Home Nutri-epigenomics: lifelong remodelling of our epigenomes by nutritional and metabolic factors and beyond
Article
Licensed
Unlicensed Requires Authentication

Nutri-epigenomics: lifelong remodelling of our epigenomes by nutritional and metabolic factors and beyond

  • Catherine Gallou-Kabani , Alexandre Vigé , Marie-Sylvie Gross and Claudine Junien
Published/Copyright: March 1, 2007
Become an author with De Gruyter Brill
Submit Manuscript Author Information
Clinical Chemistry and Laboratory Medicine (CCLM)
From the journal Volume 45 Issue 3

Abstract

The phenotype of an individual is the result of complex interactions between genotype, epigenome and current, past and ancestral environment, leading to lifelong remodelling of our epigenomes. Various replication-dependent and -independent epigenetic mechanisms are involved in developmental programming, lifelong stochastic and environmental deteriorations, circadian deteriorations, and transgenerational effects. Several types of sequences can be targets of a host of environmental factors and can be associated with specific epigenetic signatures and patterns of gene expression. Depending on the nature and intensity of the insult, the critical spatiotemporal windows and developmental or lifelong processes involved, these epigenetic alterations can lead to permanent changes in tissue and organ structure and function, or to reversible changes using appropriate epigenetic tools. Given several encouraging trials, prevention and therapy of age- and lifestyle-related diseases by individualised tailoring of optimal epigenetic diets or drugs are conceivable. However, these interventions will require intense efforts to unravel the complexity of these epigenetic, genetic and environment interactions and to evaluate their potential reversibility with minimal side effects.

Clin Chem Lab Med 2007;45:321–7.

Keywords: environment; epigenetics; fetal programming; metabolic syndrome; nutrition; transgenerational effects
:
Corresponding author: Claudine Junien, Inserm Unit 781, Clinique Maurice Lamy, porte 15, Hôpital Necker-Enfants Malades, 149 rue de Sèvres, 75743 Paris, France Phone: +33-1-44494479, Fax: +33-1-47833206,

References

1. Barker DJ. The fetal origins of diseases of old age. Eur J Clin Nutr1992;46(Suppl 3):S3–9.Search in Google Scholar

2. Feil R. Environmental and nutritional effects on the epigenetic regulation of genes. Mutat Res2006;600:46–57.10.1016/j.mrfmmm.2006.05.029Search in Google Scholar PubMed

3. Kroes HY, Takahashi M, Zijlstra RJ, Baert JA, Kooi KA, Hofstra RM, et al. Two cases of the caudal duplication anomaly including a discordant monozygotic twin. Am J Med Genet2002;112:390–3.10.1002/ajmg.10594Search in Google Scholar PubMed

4. Weksberg R, Shuman C, Caluseriu O, Smith AC, Fei YL, Nishikawa J, et al. Discordant KCNQ1OT1 imprinting in sets of monozygotic twins discordant for Beckwith-Wiedemann syndrome. Hum Mol Genet2002;11:1317–25.10.1093/hmg/11.11.1317Search in Google Scholar PubMed

5. Petronis A, Gottesman, II, Kan P, Kennedy JL, Basile VS, Paterson AD, et al. Monozygotic twins exhibit numerous epigenetic differences: clues to twin discordance? Schizophr Bull2003;29:169–78.10.1093/oxfordjournals.schbul.a006988Search in Google Scholar PubMed

6. Phillips DI, Hales CN, Barker DJ. Can twin studies assess the genetic component in type 2 (non-insulin-dependent) diabetes mellitus? Diabetologia1993;36:471–2.10.1007/BF00402287Search in Google Scholar PubMed

7. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA2005;102:10604–9.10.1073/pnas.0500398102Search in Google Scholar PubMed PubMed Central

8. Petronis A. Epigenetics and twins: three variations on the theme. Trends Genet2006;22:347–50.10.1016/j.tig.2006.04.010Search in Google Scholar PubMed

9. Sing CF, Stengard JH, Kardia SL. Genes, environment, and cardiovascular disease. Arterioscler Thromb Vasc Biol2003;23:1190–6.10.1161/01.ATV.0000075081.51227.86Search in Google Scholar PubMed

10. Rankinen T, Zuberi A, Chagnon YC, Weisnagel SJ, Argyropoulos G, Walts B, et al. The human obesity gene map: the 2005 update. Obesity (Silver Spring)2006;14:529–644.10.1038/oby.2006.71Search in Google Scholar PubMed

11. Gallou-Kabani C, Junien C. Nutritional epigenomics of metabolic syndrome. Diabetes2005;54:1899–906.10.2337/diabetes.54.7.1899Search in Google Scholar PubMed

