Gene × environment interaction by a longitudinal epigenome-wide association study (LEWAS) overcomes limitations of genome-wide association study (GWAS)

Epigenomics

Volumn 4, Issue 6, 2012, Pages 685-699

  Lahiri, Debomoy K ^a   Maloney, Bryan ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

association study; environment; epigenetics; epigenomics; genomics; GWAS; LEWAS

Indexed keywords

HEAVY METAL;

DIET SUPPLEMENTATION; DNA METHYLATION; DNA SEQUENCE; ENVIRONMENTAL FACTOR; EPIGENETICS; EXERCISE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOMICS; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; LONGITUDINAL EPIGENOME WIDE ASSOCIATION STUDY; MATERNAL CARE; OXIDATION; PRIORITY JOURNAL; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

EPIGENESIS, GENETIC; GENE-ENVIRONMENT INTERACTION; GENOME, HUMAN; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LONGITUDINAL STUDIES;

EID: 84871454822     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.12.60     Document Type: Review

References (112)

1. Goldstein DB. Common genetic variation and human traits. N. Engl. J. Med. 360(17), 1696-1698 (2009).
2. Kraft P, Hunter DJ. Genetic risk prediction -are we there yet? N. Engl. J. Med. 360(17), 1701-1703 (2009).
3. Hirschhorn JN. Genomewide association studies -illuminating biologic pathways. N. Engl. J. Med. 360(17), 1699-1701 (2009).
4. Klein RJ, Zeiss C, Chew EY et al. Complement factor H polymorphism in age-related macular degeneration. Science 308(5720), 385-389 (2005). (Pubitemid 40530070)
5. Galton F. Regression towards mediocrity in hereditary stature. J. Anthropol. Inst. 15, 246-263 (1886).
6. Aulchenko YS, Struchalin MV, Belonogova NM et al. Predicting human height by victorian and genomic methods. Eur. J. Hum. Genet. 17(8), 1070-1075 (2009).
7. Corder EH, Saunders AM, Strittmatter WJ et al. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261(5123), 921-923 (1993). (Pubitemid 23275809)
8. Hall K, Murrell J, Ogunniyi A et al. Cholesterol, APOE genotype, and Alzheimer disease: an epidemiologic study of Nigerian Yoruba. Neurology 66(2), 223-227 (2006). (Pubitemid 43970158)
9. Maloney B, Ge YW, Petersen RC et al. Functional characterization of three single-nucleotide polymorphisms present in the human APOE promoter sequence: Differential effects in neuronal cells and on DNA-protein interactions. Am. J. Med. Genet. B Neuropsychiatr. Genet. 153B(1), 185-201 (2010).
10. Selkoe DJ, Podlisny MB. Deciphering the genetic basis of Alzheimer's disease. Annu. Rev. Genomics Hum. Genet. 3, 67-99 (2002). (Pubitemid 35217431)
11. Lahiri DK. Prions: a piece of the puzzle? Science 337(6099), 1172 (2012).
12. Zelko IN, Mueller MR, Folz RJ. CpG methylation attenuates Sp1 and Sp3 binding to the human extracellular superoxide dismutase promoter and regulates its cell-specific expression. Free Radic. Biol. Med. 48(7), 895-904 (2010).
13. Valinluck V, Tsai HH, Rogstad DK, Burdzy A, Bird A, Sowers LC. Oxidative damage to methyl CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res. 32(14), 4100-4108 (2004). (Pubitemid 39232282)
14. Ghosh R, Mitchell DL. Effect of oxidative DNA damage in promoter elements on transcription factor binding. Nucleic Acids Res. 27(15), 3213-3218 (1999). (Pubitemid 29355738)
15. Zawia NH, Lahiri DK, Cardozo-Pelaez F. Epigenetics, oxidative stress, and Alzheimer disease. Free Radic. Biol. Med. 46(9), 1241-1249 (2009).
16. Ko M, Huang Y, Jankowska AM et al. Impaired hydroxylation of 5 methylcytosine in myeloid cancers with mutant TET2. Nature 468(7325), 839-843 (2010).
17. Maunakea AK, Chepelev I, Zhao K, Bruneau B. Epigenome mapping in normal and disease States. Circ. Res. 107(3), 327-339 (2010).
18. Lahiri DK, Maloney B, Zawia NH. The LEARn model: an epigenetic explanation for idiopathic neurobiological diseases. Mol. Psychiatry 14(11), 992-1003 (2009).
19. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 8(4), 253-262 (2007). (Pubitemid 46439287)
