ENVIRONMENT-DEPENDENT HUMAN DISEASES: THE EPIGENETIC MECHANISMS OF THEIR DEVELOPMENT AND INHERITANCE



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Abstract

The review presents a critical assessment of recent data about links between ecotoxicology and epigenetics. The major epigenetic changes occurring in embryogenesis and gametogenesis are described as they are influenced by ecotoxicants, primarily bisphenol A (BPA), including its effects on development and differentiation as well as on cognition and behavior. Data about the intergenerational transfer of epigenetic and epigenomic disorders induced by different toxicants during spermatogenesis and early embryogenesis are discussed. Outlined are possible directions of further studies of the role and possible mechanisms of the influences of ecotoxicants on epigenetic disturbances, including DNA methylation and histone acetylation, and of the intergenerational transfer of susceptibility to diseases.

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About the authors

E L Patkin

Institute of Experimental Medicine

Email: lp44@mail.ru
St. Petersburg, Russia

G A Sofronov

Institute of Experimental Medicine

Academic RAS St. Petersburg, Russia

References

  1. Vandegehuchte M. B., Janssen C. R. Epigenetics and its implications for ecotoxicology // Ecotoxicology.- 2011.- Vol. 20.- P. 607-624.
  2. Head J. A., Dolinoy D. C., Basu N. Epigenetics for ecotoxicologist // Environ. Toxicol. Chem.- 2012 - Vol. 31 - P. 221-227.
  3. Hala D., Huggett D. B., Burggren W. W. Environmental stressors and the epigenome // Drug Discov. Today Technol.- 2014.- Vol. 12.- P. 3-8.
  4. Newman M. C., Clements W. H. Ecotoxicology: A Comprehensive Treatment.- Boca Raton, FL: CRC Press, 2008.- 880 c.
  5. Паткин Е. Л., Софронов Г. А. Эпигенетика популяций, экотоксикогенетика и болезни человека // Эколог. генет.- 2012.- Т. 10, № 4.- С. 14-28.
  6. Meagher R. B., Müssar K. J. The influence of DNA sequence on epigenome-induced pathologies // Epigenetics and Chromatin.- 2012.- Vol. 5.- P. 11.
  7. Vandegehuchte M. B., Janssen C. R. Epigenetics in an ecotoxicological context // Mutat. Res. Genet. Toxicol. Environ. Mutagen.- 2014.- Vol. 764-765.- P. 36-45.
  8. Kim M., Bae M., Na H., Yang M. Environmental toxicants-induced epigenetic alterations and their reversers // J. Environ. Sci. Health Environ. Carcinog. Ecotoxicol. Rev.- 2012.- Vol. 30.- P. 323-367.
  9. Паткин Е. Л., Павлинова Л. И., Софронов Г. А. Влияние экотоксикантов на эмбриогенез и гаметогенез млекопитающих: эпигенетические механизмы // Биосфера.- 2013.- Vol. 5.- P. 450-472.
  10. Stern S., Fridmann-Sirkis Y., Braun E., Soen Y. Epigenetically heritable alteration of fly development in response to toxic challenge // Cell Rep.- 2012.- Vol. 1.- P. 528-542.
  11. Ou X. F., Zhang Y. H., Xu C. M., Lin X. Y., Zang Q., Zhuang T. T., Jiang L. L., von Wettstein D., Liu B. Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryzasativa L.) // PLoS ONE.- 2012.- Vol. 7.- P. e41143.
  12. Manikkam M., Tracey R., Guerrero-Bosagna C., Skinner M. K. Pesticide and insect repellent mixture (permethrin and DEET) induces epigenetic transgenerational inheritance of disease and sperm epimutations // Reprod. Toxicol.- 2012.- Vol. 34.- P. 708-719.
  13. Manikkam M., Tracey R., Guerrero-Bosagna C., Skinner M. K. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations // PLoS ONE - 2013.- Vol. 8 - P. e55387.
  14. Anway M. D., Cupp A. S., Uzumcu M., Skinner M. K. Epigenetic transgenerational actions of endocrine disruptors and male fertility // Science.- 2005.- Vol. 308.- P. 1466-1469.