12. Whitelaw NC, Whitelaw E. How lifetimes shape epigenotype within and across generations. Hum Mol Genet2006;15(Suppl 2):R131–7.10.1093/hmg/ddl200Search in Google Scholar PubMed

13. Waddington C. Canalisation of development and inheritance of acquired characters. Nature1942;152:563.10.1038/150563a0Search in Google Scholar

14. Margueron R, Trojer P, Reinberg D. The key to development: interpreting the histone code? Curr Opin Genet Dev2005;15:163–76.10.1016/j.gde.2005.01.005Search in Google Scholar PubMed

15. Lippman Z, Martienssen R. The role of RNA interference in heterochromatic silencing. Nature2004;431:364–70.10.1038/nature02875Search in Google Scholar PubMed

16. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, et al. Epigenetic programming by maternal behavior. Nat Neurosci2004;7:847–54.10.1038/nn1276Search in Google Scholar PubMed

17. Weaver IC, Meaney MJ, Szyf M. Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci USA2006;103:3480–5.10.1073/pnas.0507526103Search in Google Scholar PubMed PubMed Central

18. Lopez IP, Milagro FI, Marti A, Moreno-Aliaga MJ, Martinez JA, De Miguel C. Gene expression changes in rat white adipose tissue after a high-fat diet determined by differential display. Biochem Biophys Res Commun2004;318:234–9.10.1016/j.bbrc.2004.04.018Search in Google Scholar PubMed

19. Santoro R. The silence of the ribosomal RNA genes. Cell Mol Life Sci2005;62:2067–79.10.1007/s00018-005-5110-7Search in Google Scholar PubMed

20. Waterland RA, Lin JR, Smith CA, Jirtle RL. Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus. Hum Mol Genet2006;15:705–16.10.1093/hmg/ddi484Search in Google Scholar PubMed

21. McMinn J, Wei M, Schupf N, Cusmai J, Johnson EB, Smith AC, et al. Unbalanced placental expression of imprinted genes in human intrauterine growth restriction. Placenta2006;27:540–9.10.1016/j.placenta.2005.07.004Search in Google Scholar PubMed

22. Thompson SL, Konfortova G, Gregory RI, Reik W, Dean W, Feil R. Environmental effects on genomic imprinting in mammals. Toxicol Lett2001;120:143–50.10.1016/S0378-4274(01)00292-2Search in Google Scholar

23. Waterland RA, Jirtle RL. Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition2004;20:63–8.10.1016/j.nut.2003.09.011Search in Google Scholar PubMed

24. Rakyan VK, Preis J, Morgan HD, Whitelaw E. The marks, mechanisms and memory of epigenetic states in mammals. Biochem J2001;356:1–10.10.1042/bj3560001Search in Google Scholar

25. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol2003;23:5293–300.10.1128/MCB.23.15.5293-5300.2003Search in Google Scholar PubMed PubMed Central

26. Blewitt ME, Vickaryous NK, Paldi A, Koseki H, Whitelaw E. Dynamic reprogramming of DNA methylation at an epigenetically sensitive allele in mice. PLoS Genet2006;2:e49.10.1371/journal.pgen.0020049Search in Google Scholar PubMed PubMed Central

27. Dolinoy DC, Weidman JR, Waterland RA, Jirtle RL. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ Health Perspect2006;114:567–72.10.1289/ehp.8700Search in Google Scholar PubMed PubMed Central

28. Waterland RA, Dolinoy DC, Lin JR, Smith CA, Shi X, Tahiliani KG. Maternal methyl supplements increase offspring DNA methylation at Axin fused. Genesis2006;44:401–6.10.1002/dvg.20230Search in Google Scholar PubMed

29. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, Walter J, Reik W. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis2003;35:88–93.10.1002/gene.10168Search in Google Scholar PubMed

30. Liu L, Zhang J, Bates S, Li JJ, Peehl DM, Rhim JS, Pfeifer GP. A methylation profile of in vitro immortalized human cell lines. Int J Oncol2005;26:275–85.10.3892/ijo.26.1.275Search in Google Scholar

31. Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, et al. Role of transposable elements in heterochromatin and epigenetic control. Nature2004;430:471–6.10.1038/nature02651Search in Google Scholar PubMed

32. Garcia-Cao M, O'Sullivan R, Peters AH, Jenuwein T, Blasco MA. Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat Genet2004;36:94–9.10.1038/ng1278Search in Google Scholar

33. Waterland RA, Garza C. Potential mechanisms of metabolic imprinting that lead to chronic disease. Am J Clin Nutr1999;69:179–97.10.1093/ajcn/69.2.179Search in Google Scholar

