Nongenetic inheritance and transgenerational epigenetics

Trends in Molecular Medicine

Volumn 21, Issue 2, 2015, Pages 134-144

  Szyf, Moshe ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

DNA methylation; Epigenetics; Germline transmission; Histone modification; Noncoding RNA; Transgenerational

Indexed keywords

HISTONE; SMALL UNTRANSLATED RNA;

CONDITIONING; DNA METHYLATION; EARLY LIFE STRESS; EPIGENETICS; FEAR; GAMETE; GENOTYPE; GERM LINE; HERITABILITY; HISTONE MODIFICATION; HUMAN; INHERITANCE; MOLECULAR MECHANICS; NONHUMAN; PHENOTYPE; PRENATAL EXPOSURE; REVIEW; BIOLOGICAL MODEL; FEMALE; GENETIC EPIGENESIS; GERM CELL; HEREDITY; MALE; METABOLISM;

EPIGENESIS, GENETIC; FEMALE; GERM CELLS; HEREDITY; HUMANS; MALE; MODELS, GENETIC; PHENOTYPE;

EID: 84922890092     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2014.12.004     Document Type: Review

References (126)

1. Laforsch C., Tollrian R. Embryological aspects of inducible morphological defenses in Daphnia. J. Morphol. 2004, 262:701-707.
2. Grossniklaus U., et al. Transgenerational epigenetic inheritance: how important is it?. Nat. Rev. Genet. 2013, 14:228-235.
3. Pembrey M.E. Male-line transgenerational responses in humans. Hum. Fertil. 2010, 13:268-271.
4. Pembrey M.E., et al. Sex-specific, male-line transgenerational responses in humans. Eur. J. Hum. Genet. 2006, 14:159-166.
5. Ravelli G.P., et al. Obesity in young men after famine exposure in utero and early infancy. N. Engl. J. Med. 1976, 295:349-353.
6. Heijmans B.T., et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:17046-17049.
7. Veenendaal M.V., et al. Transgenerational effects of prenatal exposure to the 1944-45 Dutch famine. BJOG 2013, 120:548-553.
8. Seisenberger S., et al. The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol. Cell 2012, 48:849-862.
9. Santos F., et al. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol. 2002, 241:172-182.
10. Oswald J., et al. Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 2000, 10:475-478.
11. Weaver I.C., et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7:847-854.
12. Champagne F.A., et al. 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, 147:2909-2915.
13. Haig D. The (dual) origin of epigenetics. Cold Spring Harb. Symp. Quant. Biol. 2004, 69:67-70.
14. Holliday R. Epigenetics: a historical overview. Epigenetics 2006, 1:76-80.
15. Holliday R. Epigenetics: an overview. Dev. Genet. 1994, 15:453-457.
16. Jablonka E., Lamb M.J. The changing concept of epigenetics. Ann. N. Y. Acad. Sci. 2002, 981:82-96.
17. Waddington C.H. Canalization of development and genetic assimilation of acquired characters. Nature 1959, 183:1654-1655.
18. Szyf M. The early-life social environment and DNA methylation. Clin. Genet. 2012, 81:341-349.
19. Suderman M.M., et al. Conserved epigenetic sensitivity to early life experience in the rat and human hippocampus. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:17266-17272.
20. Razin A., Riggs A.D. DNA methylation and gene function. Science 1980, 210:604-610.
21. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
22. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
23. Mohammad F., et al. Long noncoding RNA-mediated maintenance of DNA methylation and transcriptional gene silencing. Development 2012, 139:2792-2803.
24. Flanagan J.M., Wild L. An epigenetic role for noncoding RNAs and intragenic DNA methylation. Genome Biol. 2007, 8:307.
25. Gold M., et al. Methylation of DNA. J. Gen. Physiol. 1966, 49:5-28.
26. Drahovsky D., Morris N.R. Mechanism of action of rat liver DNA methylase I. Interaction with double-stranded methyl-acceptor DNA. J. Mol. Biol. 1971, 57:475-489.
27. Adams R.L., et al. DNA methylation in nuclei and studies using a purified DNA methylase from ascites cells. Post-Synthetic Modification of M Macromolecules 1975, 39-48. North-Holland. F. Antoni, A. Faragom (Eds.).
28. Kriaucionis S., Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009, 324:929-930.
29. Ito S., et al. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010, 466:1129-1133.
30. Razin A., Szyf M. DNA methylation patterns. Formation and function. Biochim. Biophys. Acta 1984, 782:331-342.
