1932

Abstract

Improved understanding of the multilayer regulation of the human genome has led to a greater appreciation of environmental, nutritional, and epigenetic risk factors for human disease. Chromatin remodeling, histone tail modifications, and DNA methylation are dynamic epigenetic changes responsive to external stimuli. Careful interpretation can provide insights for actionable public health through collaboration between population and basic scientists and through integration of multiple data sources. We review key findings in environmental epigenetics both in human population studies and in animal models, and discuss the implications of these results for risk assessment and public health protection. To ultimately succeed in identifying epigenetic mechanisms leading to complex phenotypes and disease, researchers must integrate the various animal models, human clinical approaches, and human population approaches while paying attention to life-stage sensitivity, to generate effective prescriptions for human health evaluation and disease prevention.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-publhealth-032013-182513
2014-03-18
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/publhealth/35/1/annurev-publhealth-032013-182513.html?itemId=/content/journals/10.1146/annurev-publhealth-032013-182513&mimeType=html&fmt=ahah

Literature Cited

  1. Akalin A, Kormaksson M, Li S, Garrett-Bakelman FE, Figueroa ME. 1.  et al. 2012. MethylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biol. 13:R87 [Google Scholar]
  2. Anderson OS, Nahar MS, Faulk C, Jones TR, Liao C. 2.  et al. 2012. Epigenetic responses following maternal dietary exposure to physiologically relevant levels of bisphenol A. Environ. Mol. Mutagen. 53:334–42 [Google Scholar]
  3. Anderson OS, Peterson KE, Sanchez BN, Zhang Z, Mancuso P, Dolinoy DC. 3.  2013. Perinatal bisphenol A exposure promotes hyperactivity, lean body composition, and hormonal responses across the murine life course. FASEB J. 27:1784–92 [Google Scholar]
  4. Arita A, Niu J, Qu Q, Zhao N, Ruan Y. 4.  et al. 2012. Global levels of histone modifications in peripheral blood mononuclear cells of subjects with exposure to nickel. Environ. Health Perspect. 120:198–203 [Google Scholar]
  5. Arora M, Kennedy BJ, Elhlou S, Pearson NJ, Walker DM. 5.  et al. 2006. Spatial distribution of lead in human primary teeth as a biomarker of pre- and neonatal lead exposure. Sci. Total Environ. 371:55–62 [Google Scholar]
  6. Baccarelli A, Wright RO, Bollati V, Tarantini L, Litonjua AA. 6.  et al. 2009. Rapid DNA methylation changes after exposure to traffic particles. Am. J. Respir. Crit. Care Med. 179:572–78 [Google Scholar]
  7. Behrman RE, Butler AS. 7.  2006. Preterm Birth: Causes, Consequences, and Prevention Washington, DC: Natl. Acad.
  8. Bernal AJ, Dolinoy DC, Huang D, Skaar DA, Weinhouse C, Jirtle RL. 8.  2013. Adaptive radiation-induced epigenetic alterations mitigated by antioxidants. FASEB J. 27:665–71 [Google Scholar]
  9. Bird A. 9.  2002. DNA methylation patterns and epigenetic memory. Genes Dev. 16:6–21 [Google Scholar]
  10. Bollati V, Baccarelli A, Hou L, Bonzini M, Fustinoni S. 10.  et al. 2007. Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Res. 67:876–80 [Google Scholar]
  11. Bollati V, Baccarelli A, Sartori S, Tarantini L, Motta V. 11.  et al. 2010. Epigenetic effects of shiftwork on blood DNA methylation. Chronobiol. Int. 27:1093–104 [Google Scholar]
  12. Braun JM, Kalkbrenner AE, Calafat AM, Yolton K, Ye X. 12.  et al. 2011. Impact of early-life bisphenol A exposure on behavior and executive function in children. Pediatrics 128:873–82 [Google Scholar]
  13. Bygren LO. 13.  2013. Intergenerational health responses to adverse and enriched environments. Annu. Rev. Public Health 34:49–60 [Google Scholar]
  14. Caiafa P, Zampieri M. 14.  2005. DNA methylation and chromatin structure: the puzzling CpG islands. J. Cell Biochem. 94:257–65 [Google Scholar]
  15. Calafat A, Ye X, Wong L, Reidy J, Needham L. 15.  2008. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003–2004. Environ. Health Perspect. 116:39–44 [Google Scholar]