34. Ingrosso D, Cimmino A, Perna AF, Masella L, De Santo NG, De Bonis ML, et al. Folate treatment and unbalanced methylation and changes of allelic expression induced by hyperhomocysteinaemia in patients with uraemia. Lancet2003;361:1693–9.10.1016/S0140-6736(03)13372-7Search in Google Scholar

35. 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 Reprod2001;64:918–26.10.1095/biolreprod64.3.918Search in Google Scholar

36. Biniszkiewicz D, Gribnau J, Ramsahoye B, Gaudet F, Eggan K, Humpherys D, et al. Dnmt1 overexpression causes genomic hypermethylation, loss of imprinting, and embryonic lethality. Mol Cell Biol2002;22:2124–35.10.1128/MCB.22.7.2124-2135.2002Search in Google Scholar

37. Stabenau JR, Pollin W. Heredity and environment in schizophrenia, revisited. The contribution of twin and high-risk studies. J Nerv Ment Dis1993;181:290–7.10.1097/00005053-199305000-00003Search in Google Scholar

38. Oates NA, van Vliet J, Duffy DL, Kroes HY, Martin NG, Boomsma DI, et al. Increased DNA methylation at the AXIN1 gene in a monozygotic twin from a pair discordant for a caudal duplication anomaly. Am J Hum Genet2006;79:155–62.10.1086/505031Search in Google Scholar

39. Drinkwater RD, Blake TJ, Morley AA, Turner DR. Human lymphocytes aged in vivo have reduced levels of methylation in transcriptionally active and inactive DNA. Mutat Res1989;219:29–37.10.1016/0921-8734(89)90038-6Search in Google Scholar

40. Wilson VL, Smith RA, Longoria J, Liotta MA, Harper CM, Harris CC. Chemical carcinogen-induced decreases in genomic 5-methyldeoxycytidine content of normal human bronchial epithelial cells. Proc Natl Acad Sci USA1987;84:3298–301.10.1073/pnas.84.10.3298Search in Google Scholar PubMed PubMed Central

41. Fuke C, Shimabukuro M, Petronis A, Sugimoto J, Oda T, Miura K, et al. Age related changes in 5-methylcytosine content in human peripheral leukocytes and placentas: an HPLC-based study. Ann Hum Genet2004;68:196–204.10.1046/j.1529-8817.2004.00081.xSearch in Google Scholar PubMed

42. Oakes CC, Smiraglia DJ, Plass C, Trasler JM, Robaire B. Aging results in hypermethylation of ribosomal DNA in sperm and liver of male rats. Proc Natl Acad Sci USA2003;100:1775–80.10.1073/pnas.0437971100Search in Google Scholar

43. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science2001;293:1089–93.10.1126/science.1063443Search in Google Scholar

44. Doi M, Hirayama J, Sassone-Corsi P. Circadian regulator CLOCK is a histone acetyltransferase. Cell2006;125:497–508.10.1016/j.cell.2006.03.033Search in Google Scholar

45. Lund G, Andersson L, Lauria M, Lindholm M, Fraga MF, Villar-Garea A, et al. DNA methylation polymorphisms precede any histological sign of atherosclerosis in mice lacking apolipoprotein. Eur J Biol Chem2004;279:29147–54.10.1074/jbc.M403618200Search in Google Scholar

46. Dong C, Yoon W, Goldschmidt-Clermont PJ. DNA methylation and atherosclerosis. J Nutr2002;132:2406S–9S.10.1093/jn/132.8.2406SSearch in Google Scholar

47. Post WS, Goldschmidt-Clermont PJ, Wilhide CC, Heldman AW, Sussman MS, Ouyang P, et al. Methylation of the estrogen receptor gene is associated with aging and atherosclerosis in the cardiovascular system. Cardiovasc Res1999;43:985–91.10.1016/S0008-6363(99)00153-4Search in Google Scholar

48. Issa JP. Epigenetic variation and human disease. J Nutr2002;132:2388S–92S.10.1093/jn/132.8.2388SSearch in Google Scholar PubMed

49. Poirier LA, Brown AT, Fink LM, Wise CK, Randolph CJ, Delongchamp RR, et al. Blood S-adenosylmethionine concentrations and lymphocyte methylenetetrahydrofolate reductase activity in diabetes mellitus and diabetic nephropathy. Metabolism2001;50:1014–8.10.1053/meta.2001.25655Search in Google Scholar PubMed

50. Dabelea D, Hanson RL, Lindsay RS, Pettitt DJ, Imperatore G, Gabir MM, et al. Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships. Diabetes2000;49:2208–11.10.2337/diabetes.49.12.2208Search in Google Scholar PubMed

51. Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab2000;279:E83–7.10.1152/ajpendo.2000.279.1.E83Search in Google Scholar PubMed

