Biological embedding of early-life exposures and disease risk in humans: A role for DNA methylation

European Journal of Clinical Investigation

Volumn 45, Issue 3, 2015, Pages 303-332

  Demetriou, Christiana A ^a,b   van Veldhoven, Karin ^a   Relton, Caroline ^c,d   Stringhini, Silvia ^e   Kyriacou, Kyriacos ^b,f   Vineis, Paolo ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b CYPRUS INSTITUTE OF NEUROLOGY AND GENETICS   (Cyprus)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e UNIVERSITY OF LAUSANNE   (Switzerland)

^f The Cyprus School of Molecular Medicine   (Cyprus)

Author keywords

Biological embedding; Body mass index; DNA methylation, epigenetics; Early life nutrition; Early life socio economic status

Indexed keywords

BODY MASS; CHILDHOOD OBESITY; DNA METHYLATION; EMBEDDING; ENVIRONMENTAL EXPOSURE; EPIGENETICS; HUMAN; KNOWLEDGE; NUTRITION; PERSONAL EXPERIENCE; PRIORITY JOURNAL; PUBLISHING; REVIEW; SOCIOECONOMICS; ADOLESCENT; ADULT; ADVERSE EFFECTS; AGED; CHILD; CHILD NUTRITION; COMPLICATION; DISEASE PREDISPOSITION; ETIOLOGY; FEMALE; GENETIC EPIGENESIS; INFANT; LIFE EVENT; MALE; MIDDLE AGED; PHYSIOLOGY; PRESCHOOL CHILD; RISK FACTOR; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; BODY MASS INDEX; CHILD; CHILD NUTRITIONAL PHYSIOLOGICAL PHENOMENA; CHILD, PRESCHOOL; DISEASE SUSCEPTIBILITY; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPIGENESIS, GENETIC; FEMALE; HUMANS; INFANT; LIFE CHANGE EVENTS; MALE; MIDDLE AGED; PEDIATRIC OBESITY; RISK FACTORS; SOCIOECONOMIC FACTORS; YOUNG ADULT;

EID: 84923276534     PISSN: 00142972     EISSN: 13652362     Source Type: Journal    
DOI: 10.1111/eci.12406     Document Type: Review

References (96)

