Developmental programming: Prenatal BPA treatment disrupts timing of LH surge and ovarian follicular wave dynamics in adult sheep

Toxicology and Applied Pharmacology

Volumn 279, Issue 2, 2014, Pages 119-128

  Veiga Lopez, A ^a   Beckett, E M ^a   Abi Salloum, B ^a   Ye, W ^b   Padmanabhan, V ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Bisphenol A; Follicular dynamics; Infertility

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ESTRADIOL; PROGESTERONE;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; CORPUS LUTEUM; DYNAMICS; ESTRUS; FEMALE; GESTATIONAL AGE; LUTEAL PHASE; LUTEINIZING HORMONE RELEASE; NONHUMAN; OVARY FOLLICLE; OVULATION; PREGNANCY; PRENATAL EXPOSURE; PROGENY; SHEEP; TRANSRECTAL ULTRASONOGRAPHY;

BISPHENOL A; FOLLICULAR DYNAMICS; INFERTILITY;

ANIMALS; BENZHYDRYL COMPOUNDS; BIOLOGICAL MARKERS; ENDOCRINE DISRUPTORS; ESTROUS CYCLE; FEMALE; FERTILITY; GESTATIONAL AGE; INFERTILITY, FEMALE; LUTEINIZING HORMONE; MATERNAL EXPOSURE; OVARIAN FOLLICLE; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROGESTERONE; RISK ASSESSMENT; RISK FACTORS; SHEEP; TIME FACTORS; UP-REGULATION;

EID: 84903553943     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.05.016     Document Type: Article

References (69)