31. Lister R., et al. Global epigenomic reconfiguration during mammalian brain development. Science 2013, 341:1238905.
32. Lister R., et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009, 462:315-322.
33. Pastor W.A., et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 2011, 473:394-397.
34. Comb M., Goodman H.M. CpG methylation inhibits proenkephalin gene expression and binding of the transcription factor AP-2. Nucleic Acids Res. 1990, 18:3975-3982.
35. Lewis J.D., et al. Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 1992, 69:905-914.
36. Jones P.L., et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 1998, 19:187-191.
37. Nan X., et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998, 393:386-389.
38. Baubec T., et al. Methylation-dependent and -independent genomic targeting principles of the MBD protein family. Cell 2013, 153:480-492.
39. Yang X., et al. Gene body methylation can alter gene expression and is a therapeutic target in cancer. Cancer Cell 2014, 26:577-590.
40. Hellman A., Chess A. Gene body-specific methylation on the active X chromosome. Science 2007, 315:1141-1143.
41. Aran D., et al. Replication timing-related and gene body-specific methylation of active human genes. Hum. Mol. Genet. 2011, 20:670-680.
42. Gruenbaum Y., et al. Sequence specificity of methylation in higher plant DNA. Nature 1981, 292:860-862.
43. Gruenbaum Y., et al. Methylation of CpG sequences in eukaryotic DNA. FEBS Lett. 1981, 124:67-71.
44. Gruenbaum Y., et al. Substrate and sequence specificity of a eukaryotic DNA methylase. Nature 1982, 295:620-622.
45. Gopalakrishnan S., et al. DNMT3B interacts with constitutive centromere protein CENP-C to modulate DNA methylation and the histone code at centromeric regions. Hum. Mol. Genet. 2009, 18:3178-3193.
46. Walton E., et al. Maintenance of DNA methylation: Dnmt3b joins the dance. Epigenetics 2011, 6:1373-1377.
47. Okano M., et al. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999, 99:247-257.
48. Seisenberger S., et al. The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol. Cell 2012.
49. Reik W., et al. Epigenetic reprogramming in mammalian development. Science 2001, 293:1089-1093.
50. Lane N., et al. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 2003, 35:88-93.
51. Jenuwein T. Re-SET-ting heterochromatin by histone methyltransferases. Trends Cell Biol. 2001, 11:266-273.
52. Wade P.A., et al. Histone acetylation: chromatin in action. Trends Biochem. Sci. 1997, 22:128-132.
53. Shiio Y., Eisenman R.N. Histone sumoylation is associated with transcriptional repression. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13225-13230.
54. Shilatifard A. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu. Rev. Biochem. 2006, 2432:243-269.
55. Holbert M.A., Marmorstein R. Structure and activity of enzymes that remove histone modifications. Curr. Opin. Struct. Biol. 2005, 15:673-680.
56. Perry M., Chalkley R. Histone acetylation increases the solubility of chromatin and occurs sequentially over most of the chromatin. A novel model for the biological role of histone acetylation. J. Biol. Chem. 1982, 257:7336-7347.
57. Lee D.Y., et al. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 1993, 72:73-84.
58. Peters A.H., Schubeler D. Methylation of histones: playing memory with DNA. Curr. Opin. Cell Biol. 2005, 17:230-238.
59. Kooistra S.M., Helin K. Molecular mechanisms and potential functions of histone demethylases. Nat. Rev. Mol. Cell Biol. 2012, 13:297-311.
60. Roh T.Y., et al. The genomic landscape of histone modifications in human T cells. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:15782-15787.
61. Gaydos L.J., et al. Gene repression. H3K27me and PRC2 transmit a memory of repression across generations and during development. Science 2014, 345:1515-1518.
62. McManus M.T., Sharp P.A. Gene silencing in mammals by small interfering RNAs. Nat. Rev. Genet. 2002, 3:737-747.
63. Aravin A.A., et al. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 2007, 316:744-747.
64. Lau N.C., et al. Characterization of the piRNA complex from rat testes. Science 2006, 313:363-367.