1. Barouki R, Gluckman PD, Grandjean P, Hanson M, Heindel JJ. Developmental origins of non-communicable disease: implications for research and public health. Environ Health 2012;11:42.
2. McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 2005;85:571-633.
3. Hertzman C, Boyce T. How experience gets under the skin to create gradients in developmental health. Annu Rev Public Health 2010;31:329-47. 3p following 347.
4. Hertzman C. The biological embedding of early experience and its effects on health in adulthood. Ann N Y Acad Sci 1999;896:85-95.
5. Hertzman C. Putting the concept of biological embedding in historical perspective. Proc Natl Acad Sci USA 2012;109(Suppl. 2):17160-7.
6. Gluckman PD, Hanson MA. Developmental origins of disease paradigm: a mechanistic and evolutionary perspective. Pediatr Res 2004;56:311-17.
7. Gluckman PD, Hanson MA. Mismatch?: The Lifestyle Diseases Timebomb. Oxford: Oxford University Press; 2008.
8. Gluckman PD. Epigenetics and metabolism in 2011: epigenetics, the life-course and metabolic disease. Nat Rev Endocrinol 2012;8:74-6.
9. Fenton SE. Endocrine-disrupting compounds and mammary gland development: early exposure and later life consequences. Endocrinology 2006;147:s18-24.
10. Power C, Kuh D, Morton S. From developmental origins of adult disease to life course research on adult disease and aging: insights from birth cohort studies. Annu Rev Public Health 2013;34:7-28.
11. Cutler DM, Lleras-Muney A. Education and health: evaluating theories and evidence [Internet]. National Bureau of Economic Research; 2006 Jul. Report No.: 12352. Available from: http://www.nber.org/papers/w12352
12. Howe LD, Tilling K, Matijasevich A, Petherick ES, Santos AC, Fairley L et al. Linear spline multilevel models for summarising childhood growth trajectories: a guide to their application using examples from five birth cohorts. Stat Methods Med Res 2013;DOI: 10.1177/0962280213503925.
13. Power C, Matthews S. Accumulation of health risks across social groups in a national longitudinal study. In: Strickland SS, Shetty PS, editors. Hum Biol Soc Inequal. Cambridge, U.K.: Cambridge University Press; 1998: pp 36-57.
14. Ravelli AC, van Der Meulen JH, Osmond C, Barker DJ, Bleker OP. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr 1999;70:811-16.
15. Lumey LH. Decreased birthweights in infants after maternal in utero exposure to the Dutch famine of 1944-1945. Paediatr Perinat Epidemiol 1992;6:240-53.
16. Stringhini S, Polidoro S, Sacerdote C, Kelly R, van Veldhoven K, Gallo V et al. Epigenetic signatures of low socio-economic status: a prospective study. Pers Commun.
17. Rutter M. Achievements and challenges in the biology of environmental effects. Proc Natl Acad Sci USA 2012;109(Suppl. 2):17149-53.
18. Esteller M. Epigenetics in cancer. N Engl J Med 2008;358:1148-59.
19. De Smet C, Loriot A, Boon T. Promoter-dependent mechanism leading to selective hypomethylation within the 5' region of gene MAGE-A1 in tumor cells. Mol Cell Biol 2004;24:4781-90.
20. Stearns V, Zhou Q, Davidson NE. Epigenetic regulation as a new target for breast cancer therapy. Cancer Invest 2007;25:659-65.
21. White WM, Brost BC, Sun Z, Rose C, Craici I, Wagner SJ et al. Normal early pregnancy: a transient state of epigenetic change favoring hypomethylation. Epigenetics 2012;7:729-34.
22. Baccarelli A, Wright RO, Bollati V, Tarantini L, Litonjua AA, Suh HH et al. Rapid DNA methylation changes after exposure to traffic particles. Am J Respir Crit Care Med 2009;179:572-8.
23. Bellavia A, Urch B, Speck M, Brook RD, Scott JA, Albetti B et al. DNA hypomethylation, ambient particulate matter, and increased blood pressure: findings from controlled human exposure experiments. J Am Heart Assoc 2013;2:e000212.
24. Veeck J, Esteller M. Breast cancer epigenetics: from DNA methylation to microRNAs. J Mammary Gland Biol Neoplasia 2010;15:5-17.
25. Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene 2002;21:5400-13.
26. Brennan K, Flanagan JM. Is there a link between genome-wide hypomethylation in blood and cancer risk? Cancer Prev Res 2012;5:1345-57.
27. Ito Y, Koessler T, Ibrahim AEK, Rai S, Vowler SL, Abu-Amero S et al. Somatically acquired hypomethylation of IGF2 in breast and colorectal cancer. Hum Mol Genet 2008;17:2633-43.
28. Jovanovic J, Rønneberg JA, Tost J, Kristensen V. The epigenetics of breast cancer. Mol Oncol 2010;4:242-54.
