A uniform survey of allele-specific binding and expression over 1000-Genomes-Project individuals

Nature Communications

Volumn 7, Issue , 2016, Pages

  Chen, Jieming ^a   Rozowsky, Joel ^a   Galeev, Timur R ^a   Harmanci, Arif ^a   Kitchen, Robert ^a   Bedford, Jason ^a   Abyzov, Alexej ^a,d   Kong, Yong ^b,c   Regan, Lynne ^a   Gerstein, Mark ^a,b  

^a YALE UNIVERSITY   (United States)

^b Yale University   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR PU 1;

AGGREGATION; ALLELE; CHROMOSOME; DATA SET; GENE EXPRESSION; GENOME; HETEROGENEITY;

5' UNTRANSLATED REGION; ALLELE; ALLELIC IMBALANCE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; COPY NUMBER VARIATION; DNA SEQUENCE; FUNCTIONAL GENOMICS; GENE EXPRESSION; GENE FREQUENCY; GENE MAPPING; GENETIC HETEROGENEITY; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; HUMAN GENOME; INHERITANCE; MAJOR CLINICAL STUDY; PROMOTER REGION; PURIFYING SELECTION; RNA SEQUENCE; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE VARIANT; ALGORITHM; BINDING SITE; BIOLOGY; CHROMOSOMAL MAPPING; GENETIC DATABASE; GENETICS; GENOMICS; GENOTYPE; HIGH THROUGHPUT SEQUENCING; HUMAN GENOME PROJECT; INTERNET; MOLECULAR GENETICS; PERSONALIZED MEDICINE; PROCEDURES; SINGLE NUCLEOTIDE POLYMORPHISM;

ALGORITHMS; BINDING SITES; CHROMOSOME MAPPING; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; GENE EXPRESSION; GENE FREQUENCY; GENOME, HUMAN; GENOMICS; GENOTYPE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMAN GENOME PROJECT; HUMANS; INTERNET; MOLECULAR SEQUENCE ANNOTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; PRECISION MEDICINE;

EID: 84963984126     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11101     Document Type: Article

References (70)