52. Plagemann A, Harder T, Franke K, Kohlhoff R. Long-term impact of neonatal breast-feeding on body weight and glucose tolerance in children of diabetic mothers. Diabetes Care2002;25:16–22.10.2337/diacare.25.1.16Search in Google Scholar

53. Walsh CP, Chaillet JR, Bestor TH. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet1998;20:116–7.10.1038/2413Search in Google Scholar

54. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, et al. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev2002;117:15–23.10.1016/S0925-4773(02)00181-8Search in Google Scholar

55. Srinivasan M, Aalinkeel R, Song F, Patel MS. Programming of islet functions in the progeny of hyperinsulinemic/obese rats. Diabetes2003;52:984–90.10.2337/diabetes.52.4.984Search in Google Scholar

56. Drake AJ, Walker BR, Seckl JR. Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am J Physiol Regul Integr Comp Physiol2004;288:R34–8.10.1152/ajpregu.00106.2004Search in Google Scholar

57. Patel MS, Srinivasan M. Metabolic programming: causes and consequences. J Biol Chem2002;277:1629–32.10.1074/jbc.R100017200Search in Google Scholar

58. Campbell JH, Perkins P. Transgenerational effects of drug and hormonal treatments in mammals: a review of observations and ideas. Prog Brain Res1988;73:535–53.10.1016/S0079-6123(08)60525-7Search in Google Scholar

59. Skinner MK, Anway MD. Seminiferous cord formation and germ-cell programming: epigenetic transgenerational actions of endocrine disruptors. Ann NY Acad Sci2005;1061:18–32.10.1196/annals.1336.004Search in Google Scholar PubMed PubMed Central

60. Ruden DM, Xiao L, Garfinkel MD, Lu X. Hsp90 and environmental impacts on epigenetic states: a model for the trans-generational effects of diethylstibesterol on uterine development and cancer. Hum Mol Genet2005;14:R149–55.10.1093/hmg/ddi103Search in Google Scholar PubMed

61. Peaston AE, Whitelaw E. Epigenetics and phenotypic variation in mammals. Mamm Genome2006;17:365–74.10.1007/s00335-005-0180-2Search in Google Scholar PubMed PubMed Central

62. Martin JF, Johnston CS, Han CT, Benyshek DC. Nutritional origins of insulin resistance: a rat model for diabetes-prone human populations. J Nutr2000;130:741–4.10.1093/jn/130.4.741Search in Google Scholar

63. Reusens B, Remacle C. Intergenerational effect of an adverse intrauterine environment on perturbation of glucose metabolism. Twin Res2001;4:406–11.10.1375/1369052012597Search in Google Scholar

64. Drake AJ, Walker BR. The intergenerational effects of fetal programming: non-genomic mechanisms for the inheritance of low birth weight and cardiovascular risk. J Endocrinol2004;180:1–16.10.1677/joe.0.1800001Search in Google Scholar

65. Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science2005;308:1466–9.10.1126/science.1108190Search in Google Scholar

66. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KV, et al. Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc Natl Acad Sci USA2003;100:2538–43.10.1073/pnas.0436776100Search in Google Scholar

67. Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development2000;127:4195–202.10.1242/dev.127.19.4195Search in Google Scholar

68. Boucher BJ, Ewen SW, Stowers JM. Betel nut (Areca catechu) consumption and the induction of glucose intolerance in adult CD1 mice and in their F1 and F2 offspring. Diabetologia1994;37:49–55.10.1007/BF00428777Search in Google Scholar

69. Aerts L, Van Assche FA. Intra-uterine transmission of disease. Placenta2003;24:905–11.10.1016/S0143-4004(03)00115-2Search in Google Scholar

70. Haig D. Altercation of generations: genetic conflicts of pregnancy. Am J Reprod Immunol1996;35:226–32.10.1111/j.1600-0897.1996.tb00035.xSearch in Google Scholar PubMed

71. Zambrano E, Bautista CJ, Deas M, Martinez-Samayoa PM, Gonzalez-Zamorano M, Ledesma H, et al. A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol2006;571:221–30.10.1113/jphysiol.2005.100313Search in Google Scholar PubMed PubMed Central

72. Zambrano E, Martinez-Samayoa PM, Bautista CJ, Deas M, Guillen L, Rodriguez-Gonzalez GL, et al. Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J Physiol2005;566:225–36.10.1113/jphysiol.2005.086462Search in Google Scholar PubMed PubMed Central

73. Pinto ML, Shetty PS. Influence of exercise-induced maternal stress on fetal outcome in Wistar rats: inter-generational effects. Br J Nutr1995;73:645–53.10.1079/BJN19950070Search in Google Scholar PubMed