29. Avraham A, Cho SS, Uhlmann R, Polak ML, Sandbank J, Karni T et al. Tissue specific DNA methylation in normal human breast epithelium and in breast cancer. PLoS ONE 2014;9:e91805.
30. Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotech 2010;28:1057-68.
31. Dominguez-Salas P, Cox SE, Prentice AM, Hennig BJ, Moore SE. Maternal nutritional status, C1 metabolism and offspring DNA methylation: a review of current evidence in human subjects. Proc Nutr Soc 2012;71:154-65.
32. Borghol N, Suderman M, McArdle W, Racine A, Hallett M, Pembrey et al. Associations with early-life socio-economic position in adult DNA methylation. Int J Epidemiol 2012;41:62-74.
33. Obermann-Borst SA, Heijmans BT, Eilers PHC, Tobi EW, Steegers EA, Slagboom PE et al. Periconception maternal smoking and low education are associated with methylation of INSIGF in children at the age of 17 months. J Dev Orig Health Dis 2012;3:315-20.
34. Obermann-Borst SA, Eilers PHC, Tobi EW, de Jong FH, Slagboom PE, Heijmans BT et al. Duration of breastfeeding and gender are associated with methylation of the LEPTIN gene in very young children. Pediatr Res 2013;74:344-9.
35. Lam LL, Emberly E, Fraser HB, Neumann SM, Chen E, Miller GE et al. Factors underlying variable DNA methylation in a human community cohort. Proc Natl Acad Sci USA 2012;109(Suppl. 2):17253-60.
36. Beach SRH, Dogan MV, Brody GH, Philibert RA. Differential impact of cumulative SES risk on methylation of protein-protein interaction pathways as a function of SLC6A4 genetic variation in African American young adults. Biol Psychol 2014;96:28-34.
37. Tehranifar P, Wu H-C, Fan X, Flom JD, Ferris JS, Cho YH et al. Early life socioeconomic factors and genomic DNA methylation in mid-life. Epigenetics 2013;8:23-7.
38. Terry MB, Ferris JS, Pilsner R, Flom JD, Tehranifar P, Santella RM et al. Genomic DNA methylation among women in a multiethnic New York City birth cohort. Cancer Epidemiol Biomarkers Prev 2008;17:2306-10.
39. Subramanyam MA, Diez-Roux AV, Pilsner JR, Villamor E, Donohue KM, Liu Y et al. Social factors and leukocyte DNA methylation of repetitive sequences: the multi-ethnic study of atherosclerosis. PLoS ONE 2013;8:e54018.
40. Hjartåker A, Langseth H, Weiderpass E. Obesity and diabetes epidemics: cancer repercussions. Adv Exp Med Biol 2008;630:72-93.
41. Alexander JK. Obesity and coronary heart disease. Am J Med Sci 2001;321:215-24.
42. Michels KB, Harris HR, Barault L. Birthweight, maternal weight trajectories and global DNA methylation of LINE-1 repetitive elements. PLoS ONE 2011;6:e25254.
43. St-Pierre J, Hivert M-F, Perron P, Poirier P, Guay S-P, Brisson D et al. IGF2 DNA methylation is a modulator of newborn's fetal growth and development. Epigenetics 2012;7:1125-32.
44. Drake AJ, McPherson RC, Godfrey KM, Cooper C, Lillycrop KA, Hanson MA et al. An unbalanced maternal diet in pregnancy associates with offspring epigenetic changes in genes controlling glucocorticoid action and fetal growth. Clin Endocrinol 2012;77:808-15.
45. Engel SM, Joubert BR, Wu MC, Olshan AF, Håberg SE, Ueland PM et al. Neonatal genome-wide methylation patterns in relation to birth weight in the Norwegian mother and child cohort. Am J Epidemiol 2014;179:834-42.
46. Burris HH, Braun JM, Byun H-M, Tarantini L, Mercado A, Wright RJ et al. Association between birth weight and DNA methylation of IGF2, glucocorticoid receptor and repetitive elements LINE-1 and Alu. Epigenomics 2013;5:271-81.
47. Lesseur C, Armstrong DA, Paquette AG, Koestler DC, Padbury JF, Marsit CJ. Tissue-specific Leptin promoter DNA methylation is associated with maternal and infant perinatal factors. Mol Cell Endocrinol 2013;381:160-7.
48. Bouwland-Both MI, van Mil NH, Stolk L, Eilers PHC, Verbiest MMPJ, Heijmans BT et al. DNA methylation of IGF2DMR and H19 is associated with fetal and infant growth: the generation R study. PLoS ONE 2013;8:e81731.
49. Wang X, Zhu H, Snieder H, Su S, Munn D, Harshfield G et al. Obesity related methylation changes in DNA of peripheral blood leukocytes. BMC Med 2010;8:87.
50. Kuehnen P, Mischke M, Wiegand S, Sers C, Horsthemke B, Lau S et al. An Alu element-associated hypermethylation variant of the POMC gene is associated with childhood obesity. PLoS Genet 2012;8:e1002543.