65. Ashe A., et al. piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 2012, 150:88-99.
66. Castel S.E., Martienssen R.A. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 2013, 14:100-112.
67. Volpe T., Martienssen R.A. RNA interference and heterochromatin assembly. Cold Spring Harb. Perspect. Biol. 2011, 3:a003731.
68. Volpe T., et al. RNA interference is required for normal centromere function in fission yeast. Chromosome Res. 2003, 11:137-146.
69. Volpe T.A., et al. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 2002, 297:1833-1837.
70. Dorval V., et al. Circulating microRNAs in Alzheimer's disease: the search for novel biomarkers. Front. Mol. Neurosci. 2013, 6:24.
71. Creemers E.E., et al. Circulating microRNAs: novel biomarkers and extracellular communicators in cardiovascular disease?. Circ. Res. 2012, 110:483-495.
72. Mitchell P.S., et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:10513-10518.
73. Dalakouras A., Wassenegger M. Revisiting RNA-directed DNA methylation. RNA biology 2013, 10:453-455.
74. Wassenegger M., et al. RNA-directed de novo methylation of genomic sequences in plants. Cell 1994, 76:567-576.
75. Brennecke J., et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007, 128:1089-1103.
76. Carmell M.A., et al. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 2007, 12:503-514.
77. Kuramochi-Miyagawa S., et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 2008, 22:908-917.
78. Watanabe T., et al. Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 2011, 332:848-852.
79. Liu D., et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997, 277:1659-1662.
80. Francis D., et al. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 1999, 286:1155-1158.
81. Weaver I.C., et al. Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:3480-3485.
82. McGowan P.O., et al. Broad epigenetic signature of maternal care in the brain of adult rats. PLoS ONE 2011, 6:e14739.
83. Weaver I.C., et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J. Neurosci. 2005, 25:11045-11054.
84. Weaver I.C., et al. The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: altering epigenetic marks by immediate-early genes. J. Neurosci. 2007, 27:1756-1768.
85. Weaver I.C., et al. The methylated-DNA binding protein MBD2 enhances NGFI-A (egr-1)-mediated transcriptional activation of the glucocorticoid receptor. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2014, 369.
86. McGowan P.O., et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 2009, 12:342-348.
87. Cao-Lei L., et al. DNA methylation signatures triggered by prenatal maternal stress exposure to a natural disaster: project ice storm. PLoS ONE 2014, 9:e107653.
88. Howerton C.L., et al. O-GlcNAc transferase (OGT) as a placental biomarker of maternal stress and reprogramming of CNS gene transcription in development. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:5169-5174.
89. Howerton C.L., Bale T.L. Targeted placental deletion of OGT recapitulates the prenatal stress phenotype including hypothalamic mitochondrial dysfunction. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:9639-9644.
90. Quilter C.R., et al. Impact on offspring methylation patterns of maternal gestational diabetes mellitus and intrauterine growth restraint suggest common genes and pathways linked to subsequent type 2 diabetes risk. FASEB J. 2014, 28:4868-4879.
91. West N.A., et al. Exposure to Maternal Diabetes in Utero and DNA Methylation Patterns in the Offspring. Immunometabolism 2013, 1:1-9.
92. Ruchat S.M., et al. Gestational diabetes mellitus epigenetically affects genes predominantly involved in metabolic diseases. Epigenetics 2013, 8:935-943.
93. Nomura Y., et al. Global methylation in the placenta and umbilical cord blood from pregnancies with maternal gestational diabetes, preeclampsia, and obesity. Reprod Sci. 2014, 21:131-137.
94. Sasagawa I., et al. Stress and testicular germ cell apoptosis. Arch. Androl. 2001, 47:211-216.
95. Schultz R., et al. Localization of the glucocorticoid receptor in testis and accessory sexual organs of male rat. Mol. Cell. Endocrinol. 1993, 95:115-120.
