Can our understanding of epigenetics assist with primary prevention of congenital defects?

Journal of Medical Genetics

Volumn 47, Issue 2, 2010, Pages 73-80

  Martínez Frías, María Luisa ^a,b  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; DIETHYLSTILBESTROL; ENDOCRINE DISRUPTOR; HISTONE DEACETYLASE INHIBITOR; HYDRALAZINE; METHOXYCHLOR; PROCAINAMIDE; VINCLOZOLIN;

CONGENITAL DISORDER; DNA METHYLATION; EMBRYO DEVELOPMENT; EPIGENETICS; FETUS DEVELOPMENT; GENE EXPRESSION; GERM CELL; INFERTILITY THERAPY; NUTRITIONAL DEFICIENCY; PRIMARY PREVENTION; PRIORITY JOURNAL; REVIEW; SOMATIC CELL;

CONGENITAL ABNORMALITIES; ENVIRONMENT; EPIGENESIS, GENETIC; FEMALE; GENOMIC IMPRINTING; HUMANS; MALE; PREGNANCY;

EID: 77349103259     PISSN: 00222593     EISSN: 14686244     Source Type: Journal    
DOI: 10.1136/jmg.2009.070466     Document Type: Review

References (99)

1. Czeizel A. What proportion of congenital abnormalitites can be prevented? BMJ 1993;306:499-503.
2. Huddart SN, Bianchi A, Doig CM, Dickson AP. Preventing congenital abnormalities. BMJ 1993;306:857.
3. Saunders P. Preventing congenital abnormalities. BMJ 1993;306:857.
4. Martínez-Frías ML. Genetic drift. The balance of nature: reflections on the physics and mathematics structure of the living world and the human genome. Am J Med Genet A 2008;146A:1781-7.
5. Zamudio NM, Chong S, O'Bryan MK. Epigenetic regulation in male germ cells. Reproduction 2008;136:131-46.
6. Shahbazian MD, Grunstein M. Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 2007;76:75-100.
7. Cheung P, Lau P. Epigenetic regulation by histone methylation and histone variants. Mol Endocrinol 2005;19:563-73.
8. Varga-Weisz PD, Becker PB. Regulation of higher-order chromatin structures by nucleosome-remodelling factors. Curr Opin Genet Dev 2006;16:151-6.
9. Kouzarides T. Chromatin modifications and their function. Cell 2007;128:693-705.
10. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008;9:102-14.
11. Seila AC, Sharp PA. Small RNAs tell big stories in Whistler. Nat Cell Biol 2008;10:630-3.
12. Hayashi K, Chuva de Sousa Lopes SM, Kaneda M, Tang F, Hajkova P, Lao K, O'Carroll D, Das PP, Tarakhovsky A, Miska EA, Surani MA. MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS One 2008;3: e1738.
13. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S, Hodges E, Anger M, Sachidanandam R, Schultz RM, Hannon GJ. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008;453:534-8.
14. Horsthemke B, Buiting K. Genomic imprinting and imprinting defects in humans. Adv Genet 2008;61:225-46.
15. Duncan EM, Muratore-Schroeder TL, Cook RG, Garcia BA, Shabanowitz J, Hunt DF, Allis CD. Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation. Cell 2008;135:284-94.
16. Santos-Rosa H, Kirmizis A, Nelson C, Bartke T, Saksouk N, Cote J, Kouzarides T. Histone H3 tail clipping regulates gene expression. Nat Struct Mol Biol 2009;16:17-22.
17. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002;16:6-21.
18. Costello JF, Plass C. Methylation matters. J Med Genet 2001;38:285-303.
19. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin SP, Allis CD, Cheng X, Bestor TH. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007;448:714-17.
20. Song F, Mahmood S, Ghosh S, Liang P, Smiraglia DJ, Nagase H, Held WA. Tissue specific differentially methylated regions (TDMR): Changes in DNA methylation during development. Genomics 2009;93:130-9.
