Deleterious effects of endocrine disruptors are corrected in the mammalian germline by epigenome reprogramming

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Iqbal, Khursheed ^a   Tran, Diana A ^a,b   Li, Arthur X ^a   Warden, Charles ^a   Bai, Angela Y ^a,c   Singh, Purnima ^a   Wu, Xiwei ^a   Pfeifer, Gerd P ^a,d   Szabó, Piroska E ^a,d  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b Irell and Manella Graduate School of Biological Sciences   (United States)

^c City of Hope   (United States)

^d VAN ANDEL RESEARCH INSTITUTE   (United States)

Author keywords

Bisphenol A; DEHP; DNA methylation; Endocrine disruptor; Fetal germ cell; Genomic imprinting; Germline epigenetic reprogramming; Transgenerational epigenetic inheritance; Vinclozolin

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ENDOCRINE DISRUPTOR; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; VINCLOZOLIN; BENZHYDRYL DERIVATIVE; OXAZOLE DERIVATIVE; PHENOL DERIVATIVE;

ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA FLANKING REGION; DNA ISOLATION; DNA METHYLATION; EMBRYO; ENVIRONMENTAL EXPOSURE; EPIGENETICS; EPIGENOME REPROGRAMMING; FEMALE; FETUS; GAMETE; GENOME IMPRINTING; GERM CELL; GERMLINE MUTATION; INHERITANCE; MALE; MAMMALIAN GENETICS; MASS SPECTROMETRY; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; OOCYTE; PROGENY; PROMOTER REGION; PROSPERMATOGONIA; REPRODUCTIVE TOXICITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; SPERMATOGONIUM; ANIMAL; DRUG EFFECTS; GENETIC EPIGENESIS; GENETICS; PREGNANCY; REPRODUCTION; SPERMATOZOON;

MAMMALIA; MUS;

ANIMALS; BENZHYDRYL COMPOUNDS; CELLULAR REPROGRAMMING; DNA METHYLATION; ENDOCRINE DISRUPTORS; EPIGENESIS, GENETIC; FEMALE; GENOMIC IMPRINTING; GERM CELLS; MALE; MICE; OXAZOLES; PHENOLS; PREGNANCY; REPRODUCTION; SPERMATOZOA;

EID: 84935874380     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0619-z     Document Type: Article

References (63)

1. Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect. 2008;116:39-44.
2. Mendiola J, Meeker JD, Jorgensen N, Andersson AM, Liu F, Calafat AM, et al. Urinary concentrations of di(2-ethylhexyl) phthalate metabolites and serum reproductive hormones: pooled analysis of fertile and infertile men. J Androl. 2012;33:488-98.
3. Sathyanarayana S, Calafat AM, Liu F, Swan SH. Maternal and infant urinary phthalate metabolite concentrations: are they related? Environ Res. 2008;108:413-8.
4. 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;118:1055-70.
5. Wickerham EL, Lozoff B, Shao J, Kaciroti N, Xia Y, Meeker JD. Reduced birth weight in relation to pesticide mixtures detected in cord blood of full-term infants. Environ Int. 2012;47:80-5.
6. Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science. 2005;308:1466-9.
7. Swan SH, Main KM, Liu F, Stewart SL, Kruse RL, Calafat AM, et al. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect. 2005;113:1056-61.
8. Vom Saal FS, Cooke PS, Buchanan DL, Palanza P, Thayer KA, Nagel SC, et al. A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicol Ind Health. 1998;14:239-60.
9. Agarwal DK, Eustis S, Lamb JCT, Reel JR, Kluwe WM. Effects of di(2-ethylhexyl) phthalate on the gonadal pathophysiology, sperm morphology, and reproductive performance of male rats. Environ Health Perspect. 1986;65:343-50.
10. Anway MD, Memon MA, Uzumcu M, Skinner MK. Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis. J Androl. 2006;27:868-79.
11. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet. 2007;8:253-62.
12. Anway MD, Rekow SS, Skinner MK. Transgenerational epigenetic programming of the embryonic testis transcriptome. Genomics. 2008;91:30-40.
13. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner MK. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLoS One. 2013;8:e55387.
14. Skinner MK, Mohan M, Haque MM, Zhang B, Savenkova MI. Epigenetic transgenerational inheritance of somatic transcriptomes and epigenetic control regions. Genome Biol. 2012;13:R91.
15. Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet. 2008;9:129-40.
16. Guibert S, Forne T, Weber M. Global profiling of DNA methylation erasure in mouse primordial germ cells. Genome Res. 2012;22:633-41.
17. Kobayashi H, Sakurai T, Miura F, Imai M, Mochiduki K, Yanagisawa E, et al. High-resolution DNA methylome analysis of primordial germ cells identifies gender-specific reprogramming in mice. Genome Res. 2013;23:616-27.
18. Seisenberger S, Andrews S, Krueger F, Arand J, Walter J, Santos F, et al. The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell. 2012;48:849-62.
19. Singh P, Li AX, Tran DA, Oates N, Kang ER, Wu X, et al. De novo DNA methylation in the male germ line occurs by default but is excluded at sites of H3K4 methylation. Cell Rep. 2013;4:205-19.
20. Kobayashi H, Sakurai T, Imai M, Takahashi N, Fukuda A, Yayoi O, et al. Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet. 2012;8:e1002440.
21. Smallwood SA, Tomizawa S, Krueger F, Ruf N, Carli N, Segonds-Pichon A, et al. Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet. 2011;43:811-4.
22. Jirtle RL, Sander M, Barrett JC. Genomic imprinting and environmental disease susceptibility. Environ Health Perspect. 2000;108:271-8.
23. Lim AL, Ferguson-Smith AC. Genomic imprinting effects in a compromised in utero environment: implications for a healthy pregnancy. Semin Cell Dev Biol. 2010;21:201-8.
24. Grossniklaus U, Kelly B, Ferguson-Smith AC, Pembrey M, Lindquist S. Transgenerational epigenetic inheritance: how important is it? Nat Rev Genet. 2013;14:228-35.
25. Ferguson-Smith AC. Genomic imprinting: the emergence of an epigenetic paradigm. Nat Rev Genet. 2011;12:565-75.
26. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, et al. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev. 2002;117:15-23.
27. Yamazaki Y, Low EW, Marikawa Y, Iwahashi K, Bartolomei MS, McCarrey JR, et al. Adult mice cloned from migrating primordial germ cells. Proc Natl Acad Sci U S A. 2005;102:11361-6.
28. Szabó PE, Hubner K, Scholer H, Mann JR. Allele-specific expression of imprinted genes in mouse migratory primordial germ cells. Mech Dev. 2002;115:157-60.
29. Szabó PE, Mann JR. Biallelic expression of imprinted genes in the mouse germ line: implications for erasure, establishment, and mechanisms of genomic imprinting. Genes Dev. 1995;9:1857-68.
30. Kato Y, Kaneda M, Hata K, Kumaki K, Hisano M, Kohara Y, et al. Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum Mol Genet. 2007;16:2272-80.
31. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, Regev A, et al. A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature. 2012;484:339-44.
32. Kang ER, Iqbal K, Tran DA, Rivas GE, Singh P, Pfeifer GP, et al. Effects of endocrine disruptors on imprinted gene expression in the mouse embryo. Epigenetics. 2011;6:7.
33. Zhang XF, Zhang LJ, Feng YN, Chen B, Feng YM, Liang GJ, et al. Bisphenol A exposure modifies DNA methylation of imprint genes in mouse fetal germ cells. Mol Biol Rep. 2012;39:8621-8.
34. Stouder C, Paoloni-Giacobino A. Transgenerational effects of the endocrine disruptor vinclozolin on the methylation pattern of imprinted genes in the mouse sperm. Reproduction. 2010;139:373-9.