1. Abi Salloum B., Steckler T.L., Herkimer C., Lee J.S., Padmanabhan V. Developmental programming: impact of prenatal exposure to bisphenol-A and methoxychlor on steroid feedbacks in sheep. Toxicol. Appl. Pharmacol. 2013, 268:300-308.
2. Aluru N., Leatherland J.F., Vijayan M.M. Bisphenol A in oocytes leads to growth suppression and altered stress performance in juvenile rainbow trout. PLoS ONE 2010, 5:e10741.
3. Baird D.T., Campbell B.K., Mann G.E., McNeilly A.S. Inhibin and oestradiol in the control of FSH secretion in the sheep. J. Reprod. Fertil. Suppl. 1991, 43:125-138.
4. Bao B., Garverick H.A., Smith G.W., Smith M.F., Salfen B.E., Youngquist R.S. Changes in messenger ribonucleic acid encoding luteinizing hormone receptor, cytochrome P450-side chain cleavage, and aromatase are associated with recruitment and selection of bovine ovarian follicles. Biol. Reprod. 1997, 56:1158-1168.
5. Barrett D.M., Bartlewski P.M., Duggavathi R., Davies K.L., Rawlings N.C. Suppression of follicle wave emergence in cyclic ewes by supraphysiologic concentrations of estradiol-17beta and induction with a physiologic dose of exogenous ovine follicle-stimulating hormone. Biol. Reprod. 2006, 75:633-641.
6. Bartlewski P.M., Baby T.E., Giffin J.L. Reproductive cycles in sheep. Anim. Reprod. Sci. 2011, 124:259-268.
7. Battaglia D.E., Goodwin P., Klein N.A., Soules M.R. Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. Hum. Reprod. 1996, 11:2217-2222.
8. Berger R.G., Shaw J., deCatanzaro D. Impact of acute bisphenol-A exposure upon intrauterine implantation of fertilized ova and urinary levels of progesterone and 17beta-estradiol. Reprod. Toxicol. 2008, 26:94-99.
9. Brannick K.E., Craig Z.R., Himes A.D., Peretz J.R., Wang W., Flaws J.A., Raetzman L.T. Prenatal exposure to low doses of bisphenol A increases pituitary proliferation and gonadotroph number in female mice offspring at birth. Biol. Reprod. 2012, 87:82.
10. Burger H.G., Robertson D.M., Baksheev L., Collins A., Csemiczky G., Landgren B.M. The relationship between the endocrine characteristics and the regularity of menstrual cycles in the approach to menopause. Menopause 2005, 12:267-274.
11. Calafat A.M., Weuve J., Ye X., Jia L.T., Hu H., Ringer S., Huttner K., Hauser R. Exposure to bisphenol A and other phenols in neonatal intensive care unit premature infants. Environ. Health Perspect. 2009, 117:639-644.
12. Cao J., Joyner L., Mickens J.A., Leyrer S.M., Patisaul H.B. Sex-specific Esr2 mRNA expression in the rat hypothalamus and amygdala is altered by neonatal bisphenol A exposure. Reproduction 2014, 147:537-554.
13. Craig Z.R., Wang W., Flaws J.A. Endocrine-disrupting chemicals in ovarian function: effects on steroidogenesis, metabolism and nuclear receptor signaling. Reproduction 2011, 142:633-646.
14. Delclos K.B., Camacho L., Lewis S.M., Vanlandingham M.M., Latendresse J.R., Olson G.R., Davis K.J., Patton R.E., da Costa G.G., Woodling K.A., Bryant M.S., Chidambaram M., et al. Toxicity evaluation of bisphenol a administered by gavage to Sprague Dawley rats from gestation day 6 through postnatal day 90. Toxicol. Sci. 2014, 139:174-197.
15. Durando M., Kass L., Piva J., Sonnenschein C., Soto A.M., Luque E.H., Munoz-de-Toro M. Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ. Health Perspect. 2007, 115:80-86.
16. Evans N.P., Dahl G.E., Glover B.H., Karsch F.J. Central regulation of pulsatile gonadotropin-releasing hormone (GnRH) secretion by estradiol during the period leading up to the preovulatory GnRH surge in the ewe. Endocrinology 1994, 134:1806-1811.
17. Findlay J.K., Drummond A.E., Dyson M.L., Baillie A.J., Robertson D.M., Ethier J.F. Recruitment and development of the follicle; the roles of the transforming growth factor-beta superfamily. Mol. Cell. Endocrinol. 2002, 191:35-43.
