Endocrine disruptor induction of epigenetic transgenerational inheritance of disease

Molecular and Cellular Endocrinology

Volumn 398, Issue 1-2, 2014, Pages 4-12

  Skinner, Michael K ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

DNA methylation; Environment; Epimutations; Evolutionary biology; Review; Toxicants

Indexed keywords

ENDOCRINE DISRUPTOR;

ADVERSE EFFECTS; ANIMAL; DISEASE MODEL; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; GENETIC EPIGENESIS; GENETIC PREDISPOSITION; GENOTYPE ENVIRONMENT INTERACTION; HUMAN;

ANIMALS; DISEASE MODELS, ANIMAL; DNA METHYLATION; ENDOCRINE DISRUPTORS; ENVIRONMENTAL EXPOSURE; EPIGENESIS, GENETIC; GENE-ENVIRONMENT INTERACTION; GENETIC PREDISPOSITION TO DISEASE; HUMANS;

EID: 84914121565     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2014.07.019     Document Type: Review

References (98)

1. Albert O., Jegou B. A critical assessment of the endocrine susceptibility of the human testis to phthalates from fetal life to adulthood. Hum. Reprod. Update 2014, 20:231-249.
2. Anway M.D., Skinner M.K. Transgenerational effects of the endocrine disruptor vinclozolin on the prostate transcriptome and adult onset disease. Prostate 2008, 68:517-529.
3. Anway M.D., Cupp A.S., Uzumcu M., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308:1466-1469.
4. Anway M.D., Leathers C., Skinner M.K. Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 2006, 147:5515-5523.
5. Anway M.D., Memon M.A., Uzumcu M., Skinner M.K. Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis. J. Androl 2006, 27:868-879.
6. Baker T.R., Peterson R.E., Heideman W. Using zebrafish as a model system for studying the transgenerational effects of dioxin. Toxicol. Sci 2014, 138:403-411.
7. Barker D.J. The developmental origins of adult disease. J. Am. Coll. Nutr 2004, 23:588S-595S.
8. Barthelmess E.K., Naz R.K. Polycystic ovary syndrome: current status and future perspective. Front. Biosci. (Elite Ed) 2014, 6:104-119.
9. Benayoun B.A., Brunet A. Epigenetic memory of longevity in Caenorhabditis elegans. Worm 2012, 1:77-81.
10. Bergman A., Heindel J.J., Kasten T., Kidd K.A., Jobling S., Neira M., et al. The impact of endocrine disruption: a consensus statement on the state of the science. Environ. Health Perspect 2013, 121:A104-A106.
11. Bernal A.J., Jirtle R.L. Epigenomic disruption: the effects of early developmental exposures. Birth Defects Res. A. Clin Mol. Teratol 2010, 88:938-944.
12. Blewitt M., Whitelaw E. The use of mouse models to study epigenetics. Cold Spring Harb. Perspect. Biol 2013, 5:a017939.
13. Braunschweig M., Jagannathan V., Gutzwiller A., Bee G. Investigations on transgenerational epigenetic response down the male line in F2 pigs. PLoS ONE 2012, 7:e30583.
14. Brevik A., Lindeman B., Brunborg G., Duale N. Paternal benzo[a]pyrene exposure modulates microrna expression patterns in the developing mouse embryo. Int. J. Cell. Biol 2012, 2012:407431.
15. Bromer J.G., Wu J., Zhou Y., Taylor H.S. Hypermethylation of homeobox A10 by in utero diethylstilbestrol exposure: an epigenetic mechanism for altered developmental programming. Endocrinology 2009, 150:3376-3382.
16. Bruner-Tran K.L., Osteen K.G. Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations. Reprod. Toxicol 2011, 31:344-350.
17. Buescher J.L., Musselman L.P., Wilson C.A., Lang T., Keleher M., Baranski T.J., et al. Evidence for transgenerational metabolic programming in Drosophila. Dis. Model. Mech 2013, 6:1123-1132.
