Patterns of methylation heritability in a genome-wide analysis of four brain regions

Nucleic Acids Research

Volumn 41, Issue 4, 2013, Pages 2095-2104

  Quon, Gerald ^a,b   Lippert, Christoph ^a   Heckerman, David ^a   Listgarten, Jennifer ^a  

^a MICROSOFT RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR CTCF;

ARTICLE; BINDING SITE; BRAIN REGION; CELL TYPE; CHROMATIN; CHROMATIN STRUCTURE; CPG ISLAND; DNA METHYLATION; DNA SEQUENCE; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENE LOCUS; GENETIC VARIABILITY; HERITABILITY; INTERMETHOD COMPARISON; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION REGULATION; TWINS;

BRAIN; CPG ISLANDS; DNA; DNA METHYLATION; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; QUANTITATIVE TRAIT, HERITABLE; REGULATORY SEQUENCES, NUCLEIC ACID;

EID: 84876394432     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1449     Document Type: Article

References (49)

1. Hindorff, L.A., Sethupathy, P., Junkins, H.A., Ramos, E.M., Mehta, J.P., Collins, F.S. and Manolio, T.A. (2009) Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc. Natl Acad. Sci. USA, 106, 9362-9367.
2. Rakyan, V.K., Down, T.A., Balding, D.J. and Beck, S. (2011) Epigenome-wide association studies for common human diseases. Nat. Rev. Genet., 12, 529-541.
3. King, M.C. and Wilson, A.C. (1975) Evolution at two levels in humans and chimpanzees. Science, 188, 107-116.
4. Reik, W. (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature, 447, 425-432.
5. Rakyan, V.K., Hildmann, T., Novik, K.L., Lewin, J., Tost, J., Cox, A.V., Andrews, T.D., Howe, K.L., Otto, T., Olek, A. et al. (2004) DNA methylation profiling of the human major histocompatibility complex: a pilot study for the human epigenome project. PLoS Biol., 2, e405.
6. Bernstein, B.E., Meissner, A. and Lander, E.S. (2007) The mammalian epigenome. Cell, 128, 669-681.
7. Ballestar, E. (2011) Epigenetic alterations in autoimmune rheumatic diseases. Nat. Rev. Rheumatol., 7, 263-271.
8. Shoemaker, R., Deng, J., Wang, W. and Zhang, K. (2010) Allele-specific methylation is prevalent and is contributed by CpG-SNPs in the human genome. Genome Res., 20, 883-889.
9. Kerkel, K., Spadola, A., Yuan, E., Kosek, J., Jiang, L., Hod, E., Li, K., Murty, V.V., Schupf, N., Vilain, E. et al. (2008) Genomic surveys by methylation-sensitive SNP analysis identify sequence-dependent allele-specific DNA methylation. Nat. Genet., 40, 904-908.
10. Zhang, Y., Rohde, C., Reinhardt, R., Voelcker-Rehage, C. and Jeltsch, A. (2009) Non-imprinted allele-specific DNA methylation on human autosomes. Genome Biol., 10, R138.
11. Gertz, J., Varley, K.E., Reddy, T.E., Bowling, K.M., Pauli, F., Parker, S.L., Kucera, K.S., Willard, H.F. and Myers, R.M. (2011) Analysis of DNA methylation in a three-generation family reveals widespread genetic influence on epigenetic regulation. PLoS Genet., 7, e1002228.
12. Hellman, A. and Chess, A. (2010) Extensive sequence-influenced DNA methylation polymorphism in the human genome. Epigenetics Chromatin, 3, 11.
13. Gibbs, J.R., Van der Brug, M.P., Hernandez, D.G., Traynor, B.J., Nalls, M.A., Lai, S.L., Arepalli, S., Dillman, A., Rafferty, I.P., Troncoso, J. et al. (2010) Abundant quantitative trait loci exist for DNA methylation and gene expression in human brain. PLoS Genet., 6, e1000952.
14. Bell, J.T., Tsai, P.C., Yang, T.P., Pidsley, R., Nisbet, J., Glass, D., Mangino, M., Zhai, G., Zhang, F., Valdes, A. et al. (2012) Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population. PLoS Genet., 8, e1002629.
15. Bell, J.T., Pai, A.A., Pickrell, J.K., Gaffney, D.J., Pique-Regi, R., Degner, J.F., Gilad, Y. and Pritchard, J.K. (2011) DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biol., 12, R10.
16. Teng, M., Balch, C., Liu, Y., Li, M., Huang, T.H., Wang, Y., Nephew, K.P. and Li, L. (2012) The influence of cis-regulatory elements on DNA methylation fidelity. PLoS One, 7, e32928.
17. Breton, C.V., Salam, M.T. and Gilliland, F.D. (2011) Heritability and role for the environment in DNA methylation in AXL receptor tyrosine kinase. Epigenetics, 6, 895-898.
18. Gervin, K., Hammer M., Akselsen, H.E., Moe, R., Nygard, H., Brandt, I., Gjessing, H.K., Harris, J.R., Undlien, D.E. and Lyle, R. (2011) Extensive variation and low heritability of DNA methylation identified in a twin study. Genome Res., 21, 1813-1821.
19. Yang, J., Benyamin, B., McEvoy, B.P., Gordon, S., Henders, A.K., Nyholt, D.R., Madden, P.A., Heath, A.C., Martin, N.G., Montgomery, G.W. et al. (2010) Common SNPs explain a large proportion of the heritability for human height. Nat. Genet., 42, 565-569.
20. Hayes, B.J., Visscher, P.M. and Goddard, M.E. (2009) Increased accuracy of artificial selection by using the realized relationship matrix. Genet. Res., 91, 47-60.
21. Lippert, C., Listgarten, J., Liu, Y., Kadie, C.M., Davidson, R.I. and Heckerman, D. (2011) FaST linear mixed models for genome-wide association studies. Nat. Methods, 8, 833-835.
