Heritable DNA methylation in CD4+ Cells among complex families displays genetic and non-genetic effects

PLoS ONE

Volumn 11, Issue 10, 2016, Pages

  Day, Kenneth ^a   Waite, Lindsay L ^a,b   Alonso, Arnald ^a,f   Irvin, Marguerite R ^b   Zhi, Degui ^b   Thibeault, Krista S ^a   Aslibekyan, Stella ^b   Hidalgo, Bertha ^b   Borecki, Ingrid B ^c   Ordovas, Jose M ^d,e   Arnett, Donna K ^b,g   Tiwari, Hemant K ^b   Absher, Devin M ^a  

^a HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c WASHINGTON UNIVERSITY   (United States)

^d TUFTS UNIVERSITY   (United States)

^e IMDEA FOOD INSTITUTE   (Spain)

^f HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^g UNIVERSITY OF KENTUCKY COLLEGE OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CD4+ T LYMPHOCYTE; CELL LINEAGE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; GENE ONTOLOGY; GENETIC ASSOCIATION; GENOME ANALYSIS; HEREDITY; HUMAN; HUMAN CELL; PRIMORDIAL GERM CELL; QUANTITATIVE TRAIT LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE ACTIVATION; FEMALE; GENETICS; MALE; METABOLISM; MOLECULAR GENETICS; PEDIGREE;

CD4-POSITIVE T-LYMPHOCYTES; CPG ISLANDS; DNA METHYLATION; FEMALE; HUMANS; MALE; MOLECULAR SEQUENCE ANNOTATION; PEDIGREE; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI;

EID: 84994036945     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0165488     Document Type: Article

References (75)

