Life course socioeconomic status and DNA methylation in genes related to stress reactivity and inflammation: The multi-ethnic study of atherosclerosis

Epigenetics

Volumn 10, Issue 10, 2015, Pages 958-969

  Needham, Belinda L ^a   Smith, Jennifer A ^a   Zhao, Wei ^a   Wang, Xu ^b   Mukherjee, Bhramar ^a   Kardia, Sharon L R ^a   Shively, Carol A ^c   Seeman, Teresa E ^d   Liu, Yongmei ^c   Roux, Ava V Diez ^b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b DREXEL UNIVERSITY   (United States)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DNA methylation; Gene expression; Inflammation; Socioeconomic status; Stress reactivity

Indexed keywords

ADULT; AGED; ARTICLE; ATHEROSCLEROSIS; AVP GENE; CCL1 GENE; CD1D GENE; DNA METHYLATION; ETHNIC GROUP; F8 GENE; FEMALE; FKBP5 GENE; GENE; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HUMAN; INFLAMMATION; KLRG1 GENE; MALE; MONOCYTE; NLRP12 GENE; OXTR GENE; PYDC1 GENE; SOCIAL CLASS; SOCIAL STATUS; STRESS; TLR3 GENE; AFRICAN AMERICAN; CAUCASIAN; GENE EXPRESSION REGULATION; GENETICS; HISPANIC; MENTAL STRESS; MIDDLE AGED; PATHOLOGY; PROTEIN SYNTHESIS; PSYCHOLOGY; VERY ELDERLY;

AFRICAN AMERICANS; AGED; AGED, 80 AND OVER; ATHEROSCLEROSIS; DNA METHYLATION; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; GENE EXPRESSION REGULATION; HISPANIC AMERICANS; HUMANS; INFLAMMATION; MALE; MIDDLE AGED; PROTEIN BIOSYNTHESIS; SOCIAL CLASS; STRESS, PSYCHOLOGICAL;

EID: 84953872896     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.1080/15592294.2015.1085139     Document Type: Article

References (60)