74. Gallou-Kabani C, Vigé A, Gross MS, Boileau C, Rabes JP, Fruchart-Najib J, et al. Resistance to high-fat diet in the female progeny of obese mice fed a control diet during the periconceptual, gestation and lactation periods. AJP Endocrinol Metab 2007. In press. doi:10.1152/ajp-endo.00390.2006.Search in Google Scholar

75. Drake AJ, Walker BR, Seckl JR. Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am J Physiol Regul Integr Comp Physiol2005;288:R34–8.10.1152/ajpregu.00106.2004Search in Google Scholar PubMed

76. Hales BF, Barton TS, Robaire B. Impact of paternal exposure to chemotherapy on offspring in the rat. J Natl Cancer Inst Monogr 2005:28–31.10.1093/jncimonographs/lgi028Search in Google Scholar PubMed

77. Champagne FA, Weaver IC, Diorio J, Dymov S, Szyf M, Meaney MJ. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology2006;147:2909–15.10.1210/en.2005-1119Search in Google Scholar PubMed

78. Aerts L, Van Assche FA. Animal evidence for the transgenerational development of diabetes mellitus. Int J Biochem Cell Biol2006;38:894–903.10.1016/j.biocel.2005.07.006Search in Google Scholar PubMed

79. Kaati G, Bygren LO, Edvinsson S. Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period. Eur J Hum Genet2002;10:682–8.10.1038/sj.ejhg.5200859Search in Google Scholar PubMed

80. Jablonka E, Lamb MJ. The changing concept of epigenetics. Ann NY Acad Sci2002;981:82–96.10.1111/j.1749-6632.2002.tb04913.xSearch in Google Scholar PubMed

81. Pembrey M. Imprinting and transgenerational modulation of gene expression; human growth as a model. Acta Genet Med Gemellol (Roma)1996;45:111–25.10.1017/S0001566000001197Search in Google Scholar

82. Junien C, Gallou-Kabani C, Vige A, Gross MS. [Nutritional epigenomics of metabolic syndrome]. Med Sci (Paris)2005;21:396–404 (in French).10.1051/medsci/2005214396Search in Google Scholar PubMed

83. Cheng RY, Hockman T, Crawford E, Anderson LM, Shiao YH. Epigenetic and gene expression changes related to transgenerational carcinogenesis. Mol Carcinog2004;40:1–11.10.1002/mc.20022Search in Google Scholar PubMed

84. Pembrey M. Genomic imprinting and the possible role of epigenetic inheritance in trangenerational effects. In: International Genomic Imprinting Meeting, 1999:17.Search in Google Scholar

85. Junien C. L'empreinte parentale: de la guerre des sexes à la solidarité entre générations. Med Sci2000;3:336–44.10.4267/10608/1652Search in Google Scholar

86. Branca F, Lorenzetti S. Health effects of phytoestrogens. Forum Nutr2005;57:100–11.10.1159/000083773Search in Google Scholar PubMed

87. Ke X, Lei Q, James S, Kelleher S, Melnyk S, Jernigan S, et al. Uteroplacental insufficiency affects epigenetic determinants of chromatin structure in brains of neonatal and juvenile IUGR rats. Physiol Genomics2006;25:16–28.10.1152/physiolgenomics.00093.2005Search in Google Scholar PubMed

88. Vadlamudi S, Kalhan SC, Patel MS. Persistence of metabolic consequences in the progeny of rats fed a HC formula in their early postnatal life. Am J Physiol1995;269:E731–8.10.1152/ajpendo.1995.269.4.E731Search in Google Scholar PubMed

89. McKay JA, Williams EA, Mathers JC. Folate and DNA methylation during in utero development and aging. Biochem Soc Trans2004;32:1006–7.10.1042/BST0321006Search in Google Scholar PubMed

90. Young LE, Fernandes K, McEvoy TG, Butterwith SC, Gutierrez CG, Carolan C, et al. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat Genet2001;27:153–4.10.1038/84769Search in Google Scholar PubMed

91. Mann MR, Lee SS, Doherty AS, Verona RI, Nolen LD, Schultz RM, Bartolomei MS. Selective loss of imprinting in the placenta following preimplantation development in culture. Development2004;131:3727–35.10.1242/dev.01241Search in Google Scholar PubMed

92. Dean W, Bowden L, Aitchison A, Klose J, Moore T, Meneses JJ, et al. Altered imprinted gene methylation and expression in completely ES cell-derived mouse fetuses: association with aberrant phenotypes. Development1998;125:2273–82.10.1242/dev.125.12.2273Search in Google Scholar PubMed

93. Humpherys D, Eggan K, Akutsu H, Friedman A, Hochedlinger K, Yanagimachi R, et al. Abnormal gene expression in cloned mice derived from embryonic stem cell and cumulus cell nuclei. Proc Natl Acad Sci USA2002;99:12889–94.10.1073/pnas.192433399Search in Google Scholar PubMed PubMed Central