  16. Cantone L, Nordio F, Hou L, Apostoli P, Bonzini M. 16.  et al. 2011. Inhalable metal-rich air particles and histone H3K4 dimethylation and H3K9 acetylation in a cross-sectional study of steel workers. Environ. Health Perspect. 119:964–69 [Google Scholar]
  17. Champagne FA, Weaver IC, Diorio J, Dymov S, Szyf M, Meaney MJ. 17.  2006. Maternal care associated with methylation of the estrogen receptor-α1b promoter and estrogen receptor-α expression in the medial preoptic area of female offspring. Endocrinology 147:2909–15 [Google Scholar]
  18. Chanda S, Dasgupta UB, Guhamazumder D, Gupta M, Chaudhuri U. 18.  et al. 2006. DNA hypermethylation of promoter of gene p53 and p16 in arsenic-exposed people with and without malignancy. Toxicol. Sci. 89:431–37 [Google Scholar]
  19. Chen R, Mias GI, Li-Pook-Than J, Jiang L, Lam HY. 19.  et al. 2012. Personal omics profiling reveals dynamic molecular and medical phenotypes. Cell 148:1293–307 [Google Scholar]
  20. Cheung P, Lau P. 20.  2005. Epigenetic regulation by histone methylation and histone variants. Mol. Endocrinol. 19:563–73 [Google Scholar]
  21. Chu F, Ren X, Chasse A, Hickman T, Zhang L. 21.  et al. 2011. Quantitative mass spectrometry reveals the epigenome as a target of arsenic. Chem. Biol. Interact. 192:113–17 [Google Scholar]
  22. Colaneri A, Staffa N, Fargo DC, Gao Y, Wang T. 22.  et al. 2011. Expanded methyl-sensitive cut counting reveals hypomethylation as an epigenetic state that highlights functional sequences of the genome. Proc. Natl. Acad. Sci. USA 108:9715–20 [Google Scholar]
  23. Dolinoy DC, Faulk C. 23.  2012. The use of animal models to advance epigenetic science. ILAR J. 53:227–31 [Google Scholar]
  24. Dolinoy DC, Huang D, Jirtle RL. 24.  2007. Maternal nutrient supplementation counteracts bisphenol A–induced DNA hypomethylation in early development. Proc. Natl. Acad. Sci. USA 104:13056–61 [Google Scholar]
  25. Dolinoy DC, Weidman JR, Waterland RA, Jirtle RL. 25.  2006. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ. Health Perspect. 114:567–72 [Google Scholar]
  26. Doshi T, Mehta SS, Dighe V, Balasinor N, Vanage G. 26.  2011. Hypermethylation of estrogen receptor promoter region in adult testis of rats exposed neonatally to bisphenol A. Toxicology 289:74–82 [Google Scholar]
  27. Dunham I, Birney E, Lajoie BR, Sanyal A, Dong X. 27.  et al. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489:57–74 [Google Scholar]
  28. Faustman EM, Omenn GS. 28.  2013. Risk assessment. Casarett and Doull's Toxicology: The Basic Science of Poisons CD Klaassen 123–49 New York: McGraw-Hill, 8th ed.. [Google Scholar]
  29. Feinberg AP. 29.  2004. The epigenetics of cancer etiology. Semin. Cancer Biol. 14:427–32 [Google Scholar]
  30. Fish EW, Shahrokh D, Bagot R, Caldji C, Bredy T. 30.  et al. 2004. Epigenetic programming of stress responses through variations in maternal care. Ann. NY Acad. Sci. 1036:167–80 [Google Scholar]
  31. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F. 31.  et al. 2005. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl. Acad. Sci. USA 102:10604–9 [Google Scholar]
  32. Håberg SE, London SJ, Stigum H, Nafstad P, Nystad W. 32.  2009. Folic acid supplements in pregnancy and early childhood respiratory health. Arch. Dis. Child. 94:180–84 [Google Scholar]
  33. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ. 33.  et al. 2008. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci. USA 105:17046–49 [Google Scholar]
  34. Hertzman C. 34.  2013. Commentary on the symposium: biological embedding, life course development, and the emergence of a new science. Annu. Rev. Public Health 34:1–5 [Google Scholar]
  35. Ho SM, Tang WY, Belmonte de Frausto J, Prins GS. 35.  2006. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res. 66:5624–32 [Google Scholar]
  36. Hollingsworth JW, Maruoka S, Boon K, Garantziotis S, Li Z. 36.  et al. 2008. In utero supplementation with methyl donors enhances allergic airway disease in mice. J. Clin. Investig. 118:3462–69 [Google Scholar]
