Gene expression is altered after bisphenol A exposure in human fetal oocytes in vitro

Molecular Human Reproduction

Volumn 18, Issue 4, 2012, Pages 171-183

  Brieno Enriquez M A ^a,b   Reig Viader, R ^a   Cabero, L ^c   Toran, N ^c   Martinez F ^b   Roig, I ^a   Garcia Caldes M ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE SAN LUIS POTOSÍ   (Mexico)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

BPA; Gene expression; Human; Meiosis; Oocyte

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; BLOOM SYNDROME HELICASE; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGEN RECEPTOR GAMMA; HISTONE H2AX; NALP5 PROTEIN; PROTEIN; PROTEIN MLH1; RPA PROTEIN; SPO11 PROTEIN; STRA8 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME PAIRING; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MEIOSIS; OOCYTE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

CELLS, CULTURED; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; ENDOCRINE DISRUPTORS; FEMALE; GENE EXPRESSION REGULATION; GENETIC MARKERS; HUMANS; OOCYTES; OVARY; PHENOLS; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

SYNAPSIS;

EID: 84858653422     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gar074     Document Type: Article

References (66)

1. Allard P, Colaiacovo MP. Bisphenol A impairs the double-strand break repair machinery in the germline and causes chromosome abnormalities. Proc Natl Acad Sci USA 2010;107:20405-20410.
2. Avissar-Whiting M, Veiga KR, Uhl KM, Maccani MA, Gagne LA, Moen EL, Marsit CJ. Bisphenol A exposure leads to specific microRNA alterations in placental cells. Reprod Toxicol 2010;29:401-406.
3. Biles JE, White KD, McNeal TP, Begley TH. Determination of the diglycidyl ether of bisphenol A and its derivatives in canned foods. J Agric Food Chem 1999;47:1965-1969.
4. Bouskine A, Nebout M, Brucker-Davis F, Benahmed M, Fenichel P. Low doses of bisphenol A promote human seminoma cell proliferation by activating PKA and PKG via a membrane G-protein-coupled estrogen receptor. Environ Health Perspect 2009;117:1053-1058.
5. Brieño-Enriquez MA, Robles P, Garcia-Cruz R, Roig I, Cabero L, Martinez F, Garcia Caldes M. A new culture technique that allows in vitro meiotic prophase development of fetal human oocytes. Hum Reprod 2010;25:74-84.
6. Brieño-Enriquez MA, Robles P, Camats-Tarruella N, Garcia-Cruz R, Roig I, Cabero L, Martinez F, Caldes MG. Human meiotic progression and recombination are affected by Bisphenol A exposure during in vitro human oocyte development. Hum Reprod 2011 2011;26:2807-2818.
7. Can A, Semiz O, Cinar O. Bisphenol-A induces cell cycle delay and alters centrosome and spindle microtubular organization in oocytes during meiosis. Mol Hum Reprod 2005;11:389-396.
8. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, Sedelnikova OA, Reina-San-Martin B, Coppola V, Meffre E, Difilippantonio MJ et al. Genomic instability in mice lacking histone H2AX. Science 2002;296:922-927.
9. Couse JF, Hewitt SC, Bunch DO, Sar M, Walker VR, Davis BJ, Korach KS. Postnatal sex reversal of the ovaries in mice lacking estrogen receptors alpha and beta. Science 1999;286:2328-2331.
10. Chapin RE, Adams J, Boekelheide K, Gray LE Jr, Hayward SW, Lees PS, McIntyre BS, Portier KM, Schnorr TM, Selevan SG et al. NTP-CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A. Birth Defects Res B Dev Reprod Toxicol 2008;83:157-395.