20. Heindel JJ, McAllister KA, Worth L Jr, Tyson FL. Environmental epigenomics, imprinting and disease susceptibility. Epigenetics 1(1), 1-6 (2006).
21. Kikuchi Y, Yasuhara T, Agari T et al. Urinary 8 OHdG elevations in a partial lesion rat model of Parkinson's disease correlate with behavioral symptoms and nigrostriatal dopaminergic depletion. J. Cell. Physiol. 226, 1390-1398 (2010).
22. Sacco A, Issa GC, Zhang Y et al. Epigenetic modifications as key regulators of Waldenstrom's macroglobulinemia biology. J. Hematol. Oncol. 3(1), 38 (2010).
23. Levenson VV. DNA methylation as a universal biomarker. Expert Rev. Mol. Diagn. 10(4), 481-488 (2010).
24. Butcher LM, Beck S. Future impact of integrated high-throughput methylome analyses on human health and disease. J. Genet. Genomics 35(7), 391-401 (2008). (Pubitemid 351978309)
25. Patel CJ, Bhattacharya J, Butte AJ. An environment-wide association study (EWAS) on Type 2 diabetes mellitus. PLoS One 5(5), e10746 (2010).
26. Rappaport SM, Smith MT. Environment and disease risks. Science 330, 460-461 (2010).
27. De la Burde B, Choate MS Jr. Does asymptomatic lead exposure in children have latent sequelae? J. Pediatr. 81(6), 1088-1091 (1972).
28. Finch CE, Crimmins EM. Inflammatory exposure and historical changes in human life-spans. Science 305(5691), 1736-1739 (2004). (Pubitemid 39249633)
29. Lahiri DK. An integrated approach to genome studies. Science 331(6014), 147 (2011).
30. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet 2(8663), 577-580 (1989). (Pubitemid 19216205)
31. Diorio J, Meaney MJ. Maternal programming of defensive responses through sustained effects on gene expression. J. Psychiatry Neurosci. 32(4), 275-284 (2007). (Pubitemid 47057461)
32. Weaver IC, Cervoni N, Champagne FA et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7(8), 847-854 (2004). (Pubitemid 38989508)
33. McGowan PO, Sasaki A, Huang TC et al. Promoter-wide hypermethylation of the ribosomal RNA gene promoter in the suicide brain. PLoS One 3(5), e2085 (2008).
34. Rusby JS, Tasker F. Long-term effects of the British evacuation of children during World War 2 on their adult mental health. Aging Ment. Health 13(3), 391-404 (2009).
35. Gluckman PD, Hanson MA, Beedle AS. Early life events and their consequences for later disease: a life history and evolutionary perspective. Am. J. Hum. Biol. 19(1), 1-19 (2007). (Pubitemid 46062455)
36. Ben-Shlomo Y, Kuh D. A life course approach to chronic disease epidemiology: conceptual models, empirical challenges and interdisciplinary perspectives. Int. J. Epidemiol. 31(2), 285-293 (2002). (Pubitemid 34537777)
37. Lynch J, Smith GD. A life course approach to chronic disease epidemiology. Annu. Rev. Public Health 26, 1-35 (2005). (Pubitemid 40547374)
38. Singh GK, Miller BA. Health, life expectancy, and mortality patterns among immigrant populations in the United States. Can. J. Public Health 95(3), I14-I21 (2004). (Pubitemid 38967878)
39. Crimmins EM, Soldo BJ, Kim JK, Alley DE. Using anthropometric indicators for Mexicans in the United States and Mexico to understand the selection of migrants and the "Hispanic paradox". Soc. Biol. 52(3-4), 164-177 (2005).
40. Singh GK, Hiatt RA. Trends and disparities in socioeconomic and behavioural characteristics, life expectancy, and cause-specific mortality of native-born and foreign-born populations in the United States, 1979-2003. Int. J. Epidemiol. 35(4), 903-919 (2006). (Pubitemid 44540740)
41. Batty GD, Shipley MJ, Gunnell D et al. Height, wealth, and health: an overview with new data from three longitudinal studies. Econ. Hum. Biol. 7(2), 137-152 (2009).
42. Vijh AK. Inverse trend between estimated worldwide frequency of major cancers and inferred infectious burdens of populations: possible role of adaptive immune system. Med. Hypotheses 62(6), 880-888 (2004). (Pubitemid 38680352)
