Evaluating the impact of single nucleotide variants on transcription factor binding

Nucleic Acids Research

Volumn 44, Issue 21, 2016, Pages 10106-10116

  Shi, Wenqiang ^a   Fornes, Oriol ^a   Mathelier, Anthony ^a,b   Wasserman, Wyeth W ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CCAAT ENHANCER BINDING PROTEIN; CCAAT ENHANCER BINDING PROTEIN BETA; DEOXYRIBONUCLEASE I; DNA; E1A ASSOCIATED P300 PROTEIN; HISTONE; INTERFERON REGULATORY FACTOR 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR 7 LIKE 2; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR FLI 1; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR RUNX3; CHROMATIN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA SEQUENCE; GENOTYPE; HETEROZYGOSITY; HISTONE MODIFICATION; MEASUREMENT ACCURACY; PREDICTION; PROTEIN BINDING; PROTEIN DNA BINDING; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM; ALLELE; BIOLOGY; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; GENETICS; HETEROZYGOTE; HUMAN; METABOLISM; PROCEDURES;

ALLELES; BINDING SITES; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; COMPUTATIONAL BIOLOGY; DEOXYRIBONUCLEASE I; HETEROZYGOTE; HISTONES; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE; TRANSCRIPTION FACTORS;

EID: 85016141829     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw691     Document Type: Article

References (60)