21. Brown SE, Suderman MJ, Hallett M, Szyf M. DNA demethylation induced by the methyl-CpG-binding domain protein MBD3. Gene 2008;420:99-106.
22. Rountree MR, Bachman KE, Baylin SB. DNMT1 binds HDAC2 and a new corepressor, DMAP1, to form a complex at replication foci. Nat Genet 2000;25:269-77.
23. Dean W, Santos F, Reik W. Epigenetic reprogramming in early mammalian development and following somatic nuclear transfer. Semin Cell Dev Biol 2003;14:93-100.
24. Morgan HD, Santos F, Green K, Dean W, Reik W. Epigenetic reprogramming in mammals. Hum Mol Genet 2005;1:R47-58.
25. Kangaspeska S, Stride B, Métivier R, Polycarpou-Schwarz M, Ibberson D, Carmouche RP, Benes V, Gannon F, Reid G. Transient cyclical methylation of promoter DNA. Nature 2008;452:112-15.
26. Métivier R, Gallais R, Tiffoche C, Le Péron C, Jurkowska RZ, Carmouche RP, Ibberson D, Barath P, Demay F, Reid G, Benes V, Jeltsch A, Gannon F, Salbert G. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008;452:45-50.
27. Ooi SK, Bestor TH. The colorful history of active DNA demethylation. Cell 2008;133:1145-8.
28. Szyf M, McGowan P, Meaney MJ. The social environment and the epigenome. Environ Mol Mutagen 2008;49:46-60.
29. Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 2008;9:129- 40.
30. Miller CA, Sweatt JD. Covalent modification of DNA regulates memory formation [correction appears in Neuron 2008;59:1051]. Neuron 2007;53:857-69.
31. Edwards RG. Genetics, epigenetics, and gene silencing in differentiating mammalian embryos. Reprod Biomed Online 2006;13:732-53.
32. Bultman SJ, Gebuhr TC, Pan H, Svoboda P, Schultz RM, Magnuson T. Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev 2006;20:1744-54.
33. Torres-Padilla ME, Zernicka-Goetz M. Role of TIF1alpha as a modulator of embryonic transcription in the mouse zygote. J Cell Biol 2006;174:329-38.
34. Wang QT, Piotrowska K, Ciemerych MA, Milenkovic L, Scott MP, Davis RW, Zernicka-Goetz M. A genome-wide study of gene activity reveals developmental signaling pathways in the preimplantation mouse embryo. Dev Cell 2004;6:133-44.
35. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, Rossant J. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 2005;123:917-29.
36. Gardner RL. The early blastocyst is bilaterally symmetrical and its axis of symmetry is aligned with the animal-vegetal axis of the zygote in the mouse. Development 1997;124:289-301.
37. Zernicka-Goetz M. Cleavage pattern and emerging asymmetry of the mouse embryo. Nat Rev Mol Cell Biol 2005;6:919-28.
38. Plusa B, Grabarek JB, Piotrowska K, Glover DM, Zernicka-Goetz M. Site of the previous meiotic division defines cleavage orientation in the mouse embryo [correction appears in Nat Cell Biol 2002;4:912]. Nat Cell Biol 2002;4:811-15.
39. Piotrowska K, Wianny F, Pedersen RA, Zernicka-Goetz M. Blastomeres arising from the first cleavage division have distinguishable fates in normal mouse development. Development 2001;128:3739-48.
40. Plusa B, Hadjantonakis AK, Gray D, Piotrowska-Nitsche K, Jedrusik A, Papaioannou VE, Glover DM, Zernicka-Goetz M. The first cleavage of the mouse zygote predicts the blastocyst axis. Nature 2005;434:391-5.
41. Zernicka-Goetz M. The first cell-fate decisions in the mouse embryo: destiny is a matter of both chance and choice. Curr Opin Genet Dev 2006;16:406-12.
42. Gardner RL. The axis of polarity of the mouse blastocyst is specified before blastulation and independently of the zona pellucida. Hum Reprod 2007;22:798-806.
43. Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 2007;445:214-18.