1. Lee H-S. Impact of Maternal Diet on the Epigenome during In Utero Life and the Developmental Programming of Diseases in Childhood and Adulthood. Nutrients. 2015; 7: 9492-507. doi: 10.3390/ nu7115467 PMID: 26593940
2. Joubert BR, Felix JF, Yousefi P, Bakulski KM, Just AC, Breton C, et al. DNA Methylation in Newborns and Maternal Smoking in Pregnancy: Genome-wide Consortium Meta-analysis. Am J Hum Genet. 2016; 98: 680-96. doi: 10.1016/j.ajhg.2016.02.019 PMID: 27040690
3. Ambatipudi S, Cuenin C, Hernandez-Vargas H, Ghantous A, Calvez-Kelm F Le, Kaaks R, et al. Tobacco smoking-associated genome-wide DNA methylation changes in the EPIC study. Epigenomics. 2016;
4. Teschendorff AE, Yang Z, Wong A, Pipinikas CP, Jiao Y, Jones A, et al. Correlation of Smoking-Associated DNA Methylation Changes in Buccal Cells With DNA Methylation Changes in Epithelial Cancer. JAMA Oncol. 2015; 1: 476-85. doi: 10.1001/jamaoncol.2015.1053 PMID: 26181258
5. Shea JM, Serra RW, Carone BR, Shulha HP, Kucukural A, Ziller MJ, et al. Genetic and Epigenetic Variation, but Not Diet, Shape the Sperm Methylome. Dev Cell. 2015; 35: 750-758. doi: 10.1016/j.devcel. 2015.11.024 PMID: 26702833
6. de Castro Barbosa T, Ingerslev LR, Alm P, Versteyhe S, Massart J, Rasmussen M, et al. High-fat diet reprograms the epigenome of rat spermatozoa and transgenerationally affects metabolism of the offspring. Mol Metab. 2015; 5: 184-97. doi: 10.1016/j.molmet.2015.12.002 PMID: 26977389
7. Radford EJ, Ito M, Shi H, Corish JA, Yamazawa K, Isganaitis E, et al. In utero effects. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science. 2014; 345: 1255903. doi: 10.1126/science.1255903 PMID: 25011554
8. Hajkova P, Jeffries SJ, Lee C, Miller N, Jackson SP, Surani MA. Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science. 2010; 329: 78-82. doi: 10.1126/ science.1187945 PMID: 20595612
9. Tang WWC, Dietmann S, Irie N, Leitch HG, Floros VI, Bradshaw CR, et al. A Unique Gene Regulatory Network Resets the Human Germline Epigenome for Development. Cell. 2015; 161: 1453-1467. doi: 10.1016/j.cell.2015.04.053 PMID: 26046444
10. Koch L. An epigenetic twist on the missing heritability of complex traits. Nat Rev Genet. 2014; 15. doi: 10.1038/nrg3698 PMID: 24535246
11. Cortijo S, Wardenaar R, Colomé-Tatché M, Gilly A, Etcheverry M, Labadie K, et al. Mapping the epigenetic basis of complex traits. Science. 2014; 343: 1145-8. doi: 10.1126/science.1248127 PMID: 24505129
12. Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, et al. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 2009; 5: e1000530. doi: 10.1371/journal.pgen.1000530 PMID: 19557164
13. Schmitz RJ, He Y, Valdés-López O, Khan SM, Joshi T, Urich M a, et al. Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Res. 2013; 23: 1663-74. doi: 10.1101/gr.152538.112 PMID: 23739894
14. Morgan HD, Sutherland HGE, Martin DIK, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet. 1999; 23: 314-318. doi: 10.1038/15490 PMID: 10545949
15. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KVK, et al. Transgenerational inheritance of epigenetic states at the murine Axin Fu allele occurs after maternal and paternal transmission. PNAS. 2003; 100: 2538-2543. doi: 10.1073/pnas.0436776100 PMID: 12601169
16. Dias BG, Ressler KJ. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat Neurosci. 2014; 17: 89-96. doi: 10.1038/nn.3594 PMID: 24292232
17. Morgan DK, Whitelaw E. The case for transgenerational epigenetic inheritance in humans. Mamm Genome. 2008; 19: 394-7. doi: 10.1007/s00335-008-9124-y PMID: 18663528
18. Prokopuk L, Western PS, Stringer JM. Transgenerational epigenetic inheritance: adaptation through the germline epigenome? Epigenomics. 2015; 7: 829-46. doi: 10.2217/epi.15.36 PMID: 26367077
19. Zhi D, Aslibekyan S, Irvin MR, Claas S a, Borecki IB, Ordovas JM, et al. SNPs located at CpG sites modulate genome-epigenome interaction. Epigenetics. 2013; 8: 802-6. doi: 10.4161/epi.25501 PMID: 23811543
20. Shoemaker R, Deng J, Wang W, Zhang K. Allele-specific methylation is prevalent and is contributed by CpG-SNPs in the human genome. Genome Res. 2010; 20: 883-9. doi: 10.1101/gr.104695.109 PMID: 20418490
