DNA methylation changes in whole blood is associated with exposure to the environmental contaminants, mercury, lead, cadmium and bisphenol A, in women undergoing ovarian stimulation for IVF

Human Reproduction

Volumn 27, Issue 5, 2012, Pages 1401-1410

  Hanna, Courtney W ^a,b   Bloom, Michael S ^c   Robinson, Wendy P ^a,b   Kim, Dongsul ^c   Parsons, Patrick J ^c,d   Vom Saal, Frederick S ^e   Taylor, Julia A ^e   Steuerwald, Amy J ^c,d   Fujimoto, Victor Y ^f  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c STATE UNIVERSITY OF NEW YORK   (United States)

^d WADSWORTH CENTER   (United States)

^e UNIVERSITY OF MISSOURI   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bisphenol A (BPA); DNA methylation; IVF; Lead (Pb); Mercury (Hg)

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; CADMIUM; GLUTATHIONE TRANSFERASE M1; LEAD; MERCURY;

ADULT; ARTICLE; BLOOD ANALYSIS; CELL POPULATION; CPG ISLAND; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; FEMALE; FERTILIZATION IN VITRO; HUMAN; INFERTILITY; MAJOR CLINICAL STUDY; OOCYTE RETRIEVAL; OVULATION INDUCTION; PROMOTER REGION;

EID: 84860110624     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/des038     Document Type: Article

References (75)

1. Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 2005;3: 28.
2. Al-Saleh I, Coskun S, Mashhour A, Shinwari N, El-Doush I, Billedo G, Jaroudi K, Al-Shahrani A, Al-Kabra M, El Din Mohamed G. Exposure to heavy metals (lead, cadmium and mercury) and its effect on the outcome of in-vitro fertilization treatment. Int J Hyg Environ Health 2008;211: 560-579.
3. ATSDR. Toxicological Profile for Cadmium. Atlanta, GA: U.S. Agency for Toxic Substances and Disease Registry, 1999a.
4. ATSDR. Toxicological Profile for Mercury. Atlanta, GA: U.S. Agency for Toxic Substances and Disease Registry, 1999b.
5. ATSDR. Toxicological Profile for Lead. Atlanta, GA: U.S. Agency for Toxic Substances and Disease Registry, 2007.
6. Baccarelli A, Wright RO, Bollati V, Tarantini L, Litonjua AA, Suh HH, Zanobetti A, Sparrow D, Vokonas PS, Schwartz J. Rapid DNA methylation changes after exposure to traffic particles. Am J Respir Crit Care Med 2009;179: 572-578.
7. Bell A, Bell D, Weber RS, El-Naggar AK. CpG island methylation profiling in human salivary gland adenoid cystic carcinoma. Cancer 2011; 117: 2898-2909.
8. Bloom MS, Parsons PJ, Steuerwald AJ, Schisterman EF, Browne RW, Kim K, Coccaro GA, Conti GC, Narayan N, Fujimoto VY. Toxic trace metals and human oocytes during in vitro fertilization (IVF). Reprod Toxicol 2010;29: 298-305.
9. Bloom MS, Buck Louis GM, Sundaram R, Kostyniak PJ, Jain J. Associations between blood metals and fecundity among women residing in New York State. Reprod Toxicol 2011a;31: 158-163.
10. Bloom MS, Kim D, Vom Saal FS, Taylor JA, Cheng G, Lamb JD, Fujimoto VY. Bisphenol A exposure reduces the estradiol response to gonadotropin stimulation during in vitro fertilization. Fertil Steril 2011b; 96: 672-677.
11. Bloom MS, Parsons PJ, Kim D, Steuerwald AJ, Vaccari S, Cheng G, Fujimoto VY. Toxic trace metals and embryo quality indicators during in vitro fertilization (IVF). Reprod Toxicol 2011c;31: 164-170.
12. Board P, Coggan M, Johnston P, Ross V, Suzuki T, Webb G. Genetic heterogeneity of the human glutathione transferases: a complex of gene families. Pharmacol Ther 1990;48: 357-369.
13. Bollati V, Baccarelli A. Environmental epigenetics. Heredity 2010; 105: 105-112.
14. Bollati V, Baccarelli A, Hou L, Bonzini M, Fustinoni S, Cavallo D, Byun HM, Jiang J, Marinelli B, Pesatori AC et al. Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Res 2007; 67: 876-880.
15. Borja-Aburto VH, Hertz-Picciotto I, Lopez MR, Farias P, Rios C, Blanco J. Blood lead levels measured prospectively and risk of spontaneous abortion. Am J Epidemiol 1999;150: 590-597. (Pubitemid 29426903)
16. Breton CV, Byun HM, Wenten M, Pan F, Yang A, Gilliland FD. Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am J Respir Crit Care Med 2009;180: 462-467.
17. Bromer JG, Zhou Y, Taylor MB, Doherty L, Taylor HS. Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response. FASEB J 2010; 24: 2273-2280.
18. Bruchova H, Vasikova A, Merkerova M, Milcova A, Topinka J, Balascak I, Pastorkova A, Sram RJ, Brdicka R. Effect of maternal tobacco smoke exposure on the placental transcriptome. Placenta 2010;31: 186-191.
19. Buck Louis GM, Lynch CD, Cooney MA. Environmental influences on female fecundity and fertility. Semin Reprod Med 2006;24: 147-155.
20. Cabaton NJ, Wadia PR, Rubin BS, Zalko D, Schaeberle CM, Askenase MH, Gadbois JL, Tharp AP, Whitt GS, Sonnenschein C et al. Perinatal exposure to environmentally relevant levels of bisphenol A decreases fertility and fecundity in CD-1 mice. Environ Health Perspect 2011;119: 547-552.
21. Calafat AM, Weuve J, Ye X, Jia LT, 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.
22. California Occupational Blood Lead Registry. www.cdph.ca.gov/programs/ olppp/Pages/Registry.aspx, accessed July 20th, 2011, State of California Department of Public Health.
23. CDC. Fourth National Report on human exposure to environmental chemicals-updated tables, July 2010. Atlanta, GA: U.S Centers for Disease Control and Prevention 2010.
24. Chang S-H, Cheng B-H, Lee S-L, Chuang H-Y, Yang C-Y, Sung F-C, Wu T-N. Low blood lead concentration in association with infertility in women. Environ Res 2006;101: 380-386. (Pubitemid 43782673)
25. Choy CMY, Lam CWK, Cheung LTF, Briton-Jones CM, Cheung LP, Haines CJ. Infertility, blood mercury concentrations and dietary seafood consumption: a case-control study. BJOG 2002; 109: 1121-1125. (Pubitemid 35287081)
26. Cole DC, Wainman B, Sanin LH, Weber JP, Muggah H, Ibrahim S. Environmental contaminant levels and fecundability among non-smoking couples. Reprod Toxicol 2006;22: 13-19. (Pubitemid 43963320)
27. Dhillon VS, Shahid M, Husain SA. Associations of MTHFR DNMT3b 4977 bp deletion in mtDNA and GSTM1 deletion, and aberrant CpG island hypermethylation of GSTM1 in non-obstructive infertility in Indian men. Mol Hum Reprod 2007;13: 213-222. (Pubitemid 46554738)