  37. Hsu PY, Deatherage DE, Rodriguez BA, Liyanarachchi S, Weng YI. 37.  et al. 2009. Xenoestrogen-induced epigenetic repression of microRNA-9-3 in breast epithelial cells. Cancer Res. 69:5936–45 [Google Scholar]
  38. Hu H, Rabinowitz M, Smith D. 38.  1998. Bone lead as a biological marker in epidemiologic studies of chronic toxicity: conceptual paradigms. Environ. Health Perspect. 106:1–8 [Google Scholar]
  39. Huertas D, Soler M, Moreto J, Villanueva A, Martinez A. 39.  et al. 2011. Antitumor activity of a small-molecule inhibitor of the histone kinase Haspin. Oncogene 31:1408–18 [Google Scholar]
  40. Javierre BM, Fernandez AF, Richter J, Al-Shahrour F, Martin-Subero JI. 40.  et al. 2010. Changes in the pattern of DNA methylation associate with twin discordance in systemic lupus erythematosus. Genome Res. 20:170–79 [Google Scholar]
  41. Jenuwein T, Allis CD. 41.  2001. Translating the histone code. Science 293:1074–80 [Google Scholar]
  42. Kantlehner M, Kirchner R, Hartmann P, Ellwart JW, Alunni-Fabbroni M, Schumacher A. 42.  2011. A high-throughput DNA methylation analysis of a single cell. Nucleic Acids Res. 39:e44 [Google Scholar]
  43. Kile ML, Baccarelli A, Hoffman E, Tarantini L, Quamruzzaman Q. 43.  et al. 2012. Prenatal arsenic exposure and DNA methylation in maternal and umbilical cord blood leukocytes. Environ. Health Perspect. 120:1061–66 [Google Scholar]
  44. Kim J, Karnovsky A, Mahavisno V, Weymouth T, Pande M. 44.  et al. 2012. LRpath analysis reveals common pathways dysregulated via DNA methylation across cancer types. BMC Genomics 13:526 [Google Scholar]
  45. Kim JH, Rozek LS, Soliman AS, Sartor MA, Hablas A. 45.  et al. 2013. Bisphenol A-associated epigenomic changes in prepubescent girls: a cross-sectional study in Gharbiah, Egypt. Environ. Health 12:33 [Google Scholar]
  46. Kouzarides T. 46.  2007. Chromatin modifications and their function. Cell 128:693–705 [Google Scholar]
  47. Lai C-J, Bao R, Tao X, Wang J, Atoyan R. 47.  et al. 2010. CUDC-101, a multitargeted inhibitor of histone deacetylase, epidermal growth factor receptor, and human epidermal growth factor receptor 2, exerts potent anticancer activity. Cancer Res. 70:3647–56 [Google Scholar]
  48. Laird PW. 48.  2010. Principles and challenges of genomewide DNA methylation analysis. Nat. Rev. Genet. 11:191–203 [Google Scholar]
  49. Lang IA, Galloway TS, Scarlett A, Henley WE, Depledge M. 49.  et al. 2008. Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA 300:1303–10 [Google Scholar]
  50. Lave LB, Omenn GS. 50.  1985. Cost-effectiveness of short-term tests for carcinogenicity. Nature 324:29–34 [Google Scholar]
  51. Lister R, Pelizzola M, Kida YS, Hawkins RD, Nery JR. 51.  et al. 2011. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471:68–73 [Google Scholar]
  52. Liu S, Im H, Bairoch A, Cristofanilli M, Chen R. 52.  et al. 2012. A chromosome-centric human proteome project (C-HPP) to characterize the sets of proteins encoded in chromosome 17. J. Proteome Res. 12:45–57 [Google Scholar]
  53. Maffini MV, Rubin BS, Sonnenschein C, Soto AM. 53.  2006. Endocrine disruptors and reproductive health: the case of bisphenol-A. Mol. Cell Endocrinol. 254–255:179–86 [Google Scholar]
  54. Marko-Varga G, Omenn GS, Paik Y-K, Hancock WS. 54.  2012. A first step toward completion of a genome-wide characterization of the human proteome. J. Proteome Res. 12:1–5 [Google Scholar]
  55. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C. 55.  et al. 2010. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466:253–57 [Google Scholar]
  56. McGuinness D, McGlynn LM, Johnson PCD, MacIntyre A, Batty DG. 56.  et al. 2012. Socio-economic status is associated with epigenetic differences in the pSoBid cohort. Int. J. Epidemiol. 41:151–60 [Google Scholar]
  57. Meeker JD, Ehrlich S, Toth TL, Wright DL, Calafat AM. 57.  et al. 2010. Semen quality and sperm DNA damage in relation to urinary bisphenol A among men from an infertility clinic. Reprod. Toxicol. 30:532–39 [Google Scholar]