43. Majumder D, Mukherjee A. A passage through systems biology to systems medicine: adoption of middle-out rational approaches towards the understanding of therapeutic outcomes in cancer. Analyst 136, 663-678 (2010).
44. Sternberg RV. DNA codes and information: formal structures and relational causes. Acta Biotheor. 56(3), 205-232 (2008).
45. Erickson RP. Somatic gene mutation and human disease other than cancer. Mutat. Res. 543(2), 125-136 (2003). (Pubitemid 36329167)
46. Erickson RP. Somatic gene mutation and human disease other than cancer: an update. Mutat. Res. 705(2), 96-106 (2010).
47. Alzualde A, Moreno F, Martinez-Lage P et al. Somatic mosaicism in a case of apparently sporadic Creutzfeldt-Jakob disease carrying a de novo D178N mutation in the PRNP gene. Am. J. Med. Genet. B Neuropsychiatr. Genet. 153B(7), 1283-1291 (2010).
48. Beck JA, Poulter M, Campbell TA et al. Somatic and germline mosaicism in sporadic early-onset Alzheimer's disease. Hum. Mol. Genet. 13(12), 1219-1224 (2004). (Pubitemid 38877875)
49. Sgaramella V. Variability of our somatic (Epi) genomes. Science 239, 32-33 (2010).
50. Bjornsson HT, Sigurdsson MI, Fallin MD et al. Intra-individual change over time in DNA methylation with familial clustering. JAMA 299(24), 2877-2883 (2008). (Pubitemid 351930887)
51. Murgatroyd C, Patchev AV, Wu Y et al. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat. Neurosci. 12(12), 1559-1566 (2009).
52. Hamilton ML, Van Remmen H, Drake JA et al. Does oxidative damage to DNA increase with age? Proc. Natl Acad. Sci. USA 98(18), 10469-10474 (2001). (Pubitemid 32803043)
53. Lu T, Pan Y, Kao SY et al. Gene regulation and DNA damage in the ageing human brain. Nature 429(6994), 883-891 (2004). (Pubitemid 38843301)
54. Buehlmeyer K, Doering F, Daniel H, Kindermann B, Schulz T, Michna H. Alteration of gene expression in rat colon mucosa after exercise. Ann. Anat. 190(1), 71-80 (2008). (Pubitemid 351168655)
55. Campos AC, Molognoni F, Melo FH et al. Oxidative stress modulates DNA methylation during melanocyte anchorage blockade associated with malignant transformation. Neoplasia 9(12), 1111-1121 (2007). (Pubitemid 350255359)
56. van Vliet J, Oates NA, Whitelaw E. Epigenetic mechanisms in the context of complex diseases. Cell. Mol. Life Sci. 64(12), 1531-1538 (2007). (Pubitemid 46954151)
57. Evans GW, Schamberg MA. Childhood poverty, chronic stress, and adult working memory. Proc. Natl Acad. Sci. USA 106(16), 6545-6549 (2009).
58. Dias-Ferreira E, Sousa JC, Melo I et al. Chronic stress causes frontostriatal reorganization and affects decision-making. Science 325(5940), 621-625 (2009).
59. Lahiri DK, Maloney B. The "LEARn" (latent early-life associated regulation) model integrates environmental risk factors and the developmental basis of Alzheimer's disease, and proposes remedial steps. Exp. Gerontol. 45(4), 291-296 (2010).
60. Harold D, Abraham R, Hollingworth P et al. Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. Nat. Genet. 41(10), 1088-1093 (2009).
61. Lambert JC, Heath S, Even G et al. Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat. Genet. 41(10), 1094-1099 (2009).
62. Almqvist E, Lake S, Axelman K, Johansson K, Winblad B. Screening of amyloid precursor protein gene mutation (APP 717 Val->Ile) in Swedish families with Alzheimer's disease. J. Neural Transm. Park. Dis. Dement. Sect. 6(2), 151-156 (1993). (Pubitemid 24014262)
63. Lahiri DK, Farlow MR, Sambamurti K, Greig NH, Giacobini E, Schneider LS. A critical analysis of new molecular targets and strategies for drug developments in Alzheimer's disease. Curr. Drug Targets 4(2), 97-112 (2003). (Pubitemid 36553583)
64. Mastroeni D, Coleman PD, Grover A, Sue L, McKee A, Rogers J. Differential DNA methylation in neurons of identical twins discordant for Alzheimer's disease. Alzheimers Dement. 5, P145-146 (2009).
65. Mastroeni D, McKee A, Grover A, Rogers J, Coleman PD. Epigenetic differences in cortical neurons from a pair of monozygotic twins discordant for Alzheimer's disease. PLoS One 4(8), e6617 (2009).