11. Daftary GS, Taylor HS. Endocrine regulation of HOX genes. Endocr Rev 2006;27:331-355.
12. Eichenlaub-Ritter U, Vogt E, Cukurcam S, Sun F, Pacchierotti F, Parry J. Exposure of mouse oocytes to bisphenol A causes meiotic arrest but not aneuploidy. Mutat Res 2008;651:82-92.
13. Engel SM, Levy B, Liu Z, Kaplan D, Wolff MS. Xenobiotic phenols in early pregnancy amniotic fluid. Reprod Toxicol 2006;21:110-112.
14. Fowler PA, Flannigan S, Mathers A, Gillanders K, Lea RG, Wood MJ, Maheshwari A, Bhattacharya S, Collie-Duguid ES, Baker PJ et al. Gene expression analysis of human fetal ovarian primordial follicle formation. J Clin Endocrinol Metab 2009;94:1427-1435.
15. Goodson A, Summerfield W, Cooper I. Survey of bisphenol A and bisphenol F in canned foods. Food Addit Contam 2002;19:796-802.
16. Goodson A, Robin H, SummerfieldW, Cooper I. Migration of bisphenol A from can coatings-effects of damage, storage conditions and heating. Food Addit Contam 2004;21:1015-1026.
17. Guobing X, Junling S, Guohua H, Lixing Z, Tongjun W, Zhijun Z. Investigation into serum BPA and sex hormone levels of workers in epoxy resin manufacturing. J Environ Occup Med 2005;22:295-298.
18. Hoffmann ER, Borts RH. Meiotic recombination intermediates and mismatch repair proteins. Cytogenet Genome Res 2004;107:232-248.
19. Honma S, Suzuki A, Buchanan DL, Katsu Y, Watanabe H, Iguchi T. Low dose effect of in utero exposure to bisphenol A and diethylstilbestrol on female mouse reproduction. Reprod Toxicol 2002;16:117-122.
20. Horard B, Vanacker JM. Estrogen receptor-related receptors: orphan receptors desperately seeking a ligand. J Mol Endocrinol 2003;31:349-357.
21. Houmard B, Small C, Yang L, Naluai-Cecchini T, Cheng E, Hassold T, Griswold M. Global gene expression in the human fetal testis and ovary. Biol Reprod 2009;81:438-443.
22. Hunt PA, Koehler KE, Susiarjo M, Hodges CA, Ilagan A, Voigt RC, Thomas S, Thomas BF, Hassold TJ. Bisphenol a exposure causes meiotic aneuploidy in the female mouse. Curr Biol 2003;13:546-553.
23. Hunt PA, Susiarjo M, Rubio C, Hassold TJ. The bisphenol A experience: a primer for the analysis of environmental effects on mammalian reproduction. Biol Reprod 2009;81:807-813.
24. Huppunen J, Aarnisalo P. Dimerization modulates the activity of the orphan nuclear receptor ERRgamma. Biochem Biophys Res Commun 2004;314:964-970.
25. Imanaka M, Sasaki K, Nemoto S, Ueda E, Murakami E, Miyata D, Tonogai Y. Determination of bisphenol A in foods using GC/MS. Shokuhin Eiseigaku Zasshi 2001;42:71-78.
26. Iso T, Watanabe T, Iwamoto T, Shimamoto A, Furuichi Y. DNA damage caused by bisphenol A and estradiol through estrogenic activity. Biol Pharm Bull 2006;29:206-210.
27. Iso T, Futami K, Iwamoto T, Furuichi Y. Modulation of the expression of bloom helicase by estrogenic agents. Biol Pharm Bull 2007;30:266-271.
28. Kuiper GG, Shughrue PJ, Merchenthaler I, Gustafsson JA. The estrogen receptor beta subtype: a novel mediator of estrogen action in neuroendocrine systems. Front Neuroendocrinol 1998;19:253-286.
29. Kuruto-Niwa R, Tateoka Y, Usuki Y, Nozawa R. Measurement of bisphenol A concentrations in human colostrum. Chemosphere 2007; 66:1160-1164.
30. Lawson C, Gieske M, Murdoch B, Ye P, Li Y, Hassold T, Hunt PA. Gene expression in the fetal mouse ovary is altered by exposure to low doses of bisphenol A. Biol Reprod 2010;84:79-86.