35. Stouder C, Paoloni-Giacobino A. Specific transgenerational imprinting effects of the endocrine disruptor methoxychlor on male gametes. Reproduction. 2011;141:207-16.
36. Chao HH, Zhang XF, Chen B, Pan B, Zhang LJ, Li L, et al. Bisphenol A exposure modifies methylation of imprinted genes in mouse oocytes via the estrogen receptor signaling pathway. Histochem Cell Biol. 2012;137:249-59.
37. Susiarjo M, Sasson I, Mesaros C, Bartolomei MS. Bisphenol a exposure disrupts genomic imprinting in the mouse. PLoS Genet. 2013;9:e1003401.
38. Marques CJ, Carvalho F, Sousa M, Barros A. Genomic imprinting in disruptive spermatogenesis. Lancet. 2004;363:1700-2.
39. Marques CJ, Francisco T, Sousa S, Carvalho F, Barros A, Sousa M. Methylation defects of imprinted genes in human testicular spermatozoa. Fertil Steril. 2010;94:585-94.
40. Rauch TA, Pfeifer GP. The MIRA method for DNA methylation analysis. Methods Mol Biol. 2009;507:65-75.
41. Lee DH, Tran DA, Singh P, Oates N, Rivas GE, Larson GP, et al. MIRA-SNuPE, a quantitative, multiplex method for measuring allele-specific DNA methylation. Epigenetics. 2011;6:212-23.
42. Singh P, Wu X, Lee DH, Li AX, Rauch TA, Pfeifer GP, et al. Chromosome-wide analysis of parental allele-specific chromatin and DNA methylation. Mol Cell Biol. 2011;31:1757-70.
43. Guerrero-Bosagna C, Covert TR, Haque MM, Settles M, Nilsson EE, Anway MD, et al. Epigenetic transgenerational inheritance of vinclozolin induced mouse adult onset disease and associated sperm epigenome biomarkers. Reprod Toxicol. 2012;34:694-707.
44. Tickner JA, Schettler T, Guidotti T, McCally M, Rossi M. Health risks posed by use of Di-2-ethylhexyl phthalate (DEHP) in PVC medical devices: a critical review. Am J Ind Med. 2001;39:100-11.
45. Kimble J, Hirsh D. The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev Biol. 1979;70:396-417.
46. Kelly WG. Transgenerational epigenetics in the germline cycle of Caenorhabditis elegans. Epigenetics Chromatin. 2014;7:6.
47. Greer EL, Maures TJ, Ucar D, Hauswirth AG, Mancini E, Lim JP, et al. Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature. 2011;479:365-71.
48. Moore RW, Rudy TA, Lin TM, Ko K, Peterson RE. Abnormalities of sexual development in male rats with in utero and lactational exposure to the antiandrogenic plasticizer Di(2-ethylhexyl) phthalate. Environ Health Perspect. 2001;109:229-37.
49. Timms BG, Howdeshell KL, Barton L, Bradley S, Richter CA, Vom Saal FS. Estrogenic chemicals in plastic and oral contraceptives disrupt development of the fetal mouse prostate and urethra. Proc Natl Acad Sci U S A. 2005;102:7014-9.
50. Buckley J, Willingham E, Agras K, Baskin LS. Embryonic exposure to the fungicide vinclozolin causes virilization of females and alteration of progesterone receptor expression in vivo: an experimental study in mice. Environ Health. 2006;5:4.
51. Vilela ML, Willingham E, Buckley J, Liu BC, Agras K, Shiroyanagi Y, et al. Endocrine disruptors and hypospadias: role of genistein and the fungicide vinclozolin. Urology. 2007;70:618-21.
52. Elzeinova F, Novakova V, Buckiova D, Kubatova A, Peknicova J. Effect of low dose of vinclozolin on reproductive tract development and sperm parameters in CD1 outbred mice. Reprod Toxicol. 2008;26:231-8.
53. Lamb JC, Chapin RE, Teague J, Lawton AD, Reel JR. Reproductive effects of four phthalic acid esters in the mouse. Toxicol Appl Pharmacol. 1987;88:255-69.
54. Hayashi Y, Ito Y, Yanagiba Y, Kamijima M, Naito H, Nakajima T. Differences in metabolite burden of di(2-ethylhexyl)phthalate in pregnant and postpartum dams and their offspring in relation to drug-metabolizing enzymes in mice. Arch Toxicol. 2012;86:563-9.
55. Kawamoto Y, Matsuyama W, Wada M, Hishikawa J, Chan MP, Nakayama A, et al. Development of a physiologically based pharmacokinetic model for bisphenol A in pregnant mice. Toxicol Appl Pharmacol. 2007;224:182-91.
56. Susiarjo M, Hassold TJ, Freeman E, Hunt PA. Bisphenol A exposure in utero disrupts early oogenesis in the mouse. PLoS Genet. 2007;3:e5.
57. Lawson C, Gieske M, Murdoch B, Ye P, Li Y, Hassold T, et al. Gene expression in the fetal mouse ovary is altered by exposure to low doses of bisphenol A. Biol Reprod. 2011;84:79-86.
58. Lee DH, Singh P, Tsai SY, Oates N, Spalla A, Spalla C, et al. CTCF-dependent chromatin bias constitutes transient epigenetic memory of the mother at the H19-Igf2 imprinting control region in prospermatogonia. PLoS Genet. 2010;6:e1001224.
59. Rauch TA, Pfeifer GP. DNA methylation profiling using the methylated-CpG island recovery assay (MIRA). Methods. 2010;52:213-7.
60. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4:249-64.
61. Szabó PE, Tang SH, Reed MR, Silva FJ, Tsark WM, Mann JR. The chicken beta-globin insulator element conveys chromatin boundary activity but not imprinting at the mouse Igf2/H19 domain. Development. 2002;129:897-904.
62. Singh P, Cho J, Tsai SY, Rivas GE, Larson GP, Szabó PE. Coordinated allele-specific histone acetylation at the differentially methylated regions of imprinted genes. Nucleic Acids Res. 2010;38:7974-90.
63. Singh P, Han L, Rivas GE, Lee DH, Nicholson TB, Larson GP, et al. Allele-specific H3K79 Di- versus trimethylation distinguishes opposite parental alleles at imprinted regions. Mol Cell Biol. 2010;30:2693-707.