Discover hidden splicing variations by mapping personal transcriptomes to personal genomes

Nucleic Acids Research

Volumn 43, Issue 22, 2015, Pages 10612-10622

  Stein, Shayna ^a   Lu, Zhi Xiang ^a   Bahrami Samani, Emad ^a   Park, Juw Won ^a   Xing, Yi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME; RNA SPLICING;

ARTICLE; CONTROLLED STUDY; GENE; GENE MAPPING; GENETIC TRAIT; GENETIC VARIABILITY; GENOME ANALYSIS; GENOME-WIDE ASSOCIATION STUDY; HUMAN; ICA1 GENE; OAS1 GENE; PRIORITY JOURNAL; RNA SEQUENCE; RNA SPLICING; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM; VALIDATION PROCESS; ALTERNATIVE RNA SPLICING; DISEASES; EVALUATION STUDY; GENE EXPRESSION PROFILING; GENETICS; HUMAN GENOME; PROCEDURES; SEQUENCE ANALYSIS;

ALTERNATIVE SPLICING; DISEASE; GENE EXPRESSION PROFILING; GENOME, HUMAN; GENOME-WIDE ASSOCIATION STUDY; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA SPLICE SITES; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84964751119     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1099     Document Type: Article

References (80)

1. Nilsen, T.W. and Graveley, B.R. (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature, 463, 457-463.
2. Wang, E.T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S.F., Schroth, G.P. and Burge, C.B. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature, 456, 470-476.
3. Pan, Q., Shai, O., Lee, L.J., Frey, B.J. and Blencowe, B.J. (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet., 40, 1413-1415.
4. Wang, G.S. and Cooper, T.A. (2007) Splicing in disease: disruption of the splicing code and the decoding machinery. Nat. Rev. Genet., 8, 749-761.
5. Teraoka, S.N., Telatar, M., Becker-Catania, S., Liang, T., Onengut, S., Tolun, A., Chessa, L., Sanal, O., Bernatowska, E., Gatti, R.A. et al. (1999) Splicing defects in the ataxia-telangiectasia gene, ATM: underlying mutations and consequences. Am. J. Hum. Genet., 64, 1617-1631.
6. Ars, E., Serra, E., Garcia, J., Kruyer, H., Gaona, A., Lazaro, C. and Estivill, X. (2000) Mutations affecting mRNA splicing are the most common molecular defects in patients with neurofibromatosis type 1. Hum. Mol. Genet., 9, 237-247.
7. Hull, J., Campino, S., Rowlands, K., Chan, M.S., Copley, R.R., Taylor, M.S., Rockett, K., Elvidge, G., Keating, B., Knight, J. et al. (2007) Identification of common genetic variation that modulates alternative splicing. PLoS Genet., 3, e99.
8. Kwan, T., Benovoy, D., Dias, C., Gurd, S., Provencher, C., Beaulieu, P., Hudson, T.J., Sladek, R. and Majewski, J. (2008) Genome-wide analysis of transcript isoform variation in humans. Nat. Genet., 40, 225-231.
9. 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.
10. Coulombe-Huntington, J., Lam, K.C., Dias, C. and Majewski, J. (2009) Fine-scale variation and genetic determinants of alternative splicing across individuals. PLoS Genet., 5, e1000766.
11. Garcia-Blanco, M.A., Baraniak, A.P. and Lasda, E.L. (2004) Alternative splicing in disease and therapy. Nat. Biotechnol., 22, 535-546.
12. Ward, A.J. and Cooper, T.A. (2010) The pathobiology of splicing. J. Pathol., 220, 152-163.
13. Lu, Z.X., Jiang, P. and Xing, Y. (2012) Genetic variation of pre-mRNA alternative splicing in human populations. Wiley Interdiscip. Rev. RNA, 3, 581-592.
14. Wang, Z. and Burge, C.B. (2008) Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA, 14, 802-813.
15. Sheth, N., Roca, X., Hastings, M.L., Roeder, T., Krainer, A.R. and Sachidanandam, R. (2006) Comprehensive splice-site analysis using comparative genomics. Nucleic Acids Res., 34, 3955-3967.
16. Kurmangaliyev, Y.Z., Sutormin, R.A., Naumenko, S.A., Bazykin, G.A. and Gelfand, M.S. (2013) Functional implications of splicing polymorphisms in the human genome. Hum. Mol. Genet., 22, 3449-3459.