96. Kaufmann S.H., et al. Evidence that rodent epididymal sperm contain the Mr approximately 94,000 glucocorticoid receptor but lack the Mr approximately 90,000 heat shock protein. Endocrinology 1992, 130:3074-3084.
97. Belyaev D.K., et al. Effect of hydrocortisone on the phenotypic expression and inheritance of the Fused gene in mice. Theor. Appl. Genet. 1983, 64:275-281.
98. Belyaev D.K., et al. Inheritance of alternative states of the fused gene in mice. J. Hered. 1981, 72:107-112.
99. Petropoulos S., et al. Adult glucocorticoid exposure leads to transcriptional and DNA methylation changes in nuclear steroid receptors in the hippocampus and kidney of mouse male offspring. Biol. Reprod. 2014, 90:43.
100. Morgan C.P., Bale T.L. Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. J. Neurosci. 2011, 31:11748-11755.
101. Rodgers A.B., et al. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J. Neurosci. 2013, 33:9003-9012.
102. Jablonka E., Raz G. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 2009, 84:131-176.
103. Jablonka E. Epigenetic inheritance and plasticity: the responsive germline. Prog. Biophys. Mol. Biol. 2013, 111:99-107.
104. Anway M.D., et al. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308:1466-1469.
105. Skinner M.K., et al. Transgenerational epigenetic programming of the brain transcriptome and anxiety behavior. PLoS ONE 2008, 3:e3745.
106. Manikkam M., et al. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLoS ONE 2013, 8:e55387.
107. Tracey R., et al. Hydrocarbons (jet fuel JP-8) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. Reprod. Toxicol. 2013, 36:104-116.
108. Skinner M.K., et al. Ancestral dichlorodiphenyltrichloroethane (DDT) exposure promotes epigenetic transgenerational inheritance of obesity. BMC Med. 2013, 11:228.
109. Skinner M.K., Guerrero-Bosagna C. Role of CpG deserts in the epigenetic transgenerational inheritance of differential DNA methylation regions. BMC Genomics 2014, 15:692.
110. Crews D., et al. Transgenerational epigenetic imprints on mate preference. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:5942-5946.
111. Franklin T.B., et al. Epigenetic transmission of the impact of early stress across generations. Biol. Psychiatry 2010, 68:408-415.
112. Gapp K., et al. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat. Neurosci. 2014, 17:667-669.
113. Liebers R., et al. Epigenetic regulation by heritable RNA. PLoS Genet. 2014, 10:e1004296.
114. Dias B.G., Ressler K.J. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat. Neurosci. 2013, 17:89-96.
115. Francis G. Too much success for recent groundbreaking epigenetic experiments. Genetics 2014, 198:449-451.
116. Waterland R.A., Jirtle R.L. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol. Cell. Biol. 2003, 23:5293-5300.
117. Dolinoy D.C., et al. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ. Health Perspect. 2006, 114:567-572.
118. Dolinoy D.C., et al. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:13056-13061.
119. Waterland R.A., et al. Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. FASEB J. 2007, 21:3380-3385.
120. Cropley J.E., et al. The penetrance of an epigenetic trait in mice is progressively yet reversibly increased by selection and environment. Proc. Biol. Sci. 2012, 279:2347-2353.
121. Rechavi O., et al. Starvation-induced transgenerational inheritance of small RNAs in C. elegans. Cell 2014, 158:277-287.
122. Ng S.F., et al. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 2010, 467:963-966.
123. Ng S.F., et al. Paternal high-fat diet consumption induces common changes in the transcriptomes of retroperitoneal adipose and pancreatic islet tissues in female rat offspring. FASEB J. 2014, 28:1830-1841.
124. Vassoler F.M., et al. Epigenetic inheritance of a cocaine-resistance phenotype. Nat. Neurosci. 2013, 16:42-47.
125. Vassoler F.M., et al. The impact of exposure to addictive drugs on future generations: Physiological and behavioral effects. Neuropharmacology 2014, 76:269-275.
126. Zeybel M., et al. Multigenerational epigenetic adaptation of the hepatic wound-healing response. Nat. Med. 2012, 18:1369-1377.