On the identification of potential regulatory variants within genome wide association candidate SNP sets

BMC Medical Genomics

Volumn 7, Issue 1, 2014, Pages

  Chen, Chih Yu ^a,b   Chang, I Shou ^c   Hsiung, Chao A ^c   Wasserman, Wyeth W ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

Enhancer; Gene regulation; GWAS; Lung cancer; Regulatory regions; Topological domains; Transcription factor binding site alteration

Indexed keywords

TRANSCRIPTION FACTOR;

ARTICLE; BINDING AFFINITY; BINDING SITE; BREAST CANCER; CANCER SUSCEPTIBILITY; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EPIGENETICS; GENE CONTROL; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCATION; GENE LOCUS; GENE TARGETING; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; LUNG CANCER; MALE; PREDICTION; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM;

ALLELES; CELL LINE, TUMOR; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA, INTERGENIC; ENHANCER ELEMENTS, GENETIC; GENETIC PREDISPOSITION TO DISEASE; GENOME, HUMAN; GENOME-WIDE ASSOCIATION STUDY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MOLECULAR SEQUENCE ANNOTATION; NEOPLASMS; POLYMORPHISM, SINGLE NUCLEOTIDE; POSITION-SPECIFIC SCORING MATRICES; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID; TRANSCRIPTION FACTORS;

EID: 84903382385     PISSN: None     EISSN: 17558794     Source Type: Journal    
DOI: 10.1186/1755-8794-7-34     Document Type: Article

References (56)