1. Adler NE, Rehkopf DH. US disparities in health: Descriptions, causes, and mechanisms. Ann Rev Public Health 2008; 29:235-52.; PMID:18031225; http://dx.doi.org/10.1146/annurev.publhealth.29.020907.090852
2. Glaser R, Kiecolt-Glaser JK. Stress-induced immune dysfunction: implications for health. Nat Rev Immunol 2005; 5:243-51.; PMID:15738954; http://dx.doi.org/10.1038/nri1571
3. Cohen S, Schwartz J, Epel E, Kirschbaum C, Sidney S, Seeman T. Socioeconomic status, race, and diurnal cortisol decline in the Coronary Artery Risk Development in Young Adults (CARDIA) Study. Psychosom Med 2006; 68:41-50.; PMID:16449410; http://dx.doi.org/10.1097/01.psy.0000195967.51768.ea
4. Janicki-Deverts D, Cohen S, Adler N, Schwartz J, Matthews K, Seeman T. Socioeconomic status is related to urinary catecholamines in the Coronary Artery Risk Development in Young Adults (CARDIA) study. Psychosom Med 2007; 69:514-20.; PMID:17636147; http://dx.doi.org/10.1097/PSY.0b013e3180f60645
5. Stringhini S, Batty GD, Bovet P, Shipley MJ, Marmot MG, Kumari M, Tabak AG, Kivimaki M. Association of lifecourse socioeconomic status with chronic inflammation and type 2 diabetes risk: the Whitehall II prospective cohort study. PLoS Medicine 2013; 10: e1001479
6. Champagne FA. Epigenetic influence of social experiences across the lifespan. Dev Psychobiol 2010; 52:299-311; http://dx.doi.org/10.1002/dev.20436
7. McGowan PO, Szyf M. The epigenetics of social adversity in early life: implications for mental health outcomes. Neurobiol Disease 2010; 39:66-72; http://dx.doi.org/10.1016/j.nbd.2009.12.026
8. Szyf M, Meaney MJ. Epigenetics, behaviour, and health. Allergy Asthma and Clin Immunol 2008; 4:37-49.; PMID:20525124; http://dx.doi.org/10.1186/1710-1492-4-1-37
9. Szyf M. DNA methylation, behavior and early life adversity. J Genet Genomics 2013; 40:331-8.; PMID:23876773; http://dx.doi.org/10.1016/j.jgg.2013.06.004
10. Szyf M. Mind-body interrelationship in DNA methylation. Chem Immunol Allergy 2012; 98:85-99.; PMID:22767059; http://dx.doi.org/10.1159/000336503
11. Borghol N, Suderman M, McArdle W, Racine A, Hallett M, Pembrey M, Hertzman C, Power C, Szyf M. Associations with early-life socio-economic position in adult DNA methylation. Int J Epidemiol 2012; 41:62-74.; PMID:22422449; http://dx.doi.org/10.1093/ije/dyr147
12. Lam LL, Emberly E, Fraser HB, Neumann SM, Chen E, Miller GE, Kobor MS. Factors underlying variable DNA methylation in a human community cohort. Proc Natl Acad Sci USA 2012; 109 Suppl 2:17253-60; http://dx.doi.org/10.1073/pnas.1121249109
13. McGuinness D, McGlynn LM, Johnson PC, MacIntyre A, Batty GD, Burns H, Cavanagh J, Deans KA, Ford I, McConnachie A, et al. Socio-economic status is associated with epigenetic differences in the pSoBid cohort. Int J Epidemiol 2012; 41:151-60.; PMID:22253320; http://dx.doi.org/10.1093/ije/dyr215
14. Tehranifar P, Wu HC, Fan X, Flom JD, Ferris JS, Cho YH, Gonzalez K, Santella RM, Terry MB. Early life socioeconomic factors and genomic DNA methylation in mid-life. Epigenetics 2013; 8:23-7; http://dx.doi.org/10.4161/epi.22989
15. Subramanyam MA, Diez-Roux AV, Pilsner JR, Villamor E, Donohue KM, Liu Y, Jenny NS. Social factors and leukocyte DNA methylation of repetitive sequences: the multi-ethnic study of atherosclerosis. PLoS One 2013; 8:e54018.; PMID:23320117; http://dx.doi.org/10.1371/journal.pone.0054018
16. Perng W, Rozek LS, Mora-Plazas M, Duchin O, Marin C, Forero Y, Baylin A, Villamor E. Micronutrient status and global DNA methylation in school-age children. Epigenetics 2012; 7:1133-41; http://dx.doi.org/10.4161/epi.21915
17. Obermann-Borst SA, Heijmans BT, Eilers PH, Tobi EW, Steegers EA, Slagboom PE, Steegers-Theunissen RP. 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.; PMID:25102259; http://dx.doi.org/10.1017/S2040174412000293
18. Appleton AA, Armstrong DA, Lesseur C, Lee J, Padbury JF, Lester BM, Marsit CJ. Patterning in placental 11-B hydroxysteroid dehydrogenase methylation according to prenatal socioeconomic adversity. PLoS One 2013; 8:e74691.; PMID:24040322; http://dx.doi.org/10.1371/journal.pone.0074691
19. Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmuhl Y, Fischer D, Holsboer F, Wotjak CT, Almeida OF, Spengler D. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 2009; 12:1559-66.; PMID:19898468; http://dx.doi.org/10.1038/nn.2436