  15. Inawaka K., Kawabe M., Takahashi S., Doi Y., Tomigahara Y., Tarui H., Abe J., Kawamura S., Shirai T. Maternal exposure to anti-androgenic compounds, vinclozolin, flutamide and procymidone, has no effects on spermatogenesis and DNA methylation in male rats of subsequent generations // Toxicol. Appl. Pharmacol.- 2009.- Vol. 237.- P. 178-187.
  16. Schneider S., Marxfeld H., Gröters S., Buesen R., van Ravenzwaay B. Vinclozolin - no transgenerational inheritance of anti-androgenic effects after maternal exposure during organogenesis via the intraperitoneal route // Reprod. Toxicol.- 2013.- Vol. 37.- P. 6-14.
  17. Stouder C., Paoloni-Giacobino A. Transgenerational effects of the endocrine disruptor vinclozolin on the methylation pattern of imprinted genes in the mouse sperm // Reprod. Fertil.- 2010.- Vol. 139.- P. 373-379.
  18. Doshi T., D’Souza C., Dighe V., Vanage G. Effect of neonatal exposure onmale rats to bisphenol a on the expression of DNA methylation machinery in the postimplantation embryo // J. Biochem. Mol. Toxicicol.- 2012.- Vol. 26 - P. 337-343.
  19. Ficz G., Branco M. R., Seisenberger S., Santos F., Krueger F., Hore T. A., Marques C. J., Andrews S., Reik W. Dynamic regulation of 5hydroxymethylcytosine in mouse ES cells and during differentiation // Nature.- 2011.- Vol. 473.- P. 398-402.
  20. Wing T., Pan Q., Lin L., Szulwach K.E., Song C.X., He C., Wu H., Warren S.T., Jin P., Duan R., Li X. Genome-wide DNA hydroxymethylation changes are associated with neurodevelopmental genes in the developing human cerebellum // Hum. Mol. Genet.- 2012 - Vol. 21.- P. 5500-5510.
  21. Kato T., Iwamoto K. Comprehensive DNA methylation and hydroxymethylation analysis in the human brain and its implication in mental disorders // Neuropharmacology.- 2014.- Vol. 80.- P. 133-139.
  22. Suzuki M. M., Bird A. DNA methylation landscapes: provocative insights from epigenomics // Nat. Rev. Genet.- 2008.- Vol. 9.- P. 465-476.
  23. Franchini D. M., Schmitz K. M., Petersen-Mahrt S. K. 5-Methylcytosine DNA demethylation: more than losing a methyl group // Annu. Rev. Genet.- 2012.- Vol. 46.- P. 419-441.
  24. Patkin E. L. Epigenetic mechanisms for primary differentiation in mammalian embryos // Internat. Rev. Cytol.- 2002.- Vol. 216.- P. 81-130.
  25. Patkin E. L., Grudinina N. A., Sasina L. K., Noniashvili E. M., Pavlinova L. I., Suchkova I. O., Kustova M. E., Sofronov G. A. DNA methylation differs between sister chromatids, and this difference correlates with the degree of differentiation potential // Mol. Reprod. Dev.- 2015 - doi: 10.1002/mrd.22519. [Epub ahead of print]
  26. Ito S., D'Alessio A. C., Taranova O. V., Hong K., Sowers L. C., Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification // Nature - 2010 - Vol. 466.- P. 1129-1133.
  27. Tahiliani M., Koh K. P., Shen Y., Pastor W. A., Bandukwala H., Brudno Y., Agarwal S., Iyer L. M., Liu D. R., Aravind L., Rao A. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1 // Science - 2009 - Vol. 324 - P. 930-935.
  28. Liu J., Casaccia P. Epigenetic regulation of oligodendrocyte identity // Trends Neurosci.- 2010 - Vol. 33 - P. 193-201.
  29. Kriaucionis S., Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain // Science - 2009 - Vol. 324 - P. 929-930.
  30. Shen L., Wu H., Diep D., Yamaguchi S., D'Alessio A. C., Fung H. L., Zhang K., Zhang Y. Genome-wide analysis reveals TET- and TDG-dependent 5-methylcytosine oxidation dynamics // Cell.- 2013.- Vol. 153.- P. 692-706.
