Genetic Control of Chromatin States in Humans Involves Local and Distal Chromosomal Interactions

Cell

Volumn 162, Issue 5, 2015, Pages 1051-1065

  Grubert, Fabian ^a   Zaugg, Judith B ^a,b   Kasowski, Maya ^a   Ursu, Oana ^a   Spacek, Damek V ^a   Martin, Alicia R ^a   Greenside, Peyton ^a   Srivas, Rohith ^a   Phanstiel, Doug H ^a   Pekowska, Aleksandra ^b   Heidari, Nastaran ^a   Euskirchen, Ghia ^a   Huber, Wolfgang ^b   Pritchard, Jonathan K ^a,c   Bustamante, Carlos D ^a   Steinmetz, Lars M ^a,b   Kundaje, Anshul ^a,d   Snyder, Michael ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c STANFORD UNIVERSITY   (United States)

^d Stanford University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; CHROMATIN; HISTONE;

ARTICLE; AUTOIMMUNE DISEASE; CHROMATIN; CHROMOSOME; CONTROLLED STUDY; ENHANCER REGION; GENE REGULATORY NETWORK; GENE TARGETING; GENETIC ASSOCIATION; GENETIC REGULATION; GENETIC VARIABILITY; HUMAN; LYMPHOBLASTOID CELL LINE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE TRAIT LOCUS; QUANTITATIVE TRAIT LOCUS MAPPING; REGULATORY SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; CELL LINE; CHEMISTRY; COHORT ANALYSIS; FEMALE; HUMAN CHROMOSOME; HUMAN GENOME PROJECT; LYMPHOCYTE; MALE; METABOLISM;

CELL LINE; CHROMATIN; CHROMOSOMES, HUMAN; COHORT STUDIES; FEMALE; GENE REGULATORY NETWORKS; GENOME-WIDE ASSOCIATION STUDY; HISTONES; HUMAN GENOME PROJECT; HUMANS; LYMPHOCYTES; MALE; QUANTITATIVE TRAIT LOCI; REGULATORY ELEMENTS, TRANSCRIPTIONAL;

EID: 84940391986     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.07.048     Document Type: Article

References (40)