17. Krawczak, M., Reiss, J. and Cooper, D.N. (1992) The mutational spectrum of single base-pair substitutions in mRNA splice junctions of human genes: causes and consequences. Hum. Genet., 90, 41-54.
18. Katz, Y., Wang, E.T., Airoldi, E.M. and Burge, C.B. (2010) Analysis and design of RNA sequencing experiments for identifying isoform regulation. Nat. Methods, 7, 1009-1015.
19. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 5, 621-628.
20. Shen, S., Park, J.W., Huang, J., Dittmar, K.A., Lu, Z.X., Zhou, Q., Carstens, R.P. and Xing, Y. (2012) MATS: A Bayesian framework for flexible detection of differential alternative splicing from RNA-Seq data. Nucleic Acids Res., 40, e61.
21. Shen, S., Park, J.W., Lu, Z.X., Lin, L., Henry, M.D., Wu, Y.N., Zhou, Q. and Xing, Y. (2014) rMATS: robust and flexible detection of differential alternative splicing from replicate RNA-Seq data. Proc. Natl. Acad. Sci. U.S.A., 111, E5593-E5601.
22. Gutierrez-Arcelus, M., Ongen, H., Lappalainen, T., Montgomery, S.B., Buil, A., Yurovsky, A., Bryois, J., Padioleau, I., Romano, L., Planchon, A. et al. (2015) Tissue-specific effects of genetic and epigenetic variation on gene regulation and splicing. PLoS Genet., 11, e1004958.
23. Lappalainen, T., Sammeth, M., Friedlander, M.R., t Hoen, P.A., Monlong, J., Rivas, M.A., Gonzalez-Porta, M., Kurbatova, N., Griebel, T., Ferreira, P.G. et al. (2013) Transcriptome and genome sequencing uncovers functional variation in humans. Nature, 501, 506-511.
24. Lalonde, E., Ha, K.C., Wang, Z., Bemmo, A., Kleinman, C.L., Kwan, T., Pastinen, T. and Majewski, J. (2011) RNA sequencing reveals the role of splicing polymorphisms in regulating human gene expression. Genome Res., 21, 545-554.
25. Mele, M., Ferreira, P.G., Reverter, F., DeLuca, D.S., Monlong, J., Sammeth, M., Young, T.R., Goldmann, J.M., Pervouchine, D.D., Sullivan, T.J. et al. (2015) Human genomics. The human transcriptome across tissues and individuals. Science, 348, 660-665.
26. Zhao, K., Lu, Z.X., Park, J.W., Zhou, Q. and Xing, Y. (2013) GLiMMPS: robust statistical model for regulatory variation of alternative splicing using RNA-seq data. Genome Biol., 14, R74.
27. Pickrell, J.K., Marioni, J.C., Pai, A.A., Degner, J.F., Engelhardt, B.E., Nkadori, E., Veyrieras, J.B., Stephens, M., Gilad, Y. and Pritchard, J.K. (2010) Understanding mechanisms underlying human gene expression variation with RNA sequencing. Nature, 464, 768-772.
28. Battle, A., Mostafavi, S., Zhu, X., Potash, J.B., Weissman, M.M., McCormick, C., Haudenschild, C.D., Beckman, K.B., Shi, J., Mei, R. et al. (2014) Characterizing the genetic basis of transcriptome diversity through RNA-sequencing of 922 individuals. Genome Res., 24, 14-24.
29. Lee, J.H., Ang, J.K. and Xiao, X. (2013) Analysis and design of RNA sequencing experiments for identifying RNA editing and other single-nucleotide variants. RNA, 19, 725-732.
30. Munger, S.C., Raghupathy, N., Choi, K., Simons, A.K., Gatti, D.M., Hinerfeld, D.A., Svenson, K.L., Keller, M.P., Attie, A.D., Hibbs, M.A. et al. (2014) RNA-Seq alignment to individualized genomes improves transcript abundance estimates in multiparent populations. Genetics, 198, 59-73.
31. 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.
32. 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.
33. Trapnell, C., Pachter, L. and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
34. Au, K.F., Jiang, H., Lin, L., Xing, Y. and Wong, W.H. (2010) Detection of splice junctions from paired-end RNA-seq data by SpliceMap. Nucleic Acids Res., 38, 4570-4578.
35. Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M. and Gingeras, T.R. (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics, 29, 15-21.
36. Kim, D., Langmead, B. and Salzberg, S.L. (2015) HISAT: A fast spliced aligner with low memory requirements. Nat. Methods, 12, 357-360.