18. European Food Safety Authority Opinion on Bisphenol A (BPA) - Assessment of Human Health Risks 2014, (Last accessed: 04/16/2014).
19. Ginther O.J., Kot K., Wiltbank M.C. Associations between emergence of follicular waves and fluctuations in FSH concentrations during the estrous cycle in ewes. Theriogenology 1995, 43:689-703.
20. Gong J.G., Bramley T., Webb R. The effect of recombinant bovine somatotropin on ovarian function in heifers: follicular populations and peripheral hormones. Biol. Reprod. 1991, 45:941-949.
21. Harlow C.R., Hillier S.G., Hodges J.K. Androgen modulation of follicle-stimulating hormone-induced granulosa cell steroidogenesis in the primate ovary. Endocrinology 1986, 119:1403-1405.
22. Hartgens F., Kuipers H. Effects of androgenic-anabolic steroids in athletes. Sports Med. 2004, 34:513-554.
23. Hotchkiss A.K., Rider C.V., Blystone C.R., Wilson V.S., Hartig P.C., Ankley G.T., Foster P.M., Gray C.L., Gray L.E. 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.
24. Howdeshell K.L., Hotchkiss A.K., Thayer K.A., Vandenbergh J.G., vom Saal F.S. Exposure to bisphenol A advances puberty. Nature 1999, 401:763-764.
25. Hunt P.A., Lawson C., Gieske M., Murdoch B., Smith H., Marre A., Hassold T., VandeVoort C.A. Bisphenol A alters early oogenesis and follicle formation in the fetal ovary of the rhesus monkey. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:17525-17530.
26. I'Anson H., Manning J.M., Herbosa C.G., Pelt J., Friedman C.R., Wood R.I., Bucholtz D.C., Foster D.L. Central inhibition of gonadotropin-releasing hormone secretion in the growth-restricted hypogonadotropic female sheep. Endocrinology 2000, 141:520-527.
27. Ikezuki Y., Tsutsumi O., Takai Y., Kamei Y., Taketani Y. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum. Reprod. 2002, 17:2839-2841.
28. Kiyma Z., Alexander B.M., Van Kirk E.A., Murdoch W.J., Hallford D.M., Moss G.E. Effects of feed restriction on reproductive and metabolic hormones in ewes. J. Anim. Sci. 2004, 82:2548-2557.
29. Knight B.S., Pennell C.E., Adamson S.L., Lye S.J. The impact of murine strain and sex on postnatal development after maternal dietary restriction during pregnancy. J. Physiol. 2007, 581:873-881.
30. Kwintkiewicz J., Nishi Y., Yanase T., Giudice L.C. Peroxisome proliferator-activated receptor-gamma mediates bisphenol A inhibition of FSH-stimulated IGF-1, aromatase, and estradiol in human granulosa cells. Environ. Health Perspect. 2010, 118:400-406.
31. Lawson C., Gieske M., Murdoch B., Ye P., Li Y., Hassold T., Hunt P.A. Gene expression in the fetal mouse ovary is altered by exposure to low doses of bisphenol A. Biol. Reprod. 2011, 84:79-86.
32. Lee S.G., Kim J.Y., Chung J.Y., Kim Y.J., Park J.E., Oh S., Yoon Y.D., Yoo K.S., Yoo Y.H., Kim J.M. Bisphenol A exposure during adulthood causes augmentation of follicular atresia and luteal regression by decreasing 17beta-estradiol synthesis via downregulation of aromatase in rat ovary. Environ. Health Perspect. 2013, 121:663-669.
33. Luense L.J., Veiga-Lopez A., Padmanabhan V., Christenson L.K. Developmental programming: gestational testosterone treatment alters fetal ovarian gene expression. Endocrinology 2011, 152:4974-4983.
34. Mahoney M.M., Padmanabhan V. Developmental programming: impact of fetal exposure to endocrine-disrupting chemicals on gonadotropin-releasing hormone and estrogen receptor mRNA in sheep hypothalamus. Toxicol. Appl. Pharmacol. 2010, 247:98-104.
35. Malcolm K.D., Jackson L.M., Bergeon C., Lee T.M., Padmanabhan V., Foster D.L. Long-term exposure of female sheep to physiologic concentrations of estradiol: effects on the onset and maintenance of reproductive function, pregnancy, and social development in female offspring. Biol. Reprod. 2006, 75:844-852.