22. Self, S.G. and Liang, K.Y. (1987) Asymptotic properties of maximum likelihood estimators and likelihood ratio tests under nonstandard conditions. J. Am. Stat. Assoc., 82, 605-610.
23. Dominicus, A., Skrondal, A., Gjessing, H.K., Pedersen, N.L. and Palmgren, J. (2006) Likelihood ratio tests in behavioral genetics: problems and solutions. Behav. Genet., 36, 331-40.
24. Pinheiro, J. and Bates, D. (2000) Mixed-Effects Models in S and S-PLUS. Springer-Verlag, New York.
25. Listgarten, J., Lippert, C. and Heckerman, D. (2012) An efficient group test for genetic markers that handles confounding, ArXiv:1205.0793.
26. Wu, M.C., Lee, S., Cai, T., Li, Y., Boehnke, M. and Lin, X. (2011) Rare-variant association testing for sequencing data with the sequence kernel association test. Am. J. Hum. Genet., 89, 82-93.
27. Lee, S.H., Wray, N.R., Goddard, M.E. and Visscher, P.M. (2011) Estimating missing heritability for disease from genome-wide association studies. Am. J. Hum. Genet., 88, 294-305.
28. Devlin, B. and Roeder, K. (1999) Genomic control for association studies. Biometrics, 55, 997-1004.
29. Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Dolinski, K., Dwight, S.S., Eppig, J.T. et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet., 25, 25-29.
30. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S. et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA, 102, 15545-15550.
31. McDonagh, E.M., Whirl-Carrillo, M., Garten, Y., Altman, R.B. and Klein, T.E. (2011) From pharmacogenomic knowledge acquisition to clinical applications: the PharmGKB as a clinical pharmacogenomic biomarker resource. Biomark. Med., 5, 795-806.
32. Zeeberg, B., Feng, W., Wang, G., Wang, M., Fojo, A., Sunshine, M., Narasimhan, S., Kane, D., Reinhold, W., Lababidi, S. et al. (2003) GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol., 4, R28.
33. The ENCODE Consortium. (2011) A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol., 9, e1001046.
34. Dreszer, T.R., Karolchik, D., Zweig, A.S., Hinrichs, A.S., Raney, B.J., Kuhn, R.M., Meyer, L.R., Wong, M., Sloan, C.A., Rosenbloom, K.R. et al. (2012) The UCSC Genome Browser database: extensions and updates 2011. Nucleic Acids Res., 40, D918-D923.
35. Griffith, O.L., Montgomery, S.B., Bernier, B., Chu, B., Kasaian, K., Aerts, S., Mahony, S., Sleumer, M.C., Bilenky, M., Haeussler, M. et al. (2008) ORegAnno: an open-access community-driven resource for regulatory annotation. Nucleic Acids Res., 36, D107-D113.
36. Quinlan, A.R. and Hall, I.M. (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26, 841-842.
37. Su, A.I., Wiltshire, T., Batalov, S., Lapp, H., Ching, K.A., Block, D., Zhang, J., Soden, R., Hayakawa, M., Kreiman, G. et al. (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl Acad. Sci. USA, 101, 6062-6067.
38. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J. et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol., 5, R80.
39. Dai, M., Wang, P., Boyd, A.D., Kostov, G., Athey, B., Jones, E.G., Bunney, W.E., Myers, R.M., Speed, T.P., Akil, H. et al. (2005) Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res., 33, e175.
40. Listgarten, J., Lippert, C., Kadie, C.M., Davidson, R.I., Eskin, E. and Heckerman, D. (2012) Improved linear mixed models for genome-wide association studies. Nat. Methods, 9, 525-526.
41. Listgarten, J., Lippert, C. and Heckerman, D. (2012) Fast-LMM-Select for confounding from spatial structure and rare variants. Nat. Genet., in press.
42. Price, A.L., Helgason, A., Thorleifsson, G., McCarroll, S.A., Kong, A. and Stefansson, K. (2011) Single-tissue and cross-tissue heritability of gene expression via identity-by-descent in related or unrelated individuals. PLoS Genet., 7, e1001317.
43. Phillips, J.E. and Corces, V.G. (2009) CTCF: master weaver of the genome. Cell, 137, 1194-1211.
44. Bell, A.C. and Felsenfeld, G. (2000) Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature, 405, 482-485.
45. Kwan, T., Benovoy, D., Dias, C., Gurd, S., Serre, D., Zuzan, H., Clark, T.A., Schweitzer, A., Staples, M.K., Wang, H. et al. (2007) Heritability of alternative splicing in the human genome. Genome Res., 17, 1210-1218.
46. Visscher, P.M., Hill, W.G. and Wray, N.R. (2008) Heritability in the genomics era-concepts and misconceptions. Nat. Rev. Genet., 9, 255-266.
47. Benjamin, D.J., Cesarini, D., Van der Loos, M.J., Dawes, C.T., Koellinger, P.D., Magnusson, P.K., Chabris, C.F., Conley, D., Laibson, D., Johannesson, M. et al. (2012) The genetic architecture of economic and political preferences. Proc. Natl Acad. Sci. USA, 109, 8026-8031.
48. Charney, E. (2008) Genes and ideologies. Perspect. Polit., 6, 299-319.
49. Zuk, O., Hechter, E., Sunyaev, S.R. and Lander, E.S. (2012) The mystery of missing heritability: genetic interactions create phantom heritability. Proc. Natl Acad. Sci. USA, 109, 1193-1198.