21. Zhang Y, Rohde C, Reinhardt R, Voelcker-Rehage C, Jeltsch A. Non-imprinted allele-specific DNA methylation on human autosomes. Genome Biol. 2009; 10: R138. doi: 10.1186/gb-2009-10-12-r138 PMID: 19958531
22. Meaburn EL, Schalkwyk LC, Mill J. Allele-specific methylation in the human genome: implications for genetic studies of complex disease. Epigenetics. 2010; 5: 578-82. doi: 10.4161/epi.5.7.12960 PMID: 20716955
23. Gertz J, Varley KE, Reddy TE, Bowling KM, Pauli F, Parker SL, et al. Analysis of DNA methylation in a three-generation family reveals widespread genetic influence on epigenetic regulation. PLoS Genet. 2011; 7: e1002228. doi: 10.1371/journal.pgen.1002228 PMID: 21852959
24. Gibbs JR, van der Brug MP, Hernandez DG, Traynor BJ, Nalls M a, Lai S-L, et al. Abundant quantitative trait loci exist for DNA methylation and gene expression in human brain. PLoS Genet. 2010; 6: e1000952. doi: 10.1371/journal.pgen.1000952 PMID: 20485568
25. Bell JT, Pai A a, Pickrell JK, Gaffney DJ, Pique-Regi R, Degner JF, et al. DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biol. 2011; 12: R10. doi: 10.1186/gb-2011-12-1-r10 PMID: 21251332
26. Wagner JR, Busche S, Ge B, Kwan T, Pastinen T, Blanchette M. The relationship between DNA methylation, genetic and expression inter-individual variation in untransformed human fibroblasts. Genome Biol. 2014; 15: R37. doi: 10.1186/gb-2014-15-2-r37 PMID: 24555846
27. Czyz W, Morahan JM, Ebers GC, Ramagopalan S V. Genetic, environmental and stochastic factors in monozygotic twin discordance with a focus on epigenetic differences. BMC Med. 2012; 10: 93. doi: 10. 1186/1741-7015-10-93 PMID: 22898292
28. Kaminsky Z a, Tang T, Wang S-C, Ptak C, Oh GHT, Wong AHC, et al. DNA methylation profiles in monozygotic and dizygotic twins. Nat Genet. 2009; 41: 240-5. doi: 10.1038/ng.286 PMID: 19151718
29. Ollikainen M, Smith KR, Joo EJ-H, Ng HK, Andronikos R, Novakovic B, et al. DNA methylation analysis of multiple tissues from newborn twins reveals both genetic and intrauterine components to variation in the human neonatal epigenome. Hum Mol Genet. 2010; 19: 4176-88. doi: 10.1093/hmg/ddq336 PMID: 20699328
30. 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 U S A. 2005; 102: 10604-9. doi: 10.1073/ pnas.0500398102 PMID: 16009939
31. van Dongen J, Nivard MG, Willemsen G, Hottenga J-J, Helmer Q, Dolan C V, et al. Genetic and environmental influences interact with age and sex in shaping the human methylome. Nat Commun. 2016; 7: 11115. doi: 10.1038/ncomms11115 PMID: 27051996
32. McRae AF, Powell JE, Henders AK, Bowdler L, Hemani G, Shah S, et al. Contribution of genetic variation to transgenerational inheritance of DNA methylation. Genome Biol. 2014; 15: R73. doi: 10.1186/ gb-2014-15-5-r73 PMID: 24887635
33. Gaunt TR, Shihab HA, Hemani G, Min JL, Woodward G, Lyttleton O, et al. Systematic identification of genetic influences on methylation across the human life course. Genome Biol. 2016; 17: 61. doi: 10. 1186/s13059-016-0926-z PMID: 27036880
34. Shah S, McRae AF, Marioni RE, Harris SE, Gibson J, Henders AK, et al. Genetic and environmental exposures constrain epigenetic drift over the human life course. Genome Res. 2014; 24: 1725-33. doi: 10.1101/gr.176933.114 PMID: 25249537
35. Talens RP, Christensen K, Putter H, Willemsen G, Christiansen L, Kremer D, et al. Epigenetic variation during the adult lifespan: cross-sectional and longitudinal data on monozygotic twin pairs. Aging Cell. 2012; 11: 694-703. doi: 10.1111/j.1474-9726.2012.00835.x PMID: 22621408
36. Irvin MR, Kabagambe EK, Tiwari HK, Parnell LD, Straka RJ, Tsai M, et al. Apolipoprotein E polymorphisms and postprandial triglyceridemia before and after fenofibrate treatment in the Genetics of Lipid Lowering and Diet Network (GOLDN) Study. Circ Cardiovasc Genet. 2010; 3: 462-7. doi: 10.1161/ CIRCGENETICS.110.950667 PMID: 20729559
37. Irvin MR, Zhi D, Joehanes R, Mendelson M, Aslibekyan S, Claas S a, et al. Epigenome-Wide Association Study of Fasting Blood Lipids in the Genetics of Lipid Lowering Drugs and Diet Network Study. Circulation. 2014; 130: 565-572. doi: 10.1161/CIRCULATIONAHA.114.009158 PMID: 24920721
