Rep. 44: 435–445.
   PubMed Web of Science ®Google Scholar
• Kostelac, D., Rechkemmer, G., and Briviba, K. 2003. Phytoestrogens modulate binding response of estrogen receptors alpha and beta to the estrogen response element. J. Agric. Food Chem. 51: 7632–7635.
   PubMed Web of Science ®Google Scholar
• Kwack, S. J., Kim, K. B., Kim, H. S., Yoon, K. S., and Lee, B. M. 2009. Risk assessment of soybean-based phytoestrogens. J. Toxicol. Environ. Health A 72: 1254–1261.
   PubMed Web of Science ®Google Scholar
• Lacey, M., Bohday, J., Fonseka, S. M., Ullah, A. I., and Whitehead, S. A. 2005. Dose-response effects of phytoestrogens on the activity and expression of 3beta-hydroxysteroid dehydrogenase and aromatase in human granulosa-luteal cells. J. Steroid Biochem. Mol. Biol. 96: 279–286.
   PubMed Web of Science ®Google Scholar
• Lamartiniere, C. A., Wang, J., Smith-Johnson, M., and Eltoum, I. E. 2002. Daidzein: Bioavailability, potential for reproductive toxicity, and breast cancer chemoprevention in female rats. Toxicol. Sci. 65: 228–238.
   PubMed Web of Science ®Google Scholar
• Makri, A., Goveia, M., Balbus, J., and Parkin, R. 2004. Children’s susceptibility to chemicals: A review by developmental stage. J. Toxicol. Environ. Health B 7: 417–435.
   PubMed Web of Science ®Google Scholar
• Margeat, E., Bourdoncle, A., Margueron, R., Poujol, N., Cavailles, V., and Royer, C. 2003. Ligands differentially modulate the protein interactions of the human estrogen receptors alpha and beta. J. Mol. Biol. 326: 77–92.
   PubMed Web of Science ®Google Scholar
• Matsuda, F., Inoue, N., Manabe, N., and Ohkura, S. 2012. Follicular growth and atresia in Mammalian ovaries: Regulation by survival and death of granulosa cells. J. Reprod. Dev. 58: 44–50.
   PubMed Web of Science ®Google Scholar
• McCarver, G., Bhatia, J., Chambers, C., Clarke, R., Etzel, R., Foster, W., Hoyer, P., Leeder, J. S., Peters, J. M., Rissman, E., Rybak, M., Sherman, C., Toppari, J., and Turner, K. 2011. NTP-CERHR expert panel report on the developmental toxicity of soy infant formula. Birth Defects Res. B Dev. Reprod. Toxicol. 92: 421–468.
   PubMed Web of Science ®Google Scholar
• McLemore, M. R., Miaskowski, C., Aouizerat, B. E., Chen, L., and Dodd, M. J. 2009. Epidemiologic and genetic factors associated with ovarian cancer. Cancer Nurs. 32: 281–290.
   PubMed Web of Science ®Google Scholar
• Pedersen, T., and Peters, H. 1968. Proposal for a classification of oocytes and follicles in the mouse ovary. J. Reprod. Fertil. 17: 555–557.
   PubMedGoogle Scholar
• Plowchalk, D. R, Smith, B. J., and Mattison, D. R. 1993. Assessment of toxicity to the ovary using follicle quantitation and morphometrics. In Methods in toxicology, vol. 3, ed. J. J. Heindel and R. E. Chapin, 57–68. San Diego, CA: Academic Press.
   Google Scholar
• Rice, S., Mason, H. D., and Whitehead, S. A. 2006. Phytoestrogens and their low dose combinations inhibit mRNA expression and activity of aromatase in human granulosa-luteal cells. J. Steroid Biochem. Mol. Biol. 101: 216–225.
   PubMed Web of Science ®Google Scholar
• Sacks, F. M. 2005. Dietary phytoestrogens to prevent cardiovascular disease: Early promise unfulfilled. Circulation 111: 385–387.
   PubMed Web of Science ®Google Scholar
• Schnaper, H. W., McGowan, K. A., Kim-Schulze, S., and Cid, M. C. 1996. Oestrogen and endothelial cell angiogenic activity. Clin. Exp. Pharmacol. Physiol. 23: 247–250.
   PubMed Web of Science ®Google Scholar
• Setchell, K. D., Gosselin, S. J., Welsh, M. B., Johnston, J. O., Balistreri, W. F., Kramer, L. W., Dresser, B. L., and Tarr, M. J. 1987. Dietary estrogens—A probable cause of infertility and liver disease in captive cheetahs. Gastroenterology 93: 225–233.
   PubMed Web of Science ®Google Scholar
• Shor D., Sathyapalan T., Atkin S. L., and Thatcher N. J. 2012. Does equol production determine soy endocrine effects? Eur. J. Nutr. 51: 389–398.
   PubMed Web of Science ®Google Scholar
• Symonds, D., Tomic, D., Borgeest, C., McGee, E., and Flaws, J. A. 2003. Smad 3 regulates proliferation of the mouse ovarian surface epithelium. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 273: 681–686.
   PubMedGoogle Scholar
• Talsness, C. E., Kuriyama, S. N., Sterner-Kock, A., Schnitker, P., Grande, S. W., Shakibaei, M., Andrade, A., Grote, K., and Chahoud, I. 2008. In utero and lactational exposures to low doses of polybrominated diphenyl ether-47 alter the reproductive system and thyroid gland of female rat offspring. Environ. Health Perspect. 116: 308–314.
   PubMed Web of Science ®Google Scholar
• Tierschutzgesetz 25 May. 1998. BGBl. I S. 1105, 1818 [The German Animal Protection Act].
   Google Scholar
• Todaka, E., Sakurai, K., Fukata, H., Miyagawa, H., Uzuki, M., Omori, M., Osada, H., Ikezuki, Y., Tsutsumi, O., Iguchi, T., and Mori, C. 2005. Fetal exposure to phytoestrogens—The difference in phytoestrogen status between mother and fetus. Environ. Res. 99: 195–203.
   PubMed Web of Science ®Google Scholar
• Totta, P., Acconcia, F., Virgili, F., Cassidy, A., Weinberg, P.D., Rimbach, G., and Marino, M. 2005. Daidzein-sulfate metabolites affect transcriptional and antiproliferative activities of estrogen receptor-beta in cultured human cancer cells. J. Nutr. 135: 2687–2693.
   PubMed Web of Science ®Google Scholar
• Vanholder, T., Opsomer, G., and de Kruif, A. 2006. Aetiology and pathogenesis of cystic ovarian follicles in dairy cattle: A review. Reprod. Nutr. Dev. 46: 105–119.
   PubMedGoogle Scholar
• Yasuda, Y., Kihara, T., and Nishimura, H. 1977. Effect of prenatal treatment with ethinyl estradiol on the mouse uterus and ovary. Am. J. Obstet. Gynecol. 127: 832–836.
   PubMed Web of Science ®Google Scholar
• Yoon, K., Kwack, S. J., Kim, H. S., and Lee, B. M. 2014. Estrogenic endocrine-disrupting chemicals: Molecular mechanisms of actions on putative human diseases. J. Toxicol. Environ. Health B 17: 127–174.
   PubMed Web of Science ®Google Scholar
• Zimmermann, R. C., Hartman, T., Kavic, S., Pauli, S. A., Bohlen, P., Sauer, M. V., and Kitajewski, J. 2003. Vascular endothelial growth factor receptor 2-mediated angiogenesis is essential for gonadotropin-dependent follicle development. J. Clin. Invest. 112: 659–669.
   PubMed Web of Science ®Google Scholar