Neonatal exposure to 17α-ethynyl estradiol affects ovarian gene expression and disrupts reproductive cycles in female rats

Reproductive Toxicology

Volumn 46, Issue , 2014, Pages 77-84

  Nozawa, Kaori ^a   Nagaoka, Kentaro ^a   Zhang, Haolin ^a   Usuda, Kento ^a   Okazaki, Sachiko ^a   Taya, Kazuyoshi ^a   Yoshida, Midori ^b   Watanabe, Gen ^a  

^a TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^b NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

17 Ethynyl estradiol; Endocrine disruptor; Luteinizing hormone chorionic gonadotropin receptor; Ovary

Indexed keywords

CASPASE 3; CELL PROTEIN; ETHINYLESTRADIOL; LUTEINIZING HORMONE; LUTEINIZING HORMONE RECEPTOR; MESSENGER RNA; FOLLITROPIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENVIRONMENTAL EXPOSURE; ESTRUS CYCLE; FEMALE; GENE EXPRESSION; GENE EXPRESSION ASSAY; GENE EXPRESSION REGULATION; GENITAL SYSTEM DISEASE; HORMONAL REGULATION; HORMONE ACTION; HORMONE BLOOD LEVEL; IN VITRO STUDY; INTERSTITIUM; LHCGR GENE; LUTEINIZATION; NEWBORN; NONHUMAN; OVARY; PROESTRUS; PROTEIN LOCALIZATION; RAT; ANIMAL; BIOSYNTHESIS; BLOOD; BODY WEIGHT; DRUG EFFECTS; GENETICS; METABOLISM; ORGAN SIZE; TOXICITY; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; ESTROUS CYCLE; ETHINYL ESTRADIOL; FEMALE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION REGULATION; LUTEINIZING HORMONE; ORGAN SIZE; OVARY; RATS; RATS, WISTAR; RNA, MESSENGER;

EID: 84897094506     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2014.03.001     Document Type: Article

References (41)

