Epigenetics: Definition, mechanisms and clinical perspective

Seminars in Reproductive Medicine

Volumn 27, Issue 5, 2009, Pages 351-357

  Dupont, Cathérine ^a   Armant, D Randall ^a,b   Brenner, Carol A ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Epigenetics; Imprinting; Transgenerational inheritance; X chromosome inactivation

Indexed keywords

DNA; RNA;

CELL MATURATION; COW; EMBRYO DEVELOPMENT; EMBRYO TRANSFER; EPIGENETICS; FERTILIZATION IN VITRO; GENETIC DISORDER; GERM CELL; HUMAN; REVIEW; X CHROMOSOME INACTIVATION;

CHROMOSOME ABERRATIONS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC DISEASES, INBORN; GENOMIC IMPRINTING; HUMANS; INHERITANCE PATTERNS; MALE; REPRODUCTION; REPRODUCTIVE TECHNIQUES, ASSISTED; X CHROMOSOME INACTIVATION;

EID: 69349098474     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0029-1237423     Document Type: Review

References (91)

1. Waddington CH. The epigenotype. Endeavour 1942;1: 18-20
2. Waddington CH. The Basic Ideas of Biology. Towards a Theoretical Biology. Edinburgh, Scotland: Edinburgh University Press; 1968:1-32
3. Wu Ct, Morris JR. Genes, genetics, and epigenetics: a correspondence. Science 2001;293(5532):1103-1105
4. Daskalos A, Nikolaidis G, Xinarianos G, et al. Hypomethylation of retrotransposable elements correlates with genomic instability in non-small cell lung cancer. Int J Cancer 2009; 124(1):81-87
5. Zaratiegui M, Irvine DV, Martienssen RA. Noncoding RNAs and gene silencing. Cell 2007;128(4):763-776
6. Dodge JE, Okano M, Dick F, et al. Inactivation of Dnmt3b in mouse embryonic fibroblasts results in DNA hypomethylation, chromosomal instability, and spontaneous immortalization. J Biol Chem 2005;280(18):17986-17991 (Pubitemid 41389041)
7. Hotchkiss RD. The quantitative separation of purines, pyrimidines, and nucleosides by paper chromatography. J Biol Chem 1948;175(1):315-332
8. Griffith JS, Mahler HR. DNA ticketing theory of memory. Nature 1969;223(5206):580-582
9. Ratel D, Ravanat JL, Berger F, Wion D. N6-methyladenine: the other methylated base of DNA. Bioessays 2006;28(3): 309-315
10. Sinsheimer RL. The action of pancreatic deoxyribonuclease. II. Isomeric dinucleotides. J Biol Chem 1955;215(2):579-583
11. Woodcock DM, Crowther PJ, Diver WP. The majority of methylated deoxycytidines in human DNA are not in the CpG dinucleotide. Biochem Biophys Res Commun 1987; 145(2):888-894
12. Nyce J, Liu L, Jones PA. Variable effects of DNA-synthesis inhibitors upon DNA methylation in mammalian cells. Nucleic Acids Res 1986;14(10):4353-4367 (Pubitemid 17189635)
13. Ramsahoye BH, Biniszkiewicz D, Lyko F, Clark V, Bird AP, Jaenisch R. Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc Natl Acad Sci U S A 2000;97(10):5237-5242 (Pubitemid 30313702)
14. Naveh-Many T, Cedar H. Active gene sequences are undermethylated. Proc Natl Acad Sci U S A 1981;78(7): 4246-4250 (Pubitemid 11010310)
15. Waechter DE, Baserga R. Effect of methylation on expression of microinjected genes. Proc Natl Acad Sci U S A 1982; 79(4):1106-1110
16. Watt F, Molloy PL. Cytosine methylation prevents binding to DNA of a HeLa cell transcription factor required for optimal expression of the adenovirus major late promoter. Genes Dev 1988;2(9):1136-1143
17. Boyes J, Bird A. DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell 1991; 64(6):1123-1134 (Pubitemid 121001199)
18. Hendrich B, Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 1998;18(11):6538-6547 (Pubitemid 28500543)
19. Jones PL, Veenstra GJ, Wade PA, et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 1998;19(2):187-191 (Pubitemid 28248804)
20. Nan X, Ng HH, Johnson CA, et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998;393 (6683): 386-389 (Pubitemid 28269714)