20. Roth TL, Zoladz PR, Sweatt JD, Diamond DM. Epigenetic modification of hippocampal Bdnf DNA in adult rats in an animal model of post-traumatic stress disorder. J Psychiatric Res 2011; 45:919-26.; PMID:21306736; http://dx.doi.org/10.1016/j.jpsychires.2011.01.013
21. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 2006; 9:519-25.; PMID:16501568; http://dx.doi.org/10.1038/nn1659
22. Elliott E, Ezra-Nevo G, Regev L, Neufeld-Cohen A, Chen A. Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice. Nat Neurosci 2010; 13:1351-3.; PMID:20890295; http://dx.doi.org/10.1038/nn.2642
23. Lee RS, Tamashiro KL, Yang X, Purcell RH, Huo Y, Rongione M, Potash JB, Wand GS. A measure of glucocorticoid load provided by DNA methylation of Fkbp5 in mice. Psychopharmacology 2011; 218:303-12.; PMID:21509501; http://dx.doi.org/10.1007/s00213-011-2307-3
24. Francis DD, Champagne FA, Liu D, Meaney MJ. Maternal care, gene expression, and the development of individual differences in stress reactivity. Ann N Y Acad Sci 1999; 896:66-84.; PMID:10681889; http://dx.doi.org/10.1111/j.1749-6632.1999.tb08106.x
25. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 1997; 277:1659-62.; PMID:9287218; http://dx.doi.org/10.1126/science.277.5332.1659
26. Weaver IC, Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. Epigenetic programming by maternal behavior. Nat Neurosci 2004; 7:847-54.; PMID:15220929; http://dx.doi.org/10.1038/nn1276
27. McGowan PO, Sasaki A, D’Alessio AC, Dymov S, Labonte B, Szyf M, Turecki G, Meaney MJ. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci 2009; 12:342-8.; PMID:19234457; http://dx.doi.org/10.1038/nn.2270
28. Tyrka AR, Price LH, Marsit C, Walters OC, Carpenter LL. Childhood adversity and epigenetic modulation of the leukocyte glucocorticoid receptor: preliminary findings in healthy adults. PLoS One 2012; 7:e30148.; PMID:22295073; http://dx.doi.org/10.1371/journal.pone.0030148
29. Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008; 3:97-106; http://dx.doi.org/10.4161/epi.3.2.6034
30. Unternaehrer E, Luers P, Mill J, Dempster E, Meyer AH, Staehli S, Lieb R, Hellhammer DH, Meinlschmidt G. Dynamic changes in DNA methylation of stressassociated genes (OXTR, BDNF) after acute psychosocial stress. Translational Psychiatry 2012; 2:e150.; PMID:22892716; http://dx.doi.org/10.1038/tp.2012.77
31. Kinnally EL, Capitanio JP, Leibel R, Deng L, LeDuc C, Haghighi F, Mann JJ. Epigenetic regulation of serotonin transporter expression and behavior in infant rhesus macaques. Genes Brain Behav 2010; 9:575-82.; PMID:20398062; http://dx.doi.org/10.1111/j.1601-183X.2009.00533.x
32. Beach SR, Brody GH, Todorov AA, Gunter TD, Philibert RA. Methylation at 5HTT mediates the impact of child sex abuse on women’s antisocial behavior: an examination of the Iowa adoptee sample. Psychosom Med 2011; 73:83-7.; PMID:20947778; http://dx.doi.org/10.1097/PSY.0b013e3181fdd074
33. Philibert RA, Sandhu H, Hollenbeck N, Gunter T, Adams W, Madan A. The relationship of 5HTT (SLC6A4) methylation and genotype on mRNA expression and liability to major depression and alcohol dependence in subjects from the Iowa Adoption Studies. Am J Med Genet Neuropsychiatric Genet 2008; 147B:543-9.; PMID:17987668; http://dx.doi.org/10.1002/ajmg.b.30657
34. Kinnally EL. Epigenetic plasticity following early stress predicts long-term health outcomes in rhesus macaques. Am J Phys Anthropol 2014; 155:192-9.; PMID:25100197; http://dx.doi.org/10.1002/ajpa.22565
35. Uddin M, Aiello AE, Wildman DE, Koenen KC, Pawelec G, de Los Santos R, Goldmann E, Galea S. Epigenetic and immune function profiles associated with posttraumatic stress disorder. Proc Natl Acad Sci U S A 2010; 107:9470-5.; PMID:20439746; http://dx.doi.org/10.1073/pnas.0910794107
36. Kuh D, Ben-Shlomo Y, Lynch J, Hallqvist J, Power C. Life course epidemiology. J Epidemiol Community Health 2003; 57:778-83.; PMID:14573579; http://dx.doi.org/10.1136/jech.57.10.778
37. Bild DE, Bluemke DA, Burke GL, Detrano R, Diez Roux AV, Folsom AR, Greenland P, Jacob DR, Jr., Kronmal R, Liu K, et al. Multi-ethnic study of atherosclerosis: objectives and design. Am J Epidemiol 2002; 156:871-81.; PMID:12397006; http://dx.doi.org/10.1093/aje/kwf113
38. Du P, Kibbe WA, Lin SM. lumi: a pipeline for processing Illumina microarray. Bioinformatics 2008; 24:1547-8.; PMID:18467348; http://dx.doi.org/10.1093/bioinformatics/btn224