44. Ratnam S, Mertineit C, Ding F, Howell CY, Clarke HJ, Bestor TH, Chaillet JR, Trasler JM. Dynamics of Dnmt1 methyltransferase expression and intracellular localization during oogenesis and preimplantation development. Dev Biol 2002;245:304-14.
45. Cirio MC, Ratnam S, Ding F, Reinhart B, Navara C, Chaillet JR. Preimplantation expression of the somatic form of Dnmt1 suggests a role in the inheritance of genomic imprints. BMC Dev Biol 2008;8:9.
46. Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, Beck F, Rossant J. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 2005;132:2093-102.
47. Jedrusik A, Parfitt DE, Guo G, Skamagki M, Grabarek JB, Johnson MH, Robson P, Zernicka-Goetz M. Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo. Genes Dev 2008;22:2692-706.
48. Bischoff M, Parfitt DE, Zernicka-Goetz M. Formation of the embryonic-abembryonic axis of the mouse blastocyst: relationships between orientation of early cleavage divisions and pattern of symmetric/asymmetric divisions. Development 2008;135:953-62.
49. Reik W, Dean W. DNA methylation and mammalian epigenetics. Electrophoresis 2001;22:2838-43.
50. Santos F, Hendrich B, Reik W, Dean W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 2002;241:172-82.
51. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 2002;3:662-73.
52. Seki Y, Hayashi K, Itoh K, Mizugaki M, Saitou M, Matsui Y. Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev Biol 2005;278:440-58.
53. Seki Y, Yamaji M, Yabuta Y, Sano M, Shigeta M, Matsui Y, Saga Y, Tachibana M, Shinkai Y, Saitou M. Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice. Development 2007;134:2627-38.
54. Hiramatsu R, Matoba S, Kanai-Azuma M, Tsunekawa N, Katoh-Fukui Y, Kurohmaru M, Morohashi K, Wilhelm D, Koopman P, Kanai Y. A critical time window of Sry action in gonadal sex determination in mice. Development 2009;136:129-38.
55. Bromfield J, Messamore W, Albertini DF. Epigenetic regulation during mammalian oogenesis. Reprod Fertil Dev 2008;20:74-80.
56. Wassarman PM, Litscher ES. Mammalian fertilization: the egg's multifunctional zona pellucida. Int J Dev Biol 2008;52:665-76.
57. Wassarman PM, Litscher ES. Mammalian fertilization is dependent on multiple membrane fusion events. Methods Mol Biol 2008;475:99- 113.
58. Zheng J, Xia X, Ding H, Yan A, Hu S, Gong X, Zong S, Zhang Y, Sheng HZ. Erasure of the paternal transcription program during spermiogenesis: the first step in the reprogramming of sperm chromatin for zygotic development [correction appears in Dev Dyn 2008;237:2279-81]. Dev Dyn 2008;237:1463-76.
59. Detich N, Bovenzi V, Szyf M. Valproate induces replication-independent active demethylation. J Biol Chem 2003;278:27586-92.
60. Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J, Thurston A, Huntley JF, Rees WD, Maloney CA, Lea RG, Craigon J, McEvoy TG, Young LE. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci U S A 2007;104:19351-6.
61. Schaefer CB, Ooi SK, Bestor TH, Bourćhis D. Epigenetic decisions in mammalian germ cells. Science 2007;316:398-9.
62. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 1999;23:314-18.
63. Day JK, Bauer AM, DesBordes C, Zhuang Y, Kim BE, Newton LG, Nehra V, Forsee KM, MacDonald RS, Besch-Williford C, Huang TH, Lubahn DB. Genistein alters methylation patterns in mice. J Nutr 2002;132(8 Suppl):2419S-23S.
64. Bruniquel D, Schwartz RH. Selective, stable demethylation of the interleukin-2 gene enhances transcription by an active process. Nat Immunol 2003; 4:235-40.