1. GWASdb: a database for human genetic variants identified by genome-wide association studies. Li MJ, Wang P, Liu X, Lim EL, Wang Z, Yeager M, Wong MP, Sham PC, Chanock SJ, Wang J, Nucleic Acids Res 2012 40 1047 D1054 10.1093/nar/gkr1182 22139925
2. ENCODE whole-genome data in the UCSC Genome Browser: update 2012. Rosenbloom KR, Dreszer TR, Long JC, Malladi VS, Sloan CA, Raney BJ, Cline MS, Karolchik D, Barber GP, Clawson H, Diekhans M, Fujita PA, Goldman M, Gravell RC, Harte RA, Hinrichs AS, Kirkup VM, Kuhn RM, Learned K, Maddren M, Meyer LR, Pohl A, Rhead B, Wong MC, Zweig AS, Haussler D, Kent WJ, Nucleic Acids Res 2012 40 912 917 10.1093/nar/gkr1012 22075998
3. Enhancer identification in mouse embryonic stem cells using integrative modeling of chromatin and genomic features. Chen CY, Morris Q, Mitchell JA, BMC Genomics 2012 13 152 10.1186/1471-2164-13-152 22537144
4. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B, Nat Genet 2007 39 311 318 10.1038/ng1966 17277777
5. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, Boyer LA, Young RA, Jaenisch R, Proc Natl Acad Sci U S A 2010 107 21931 21936 10.1073/pnas. 1016071107 21106759
6. Epigenomic enhancer profiling defines a signature of colon cancer. Akhtar-Zaidi B, Cowper-Sal-lari R, Corradin O, Saiakhova A, Bartels CF, Balasubramanian D, Myeroff L, Lutterbaugh J, Jarrar A, Kalady MF, Willis J, Moore JH, Tesar PJ, Laframboise T, Markowitz S, Lupien M, Scacheri PC, Science 2012 336 736 739 10.1126/science.1217277 22499810
7. An 8q24 gene desert variant associated with prostate cancer risk confers differential in vivo activity to a MYC enhancer. Wasserman NF, Aneas I, Nobrega MA, Genome Res 2010 20 1191 1197 10.1101/gr.105361.110 20627891
8. Integrative functional genomics identifies an enhancer looping to the SOX9 gene disrupted by the 17q24.3 prostate cancer risk locus. Zhang X, Cowper-Sal lari R, Bailey SD, Moore JH, Lupien M, Genome Res 2012 22 1437 1446 10.1101/gr.135665.111 22665440
9. Predicting cell types and genetic variations contributing to disease by combining GWAS and epigenetic data. Gerasimova A, Chavez L, Li B, Seumois G, Greenbaum J, Rao A, Vijayanand P, Peters B, PLoS One 2013 8 54359 10.1371/journal.pone.0054359 23382893
10. Maps of open chromatin highlight cell type-restricted patterns of regulatory sequence variation at hematological trait loci. Paul DS, Albers CA, Rendon A, Voss K, Stephens J, van der Harst P, Chambers JC, Soranzo N, Ouwehand WH, Deloukas P, Genome Res 2013 23 1130 1141 10.1101/gr.155127.113 23570689
11. Linking disease associations with regulatory information in the human genome. Schaub MA, Boyle AP, Kundaje A, Batzoglou S, Snyder M, Genome Res 2012 22 1748 1759 10.1101/gr.136127.111 22955986
12. Identification of cis-regulatory sequence variations in individual genome sequences. Worsley-Hunt R, Bernard V, Wasserman WW, Genome Med 2011 3 65 10.1186/gm281 21989199
13. In silico detection of sequence variations modifying transcriptional regulation. Andersen MC, Engstrom PG, Lithwick S, Arenillas D, Eriksson P, Lenhard B, Wasserman WW, Odeberg J, PLoS Comput Biol 2008 4 5 10.1371/journal.pcbi.0040005 18208319
14. Architecture of the human regulatory network derived from ENCODE data. Gerstein MB, Kundaje A, Hariharan M, Landt SG, Yan KK, Cheng C, Mu XJ, Khurana E, Rozowsky J, Alexander R, Min R, Alves P, Abyzov A, Addleman N, Bhardwaj N, Boyle AP, Cayting P, Charos A, Chen DZ, Cheng Y, Clarke D, Eastman C, Euskirchen G, Frietze S, Fu Y, Gertz J, Grubert F, Harmanci A, Jain P, Kasowski M, et al. Nature 2012 489 91 100 10.1038/nature11245 22955619
15. Analysis of variation at transcription factor binding sites in Drosophila and humans. Spivakov M, Akhtar J, Kheradpour P, Beal K, Girardot C, Koscielny G, Herrero J, Kellis M, Furlong EE, Birney E, Genome Biol 2012 13 49 10.1186/gb-2012-13-9-r49 22950968
16. HaploReg: a resource for exploring chromatin states, conservation, and regulatory motif alterations within sets of genetically linked variants. Ward LD, Kellis M, Nucleic Acids Res 2012 40 930 D934 10.1093/nar/gkr917 22064851
17. Annotation of functional variation in personal genomes using RegulomeDB. Boyle AP, Hong EL, Hariharan M, Cheng Y, Schaub MA, Kasowski M, Karczewski KJ, Park J, Hitz BC, Weng S, Cherry JM, Snyder M, Genome Res 2012 22 1790 1797 10.1101/gr.137323.112 22955989
18. Comprehensive functional annotation of seventy-one breast cancer risk Loci. Rhie SK, Coetzee SG, Noushmehr H, Yan C, Kim JM, Haiman CA, Coetzee GA, PLoS One 2013 8 63925 10.1371/journal.pone.0063925 23717510