28. Dolinoy DC, Huang D, Jirtle RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci USA 2007;104: 13056-13061. (Pubitemid 351737592)
29. Edwards TM, Myers JP. Environmental exposures and gene regulation in disease etiology. Environ Health Perspect 2007;115: 1264-1270. (Pubitemid 47484765)
30. 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-Gen Toxicol Environ Mutag 2008; 651: 82-92.
31. Etcheverry A, Aubry M, de Tayrac M, Vauleon E, Boniface R, Guenot F, Saikali S, Hamlat A, Riffaud L, Menei P et al. DNA methylation in glioblastoma: impact on gene expression and clinical outcome. BMC Genomics 2010;11: 701.
32. Fujimoto VY, Kim D, vom Saal FS, Lamb JD, Taylor JA, Bloom MS. Serum unconjugated bisphenol A concentrations in women may adversely influence oocyte quality during in vitro fertilization. Fertil Steril 2011; 95: 1816-1819.
33. Hengstler JG, Foth H, Gebel T, Kramer P-J, Lilienblum W, Schweinfurth H, Vö lkel W, Wollin K-M, Gundert-Remy U. Critical evaluation of key evidence on the human health hazards of exposure to bisphenol A. Crit Rev Toxicol 2011;41: 263-291.
34. Ho SM, Tang WY, Belmonte De Frausto J, Prins GS. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res 2006;66: 5624-5632. (Pubitemid 43927114)
35. 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. (Pubitemid 36391931)
36. Jiang G, Xu L, Song S, Zhu C, Wu Q, Zhang L, Wu L. Effects of long-term low-dose cadmium exposure on genomic DNA methylation in human embryo lung fibroblast cells. Toxicology 2008;244: 49-55. (Pubitemid 50013239)
37. Kandaraki E, Chatzigeorgiou A, Livadas S, Palioura E, Economou F, Koutsilieris M, Palimeri S, Panidis D, Diamanti-Kandarakis E. Endocrine disruptors and Polycystic ovary syndrome (PCOS): elevated serum levels of bisphenol A in women with PCOS. J Clin Endocrinol Metab 2011;96: E480-E484.
38. Mannervik B. The isoenzymes of glutathione transferase. Adv Enzymol Relat Areas Mol Biol 1985;57: 357-417.
39. Matthews JB, Twomey K, Zacharewski TR. In vitro and in vivo interactions of bisphenol A and its metabolite, bisphenol A glucuronide, with estrogen receptors a and b. Chem Res Toxicol 2001;14: 149-157. (Pubitemid 32173316)
40. Mendola P, Messer LC, Rappazzo K. Science linking environmental contaminant exposures with fertility and reproductive health impacts in the adult female. Fertil Steril 2008;89: e81-e94. (Pubitemid 351749398)
41. Minnich MG, Miller DC, Parsons PJ. Determination of As, Cd, Pb, and Hg in urine using inductively coupled plasma mass spectrometry with the direct injection high efficiency nebulizer. Spectrochim Acta Part B At Spectrosc 2008;63: 389-395.
42. Mok-Lin E, Ehrlich S, Williams PL, Petrozza J, Wright DL, Calafat AM, Ye X, Hauser R. Urinary bisphenol A concentrations and ovarian response among women undergoing IVF. Int J Androl 2010; 33: 385-393.
43. Nelson HH, Marsit CJ, Kelsey KT. 'Global methylation' in exposure biology and translational medical science. Environ Health Perspect 2011; 119: 1523-1528.
44. Newbold RR. Prenatal exposure to diethylstilbestrol (DES). Fertil Steril 2008;89: e55-e56. (Pubitemid 351756456)
45. Padmanabhan V, Siefert K, Ransom S, Johnson T, Pinkerton J, Anderson L, Tao L, Kannan K. Maternal bisphenol-A levels at delivery: a looming problemi J Perinatol 2008;28: 258-263. (Pubitemid 351493659)
46. Palmer CD, Lewis ME Jr, Geraghty CM, Barbosa F Jr, Parsons PJ. Determination of lead, cadmium and mercury in blood for assessment of environmental exposure: a comparison between inductively coupled plasma-mass spectrometry and atomic absorption spectrometry. Spectrochim Acta Part B At Spectrosc 2006;61: 980-990. (Pubitemid 44636085)
47. Pearson WR, Vorachek WR, Xu SJ, Berger R, Hart I, Vannais D, Patterson D. Identification of class-mu glutathione transferase genes GSTM1-GSTM5 on human chromosome Ip13. Am J Hum Genet 1993; 53: 220-233. (Pubitemid 23313753)
48. Peng DF, Razvi M, Chen H, Washington K, Roessner A, Schneider-Stock R, El-Rifai W. DNA hypermethylation regulates the expression of members of the Mu-class glutathione S-transferases and glutathione peroxidases in Barrett's adenocarcinoma. Gut 2009; 58: 5-15.
49. Prins GS, Tang WY, Belmonte J, Ho SM. Perinatal exposure to oestradiol and bisphenol A alters the prostate epigenome and increases susceptibility to carcinogenesis. Basic Clin Pharmacol Toxicol 2008; 102: 134-138. (Pubitemid 351143423)
50. Richter CA, Birnbaum LS, Farabollini F, Newbold RR, Rubin BS, Talsness CE, Vandenbergh JG, Walser-Kuntz DR, vom Saal FS. In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 2007;24: 199-224. (Pubitemid 47385096)