18. Burdge G.C., Slater-Jefferies J., Torrens C., Phillips E.S., Hanson M.A., Lillycrop K.A. Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br. J. Nutr 2007, 97:435-439.
19. Burdge G.C., Hoile S.P., Uller T., Thomas N.A., Gluckman P.D., Hanson M.A., et al. Progressive, transgenerational changes in offspring phenotype and epigenotype following nutritional transition. PLoS ONE 2011, 6:e28282.
20. Chamorro-Garcia R., Sahu M., Abbey R.J., Laude J., Pham N., Blumberg B. Transgenerational inheritance of increased fat depot size, stem cell reprogramming, and hepatic steatosis elicited by prenatal exposure to the obesogen tributyltin in mice. Environ. Health Perspect 2013, 121:359-366.
21. Crews D., Gore A.C., Hsu T.S., Dangleben N.L., Spinetta M., Schallert T., et al. Transgenerational epigenetic imprints on mate preference. Proc. Natl Acad. Sci. USA 2007, 104:5942-5946.
22. Crews D., Gillette R., Scarpino S.V., Manikkam M., Savenkova M.I., Skinner M.K. Epigenetic transgenerational inheritance of altered stress responses. Proc. Natl Acad. Sci. USA 2012, 109:9143-9148.
23. Darwin C. The Descent of Man, and Selection in Relation to Sex 1871, T. Murray, London.
24. Daxinger L., Whitelaw E. Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat. Rev. Genet 2012, 13:153-162.
25. Day T., Bonduriansky R. A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am. Nat 2011, 178:E18-E36.
26. Dias B.G., Ressler K.J. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat. Neurosci 2014, 17:89-96.
27. Doyle T.J., Bowman J.L., Windell V.L., McLean D.J., Kim K.H. Transgenerational effects of di-(2-ethylhexyl) phthalate on testicular germ cell associations and spermatogonial stem cells in mice. Biol. Reprod 2013, 88:112.
28. Dunn G.A., Morgan C.P., Bale T.L. Sex-specificity in transgenerational epigenetic programming. Horm. Behav 2011, 59:290-295.
29. Feng S., Jacobsen S.E., Reik W. Epigenetic reprogramming in plant and animal development. Science 2010, 330:622-627.
30. Fowler P.A., Bellingham M., Sinclair K.D., Evans N.P., Pocar P., Fischer B., et al. Impact of endocrine-disrupting compounds (EDCs) on female reproductive health. Mol. Cell. Endocrinol 2012, 355:231-239.
31. Gapp K., Jawaid A., Sarkies P., Bohacek J., Pelczar P., Prados J., et al. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat. Neurosci 2014, 17:667-669.
32. Geoghegan J.L., Spencer H.G. Exploring epiallele stability in a population-epigenetic model. Theor. Popul. Biol 2013, 83:136-144.
33. Govorko D., Bekdash R.A., Zhang C., Sarkar D.K. Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations. Biol. Psychiatry 2012, 72:378-388.
34. Grentzinger T., Armenise C., Brun C., Mugat B., Serrano V., Pelisson A., et al. piRNA-mediated transgenerational inheritance of an acquired trait. Genome Res 2012, 22:1877-1888.
35. Guerrero-Bosagna C., Sabat P., Valladares L. Environmental signaling and evolutionary change: can exposure of pregnant mammals to environmental estrogens lead to epigenetically induced evolutionary changes in embryos?. Evol. Dev 2005, 7:341-350.
36. Guerrero-Bosagna C., Settles M., Lucker B., Skinner M. Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS ONE 2010, 5:e13100.
37. Guerrero-Bosagna C., Covert T., Haque M.M., Settles M., Nilsson E.E., Anway M.D., et al. Epigenetic transgenerational inheritance of vinclozolin induced mouse adult onset disease and associated sperm epigenome biomarkers. Reprod. Toxicol 2012, 34:694-707.