1. R. Bourgon, R. Gentleman, and W. Huber Independent filtering increases detection power for high-throughput experiments Proc. Natl. Acad. Sci. USA 107 2010 9546 9551
2. J.F. Degner, A.A. Pai, R. Pique-Regi, J.B. Veyrieras, D.J. Gaffney, J.K. Pickrell, S. De Leon, K. Michelini, N. Lewellen, G.E. Crawford, and et al. DNaseI sensitivity QTLs are a major determinant of human expression variation Nature 482 2012 390 394
3. J.R. Dixon, S. Selvaraj, F. Yue, A. Kim, Y. Li, Y. Shen, M. Hu, J.S. Liu, and B. Ren Topological domains in mammalian genomes identified by analysis of chromatin interactions Nature 485 2012 376 380
4. I. Dunham, A. Kundaje, S.F. Aldred, P.J. Collins, C.A. Davis, F. Doyle, C.B. Epstein, S. Frietze, J. Harrow, R. Kaul, et al. ENCODE Project Consortium An integrated encyclopedia of DNA elements in the human genome Nature 489 2012 57 74
5. J. Ernst, P. Kheradpour, T.S. Mikkelsen, N. Shoresh, L.D. Ward, C.B. Epstein, X. Zhang, L. Wang, R. Issner, M. Coyne, and et al. Mapping and analysis of chromatin state dynamics in nine human cell types Nature 473 2011 43 49
6. A. Franke, D.P. McGovern, J.C. Barrett, K. Wang, G.L. Radford-Smith, T. Ahmad, C.W. Lees, T. Balschun, J. Lee, R. Roberts, and et al. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci Nat. Genet. 42 2010 1118 1125
7. M.J. Fullwood, M.H. Liu, Y.F. Pan, J. Liu, H. Xu, Y.B. Mohamed, Y.L. Orlov, S. Velkov, A. Ho, P.H. Mei, and et al. An oestrogen-receptor-alpha-bound human chromatin interactome Nature 462 2009 58 64
8. E. Gjoneska, A.R. Pfenning, H. Mathys, G. Quon, A. Kundaje, L.H. Tsai, and M. Kellis Conserved epigenomic signals in mice and humans reveal immune basis of Alzheimer's disease Nature 518 2015 365 369
9. O. Harismendy, D. Notani, X. Song, N.G. Rahim, B. Tanasa, N. Heintzman, B. Ren, X.D. Fu, E.J. Topol, M.G. Rosenfeld, and K.A. Frazer 9p21 DNA variants associated with coronary artery disease impair interferon-γ signalling response Nature 470 2011 264 268
10. J. Harrow, A. Frankish, J.M. Gonzalez, E. Tapanari, M. Diekhans, F. Kokocinski, B.L. Aken, D. Barrell, A. Zadissa, S. Searle, and et al. GENCODE: the reference human genome annotation for The ENCODE Project Genome Res. 22 2012 1760 1774
11. L.A. Hindorff, P. Sethupathy, H.A. Junkins, E.M. Ramos, J.P. Mehta, F.S. Collins, and T.A. Manolio Potential etiologic and functional implications of genome-wide association loci for human diseases and traits Proc. Natl. Acad. Sci. USA 106 2009 9362 9367
12. F. Jin, Y. Li, J.R. Dixon, S. Selvaraj, Z. Ye, A.Y. Lee, C.A. Yen, A.D. Schmitt, C.A. Espinoza, and B. Ren A high-resolution map of the three-dimensional chromatin interactome in human cells Nature 503 2013 290 294
13. K.J. Karczewski, J.T. Dudley, K.R. Kukurba, R. Chen, A.J. Butte, S.B. Montgomery, and M. Snyder Systematic functional regulatory assessment of disease-associated variants Proc. Natl. Acad. Sci. USA 110 2013 9607 9612
14. M. Kasowski, S. Kyriazopoulou-Panagiotopoulou, F. Grubert, J.B. Zaugg, A. Kundaje, Y. Liu, A.P. Boyle, Q.C. Zhang, F. Zakharia, D.V. Spacek, and et al. Extensive variation in chromatin states across humans Science 342 2013 750 752
15. P. Kheradpour, and M. Kellis Systematic discovery and characterization of regulatory motifs in ENCODE TF binding experiments Nucleic Acids Res. 42 2014 2976 2987
16. H. Kilpinen, S.M. Waszak, A.R. Gschwind, S.K. Raghav, R.M. Witwicki, A. Orioli, E. Migliavacca, M. Wiederkehr, M. Gutierrez-Arcelus, N.I. Panousis, and et al. Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription Science 342 2013 744 747
17. D.A. Kleinjan, and V. van Heyningen Long-range control of gene expression: emerging mechanisms and disruption in disease Am. J. Hum. Genet. 76 2005 8 32
18. A. Koren, P. Polak, J. Nemesh, J.J. Michaelson, J. Sebat, S.R. Sunyaev, and S.A. McCarroll Differential relationship of DNA replication timing to different forms of human mutation and variation Am. J. Hum. Genet. 91 2012 1033 1040
19. A. Kundaje, S. Kyriazopoulou-Panagiotopoulou, M. Libbrecht, C.L. Smith, D. Raha, E.E. Winters, S.M. Johnson, M. Snyder, S. Batzoglou, and A. Sidow Ubiquitous heterogeneity and asymmetry of the chromatin environment at regulatory elements Genome Res. 22 2012 1735 1747
20. J.C. Lambert, C.A. Ibrahim-Verbaas, D. Harold, A.C. Naj, R. Sims, C. Bellenguez, A.L. DeStafano, J.C. Bis, G.W. Beecham, B. Grenier-Boley, et al. European Alzheimer's Disease Initiative (EADI) Genetic and Environmental Risk in Alzheimer's Disease Alzheimer's Disease Genetic Consortium Cohorts for Heart and Aging Research in Genomic Epidemiology Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease Nat. Genet. 45 2013 1452 1458