66. Grayson DR, Jia X, Chen Y et al. Reelin promoter hypermethylation in schizophrenia. Proc. Natl Acad. Sci. USA 102(26), 9341-9346 (2005). (Pubitemid 40923565)
67. Mastroeni D, Grover A, Delvaux E, Whiteside C, Coleman PD, Rogers J. Epigenetic changes in Alzheimer's disease: decrements in DNA methylation. Neurobiol. Aging 31(12), 2025-2037 (2010).
68. Siegmund KD, Connor CM, Campan M et al. DNA methylation in the human cerebral cortex is dynamically regulated throughout the life span and involves differentiated neurons. PLoS One 2(9), e895 (2007).
69. Tochigi M, Iwamoto K, Bundo M et al. Methylation status of the reelin promoter region in the brain of schizophrenic patients. Biol. Psychiatry 63(5), 530-533 (2008). (Pubitemid 351220790)
70. Barrachina M, Ferrer I. DNA methylation of Alzheimer disease and tauopathy-related genes in postmortem brain. J. Neuropathol. Exp. Neurol. 68(8), 880-891 (2009).
71. Schwob NG, Nalbantoglu J, Hastings KE, Mikkelsen T, Cashman NR. DNA cytosine methylation in brain of patients with Alzheimer's disease. Ann. Neurol. 28(1), 91-94 (1990). (Pubitemid 20222158)
72. Shen X, He Z, Li H et al. Distinct functional patterns of gene promoter hypomethylation and hypermethylation in cancer genomes. PLoS One 7(9), e44822 (2012).
73. Wu SC, Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 11(9), 607-620 (2010).
74. Miller CA, Sweatt JD. Covalent modification of DNA regulates memory formation. Neuron 53(6), 857-869 (2007). (Pubitemid 46367557)
75. Avery OT, MacLeod CM, McCarty M. Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type Iii. J. Exp. Med. 79(2), 137-158 (1944).
76. Vassar R, Bennett BD, Babu-Khan S et al. b-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286(5440), 735-741 (1999).
77. Esch FS, Keim PS, Beattie EC et al. Cleavage of amyloid b peptide during constitutive processing of its precursor. Science 248(4959), 1122-1124 (1990).
78. Small DH, Klaver DW, Foa L. Presenilins and the g-secretase: still a complex problem. Mol. Brain 3(1), 7 (2010).
79. Williams K, Christensen J, Pedersen MT et al. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473(7347), 343-348 (2011).
80. Guo JU, Su Y, Zhong C, Ming GL, Song H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145(3), 423-434 (2011).
81. Dolinoy DC, Huang D, Jirtle RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl Acad. Sci. USA 104(32), 13056-13061 (2007). (Pubitemid 351737592)
82. Branchi I, Karpova NN, D'Andrea I, Castren E, Alleva E. Epigenetic modifications induced by early enrichment are associated with changes in timing of induction of BDNF expression. Neurosci. Lett. 495(3), 168-172 (2011).
83. Vucetic Z, Kimmel J, Reyes TM. Chronic high-fat diet drives postnatal epigenetic regulation of mu-opioid receptor in the brain. Neuropsychopharmacology 36(6), 1199-1206 (2011).
84. American Association for Cancer Research Human Epigenome Task Force; European Union, Network of Excellence, Scientific Advisory Board. Moving AHEAD with an international human epigenome project. Nature 454(7205), 711-715 (2008).
85. Brena RM, Huang TH, Plass C. Toward a human epigenome. Nat. Genet. 38(12), 1359-1360 (2006). (Pubitemid 44837552)
86. Hughes LA, van den Brandt PA, de Bruine AP et al. Early life exposure to famine and colorectal cancer risk: a role for epigenetic mechanisms. PLoS One 4(11), e7951 (2009).
87. Waterland RA. Is epigenetics an important link between early life events and adult disease? Horm. Res. 71(Suppl. 1), 13-16 (2009).
88. Symonds ME, Sebert SP, Hyatt MA, Budge H. Nutritional programming of the metabolic syndrome. Nat. Rev. Endocrinol. 5(11), 604-610 (2009).
89. Basha MR, Wei W, Bakheet SA et al. The fetal basis of amyloidogenesis: exposure to lead and latent overexpression of amyloid precursor protein and b-amyloid in the aging brain. J. Neurosci. 25(4), 823-829 (2005). (Pubitemid 40170996)
