Epigenome changes during development

Epigenetic Epidemiology

Volumn , Issue , 2012, Pages 77-103

  Kelsey, Gavin ^a,b  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84931471793     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-94-007-2495-2_6     Document Type: Chapter

References (134)

1. Sasaki H, Matsui Y (2008) Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 9:129-140
2. Hemberger M, Dean W, Reik W (2009) Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nat Rev Mol Cell Biol 10:526-537
3. Hajkova P (2010) Epigenetic reprogramming-taking a lesson from the embryo. Curr Opin Cell Biol 22:342-350
4. Ferguson-Smith AC, Surani MA (2001) Imprinting and the epigenetic asymmetry between parental genomes. Science 293:1086-1089
5. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G et al (2007) Genomewide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448:553-560
6. Bock C, Tomazou EM, Brinkman AB, Müller F, Simmer F, Gu H et al (2010) Quantitative comparison of genome-wide DNA methylation mapping technologies. Nat Biotechnol 28:1106-1114
7. Hayashi K, de Sousa Lopes SM, Surani MA (2007) Germ cell specification in mice. Science 316:394-396
8. Saitou M, Barton SC, Surani MA (2002) A molecular programme for the specification of germ cell fate in mice. Nature 418:293-300
9. Ohinata Y, Payer B, O'Carroll D, Ohinata Y, Surani MA (2005) Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436:207-213
10. Ancelin K, Lange UC, Hajkova P, Schneider R, Bannister AJ, Kouzarides T et al (2006) Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat Cell Biol 8:623-630
11. Yamaji M, Seki Y, Kurimoto K, Yabuta Y, Yuasa M, Shigeta M et al (2008) Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat Genet 40:1016-1022
12. Seki Y, Hayashi K, Itoh K, Mizugaki M, Saitou M, Matsui Y (2005) Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev Biol 278:440-458
13. Hajkova P, Ancelin K, Waldmann T, Lacoste N, Lange UC, Cesari F et al (2008) Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452:877-881
14. Santos F, Dean W (2004) Epigenetic reprogramming during early development in mammals. Reproduction 127(6):643-651
15. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W et al (2002) Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 117:15-23
16. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, Walter J et al (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35:88-93
17. Hajkova P, Jeffries SJ, Lee C, Miller N, Jackson SP, Surani MA (2010) Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329:78-82
18. Popp C, Dean W, Feng S, Cokus SJ, Andrews S, Pellegrini M et al (2010) Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463:1101-1105
19. Lucifero D, Mann MR, Bartolomei MS, Trasler JM (2004) Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet 13:839-849
20. Hiura H, Obata Y, Komiyama J, Shirai M, Kono T (2006) Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells 11:353-361
21. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH (2001) Dnmt3L and the establishment of maternal genomic imprints. Science 294:2536-2539
22. Hata K, Okano M, Lei H, Li E (2002) Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129:1983-1993
23. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E et al (2004) Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429:900-903
24. Kaneda M, Hirasawa R, Chiba H, Okano M, Li E, Sasaki H (2010) Genetic evidence for Dnmt3a-dependent imprinting during oocyte growth obtained by conditional knockout with Zp3-Cre and complete exclusion of Dnmt3b by chimera formation. Genes Cells 15:169-179
25. Smallwood SA, Tomizawa S, Krueger F, Ruf N, Carli N, Sato S et al (2011) Dynamic CpG island methylation landscape in oocytes and its fate in preimplantation embryos. Nat Genet. 43:811-814
26. Tomizawa S, Kobayashi H, Watanabe T, Andrews S, Hata K, Kelsey G et al (2011) Dynamic stage-specific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes. Development 138:811-820
27. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z et al (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448:714-71
