Developmental programming: Gestational bisphenol-A treatment alters trajectory of fetal ovarian gene expression

Endocrinology

Volumn 154, Issue 5, 2013, Pages 1873-1884

  Veiga Lopez, Almudena ^a   Luense, Lacey J ^b   Christenson, Lane K ^b   Padmanabhan, Vasantha ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; AROMATASE; GONADOTROPIN RECEPTOR; INSULIN RECEPTOR; MESSENGER RNA; MICRORNA; RNA; STEM CELL FACTOR; STEROID; STEROID 5ALPHA REDUCTASE; TRANSCRIPTION FACTOR SOX; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DRUG BLOOD LEVEL; ENVIRONMENTAL EXPOSURE; EWE; FETUS; GENE EXPRESSION; GESTATIONAL AGE; MATERNAL BLOOD; NONHUMAN; OVARY; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEROIDOGENESIS; UMBILICAL ARTERY;

ANIMALS; BENZHYDRYL COMPOUNDS; EMBRYONIC DEVELOPMENT; ENDOCRINE DISRUPTORS; FEMALE; FETUS; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; MATERNAL EXPOSURE; OVARY; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SHEEP;

EID: 84876767001     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-2129     Document Type: Article

References (76)

1. Hartgens F, Kuipers H. Effects of androgenic-Anabolic steroids in athletes. Sports Med. 2004;34:513-554.
2. Waller DK, Gallaway MS, Taylor LG, et al. Use of oral contraceptives in pregnancy and major structural birth defects in offspring. Epidemiology. 2010;21:232-239.
3. Hotchkiss AK, Rider CV, Blystone CR, 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.
4. Heindel JJ, vom Saal FS. Role of nutrition and environmental endocrine disrupting chemicals during the perinatal period on the aetiology of obesity. Mol Cell Endocrinol. 2009;304:90-96.
5. vom Saal FS, 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.
6. Kuch HM, Ballschmiter K. Determination of endocrine-disrupting phenolic compounds and estrogens in surface and drinking water by HRGC-(NCI)-MS in the picogram per liter range. Environ Sci Technol. 2001;35:3201-3206.
7. Rudel RA, Brody JG, Spengler JD, et al. Identification of selected hormonally active agents and animal mammary carcinogenesis in commercial and residential air and dust samples. J Air Waste Manage Assoc. 2001;51:499-513.
8. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol. 2007;24: 139-177.
9. Vandenberg LN, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, Schoenfelder G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Perspect. 2010;118:1055-1070.
10. Padmanabhan V, Siefert K, Ransom S, et al. Maternal bisphenol-A levels at delivery: a looming problem? J Perinatol. 2008;28:258-263.
11. 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.
12. Schonfelder G, Wittfoht W, Hopp H, Talsness CE, Paul M, Chahoud I. Parent bisphenol A accumulation in the human maternalfetal-placental unit. Environ Health Perspect. 2002;110:A703-A707.
13. Edlow AG, Chen M, Smith NA, Lu C, McElrath TF. Fetal bisphenol A exposure: concentration of conjugated and unconjugated bisphenol A in amniotic fluid in the second and third trimesters. Reprod Toxicol. 2012;34:1-7.
14. 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.
15. CalafatAM,Weuve J, Ye X, et al. Exposure to bisphenolAand other phenols in neonatal intensive care unit premature infants. Environ Health Perspect. 2009;117:639-644.
16. Quesada I, Fuentes E, Viso-Leon MC, Soria B, Ripoll C, Nadal A. Low doses of the endocrine disruptor bisphenol-A and the native hormone 17-estradiol rapidly activate transcription factor CREB. FASEB J. 2002;16:1671-1673.