90. Wu J, Basha MR, Brock B et al. Alzheimer's disease (AD)-like pathology in aged monkeys after infantile exposure to environmental metal lead (Pb), evidence for a developmental origin and environmental link for AD. J. Neurosci. 28(1), 3-9 (2008).
91. Wang Z, Willard HF. Evidence for sequence biases associated with patterns of histone methylation. BMC Genomics 13(1), 367 (2012).
92. Holliday R, Grigg GW. DNA methylation and mutation. Mutat. Res. 285(1), 61-67 (1993). (Pubitemid 23029555)
93. Jena NR. DNA damage by reactive species: mechanisms, mutation and repair. J. Biosci. 37(3), 503-517 (2012).
94. Kusch T, Florens L, Macdonald WH et al. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306(5704), 2084-2087 (2004). (Pubitemid 40007658)
95. Guzzetta G, Jurman G, Furlanello C. A machine learning pipeline for quantitative phenotype prediction from genotype data. BMC Bioinformat. 11(Suppl. 8), S3 (2010).
96. Yang Q, Wu H, Guo CY, Fox CS. Analyze multivariate phenotypes in genetic association studies by combining univariate association tests. Genet. Epidemiol. 34(5), 444-454 (2010).
97. Tanimura Y, Shimizu K, Tanabe K, Kono I, Ajisaka R. Effects of three consecutive days exercise on lymphocyte DNA damage in young men. Eur. J. Appl. Physiol. 110(2), 307-314 (2010).
98. Helbock HJ, Beckman KB, Shigenaga MK et al. DNA oxidation matters: the HPLC-electrochemical detection assay of 8 oxo deoxyguanosine and 8 oxo guanine. Proc. Natl Acad. Sci. USA 95(1), 288-293 (1998).
99. Ohno M, Miura T, Furuichi M et al. A genome-wide distribution of 8-oxoguanine correlates with the preferred regions for recombination and single nucleotide polymorphism in the human genome. Genome Res. 16(5), 567-575 (2006).
100. Fowler RG, White SJ, Koyama C, Moore SC, Dunn RL, Schaaper RM. Interactions among the Escherichia coli mutT, mutM, and mutY damage prevention pathways. DNA Repair (Amst.). 2(2), 159-173 (2003). (Pubitemid 36071503)
101. Struthers L, Patel R, Clark J, Thomas S. Direct detection of 8 oxodeoxyguanosine and 8-oxoguanine by avidin and its analogues. Anal. Biochem. 255(1), 20-31 (1998). (Pubitemid 28047615)
102. Kim YS, Leventhal BL, Koh YJ et al. Prevalence of autism spectrum disorders in a total population sample. Am. J. Psychiatry 168(9), 904-912 (2011).
103. Ferguson CJ. Is psychological research really as good as medical research? Effect size comparisons between psychology and medicine. Rev. Gen. Psych. 13(2), 130-136 (2009).
104. Bell CG, Beck S. The epigenomic interface between genome and environment in common complex diseases. Brief Funct. Genomics 9, 477-485 (2010).
105. Perry C, Mackay-Sim A, Feron F, McGrath J. Olfactory neural cells: an untapped diagnostic and therapeutic resource. The 2000 Ogura Lecture. Laryngoscope 112(4), 603-607 (2002). (Pubitemid 34285922)
106. Merikangas AK, Corvin AP, Gallagher L. Copy-number variants in neurodevelopmental disorders: promises and challenges. Trends Genet. 25(12), 536-544 (2009).
107. Need AC, Ge D, Weale ME et al. A genome-wide investigation of SNPs and CNVs in schizophrenia. PLoS Genet. 5(2), e1000373 (2009).
108. Jung SH, Yim SH, Hu HJ et al. Copy number alterations and expression profiles of candidate genes in a pulmonary inflammatory myofibroblastic tumor. Lung Cancer 70(2), 152-157 (2010).
109. Lu Y, Wu X, Dong Y, Xu Z, Zhang Y, Xie Z. Anesthetic sevoflurane causes neurotoxicity differently in neonatal naive and Alzheimer disease transgenic mice. Anesthesiology 112(6), 1404-1416 (2010).
110. Lahiri DK, Maloney B. Genes are not our destiny: the somatic epitype bridges between the genotype and the phenotype. Nat. Rev. Neurosci. 7 (2006). www.nature.com/nrn/journal/v7/n12/full/ nrn2022-c1.html
111. ADNI 2 Study. www.adcs.org/Studies/ImagineADNI2.aspx
112. Candy Dynamics Expands Recall to all Toxic Waste® Brand Nuclear Sludge® Products all Flavors and all Sizes. www.fda.gov/Safety/Recalls/ ucm241359.htm