37. Genomes Project, C., Abecasis, G.R., Auton, A., Brooks, L.D., DePristo, M.A., Durbin, R.M., Handsaker, R.E., Kang, H.M., Marth, G.T. and McVean, G.A. (2012) An integrated map of genetic variation from 1, 092 human genomes. Nature, 491, 56-65.
38. Li, M.J., Wang, P., Liu, X., Lim, E.L., Wang, Z., Yeager, M., Wong, M.P., Sham, P.C., Chanock, S.J. and Wang, J. (2012) GWASdb: A database for human genetic variants identified by genome-wide association studies. Nucleic Acids Res., 40, D1047-D1054.
39. Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A., Bender, D., Maller, J., Sklar, P., de Bakker, P.I., Daly, M.J. et al. (2007) PLINK: A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet., 81, 559-575.
40. Barrett, J.C., Fry, B., Maller, J. and Daly, M.J. (2005) Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics, 21, 263-265.
41. Yeo, G. and Burge, C.B. (2004) Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J. Comput. Biol., 11, 377-394.
42. Lu, Z.X., Jiang, P., Cai, J.J. and Xing, Y. (2011) Context-dependent robustness to 5' splice site polymorphisms in human populations. Hum. Mol. Genet., 20, 1084-1096.
43. Konta, T., Takasaki, S., Ichikawa, K., Emi, M., Toriyama, S., Satoh, H., Ikeda, A., Suzuki, K., Mashima, Y., Shibata, Y. et al. (2010) The novel and independent association between single-point SNP of NPHP4 gene and renal function in non-diabetic Japanese population: The Takahata study. J. Hum. Genet., 55, 791-795.
44. Flicek, P., Amode, M.R., Barrell, D., Beal, K., Billis, K., Brent, S., Carvalho-Silva, D., Clapham, P., Coates, G., Fitzgerald, S. et al. (2014) Ensembl 2014. Nucleic Acids Res., 42, D749-D755.
45. Graham, R.R., Kozyrev, S.V., Baechler, E.C., Reddy, M.V., Plenge, R.M., Bauer, J.W., Ortmann, W.A., Koeuth, T., Gonzalez Escribano, M.F., Argentine et al. (2006) A common haplotype of interferon regulatory factor 5 (IRF5) regulates splicing and expression and is associated with increased risk of systemic lupus erythematosus. Nat. Genet., 38, 550-555.
46. Clark, D.N., Lambert, J.P., Till, R.E., Argueta, L.B., Greenhalgh, K.E., Henrie, B., Bills, T., Hawkley, T.F., Roznik, M.G., Sloan, J.M. et al. (2014) Molecular effects of autoimmune-risk promoter polymorphisms on expression, exon choice, and translational efficiency of interferon regulatory factor 5. J. Interferon Cytokine Res., 34, 354-365.
47. Clark, D.N., Read, R.D., Mayhew, V., Petersen, S.C., Argueta, L.B., Stutz, L.A., Till, R.E., Bergsten, S.M., Robinson, B.S., Baumann, D.G. et al. (2013) Four Promoters of IRF5 Respond Distinctly to Stimuli and are Affected by Autoimmune-Risk Polymorphisms. Front. Immunol., 4, 360.
48. Dieguez-Gonzalez, R., Calaza, M., Perez-Pampin, E., de la Serna, A.R., Fernandez-Gutierrez, B., Castaneda, S., Largo, R., Joven, B., Narvaez, J., Navarro, F. et al. (2008) Association of interferon regulatory factor 5 haplotypes, similar to that found in systemic lupus erythematosus, in a large subgroup of patients with rheumatoid arthritis. Arthritis Rheum., 58, 1264-1274.
49. Kristjansdottir, G., Sandling, J.K., Bonetti, A., Roos, I.M., Milani, L., Wang, C., Gustafsdottir, S.M., Sigurdsson, S., Lundmark, A., Tienari, P.J. et al. (2008) Interferon regulatory factor 5 (IRF5) gene variants are associated with multiple sclerosis in three distinct populations. J. Med. Genet., 45, 362-369.
50. Hiller, M., Huse, K., Szafranski, K., Jahn, N., Hampe, J., Schreiber, S., Backofen, R. and Platzer, M. (2006) Single-nucleotide polymorphisms in NAGNAG acceptors are highly predictive for variations of alternative splicing. Am. J. Hum. Genet., 78, 291-302.