17. Zsarnovszky A, Le HH, Wang HS, Belcher SM. Ontogeny of rapid estrogen-mediated extracellular signal-regulated kinase signaling in the rat cerebellar cortex: potent nongenomic agonist and endocrine disrupting activity of the xenoestrogen bisphenol A. Endocrinology. 2005;146:5388-5396.
18. Sohoni P, Sumpter JP. Several environmental oestrogens are also anti-Androgens. J Endocrinol. 1998;158:327-339.
19. Kitamura S, Suzuki T, Sanoh S, et al. Comparative study of the endocrine-disrupting activity of bisphenol A and 19 related compounds. Toxicol Sci. 2005;84:249-259.
20. Moriyama K, Tagami T, Akamizu T, et al. Thyroid hormone action is disrupted by bisphenol A as an antagonist, J Clin Endocrinol Metab. 2002;87:5185-5190.
21. Prasanth GK, Divya LM, Sadasivan C. Bisphenol-A can bind to human glucocorticoid receptor as an agonist: an in silico study. J Appl Toxicol. 2010;30:769-774.
22. Alonso-Magdalena P, Vieira E, Soriano S, et al. Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect. 2010;118:1243-1250.
23. Padmanabhan V, Sarma HN, Savabieasfahani M, Steckler TL, Veiga-Lopez A. Developmental reprogramming of reproductive and metabolic dysfunction in sheep: native steroids vs. environmental steroid receptor modulators. Int J Androl. 2010;33:394-404.
24. Padmanabhan V, Veiga-Lopez A. Developmental origin of reproductive and metabolic dysfunctions: androgenic versus estrogenic reprogramming. Semin Reprod Med. 2011;29:173-186.
25. Luense LJ, Veiga-Lopez A, Padmanabhan V, Christenson LK. Developmental programming: gestational testosterone treatment alters fetal ovarian gene expression. Endocrinology. 2011;152:4974-4983.
26. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet. 2008;9:102-114.
27. Ortega HH, Salvetti NR, Padmanabhan V. Developmental programming: prenatal androgen excess disrupts ovarian steroid receptor balance. Reproduction. 2009;137:865-877.
28. Ortega HH, Rey F, VelazquezMM,Padmanabhan V. Developmental programming: effect of prenatal steroid excess on intraovarian components of insulin signaling pathway and related proteins in sheep. Biol Reprod. 2010;82:1065-1075.
29. Savabieasfahani M, Kannan K, Astapova O, Evans NP, Padmanabhan V. Developmental programming: differential effects of prenatal exposure to bisphenol-A or methoxychlor on reproductive function. Endocrinology. 2006;147:5956-5966.
30. Padmanabhan V, Halubai S, Veiga-Lopez A, Liao C, Domino S, Kannan K. 2011 Maternal-cord blood levels of bisphenol-A (BPA) in human and following BPA administration in pregnant sheep. Paper presented at: Society of Toxicology, 50th Annual Meeting, Washington, DC, March 6-10, 2011; Abstract 2186:310.
31. Mandon-Pepin B, Oustry-Vaiman A, Vigier B, Piumi F, Cribiu E, Cotinot C. Expression profiles and chromosomal localization of genes controlling meiosis and follicular development in the sheep ovary. Biol Reprod. 2003;68:985-995.
32. Juengel JL, Bodensteiner KJ, Heath DA, et al. Physiology of GDF9 and BMP15 signalling molecules. Anim Reprod Sci. 2004;82-83: 447-460.
33. Hogg K, McNeilly AS, Duncan WC. Prenatal androgen exposure leads to alterations in gene and protein expression in the ovine fetal ovary. Endocrinology. 2011;152:2048-2059.
34. Sawyer HR, Smith P, Heath DA, Juengel JL, Wakefield SJ, McNatty KP. Formation of ovarian follicles during fetal development in sheep. Biol Reprod. 2002;66:1134-1150.
35. Payen E, Pailhoux E, Abou Merhi R, et al. Characterization of ovine SRY transcript and developmental expression of genes involved in sexual differentiation. Int J Dev Biol. 1996;40:567-575.
