DNA methylation in white blood cells: Association with risk factors in epidemiologic studies

Epigenetics

Volumn 6, Issue 7, 2011, Pages 828-837

  Terry, Mary Beth ^a   Delgado Cruzata, Lissette ^a   Vin Raviv, Neomi ^a   Wu, Hui Chen ^a   Santella, Regina M ^a  

^a

^b United States

Author keywords

DNA methylation; Epidemiology; Gene specific; Global; Risk factors; White blood cells

Indexed keywords

ALCOHOL; ARSENIC; BENZENE; CELL DNA; FOLIC ACID; NONSTEROID ANTIINFLAMMATORY AGENT; PLACEBO;

AGE; AIR POLLUTION; ALCOHOL CONSUMPTION; ALZHEIMER DISEASE; ARTICLE; ASTHMA; BODY MASS; BODY SIZE; CIGARETTE SMOKING; CPG ISLAND; DIETARY INTAKE; DNA METHYLATION; EPIGENETICS; ETHNICITY; GENDER; GENE EXPRESSION REGULATION; HISTONE MODIFICATION; HUMAN; LEUKOCYTE; LEUKOCYTOSIS; PHYSICAL ACTIVITY; PRENATAL EXPOSURE; RACE; RISK FACTOR;

EID: 79960124631     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.6.7.16500     Document Type: Article

References (94)

1. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002; 3:415-428.
2. Feinberg AP, Tycko B. The history of cancer epigenetics. Nat Rev Cancer 2004; 4:143-153.
3. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 1983; 301:89-92.
4. Tyko B. Genetic and epigenetic mosaicism in cancer precursor tissues. Ann NY Acad Sci 2003; 983:43-54.
5. Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene 2002; 21:5400-5413.
6. Feinberg AP. The epigenetics of cancer etiology. Semin Cancer Biol 2004; 14:427-432.
7. Feinberg AP, Gehrke CW, Kuo KC, Ehrlich M. Reduced genomic 5-methylcytosine content in human colonic neoplasia. Cancer Res 1988; 48:1159-1161.
8. Fraga MF, Esteller M. DNA methylation: a profile of methods and applications. Biotechniques 2002; 33: 636-649.
9. Bjornsson HT, Sigurdsson MI, Fallin MD, Irizarry RA, Aspelund T, Cui H, et al. Intra-individual change over time in DNA methylation with familial clustering. JAMA 2008; 299:2877-2883.
10. Breitling Lutz P, Yang R, Korn B, Burwinkel B, Brenner H. Tobacco-smoking-related differential DNA methylation: 27K discovery and replication. Am J Hum Genet 2011; 88:450-7.
11. Teschendorff AE, Menon U, Gentry-Maharaj A, Ramus SJ, Gayther SA, Apostolidou S, et al. An epigenetic signature in peripheral blood predicts active ovarian Ccancer. PLoS One 2009; 4:8274.
12. Taby R, Issa JPJ. Cancer epigenetics. CA Cancer J Clin 2010; 60:376-392.
13. Zhang YJ, Wu HC, Shen J, Ahsan H, Tsai WY, Yang HI, et al. Predicting hepatocellular carcinoma by detection of aberrant promoter methylation in serum DNA. Clin Cancer Res 2007; 13:2378-2384.
14. Lim U, Flood A, Choi SW, Albanes D, Cross AJ, Schatzkin A, et al. Genomic methylation of leukocyte DNA in relation to colorectal adenoma among asymptomatic women. Gastroenterology 2008; 134:47-55.
15. Pufulete M, Al-Ghnaniem R, Leather AJM, Appleby P, Gout S, Terry C, et al. Folate status, genomic DNA hypomethylation and risk of colorectal adenoma and cancer: a case control study. Gastroenterology 2003; 124:1240-1248.
16. Cash HL, Tao L, Yuan JM, Marsit CJ, Houseman EA, Xiang YB, et al. LINE-1 hypomethylation is associated with bladder cancer risk among non-smoking Chinese. Int J Cancer 2011.
17. Wilhelm CS, Kelsey KT, Butler R, Plaza S, Gagne L, Zens MS, et al. Implications of LINE1 methylation for bladder cancer risk in women. Clin Cancer Res 2010; 16:1682-1689.
18. Moore LE, Pfeiffer RM, Poscablo C, Real FX, Kogevinas M, Silverman D, et al. Genomic DNA hypomethylation as a biomarker for bladder cancer susceptibility in the Spanish Bladder Cancer Study: a case-control study. Lancet Oncol 2008; 9: 359-366.
19. Hou L, Wang H, Sartori S, Gawron A, Lissowska J, Bollati V, et al. Blood leukocyte DNA hypomethylation and gastric cancer risk in a high-risk Polish population. Int J Cancer 2010; 127:1866-1874.
20. Choi JY, James SR, Link PA, McCann SE, Hong CC, Davis W, et al. Association between global DNA hypomethylation in leukocytes and risk of breast cancer. Carcinogenesis 2009; 30:1889-1897.
21. Hsiung D, Marsit C, Houseman E, Eddy K, Furniss C, McClean M, et al. Global DNA methylation level in whole blood as a biomarker in head and neck squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 2007; 16:108-114.
22. Widschwendter M, Apostolidou S, Raum E, Rothenbacher D, Fiegl H, Menon U, et al. Epigenotyping in peripheral blood cell DNA and breast cancer risk: A proof of principle study. PLoS One 2008; 3:2656.
23. Flanagan JM, Munoz-Alegre M, Henderson S, Tang T, Sun P, Johnson N, et al. Gene-body hypermethylation of ATM in peripheral blood DNA of bilateral breast cancer patients. Hum Mol Genet 2009; 18:1332-1342.
24. Kaaks R, Stattin P, Villar S, Poetsch AR, Dossus L, Nieters A, et al. Insulin-like growth factor-II methylation status in lymphocyte DNA and colon cancer risk in the northern Sweden Health and Disease Cohort. Cancer Res 2009; 69:5400-5405.
25. Hoffman AE, Yi CH, Zheng T, Stevens RG, Leaderer D, Zhang Y, et al. CLOCK in breast tumorigenesis: Genetic, epigenetic and transcriptional profiling analyses. Cancer Res 2010; 70:1459-1468.
26. Iwamoto T, Yamamoto N, Taguchi T, Tamaki Y, Noguchi S. BRCA1 promoter methylation in peripheral blood cells is associated with increased risk of breast cancer with BRCA1 promoter methylation. Breast Cancer Res Treat 2010; 1-9.