  31. Yildirim O., Li R., Hung J. H., Chen P. B., Dong X., Ee L. S., Weng Z., Rando O. J., Fazzio T. G. Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells // Cell.- 2011.- Vol. 147.- P. 1498-1510.
  32. Lister R., Mukamel E.A., Nery J.R., Urich M., Puddifoot C.A., Johnson N.D., Lucero J., Huang Y., Dwork A. J., Schultz M. D., Yu M., Tonti-Filippini J., Heyn H., Hu S., Wu J.C., Rao A., Esteller M., He C., Haghighi F. G., Sejnowski T. J., Behrens M. M., Ecker J. R. Global epigenomic reconfiguration during mammalian brain development // Science.- 2013.- Vol. 341.- P. 1237905.
  33. Bachman M., Uribe-Lewis S., Yang X., Burgess H.E., Iurlaro M., Reik W., Murrell A. Balasubramanian S. 5-Formylcytosine can be a stable DNA modification in mammals // Nature Chem. Biol.- 2015 - Vol. 11 (8).- P. 555-557.
  34. Campos E. I., Stafford J. M., Reinberg D. Epigenetic inheritance: histone bookmarks across generations // Trends Cell Biol.- 2014.- Vol. 24.- P. 664-674.
  35. Talbert P. B., Henikoff S. Environmental responses mediated by histone variants // Trends Cell Biol.- 2014.- Vol. 24.- P. 642-650.
  36. Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development // Nature.- 2007.- Vol. 447.- P. 425-432.
  37. Li B., Carey M., Workman J. L. The role of chromatin during transcription // Cell.- 2007.- Vol. 128.- P. 707-719.
  38. Klose R. J, Bird A. P. Genomic DNA methylation: the mark and its mediators // Trends Biochem. Sci.- 2006.- Vol. 31.- P. 89-97.
  39. Berger S. L. The complex language of chromatin regulation during transcription // Nature.- 2007.- Vol. 447.- P. 407-412.
  40. Fuks F. DNA methylation and histone modifications: teaming up to silence genes // Curr. Opin. Genet. Dev.- 2005.- Vol. 15.- P. 490-495.
  41. Feng S., Jacobsen S. E., Reik W. Epigenetic reprogramming in plant and animal development // Science.- 2010.- Vol. 330.- P. 622-627.
  42. Hackett J. A., Dietmann S., Murakami K., Down T. A., Leitch H. G., Surani M. A. Synergistic mechanisms of DNA demethylation during transition to ground-state pluripotency // Stem Cell Reports.- 2013.- Vol. 1.- P. 518-531.
  43. Паткин Е. Л., Сучкова И. О. Регуляторные механизмы импринтинга у млекопитающих // Цитология.- 2006 - Т. 48.- С. 578-594.
  44. Kundakovic M., Frances A., Champagne F. A. Epigenetic perspective on the developmental effects of bisphenol A // Brain Behav. Immun.- 2011.- Vol. 25.- P. 1084-1093.
  45. Golebiewska A., Atkinson S. P., Lako M., Armstrong L. Epigenetic landscaping during hESC differentiation to neural cells // Stem Cells.- 2009.- Vol. 27.- P. 1298-1308.
  46. Liu J., Sandoval J., Doh S. T., Cai L., Lôpez-Rodas G., Casaccia P. Epigenetic modifiers are necessary but not sufficient for reprogramming non-myelinating cells into myelin gene-expressing cells // PLoS One.- 2010.- Vol. 7.- P. e13023.
  47. Barker D. J., Clark P. M. Fetal undernutrition and disease in later life // Rev. Reprod.- 1997.- Vol. 2 - P. 105-112.
  48. Barker D., Eriksson J., Forsen T., Osmond C. Fetal origins of adult disease: Strength of effects and biological basis // Int. J. Epidemiol.- 2002.- Vol. 31.- P. 1235-1239.