51. Romero R, Friel LA, Velez Edwards DR, Kusanovic JP, Hassan SS, Mazaki-Tovi S, Vaisbuch E, Kim CJ, Erez O, Chaiworapongsa T et al. A genetic association study of maternal and fetal candidate genes that predispose to preterm prelabor rupture of membranes (PROM). Am J Obstet Gynecol 2010;203: 361.e1-361.e30.
52. Rusiecki JA, Baccarelli A, Bollati V, Tarantini L, Moore LE, Bonefeld-Jorgensen EC. Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic inuit. Environ Health Perspect 2008;116: 1547-1552.
53. Sajiki J, Takahashi K, Yonekubo J. Sensitive method for the determination of bisphenol-A in serum using two systems of high-performance liquid chromatography. J Chromatogr B Biomed Appl 1999;736: 255-261.
54. Sata F, Yamada H, Kondo T, Gong Y, Tozaki S, Kobashi G, Kato EH, Fujimoto S, Kishi R. Glutathione S-transferase M1 and T1 polymorphisms and the risk of recurrent pregnancy loss. Mol Hum Reprod 2003;9: 165-169. (Pubitemid 36503457)
55. Schisterman EF, Vexler A, Whitcomb BW, Liu A. The limitations due to exposure detection limits for regression models. Am J Epidemiol 2006; 163: 374-383. (Pubitemid 43238432)
56. Shan J, Yuan L, Xiao Q, Chiorazzi N, Budman D, Teichberg S, Xu HP. TSP50, a possible protease in human testes, is activated in breast cancer epithelial cells. Cancer Res 2002;62: 290-294. (Pubitemid 34074017)
57. Shkolnik K, Tadmor A, Ben-Dor S, Nevo N, Galiani D, Dekel N. Reactive oxygen species are indispensable in ovulation. Proc Natl Acad Sci USA 2011;108: 1462-1467.
58. Strange RC, Matharoo B, Faulder GC, Jones P, Cotton W, Elder JB, Deakin M. The human glutathione S-transferase: a case-control study of the incidence of the GST1 0 phenotype in patients with adenocarcinoma. Carcinogenesis 1991;12: 25-28.
59. Sugiura-Ogasawara M, Ozaki Y, Sonta SI, Makino T, Suzumori K. Exposure to bisphenol A is associated with recurrent miscarriage. Hum Reprod 2005;20: 2325-2329. (Pubitemid 41418526)
60. Susiarjo M, Hassold TJ, Freeman E, Hunt PA. Bisphenol A exposure in utero disrupts early oogenesis in the mouse. PLoS Genet 2007; 3: 0063-0070. (Pubitemid 46168833)
61. 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. (Pubitemid 38657551)
62. Thompson J, Bannigan J. Cadmium: toxic effects on the reproductive system and the embryo. Reprod Toxicol 2008;25: 304-315.
63. Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007;39: 44-84. (Pubitemid 44566469)
64. Van Poppel G, De Vogel N, Van Balderen PJ, Kok FJ. Increased cytogenetic damage in smokers deficient in glutathione S-transferase isozyme. Carcinogenesis 1992;13: 303-305.
65. Vandenberg LN, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJR, Schoenfelder G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Perspect 2010;118: 1055-1070.
66. vom Saal FS, Akingbemi BT, Belcher SM, Birnbaum LS, Crain DA, Eriksen M, Farabollini F, Guillette LJ Jr, Hauser R, Heindel JJ et al Chapel Hill bisphenol A expert panel consensus statement: integration of mechanisms, effects in animals and potential to impact human health at current levels of exposure. Reprod Toxicol 2007, 24, 131-138. (Pubitemid 47385099)
67. Weng YI, Hsu PY, Liyanarachchi S, Liu J, Deatherage DE, Huang YW, Zuo T, Rodriguez B, Lin CH, Cheng AL et al. Epigenetic influences of low-dose bisphenol A in primary human breast epithelial cells. Toxicol Appl Pharmacol 2010;248: 111-121.
68. 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. (Pubitemid 47385095)
69. Wright RO, Schwartz J, Wright RJ, Bollati V, Tarantini L, Park SK, Hu H, Sparrow D, Vokonas P, Baccarelli A. Biomarkers of lead exposure and DNA methylation within retrotransposons. Environ Health Perspect 2010;118: 790-795.
70. Wu HC, Delgado-Cruzata L, Flom JD, Kappil M, Ferris JS, Liao Y, Santella RM, Terry MB. Global methylation profles in DNA from different blood cell types. Epigenetics 2011;6: 76-85.
71. Xu SJ,Wang YP, Roe B, Pearson WR. Characterization of the human class Mu glutathione S-transferase gene cluster and the GSTM1 deletion. J Biol Chem 1998;273: 3517-3527. (Pubitemid 28109774)
72. Yaoi T, Itoh K, Nakamura K, Ogi H, Fujiwara Y, Fushiki S. Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A. Biochem Biophys Res Commun 2008;376: 563-567.
73. Younglai EV, Foster WG, Hughes EG, Trim K, Jarrell JF. Levels of environmental contaminants in human follicular fluid, serum, and seminal plasma of couples undergoing in vitro fertilization. Arch Environ Contam Toxicol 2002;43: 121-126. (Pubitemid 34666301)
74. Younglai EV, Holloway AC, Foster WG. Environmental and occupational factors affecting fertility and IVF success. Hum Reprod Update 2005; 11: 43-57. (Pubitemid 40201975)
75. Yuan L, Shan J, De Risi D, Broome J, Lovecchio J, Gal D, Vinciguerra V, Hao-Peng X. Isolation of a novel gene, TSP50, by a hypomethylated DNA fragment in human breast cancer. Cancer Res 1999;59: 3215-3221. (Pubitemid 29316025)