19. FunciSNP: an R/bioconductor tool integrating functional non-coding data sets with genetic association studies to identify candidate regulatory SNPs. Coetzee SG, Rhie SK, Berman BP, Coetzee GA, Noushmehr H, Nucleic Acids Res 2012 40 139 10.1093/nar/gks542 22684628
20. ChroMoS: an integrated web tool for SNP classification, prioritization and functional interpretation. Barenboim M, Manke T, Bioinformatics 2013 29 2197 2198 10.1093/bioinformatics/btt356 23782616
21. A genome-wide association study of lung cancer identifies a region of chromosome 5p15 associated with risk for adenocarcinoma. Landi MT, Chatterjee N, Yu K, Goldin LR, Goldstein AM, Rotunno M, Mirabello L, Jacobs K, Wheeler W, Yeager M, Bergen AW, Li Q, Consonni D, Pesatori AC, Wacholder S, Thun M, Diver R, Oken M, Virtamo J, Albanes D, Wang Z, Burdette L, Doheny KF, Pugh EW, Laurie C, Brennan P, Hung R, Gaborieau V, McKay JD, Lathrop M, et al. Am J Hum Genet 2009 85 679 691 10.1016/j.ajhg.2009.09.012 19836008
22. R: A language and environment for statistical computing. [ http://www.R-project.org ]
23. Bioconductor: open software development for computational biology and bioinformatics. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J, Genome Biol 2004 5 80 10.1186/gb-2004-5-10-r80 15461798
24. A catalog of published genome-wide association studies. [ http://www.genome.gov/gwastudies ]
25. SNAP: a web-based tool for identification and annotation of proxy SNPs using HapMap. Johnson AD, Handsaker RE, Pulit SL, Nizzari MM, O'Donnell CJ, de Bakker PI, Bioinformatics 2008 24 2938 2939 10.1093/bioinformatics/btn564 18974171
26. Enhancers in embryonic stem cells are enriched for transposable elements and genetic variations associated with cancers. Teng L, Firpi HA, Tan K, Nucleic Acids Res 2011 39 7371 7379 10.1093/nar/gkr476 21685454
27. Statistical significance for genomewide studies. Storey JD, Tibshirani R, Proc Natl Acad Sci U S A 2003 100 9440 9445 10.1073/pnas.1530509100 12883005
28. Applied bioinformatics for the identification of regulatory elements. Wasserman WW, Sandelin A, Nat Rev Genet 2004 5 276 287 10.1038/nrg1315 15131651
29. TFBS: Computational framework for transcription factor binding site analysis. Lenhard B, Wasserman WW, Bioinformatics 2002 18 1135 1136 10.1093/bioinformatics/18.8.1135 12176838
30. JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, Valen E, Yusuf D, Lenhard B, Wasserman WW, Sandelin A, Nucleic Acids Res 2010 38 105 D110 10.1093/nar/gkp950 19906716
31. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B, Nature 2012 485 376 380 10.1038/nature11082 22495300
32. The UCSC Genome Browser Database: update 2006. Hinrichs AS, Karolchik D, Baertsch R, Barber GP, Bejerano G, Clawson H, Diekhans M, Furey TS, Harte RA, Hsu F, Hillman-Jackson J, Kuhn RM, Pedersen JS, Pohl A, Raney BJ, Rosenbloom KR, Siepel A, Smith KE, Sugnet CW, Sultan-Qurraie A, Thomas DJ, Trumbower H, Weber RJ, Weirauch M, Zweig AS, Haussler D, Kent WJ, Nucleic Acids Res 2006 34 590 598 10.1093/nar/gkj144 16381938
33. HiTC: exploration of high-throughput 'C' experiments. Servant N, Lajoie BR, Nora EP, Giorgetti L, Chen CJ, Heard E, Dekker J, Barillot E, Bioinformatics 2012 28 2843 2844 10.1093/bioinformatics/bts521 22923296
34. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, Ching KA, Antosiewicz-Bourget JE, Liu H, Zhang X, Green RD, Lobanenkov VV, Stewart R, Thomson JA, Crawford GE, Kellis M, Ren B, Nature 2009 459 108 112 10.1038/nature07829 19295514
35. Precise temporal control of the eye regulatory gene Pax6 via enhancer-binding site affinity. Rowan S, Siggers T, Lachke SA, Yue Y, Bulyk ML, Maas RL, Genes Dev 2010 24 980 985 10.1101/gad.1890410 20413611
36. Beyond GWASs: illuminating the dark road from association to function. Edwards SL, Beesley J, French JD, Dunning AM, Am J Hum Genet 2013 93 779 797 10.1016/j.ajhg.2013.10.012 24210251
37. Large-scale genotyping identifies 41 new loci associated with breast cancer risk. Michailidou K, Hall P, Gonzalez-Neira A, Ghoussaini M, Dennis J, Milne RL, Schmidt MK, Chang-Claude J, Bojesen SE, Bolla MK, Wang Q, Dicks E, Lee A, Turnbull C, Rahman N, Fletcher O, Peto J, Gibson L, Dos Santos Silva I, Nevanlinna H, Muranen TA, Aittomaki K, Blomqvist C, Czene K, Irwanto A, Liu J, Waisfisz Q, Meijers-Heijboer H, Adank M, van der Luijt RB, Nat Genet 2013 45 353 361 361e351-352 10.1038/ng.2563 23535729