28. Zhang Y, Jurkowska R, Soeroes S, Rajavelu A, Dhayalan A, Bock I et al (2010) Chromatin methylation activity of Dnmt3a and Dnmt3a/3 L is guided by interaction of the ADD domain with the histone H3 tail. Nucleic Acids Res 38:4246-4253
29. Ciccone DN, Su H, Hevi S, Gay F, Lei H, Bajko J et al (2009) KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature 461:415-418
30. Chotalia M, Smallwood SA, Ruf N, Dawson C, Lucifero D, Frontera M et al (2009) Transcription is required for establishment of germline methylation marks at imprinted genes. Genes Dev 23:105-117
31. Murdoch S, Djuric U, Mazhar B, Seoud M, Khan R, Kuick R et al (2006) Mutations in NALP7 cause recurrent hydatidiform moles and reproductive wastage in humans. Nat Genet 38:300-302
32. Meyer E, Lim D, Pasha S, Tee LJ, Rahman F, Yates JRW et al (2009) Germline mutation in NLRP2 (NALP2) in a familial imprinting disorder (Beckwith-Wiedemann Syndrome). PLoS Genet 5:e1000423
33. Davis TL, Yang GJ, McCarrey JR, Bartolomei MS (2000) The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum Mol Genet 9:2885-2894
34. Ariel M, Cedar H, McCarrey J (1994) Developmental changes in methylation of spermatogenesisspecifi c genes include reprogramming in the epididymis. Nat Genet 7:59-63
35. Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM (2007) Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. Dev Biol 307:368-379
36. Kato Y, Kaneda M, Hata K, Kumaki K, Hisano M, Kohara Y et al (2007) 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 16:2272-2280
37. Kota SK, Feil R (2010) Epigenetic transitions in germ cell development and meiosis. Dev Cell 19:675-686
38. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF et al (2008) A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31:785-799
39. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Takamatsu K, Chuma S, Kojima-Kita K et al (2010) DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22:908-917
40. Watanabe T, Tomizawa S, Mitsuya K, Totoki Y, Yamamoto Y, Kuramochi-Miyagawa S et al (2011) Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 332:848-852
41. Borgel J, Guibert S, Li Y, Chiba H, Schübeler D, Sasaki H et al (2010) Targets and dynamics of promoter DNA methylation during early mouse development. Nat Genet 42:1093-1100
42. Weber M, Hellmann I, Stadler MB, Ramos L, Pääbo S, Rebhan M et al (2007) Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39:457-466
43. Schulz R, Proudhon C, Bestor TH, Woodfine K, Lin CS, Lin SP et al (2010) The parental non-equivalence of imprinting control regions during mammalian development and evolution. PLoS Genet 6:e1001214
44. Flanagan JM, Popendikyte V, Pozdniakovaite N, Sobolev M, Assadzadeh A, Schumacher A et al (2006) Intra-and interindividual epigenetic variation in human germ cells. Am J Hum Genet 79:67-84
45. Kobayashi H, Hiura H, John RM, Sato A, Otsu E, Kobayashi N et al (2009) DNA methylation errors at imprinted loci after assisted conception originate in the parental sperm. Eur J Hum Genet 17:1582-1591
46. Poplinski A, Tüttelmann F, Kanber D, Horsthemke B, Gromoll J (2010) Idiopathic male infertility is strongly associated with aberrant methylation of MEST and IGF2/H19 ICR1. Int J Androl 33:642-649
47. Kimmins S, Sassone-Corsi P (2005) Chromatin remodelling and epigenetic features of germ cells. Nature 434:583-589
48. Hayashi K, Yoshida K, Matsui Y (2005) A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438:374-378
49. Tachibana M, Nozaki M, Takeda N, Shinkai Y (2007) Functional dynamics of H3K9 methylation during meiotic prophase progression. EMBO J 26:3346-3359
50. Peters AH, O'Carroll D, Scherthan H, Mechtler K, Sauer S, Schöfer C et al (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323-337
51. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR (2009) Distinctive chromatin in human sperm packages genes for embryo development. Nature 460:473-478
52. Brykczynska U, Hisano M, Erkek S, Ramos L, Oakeley EJ, Roloff TC et al (2010) Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol 17:679-687
53. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R et al (2010) Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143:1084-1096
54. Santos F, Peters AH, Otte AP, Reik W, Dean W (2005) Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev Biol 280:225-236
55. Puschendorf M, Terranova R, Boutsma E, Mao X, Isono K, Brykczynska U et al (2008) PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat Genet 40:411-420
56. Terranova R, Yokobayashi S, Stadler MB, Otte AP, van Lohuizen M, Orkin SH et al (2008) Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos. Dev Cell 15:668-679
57. Mayer W, Niveleau A, Walter J, Fundele R, Haaf T (2000) Demethylation of the zygotic paternal genome. Nature 403:501-502
58. Oswald J, Engemann S, Lane N, Mayer W, Olek A, Fundele R et al (2000) Active demethylation of the paternal genome in the mouse zygote. Curr Biol 10:475-478
59. Santos F, Hendrich B, Reik W, Dean W (2002) Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 241:172-182
60. Okada Y, Yamagata K, Hong K, Wakayama T, Zhang Y (2010) A role for the elongator complex in zygotic paternal genome demethylation. Nature 463:554-558
61. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y et al (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324:930-935
62. Iqbal K, Jin SG, Pfeifer GP, Szabó PE (2011) Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci USA 108:3642-3647
63. Inoue A, Zhang Y (2011) Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 334:194 doi: 10.1126/science.1212483
64. Kriaucionis S, Heintz N (2009) The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324:929-930
65. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y (2010) Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466:1129-1133
66. Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA et al (2011) Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473:398-402
67. Koh KP, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J et al (2011) Tet1 and tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 8:200-213
68. Nakamura T, Arai Y, Umehara H, Masuhara M, Kimura T, Taniguchi H et al (2007) PGC7/ Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol 9:64-71
69. Howell CY, Bestor TH, Ding F, Latham KE, Mertineit C, Trasler JM et al (2001) Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 104:829-838
70. Ratnam S, Mertineit C, Ding F, Howell CY, Clarke HJ, Bestor TH et al (2002) Dynamics of Dnmt1 methyltransferase expression and intracellular localization during oogenesis and preimplantation development. Dev Biol 245:304-314
71. Hirasawa R, Chiba H, Kaneda M, Tajima S, Li E, Jaenisch R et al (2008) Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev 15:1607-1616
72. Mohan KN, Ding F, Chaillet JR (2011) Distinct roles of DMAP1 in mouse development. Mol Cell Biol 31:1861-1869
73. Li X, Ito M, Zhou F, Youngson N, Zuo X, Leder P et al (2008) A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev Cell 15:547-557
74. Mackay DJ, Callaway JL, Marks SM, White HE, Acerini CL, Boonen SE et al (2008) Hypomethylation of multiple imprinted loci in individuals with transient neonatal diabetes is associated with mutations in ZFP57. Nat Genet 40:949-951
75. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T et al (2010) KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463:237-240
76. Chapman V, Forrester L, Sanford J, Hastie N, Rossant J (1984) Cell lineage-specific undermethylation of mouse repetitive DNA. Nature 307:284-286
77. Sarmento OF, Digilio LC, Wang Y, Perlin J, Herr JC, Allis CD et al (2004) Dynamic alterations of specific histone modifications during early murine development. J Cell Sci 117:4449-4459
78. Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M (2007) Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445:214-218
79. Parfitt DE, Zernicka-Goetz M (2010) Epigenetic modification affecting expression of cell polarity and cell fate genes to regulate lineage specification in the early mouse embryo. Mol Biol Cell 21:2649-2660
80. Jedrusik A, Parfitt DE, Guo G et al (2008) Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo. Genes Dev 22:2692-2706