94. Baqir S, Smith LC. Growth restricted in vitro culture conditions alter the imprinted gene expression patterns of mouse embryonic stem cells. Cloning Stem Cells2003;5:199–212.10.1089/153623003769645866Search in Google Scholar

95. Pantoja C, de Los Rios L, Matheu A, Antequera F, Serrano M. Inactivation of imprinted genes induced by cellular stress and tumorigenesis. Cancer Res2005;65:26–33.10.1158/0008-5472.26.65.1Search in Google Scholar

96. McLachlan JA, Burow M, Chiang TC, Li SF. Gene imprinting in developmental toxicology: a possible interface between physiology and pathology. Toxicol Lett2001;120:161–4.10.1016/S0378-4274(01)00295-8Search in Google Scholar

97. O'Neil JS, Burow ME, Green AE, McLachlan JA, Henson MC. Effects of estrogen on leptin gene promoter activation in MCF-7 breast cancer and JEG-3 choriocarcinoma cells: selective regulation via estrogen receptors alpha and beta. Mol Cell Endocrinol2001;176:67–75.10.1016/S0303-7207(01)00473-7Search in Google Scholar

98. Li S, Hansman R, Newbold R, Davis B, McLachlan JA, Barrett JC. Neonatal diethylstilbestrol exposure induces persistent elevation of c-fos expression and hypomethylation in its exon-4 in mouse uterus. Mol Carcinog2003;38:78–84.10.1002/mc.10147Search in Google Scholar PubMed

99. Wilson IM, Davies JJ, Weber M, Brown CJ, Alvarez CE, MacAulay C, et al. Epigenomics: mapping the methylome. Cell Cycle2006;5:155–8.10.4161/cc.5.2.2367Search in Google Scholar PubMed

100. Murrell A, Rakyan VK, Beck S. From genome to epigenome. Hum Mol Genet2005;14:R3–10.10.1093/hmg/ddi110Search in Google Scholar PubMed

101. Hitchins M, Williams R, Cheong K, Halani N, Lin VA, Packham D, et al. MLH1 germline epimutations as a factor in hereditary nonpolyposis colorectal cancer. Gastroenterology2005;129:1392–9.10.1053/j.gastro.2005.09.003Search in Google Scholar PubMed

102. Sandovici I, Kassovska-Bratinova S, Loredo-Osti JC, Leppert M, Suarez A, Stewart R, et al. Interindividual variability and parent of origin DNA methylation differences at specific human Alu elements. Hum Mol Genet2005;14:2135–43.10.1093/hmg/ddi218Search in Google Scholar PubMed

103. Flanagan JM, Popendikyte V, Pozdniakovaite N, Sobolev M, Assadzadeh A, Schumacher A, et al. Intra- and interindividual epigenetic variation in human germ cells. Am J Hum Genet2006;79:67–84.10.1086/504729Search in Google Scholar PubMed PubMed Central

104. Paz MF, Wei S, Cigudosa JC, Rodriguez-Perales S, Peinado MA, Huang TH, et al. Genetic unmasking of epigenetically silenced tumor suppressor genes in colon cancer cells deficient in DNA methyltransferases. Hum Mol Genet2003;12:2209–19.10.1093/hmg/ddg226Search in Google Scholar PubMed

105. Polesskaya OO, Aston C, Sokolov BP. Allele C-specific methylation of the 5-HT2A receptor gene: evidence for correlation with its expression and expression of DNA methylase DNMT1. J Neurosci Res2006;83:362–73.10.1002/jnr.20732Search in Google Scholar PubMed

106. Yamada Y, Watanabe H, Miura F, Soejima H, Uchiyama M, Iwasaka T, et al. A comprehensive analysis of allelic methylation status of CpG islands on human chromosome 21q. Genome Res2004;14:247–66.10.1101/gr.1351604Search in Google Scholar PubMed PubMed Central

107. Frazier ML, Xi L, Zong J, Viscofsky N, Rashid A, Wu EF, et al. Association of the CpG island methylator phenotype with family history of cancer in patients with colorectal cancer. Cancer Res2003;63:4805–8.Search in Google Scholar

108. Suter CM, Martin DI, Ward RL. Germline epimutation of MLH1 in individuals with multiple cancers. Nat Genet2004;36:497–501.10.1038/ng1342Search in Google Scholar PubMed

109. Popendikyte V, Laurinavicius A, Paterson AD, Macciardi F, Kennedy JL, Petronis A. DNA methylation at the putative promoter region of the human dopamine D2 receptor gene. Neuroreport1999;10:1249–55.10.1097/00001756-199904260-00018Search in Google Scholar PubMed