  49. Wadhwa P., Buss C., Entringer S., Swanson J. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms // Semin. Reprod. Med.- 2009.- Vol. 27.- P. 358-368.
  50. Hanson M. A., Gluckman P. D. Developmental origins of health and disease: New insights // Basic Clinical Pharmacol. Toxicol.- 2007.- Vol. 102.- P. 90-93.
  51. Mathers J. C., McKay J. A. Epigenetics - potential contribution to fetal programming // Adv. Exp. Med. Biol.- 2009.- Vol. 646.- P. 119-123.
  52. Murphy S. K., Jirtle R. L. Imprinting evolution and the price of silence // Bioessays.- 2003.- Vol. 25.- P. 577-588.
  53. Bernal A. J., Jirtle R. L. Epigenomic disruption: The effects of early developmental exposures // Birth Defects Res. A Clin. Mol. Teratol.- 2010.- Vol. 88.- P. 938-944.
  54. Weaver J. R., Susiarjo M. Imprinting and epigenetic changes in the early embryo // Mamm. Genome.- 2009.- Vol. 20.- P. 532-543.
  55. Das R., Hampton D., Jirtle R. Imprinting evolution and human health // Mamm. Genome.- 2009.- Vol. 20 - P. 563-572.
  56. Jirtle R. L., Skinner M. K. Environmental epigenomics and disease susceptibility // Nat. Rev. Genet.- Vol. 8.- P. 253-262.
  57. Veurink M., Koster M., Berg L. T. The history of DES, lessons to be learned // Pharm. World Sci.- 2005.- Vol. 27.- P. 139-143.
  58. Newbold R. R., Hanson R. B., Jefferson W. N., Bullock B. C., Haseman J., McLachlan J. A. Increased tumors but uncompromised fertility in the female descendants of mice exposed developmentally to diethylstilbestrol // Carcinogenesis.- 1998.- Vol. 19.- P. 1655-1663.
  59. Newbold R. R., Hanson R. B., Jefferson W. N., Bullock B. C., Haseman J., McLachlan J. A. Proliferative lesions and reproductive tract tumors in male descendants of mice exposed developmentally to diethylstilbestrol // Carcinogenesis.- 2000.- Vol. 21.- Р. 1355-1363.
  60. Lange U. C., Schneider R. What an epigenome remembers // Bioessays.- 2010.- Vol. 32.- P. 659-668.
  61. Guerrero-Bosagna C., Settles M., Lucker B., Skinner M. K. Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome // PLoS ONE.- 2010.- Vol. 5.- P. 13100.
  62. Anway M. D., Skinner M. K. Epigenetic transgenerational actions of endocrine disruptors // Endocrinology.- 2006.- Vol. 147.- P. S43-S49.
  63. Ling C., Groop L. Epigenetics: a molecular link between environmental factors and type 2 diabetes // Diabetes - 2006 - Vol. 58.- P. 2718-2725.
  64. Somm E., Schwitzgebel V., Toulotte A., Cederroth C., Combescure C., Nef S., Aubert M., Huppi P. Perinatal exposure to bisphenol A alters early adipogenesis in the rat // Environ. Health Perspect.- 2009.- Vol. 117.- P. 1549-1555.
  65. Price T., Murphy S., Younglai E. Perspectives: The possible influence of assisted reproductive technologies on transgenerational reproductive effects of environmental endocrine disruptors // Toxicol. Sci.- 2007.- Vol. 96.- P. 218-226.
  66. Vom Saal F. S., Akingbemi B. T., Belcher S. M. 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.- Vol. 24.- P. 131-138.
  67. Calafat A. M., Kuklenyik Z., Reidy J. A., Caudill S. P., Ekong J., Needham L. L. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population // Environ. Health Perspect.- 2005.- Vol. 113.- P. 391-395.
  68. Lang I. A., Galloway T. S., Scarlett A., Henley W. E., Depledge M., Wallace R. B., Melzer D. Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults // JAMA.- 2008.- Vol. 300.- P. 1303-1310.