38. Guerrero-Bosagna C., Savenkova M., Haque M.M., Sadler-Riggleman I., Skinner M.K. Environmentally induced epigenetic transgenerational inheritance of altered sertoli cell transcriptome and epigenome: molecular etiology of male infertility. PLoS ONE 2013, 8:e59922.
39. Hauser M.T., Aufsatz W., Jonak C., Luschnig C. Transgenerational epigenetic inheritance in plants. Biochim. Biophys. Acta 2011, 1809:459-468.
40. Henckel A., Chebli K., Kota S.K., Arnaud P., Feil R. Transcription and histone methylation changes correlate with imprint acquisition in male germ cells. EMBO J. 2012, 31:606-615.
41. Holliday R., Pugh J.E. DNA modification mechanisms and gene activity during development. Science 1975, 187:226-232.
42. Jang Y.J., Park H.R., Kim T.H., Yang W.J., Lee J.J., Choi S.Y., et al. High dose bisphenol A impairs hippocampal neurogenesis in female mice across generations. Toxicology 2012, 296:73-82.
43. Jefferson W.N., Padilla-Banks E., Newbold R.R. Disruption of the female reproductive system by the phytoestrogen genistein. Reprod. Toxicol 2007, 23:308-316.
44. Jirtle R.L., Skinner M.K. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet 2007, 8:253-262.
45. Jurisicova A., Taniuchi A., Li H., Shang Y., Antenos M., Detmar J., et al. Maternal exposure to polycyclic aromatic hydrocarbons diminishes murine ovarian reserve via induction of Harakiri. J. Clin. Invest 2007, 117:3971-3978.
46. Kalfa N., Paris F., Soyer-Gobillard M.O., Daures J.P., Sultan C. Prevalence of hypospadias in grandsons of women exposed to diethylstilbestrol during pregnancy: a multigenerational national cohort study. Fertil. Steril 2011, 95:2574-2577.
47. Kelly W.G. Transgenerational epigenetics in the germline cycle of Caenorhabditis elegans. Epigenetics Chromatin 2014, 7:6.
48. Klironomos F.D., Berg J., Collins S. How epigenetic mutations can affect genetic evolution: model and mechanism. Bioessays 2013, 35:571-578.
49. Kornfeld J.W., Bruning J.C. Regulation of metabolism by long, non-coding RNAs. Front Genet 2014, 5:57.
50. Lamarck J. Recherches Sur L'organisation des Corps Vivans 1802, Chez L'auteur, Maillard, Paris.
51. Lee J.T., Bartolomei M.S. X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell 2013, 152:1308-1323.
52. Manikkam M., Guerrero-Bosagna C., Tracey R., Haque M.M., Skinner M.K. Transgenerational actions of environmental compounds on reproductive disease and epigenetic biomarkers of ancestral exposures. PLoS ONE 2012, 7:e31901.
53. Manikkam M., Tracey R., Guerrero-Bosagna C., Skinner M. Pesticide and insect repellent mixture (permethrin and DEET) induces epigenetic transgenerational inheritance of disease and sperm epimutations. Reprod. Toxicol 2012, 34:708-719.
54. Manikkam M., Tracey R., Guerrero-Bosagna C., Skinner M.K. Dioxin (TCDD) induces epigenetic transgenerational inheritance of adult onset disease and sperm epimutations. PLoS ONE 2012, 7:e46249.
55. Manikkam M., Tracey R., Guerrero-Bosagna C., Skinner M. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of adult-onset disease and sperm epimutations. PLoS ONE 2013, 8:e55387.
56. Manikkam M., Haque M.M., Guerrero-Bosagna C., Nilsson E., Skinner M. Pesticide methoxychlor promotes the epigenetic transgenerational inheritance of adult onset disease through the female germline. PLoS ONE 2014, 9:e102091.
57. Matthews S.G., Phillips D.I. Transgenerational inheritance of stress pathology. Exp. Neurol 2012, 233:95-101.