51. Groom A, Potter C, Swan DC, Fatemifar G, Evans DM, Ring SM et al. Postnatal growth and DNA methylation are associated with differential gene expression of the TACSTD2 gene and childhood fat mass. Diabetes 2012;61:391-400.
52. Huang R-C, Galati JC, Burrows S, Beilin LJ, Li X, Pennell CE et al. DNA methylation of the IGF2/H19 imprinting control region and adiposity distribution in young adults. Clin Epigenetics 2012;4:21.
53. Xu X, Su S, Barnes VA, De Miguel C, Pollock J, Ownby D et al. A genome-wide methylation study on obesity: differential variability and differential methylation. Epigenetics 2013;8:522-33.
54. Su S, Zhu H, Xu X, Wang X, Dong Y, Kapuku G et al. DNA methylation of the LY86 gene is associated with obesity, insulin resistance, and inflammation. Twin Res Hum Genet 2014;17:183-91.
55. García-Cardona MC, Huang F, María García-Vivas J, López-Camarillo C, Del Río Navarro BE, Olivos EN et al. DNA methylation of leptin and adiponectin promoters in children is reduced by the combined presence of obesity and insulin resistance. Int J Obes 2014;38:1457-65.
56. Godfrey KM, Sheppard A, Gluckman PD, López-Camarillo C, Del Río Navarro BE, Olivos EN et al. Epigenetic gene promoter methylation at birth is associated with child's later adiposity. Diabetes 2011;60:1528-34.
57. Perkins E, Murphy SK, Murtha AP, Schildkraut J, Jirtle RL, Demark-Wahnefried W et al. Insulin-like growth factor 2/H19 methylation at birth and risk of overweight and obesity in children. J Pediatr 2012;161:31-9.
58. Relton CL, Groom A, St Pourcain B, Sayers AE, Swan DC, Embleton ND et al. DNA methylation patterns in cord blood DNA and body size in childhood. PLoS ONE 2012;7:e31821.
59. Azzi S, Sas TC, Koudou Y, Le Bouc Y, Souberbielle J-C, Dargent-Molina P et al. Degree of methylation of ZAC1 (PLAGL1) is associated with prenatal and post-natal growth in healthy infants of the EDEN mother child cohort. Epigenetics 2014;9:338-45.
60. Perng W, Mora-Plazas M, Marín C, Rozek LS, Baylin A, Villamor E. A prospective study of LINE-1DNA methylation and development of adiposity in school-age children. PLoS ONE 2013;8:e62587.
61. Clarke-Harris R, Wilkin TJ, Hosking J, Pinkney J, Jeffery AN, Metcalf BS et al. PGC1α promoter methylation in blood at 5-7 years predicts adiposity from 9 to 14 years (earlybird 50). Diabetes 2014;63:2528-37.
62. Dick KJ, Nelson CP, Tsaprouni L, Sandling JK, Aïssi D, Wahl S et al. DNA methylation and body-mass index: a genome-wide analysis. Lancet 2014;383:1990-8.
63. Jiménez-Chillarón JC, Díaz R, Martínez D, Pentinat T, Ramón-Krauel M, Ribó S et al. The role of nutrition on epigenetic modifications and their implications on health. Biochimie 2012;94:2242-63.
64. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA 2008;105:17046-9.
65. Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD et al. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet 2009;18:4046-53.
66. Lumey LH, Terry MB, Delgado-Cruzata L, Liao Y, Wang Q, Susser E et al. Adult global DNA methylation in relation to pre-natal nutrition. Int J Epidemiol 2012;41:116-23.
67. Waterland RA, Kellermayer R, Laritsky E, Rayco-Solon P, Harris RA, Travisano M et al. Season of conception in rural Gambia affects DNA methylation at putative human metastable epialleles. PLoS Genet 2010;6:e1001252.
68. Steegers-Theunissen RP, Obermann-Borst SA, Kremer D, Lindemans J, Siebel C, Steegers EA et al. Periconceptional maternal folic acid use of 400 micrograms per day is related to increased methylation of the IGF2 gene in the very young child. PLoS ONE 2009;4:e7845.
69. Hoyo C, Murtha AP, Schildkraut JM, Jirtle RL, Demark-Wahnefried W, Forman MR et al. Methylation variation at IGF2 differentially methylated regions and maternal folic acid use before and during pregnancy. Epigenetics 2011;6:928-36.
70. Haggarty P, Hoad G, Campbell DM, Horgan GW, Piyathilake C, McNeill G. Folate in pregnancy and imprinted gene and repeat element methylation in the offspring. Am J Clin Nutr 2013;97:94-9.
71. Khulan B, Cooper WN, Skinner BM, Bauer J, Owens S, Prentice AM et al. Periconceptional maternal micronutrient supplementation is associated with widespread gender related changes in the epigenome: a study of a unique resource in the Gambia. Hum Mol Genet 2012;21:2086-101.
72. Cooper WN, Khulan B, Owens S, Elks CE, Seidel V, Prentice AM et al. DNA methylation profiling at imprinted loci after periconceptional micronutrient supplementation in humans: results of a pilot randomized controlled trial. FASEB J 2012;26:1782-90.