31. Lehmann L, Metzler M. Bisphenol A and its methylated congeners inhibit growth and interfere with microtubules in human fibroblasts in vitro. Chem Biol Interact 2004;147:273-285.
32. Lemmen JG, Arends RJ, van der Saag PT, van der Burg B. In vivo imaging of activated estrogen receptors in utero by estrogens and bisphenol A. Environ Health Perspect 2004;112:1544-1549.
33. Lenie S, Cortvrindt R, Eichenlaub-Ritter U, Smitz J. Continuous exposure to bisphenol A during in vitro follicular development induces meiotic abnormalities. Mutat Res 2008;651:71-81.
34. Mariscal-Arcas M, Rivas A, Granada A, Monteagudo C, Murcia MA, Olea-Serrano F. Dietary exposure assessment of pregnant women to bisphenol-A from cans and microwave containers in Southern Spain. Food Chem Toxicol 2009;47:506-510.
35. Miyamoto T, Shiozawa T, Kashima H, Feng YZ, Suzuki A, Kurai M, Nikaido T, Konishi I. Estrogen up-regulates mismatch repair activity in normal and malignant endometrial glandular cells. Endocrinology 2006; 147:4863-4870.
36. Mlynarcikova A, Nagyova E, Fickova M, Scsukova S. Effects of selected endocrine disruptors on meiotic maturation, cumulus expansion, synthesis of hyaluronan and progesterone by porcine oocyte-cumulus complexes. Toxicol In Vitro 2009;23:371-377.
37. Myers JP, vom Saal FS, Akingbemi BT, Arizono K, Belcher S, Colborn T, Chahoud I, Crain DA, Farabollini F, Guillette LJ Jr et al. Why public health agencies cannot depend on good laboratory practices as a criterion for selecting data: the case of bisphenol A. Environ Health Perspect 2009;117:309-315.
38. Naciff JM, Jump ML, Torontali SM, Carr GJ, Tiesman JP, Overmann GJ, Daston GP. Gene expression profile induced by 17alpha-ethynyl estradiol, bisphenol A, and genistein in the developing female reproductive system of the rat. Toxicol Sci 2002;68:184-199.
39. Oakley GG, Patrick SM. Replication protein A: directing traffic at the intersection of replication and repair. Front Biosci 2010;15:883-900.
40. Okada H, Tokunaga T, Liu X, Takayanagi S, Matsushima A, Shimohigashi Y. Direct evidence revealing structural elements essential for the high binding ability of bisphenol A to human estrogen-related receptor-gamma. Environ Health Perspect 2008;116:32-38.
41. Onn Wong K,Woon Leo L, Leng Seah H. Dietary exposure assessment of infants to bisphenol A from the use of polycarbonate baby milk bottles. Food Addit Contam 2005;22:280-288.
42. Pennie WD, Aldridge TC, Brooks AN. Differential activation by xenoestrogens of ER alpha and ER beta when linked to different response elements. J Endocrinol 1998;158:R11-R14.
43. Rockmill B, Fung JC, Branda SS, Roeder GS. The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr Biol 2003; 13:1954-1962.
44. Rodrigue A, Lafrance M, Gauthier MC, McDonald D, Hendzel M, West SC, Jasin M, Masson JY. Interplay between human DNA repair proteins at a unique double-strand break in vivo. EMBO J 2006;25:222-31.
45. Roig I, Vanrell I, Ortega A, Cabero L, Egozcue J, Garcia M. The use of foetal ovarian stromal cell culture for cytogenetic diagnosis. Stromal ovarian culture cytogenetic diagnosis. Cytotechnology 2003;41:45-9.
46. Schonfelder G, Wittfoht W, Hopp H, Talsness CE, Paul M, Chahoud I. Parent bisphenol A accumulation in the human maternal-fetal-placental unit. Environ Health Perspect 2002;110:A703-A707.
47. Schonfelder G, Friedrich K, Paul M, Chahoud I. Developmental effects of prenatal exposure to bisphenol a on the uterus of rat offspring. Neoplasia 2004;6:584-594.
