Unconstrained mining of transcript data reveals increased alternative splicing complexity in the human transcriptome

Nucleic Acids Research

Volumn 38, Issue 14, 2010, Pages 4740-4754

  Mollet, I G ^a   Ben Dov, Claudia ^b   Felício Silva, Daniel ^a   Grosso, A R ^a   Eleutério, Pedro ^a   Alves, Ruben ^a   Staller, Ray ^c   Silva, Tito Santos ^d   Carmo Fonseca, Maria ^a  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c Faculdade de Engenharia Universidade Católica Portuguesa ^*

^d CATHOLIC UNIVERSITY OF PORTUGAL   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME; ISOPROTEIN; MESSENGER RNA; UNTRANSLATED RNA;

ALGORITHM; ARTICLE; DATA MINING; EXON; GENE CONTROL; GENE EXPRESSION; GENE MAPPING; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC CONSERVATION; GENETIC DATABASE; GENETIC VARIABILITY; HUMAN; INTRON; OPEN READING FRAME; PRIORITY JOURNAL; RNA SPLICING; SEQUENCE ALIGNMENT; ALTERNATIVE RNA SPLICING; ANIMAL; CHEMISTRY; DNA BASE COMPOSITION; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; GENOMICS; METABOLISM; MOUSE; NUCLEOTIDE SEQUENCE; PROCEDURES;

CANIS FAMILIARIS; EQUIDAE; PRIMATES; RODENTIA;

ALGORITHMS; ALTERNATIVE SPLICING; ANIMALS; BASE COMPOSITION; BASE SEQUENCE; CONSERVED SEQUENCE; DATA MINING; EXONS; GENE EXPRESSION PROFILING; GENOMICS; HUMANS; INTRONS; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN ISOFORMS; RNA, MESSENGER; RNA, UNTRANSLATED; SEQUENCE ALIGNMENT;

EID: 77955793696     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq197     Document Type: Article

References (78)