1. Li, M.J., Wang, L.Y., Xia, Z., Sham, P.C. and Wang, J. (2013) GWAS3D: Detecting human regulatory variants by integrative analysis of genome-wide associations, chromosome interactions and histone modifications. Nucleic Acids Res., 41, W150-W158.
2. Khurana, E., Fu, Y., Colonna, V., Mu, X.J., Kang, H.M., Lappalainen, T., Sboner, A., Lochovsky, L., Chen, J., Harmanci, A. et al. (2013) Integrative annotation of variants from 1092 humans: Application to cancer genomics. Science, 342, 1235587.
3. Andersen, M.C., Engstrom, P.G., Lithwick, S., Arenillas, D., Eriksson, P., Lenhard, B., Wasserman, W.W. and Odeberg, J. (2008) In silico detection of sequence variations modifying transcriptional regulation. PLoS Comput. Biol., 4, e5.
4. Macintyre, G., Bailey, J., Haviv, I. and Kowalczyk, A. (2010) is-rSNP: A novel technique for in silico regulatory SNP detection. Bioinformatics, 26, i524-i530.
5. Wang, J. and Batmanov, K. (2015) BayesPI-BAR:A new biophysical model for characterization of regulatory sequence variations. Nucleic Acids Res., 43, e147.
6. Lee, D., Gorkin, D.U., Baker, M., Strober, B.J., Asoni, A.L., McCallion, A.S. and Beer, M.A. (2015) A method to predict the impact of regulatory variants from DNA sequence. Nat. Genet., 47, 955-961.
7. Kasowski, M., Grubert, F., Heffelfinger, C., Hariharan, M., Asabere, A., Waszak, S.M., Habegger, L., Rozowsky, J., Shi, M., Urban, A.E. et al. (2010) Variation in transcription factor binding among humans. Science, 328, 232-235.
8. Boyle, A.P., Hong, E.L., Hariharan, M., Cheng, Y., Schaub, M.A., Kasowski, M., Karczewski, K.J., Park, J., Hitz, B.C., Weng, S. et al. (2012) Annotation of functional variation in personal genomes using RegulomeDB. Genome Res., 22, 1790-1797.
9. Herrmann, C., Van de Sande, B., Potier, D. and Aerts, S. (2012) i-cisTarget: An integrative genomics method for the prediction of regulatory features and cis-regulatory modules. Nucleic Acids Res., 40, e114.
10. Karczewski, K.J., Dudley, J.T., Kukurba, K.R., Chen, R., Butte, A.J., Montgomery, S.B. and Snyder, M. (2013) Systematic functional regulatory assessment of disease-Associated variants. Proc. Natl. Acad. Sci. U.S.A., 110, 9607-9612.
11. Consortium, E.P. (2012) An integrated encyclopedia of DNA elements in the human genome. Nature, 489, 57-74.
12. Kellis, M., Wold, B., Snyder, M.P., Bernstein, B.E., Kundaje, A., Marinov, G.K., Ward, L.D., Birney, E., Crawford, G.E., Dekker, J. et al. (2014) Defining functional DNA elements in the human genome. Proc. Natl. Acad. Sci. U.S.A., 111, 6131-6138.
13. Rozowsky, J., Abyzov, A., Wang, J., Alves, P., Raha, D., Harmanci, A., Leng, J., Bjornson, R., Kong, Y., Kitabayashi, N. et al. (2011) AlleleSeq: Analysis of allele-specific expression and binding in a network framework. Mol. Syst. Biol., 7, 522.
14. Younesy, H., Möller, T., Heravi-Moussavi, A., Cheng, J.B., Costello, J.F., Lorincz, M.C., Karimi, M.M. and Jones, S.J.M. (2014) ALEA: A toolbox for allele-specific epigenomics analysis. Bioinformatics, 30, 1172-1174.
15. Bailey, S.D., Virtanen, C., Haibe-Kains, B. and Lupien, M. (2015) ABC: A tool to identify SNVs causing allele-specific transcription factor binding from ChIP-Seq experiments. Bioinformatics, 31, 3507-3509.
16. Zuo, C., Shin, S. and Keles, S. (2015) atSNP: Transcription factor binding affinity testing for regulatory SNP detection. Bioinformatics, 31, 3353-3355.
17. Chen, J., Rozowsky, J., Galeev, T.R., Harmanci, A., Kitchen, R., Bedford, J., Abyzov, A., Kong, Y., Regan, L. and Gerstein, M. (2016) A uniform survey of allele-specific binding and expression over 1000-Genomes-Project individuals. Nat. Commun., 7, 11101.
18. Reddy, T.E., Gertz, J., Pauli, F., Kucera, K.S., Varley, K.E., Newberry, K.M., Marinov, G.K., Mortazavi, A., Williams, B.A., Song, L. et al. (2012) Effects of sequence variation on differential allelic transcription factor occupancy and gene expression. Genome Res., 22, 860-869.
19. Drmanac, R., Sparks, A.B., Callow, M.J., Halpern, A.L., Burns, N.L., Kermani, B.G., Carnevali, P., Nazarenko, I., Nilsen, G.B., Yeung, G. et al. (2010) Human genome sequencing using unchained base reads on self-Assembling DNA nanoarrays. Science, 327, 78-81.