27. Wong EM, Southey MC, Fox SB, Brown MA, Dowty JG, Jenkins MA, et al. Constitutional methylation of the BRCA1 promoter is specifically associated with BRCA1 mutation-associated pathology in early-onset breast cancer. Cancer Prev Res 2011; 4:23-33.
28. Brooks WH, Le Dantec C, Pers JO, Youinou P, Renaudineau Y. Epigenetics and autoimmunity. J Autoimmun 2010; 34:207-219.
29. Ho SM. Environmental epigenetics of asthma: An update. J Allergy Clin Immunol 2010; 126:453-465.
30. Chouliaras L, Rutten BPF, Kenis G, Peerbooms O, Visser PJ, Verhey F, et al. Epigenetic regulation in the pathophysiology of Alzheimer's disease. Prog Neurobiol 2010; 90:498-510.
31. Shimabukuro M, Sasaki T, Imamura A, Tsujita T, Fuke C, Umekage T, et al. Global hypomethylation of peripheral leukocyte DNA in male patients with schizophrenia: A potential link between epigenetics and schizophrenia. J Psychiatr Res 2007; 41:1042-1046.
32. Romermann D, Hasemeier B, Metzig K, Gohring G, Schlegelberger B, Langer F, et al. Global increase in DNA methylation in patients with myelodysplastic syndrome. Leukemia 2008; 22:1954-1956.
33. 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 Genet 2004; 68:196-204.
34. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Nat Acad Sci USA 2005; 102:10604-10609.
35. Pilsner JR, Liu X, Ahsan H, Ilievski V, Slavkovich V, Levy D, et al. Genomic methylation of peripheral blood leukocyte DNA: influences of arsenic and folate in Bangladeshi adults. Am J Clin Nutr 2007; 86:1179-1186.
36. Bollati V, Schwartz J, Wright R, Litonjua A, Tarantini L, Suh H, et al. Decline in genomic DNA methylation through aging in a cohort of elderly subjects. Mech Ageing Dev 2009; 130:234-239.
37. Zhu ZZ, Hou L, Bollati V, Tarantini L, Marinelli B, Cantone L, et al. Predictors of global methylation levels in blood DNA of healthy subjects: a combined analysis. Int J Epidemiol 2010; 1-10.
38. El-Maarri O, Walier M, Behne F, van uum J, Singer H, Diaz-Lacava A, et al. Methylation at global LINE-1 repeats in human blood are affected by gender but not by age or natural hormone cycles. PLoS One 2011; 6:16252.
39. Zhang FF, Cardarelli R, Carroll J, Fulda KG, Kaur M, Gonzalez K, et al. Significant differences in global genomic DNA methylation by gender and race/ethnicity in peripheral blood. Epigenetics 2011; 6.
40. Chalitchagorn K, Shuangshoti S, Hourpai N, Kongruttanachok N, Tangkijvanich P, Thong-ngam D, et al. Distinctive pattern of LINE-1 methylation level in normal tissues and the association with carcinogenesis. Oncogene 2004; 23:8841-8846.
41. Kim KY, Kim DS, Lee SK, Lee IK, Kang JH, Chang YS, et al. Association of low-dose exposure to persistent organic pollutants with global DNA hypomethylation in healthy Koreans. Environ Health Perspect 2009; 118.
42. Sarter B, Long TI, Tsong WH, Koh WP, Yu MC, Laird PW. Sex differential in methylation patterns of selected genes in Singapore Chinese. Hum Genet 2005; 117:402-403.
43. Tra J, Kondo T, Lu Q, Kuick R, Hanash S, Richardson B. Infrequent occurrence of age-dependent changes in CpG island methylation as detected by restriction landmark genome scanning. Mech Ageing Dev 2002; 123:1487-1503.
44. Boks MP, Derks EM, Weisenberger DJ, Strengman E, Janson E, Sommer IE, et al. The relationship of DNA methylation with age, gender and genotype in twins and healthy controls. PLoS One 2009; 4:6767.
45. Eckhardt F, Lewin J, Cortese R, Rakyan VK, Attwood J, Burger M, et al. DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 2006; 38: 1378-1385.
46. El-Maarri O, Becker T, Junen J, Manzoor S, Diaz-Lacava A, Schwaab R, et al. Gender specific differences in levels of DNA methylation at selected loci from human total blood: a tendency toward higher methylation levels in males. Hum Genet 2007; 122: 505-514.
47. Foley DL, Craig JM, Morley R, Olsson CJ, Dwyer T, Smith K, et al. Prospects for epigenetic epidemiology. Am J Epidemiol 2009; 169:389-400.
48. Jaenisch R, Hochedlinger K, Blelloch R, Yamada Y, Baldwin K, Eggan K. Nuclear cloning, epigenetic reprogramming and cellular differentiation. Cold Spring Harb Symp Quant Biol 2004; 69: 19-27.
49. Bjornsson HT, Fallin MD, Feinberg AP. An integrated epigenetic and genetic approach to common human disease. Trends Genet 2004; 20:350-358.