  58. Meeker JD, Hu H, Cantonwine DE, Lamadrid-Figueroa H, Calafat AM. 58.  et al. 2009. Urinary phthalate metabolites in relation to preterm birth in Mexico City. Environ. Health Perspect. 117:1587–92 [Google Scholar]
  59. Nahar MS, Liao C, Kannan K, Dolinoy DC. 59.  2013. Fetal liver bisphenol A concentrations and biotransformation gene expression reveal variable exposure and altered capacity for metabolism in humans. J. Biochem. Mol. Toxicol. 27:116–23 [Google Scholar]
  60. Nahar MS, Soliman AS, Colacino JA, Calafat AM, Battige K. 60.  et al. 2012. Urinary bisphenol A concentrations in girls from rural and urban Egypt: a pilot study. Environ. Health 11:20 [Google Scholar]
  61. 61. Natl. Res. Counc 1983. Risk Assessment in the Federal Government: Managing the Process. Washington, DC: Natl. Acad.
  62. 62. Natl. Res. Counc 1989. Biological Markers in Pulmonary Toxicology. Washington, DC: Natl. Acad.
  63. 63. Natl. Res. Counc 2010. Toxicity Pathway-Based Risk Assessment: Preparing for Paradigm Change: A Symposium Summary. Washington, DC: Natl. Acad.
  64. Nie Y, Liu H, Sun X. 64.  2013. The patterns of histone modifications in the vicinity of transcription factor binding sites in human lymphoblastoid cell lines. PLoS ONE 8:e60002 [Google Scholar]
  65. Nilsson E, Larsen G, Manikkam M, Guerrero-Bosagna C, Savenkova MI, Skinner MK. 65.  2012. Environmentally induced epigenetic transgenerational inheritance of ovarian disease. PLoS ONE 7:e36129 [Google Scholar]
  66. O'Neill MS, Osornio-Vargas A, Buxton MA, Sánchez BN, Rojas-Bracho L. 66.  et al. 2012. Air pollution, inflammation and preterm birth in Mexico City: study design and methods. Sci. Total Environ. 448:79–83 [Google Scholar]
  67. O'Geen H, Echipare L, Farnham PJ. 67.  2011. Using ChIP-seq technology to generate high-resolution profiles of histone modifications. Methods in Molecular Biology 791 Epigenetics Protocols TO Tollefsbol 265–86 New York: Humana [Google Scholar]
  68. Odgers CL, Jaffee SR. 68.  2013. Routine versus catastrophic influences on the developing child. Annu. Rev. Public Health 34:29–48 [Google Scholar]
  69. Omenn GS. 69.  2012. Gene-environment interactions: eco-genetics and toxicogenomics. Genomic and Personalized Medicine GS Ginsburg, HF Willard 50–59 London: Academic, 2nd ed.. [Google Scholar]
  70. Omenn GS, Stuebbe S, Lave LB. 70.  1995. Predictions of rodent carcinogenicity testing results: interpretation in light of the Lave-Omenn value-of-information model. Mol. Carcinog. 14:37–45 [Google Scholar]
  71. Pavanello S, Bollati V, Pesatori AC, Kapka L, Bolognesi C. 71.  et al. 2009. Global and gene-specific promoter methylation changes are related to anti-B[a]PDE-DNA adduct levels and influence micronuclei levels in polycyclic aromatic hydrocarbon-exposed individuals. Int. J. Cancer 125:1692–97 [Google Scholar]
  72. Perera F, Herbstman J. 72.  2011. Prenatal environmental exposures, epigenetics, and disease. Reprod. Toxicol. 31:363–73 [Google Scholar]
  73. Perera F, Tang WY, Herbstman J, Tang D, Levin L. 73.  et al. 2009. Relation of DNA methylation of 5′-CpG island of ACSL3 to transplacental exposure to airborne polycyclic aromatic hydrocarbons and childhood asthma. PLoS ONE 4:e4488 [Google Scholar]
  74. Perera FP, Jedrychowski W, Rauh V, Whyatt RM. 74.  1999. Molecular epidemiologic research on the effects of environmental pollutants on the fetus. Environ. Health Perspect. 107:Suppl. 3451–60 [Google Scholar]
  75. Perera FP, Whyatt RM, Jedrychowski W, Rauh V, Manchester D. 75.  et al. 1998. Recent developments in molecular epidemiology: a study of the effects of environmental polycyclic aromatic hydrocarbons on birth outcomes in Poland. Am. J. Epidemiol. 147:309–14 [Google Scholar]
  76. Power C, Kuh D, Morton S. 76.  2013. From developmental origins of adult disease to life course research on adult disease and aging: insights from birth cohort studies. Annu. Rev. Public Health 34:7–28 [Google Scholar]
  77. 77. Pres./Congr. Comm. Risk Assess. Risk Manag 1997. Risk Assessment and Risk Management in Regulatory Decision-Making. Washington, DC: US Gov. Print. Off.