36. Manikkam M., Crespi E.J., Doop D.D., Herkimer C., Lee J.S., Yu S., Brown M.B., Foster D.L., Padmanabhan V. Fetal programming: prenatal testosterone excess leads to fetal growth retardation and postnatal catch-up growth in sheep. Endocrinology 2004, 145:790-798.
37. Markey C.M., Coombs M.A., Sonnenschein C., Soto A.M. Mammalian development in a changing environment: exposure to endocrine disruptors reveals the developmental plasticity of steroid-hormone target organs. Evol. Dev. 2003, 5:67-75.
38. Matthews J., Gustafsson J.A. Estrogen signaling: a subtle balance between ER alpha and ER beta. Mol. Interv. 2003, 3:281-292.
39. Molina A.M., Lora A.J., Blanco A., Monterde J.G., Ayala N., Moyano R. Endocrine-active compound evaluation: qualitative and quantitative histomorphological assessment of zebrafish gonads after bisphenol-A exposure. Ecotoxicol. Environ. Saf. 2013, 88:155-162.
40. Nagel S.C., vom Saal F.S., Welshons W.V. Developmental effects of estrogenic chemicals are predicted by an in vitro assay incorporating modification of cell uptake by serum. J. Steroid Biochem. Mol. Biol. 1999, 69:343-357.
41. Nakagawa S., Cuthill I.C. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol. Rev. Camb. Philos. Soc. 2007, 82:591-605.
42. Newbold R.R., Jefferson W.N., Padilla-Banks E. Long-term adverse effects of neonatal exposure to bisphenol A on the murine female reproductive tract. Reprod. Toxicol. 2007, 24:253-258.
43. Niswender G.D., Reichert L.E., Midgley A.R., Nalbandov A.V. Radioimmunoassay for bovine and ovine luteinizing hormone. Endocrinology 1969, 84:1166-1173.
44. Padmanabhan V., Veiga-Lopez A. Developmental origin of reproductive and metabolic dysfunctions: androgenic versus estrogenic reprogramming. Semin. Reprod. Med. 2011, 29:173-186.
45. Padmanabhan V., Veiga-Lopez A. Sheep models of polycystic ovary syndrome phenotype. Mol. Cell. Endocrinol. 2013, 373:8-20.
46. Padmanabhan V., Evans N.P., Dahl G.E., McFadden K.L., Mauger D.T., Karsch F.J. Evidence for short or ultrashort loop negative feedback of gonadotropin-releasing hormone secretion. Neuroendocrinology 1995, 62:248-258.
47. Padmanabhan V., Siefert K., Ransom S., Johnson T., Pinkerton J., Anderson L., Tao L., Kannan K. Maternal bisphenol-A levels at delivery: a looming problem?. J. Perinatol. 2008, 28:258-263.
48. Peretz J., Gupta R.K., Singh J., Hernandez-Ochoa I., Flaws J.A. Bisphenol A impairs follicle growth, inhibits steroidogenesis, and downregulates rate-limiting enzymes in the estradiol biosynthesis pathway. Toxicol. Sci. 2011, 119:209-217.
49. Peretz J.R., Vrooman L., Ricke W.A., Hunt P.A., Ehrlich S., Hauser R., Padmanabhan V., Taylor H.S., Swan S.H., VandeVoort C.A., Flaws J.A. Bisphenol A and reproductive health: update of experimental and human evidence. Environ. Health Perspect. 2014, PMID: 24896072, (in press). 10.1289/ehp.1307728.
50. Ranjit N., Siefert K., Padmanabhan V. Bisphenol-A and disparities in birth outcomes: a review and directions for future research. J. Perinatol. 2010, 30:2-9.
51. Rouillier P., Sirard M.A., Matton P., Guilbault L.A. Immunoneutralization of transforming growth factor alpha present in bovine follicular fluid prevents the suppression of the follicle-stimulating hormone-induced production of estradiol by bovine granulosa cells cultured in vitro. Biol. Reprod. 1997, 57:341-346.
52. Ryan B.C., Hotchkiss A.K., Crofton K.M., Gray L.E. In utero and lactational exposure to bisphenol A, in contrast to ethinyl estradiol, does not alter sexually dimorphic behavior, puberty, fertility, and anatomy of female LE rats. Toxicol. Sci. 2010, 114:133-148.
53. Santoro N., Isaac B., Neal-Perry G., Adel T., Weingart L., Nussbaum A., Thakur S., Jinnai H., Khosla N., Barad D. Impaired folliculogenesis and ovulation in older reproductive aged women. J. Clin. Endocrinol. Metab. 2003, 88:5502-5509.