58. McCarrey J.R. The epigenome as a target for heritable environmental disruptions of cellular function. Mol. Cell. Endocrinol 2012, 354:9-15.
59. Messerschmidt D.M., Knowles B.B., Solter D. DNA methylation dynamics during epigenetic reprogramming in the germline and preimplantation embryos. Genes Dev 2014, 28:812-828.
60. Newbold R.R. Lessons learned from perinatal exposure to diethylstilbestrol. Toxicol. Appl. Pharmacol 2004, 199:142-150.
61. Nilsson E.E., Anway M.D., Stanfield J., Skinner M.K. Transgenerational epigenetic effects of the endocrine disruptor vinclozolin on pregnancies and female adult onset disease. Reproduction 2008, 135:713-721.
62. Nilsson E., Larsen G., Manikkam M., Guerrero-Bosagna C., Savenkova M., Skinner M. Environmentally induced epigenetic transgenerational inheritance of ovarian disease. PLoS ONE 2012, 7:e36129.
63. Norouzitallab P., Baruah K., Vandegehuchte M., Van Stappen G., Catania F., Vanden Bussche J., et al. Environmental heat stress induces epigenetic transgenerational inheritance of robustness in parthenogenetic Artemia model. FASEB J. 2014, Epub ahead of print.
64. Padmanabhan N., Watson E.D. Lessons from the one-carbon metabolism: passing it along to the next generation. Reprod. Biomed. Online 2013, 27:637-643.
65. Painter R.C., Osmond C., Gluckman P., Hanson M., Phillips D.I., Roseboom T.J. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 2008, 115:1243-1249.
66. Paoloni-Giacobino A. Epigenetic effects of methoxychlor and vinclozolin on male gametes. Vitam. Horm 2014, 94:211-227.
67. Pembrey M.E. Male-line transgenerational responses in humans. Hum. Fertil. (Camb.) 2010, 13:268-271.
68. Pembrey M.E., Bygren L.O., Kaati G., Edvinsson S., Northstone K., Sjostrom M., et al. Sex-specific, male-line transgenerational responses in humans. Eur. J. Hum. Genet 2006, 14:159-166.
69. Pistek V.L., Furst R.W., Kliem H., Bauersachs S., Meyer H.H., Ulbrich S.E. HOXA10 mRNA expression and promoter DNA methylation in female pig offspring after in utero estradiol-17beta exposure. J. Steroid Biochem. Mol. Biol 2013, 138:435-444.
70. Rehan V.K., Liu J., Sakurai R., Torday J.S. Perinatal nicotine-induced transgenerational asthma. Am. J. Physiol. Lung Cell. Mol. Physiol 2013, 305:L501-L507.
71. Salian S., Doshi T., Vanage G. Impairment in protein expression profile of testicular steroid receptor coregulators in male rat offspring perinatally exposed to Bisphenol A. Life Sci 2009, 85:11-18.
72. Schmidt C.W. Uncertain inheritance transgenerational effects of environmental exposures. Environ. Health Perspect 2013, 121:A298-A303.
73. Schmitz R.J., Schultz M.D., Urich M.A., Nery J.R., Pelizzola M., Libiger O., et al. Patterns of population epigenomic diversity. Nature 2013, 495:193-198.
74. Seisenberger S., Peat J.R., Reik W. Conceptual links between DNA methylation reprogramming in the early embryo and primordial germ cells. Curr. Opin. Cell Biol 2013, 25:281-288.
75. Singer J., Roberts-Ems J., Riggs A.D. Methylation of mouse liver DNA studied by means of the restriction enzymes msp I and hpa II. Science 1979, 203:1019-1021.
76. Skinner M.K. What is an epigenetic transgenerational phenotype? F3 or F2. Reprod. Toxicol 2008, 25:2-6.
77. Skinner M.K. Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability. Epigenetics 2011, 6:838-842.
78. Skinner M.K., Anway M.D., Savenkova M.I., Gore A.C., Crews D. Transgenerational epigenetic programming of the brain transcriptome and anxiety behavior. PLoS ONE 2008, 3:e3745.