50. Herceg Z. Epigenetics and cancer: towards an evaluation of the impact of environmental and dietary factors. Mutagenesis 2007; 22:91-103.
51. Shen Y, Matsuno Y, Fouse SD, Rao N, Root S, Xu R, et al. X-inactivation in female human embryonic stem cells is in a nonrandom pattern and prone to epigenetic alterations. Proc Natl Acad Sci USA 2008; 105:4709-4714.
52. Wong CC, Caspi A, Williams B, Craig IW, Houts R, Ambler A, et al. A longitudinal study of epigenetic variation in twins. Epigenetics 2010; 5:516-526.
53. 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; 17:2306-2310.
54. Axume J, Smith SS, Pogribny IP, Moriarty DJ, Caudill MA. Global leukocyte DNA methylation is similar in African American and Caucasian women under conditions of controlled folate intake. Epigenetics 2007; 2:66-68.
55. Bollati V, Baccarelli A, Hou L, Bonzini M, Fustinoni S, Cavallo D, et al. Changes in DNA methylation patterns in subjects exposed to low-dose Benzene. Cancer Res 2007; 67:876-880.
56. Xing C, Wang Qf, Li B, Tian H, Ni Y, Yin S, et al. Methylation and expression analysis of tumor suppressor genes p15 and p16 in benzene poisoning. Chem Biol Interact 2010; 184:306-9.
57. Rusiecki JA, Baccarelli A, Bollati V, Tarantini L, Moore LE, Bonefeld-Jorgensen EC. Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic Inuit. Environ Health Perspect 2008; 116.
58. Pilsner JR, Hu H, Ettinger A, Sánchez BN, Wright RO, Cantonwine D, et al. Influence of prenatal lead exposure on genomic methylation of cord blood DNA. Environ Health Perspect 2009; 117.
59. Wright RO, Schwartz J, Wright RJ, Bollati V, Tarantini L, Park SK, et al. Biomarkers of lead exposure and DNA methylation within retrotransposons. Environ Health Perspect 2010; 118.
60. Chanda S, Dasgupta UB, GuhaMazumder D, Gupta M, Chaudhuri U, Lahiri S, et al. DNA hypermethylation of promoter of gene p53 and p16 in arsenic-exposed people with and without malignancy. Toxicol Sci 2006; 89: 431-437.
61. Zhang AH, Bin HH, Pan XL, Xi XG. Analysis of p16 gene mutation, deletion and methylation in patients with arseniasis produced by indoor unventilated-stove coal usage in Guizhou, China. J Toxicol Environ Health A 2007; 70:970-975.
62. Tarantini L, Bonzini M, Apostoli P, Pegoraro V, Bollati V, Marinelli B, et al. Effects of particulate matter on genomic DNA methylation content and iNOS promoter methylation. Environ Health Perspect 2009; 117.
63. 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; 179:572-578.
64. Madrigano J, Baccarelli A, Mittleman MA, Wright RO, Sparrow D, Vokonas PS, et al. Prolonged exposure to particulate pollution, genes associated with glutathione pathways and DNA methylation in a cohort of older men. Environ Health Perspect 2011.
65. DeMarini DM. Genotoxicity of tobacco smoke and tobacco smoke condensate: a review. Mutat Res 2004; 567:447-474.
66. Piyathilake CJ, Macaluso M, Hine RJ, Richards EW, Krumdieck CL. Local and systemic effects of cigarette smoking on folate and vitamin B-12. Am J Clin Nutr 1994; 60:559-566.
67. Mortusewicz O, Schermelleh L, Walter J, Cardoso MC, Leonhardt H. Recruitment of DNA methyltransferase I to DNA repair sites. Proc Nat Acad Sci USA 2005; 102:8905-8909.
68. Hillemacher T, Frieling H, Moskau S, Muschler MAN, Semmler A, Kornhuber J, et al. Global DNA methylation is influenced by smoking behaviour. Eur Neuropsychopharmacol 2008; 18:295-298.
69. Figueiredo JC, Grau MV, Wallace K, Levine AJ, Shen L, Hamdan R, et al. Global DNA hypomethylation (LINE-1) in the normal colon and lifestyle characteristics and dietary and genetic factors. Cancer Epidemiol Biomarkers Prev 2009; 18:1041-1049.
70. Leger AJ, Covic L, Kuliopulos A. Protease-activated receptors in cardiovascular diseases. Circulation 2006; 114:1070-1077.
71. Philibert RA, Beach SRH, Gunter TD, Brody GH, Madan A, Gerrard M. The effect of smoking on MAOA promoter methylation in DNA prepared from lymphoblasts and whole blood. Am J Med Genet B Neuropsychiatr Genet 2009; 153:619-628.
72. Xu Q, Ma JZ, Payne TJ, Li MD. Determination of methylated CpG sites in the promoter region of catecholo-methyltransferase (COMT) and their involvement in the etiology of tobacco smoking. Front Psychiatry 2010; 1:16.