54. Savabieasfahani M., Kannan K., Astapova O., Evans N.P., Padmanabhan V. Developmental programming: differential effects of prenatal exposure to bisphenol-A or methoxychlor on reproductive function. Endocrinology 2006, 147:5956-5966.
55. Steckler T., Manikkam M., Inskeep E.K., Padmanabhan V. Developmental programming: follicular persistence in prenatal testosterone-treated sheep is not programmed by androgenic actions of testosterone. Endocrinology 2007, 148:3532-3540.
56. Sun Y., Irie M., Kishikawa N., Wada M., Kuroda N., Nakashima K. Determination of bisphenol A in human breast milk by HPLC with column-switching and fluorescence detection. Biomed. Chromatogr. 2004, 18:501-507.
57. Thayer K., Belcher S. Mechanisms of action of bisphenol A and other biochemical/molecular interactions. FAO/WHO Expert Meeting on Bisphenol A (BPA). Ottawa, Canada, 2-5 November 2010 2010, 1-21.
58. Vandenberg L.N., Hunt P.A., Myers J.P., Vom Saal F.S. Human exposures to bisphenol A: mismatches between data and assumptions. Rev. Environ. Health 2013, 28:37-58.
59. Varayoud J., Ramos J.G., Bosquiazzo V.L., Lower M., Munoz-de-Toro M., Luque E.H. Neonatal exposure to bisphenol A alters rat uterine implantation-associated gene expression and reduces the number of implantation sites. Endocrinology 2011, 152:1101-1111.
60. Veiga-Lopez A., Ye W., Phillips D.J., Herkimer C., Knight P.G., Padmanabhan V. Developmental programming: deficits in reproductive hormone dynamics and ovulatory outcomes in prenatal, testosterone-treated sheep. Biol. Reprod. 2008, 78:636-647.
61. Veiga-Lopez A., Luense L.J., Christenson L.K., Padmanabhan V. Developmental programming: gestational bisphenol-A treatment alters trajectory of fetal ovarian gene expression. Endocrinology 2013, 154:1873-1884.
62. Veiga-Lopez A., Wurst A.K., Steckler T.L., Ye W., Padmanabhan V. developmental programming: postnatal estradiol amplifies ovarian follicular defects induced by fetal exposure to excess testosterone and dihydrotestosterone in sheep. Reprod. Sci. 2014, 21:444-455.
63. vom Saal F.S., Hughes C. An extensive new literature concerning low-dose effects of bisphenol A shows the need for a new risk assessment. Environ. Health Perspect. 2005, 113:926-933.
64. Vonnahme K.A., Hess B.W., Nijland M.J., Nathanielsz P.W., Ford S.P. Placentomal differentiation may compensate for maternal nutrient restriction in ewes adapted to harsh range conditions. J. Anim. Sci. 2006, 84:3451-3459.
65. Waller D.K., Gallaway M.S., Taylor L.G., Ramadhani T.A., Canfield M.A., Scheuerle A., Hernandez-Diaz S., Louik C., Correa A. Use of oral contraceptives in pregnancy and major structural birth defects in offspring. Epidemiology 2010, 21:232-239.
66. Wintermantel T.M., Campbell R.E., Porteous R., Bock D., Grone H.J., Todman M.G., Korach K.S., Greiner E., Perez C.A., Schutz G., Herbison A.E. Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 2006, 52:271-280.
67. Xiao S., Diao H., Smith M.A., Song X., Ye X. Preimplantation exposure to bisphenol A (BPA) affects embryo transport, preimplantation embryo development, and uterine receptivity in mice. Reprod. Toxicol. 2011, 32:434-441.
68. Ying S.J., Xiao S.H., Wang C.L., Zhong B.S., Zhang G.M., Wang Z.Y., He D.Y., Ding X.L., Xing H.J., Wang F. Effect of nutrition on plasma lipid profile and mRNA levels of ovarian genes involved in steroid hormone synthesis in Hu sheep during luteal phase. J. Anim. Sci. 2013, 91:5229-5239.
69. Zhang H.Q., Zhang X.F., Zhang L.J., Chao H.H., Pan B., Feng Y.M., Li L., Sun X.F., Shen W. Fetal exposure to bisphenol A affects the primordial follicle formation by inhibiting the meiotic progression of oocytes. Mol. Biol. Rep. 2012, 39:5651-5657.