81. Ng RK, Dean W, Dawson C, Lucifero D, Madeja Z, Reik W et al (2008) Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat Cell Biol 10:1280-1290
82. Hayashi K, Lopes SM, Tang F, Surani MA (2008) Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 3:391-401
83. Ji H, Ehrlich LI, Seita J, Murakami P, Doi A, Lindau P et al (2010) Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature 467:338-342
84. Satterlee JS, Schübeler D, Ng HH (2010) Tackling the epigenome: challenges and opportunities for collaboration. Nat Biotechnol 28:1039-1044
85. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J et al (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315-326
86. Mikkelsen TS, Hanna J, Zhang X, Ku M, Wernig M, Schorderet P et al (2008) Dissecting direct reprogramming through integrative genomic analysis. Nature 454:49-55
87. Lister R, Pelizzola M, Kida YS, Hawkins RD, Nery JR, Hon G et al (2011) Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471:68-73
88. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S et al (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40:897-903
89. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF et al (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459:108-112
90. Mikkelsen TS, Xu Z, Zhang X, Wang L, Gimble JM, Lander ES et al (2010) Comparative epigenomic analysis of murine and human adipogenesis. Cell 143:156-169
91. Illingworth RS, Bird AP (2009) CpG islands-'a rough guide'. FEBS Lett 583:1713-1120
92. Illingworth R, Kerr A, Desousa D, Jørgensen H, Ellis P, Stalker J et al (2008) A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol 6:e22
93. Illingworth RS, Gruenewald-Schneider U, Webb S, Kerr AR, James KD, Turner DJ et al (2010) Orphan CpG islands identify numerous conserved promoters in the mammalian genome. PLoS Genet 6:e1001134
94. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD et al (2010) Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466:253-257
95. Irizarry RA, Ladd-Acosta C, Wen B et al (2008) The human colon cancer methylome shows similar hypo-and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 41:178-186
96. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A et al (2008) Genomescale DNA methylation maps of pluripotent and differentiated cells. Nature 454:766-770
97. Thomson JP, Skene PJ, Selfridge J, Clouaire T, Guy J, Webb S et al (2010) CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature 464:1082-1086
98. Blackledge NP, Zhou JC, Tolstorukov MY, Farcas AM, Park PJ, Klose RJ (2010) CpG islands recruit a histone H3 lysine 36 demethylase. Mol Cell 38:179-190
99. Hernandez-Munoz I, Taghavi P, Kuijl C, Neefjes J, van Lohuizen M (2005) Association of BMI1 with polycomb bodies is dynamic and requires PRC2/EZH2 and the maintenance DNA methyltransferase DNMT1. Mol Cell Biol 25:11047-11058
100. Viré E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C et al (2006) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439:871-874
101. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L et al (2007) A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 39:237-242
102. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J et al (2007) Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 39:232-236
103. Bostick M, Kim JK, Estève PO, Clark A, Pradhan S, Jacobsen SE (2007) UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317:1760-1764
104. Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo TA et al (2007) The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450:908-912
105. Margueron R, Reinberg D (2010) Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet 11:285-296
106. Espada J, Ballestar E, Fraga MF, Villar-Garea A, Juarranz A, Stockert JC et al (2004) Human DNA methyltransferase 1 is required for maintenance of the histone H3 modification pattern. J Biol Chem 279:37175-37184
107. Kacem S, Feil R (2009) Chromatin mechanisms in genomic imprinting. Mamm Genome 20:544-556
108. Tucker KL, Beard C, Dausmann J, Jackson-Grusby L, Laird PW, Lei H et al (1996) Germline passage is required for establishment of methylation and expression patterns of imprinted but not of nonimprinted genes. Genes Dev 10:1008-1020