51. Tang, W., Basu, S., Kong, X., Pankow, J.S., Aleksic, N., Tan, A., Cushman, M., Boerwinkle, E. and Folsom, A.R. (2010) Genome-wide association study identifies novel loci for plasma levels of protein C: The ARIC study. Blood, 116, 5032-5036.
52. Chakrabarti, A., Jha, B.K. and Silverman, R.H. (2011) New insights into the role of RNase L in innate immunity. J. Interferon Cytokine Res., 31, 49-57.
53. Bonnevie-Nielsen, V., Field, L.L., Lu, S., Zheng, D.J., Li, M., Martensen, P.M., Nielsen, T.B., Beck-Nielsen, H., Lau, Y.L. and Pociot, F. (2005) Variation in antiviral 2', 5'-oligoadenylate synthetase (2'5'AS) enzyme activity is controlled by a single-nucleotide polymorphism at a splice-acceptor site in the OAS1 gene. Am. J. Hum. Genet., 76, 623-633.
54. Oppermann, U.C. and Maser, E. (2000) Molecular and structural aspects of xenobiotic carbonyl metabolizing enzymes. Role of reductases and dehydrogenases in xenobiotic phase I reactions. Toxicology, 144, 71-81.
55. Oppermann, U., Filling, C., Hult, M., Shafqat, N., Wu, X., Lindh, M., Shafqat, J., Nordling, E., Kallberg, Y., Persson, B. et al. (2003) Short-chain dehydrogenases/reductases (SDR): The 2002 update. Chem. Biol. Interact., 143-144, 247-253.
56. Nobel, S., Abrahmsen, L. and Oppermann, U. (2001) Metabolic conversion as a pre-receptor control mechanism for lipophilic hormones. Eur. J. Biochem., 268, 4113-4125.
57. Oppermann, U.C., Filling, C. and Jornvall, H. (2001) Forms and functions of human SDR enzymes. Chem. Biol. Interact., 130-132, 699-705.
58. Ioannidis, J.P., Thomas, G. and Daly, M.J. (2009) Validating, augmenting and refining genome-wide association signals. Nat. Rev. Genet., 10, 318-329.
59. Schaub, M.A., Boyle, A.P., Kundaje, A., Batzoglou, S. and Snyder, M. (2012) Linking disease associations with regulatory information in the human genome. Genome Res., 22, 1748-1759.
60. Welter, D., MacArthur, J., Morales, J., Burdett, T., Hall, P., Junkins, H., Klemm, A., Flicek, P., Manolio, T., Hindorff, L. et al. (2014) The NHGRI GWAS Catalog, a curated resource of SNP-trait associations. Nucleic Acids Res., 42, D1001-D1006.
61. Buffa, L., Fuchs, E., Pietropaolo, M., Barr, F. and Solimena, M. (2008) ICA69 is a novel Rab2 effector regulating ER-Golgi trafficking in insulinoma cells. Eur. J. Cell Biol., 87, 197-209.
62. Friday, R.P., Pietropaolo, S.L., Profozich, J., Trucco, M. and Pietropaolo, M. (2003) Alternative core promoters regulate tissue-specific transcription from the autoimmune diabetes-related ICA1 (ICA69) gene locus. J. Biol. Chem., 278, 853-863.
63. Martin, S., Kardorf, J., Schulte, B., Lampeter, E.F., Gries, F.A., Melchers, I., Wagner, R., Bertrams, J., Roep, B.O. and Pfutzner, A. (1995) Autoantibodies to the islet antigen ICA69 occur in IDDM and in rheumatoid arthritis. Diabetologia, 38, 351-355.
64. Winer, S., Astsaturov, I., Cheung, R., Tsui, H., Song, A., Gaedigk, R., Winer, D., Sampson, A., McKerlie, C., Bookman, A. et al. (2002) Primary Sjogren's syndrome and deficiency of ICA69. Lancet, 360, 1063-1069.
65. Tarricone, C., Xiao, B., Justin, N., Walker, P.A., Rittinger, K., Gamblin, S.J. and Smerdon, S.J. (2001) The structural basis of Arfaptin-mediated cross-talk between Rac and Arf signalling pathways. Nature, 411, 215-219.
66. Cherfils, J. (2001) Structural mimicry of DH domains by Arfaptin suggests a model for the recognition of Rac-GDP by its guanine nucleotide exchange factors. FEBS Lett., 507, 280-284.