  69. Alonso-Magdalena P., Morimoto S., Ripoll C., Fuentes E., Nadal A. The estrogenic effect of bisphenol A disrupts pancreatic beta-cell function in vivo and induces insulin resistance // Environ. Health Perspect.- 2006.- Vol. 114.- P. 106-112.
  70. Carwile J. L., Michels K. B. Urinary bisphenol A and obesity: NHANES 2003-2006 // Environ. Res.- 2011 - Vol. 111 - P. 825-830.
  71. Heindel J. J., vom Saal F. S. Role of nutrition and environmental endocrine disrupting chemicals during the perinatal period on the aetiology of obesity // Mol. Cell Endocrinol.- 2009.- Vol. 304.- P. 90-96.
  72. Caserta D., Di Segni N., Mallozzi M., Giovanale V., Mantovani A., Marci R., Moscarini M. Bisphenol A and the female reproductive tract: An overview of recent laboratory evidence and epidemiological studies // Reprod. Biol. Endocrinol.- 2014.- Vol. 12.- P. 37.
  73. Durando M., Kass L., Piva J., Sonnenschein C., Soto A. M., Luque E. H., Munoz-de-Toro M. Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats // Environ. Health Perspect.- 2007.- Vol. 115 - P. 80-86.
  74. Prins G. S., Hu W. Y., Shi G. B., Hu D. P., Majumdar S., Li G., Huang K., Nelles J. L., Ho S. M., Walker C. L., Kajdacsy-Balla A., van Breemen R. B. Bisphenol A promotes human prostate stem-progenitor cell self-renewal and increases in vivo carcinogenesis in human prostate epithelium // Endocrinology.- 2014.- Vol. 155.- P. 805-817.
  75. Hassan Z. K., Elobeid M. A., Virk P., Omer S. A., ElAmin M., Daghestani M. H., Alolayan E. M. Bisphenol A induces hepatotoxicity through oxidative stress in rat model // Oxid. Med. Cell. Longev.- 2012.- Vol. 2012.- P. 194829.
  76. Hajszan T., Leranth C. Bisphenol A interferes with synaptic remodeling // Front. Neuroendocrinol.- 2010.- Vol. 31.- P. 519-530.
  77. Xu X., Hong X., Xie L., Li T., Yang Y., Zhang Q., Zhang G., Liu X. Gestational and lactational exposure to bisphenol-A affects anxiety- and depression-like behaviors in mice // Horm. Behav.- 2012.- Vol. 62.- P. 480-490.
  78. Fujimoto T., Kubo K., Aou S. Prenatal exposure to bisphenol A impairs sexual differentiation of exploratory behavior and increases depression-like behavior in rats // Brain Res.- 2006 - Vol. 1068.- P. 49-55.
  79. Wolstenholme J. T., Rissman E. F., Connelly J. J. The role of Bisphenol A in shaping the brain, epigenome and behavior // Horm. Behav.- 2011.- Vol. 59.- P. 296-305.
  80. Chen M., Zhou K., Chen X., Qiao S., Hu Y., Xu B. Metabolomic analysis reveals metabolic changes caused by bisphenol A in rats // Toxicol. Sci.- 2014.- Vol. 138.- P. 256-267.
  81. McLachlan J. A. Environmental signaling: what embryos and evolution teach us about endocrine disrupting chemicals // Endocr. Rev. - 2001. - Vol. 22.- P. 319-341.
  82. Dolinoy D. C., Huang D., Jirtle R. L. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development // Proc. Natl. Acad. Sci. USA.- 2007.- Vol. 104.- P. 13056-13061.
  83. Rosenfeld C. S. Animal models to study environmental epigenetics // Biol. Reprod.- 2010.- Vol. 82.- P. 473-488.
  84. Cooney C. A., Dave A. A., Wolff G. L. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring // J. Nutr.- 2002.- Vol. 132.- P. 393-400.
  85. Biddie S. C. Chromatin architecture and the regulation of nuclear receptor inducible transcription // J. Neuroendocrinol.- 2011.- Vol. 23.- P. 94-106.
  86. Metivier R., Gallais R., Tiffoche C., Le Peron C., Jurkowska R. Z., Carmouche R. P. Cyclical DNA methylation of a transcriptionally active promoter // Nature.- 2008.- Vol. 452.- P. 45-50.