  78. Reichard JF, Puga A. 78.  2010. Effects of arsenic exposure on DNA methylation and epigenetic gene regulation. Epigenomics 2:87–104 [Google Scholar]
  79. Rudiger HW, Nowak D, Hartmann K, Cerutti P. 79.  1985. Enhanced formation of benzo(a)pyrene:DNA adducts in monocytes of patients with a presumed predisposition to lung cancer. Cancer Res. 45:5890–94 [Google Scholar]
  80. Rusiecki JA, Baccarelli A, Bollati V, Tarantini L, Moore LE, Bonefeld-Jorgensen EC. 80.  2008. Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic Inuit. Environ. Health Perspect. 116:1547–52 [Google Scholar]
  81. Saha A, Wittmeyer J, Cairns BR. 81.  2006. Chromatin remodelling: the industrial revolution of DNA around histones. Nat. Rev. Mol. Cell Biol. 7:437–47 [Google Scholar]
  82. Sartor MA, Dolinoy DC, Rozek LS, Omenn GS. 82.  2012. Bioinformatics for high-throughput toxicoepigenomic studies. Toxicology and Epigenetics SC Sahu 569–88 New York: Wiley [Google Scholar]
  83. Sartor MA, Leikauf GD, Medvedovic M. 83.  2009. LRpath: a logistic regression approach for identifying enriched biological groups in gene expression data. Bioinformatics 25:211–17 [Google Scholar]
  84. Sartor MA, Mahavisno V, Keshamouni VG, Cavalcoli J, Wright Z. 84.  et al. 2010. ConceptGen: a gene set enrichment and gene set relation mapping tool. Bioinformatics 26:456–63 [Google Scholar]
  85. Schaub MA, Boyle AP, Kundaje A, Batzoglou S, Snyder M. 85.  2012. Linking disease associations with regulatory information in the human genome. Genome Res. 22:1748–59 [Google Scholar]
  86. Skinner MK, Manikkam M, Guerrero-Bosagna C. 86.  2011. Epigenetic transgenerational actions of endocrine disruptors. Reprod. Toxicol. 31:337–43 [Google Scholar]
  87. Sugiura-Ogasawara M, Ozaki Y, Sonta S, Makino T, Suzumori K. 87.  2005. Exposure to bisphenol A is associated with recurrent miscarriage. Hum. Reprod. 20:2325–29 [Google Scholar]
  88. Susiarjo M, Sasson I, Mesaros C, Bartolomei MS. 88.  2013. Bisphenol A exposure disrupts genomic imprinting in the mouse. PLoS Genet. 9:e1003401 [Google Scholar]
  89. Taher L, Ovcharenko I. 89.  2009. Variable locus length in the human genome leads to ascertainment bias in functional inference for non-coding elements. Bioinformatics 25:578–84 [Google Scholar]
  90. Tang F, Barbacioru C, Wang Y, Nordman E, Lee C. 90.  et al. 2009. mRNA-Seq whole-transcriptome analysis of a single cell. Nat. Methods 6:377–82 [Google Scholar]
  91. Tang WY, Morey LM, Cheung YY, Birch L, Prins GS, Ho SM. 91.  2012. Neonatal exposure to estradiol/bisphenol A alters promoter methylation and expression of Nsbp1 and Hpcal1 genes and transcriptional programs of Dnmt3a/b and Mbd2/4 in the rat prostate gland throughout life. Endocrinology 153:42–55 [Google Scholar]
  92. Terry MB, Ferris JS, Pilsner R, Flom JD, Tehranifar P. 92.  et al. 2008. Genomic DNA methylation among women in a multiethnic New York City birth cohort. Cancer Epidemiol. Biomark. Prev. 17:2306–10 [Google Scholar]
  93. Tetz LM, Cheng A, Korte C, Giese R, Wang P. 93.  et al. 2013. Mono-2-ethylhexyl phthalate induces oxidative stress responses in human placental cells in vitro. Toxicol. Appl. Pharmacol. 268:47–54 [Google Scholar]