73. Flom J, Ferris J, Gonzalez K, Santella R, Terry MB. Prenatal tobacco smoke exposure and genomewide methylation in adulthood. Cancer Epidemiol Biomarkers Prev 2011; 20:720.
74. Toledo-Rodriguez M, Lotfipour S, Leonard G, Perron M, Richer L, Veillette S, et al. Maternal smoking during pregnancy is associated with epigenetic modifications of the brain-derived neurotrophic factor-6 exon in adolescent offspring. Am J Med Genet B Neuropsychiatr Genet 2010; 153:1350-1354.
75. Tobi EW, Heijmans BT, Kremer D, Putter H, Delemarre-van de Waal HA, Finken MJ, et al. DNA methylation of IGF2, GNASAS, INSIGF and LEP and being born small for gestational age. Epigenetics 2011; 6:171-176.
76. Hamid A, Wani NA, Kaur J. New perspectives on folate transport in relation to alcoholism-induced folate malabsorption- association with epigenome stability and cancer development. FEBS J 2009; 276:2175-2191.
77. Bönsch D, Lenz B, Reulbach U, Kornhuber J, Bleich S. Homocysteine associated genomic DNA hypermethylation in patients with chronic alcoholism. J Neural Transm 2004; 111:1611-1616.
78. Bleich S, Lenz B, Ziegenbein M, Beutler S, Frieling H, Kornhuber J, et al. Epigenetic DNA hypermethylation of the HERP gene promoter induces downregulation of its mRNA expression in patients with alcohol dependence. Alcohol Clin Exp Res 2006; 30:587-591.
79. Zhang FF, Cardarelli R, Carroll J, Zhang S, Fulda KG, Gonzalez K, et al. Physical activity and global genomic DNA methylation in a cancer-free population. Epigenetics 2011; 6:293-299.
80. Piyathilake C, Badiga S, Johanning G, Alvarez R, Partridge E. Predictors and health consequences of epigenetic changes associated with excess body weight in women of child-bearing age. Cancer Epidemiol Biomarkers Prev 2011; 20:719.
81. Kok RM, Smith DE, Barto R, Spijkerman AM, Teerlink T, Gellekink HJ, et al. Global DNA methylation measured by liquid chromatography-tandem mass spectrometry: analytical technique, reference values and determinants in healthy subjects. Clin Chem Lab Med 2007; 45:903-911.
82. 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; 105:17046-17049.
83. Simonetta F, Stefania LF, Hyeran J, J SE, Roberto C, Sang-Woon C. Oestrogen replacement therapy reduces total plasma homocysteine and enhances genomic DNA methylation in postmenopausal women. Br J Nutr 2007; 97:617-621.
84. Jacob RA, Gretz DM, Taylor PC, James SJ, Pogribny IP, Miller BJ, et al. Moderate folate depletion increases plasma homocysteine and decreases lymphocyte DNA methylation in postmenopausal women. J Nutr 1998; 128:1204-1212.
85. Fenech M, Aitken C, Rinaldi J. Folate, vitamin B12, homocysteine status and DNA damage in young Australian adults. Carcinogenesis 1998; 19:1163-1171.
86. Rampersaud GC, Kauwell GP, Hutson AD, Cerda JJ, Bailey LB. Genomic DNA methylation decreases in response to moderate folate depletion in elderly women. Am J Clin Nutr 2000; 72:998-1003.
87. Shelnutt KP, Kauwell GPA, Gregory JF, Maneval DR, Quinlivan EP, Theriaque DW, et al. Methylenetetrahydrofolate reductase 677Câ†'T polymorphism affects DNA methylation in response to controlled folate intake in young women. J Nutr Biochem 2004; 15:554-560.
88. Basten GP, Duthie SJ, Pirie L, Vaughan N, Hill MH, Powers HJ. Sensitivity of markers of DNA stability and DNA repair activity to folate supplementation in healthy volunteers. Br J Cancer 2006; 94:1942-1947.
89. Axume J, Smith SS, Pogribny IP, Moriarty DJ, Caudill MA. The MTHFR 677TT genotype and folate intake interact to lower global leukocyte DNA methylation in young Mexican American women. Nutr Res 2007; 27:1365-1417.
90. Wu HC, 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.
91. Quindry JC, Stone WL, King J, Broeder CE. The effects of acute exercise on neutrophils and plasma oxidative stress. Med Sci Sports Exerc 2003; 35:1139-1145.
92. Zorrilla EP, Luborsky L, McKay JR, Rosenthal R, Houldin A, Tax A, et al. The relationship of depression and stressors to immunological assays: a meta-analyticreview. Brain Behav Immun 2001; 15:199-226.
93. Tavares-Murta BM, Mendonça MA, Duarte NL, da Silva JA, Mutão TS, Garcia CB, et al. Systemic leukocyte alterations are associated with invasive uterine cervical cancer. Int J Gynecol Cancer 2010; 20:1154-1159.
94. Martin GM. Epigenetic drift in aging identical twins. Proc Nat Acad Sci USA 2005; 102:10413-10414.