21. Leonhardt H, Page AW, Weier HU, Bestor TH. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 1992;71(5): 865-873
22. Smith SS, Kaplan BE, Sowers LC, Newman EM. Mechanism of human methyl-directed DNA methyltransferase and the fidelity of cytosine methylation. Proc Natl Acad Sci U S A 1992;89(10):4744-4748
23. Bestor T, Laudano A, Mattaliano R, Ingram V. Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J Mol Biol 1988;203(4):971-983 (Pubitemid 18269490)
24. Okano M, Xie S, Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 1998;19(3):219-220 (Pubitemid 28309328)
25. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999;99(3): 247-257 (Pubitemid 29519904)
26. Kaneda M, Okano M, Hata K, et al. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 2004;429(6994):900-903 (Pubitemid 38843304)
27. Klose RJ, Bird AP. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 2006;31(2):89-97 (Pubitemid 43221841)
28. Perche PY, Robert-Nicoud M, Khochbin S, Vourc'h C. Nucleosome differentiation: role of histone H2A variants [in French]. Med Sci (Paris) 2003;19(11):1137-1145
29. Redon C, Pilch D, Rogakou E, Sedelnikova O, Newrock K, Bonner W. Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev 2002;12(2):162-169 (Pubitemid 34219488)
30. Hake SB, Allis CD. Histone H3 variants and their potential role in indexing mammalian genomes: the "H3 barcode hypothesis". Proc Natl Acad Sci U S A 2006;103(17):6428-6435
31. Phillips DM, Johns EW. A fractionation of the histones of group F2a from calf thymus. Biochem J 1965;94:127-130
32. Kornberg RD. Chromatin structure: a repeating unit of histones and DNA. Science 1974;184(139):868-871
33. Kouzarides T. Chromatin modifications and their function. Cell 2007;128(4):693-705
34. Marmorstein R, Trievel RC. Histone modifying enzymes: structures, mechanisms, and specificities. Biochim Biophys Acta 2009;1789(1):58-68
35. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000;403(6765):41-45
36. Pogo BG, Allfrey VG, Mirsky AE. RNA synthesis and histone acetylation during the course of gene activation in lymphocytes. Proc Natl Acad Sci U S A 1966;55(4):805-812
37. Allfrey VG, Faulkner R, Mirsky AE. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc Natl Acad Sci U S A 1964;51:786-794
38. Sealy L, Chalkley R. DNA associated with hyperacetylated histone is preferentially digested by DNase I. Nucleic Acids Res 1978;5(6):1863-1876 (Pubitemid 8350960)
39. Hong L, Schroth GP, Matthews HR, Yau P, Bradbury EM. Studies of the DNA binding properties of histone H4 amino terminus. Thermal denaturation studies reveal that acetylation markedly reduces the binding constant of the H4 "tail" to DNA. J Biol Chem 1993;268(1):305-314
40. Norton VG, Imai BS, Yau P, Bradbury EM. Histone acetylation reduces nucleosome core particle linking number change. Cell 1989;57(3):449-457 (Pubitemid 19126278)
41. Sims RJ III, Nishioka K, Reinberg D. Histone lysine methylation: a signature for chromatin function. Trends Genet 2003;19(11):629-639 (Pubitemid 37338383)
42. Parra MA,Wyrick JJ. Regulation of gene transcription by the histone H2A N-terminal domain. Mol Cell Biol 2007; 27(21):7641-7648
43. Parra MA, Kerr D, Fahy D, Pouchnik DJ, Wyrick JJ. Deciphering the roles of the histone H2B N-terminal domain in genome-wide transcription. Mol Cell Biol 2006; 26(10):3842-3852 (Pubitemid 43726401)
44. Weinberg MS, Villeneuve LM, Ehsani A, et al. The antisense strand of small interfering RNAs directs histone methylation and transcriptional gene silencing in human cells. RNA 2006;12(2):256-262 (Pubitemid 43121930)