36. Xi W, Lee CK, Yeung WS, et al. Effect of perinatal and postnatal bisphenolAexposure to the regulatory circuits at the hypothalamuspituitary- gonadal axis of CD-1 mice. Reprod Toxicol. 2011;31: 409-417.
37. Nativelle-Serpentini C, Richard S, Séralini GE, Sourdaine P. Aromatase activity modulation by lindane and bisphenol-A in human placental JEG-3 and transfected kidney E293 cells. Toxicol In Vitro. 2003;17:413-422.
38. ChungE, GencoMC,Megrelis L, Ruderman JV. Effects of bisphenol A and triclocarban on brain-specific expression of aromatase in early zebrafish embryos. Proc Natl Acad SciUSA. 2011;108:17732-17737.
39. Kubo K, Arai O, Omura M, Watanabe R, Ogata R, Aou S. Low dose effects of bisphenol A on sexual differentiation of the brain and behavior in rats. Neurosci Res. 2003;45:345-356.
40. Kim JY, Han EH, Kim HG, et al. Bisphenol A-induced aromatase activation is mediated by cyclooxygenase-2 up-regulation in rat testicular Leydig cells. Toxicol Lett. 2010;193:200-208.
41. Ye L, Zhao B, Hu G, Chu Y, Ge RS. Inhibition of human and rat testicular steroidogenic enzyme activities by bisphenol A. Toxicol Lett. 2011;207:137-142.
42. Grasselli F, Baratta L, Baioni L, et al. BisphenolAdisrupts granulosa cell function. Domest Anim Endocrinol. 2010;39:34-39.
43. Peretz J, Gupta RK, Singh J, Hernandez-Ochoa I, Flaws JA. Bisphenol A impairs follicle growth, inhibits steroidogenesis, and downregulates rate-limiting enzymes in the estradiol biosynthesis pathway. Toxicol Sci. 2011;119:209-217.
44. Kwintkiewicz J, Nishi Y, Yanase T, Giudice LC. Peroxisome proliferator-Activated receptor-α mediates bisphenol A inhibition of FSH-stimulated IGF-1, aromatase, and estradiol in human granulosa cells. Environ Health Perspect. 2010;118:400-406.
45. Lei L, Jin S, Gonzalez G, Behringer RR, Woodruff TK. The regulatory role of Dicer in folliculogenesis in mice. Mol Cel Endocr. 2010;315:63-73.
46. Hong X, Luense LJ, McGinnis LK, Nothnick WB, Christenson LK. Dicer1 is essential for female fertility and normal development of the female reproductive system. Endocrinology. 2008;149:6207-6212.
47. Nagaraja AK, Andreu-Vieyra C, Franco HL, et al. Deletion of Dicer in somatic cells of the female reproductive tract causes sterility. Mol Endocrinol. 2008;22:2336-2352.
48. Torley KJ, da Silveira JC, Smith P, Anthony RV, Veeramachaneni DN, Winger QA, Bouma GJ. Expression of miRNAs in ovine fetal gonads: potential role in gonadal differentiation. Reprod Biol Endocrinol. 2011;9:2.
49. Bannister SC, Smith CA, Roeszler KN, Doran TJ, Sinclair AH, Tizard ML. Manipulation of estrogen synthesis alters MIR202 expression in embryonic chicken gonads. Biol Reprod. 2011;85:22-30.
50. Mishima T, Takizawa T, Luo SS, et al. MicroRNA (miRNA) cloning analysis reveals sex differences in miRNA expression profiles between adult mouse testis and ovary. Reproduction. 2008;136: 811-822.
51. Menghini R, Casagrande V, Cardellini M, et al. MicroRNA 217 modulates endothelial cell senescence via silent information regulator 1. Circulation. 2009;120:1524-1532.
52. Maes OC, An J, Sarojini H, Wu H, Wang E. Changes in MicroRNA expression patterns in human fibroblasts after low-LET radiation. J Cell Biochem. 2008;105:824-834.
53. Hsu PY, Deatherage DE, Rodriguez BA, et al. Xenoestrogen-induced epigenetic repression of microRNA-9-3 in breast epithelial cells. Cancer Res. 2009;69:5936-5945.
54. Hou L, Wang D, Baccarelli A. Environmental chemicals and microRNAs. Mutat Res. 2011;714:105-112.
55. Avissar-Whiting M, Veiga KR, Uhl KM, et al. BisphenolAexposure leads to specific microRNA alterations in placental cells. Reprod Tox. 2010;29:401-406.