1. Wheeler, D. A. et al. The complete genome of an individual by massively parallel DNA sequencing. Nature 452, 872-876 (2008).
2. Lupski, J. R. et al. Whole-genome sequencing in a patient with Charcot-Marie-Tooth neuropathy. N. Engl. J. Med. 362, 1181-1191 (2010).
3. Abecasis, G. R. et al. An integrated map of genetic variation from 1,092 human genomes. Nature 491, 56-65 (2012).
4. Muddyman, D., Smee, C., Griffin, H. & Kaye, J. Implementing a successful data-management framework: the UK10K managed access model. Genome Med. 5, 100 (2013).
5. Pickrell, J. K. et al. Understanding mechanisms underlying human gene expression variation with RNA sequencing. Nature 464, 768-772 (2010).
6. Majewski, J. & Pastinen, T. The study of eQTL variations by RNA-seq: from SNPs to phenotypes. Trends Genet. 27, 72-79 (2011).
7. Montgomery, S. B., Lappalainen, T., Gutierrez-Arcelus, M. & Dermitzakis, E. T. Rare and common regulatory variation in population-scale sequenced human genomes. PLoS Genet. 7, e1002144 (2011).
8. Djebali, S. et al. Landscape of transcription in human cells. Nature 489, 101-108 (2012).
9. McDaniell, R. et al. Heritable individual-specific and allele-specific chromatin signatures in humans. Science 328, 235-239 (2010).
10. Yan, H., Yuan, W., Velculescu, V. E., Vogelstein, B. & Kinzler, K. W. Allelic variation in human gene expression. Science 297, 1143 (2002).
11. Lo, H. S. et al. Allelic variation in gene expression is common in the human genome. Genome Res. 13, 1855-1862 (2003).
12. Lappalainen, T. et al. Transcriptome and genome sequencing uncovers functional variation in humans. Nature 501, 506-511 (2013).
13. Rozowsky, J. et al. AlleleSeq: analysis of allele-specific expression and binding in a network framework. Mol. Syst. Biol. 7, 522 (2011).
14. Kilpinen, H. et al. Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription. Science 342, 744-747 (2013).
15. Kasowski, M. et al. Extensive variation in chromatin states across humans. Science 342, 750-752 (2013).
16. Stevenson, K. R., Coolon, J. D. & Wittkopp, P. J. Sources of bias in measures of allele-specific expression derived from RNA-sequence data aligned to a single reference genome. BMC Genomics 14, 536 (2013).
17. Degner, J. F. et al. Effect of read-mapping biases on detecting allele-specific expression from RNA-sequencing data. Bioinformatics 25, 3207-3212 (2009).
18. Kent, W. J. et al. The human genome browser at UCSC. Genome Res. 12, 996-1006 (2002).
19. Li, X. et al. Transcriptome sequencing of a large human family identifies the impact of rare noncoding variants. Am. J. Hum. Genet. 95, 245-256 (2014).
20. Bernstein, B. E. et al. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
21. Goldmit, M. & Bergman, Y. Monoallelic gene expression: a repertoire of recurrent themes. Immunol. Rev. 200, 197-214 (2004).
22. Zakharova, I. S., Shevchenko, A. I. & Zakian, S. M. Monoallelic gene expression in mammals. Chromosoma 118, 279-290 (2009).
23. Morison, I. M., Paton, C. J. & Cleverley, S. D. The imprinted gene and parentof-origin effect database. Nucleic Acids Res. 29, 275-276 (2001).
24. Olender, T., Nativ, N. & Lancet, D. HORDE: comprehensive resource for olfactory receptor genomics. Methods Mol. Biol. 1003, 23-38 (2013).
25. Harrow, J. et al. GENCODE: the reference human genome annotation for the ENCODE Project. Genome Res. 22, 1760-1774 (2012).
26. Horsthemke, B. & Buiting, K. Imprinting defects on human chromosome 15. Cytogenet. Genome Res. 113, 292-299 (2006).
27. Pollard, K. S. et al. A genome-wide approach to identifying novel-imprinted genes. Hum. Genet. 122, 625-634 (2008).
28. Khurana, E. et al. Integrative annotation of variants from 1092 humans: application to cancer genomics. Science 342, 1235587 (2013).
29. Skelly, D. A., Johansson, M., Madeoy, J., Wakefield, J. & Akey, J. M. A powerful and flexible statistical framework for testing hypotheses of allele-specific gene expression from RNA-seq data. Genome Res. 21, 1728-1737 (2011).
30. Zhang, S. et al. Genome-wide identification of allele-specific effects on gene expression for single and multiple individuals. Gene 533, 366-373 (2014).
31. Castel, S. E., Levy-Moonshine, A., Mohammadi, P., Banks, E. & Lappalainen, T. Tools and best practices for data processing in allelic expression analysis. Genome Biol. 16, 195 (2015).
32. Satya, R. V., Zavaljevski, N. & Reifman, J. A new strategy to reduce allelic bias in RNA-Seq readmapping. Nucleic Acids Res. 40, e127 (2012).
33. Panousis, N. I., Gutierrez-Arcelus, M., Dermitzakis, E. T. & Lappalainen, T. Allelic mapping bias in RNA-sequencing is not a major confounder in eQTL studies. Genome Biol. 15, 467 (2014).
34. Sudmant, P. H. et al. An integrated map of structural variation in 2,504 human genomes. Nature 526, 75-81 (2015).
35. van de Geijn, B., McVicker, G., Gilad, Y. & Pritchard, J. K. WASP: allele-specific software for robust molecular quantitative trait locus discovery. Nat. Methods 12, 1061-1063 (2015).