110. Murrell A, Heeson S, Cooper WN, Douglas E, Apostolidou S, Moore GE, et al. An association between variants in the IGF2 gene and Beckwith-Wiedemann syndrome: interaction between genotype and epigenotype. Hum Mol Genet2004;13:247–55.10.1093/hmg/ddh013Search in Google Scholar PubMed

111. Zogel C, Bohringer S, Gross S, Varon R, Buiting K, Horsthemke B. Identification of cis- and trans-acting factors possibly modifying the risk of epimutations on chromosome 15. Eur J Hum Genet2006;14:752–8.10.1038/sj.ejhg.5201602Search in Google Scholar PubMed

112. Polesskaya OO, Sokolov BP. Differential expression of the “C” and “T” alleles of the 5-HT2A receptor gene in the temporal cortex of normal individuals and schizophrenics. J Neurosci Res2002;67:812–22.10.1002/jnr.10173Search in Google Scholar PubMed

113. Cebrian A, Pharoah PD, Ahmed S, Ropero S, Fraga MF, Smith PL, et al. Genetic variants in epigenetic genes and breast cancer risk. Carcinogenesis2006;27:1661–9.10.1093/carcin/bgi375Search in Google Scholar PubMed

114. Bjornsson HT, Fallin MD, Feinberg AP. An integrated epigenetic and genetic approach to common human disease. Trends Genet2004;20:350–8.10.1016/j.tig.2004.06.009Search in Google Scholar PubMed

115. de Rooij SR, Painter RC, Phillips DI, Osmond C, Tanck MW, Defesche JC, et al. The effects of the Pro12Ala polymorphism of the peroxisome proliferator-activated receptor-gamma2 gene on glucose/insulin metabolism interact with prenatal exposure to famine. Diabetes Care2006;29:1052–7.10.2337/dc05-1993Search in Google Scholar

116. Van den Veyver IB. Genetic effects of methylation diets. Annu Rev Nutr2002;22:255–82.10.1146/annurev.nutr.22.010402.102932Search in Google Scholar PubMed

117. Waterland RA. Assessing the effects of high methionine intake on DNA methylation. J Nutr2006;136:1706S–10S.10.1093/jn/136.6.1706SSearch in Google Scholar PubMed

118. Srinivasan M, Aalinkeel R, Song F, Mitrani P, Pandya JD, Strutt B, et al. Maternal hyperinsulinemia predisposes rat fetuses for hyperinsulinemia, and adult-onset obesity and maternal mild food restriction reverses this phenotype. Am J Physiol Endocrinol Metab2006;290:E129–E34.10.1152/ajpendo.00248.2005Search in Google Scholar PubMed

119. Weaver IC, Champagne FA, Brown SE, Dymov S, Sharma S, Meaney MJ, et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci2005;25:11045–54.10.1523/JNEUROSCI.3652-05.2005Search in Google Scholar PubMed PubMed Central

120. Mager J, Bartolomei MS. Strategies for dissecting epigenetic mechanisms in the mouse. Nat Genet2005;37:1194–200.10.1038/ng1664Search in Google Scholar PubMed