65. Szyf M. The dynamic epigenome and its implications in toxicology. Toxicol Sci 2007;100:7-23.
66. Mackay DJ, Boonen SE, Clayton-Smith J, Goodship J, Hahnemann JM, Kant SG, Njølstad PR, Robin NH, Robinson DO, Siebert R, Shield JP, White HE, Temple IK. A maternal hypomethylation syndrome presenting as transient neonatal diabetes mellitus. Hum Genet 2006;120:262-9.
67. Mackay DJ, Callaway JL, Marks SM, White HE, Acerini CL, Boonen SE, Dayanikli P, Firth HV, Goodship JA, Haemers AP, Hahnemann JM, Kordonouri O, Masoud AF, Oestergaard E, Storr J, Ellard S, Hattersley AT, Robinson DO, Temple IK. Hypomethylation of multiple imprinted loci in individuals with transient neonatal diabetes is associated with mutations in ZFP57. Nat Genet 2008;40:949-51.
68. Barker DJ, Eriksson JG, Forsén T, Osmond C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 2002;31:1235-9.
69. Huang WW, Yin Y, Bi Q, Chiang TC, Garner N, Vuoristo J, McLachlan JA, Ma L. Developmental diethylstilbestrol exposure alters genetic pathways of uterine cytodifferentiation. Mol Endocrinol 2005;19:669-82.
70. Brouwers MM, Feitz WF, Roelofs LA, Kiemeney LA, de Gier RP, Roeleveld N. Hypospadias: a transgenerational effect of diethylstilbestrol? Hum Reprod 2006;21:666-9.
71. Troisi R, Hatch EE, Titus-Ernstoff L, Hyer M, Palmer JR, Robboy SJ, Strohsnitter WC, Kaufman R, Herbst AL, Hoover RN. Cancer risk in women prenatally exposed to diethylstilbestrol. Int J Cancer 2007;121:356-60.
72. Palmer JR, Wise LA, Hatch EE, Troisi R, Titus-Ernstoff L, Strohsnitter W, Kaufman R, Herbst AL, Noller KL, Hyer M, Hoover RN. Prenatal diethylstilbestrol exposure and risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2006;15:1509-14.
73. Newbold RR, Padilla-Banks E, Jefferson WN. Adverse effects of the model environmental estrogen diethylstilbestrol are transmitted to subsequent generations. Endocrinology 2006;147(6 Suppl):S11-17.
74. Block K, Kardana A, Igarashi P, Taylor HS. In utero diethylstilbestrol (DES) exposure alters Hox gene expression in the developing müllerian system. FASEB J 2000;14:1101-8.
75. Eun Kwon H, Taylor HS. The role of HOX genes in human implantation. Ann N Y Acad Sci 2004;1034:1-18.
76. Akbas GE, Song J, Taylor HS. A HOXA10 estrogen response element (ERE) is differentially regulated by 17 beta-estradiol and diethylstilbestrol (DES). J Mol Biol 2004;340:1013-23.
77. Nilsson EE, Anway MD, Stanfield J, Skinner MK. Transgenerational epigenetic effects of the endocrine disruptor vinclozolin on pregnancies and female adult onset disease. Reproduction 2008;135:713-21.
78. Anway MD, Skinner MK. Epigenetic programming of the germ line: effects of endocrine disruptors on the development of transgenerational disease. Reprod Biomed Online 2008;16:23-5.
79. Vine MF, Setzer RW Jr, Everson RB, Wyrobek AJ. Human sperm morphometry and smoking, caffeine, and alcohol consumption. Reprod Toxicol 1997;11:179-84.
80. Frazier LM. Reproductive disorders associated with pesticide exposure. J Agromedicine 2007;12:27-37.
81. Skinner MK, Anway MD. Seminiferous cord formation and germ-cell programming: epigenetic transgenerational actions of endocrine disruptors. Ann N Y Acad Sci 2005;1061:18-32.
82. Gurvich N, Berman MG, Wittner BS, Gentleman RC, Klein PS, Green JB. Association of valproate-induced teratogenesis with histone deacetylase inhibition in vivo. FASEB J 2005;19:1166-8.