79. Skinner M.K., Manikkam M., Guerrero-Bosagna C. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol. Metab 2010, 21:214-222.
80. Skinner M.K., Manikkam M., Guerrero-Bosagna C. Epigenetic transgenerational actions of endocrine disruptors. Reprod. Toxicol 2011, 31:337-343.
81. Skinner M.K., Manikkam M., Haque M.M., Zhang B., Savenkova M. Epigenetic transgenerational inheritance of somatic transcriptomes and epigenetic control regions. Genome Biol 2012, 13:R91.
82. Skinner M., Guerrero-Bosagna C., Haque M.M., Nilsson E., Bhandari R., McCarrey J. Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and subsequent germline. PLoS ONE 2013, 8:e66318.
83. Skinner M.K., Manikkam M., Tracey R., Nilsson E., Haque M.M., Guerrero-Bosagna C. Ancestral DDT exposures promote epigenetic transgenerational inheritance of obesity. BMC Med 2013, 11:228.
84. Skinner M.K., Savenkova M., Zhang B., Crews D. Gene bionetworks involved in epigenetic transgenerational inheritance of altered mate preference: environmental epigenetics and evolutionary biology. BMC Genomics 2014, 15:377.
85. Skinner M.K., Guerrero-Bosagna C., Haque M., Knutie S., Koop J., Clayton D. Role of epigenetics in the speciation and evolution of Darwin's finches. Genome Biol. Evol 2014, 6(8):1972-1989.
86. Song J., Irwin J., Dean C. Remembering the prolonged cold of winter. Curr. Biol 2013, 23:R807-R811.
87. Suter L., Widmer A. Environmental heat and salt stress induce transgenerational phenotypic changes in Arabidopsis thaliana. PLoS ONE 2013, 8:e60364.
88. Tracey R., Manikkam M., Guerrero-Bosagna C., Skinner M. Hydrocarbon (Jet Fuel JP-8) induces epigenetic transgenerational inheritance of adult-onset disease and sperm epimutations. Reprod. Toxicol 2013, 36:104-116.
89. Veenendaal M.V., Painter R.C., de Rooij S.R., Bossuyt P.M., van der Post J.A., Gluckman P.D., et al. Transgenerational effects of prenatal exposure to the 1944-45 Dutch famine. BJOG 2013, 120:548-553.
90. Visscher P.M., Brown M.A., McCarthy M.I., Yang J. Five years of GWAS discovery. Am. J. Hum. Genet 2012, 90:7-24.
91. Waddington C.H. The epigenotype. Endeavour 1942, 1:18-20.
92. Waterland R.A. Epigenetic mechanisms affecting regulation of energy balance: many questions, few answers. Annu. Rev. Nutr 2014, 34:337-355. Epub ahead of print.
93. Wolstenholme J.T., Edwards M., Shetty S.R., Gatewood J.D., Taylor J.A., Rissman E.F., et al. Gestational exposure to bisphenol A produces transgenerational changes in behaviors and gene expression. Endocrinology 2012, 153:3828-3838.
94. Wolstenholme J.T., Goldsby J.A., Rissman E.F. Transgenerational effects of prenatal bisphenol A on social recognition. Horm. Behav 2013, 64:833-839.
95. Yaniv, M., 2014. Chromatin remodeling: from transcription to cancer. Cancer Genet [Epub ahead of print].
96. Zama A.M., Uzumcu M. Epigenetic effects of endocrine-disrupting chemicals on female reproduction: an ovarian perspective. Front. Neuroendocrinol 2010, 31:420-439.
97. Zhao H., Chen Z.J. Genetic association studies in female reproduction: from candidate-gene approaches to genome-wide mapping. Mol. Hum. Reprod 2013, 19:644-654.
98. Zheng X., Chen L., Li M., Lou Q., Xia H., Wang P., et al. Transgenerational variations in DNA methylation induced by drought stress in two rice varieties with distinguished difference to drought resistance. PLoS ONE 2013, 8:e80253.