  87. Alworth L. C., Howdeshell K. L., Ruhlen R. L., Day J. K., Lubahn D. B., Huang T. H., Besch-Williford C. L., vom Saal F. S. Uterine responsiveness to estradiol and DNA methylation are altered by fetal exposure to diethylstilbestrol andmethoxychlor in CD-1 mice: effects of low versus high doses // Toxicol. Appl. Pharmacol.- 2002.- Vol. 183.- P. 10-22.
  88. Bromer J. G., Zhou Y., Taylor M. B., Doherty L., Taylor H. S. Bisphenol-A exposure in utero leads to epigenetic alterations in the developmental programming of uterine estrogen response // FASEB J.- 2010.- Vol. 24.- P. 2273-2280.
  89. Yin R., Gu L., Li M., Jiang C., Cao T., Zhang X., Yin R., Gu L., Li M., Jiang C., Cao T. Gene expression profiling analysis of bisphenol A-induced perturbation in biological processes in ER negative HEK293 cells // PLoS ONE.- 2014.- Vol. 9 (6).- P. e98635.
  90. Champagne F. A., Curley J. P. Maternal regulation of estrogen receptor alpha methylation // Curr. Opin. Pharmacol.- 2008.- Vol. 8.- P. 735-739.
  91. Kawai K., Murakami S., Senba E., Yamanaka T., Fujiwara Y., Arimura C., Nozaki T., Takii M., Kubo C. Changes in estrogen receptors alpha and beta expression in the brain of mice exposed prenatally to bisphenol A // Regul. Toxicol. Pharmacol.- 2007.- Vol. 47.- P. 166-170.
  92. Miao S., Gao Z., Kou Z., Xu G., Su C., Liu N. Influence of bisphenol a on developing rat estrogen receptors and some cytokines in rats: a two generational study // J. Toxicol. Environ. Health A.- 2008.- Vol. 71.- P. 1000-1008.
  93. Champagne F. A., Weaver I. C., Diorio J., Dymov S., Szyf M., Meaney M. J. Maternal care associated with methylation of the estrogen receptor -alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring / / Endocrinology.- 2006.- Vol. 147.- P. 2909-2915.
  94. Ramsahoye B. H., Biniszkiewicz D., Lyko F., Clark V., Bird A. P., Jaenisch R. Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3A // Proc. Natl. Acad. Sci. USA.- 2000.- Vol. 97.- P. 5237-5242.
  95. Gupta R., Nagarajan A., Wajapeyee N. Advances in genome-wide DNA methylation analysis // Biotechniques.- 2010.- Vol. 49.- P. iii-xi.
  96. Guo W., Chung W. Y., Qian M., Pellegrini M., Zhang M. Q. Characterizing the strand-specific distribution of non-CpG methylation in human pluripotent cells // Nucleic Acids Res.- 2014.- Vol. 42.- P. 3009-3016.
  97. Mattout A., Meshorer E. Chromatin plasticity and genome organization in pluripotent embryonic stem cells // Curr. Opin. Cell. Biol.- 2010.- Vol. 22 - P. 334-341.
  98. Sato N., Yamakawa N., Masuda M., Sudo K., Hatada I., Muramatsu M. Genome-wide DNA methylation analysis reveals phytoestrogen modification of promoter methylation patterns during embryonic stem cell differentiation // PLoS ONE.- 2011.- Vol. 6.- P. e19278.
  99. Singh S., Li S. S-L. Epigenetic effects of environmental chemicals bisphenol A and phthalates // Int. J. Mol. Sci.- 2012.- Vol. 13.- P. 10143-10153.
  100. Chao H.-H., Zhang X.-F., Chen B., Pan B., Zhang L.-J., Li L., Sun X.-F., Shi Q.-H., Shen W. Bisphenol A exposure modifies methylation of imprinted genes in mouse oocytes via the estrogen receptor signaling pathway // Histochem. Cell Biol.- 2012.- Vol. 237.- P. 249-259.