67. Martin, J.E., Assassi, S., Diaz-Gallo, L.M., Broen, J.C., Simeon, C.P., Castellvi, I., Vicente-Rabaneda, E., Fonollosa, V., Ortego-Centeno, N., Gonzalez-Gay, M.A. et al. (2013) A systemic sclerosis and systemic lupus erythematosus pan-meta-GWAS reveals new shared susceptibility loci. Hum. Mol. Genet., 22, 4021-4029.
68. Damgaard, C.K., Kahns, S., Lykke-Andersen, S., Nielsen, A.L., Jensen, T.H. and Kjems, J. (2008) A 5' splice site enhances the recruitment of basal transcription initiation factors in vivo. Mol. Cell, 29, 271-278.
69. Bieberstein, N.I., Carrillo Oesterreich, F., Straube, K. and Neugebauer, K.M. (2012) First exon length controls active chromatin signatures and transcription. Cell Rep., 2, 62-68.
70. Almada, A.E., Wu, X., Kriz, A.J., Burge, C.B. and Sharp, P.A. (2013) Promoter directionality is controlled by U1 snRNP and polyadenylation signals. Nature, 499, 360-363.
71. Monlong, J., Calvo, M., Ferreira, P.G. and Guigo, R. (2014) Identification of genetic variants associated with alternative splicing using sQTLseekeR. Nat. Commun., 5, 4698.
72. Samani, N.J., Erdmann, J., Hall, A.S., Hengstenberg, C., Mangino, M., Mayer, B., Dixon, R.J., Meitinger, T., Braund, P., Wichmann, H.E. et al. (2007) Genomewide association analysis of coronary artery disease.N. Engl. J. Med., 357, 443-453.
73. Wellcome Trust Case Control, C. (2007) Genome-wide association study of 14, 000 cases of seven common diseases and 3, 000 shared controls. Nature, 447, 661-678.
74. Wright, F.A., Strug, L.J., Doshi, V.K., Commander, C.W., Blackman, S.M., Sun, L., Berthiaume, Y., Cutler, D., Cojocaru, A., Collaco, J.M. et al. (2011) Genome-wide association and linkage identify modifier loci of lung disease severity in cystic fibrosis at 11p13 and 20q13.2. Nat. Genet., 43, 539-546.
75. Painter, J.N., Anderson, C.A., Nyholt, D.R., Macgregor, S., Lin, J., Lee, S.H., Lambert, A., Zhao, Z.Z., Roseman, F., Guo, Q. et al. (2011) Genome-wide association study identifies a locus at 7p15.2 associated with endometriosis. Nat. Genet., 43, 51-54.
76. Fellay, J., Shianna, K.V., Ge, D., Colombo, S., Ledergerber, B., Weale, M., Zhang, K., Gumbs, C., Castagna, A., Cossarizza, A. et al. (2007) A whole-genome association study of major determinants for host control of HIV-1. Science, 317, 944-947.
77. Verderio, P., Pizzamiglio, S., Southey, M.C., Spurdle, A.B., Hopper, J.L., Chen, X., Beesley, J. and Australian Ovarian Cancer Study Group, K.Australian Ovarian Cancer Study Group, K., Schmutzler, R.K., Engel, C. et al. (2010) A BRCA1 promoter variant (rs11655505) and breast cancer risk. J. Med. Genet., 47, 268-270.
78. Wain, L.V., Verwoert, G.C., O'Reilly, P.F., Shi, G., Johnson, T., Johnson, A.D., Bochud, M., Rice, K.M., Henneman, P., Smith, A.V. et al. (2011) Genome-wide association study identifies six new loci influencing pulse pressure and mean arterial pressure. Nat. Genet., 43, 1005-1011.
79. Wijsman, E.M., Pankratz, N.D., Choi, Y., Rothstein, J.H., Faber, K.M., Cheng, R., Lee, J.H., Bird, T.D., Bennett, D.A., Diaz-Arrastia, R. et al. (2011) Genome-wide association of familial late-onset Alzheimer's disease replicates BIN1 and CLU and nominates CUGBP2 in interaction with APOE. PLoS Genet., 7, e1001308.
80. Cusanovich, D.A., Billstrand, C., Zhou, X., Chavarria, C., De Leon, S., Michelini, K., Pai, A.A., Ober, C. and Gilad, Y. (2012) The combination of a genome-wide association study of lymphocyte count and analysis of gene expression data reveals novel asthma candidate genes. Hum. Mol. Genet., 21, 2111-2123.