21. T. Lappalainen, M. Sammeth, M.R. Friedländer, P.A. 't Hoen, J. Monlong, M.A. Rivas, M. Gonzàlez-Porta, N. Kurbatova, T. Griebel, P.G. Ferreira, et al. Geuvadis Consortium Transcriptome and genome sequencing uncovers functional variation in humans Nature 501 2013 506 511
22. G. Li, X. Ruan, R.K. Auerbach, K.S. Sandhu, M. Zheng, P. Wang, H.M. Poh, Y. Goh, J. Lim, J. Zhang, and et al. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation Cell 148 2012 84 98
23. E. Lieberman-Aiden, N.L. van Berkum, L. Williams, M. Imakaev, T. Ragoczy, A. Telling, I. Amit, B.R. Lajoie, P.J. Sabo, M.O. Dorschner, and et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome Science 326 2009 289 293
24. M.T. Maurano, R. Humbert, E. Rynes, R.E. Thurman, E. Haugen, H. Wang, A.P. Reynolds, R. Sandstrom, H. Qu, J. Brody, and et al. Systematic localization of common disease-associated variation in regulatory DNA Science 337 2012 1190 1195
25. G. McVicker, B. van de Geijn, J.F. Degner, C.E. Cain, N.E. Banovich, A. Raj, N. Lewellen, M. Myrthil, Y. Gilad, and J.K. Pritchard Identification of genetic variants that affect histone modifications in human cells Science 342 2013 747 749
26. D.L. Nicolae, E. Gamazon, W. Zhang, S. Duan, M.E. Dolan, and N.J. Cox Trait-associated SNPs are more likely to be eQTLs: annotation to enhance discovery from GWAS PLoS Genet. 6 2010 e1000888
27. M.A. Nobrega, I. Ovcharenko, V. Afzal, and E.M. Rubin Scanning human gene deserts for long-range enhancers Science 302 2003 413
28. R. Patro, S.M. Mount, and C. Kingsford Sailfish enables alignment-free isoform quantification from RNA-seq reads using lightweight algorithms Nat. Biotechnol. 32 2014 462 464
29. D.H. Phanstiel, A.P. Boyle, N. Heidari, and M.P. Snyder Mango: a bias-correcting ChIA-PET analysis pipeline Bioinformatics 2015 btv336
30. M.M. Pomerantz, N. Ahmadiyeh, L. Jia, P. Herman, M.P. Verzi, H. Doddapaneni, C.A. Beckwith, J.A. Chan, A. Hills, M. Davis, and et al. The 8q24 cancer risk variant rs6983267 shows long-range interaction with MYC in colorectal cancer Nat. Genet. 41 2009 882 884
31. S.S. Rao, M.H. Huntley, N.C. Durand, E.K. Stamenova, I.D. Bochkov, J.T. Robinson, A.L. Sanborn, I. Machol, A.D. Omer, E.S. Lander, and E.L. Aiden A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping Cell 159 2014 1665 1680
32. M.A. Rivas, M. Beaudoin, A. Gardet, C. Stevens, Y. Sharma, C.K. Zhang, G. Boucher, S. Ripke, D. Ellinghaus, N. Burtt, et al. National Institute of Diabetes and Digestive Kidney Diseases Inflammatory Bowel Disease Genetics Consortium (NIDDK IBDGC) United Kingdom Inflammatory Bowel Disease Genetics Consortium International Inflammatory Bowel Disease Genetics Consortium Deep resequencing of GWAS loci identifies independent rare variants associated with inflammatory bowel disease Nat. Genet. 43 2011 1066 1073
33. A. Sanyal, B.R. Lajoie, G. Jain, and J. Dekker The long-range interaction landscape of gene promoters Nature 489 2012 109 113
34. M.A. Schaub, A.P. Boyle, A. Kundaje, S. Batzoglou, and M. Snyder Linking disease associations with regulatory information in the human genome Genome Res. 22 2012 1748 1759
35. S. Smemo, J.J. Tena, K.H. Kim, E.R. Gamazon, N.J. Sakabe, C. Gómez-Marín, I. Aneas, F.L. Credidio, D.R. Sobreira, N.F. Wasserman, and et al. Obesity-associated variants within FTO form long-range functional connections with IRX3 Nature 507 2014 371 375
36. O. Stegle, L. Parts, R. Durbin, and J. Winn A Bayesian framework to account for complex non-genetic factors in gene expression levels greatly increases power in eQTL studies PLoS Comput. Biol. 6 2010 e1000770
37. J. Van Limbergen, D.C. Wilson, and J. Satsangi The genetics of Crohn's disease Annu. Rev. Genomics Hum. Genet. 10 2009 89 116
38. A. Visel, E.M. Rubin, and L.A. Pennacchio Genomic views of distant-acting enhancers Nature 461 2009 199 205
39. Y. Zhang, T. Liu, C.A. Meyer, J. Eeckhoute, D.S. Johnson, B.E. Bernstein, C. Nusbaum, R.M. Myers, M. Brown, W. Li, and X.S. Liu Model-based analysis of ChIP-Seq (MACS) Genome Biol. 9 2008 R137
40. O. Zuk, S.F. Schaffner, K. Samocha, R. Do, E. Hechter, S. Kathiresan, M.J. Daly, B.M. Neale, S.R. Sunyaev, and E.S. Lander Searching for missing heritability: designing rare variant association studies Proc. Natl. Acad. Sci. USA 111 2014 E455 E464