38. ChIP-seq accurately predicts tissue-specific activity of enhancers. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, Afzal V, Ren B, Rubin EM, Pennacchio LA, Nature 2009 457 854 858 10.1038/nature07730 19212405
39. An atlas of active enhancers across human cell types and tissues. Andersson R, Gebhard C, Miguel-Escalada I, Hoof I, Bornholdt J, Boyd M, Chen Y, Zhao X, Schmidl C, Suzuki T, Ntini E, Arner E, Valen E, Li K, Schwarzfischer L, Glatz D, Raithel J, Lilje B, Rapin N, Bagger FO, Jorgensen M, Andersen PR, Bertin N, Rackham O, Burroughs AM, Baillie JK, Ishizu Y, Shimizu Y, Furuhata E, Maeda S, et al. Nature 2014 507 455 461 10.1038/nature12787 24670763
40. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, Piolot T, van Berkum NL, Meisig J, Sedat J, Gribnau J, Barillot E, Bluthgen N, Dekker J, Heard E, Nature 2012 485 381 385 10.1038/nature11049 22495304
41. Clustering of tissue-specific Sub-TADs accompanies the regulation of HoxA genes in developing limbs. Berlivet S, Paquette D, Dumouchel A, Langlais D, Dostie J, Kmita M, PLoS Genet 2013 9 1004018 10.1371/journal.pgen.1004018 24385922
42. Genome-wide association analysis identifies three new breast cancer susceptibility loci. Ghoussaini M, Fletcher O, Michailidou K, Turnbull C, Schmidt MK, Dicks E, Dennis J, Wang Q, Humphreys MK, Luccarini C, Baynes C, Conroy D, Maranian M, Ahmed S, Driver K, Johnson N, Orr N, Dos Santos Silva I, Waisfisz Q, Meijers-Heijboer H, Uitterlinden AG, Rivadeneira F, Hall P, Czene K, Irwanto A, Liu J, Nevanlinna H, Aittomaki K, Blomqvist C, Meindl A, et al. Nat Genet 2012 44 312 318 10.1038/ng.1049 22267197
43. Reconstruction of nuclear receptor network reveals that NR2E3 is a novel upstream regulator of ESR1 in breast cancer. Park YY, Kim K, Kim SB, Hennessy BT, Kim SM, Park ES, Lim JY, Li J, Lu Y, Gonzalez-Angulo AM, Jeong W, Mills GB, Safe S, Lee JS, EMBO Mol Med 2012 4 52 67 10.1002/emmm.201100187 22174013
44. ROR1 is expressed in human breast cancer and associated with enhanced tumor-cell growth. Zhang S, Chen L, Cui B, Chuang HY, Yu J, Wang-Rodriguez J, Tang L, Chen G, Basak GW, Kipps TJ, PLoS One 2012 7 31127 10.1371/journal.pone. 0031127 22403610
45. Use of the receptor tyrosine kinase-like orphan receptor 1 (ROR1) as a diagnostic tool in chronic lymphocytic leukemia (CLL). Uhrmacher S, Schmidt C, Erdfelder F, Poll-Wolbeck SJ, Gehrke I, Hallek M, Kreuzer KA, Leuk Res 2011 35 1360 1366 10.1016/j.leukres.2011.04.006 21531460
46. Oncogenic miR-544 is an important molecular target in gastric cancer. Zhi Q, Guo X, Guo L, Zhang R, Jiang J, Ji J, Zhang J, Zhang J, Chen X, Cai Q, Li J, Liu B, Zhu Z, Yu Y, Anticancer Agents Med Chem 2013 13 270 275 10.2174/1871520611313020013 22934698
47. Perturbation of 14q32 miRNAs-cMYC gene network in osteosarcoma. Thayanithy V, Sarver AL, Kartha RV, Li L, Angstadt AY, Breen M, Steer CJ, Modiano JF, Subramanian S, Bone 2012 50 171 181 10.1016/j.bone.2011.10.012 22037351
48. An in silico analysis of dynamic changes in microRNA expression profiles in stepwise development of nasopharyngeal carcinoma. Luo Z, Zhang L, Li Z, Li X, Li G, Yu H, Jiang C, Dai Y, Guo X, Xiang J, Li G, BMC Med Genomics 2012 5 3 10.1186/1755-8794-5-3 22260379
49. MYC oncogenes and human neoplastic disease. Nesbit CE, Tersak JM, Prochownik EV, Oncogene 1999 18 3004 3016 10.1038/sj.onc.1202746 10378696
50. Deconstructing myc. Eisenman RN, Genes Dev 2001 15 2023 2030 10.1101/gad928101 11511533
51. The role of Sp1 and Sp3 in normal and cancer cell biology. Li L, Davie JR, Ann Anat 2010 192 275 283 10.1016/j.aanat.2010.07.010 20810260
52. JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, Arenillas DJ, Buchman S, Chen CY, Chou A, Ienasescu H, Lim J, Shyr C, Tan G, Zhou M, Lenhard B, Sandelin A, Wasserman WW, Nucleic Acids Res 2014 42 142 147 10.1093/nar/gkt997 24194598
53. HOCOMOCO: a comprehensive collection of human transcription factor binding sites models. Kulakovskiy IV, Medvedeva YA, Schaefer U, Kasianov AS, Vorontsov IE, Bajic VB, Makeev VJ, Nucleic Acids Res 2013 41 195 D202 10.1093/nar/gks1089 23175603
54. Unsupervised pattern discovery in human chromatin structure through genomic segmentation. Hoffman MM, Buske OJ, Wang J, Weng Z, Bilmes JA, Noble WS, Nat Methods 2012 9 473 476 10.1038/nmeth.1937 22426492
55. ChromHMM: automating chromatin-state discovery and characterization. Ernst J, Kellis M, Nat Methods 2012 9 215 216 10.1038/nmeth.1906 22373907
56. Additivity in protein-DNA interactions: how good an approximation is it? Benos PV, Bulyk ML, Stormo GD, Nucleic Acids Res 2002 30 4442 4451 10.1093/nar/gkf578 12384591