  101. Kim K., Son T. G., Park H. R., Kim S. J., Kim H. S., Han S. Y., Lee J. Potencies of bisphenol A on the neuronal differentiation and hippocampal neurogenesis // J. Toxicol. Environ. Health A.- 2009.- Vol. 72.- P. 1343-1351.
  102. Huang B., Jiang C., Luo J., Cui Y., Qin L., Liu J. Maternal exposure to bisphenol A may increase the risks of Parkinson’s disease through down-regulation of fetal IGF-1 expression // Medical Hypotheses.- 2014.- Vol. 82.- P. 245-249.
  103. Lister R., Pelizzola M., Dowen R. H., Hawkins R. D., Hon G., Tonti-Filippini J., Nery J. R., Lee L., Thomson J. A., Ren B., Ecker J. R. Human DNA methylomes at base resolution show widespread epigenomic differences // Nature.- 2009.- Vol. 462.- P. 315-322.
  104. Petronis A. Epigenetics as a unifying principle in the aetiology of complex traits and diseases // Nature.- 2010.- Vol. 465.- P. 721-727.
  105. Yao B., Jin P. Cytosine modifications in neurodevelopment and diseases // Cell. Mol. Life Sci.- 2014.- Vol. 71.- P. 405-418.
  106. Mileva G., Bielajew C., Konkle A. T. Estrous cycle: Physiology, endocrinology and role in breeding and reproductive management. In sex differences in physiology and behaviour: The importance of hormones and rearing environment / / Durand L., ed.. - Nova Science Publisher: Hauppauge, NY, USA, 2013.- 876 p.
  107. Mileva G., Baker S. L., Konkle A. T., Bielajew C. Bisphenol-A: Epigenetic reprogramming and effects on reproduction and behavior // Int. J. Environ. Res. Public Health.- 2014.- Vol. 11.- P. 7537-7561.
  108. Kubo K., Arai O., Ogata R., Omura M., Hori T., Aou S. Exposure to bisphenol A during the fetal and suckling periods disrupts sexual differentiation of the locus coeruleus and of behavior in the rat // Neurosci. Lett.- 2001.- Vol. 304.- P. 73-76.
  109. Gioiosa L., Fissore E., Ghirardelli G., Parmigiani S., Palanza P. Developmental exposure to low-dose estrogenic endocrine disruptors alters sex differences in exploration and emotional responses in mice // Horm. Behav.- 2007 - Vol. 52 - P. 307-316.
  110. Dessi-Fulgheri F., Porrini S., Farabollini F. Effects of perinatal exposure to bisphenol A on play behavior of female and male juvenile rats // Environ. Health Perspect.- 2002 - Vol. 110 - P. 403-407.
  111. Komada M., Asai Y., Morii M., Matsuki M., Sato M., Nagao T. Maternal bisphenol A oral dosing relates to the acceleration of neurogenesis in the developing neocortex of mouse fetuses // Toxicology.- 2012.- Vol. 295.- P. 31-38.
  112. Rasmussen T. P. The epigenetics of early development: inferences from stem cells // Mol. Reprod. Dev.- 2014 - Vol. 81.- P. 194-201.
  113. Chen X., Xu B., Han X., Mao Z., Talbot P., Chen M., Du G., Chen A., Liu J., Wanga X., Xia Y. Effect of bisphenol A on pluripotency of mouse embryonic stem cells and differentiation capacity in mouse embryoid bodies // Toxicol. in Vitro.- 2013.- Vol. 27.- P. 2249-2255.
  114. Kraushaar D. C., Zhao K. The epigenomics of embryonic stem cell differentiation // Int. J. Biol. Sci.- 2013.- Vol. 99.- P. 1134-1144.
  115. Zhao Z., Fan L., Frick K. M. Epigenetic alterations regulate estradiol-induced enhancement of memory consolidation // Proc. Natl. Acad. Sci. USA.- 2010.- Vol. 107.- P. 5605-5610.
  116. Matsui Y., Mochizuki K. A current view of the epigenome in mouse primordial germ cells // Mol. Reprod. Dev.- 2014.- Vol. 81.- P. 160-170.

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