Published Online: 2007-03-01
Published in Print: 2007-03-01

©2007 by Walter de Gruyter Berlin New York

Articles in the same Issue

  1. From human genetic variations to prediction of risks and responses to drugs and the environment
  2. Nutrigenomics – 2006 update
  3. How to comprehensively analyse proteins and how this influences nutritional research
  4. Genotypes, obesity and type 2 diabetes – can genetic information motivate weight loss? A review
  5. The Gene-Diet Attica Investigation on childhood obesity (GENDAI): overview of the study design
  6. Polymorphisms in the APOA1/C3/A4/A5 gene cluster and cholesterol responsiveness to dietary change
  7. Nutri-epigenomics: lifelong remodelling of our epigenomes by nutritional and metabolic factors and beyond
  8. Emerging role of cathepsin S in obesity and its associated diseases
  9. Association analysis of hepatitis virus B infection with haplotypes of the TBX21 gene promoter region in the Chinese population
  10. Multiplex polymerase chain reaction on FTA cards vs. flow cytometry for B-lymphocyte clonality
  11. Real-time multiplex PCR assay for genotyping of three apolipoprotein E alleles and two choline acetyltransferase alleles with three hybridization probes
  12. Immunomagnetic CD45 depletion does not improve cytokeratin 20 RT-PCR in colorectal cancer
  13. Analysis of the components of hypertransaminasemia after liver resection
  14. Fine characterization of mitral valve glycosaminoglycans and their modification with degenerative disease
  15. Oxidative stress evaluated using an automated method for hydroperoxide estimation in patients with coronary artery disease
  16. Secretory phospholipase A2 activity and release kinetics of vascular tissue remodelling biomarkers after coronary artery bypass grafting with and without cardiopulmonary bypass
  17. Clustered components of the metabolic syndrome and platelet counts in Japanese females
  18. International Standard for serum vitamin B12 and serum folate: international collaborative study to evaluate a batch of lyophilised serum for B12 and folate content
  19. Multicentre physiological reference intervals for serum concentrations of immunoglobulins A, G and M, complement C3c and C4 measured with Tina-Quant® reagents systems
  20. In vivo and in vitro allergy diagnostics: it's time to reappraise the costs
  21. Experience with post-market surveillance of in-vitro diagnostic medical devices for lay use in Germany
  22. Evaluation of the high-sensitivity, full-range Olympus CRP OSR6199 application on the Olympus AU640®
  23. How to improve the teaching of urine microscopy
  24. In vitro determination of allergen-specific serum IgE. Comparative analysis of three methods
  25. Efficacy of a new blocker against anti-ruthenium antibody interference in the Elecsys free triiodothyronine assay
  26. Clinical indications for plasma protein assays: transthyretin (prealbumin) in inflammation and malnutrition: International Federation of Clinical Chemistry and Laboratory Medicine (IFCC): IFCC Scientific Division Committee on Plasma Proteins (C-PP)
  27. Meeting Report: From human genetic variations to prediction of risks and responses to drugs and the environment
https://doi.org/10.1515/CCLM.2007.081
Keywords for this article
environment; epigenetics; fetal programming; metabolic syndrome; nutrition; transgenerational effects

Articles in the same Issue

  1. From human genetic variations to prediction of risks and responses to drugs and the environment
  2. Nutrigenomics – 2006 update
  3. How to comprehensively analyse proteins and how this influences nutritional research
  4. Genotypes, obesity and type 2 diabetes – can genetic information motivate weight loss? A review
  5. The Gene-Diet Attica Investigation on childhood obesity (GENDAI): overview of the study design
  6. Polymorphisms in the APOA1/C3/A4/A5 gene cluster and cholesterol responsiveness to dietary change
  7. Nutri-epigenomics: lifelong remodelling of our epigenomes by nutritional and metabolic factors and beyond
  8. Emerging role of cathepsin S in obesity and its associated diseases
  9. Association analysis of hepatitis virus B infection with haplotypes of the TBX21 gene promoter region in the Chinese population
  10. Multiplex polymerase chain reaction on FTA cards vs. flow cytometry for B-lymphocyte clonality
  11. Real-time multiplex PCR assay for genotyping of three apolipoprotein E alleles and two choline acetyltransferase alleles with three hybridization probes
  12. Immunomagnetic CD45 depletion does not improve cytokeratin 20 RT-PCR in colorectal cancer
  13. Analysis of the components of hypertransaminasemia after liver resection
  14. Fine characterization of mitral valve glycosaminoglycans and their modification with degenerative disease
  15. Oxidative stress evaluated using an automated method for hydroperoxide estimation in patients with coronary artery disease
  16. Secretory phospholipase A2 activity and release kinetics of vascular tissue remodelling biomarkers after coronary artery bypass grafting with and without cardiopulmonary bypass
  17. Clustered components of the metabolic syndrome and platelet counts in Japanese females
  18. International Standard for serum vitamin B12 and serum folate: international collaborative study to evaluate a batch of lyophilised serum for B12 and folate content
  19. Multicentre physiological reference intervals for serum concentrations of immunoglobulins A, G and M, complement C3c and C4 measured with Tina-Quant® reagents systems
  20. In vivo and in vitro allergy diagnostics: it's time to reappraise the costs
  21. Experience with post-market surveillance of in-vitro diagnostic medical devices for lay use in Germany
  22. Evaluation of the high-sensitivity, full-range Olympus CRP OSR6199 application on the Olympus AU640®
  23. How to improve the teaching of urine microscopy
  24. In vitro determination of allergen-specific serum IgE. Comparative analysis of three methods
  25. Efficacy of a new blocker against anti-ruthenium antibody interference in the Elecsys free triiodothyronine assay
  26. Clinical indications for plasma protein assays: transthyretin (prealbumin) in inflammation and malnutrition: International Federation of Clinical Chemistry and Laboratory Medicine (IFCC): IFCC Scientific Division Committee on Plasma Proteins (C-PP)
  27. Meeting Report: From human genetic variations to prediction of risks and responses to drugs and the environment
Sign up now to receive a 20% welcome discount
Institutional Access
How does access work?
Have an idea on how to improve our website?
Please write us.
© 2025 De Gruyter Brill
Downloaded on 11.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/CCLM.2007.081/html
Scroll to top button