83. Menegola E, Di Renzo F, Broccia ML, Giavini E. Inhibition of histone deacetylase as a new mechanism of teratogenesis. Birth Defects Res C Embryo Today 2006;78:345-53.
84. Milutinovic S, D'Alessio AC, Detich N, Szyf M. Valproate induces widespread epigenetic reprogramming which involves demethylation of specific genes. Carcinogenesis 2007;28:560-71.
85. Hunt S, Russell A, Smithson WH, Parsons L, Robertson I, Waddell R, Irwin B, Morrison PJ, Morrow J, Craig J, UK Epilepsy and Pregnancy Register. Topiramate in pregnancy: preliminary experience from the UK Epilepsy and Pregnancy Register. Neurology 2008;71:272-6.
86. Martínez-Frías ML. Topiramate in pregnancy: Preliminary experience from the UK epilepsy and pregnancy register. Neurology 2009;72:2054-5.
87. Zhang B, Huang T, Liu K, Chen J, Wang G. Effects of 5-Aza-CdR on cell proliferation of breast cancer cell line MDA-MB-435S and expression of maspin gene. J Huazhong Univ Sci Technolog Med Sci 2007;27:543-6.
88. Balada E, Ordi-Ros J, Serrano-Acedo S, Martinez-Lostao L, Vilardell-Tarrés M. Transcript overexpression of the MBD2 and MBD4 genes in CD4+ T cells from systemic lupus erythematosus patients. J Leukoc Biol 2007;81:1609-16.
89. Cornacchia E, Golbus J, Maybaum J, Strahler J, Hanash S, Richardson B. Hydralazine and procainamide inhibit T cell DNA methylation and induce autoreactivity. J Immunol 1988;140:2197-200.
90. Simmons RA. Developmental origins of diabetes: the role of epigenetic mechanisms. Curr Opin Endocrinol Diabetes Obes 2007;14:13-16.
91. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suñer D, Cigudosa JC, Urioste M, Benitez J, Boix-Chornet M, Sanchez-Aguilera A, Ling C, Carlsson E, Poulsen P, Vaag A, Stephan Z, Spector TD, Wu YZ, Plass C, Esteller M. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A 2005;102:10604-9.
92. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A 2008;105:17046-9.
93. Painter RC, Osmond C, Gluckman P, Hanson M, Phillips DI, Roseboom TJ. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 2008;115:1243-9.
94. Lam PK, Torfs CP. Interaction between maternal smoking and malnutrition in infant risk of gastroschisis. Birth Defects Res A Clin Mol Teratol 2006; 76:182-6.
95. Rossignol S, Steunou V, Chalas C, Kerjean A, Rigolet M, Viegas-Pequignot E, Jouannet P, Le Bouc Y, Gicquel C. The epigenetic imprinting defect of patients with Beckwith-Wiedemann syndrome born after assisted reproductive technology is not restricted to the 11p15 region. J Med Genet 2006;43:902-7.
96. Kagami M, Nagai T, Fukami M, Yamazawa K. Ogata T.Silver-Russell syndrome in a girl born after in vitro fecundation: partial hypermethylation at the differentially methylated region of PEG1/MEST. J Assist Reprod Genet 2007;24:131-6.
97. Kurihara Y, Kawamura Y, Uchijima Y, Amamo T, Kobayashi H, Asano T, Kurihara H. Maintenance of genomic methylation patterns during preimplantation development requires the somatic form of DNA methyltransferase 1. Dev Biol 2008;313:335-46.
98. Weksberg R, Shuman C, Caluseriu O, Smith AC, Fei YL, Nishikawa J, Stockley TL, Best L, Chitayat D, Olney A, Ives E, Schneider A, Bestor TH, Li M, Sadowski P, Squire J. Discordant KCNQ1OT1 imprinting in sets of monozygotic twins discordant for Beckwith-Wiedemann syndrome. Hum Mol Genet 2002;11:1317-25.
99. Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM. A unique configuration of genome-wide DNA methylation patterns in the testis. Proc Natl Acad Sci U S A 2007;104:228-33.