45. Han J, Kim D, Morris KV. Promoter-associated RNA is required for RNA-directed transcriptional gene silencing in human cells. Proc Natl Acad Sci U S A 2007;104(30):12422-12427 (Pubitemid 47206153)
46. Kim DH, Villeneuve LM, Morris KV, Rossi JJ. Argonaute- 1 directs siRNA-mediated transcriptional gene silencing in human cells. Nat Struct Mol Biol 2006; 13(9):793-797 (Pubitemid 44338773)
47. Köhler C, Villar CB. Programming of gene expression by Polycomb group proteins. Trends Cell Biol 2008;18(5):236-243
48. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 2004;116(1):51-61 (Pubitemid 38156183)
49. Henikoff S, Furuyama T, Ahmad K. Histone variants, nucleosome assembly and epigenetic inheritance. Trends Genet 2004;20(7):320-326 (Pubitemid 38798541)
50. Payer B, Lee JT. X chromosome dosage compensation: how mammals keep the balance. Annu Rev Genet 2008;42:733-772
51. Huynh KD, Lee JT. X-chromosome inactivation: a hypothesis linking ontogeny and phylogeny. Nat Rev Genet 2005;6(5):410-418
52. Adler DA, Rugarli EI, Lingenfelter PA, et al. Evidence of evolutionary up-regulation of the single active X chromosome in mammals based on Clc4 expression levels in Mus spretus and Mus musculus. Proc Natl Acad Sci U S A 1997; 94(17):9244-9248
53. Lyon MF. Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 1961;190:372-373
54. Sharman GB. Late DNA replication in the paternally derived X chromosome of female kangaroos. Nature 1971;230(5291): 231-232
55. Cooper DW, VandeBerg JL, Sharman GB, Poole WE. Phosphoglycerate kinase polymorphism in kangaroos provides further evidence for paternal X inactivation. Nat New Biol 1971;230(13):155-157
56. Huynh KD, Lee JT. Inheritance of a pre-inactivated paternal X chromosome in early mouse embryos. Nature 2003; 426(6968):857-862
57. Takagi N, Sasaki M. Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse. Nature 1975;256(5519):640-642
58. Sado T, Fenner MH, Tan SS, Tam P, Shioda T, Li E. X inactivation in the mouse embryo deficient for Dnmt1: distinct effect of hypomethylation on imprinted and random X inactivation. Dev Biol 2000;225(2):294-303 (Pubitemid 30745932)
59. Wang J, Mager J, Chen Y, et al. Imprinted X inactivation maintained by a mouse Polycomb group gene. Nat Genet 2001;28(4):371-375 (Pubitemid 32702428)
60. Heard E, Disteche CM. Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev 2006;20(14):1848-1867 (Pubitemid 44079323)
61. Lifschytz E, Lindsley DL. The role of X-chromosome inactivation during spermatogenesis (Drosophila-allocyclychromosome evolution-male sterility-dosage compensation). Proc Natl Acad Sci U S A 1972;69(1):182-186
62. Okamoto I, Arnaud D, Le Baccon P, et al. Evidence for de novo imprinted X-chromosome inactivation independent of meiotic inactivation in mice. Nature 2005;438(7066):369-373 (Pubitemid 41643954)
63. van der Heijden GW, Dieker JW, Derijck AA, et al. Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech Dev 2005;122(9):1008-1022
64. Tada T, Obata Y, Tada M, et al. Imprint switching for nonrandom X-chromosome inactivation during mouse oocyte growth. Development 2000;127(14):3101-3105 (Pubitemid 30611902)
65. Norris DP, Patel D, Kay GF, et al. Evidence that random and imprinted Xist expression is controlled by preemptive methylation. Cell 1994;77(1):41-51 (Pubitemid 24184686)
66. Surani MA, Barton SC, Norris ML. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 1984;308(5959):548-550
67. McGrath J, Solter D. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 1984; 37(1):179-183 (Pubitemid 14079849)
68. Bartolomei MS, Zemel S, Tilghman SM. Parental imprinting of the mouse H19 gene. Nature 1991;351(6322):153-155 (Pubitemid 21896555)