20. Adey, A., Burton, J.N., Kitzman, J.O., Hiatt, J.B., Lewis, A.P., Martin, B.K., Qiu, R., Lee, C. and Shendure, J. (2013) The haplotype-resolved genome and epigenome of the aneuploid HeLa cancer cell line. Nature, 500, 207-211.
21. DePristo, M.A., Banks, E., Poplin, R., Garimella, K.V., Maguire, J.R., Hartl, C., Philippakis, A.A., del Angel, G., Rivas, M.A., Hanna, M. et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet., 43, 491-498.
22. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R. and 1000 Genome Project Data Processing Subgroup (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25, 2078-2079.
23. Degner, J.F., Marioni, J.C., Pai, A.A., Pickrell, J.K., Nkadori, E., Gilad, Y. and Pritchard, J.K. (2009) Effect of read-mapping biases on detecting allele-specific expression from RNA-sequencing data. Bioinformatics, 25, 3207-3212.
24. Landt, S.G., Marinov, G.K., Kundaje, A., Kheradpour, P., Pauli, F., Batzoglou, S., Bernstein, B.E., Bickel, P., Brown, J.B., Cayting, P. et al. (2012) ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res., 22, 1813-1831.
25. Wilbanks, E.G. and Facciotti, M.T. (2010) Evaluation of algorithm performance in ChIP-seq peak detection. PloS One, 5, e11471.
26. Worsley Hunt, R., Mathelier, A., Del Peso, L. and Wasserman, W.W. (2014) Improving analysis of transcription factor binding sites within ChIP-Seq data based on topological motif enrichment. BMC Genomics, 15, 472.
27. Maurano, M.T., Haugen, E., Sandstrom, R., Vierstra, J., Shafer, A., Kaul, R. and Stamatoyannopoulos, J.A. (2015) Large-scale identification of sequence variants influencing human transcription factor occupancy in vivo. Nat. Genet., 47, 1393-1401.
28. Mathelier, A., Zhao, X., Zhang, A.W., Parcy, F., Worsley-Hunt, R., Arenillas, D.J., Buchman, S., Chen, C.Y., Chou, A., Ienasescu, H. et al. (2014) JASPAR 2014: An extensively expanded and updated open-Access database of transcription factor binding profiles. Nucleic Acids Res., 42, D142-D147.
29. Cock, P.J., Antao, T., Chang, J.T., Chapman, B.A., Cox, C.J., Dalke, A., Friedberg, I., Hamelryck, T., Kauff, F., Wilczynski, B. et al. (2009) Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics, 25, 1422-1423.
30. Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y.C., Laslo, P., Cheng, J.X., Murre, C., Singh, H. and Glass, C.K. (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell, 38, 576-589.
31. Medina-Rivera, A., Defrance, M., Sand, O., Herrmann, C., Castro-Mondragon, J.A., Delerce, J., Jaeger, S., Blanchet, C., Vincens, P., Caron, C. et al. (2015) RSAT 2015: Regulatory Sequence Analysis Tools. Nucleic Acids Res., 43, W50-W56.
32. Breiman, L. (2001) Random forests. Mach. Learn., 45, 5-32.
33. Kuhn, M. (2008) Building predictive models in R using the caret package. Journal of Statistical Software, 28, 1-26.
34. Anaissi, A., Kennedy, P.J., Goyal, M. and Catchpoole, D.R. (2013) A balanced iterative random forest for gene selection from microarray data. BMC Bioinformatics, 14, 261.
35. Bekkar, M. and Alitouche, T.A. (2013) Imbalanced data learning approaches review. Int. J. Data Mining Knowl. Manag. Process, 3, 15-33.
36. Ghandi, M., Lee, D., Mohammad-Noori, M. and Beer, M.A. (2014) Enhanced regulatory sequence prediction using gapped k-mer features. PLoS Comput. Biol., 10, e1003711.
37. Kilpinen, H., Waszak, S.M., Gschwind, A.R., Raghav, S.K., Witwicki, R.M., Orioli, A., Migliavacca, E., Wiederkehr, M., Gutierrez-Arcelus, M., Panousis, N.I. et al. (2013) Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription. Science, 342, 744-747.
38. Wasserman, W.W. and Sandelin, A. (2004) Applied bioinformatics for the identification of regulatory elements. Nat. Rev. Genet., 5, 276-287.
39. Melton, C., Reuter, J.A., Spacek, D.V. and Snyder, M. (2015) Recurrent somatic mutations in regulatory regions of human cancer genomes. Nat. Genet., 47, 710-716.
40. Mathelier, A., Lefebvre, C., Zhang, A.W., Arenillas, D.J., Ding, J., Wasserman, W.W. and Shah, S.P. (2015) Cis-regulatory somatic mutations and gene-expression alteration in B-cell lymphomas. Genome Biol., 16, 84.