39. Pidsley R, CC YW, Volta M, Lunnon K, Mill J, Schalkwyk LC. A data-driven approach to preprocessing Illumina 450K methylation array data. BMC Genomics 2013; 14:293.; PMID:23631413; http://dx.doi.org/10.1186/1471-2164-14-293
40. Du P, Zhang X, Huang CC, Jafari N, Kibbe WA, Hou L, Lin SM. Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics 2010; 11:587.; PMID:21118553; http://dx.doi.org/10.1186/1471-2105-11-587
41. Dunning MJ, Smith ML, Ritchie ME, Tavare S. beadarray: R classes and methods for Illumina bead-based data. Bioinformatics 2007; 23:2183-4.; PMID:17586828; http://dx.doi.org/10.1093/bioinformatics/btm311
42. Liu Y, Ding J, Reynolds LM, Lohman K, Register TC, De La Fuente A, Howard TD, Hawkins GA, Cui W, Morris J, et al. Methylomics of gene expression in human monocytes. Hum Mol Genet 2013; 22 (24):5065-74.; PMID:23900078
43. Desai S, Alva S. Maternal education and child health: Is there a strong causal relationship? Demography 1998; 35:71-81.; PMID:9512911; http://dx.doi.org/10.2307/3004028
44. Aslam M, Kingdon GG. Parental Education and Child Health - Understanding the Pathways of Impact in Pakistan. World Dev 2012; 40:2014-32; http://dx.doi.org/10.1016/j.worlddev.2012.05.007
45. Chen YY, Li HB. Mother’s education and child health: Is there a nurturing effect? J Health Economics 2009; 28:413-26; http://dx.doi.org/10.1016/j.jhealeco.2008.10.005
46. Brown H, Prescott R. Applied Mixed Models in Medicine. West Sussex: John Wiley & Sons Ltd 2006
47. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate - a Practical and Powerful Approach to Multiple Testing. J Roy Stat Soc B Met 1995; 57: 289-300
48. Storey JD. A direct approach to false discovery rates. J Roy Stat Soc B 2002; 64:479-98; http://dx.doi.org/10.1111/1467-9868.00346
49. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 2003; 100:9440-5.; PMID:12883005; http://dx.doi.org/10.1073/pnas.1530509100
50. Gutierrez-Arcelus M, Lappalainen T, Montgomery SB, Buil A, Ongen H, Yurovsky A, Bryois J, Giger T, Romano L, Planchon A, et al. Passive and active DNA methylation and the interplay with genetic variation in gene regulation (vol 2, e00523, 2013). Elife 2013; 2: e00523.; PMID:23755361
51. Han H, Cortez CC, Yang X, Nichols PW, Jones PA, Liang G. DNA methylation directly silences genes with non-CpG island promoters and establishes a nucleosome occupied promoter. Hum Mol Genet 2011; 20:4299-310.; PMID:21835883; http://dx.doi.org/10.1093/hmg/ddr356
52. van Eijk KR, de Jong S, Boks MP, Langeveld T, Colas F, Veldink JH, de Kovel CG, Janson E, Strengman E, Langfelder P, et al. Genetic analysis of DNA methylation and gene expression levels in whole blood of healthy human subjects. BMC Genomics 2012; 13:636.; PMID:23157493; http://dx.doi.org/10.1186/1471-2164-13-636
53. Adler NE, Stewart J. Health disparities across the lifespan: Meaning, methods, and mechanisms. Ann N Y Acad Sci 2010; 1186:5-23.; PMID:20201865; http://dx.doi.org/10.1111/j.1749-6632.2009.05337.x
54. McLoyd VC. Socioeconomic disadvantage and child development. Am Psychol 1998; 53:185-204.; PMID:9491747; http://dx.doi.org/10.1037/0003-066X.53.2.185
55. Lantz PM, House JS, Mero RP, Williams DR. Stress, life events, and socioeconomic disparities in health: results from the Americans’ Changing Lives Study. J Health Soc Behav 2005; 46:274-88.; PMID:16259149; http://dx.doi.org/10.1177/002214650504600305
56. Sapolsky RM. Social status and health in humans and other animals. Annu Rev Anthropol 2004; 33:393-418; http://dx.doi.org/10.1146/annurev.anthro.33.070203.144000
57. Jaffe AE, Murakami P, Lee H, Leek JT, Fallin MD, Feinberg AP, Irizarry RA. Bump hunting to identify differentially methylated regions in epigenetic epidemiology studies. Int J Epidemiol 2012; 41:200-9.; PMID:22422453; http://dx.doi.org/10.1093/ije/dyr238
58. Zhang W, Spector TD, Deloukas P, Bell JT, Engelhardt BE. Predicting genome-wide DNA methylation using methylation marks, genomic position, and DNA regulatory elements. Genome Biol 2015; 16:14.; PMID:25616342; http://dx.doi.org/10.1186/s13059-015-0581-9
59. Davies MN, Volta M, Pidsley R, Lunnon K, Dixit A, Lovestone S, Coarfa C, Harris RA, Milosavljevic A, Troakes C, et al. Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Genome Biol 2012; 13:R43.; PMID:22703893
60. Mirowsky J, Ross CE. Education, social status, and health. New York: Aldine de Gruyter 2003