69. Barlow DP, Stöger R, Herrmann BG, Saito K, Schweifer N. The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the Tme locus. Nature 1991; 349(6304):84-87 (Pubitemid 21912022)
70. DeChiara TM, Robertson EJ, Efstratiadis A. Parental imprinting of the mouse insulin-like growth factor II gene. Cell 1991;64(4):849-859 (Pubitemid 121001171)
71. Wilkins JF, Haig D. What good is genomic imprinting: the function of parent-specific gene expression. Nat Rev Genet 2003;4(5):359-368 (Pubitemid 36538360)
72. Spahn L, Barlow DP. An ICE pattern crystallizes. Nat Genet 2003;35(1):11-12
73. Obata Y, Kaneko-Ishino T, Koide T, et al. Disruption of primary imprinting during oocyte growth leads to the modified expression of imprinted genes during embryogenesis. Development 1998;125(8):1553-1560 (Pubitemid 28239365)
74. Davis TL, Yang GJ, McCarrey JR, Bartolomei MS. The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum Mol Genet 2000;9(19):2885-2894
75. Ueda T, Abe K, Miura A, et al. The paternal methylation imprint of the mouse H19 locus is acquired in the gonocyte stage during foetal testis development. Genes Cells 2000; 5(8):649-659 (Pubitemid 30641957)
76. Li JY, Lees-Murdock DJ, Xu GL, Walsh CP. Timing of establishment of paternal methylation imprints in the mouse. Genomics 2004;84(6):952-960
77. Lucifero D, Mann MR, Bartolomei MS, Trasler JM. Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet 2004;13(8):839-849 (Pubitemid 38515213)
78. Hiura H, Obata Y, Komiyama J, Shirai M, Kono T. Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells 2006;11(4):353-361
79. Lee JT. Molecular links between X-inactivation and autosomal imprinting: X-inactivation as a driving force for the evolution of imprinting? Curr Biol 2003;13(6):R242-R254
80. Dean W, Santos F, Reik W. Epigenetic reprogramming in early mammalian development and following somatic nuclear transfer. Semin Cell Dev Biol 2003;14(1):93-100 (Pubitemid 36259940)
81. Nakamura T, Arai Y, Umehara H, et al. PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat Cell Biol 2007;9(1):64-71 (Pubitemid 46024198)
82. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 1999;23(3):314-318 (Pubitemid 29526429)
83. Lane N, Dean W, Erhardt S, et al. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 2003;35(2): 88-93 (Pubitemid 36330631)
84. Maher ER, Afnan M, Barratt CL. Epigenetic risks related to assisted reproductive technologies: epigenetics, imprinting, ART and icebergs? Hum Reprod 2003;18(12):2508-2511
85. Barker DJ. Intrauterine programming of coronary heart disease and stroke. Acta Paediatr Suppl 1997;423:178-182; discussion 183
86. Doherty AS, Mann MR, Tremblay KD, Bartolomei MS, Schultz RM. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod 2000;62(6):1526-1535
87. Li T, Vu TH, Ulaner GA, et al. IVF results in de novo DNA methylation and histone methylation at an Igf2-H19 imprinting epigenetic switch. Mol Hum Reprod 2005;11(9): 631-640 (Pubitemid 41672242)
88. Khosla S, Dean W, Brown D, Reik W, Feil R. Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol Reprod 2001; 64(3):918-926 (Pubitemid 32174065)
89. Khosla S, Dean W, Reik W, Feil R. Culture of preimplantation embryos and its long-term effects on gene expression and phenotype. Hum Reprod Update 2001;7(4): 419-427 (Pubitemid 32655328)
90. Wu Q, Ohsako S, Ishimura R, Suzuki JS, Tohyama C. Exposure of mouse preimplantation embryos to 2,3,7,8- tetrachlorodibenzo-p-dioxin (TCDD) alters the methylation status of imprinted genes H19 and Igf2. Biol Reprod 2004; 70(6):1790-1797
91. Shao WJ, Tao LY, Xie JY, Gao C, Hu JH, Zhao RQ. Exposure of preimplantation embryos to insulin alters expression of imprinted genes. Comp Med 2007;57(5):482-486 (Pubitemid 351773342)