38. Gutierrez-Arcelus M, Lappalainen T, Montgomery SB, Buil A, Ongen H, Yurovsky A, et al. Passive and active DNA methylation and the interplay with genetic variation in gene regulation. Elife. 2013; 2: e00523. doi: 10.7554/eLife.00523 PMID: 23755361
39. Oliver VF, Jaffe AE, Song J, Wang G, Zhang P, Branham KE, et al. Differential DNA methylation identified in the blood and retina of AMD patients. Epigenetics. Landes Bioscience; 2015; 10: 698-707. doi: 10.1080/15592294.2015.1060388 PMID: 26067391
40. Wilson GA, Butcher LM, Foster HR, Feber A, Roos C, Walter L, et al. Human-specific epigenetic variation in the immunological Leukotriene B4 Receptor (LTB4R/BLT1) implicated in common inflammatory diseases. Genome Med. BioMed Central; 2014; 6: 19. doi: 10.1186/gm536 PMID: 24598577
41. Waite LL, Weaver B, Day K, Li X, Roberts K, Gibson AW, et al. Estimation of Cell-Type Composition Including T and B Cell Subtypes for Whole Blood Methylation Microarray Data. Front Genet. 2016; 7: 23. doi: 10.3389/fgene.2016.00023 PMID: 26925097
42. Zilbauer M, Rayner TF, Clark C, Coffey AJ, Joyce CJ, Palta P, et al. Genome-wide methylation analyses of primary human leukocyte subsets identifies functionally important cell-type-specific hypomethylated regions. Blood. 2013; 122: e52-60. doi: 10.1182/blood-2013-05-503201 PMID: 24159175
43. Filion LG, Izaguirre CA, Garber GE, Huebsh L, Aye MT. Detection of surface and cytoplasmic CD4 on blood monocytes from normal and HIV-1 infected individuals. J Immunol Methods. 1990; 135: 59-69. PMID: 1703191
44. Gibbings D, Befus AD. CD4 and CD8: an inside-out coreceptor model for innate immune cells. J Leukoc Biol. 2009; 86: 251-9. doi: 10.1189/jlb.0109040 PMID: 19401396
45. Tan Q, Christiansen L, von Bornemann Hjelmborg J, Christensen K. Twin methodology in epigenetic studies. J Exp Biol. 2015; 218: 134-9. doi: 10.1242/jeb.107151 PMID: 25568460
46. Silver MJ, Kessler NJ, Hennig BJ, Dominguez-Salas P, Laritsky E, Baker MS, et al. Independent genomewide screens identify the tumor suppressor VTRNA2-1 as a human epiallele responsive to periconceptional environment. Genome Biol. 2015; 16: 118. doi: 10.1186/s13059-015-0660-y PMID: 26062908
47. 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. doi: 10.1371/journal.pgen.1001252 PMID: 21203497
48. Harris RA, Nagy-Szakal D, Kellermayer R. Human metastable epiallele candidates link to common disorders. Epigenetics. 2013; 8: 157-63. doi: 10.4161/epi.23438 PMID: 23321599
49. Grundberg E, Small KS, Hedman ÅK, Nica AC, Buil A, Keildson S, et al. Mapping cis- and trans-regulatory effects across multiple tissues in twins. Nat Genet. 2012; 44: 1084-9. doi: 10.1038/ng.2394 PMID: 22941192
50. Bell JT, Tsai PC, Yang TP, Pidsley R, Nisbet J, Glass D, et al. Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population. PLoS Genet. 2012; 8. doi: 10.1371/journal.pgen.1002629 PMID: 22532803
51. Kulkarni H, Kos MZ, Neary J, Dyer TD, Kent JW, Göring HHH, et al. Novel epigenetic determinants of type 2 diabetes in Mexican-American families. Hum Mol Genet. 2015; 24: 5330-44. doi: 10.1093/hmg/ ddv232 PMID: 26101197
52. Gordon L, Joo JE, Powell JE, Ollikainen M, Novakovic B, Li X, et al. Neonatal DNA methylation profile in human twins is specified by a complex interplay between intrauterine environmental and genetic factors, subject to tissue-specific influence. Genome Res. 2012; 22: 1395-1406. doi: 10.1101/gr.136598. 111 PMID: 22800725
53. Greaves IK, Groszmann M, Dennis ES, Peacock WJ. Trans-chromosomal methylation. Epigenetics. 2012; 7: 800-805. doi: 10.4161/epi.20820 PMID: 22705969
54. Plongthongkum N, van Eijk KR, de Jong S, Wang T, Sul JH, Boks MPM, et al. Characterization of genome-methylome interactions in 22 nuclear pedigrees. PLoS One. 2014; 9: e99313. doi: 10.1371/ journal.pone.0099313 PMID: 25019935
55. Hall MA, Ahmadi KR, Norman P, Snieder H, MacGregor AJ, Vaughan RW, et al. Genetic influence on peripheral blood T lymphocyte levels. Genes Immun. 2000; 1: 423-7. doi: 10.1038/sj.gene.6363702 PMID: 11196672