41. Karczewski, K.J., Tatonetti, N.P., Landt, S.G., Yang, X., Slifer, T., Altman, R.B. and Snyder, M. (2011) Cooperative transcription factor associations discovered using regulatory variation. Proc. Natl. Acad. Sci. U.S.A., 108, 13353-13358.
42. Stefflova, K., Thybert, D., Wilson, M.D., Streeter, I., Aleksic, J., Karagianni, P., Brazma, A., Adams, D.J., Talianidis, I., Marioni, J.C. et al. (2013) Cooperativity and rapid evolution of cobound transcription factors in closely related mammals. Cell, 154, 530-540.
43. Stark, C., Breitkreutz, B.J., Reguly, T., Boucher, L., Breitkreutz, A. and Tyers, M. (2006) BioGRID: A general repository for interaction datasets. Nucleic Acids Res., 34, D535-D539.
44. Leung, D., Jung, I., Rajagopal, N., Schmitt, A., Selvaraj, S., Lee, A.Y., Yen, C.A., Lin, S., Lin, Y., Qiu, Y. et al. (2015) Integrative analysis of haplotype-resolved epigenomes across human tissues. Nature, 518, 350-354.
45. Harvey, C.T., Moyerbrailean, G.A., Davis, G.O., Wen, X., Luca, F. and Pique-Regi, R. (2014) QuASAR: quantitative allele-specific analysis of reads. Bioinformatics, 31, 1235-1242.
46. van de Geijn, B., McVicker, G., Gilad, Y. and Pritchard, J.K. (2015) WASP: Allele-specific software for robust molecular quantitative trait locus discovery. Nat. Methods, 12, 1061-1063.
47. Steinhauser, S., Kurzawa, N., Eils, R. and Herrmann, C. (2016) A comprehensive comparison of tools for differential ChIP-seq analysis. Brief. Bioinform., bbv110.
48. Stormo, G.D. (2000) DNA binding sites: representation and discovery. Bioinformatics, 16, 16-23.
49. Manke, T., Heinig, M. and Vingron, M. (2010) Quantifying the effect of sequence variation on regulatory interactions. Hum. Mutat., 31, 477-483.
50. Huang, D. and Ovcharenko, I. (2014) Identifying causal regulatory SNPs in ChIP-seq enhancers. Nucleic Acids Res., 43, 225-236.
51. Nakahashi, H., Kwon, K.R., Resch, W., Vian, L., Dose, M., Stavreva, D., Hakim, O., Pruett, N., Nelson, S., Yamane, A. et al. (2013) A genome-wide map of CTCF multivalency redefines the CTCF code. Cell Rep., 3, 1678-1689.
52. Maerkl, S.J. and Quake, S.R. (2007) A systems approach to measuring the binding energy landscapes of transcription factors. Science, 315, 233-237.
53. Nutiu, R., Friedman, R.C., Luo, S., Khrebtukova, I., Silva, D., Li, R., Zhang, L., Schroth, G.P. and Burge, C.B. (2011) Direct measurement of DNA affinity landscapes on a high-Throughput sequencing instrument. Nat. Biotechnol., 29, 659-664.
54. Levo, M., Zalckvar, E., Sharon, E., Dantas Machado, A.C., Kalma, Y., Lotam-Pompan, M., Weinberger, A., Yakhini, Z., Rohs, R. and Segal, E. (2015) Unraveling determinants of transcription factor binding outside the core binding site. Genome Res., 25, 1018-1029.
55. Zhou, T., Yang, L., Lu, Y., Dror, I., Dantas Machado, A.C., Ghane, T., Di Felice, R. and Rohs, R. (2013) DNAshape: A method for the high-Throughput prediction of DNA structural features on a genomic scale. Nucleic Acids Res., 41, W56-W62.
56. Zhou, T., Shen, N., Yang, L., Abe, N., Horton, J., Mann, R.S., Bussemaker, H.J., Gordan, R. and Rohs, R. (2015) Quantitative modeling of transcription factor binding specificities using DNA shape. Proc. Natl. Acad. Sci. U.S.A., 112, 4654-4659.
57. Cavalli, M., Pan, G., Nord, H., Wallerman, O., Wallen Arzt, E., Berggren, O., Elvers, I., Eloranta, M.L., Ronnblom, L., Lindblad Toh, K. et al. (2016) Allele-specific transcription factor binding to common and rare variants associated with disease and gene expression. Hum. Genet., 135, 485-497.
58. Ding, Z., Ni, Y., Timmer, S.W., Lee, B.K., Battenhouse, A., Louzada, S., Yang, F., Dunham, I., Crawford, G.E., Lieb, J.D. et al. (2014) Quantitative genetics of CTCF binding reveal local sequence effects and different modes of X-chromosome association. PLoS Genet., 10, e1004798.
59. Waszak, S.M., Delaneau, O., Gschwind, A.R., Kilpinen, H., Raghav, S.K., Witwicki, R.M., Orioli, A., Wiederkehr, M., Panousis, N.I., Yurovsky, A. et al. (2015) Population variation and genetic control of modular chromatin architecture in humans. Cell, 162, 1039-1050.
60. Mathelier, A., Shi, W. and Wasserman, W.W. (2015) Identification of altered cis-regulatory elements in human disease. Trends Genet., 31, 67-76.