56. Tilghman SL, Bratton MR, Segar HC, et al. Endocrine disruptor regulation of microRNA expression in breast carcinoma cells. PLoS One. 2012;7:e32754.
57. Bannister SC, Tizard ML, Doran TJ, Sinclair AH, Smith CA. Sexually dimorphic microRNA expression during chicken embryonic gonadal development. Biol Reprod. 2009;81:165-176.
58. Sirotkin AV, Ovcharenko D, Grossmann R, Laukova M, Mlyncek M. Identification of microRNAs controlling human ovarian cell steroidogenesis via a genome-scale screen. J Cell Physiol. 2009;219: 415-420.
59. Iorio MV, Visone R, Di Leva G, et al. MicroRNA signatures in human ovarian cancer. Cancer Res. 2007;67:8699-8707.
60. Zhou Y, Zhu Y, Zhang S, Wang H, Wang S, Yang X. MicroRNA expression profiles in premature ovarian failure patients and its potential regulate functions. Chin J Birth Health Hered. 2011;19:20-22.
61. Hunt SM, Clarke CL. Expression and hormonal regulation of the Sox4 gene in mouse female reproductive tissues. Biol Reprod. 1999; 61:476-481.
62. Komatsu N, Hiraoka Y, Shiozawa M, Ogawa M, Aiso S. Cloning and expression of Xenopus laevis xSox12 cDNA. Biochim Biophys Acta. 1996;1305:117-119.
63. Narahara M, Yamada A, Hamada-Kanazawa M, Kawai Y, Miyake M. cDNA cloning of the Sry-related gene Sox6 from rat with tissuespecific expression. Biol Pharm Bull. 2002;25:705-709.
64. Chaboissier MC, Kobayashi A, Vidal VI,. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development. 2004;131:1891-1901.
65. Zhang L, Lin D, Zhang Y, Ma G, Zhang W. A homologue of Sox11 predominantly expressed in the ovary of the orange-spotted grouper Epinephelus coioides. Comp Biochem Physiol B Biochem Mol Biol. 2008;149:345-353.
66. Kiefer JC. Back to basics: Sox genes. Dev Dyn. 2007;236:2356-2366.
67. Nunez-Iglesias J, Liu CC, Morgan TE, Finch CE, Zhou XJ. Joint genome-wide profiling of miRNA and mRNA expression in Alzheimer's disease cortex reveals altered miRNA regulation. PLoS One. 2010;5:e8898.
68. Nothnick WB, Healy C, Hong X. Steroidal regulation of uterine miRNAs is associated with modulation of the miRNA biogenesis components Exportin-5 and Dicer1. Endocrine. 2010;37:265-273.
69. Davis-Dusenbery BN, Hata A. Mechanisms of control of microRNA biogenesis. J Biochem. 2010;148:381-392.
70. Chou WC, Chen JL, Lin CF, Chen YC, Shih FC, Chuang CY. Biomonitoring of bisphenol A concentrations in maternal and umbilical cord blood in regard to birth outcomes and adipokine expression: a birth cohort study in Taiwan. Environ Health. 2011;10: 94.
71. Kosarac I,KubwaboC, Lalonde K, FosterW.Anovel method for the quantitative determination of free and conjugated bisphenol A in human maternal and umbilical cord blood serum using a two-step solid phase extraction and gas chromatography/tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci. 2012; 898:90-94.
72. Vandenberg LN, MaffiniMV,Sonnenschein C, Rubin BS, SotoAM. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev. 2009;30:75-95.
73. Shelby M. National toxicology program -CERHR monograph on the potential human reproductive and developmental effects of bisphenol A.NIHpublication no 2008;08-5994. Bethesda, Maryland: National Institutes of Health.
74. Prins GS, Ye SH, Birch L, Ho SM, Kannan K. Serum bisphenol A pharmacokinetics and prostate neoplastic responses following oral and subcutaneous exposures in neonatal Sprague-Dawley rats. Reprod Toxicol. 2011;31:1-9.
75. Rubin BS. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol. 2011; 127:27-34.
76. Vandenberg LN, Colborn T, Hayes TB, et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev. 2012;33:378-455.