56. Nalls MA, Couper DJ, Tanaka T, van Rooij FJA, Chen M-H, Smith A V, et al. Multiple loci are associated with white blood cell phenotypes. PLoS Genet. 2011; 7: e1002113. doi: 10.1371/journal.pgen. 1002113 PMID: 21738480
57. Evans DM, Zhu G, Duffy DL, Montgomery GW, Frazer IH, Martin NG. Major quantitative trait locus for eosinophil count is located on chromosome 2q. J Allergy Clin Immunol. 2004; 114: 826-830. doi: 10. 1016/j.jaci.2004.05.060 PMID: 15480322
58. Evans DM, Zhu G, Duffy DL, Frazer IH, Montgomery GW, Martin NG. A major quantitative trait locus for CD4-CD8 ratio is located on chromosome 11. Genes Immun. 2004; 5: 548-552. doi: 10.1038/sj. gene.6364126 PMID: 15306848
59. Hall M a, Norman PJ, Thiel B, Tiwari H, Peiffer a, Vaughan RW, et al. Quantitative trait loci on chromosomes 1, 2, 3, 4, 8, 9, 11, 12, and 18 control variation in levels of T and B lymphocyte subpopulations. Am J Hum Genet. 2002; 70: 1172-1182. doi: 10.1086/340090 PMID: 11951176
60. Goldeck D, Larsen LA, Christiansen L, Christensen K, Hamprecht K, Pawelec G, et al. Genetic Influence on the Peripheral Blood CD4+ T-cell Differentiation Status in CMV Infection. J Gerontol A Biol Sci Med Sci. 2016; doi: 10.1093/gerona/glv230 PMID: 26755680
61. Ye CJ, Feng T, Kwon H-K, Raj T, Wilson MT, Asinovski N, et al. Intersection of population variation and autoimmunity genetics in human T cell activation. Science. 2014; 345: 1254665. doi: 10.1126/ science.1254665 PMID: 25214635
62. Rubelt F, Bolen CR, McGuire HM, Heiden JA Vander, Gadala-Maria D, Levin M, et al. Individual heritable differences result in unique cell lymphocyte receptor repertoires of naïve and antigen-experienced cells. Nat Commun. Nature Publishing Group; 2016; 7: 11112. doi: 10.1038/ncomms11112 PMID: 27005435
63. Neurauter AA, Bonyhadi M, Lien E, Nøkleby L, Ruud E, Camacho S, et al. Cell isolation and expansion using dynabeads. Advances in Biochemical Engineering/Biotechnology. 2007. pp. 41-73. doi: 10. 1007/10-2007-072 PMID: 17680228
64. Absher DM, Li X, Waite LL, Gibson A, Roberts K, Edberg J, et al. Genome-wide DNA methylation analysis of systemic lupus erythematosus reveals persistent hypomethylation of interferon genes and compositional changes to CD4+ T-cell populations. PLoS Genet. 2013; 9: e1003678. doi: 10.1371/journal. pgen.1003678 PMID: 23950730
65. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics. 2007; 8: 118-27. doi: 10.1093/biostatistics/kxj037 PMID: 16632515
66. Aslibekyan S, Kabagambe EK, Irvin MR, Straka RJ, Borecki IB, Tiwari HK, et al. A genome-wide association study of inflammatory biomarker changes in response to fenofibrate treatment in the Genetics of Lipid Lowering Drug and Diet Network (GOLDN). Pharmacogenet Genomics. 2012; 22: 191-197. doi: 10.1097/FPC.0b013e32834fdd41.A
67. Therneau T. The lmekin function. 2012.
68. Pinheiro JC, Bates DM. Mixed effects models in S and S-Plus. Springer VerlagNewYork. 2000. doi: 10.1198/tech.2001.s574
69. Hidalgo B, Irvin MR, Sha J, Zhi D, Aslibekyan S, Absher D, et al. Epigenome-wide association study of fasting measures of glucose, insulin, and HOMA-IR in the Genetics of Lipid Lowering Drugs and Diet Network study. Diabetes. 2014; 63: 801-7. doi: 10.2337/db13-1100 PMID: 24170695
70. Shabalin A a. Matrix eQTL: ultra fast eQTL analysis via large matrix operations. Bioinformatics. 2012; 28: 1353-8. doi: 10.1093/bioinformatics/bts163 PMID: 22492648
71. S.A.G.E. 6.2. Statistical Analysis for Genetic Epidemiology [Internet]. 2012.
72. Keen KJ, Elston RC. Robust asymptotic sampling theory for correlations in pedigrees. Stat Med. 2003; 22: 3229-3247. doi: 10.1002/sim.1559 PMID: 14518025
73. Mathew G, Song Y, Elston R. Interval estimation of familial correlations from pedigrees. Stat Appl Genet Mol Biol. 2011; 10: Article 11. doi: 10.2202/1544-6115.1573
74. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics. 2009; 10: 48. doi: 10.1186/1471-2105-10-48 PMID: 19192299
75. Eden E, Lipson D, Yogev S, Yakhini Z. Discovering motifs in ranked lists of DNA sequences. PLoS Comput Biol. 2007; 3: 0508-0522. doi: 10.1371/journal.pcbi.0030039 PMID: 17381235