1. Dickerson S.M., Gore A.C. Estrogenic environmental endocrine-disrupting chemical effects on reproductive neuroendocrine function and dysfunction across the life cycle. Rev Endocr Metab Disord 2007, 8:143-159.
2. Diamanti-Kandarakis E., Bourguignon J.P., Giudice L.C., Hauser R., Prins G.S., Soto A.M., et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 2009, 30:293-342.
3. Fowler P.A., Bellingham M., Sinclair K.D., Evans N.P., Pocar P., Fischer B., et al. Impact of endocrine-disrupting compounds (EDCs) on female reproductive health. Mol Cell Endocrinol 2012, 355:231-239.
4. Hotchkiss A.K., Rider C.V., Blystone C.R., Wilson V.S., Hartig P.C., Ankley G.T., et al. Fifteen years after "wingspread" - environmental endocrine disrupters and human and wildlife health: where we are today and where we need to go. Toxicol Sci 2008, 105:235-259.
5. Bakker J., Brock O. Early oestrogens in shaping reproductive networks: evidence for a potential organisational role of oestradiol in female brain development. J Neuroendocrinol 2010, 22:728-735.
6. McCarthy M.M. Estradiol and the developing brain. Physiol Rev 2008, 88:91-124.
7. Pepling M.E., Spradling A.C. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol 2001, 234:339-351.
8. Skinner M.K. Regulation of primordial follicle assembly and development. Hum Reprod Update 2005, 11:461-471.
9. Kezele P., Skinner M.K. Regulation of ovarian primordial follicle assembly and development by estrogen and progesterone: endocrine model of follicle assembly. Endocrinology 2003, 144:3329-3337.
10. Chen Y., Jefferson W.N., Newbold R.R., Padilla-Banks E., Pepling M.E. Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology 2007, 148:3580-3590.
11. Nash J.P., Kime D.E., Van der Ven L.T., Wester P.W., Brion F., Maack G, et al. Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ Health Perspect 2004, 112:1725-1733.
12. Söffker M., Tyler C.R. Endocrine disrupting chemicals and sexual behaviors in fish - a critical review on effects and possible consequences. Crit Rev Toxicol 2012, 42:653-668.
13. Pedersen J.A., Soliman M., Suffet I.H. Human pharmaceuticals, hormones, and personal care product ingredients in runoff from agricultural fields irrigated with treated wastewater. J Agric Food Chem 2005, 53:1625-1632.
14. Combalbert S., Hernandez-Raquet G. Occurrence, fate, and biodegradation of estrogens in sewage and manure. Appl Microbiol Biotechnol 2010, 86:1671-1692.
15. Lai K.M., Scrimshaw M.D., Lester J.N. Biotransformation and bioconcentration of steroid estrogens by Chlorella vulgaris. Appl Environ Microbiol 2002, 68:859-864.
16. Karnjanapiboonwong A., Chase D.A., Cañas J.E., Jackson W.A., Maul J.D., Morse A.N., et al. Uptake of 17α-ethynylestradiol and triclosan in pinto bean, Phaseolus vulgaris. Ecotoxicol Environ Saf 2011, 74:1336-1342.
17. de Assis S., Warri A., Cruz M.I., Laja O., Tian Y., Zhang B., et al. High-fat or ethinyl-oestradiol intake during pregnancy increases mammary cancer risk in several generations of offspring. Nat Commun 2012, 3:1053.
18. Sawaki M., Noda S., Muroi T., Mitoma H., Takakura S., Sakamoto S., et al. In utero through lactational exposure to ethinyl estradiol induces cleft phallus and delayed ovarian dysfunction in the offspring. Toxicol Sci 2003, 75:402-411.
19. Mathews E., Braden T.D., Williams C.S., Williams J.W., Bolden-Tiller O., Goyal H.O. Mal-development of the penis and loss of fertility in male rats treated neonatally with female contraceptive 17alpha-ethinyl estradiol: a dose-response study and a comparative study with a known estrogenic teratogen diethylstilbestrol. Toxicol Sci 2009, 112:331-343.
20. Mandrup K.R., Jacobsen P.R., Isling L.K., Axelstad M., Dreisig K., Hadrup N., et al. Effects of perinatal ethinyl estradiol exposure in male and female Wistar rats. Reprod Toxicol 2013, 42:180-191.
21. Shiorta M., Kawashima J., Nakamura T., Ogawa Y., Kamiie J., Yasuno K., et al. Delayed effects of single neonatal subcutaneous exposure of low-dose 17α-ethynylestradiol on reproductive function in female rats. J Toxicol Sci 2012, 37:681-690.
22. Takahashi M., Inoue K., Morikawa T., Matsuo S., Hayashi S., Tamura K., et al. Delayed effects of neonatal exposure to 17alpha-ethynylestradiol on the estrous cycle and uterine carcinogenesis in Wistar Hannover GALAS rats. Reprod Toxicol 2013, 40:16-23.
23. Dören M., Nilsson J.A., Johnell O. Effects of specific post-menopausal hormone therapies on bone mineral density in post-menopausal women: a meta-analysis. Hum Reprod 2003, 18:1737-1746.
24. Merz C.N., Olson M.B., McClure C., Yang Y.C., Symons J., Sopko G., et al. A randomized controlled trial of low-dose hormone therapy on myocardial ischemia in postmenopausal women with no obstructive coronary artery disease: results from the National Institutes of Health/National Heart, Lung, and Blood Institute-sponsored Women's Ischemia Syndrome Evaluation (WISE). Am Heart J 2010, 159:987.e1-987.e7.
25. Mills L.J., Chichester C. Review of evidence: are endocrine-disrupting chemicals in the aquatic environment impacting fish populations?. Sci Total Environ 2005, 343:1-34.
26. Tilton S.C., Foran C.M., Benson W.H. Relationship between ethinylestradiol-mediated changes in endocrine function and reproductive impairment in Japanese medaka (Oryzias latipes). Environ Toxicol Chem 2005, 24:352-359.
27. Liu K.C., Wu R.S., Ge W. Luteinizing hormone receptor (lhcgr) as a marker gene for characterizing estrogenic endocrine-disrupting chemicals in zebrafish ovarian follicle cells. Gen Comp Endocrinol 2013, 192:89-94.
28. Ascoli M., Fanelli F., Segaloff D.L. The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr Rev 2002, 23:141-174.
29. Lei Z.M., Mishra S., Zou W., Xu B., Foltz M., Li X., et al. Targeted disruption of luteinizing hormone/human chorionic gonadotropin receptor gene. Mol Endocrinol 2001, 15:184-200.
30. Yacobi K., Wojtowicz A., Tsafriri A., Gross A. Gonadotropins enhance caspase-3 and -7 activity and apoptosis in the theca-interstitial cells of rat preovulatory follicles in culture. Endocrinology 2004, 145:1943-1951.
31. Yacobi K., Tsafriri A., Gross A. Luteinizing hormone-induced caspase activation in rat preovulatory follicles is coupled to mitochondrial steroidogenesis. Endocrinology 2007, 148:1717-1726.
32. Couse J.F., Yates M.M., Sanford R., Nyska A., Nilson J.H., Korach K.S. Formation of cystic ovarian follicles associated with elevated luteinizing hormone requires estrogen receptor-beta. Endocrinology 2004, 145:4693-4702.
33. Mandai M., Konishi I., Kuroda H., Fujii S. LH/hCG action and development of ovarian cancer - a short review on biological and clinical/epidemiological aspects. Mol Cell Endocrinol 2007, 269:61-64.
34. Cui J., Miner B.M., Eldredge J.B., Warrenfeltz S.W., Dam P., Xu Y., et al. Regulation of gene expression in ovarian cancer cells by luteinizing hormone receptor expression and activation. BMC Cancer 2011, 11:280.
35. Sen A., Hammes S.R. Granulosa cell-specific androgen receptors are critical regulators of ovarian development and function. Mol Endocrinol 2010, 24:1393-1403.
36. Gleicher N., Barad D.H. Dehydroepiandrosterone (DHEA) supplementation in diminished ovarian reserve (DOR). Reprod Biol Endocrinol 2011, 9:67.
37. Gleicher N., Kim A., Weghofer A., Shohat-Tal A., Lazzaroni E., Lee H.J., et al. Starting and resulting testosterone levels after androgen supplementation determine at all ages in vitro fertilization (IVF) pregnancy rates in women with diminished ovarian reserve (DOR). J Assist Reprod Genet 2013, 30:49-62.
38. Gleicher N., Kim A., Weghofer A., Kushnir V.A., Shohat-Tal A., Lazzaroni E., et al. Hypoandrogenism in association with diminished functional ovarian reserve. Hum Reprod 2013, 28:1084-1091.
39. Gore A.C. Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems. Front Neuroendocrinol 2008, 29:358-374.
40. Navarro V.M., Sánchez-Garrido M.A., Castellano J.M., Roa J., García-Galiano D., Pineda R., et al. Persistent impairment of hypothalamic KiSS-1 system after exposures to estrogenic compounds at critical periods of brain sex differentiation. Endocrinology 2009, 150:2359-2367.
41. Losa S.M., Todd K.L., Sullivan A.W., Cao J., Mickens J.A., Patisaul H.B. Neonatal exposure to genistein adversely impacts the ontogeny of hypothalamic kisspeptin signaling pathways and ovarian development in the peripubertal female rat. Reprod Toxicol 2011, 31:280-289.