109. Wareham KA, Lyon MF, Glenister PH, Williams ED (1987) Age-related reactivation of an X-linked gene. Nature 327:725-727
110. Bennett-Baker PE, Wilkowski J, Burke DT (2003) Age-associated activation of epigenetically repressed genes in the mouse. Genetics 165:2055-2062
111. Carrel L, Willard HF (2005) X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434:400-404
112. Fu VX, Dobosy JR, Desotelle JA, Almassi N, Ewald JA, Srinivasan R et al (2008) Aging and cancer-related loss of insulin-like growth factor 2 imprinting in the mouse and human prostate. Cancer Res 68:6797-6802
113. Sandovici I, Leppert M, Hawk PR, Suarez A, Linares Y, Sapienza C (2003) Familial aggregation of abnormal methylation of parental alleles at the IGF2/H19 and IGF2R differentially methylated regions. Hum Mol Genet 12:1569-1578
114. Schneider E, Pliushch G, El Hajj N, Galetzka D, Puhl A, Schorsch M et al (2010) Spatial, temporal and interindividual epigenetic variation of functionally important DNA methylation patterns. Nucleic Acids Res 38:3880-3890
115. Frost JM, Monk D, Stojilkovic-Mikic T, Woodfine K, Chitty LS, Murrell A et al (2010) Evaluation of allelic expression of imprinted genes in adult human blood. PLoS One 5:e13556
116. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML et al (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 102:10604-10609
117. Grönniger E, Weber B, Heil O, Peters N, Stäb F, Wenck H et al (2010) Aging and chronic sun exposure cause distinct epigenetic changes in human skin. PLoS Genet 6:e1000971
118. Daxinger L, Whitelaw E (2010) Transgenerational epigenetic inheritance: more questions than answers. Genome Res 20:1623-1628
119. Skinner MK, Manikkam M, Guerrero-Bosagna C (2011) Epigenetic transgenerational actions of endocrine disruptors. Reprod Toxicol 31:337-343
120. Morgan HD, Sutherland HG, Martin DI, Whitelaw E (1999) Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 23:314-318
121. Blewitt ME, Vickaryous NK, Paldi A, Koseki H, Whitelaw E (2006) Dynamic reprogramming of DNA methylation at an epigenetically sensitive allele in mice. PLoS Genet 2:e49
122. Anway MD, Cupp AS, Uzumcu M, Skinner MK (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466-1469
123. Guerrero-Bosagna C, Settles M, Lucker B, Skinner MK (2010) Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS One 5:e13100
124. Kaati G, Bygren LO, Edvinsson S (2002) Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period. Eur J Hum Genet 10:682-688
125. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjöström M et al (2006) Sexspecifi c, male-line transgenerational responses in humans. Eur J Hum Genet 14:159-166
126. Teperino R, Schoonjans K, Auwerx J (2010) Histone methyl transferases and demethylases; can they link metabolism and transcription? Cell Metab 1:321-327
127. Waterland RA, Jirtle RL (2003) Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23:5293-5300
128. Cropley JE, Suter CM, Beckman KB, Martin DI (2006) Germ-line epigenetic modification of the murine Avy allele by nutritional supplementation. Proc Natl Acad Sci USA 103:17308-17312
129. Waterland RA, Travisano M, Tahiliani KG (2007) Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. FASEB J 21:3380-3385
130. Waterland RA, Kellermayer R, Laritsky E, Rayco-Solon P, Harris RA, Travisano M et al (2010) Season of conception in rural gambia affects DNA methylation at putative human metastable epialleles. PLoS Genet 6:e1001252
131. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES et al (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA 105:17046-17049
132. Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD et al (2009) DNA methylation differences after exposure to prenatal famine are common and timing-and sex-specific. Hum Mol Genet 18:4046-4053
133. Anway MD, Rekow SS, Skinner MK (2008) Transgenerational epigenetic programming of the embryonic testis transcriptome. Genomics 91:30-40
134. Richards EJ (2009) Quantitative epigenetics: DNA sequence variation need not apply. Genes Dev 23:1601-1605