48. Sugiura-Ogasawara M, Ozaki Y, Sonta S, Makino T, Suzumori K. Exposure to bisphenol A is associated with recurrent miscarriage. Hum Reprod 2005;20:2325-2329.
49. Susiarjo M, Hassold TJ, Freeman E, Hunt PA. Bisphenol A exposure in utero disrupts early oogenesis in the mouse. PLoS Genet 2007;3:e5.
50. Suzuki A, Sugihara A, Uchida K, Sato T, Ohta Y, Katsu Y, Watanabe H, Iguchi T. Developmental effects of perinatal exposure to bisphenol-A and diethylstilbestrol on reproductive organs in female mice. Reprod Toxicol 2002;16:107-116.
51. Takayanagi S, Tokunaga T, Liu X, Okada H, Matsushima A, Shimohigashi Y. Endocrine disruptor bisphenol A strongly binds to human estrogen-related receptor gamma (ERRgamma) with high constitutive activity. Toxicol Lett 2006;167:95-105.
52. Takeuchi T, Tsutsumi O. Serum bisphenol a concentrations showed gender differences, possibly linked to androgen levels. Biochem Biophys Res Commun 2002;291:76-78.
53. Takeuchi T, Tsutsumi O, Ikezuki Y, Takai Y, Taketani Y. Positive relationship between androgen and the endocrine disruptor, bisphenol A, in normal women and women with ovarian dysfunction. Endocr J 2004;51:165-169.
54. Tedesco M, La Sala G, Barbagallo F, De Felici M, Farini D. STRA8 shuttles between nucleus and cytoplasm and displays transcriptional activity. J Biol Chem 2009;284:35781-35793.
55. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A (BPA). Reprod Toxicol 2007;24:139-177.
56. Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev 2009;30:75-95.
57. 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 2010a;118:1055-1070.
58. Vandenberg LN, Chahoud I, Padmanabhan V, Paumgartten FJ, Schoenfelder G. Biomonitoring studies should be used by regulatory agencies to assess human exposure levels and safety of bisphenol A. Environ Health Perspect 2010b;118:1051-1054.
59. Vaskivuo TE, Maentausta M, Torn S, Oduwole O, Lonnberg A, Herva R, Isomaa V, Tapanainen JS. Estrogen receptors and estrogen-metabolizing enzymes in human ovaries during fetal development. J Clin Endocrinol Metab 2005;90:3752-3756.
60. Washington W, Hubert L, Jones D, Gray WG. Bisphenol a binds to the low-affinity estrogen binding site. In Vitr Mol Toxicol 2001;14:43-51.
61. Wetherill YB, Akingbemi BT, Kanno J, McLachlan JA, Nadal A, Sonnenschein C, Watson CS, Zoeller RT, Belcher SM. In vitro molecular mechanisms of bisphenol A action. Reprod Toxicol 2007; 24:178-198.
62. Willhite CC, Ball GL, McLellan CJ. Derivation of a bisphenol A oral reference dose (RfD) and drinking-water equivalent concentration. J Toxicol Environ Health B Crit Rev 2008;11:69-146.
63. Wu L, Hickson ID. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 2003;426:870-874.
64. Yamada H, Furuta I, Kato EH, Kataoka S, Usuki Y, Kobashi G, Sata F, Kishi R, Fujimoto S. Maternal serum and amniotic fluid bisphenol A concentrations in the early second trimester. Reprod Toxicol 2002; 16:735-739.
65. Yang M, Park MS, Lee HS. Endocrine disrupting chemicals: human exposure and health risks. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 2006;24:183-224.
66. Zalko D, Soto AM, Dolo L, Dorio C, Rathahao E, Debrauwer L, Faure R, Cravedi JP. Biotransformations of bisphenol A in a mammalian model: answers and new questions raised by low-dose metabolic fate studies in pregnant CD1 mice. Environ Health Perspect 2003;111:309-319.