73. Lee H-S, Barraza-Villarreal A, Biessy C, Duarte-Salles T, Sly PD, Ramakrishnan U et al. Dietary supplementation with polyunsaturated fatty acid during pregnancy modulates DNA methylation at IGF2/H19 imprinted genes and growth of infants. Physiol Genomics 2014;46:851-7.
74. Jiang X, Yan J, West AA, Perry CA, Malysheva OV, Devapatla S et al. Maternal choline intake alters the epigenetic state of fetal cortisol-regulating genes in humans. FASEB J 2012;26:3563-74.
75. Boeke CE, Baccarelli A, Kleinman KP, Burris HH, Litonjua AA, Rifas-Shiman SL et al. Gestational intake of methyl donors and global LINE-1 DNA methylation in maternal and cord blood: prospective results from a folate-replete population. Epigenetics 2012;7:253-60.
76. Ba Y, Yu H, Liu F, Geng X, Zhu C, Zhu Q et al. Relationship of folate, vitamin B12 and methylation of insulin-like growth factor-II in maternal and cord blood. Eur J Clin Nutr 2011;65:480-5.
77. Mill J, Heijmans BT. From promises to practical strategies in epigenetic epidemiology. Nat Rev Genet 2013;14:585-94.
78. Ioannidis JPA. Why most published research findings are false. PLoS Med 2005;2:e124.
79. Relton CL, Smith GD. Two-step epigenetic Mendelian randomization: a strategy for establishing the causal role of epigenetic processes in pathways to disease. Int J Epidemiol 2012;41:161-76.
80. Vineis P, Perera F. Molecular epidemiology and biomarkers in etiologic cancer research: the new in light of the old. Cancer Epidemiol Biomarkers Prev 2007;16:1954-65.
81. Wild CP. The exposome: from concept to utility. Int J Epidemiol 2012;41:24-32.
82. Herceg Z, Lambert M-P, van Veldhoven K, Demetriou C, Vineis P, Smith MT et al. Towards incorporating epigenetic mechanisms into carcinogen identification and evaluation. Carcinogenesis 2013;;34:1955-67.
83. Consortium TEP. The ENCODE (ENCyclopedia of DNA elements) project. Science 2004;306:636-40.
84. Fiorito G, Guarrera S, Valle C, Ricceri F, Russo A, Grioni S et al. B-vitamins intake, DNA-methylation of One Carbon Metabolism and homocysteine pathway genes and myocardial infarction risk: the EPICOR study. Nutr Metab Cardiovasc Dis 2014;24:483-8.
85. Christensen BC, Houseman EA, Marsit CJ, Zheng S, Wrensch MR, Wiemels JL et al. Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG Island context. PLoS Genet 2009;5:e1000602.
86. Wu H-C, Delgado-Cruzata L, Flom JD, Kappil M, Ferris JS, Liao Y et al. Global methylation profiles in DNA from different blood cell types. Epigenetics 2011;6:76-85.
87. Koestler DC, Marsit CJ, Christensen BC, Accomando W, Langevin SM, Houseman EA et al. Peripheral blood immune cell methylation profiles are associated with nonhematopoietic cancers. Cancer Epidemiol Biomarkers Prev 2012;21:1293-302.
88. Adalsteinsson BT, Gudnason H, Aspelund T, Harris TB, Launer LJ, Eiriksdottir G et al. Heterogeneity in white blood cells has potential to confound DNA methylation measurements. PLoS ONE 2012;7:e46705.
89. Scoccianti C, Ricceri F, Ferrari P, Cuenin C, Sacerdote C, Polidoro S et al. Methylation patterns in sentinel genes in peripheral blood cells of heavy smokers: influence of cruciferous vegetables in an intervention study. Epigenetics 2011;6:1114-19.
90. Verma M, Khoury MJ, Ioannidis JPA. Opportunities and challenges for selected emerging technologies in cancer epidemiology: mitochondrial, epigenomic, metabolomic, and telomerase profiling. Cancer Epidemiol Biomarkers Prev 2013;22:189-200.
91. Ma B, Wilker EH, Willis-Owen SAG, Byun H-M, Wong KCC, Motta V et al. Predicting DNA methylation level across human tissues. Nucleic Acids Res 2014;42:3515-28.
92. Herceg Z, Vaissière T. Epigenetic mechanisms and cancer: an interface between the environment and the genome. Epigenetics 2011;6:804-19.
93. Relton CL, Davey Smith G. Epigenetic epidemiology of common complex disease: prospects for prediction, prevention, and treatment. PLoS Med 2010;7:e1000356.
94. Martens JHA, Stunnenberg HG. BLUEPRINT: mapping human blood cell epigenomes. Haematologica 2013;98:1487-9.
95. Ziller MJ, Gu H, Müller F, Donaghey J, Tsai LT-Y, Kohlbacher O et al. Charting a dynamic DNA methylation landscape of the human genome. Nature 2013;500:477-81.
96. Perng W, Rozek LS, Mora-Plazas M, Duchin O, Marin C, Forero Y et al. Micronutrient status and global DNA methylation in school-age children. Epigenetics 2012;7:1133-41.