36. Tao, H., Cox, D. R. & Frazer, K. A. Allele-specific KRT1 expression is a complex trait. PLoS Genet. 2, 0848-0858 (2006).
37. Baran, Y. et al. The landscape of genomic imprinting across diverse adult human tissues. Genome Res. 25, 927-936 (2015).
38. Amin, A. S. et al. Variants in the 3′ untranslated region of the KCNQ1-encoded Kv7.1 potassium channel modify disease severity in patients with type 1 long QT syndrome in an allele-specific manner. Eur. Heart J. 33, 714-723 (2012).
39. Valle, L. et al. Germline allele-specific expression of TGFBR1 confers an increased risk of colorectal cancer. Science 321, 1361-1365 (2008).
40. Price, A. L. et al. Pooled association tests for rare variants in exon-resequencing studies. Am. J. Hum. Genet. 86, 832-838 (2010).
41. Han, F. & Pan, W. A data-adaptive sum test for disease association with multiple common or rare variants. Hum. Hered. 70, 42-54 (2010).
42. Fu, Y. et al. FunSeq2: a framework for prioritizing noncoding regulatory variants in cancer. Genome Biol. 15, 480 (2014).
43. Boodhoo, A. et al. A promoter polymorphism in the central MHC gene, IKBL, influences the binding of transcription factors USF1 and E47 on disease-associated haplotypes. Gene Expr. 12, 1-11 (2004).
44. Kim, J. D. O. et al. Identification of clustered YY1 binding sites in imprinting control regions. Genome Res. 16, 901-911 (2006).
45. Chaumeil, J. & Skok, J. A. The role of CTCF in regulating V(D)J recombination. Curr. Opin. Immunol. 24, 153-159 (2012).
46. Kitzman, J. O. et al. Haplotype-resolved genome sequencing of a Gujarati Indian individual. Nat. Biotechnol. 29, 59-63 (2011).
47. Peters, B. A. et al. Accurate whole-genome sequencing and haplotyping from 10 to 20 human cells. Nature 487, 190-195 (2012).
48. Lonsdale, J. et al. GTEx Consortium. The Genotype-Tissue Expression (GTEx) project. Nat. Genet. 45, 580-585 (2013).
49. Ardlie, K. G. et al. GTEx Consortium. The Genotype-Tissue Expression (GTEx) pilot analysis: Multitissue gene regulation in humans. Science 348, 648-660 (2015).
50. Bustamante, C. D., Burchard, E. G. & De la Vega, F. M. Genomics for the world. Nature 475, 163-165 (2011).
51. Abyzov, A., Urban, A. E., Snyder, M. & Gerstein, M. CNVnator: an approach to discover, genotype, and characterize typical and atypical CNVs from family and population genome sequencing. Genome Res. 21, 974-984 (2011).
52. Lalonde, E. et al. RNA sequencing reveals the role of splicing polymorphisms in regulating human gene expression. Genome Res. 21, 545-554 (2011).
53. Montgomery, S. B. et al. Transcriptome genetics using second generation sequencing in a Caucasian population. Nature 464, 773-777 (2010).
54. McVicker, G. et al. Identification of genetic variants that affect histone modifications in human cells. Science 342, 747-749 (2013).
55. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
56. Yee, T. VGAM: Vector Generalized Linear and Additive Models (2014; Available at Accession date: Jan 4 2015.
57. Rozowsky, J. et al. PeakSeq enables systematic scoring of ChIP-seq experiments relative to controls. Nat. Biotechnol. 27, 66-75 (2009).
58. Robinson, J. T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24-26 (2011).
59. Visscher, P. M., Hill, W. G. & Wray, N. R. Heritability in the genomics era-concepts and misconceptions. Nat. Rev. Genet. 9, 255-266 (2008).
60. Vaquerizas, J. M., Kummerfeld, S. K., Teichmann, S. A. & Luscombe, N. M. A census of human transcription factors: function, expression and evolution. Nat. Rev. Genet. 10, 252-263 (2009).
61. Gerstein, M. B. et al. Architecture of the human regulatory network derived from ENCODE data. Nature 489, 91-100 (2012).
62. Lefranc, M.-P. et al. IMGT-Choreography for immunogenetics and immunoinformatics. In Silico Biol. 5, 45-60 (2005).
63. Morison, I. M., Ramsay, J. P. & Spencer, H. G. A census of mammalian imprinting. Trends Genet. 21, 457-465 (2005).
64. Ernst, J. & Kellis, M. ChromHMM: automating chromatin-state discovery and characterization. Nat. Methods 9, 215-216 (2012).
65. Hoffman, M. M. et al. Integrative annotation of chromatin elements from ENCODE data. Nucleic Acids Res. 41, 827-841 (2013).
66. Yip, K. Y. et al. Classification of human genomic regions based on experimentally determined binding sites of more than 100 transcription-related factors. Genome Biol. 13, R48 (2012).
67. Visel, A., Minovitsky, S., Dubchak, I. & Pennacchio, L. A. VISTA Enhancer Browser-a database of tissue-specific human enhancers. Nucleic Acids Res. 35, D88-D92 (2007).
68. Eisenberg, E. & Levanon, E. Y. Human housekeeping genes, revisited. Trends Genet. 29, 569-574 (2013).
69. Kheradpour, P. & Kellis, M. Systematic discovery and characterization of regulatory motifs in ENCODE TF binding experiments. Nucleic Acids Res. 42, 2976-2987 (2014).
70. Touzet, H. & Varré, J.-S. Efficient and accurate P-value computation for Position Weight Matrices. Algorithms Mol. Biol. 2, 15 (2007).