  94. Trasande L, Attina TM, Blustein J. 94.  2012. Association between urinary bisphenol A concentration and obesity prevalence in children and adolescents. JAMA 308:1113–21 [Google Scholar]
  95. Tremolizzo L, Doueiri M-S, Dong E, Grayson DR, Davis J. 95.  et al. 2005. Valproate corrects the schizophrenia-like epigenetic behavioral modifications induced by methionine in mice. Biol. Psychiatry 57:500–9 [Google Scholar]
  96. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ. 96.  2006. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci. 9:519–25 [Google Scholar]
  97. Tsankova NM, Kumar A, Nestler EJ. 97.  2004. Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. J. Neurosci. 24:5603–10 [Google Scholar]
  98. Vandenberg LN, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, Schoenfelder G. 98.  2010. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ. Health Perspect. 118:1055–70 [Google Scholar]
  99. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr. 99.  et al. 2012. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr. Rev. 33:378–455 [Google Scholar]
  100. Virani S, Colacino JA, Kim JH, Rozek LS. 100.  2012. Cancer epigenetics: a brief review. ILAR J. 53:359–69 [Google Scholar]
  101. Weng YI, Hsu PY, Liyanarachchi S, Liu J, Deatherage DE. 101.  et al. 2010. Epigenetic influences of low-dose bisphenol A in primary human breast epithelial cells. Toxicol. Appl. Pharmacol. 248:111–21 [Google Scholar]
  102. Wiencke J, Zheng S, Morrison Z, Yeh R. 102.  2007. Differentially expressed genes are marked by histone 3 lysine 9 trimethylation in human cancer cells. Oncogene 27:2412–21 [Google Scholar]
  103. Wright RO, Schwartz J, Wright RJ, Bollati V, Tarantini L. 103.  et al. 2010. Biomarkers of lead exposure and DNA methylation within retrotransposons. Environ. Health Perspect. 118:790–95 [Google Scholar]
  104. Wu G, Yi N, Absher D, Zhi D. 104.  2011. Statistical quantification of methylation levels by next-generation sequencing. PLoS ONE 6:e21034 [Google Scholar]
  105. Yacqub-Usman K, Duong CV, Clayton RN, Farrell WE. 105.  2012. Epigenomic silencing of the BMP-4 gene in pituitary adenomas: a potential target for epidrug-induced re-expression. Endocrinology 153:3603–12 [Google Scholar]
  106. Yaoi T, Itoh K, Nakamura K, Ogi H, Fujiwara Y, Fushiki S. 106.  2008. Genome-wide analysis of epigenomic alterations in fetal mouse forebrain after exposure to low doses of bisphenol A. Biochem. Biophys. Res. Commun. 376:563–67 [Google Scholar]
  107. Yavartanoo M, Choi JK. 107.  2013. ENCODE: a sourcebook of epigenomes and chromatin language. Genomics Inform. 11:2–6 [Google Scholar]
  108. Young MD, Wakefield MJ, Smyth GK, Oshlack A. 108.  2010. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 11:R14 [Google Scholar]
  109. Zang C, Schones DE, Zeng C, Cui K, Zhao K, Peng W. 109.  2009. A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25:1952–58 [Google Scholar]
  110. Zhang Z, Alomirah H, Cho HS, Li YF, Liao C. 110.  et al. 2011. Urinary bisphenol A concentrations and their implications for human exposure in several Asian countries. Environ. Sci. Technol. 45:7044–50 [Google Scholar]
/content/journals/10.1146/annurev-publhealth-032013-182513
Loading
/content/journals/10.1146/annurev-publhealth-032013-182513
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error