1. Benson,D.A., Karsch-Mizrachi,I., Lipman,D.J., Ostell,J. and Wheeler,D.L. (2008) GenBank. Nucleic Acids Res., 36, D25-D30.
2. Matlin,A.J., Clark,F. and Smith,C.W. (2005) Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell. Biol., 6, 386-398.
3. Blencowe,B.J. (2006) Alternative splicing: new insights from global analyses. Cell, 126, 37-47.
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. Modrek,B. and Lee,C. (2002) A genomic view of alternative splicing. Nat. Genet., 30, 13-19.
6. Johnson,J.M., Castle,J., Garrett-Engele,P., Kan,Z., Loerch,P.M., Armour,C.D., Santos,R., Schadt,E.E., Stoughton,R. and Shoemaker,D.D. (2003) Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science, 302, 2141-2144.
7. Kampa,D., Cheng,J., Kapranov,P., Yamanaka,M., Brubaker,S., Cawley,S., Drenkow,J., Piccolboni,A., Bekiranov,S., Helt,G. et al. (2004) Novel RNAs identified from an in-depth analysis of the transcriptome of human chromosomes 21 and 22. Genome Res., 14, 331-342.
8. 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.
9. Sultan,M., Schulz,M.H., Richard,H., Magen,A., Klingenhoff,A., Scherf,M., Seifert,M., Borodina,T., Soldatov,A., Parkhomchuk,D. et al. (2008) A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science, 321, 956-960.
10. 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.
11. Lewis,B.P., Green,R.E. and Brenner,S.E. (2003) Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl Acad. Sci. USA, 100, 189-192.
12. Hughes,T.A. (2006) Regulation of gene expression by alternative untranslated regions. Trends Genet., 22, 119-122.
13. Lareau,L.F., Brooks,A.N., Soergel,D.A., Meng,Q. and Brenner,S.E. (2007) The coupling of alternative splicing and nonsense-mediated mRNA decay. Adv. Exp. Med. Biol., 623, 190-211.
14. Grellscheid,S.N. and Smith,C.W. (2006) An apparent pseudo-exon acts both as an alternative exon that leads to nonsense-mediated decay and as a zero-length exon. Mol. Cell. Biol., 26, 2237-2246.
15. Mollet,I., Barbosa-Morais,N.L., Andrade,J. and Carmo-Fonseca,M. (2006) Diversity of human U2AF splicing factors. FEBS J., 273, 4807-4816.
16. Kent,W.J. (2002) BLAT-the BLAST-like alignment tool. Genome Res., 12, 656-664.
17. Pruitt,K.D., Tatusova,T. and Maglott,D.R. (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res., 35, D61-D65.
18. Karolchik,D., Kuhn,R.M., Baertsch,R., Barber,G.P., Clawson,H., Diekhans,M., Giardine,B., Harte,R.A., Hinrichs,A.S., Hsu,F. et al. (2008) The UCSC Genome Browser Database: 2008 update. Nucleic Acids Res., 36, D773-D779.
19. Karolchik,D., Hinrichs,A.S., Furey,T.S., Roskin,K.M., Sugnet,C.W., Haussler,D. and Kent,W.J. (2004) The UCSC Table Browser data retrieval tool. Nucleic Acids Res., 32, D493-D496.
20. International Human Genome Sequencing Consortium. (2001) Initial sequencing and analysis of the human genome. Nature, 409, 860-921.
21. Church,D.M., Goodstadt,L., Hillier,L.W., Zody,M.C., Goldstein,S., She,X., Bult,C.J., Agarwala,R., Cherry,J.L., DiCuccio,M. et al. (2009) Lineage-specific biology revealed by a finished genome assembly of the mouse. PLoS Biol., 7, e1000112.
22. Maglott,D., Ostell,J., Pruitt,K.D. and Tatusova,T. (2007) Entrez Gene: gene-centered information at NCBI. Nucleic Acids Res., 35, D26-D31.
23. Beaudoing,E., Freier,S., Wyatt,J.R., Claverie,J.M. and Gautheret,D. (2000) Patterns of variant polyadenylation signal usage in human genes. Genome Res., 10, 1001-1010.
24. Yamashita,R., Wakaguri,H., Sugano,S., Suzuki,Y. and Nakai,K. (2010) DBTSS provides a tissue specific dynamic view of Transcription Start Sites. Nucleic Acids Res., 38, D98-D104.
25. Kapranov,P., Cheng,J., Dike,S., Nix,D.A., Duttagupta,R., Willingham,A.T., Stadler,P.F., Hertel,J., Hackermuller,J., Hofacker,I.L. et al. (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science, 316, 1484-1488.
26. Jurka,J., Kapitonov,V.V., Pavlicek,A., Klonowski,P., Kohany,O. and Walichiewicz,J. (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res., 110, 462-467.
27. Zhang,Z., Scott Schwartz,S., Wagner,L. and Webb Miller,W. (2000) A greedy algorithm for aligning DNA sequences. J. Comput. Biol., 7, 203-214.
28. Gazave,E., Marqués-Bonet,T., Fernando,O., Charlesworth,B. and Navarro,A. (2007) Patterns and rates of intron divergence between humans and chimpanzees. Genome Biol., 8, R21.
29. Griffiths-Jones,S., Grocock,R.J., van Dongen,S., Bateman,A. and Enright,A.J. (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res., 334, D140-D144.
30. Lestrade,L. and Weber,M.J. (2006) snoRNA-LBME-db, a comprehensive database of human H/ACA and C/D box snoRNAs. Nucleic Acids Res., 34, D158-D162.
31. Ma,B., Tromp,J. and Li,M. (2002) PatternHunter: faster and more sensitive homology search. Bioinformatics, 18, 440-445.
32. de la Grange,P., Dutertre,M., Correa,M. and Auboeuf,D. (2007) A new advance in alternative splicing databases: from catalogue to detailed analysis of regulation of expression and function of human alternative splicing variants. BMC Bioinformatics, 8, 180.
33. Kim,N., Alekseyenko,A.V., Roy,M. and Lee,C. (2007) The ASAP II database: analysis and comparative genomics of alternative splicing in 15 animal species. Nucleic Acids Res., 35, D93-D98.
34. Birney,E., Andrews,D., Caccamo,M., Chen,Y., Clarke,L., Coates,G., Cox,T., Cunningham,F., Curwen,V., Cutts,T. et al. (2006) Ensembl 2006. Nucleic Acids Res., 34, D556-D561.
35. Kim,E., Magen,A. and Ast,G. (2007) Different levels of alternative splicing among eukaryotes. Nucleic Acids Res., 35, 125-131.
36. Lev-Maor,G., Ram,O., Kim,E., Sela,N., Goren,A., Levanon,E.Y. and Ast,G. (2008) Intronic Alus influence alternative splicing. PLoS Genet., 4, e1000204.
37. Ram,O., Schwartz,S. and Ast,G. (2008) Multifactorial interplay controls the splicing profile of Alu-derived exons. Mol. Cell. Biol., 28, 3513-3525.
38. El-Sawy,M. and Deininger,P. (2005) Tandem insertions of alu elements. Cytogenet. Genome Res., 108, 58-62.
39. Crooks,G.E., Hon,G., Chandonia,J.M. and Brenner,S.E. (2004) WebLogo: a sequence logo generator. Genome Res., 14, 1188-1190.
40. Pacheco,T.R., Coelho,M.B., Desterro,J.M., Mollet,I. and Carmo-Fonseca,M. (2006) In vivo requirement of the small subunit of U2AF for recognition of a weak 30 splice site. Mol. Cell. Biol., 26, 8183-8190.
41. The Chimpanzee Sequencing and Analysis Consortium. (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature, 437, 69-87.
42. Rhesus Macaque Genome Sequencing and Analysis Consortium. (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science, 316, 222-234.
43. Xing,Y. and Lee,C. (2006) Alternative splicing and RNA selection pressure-evolutionary consequences for eukaryotic genomes. Nat. Rev. Genet., 7, 499-509.
44. Brett,D., Pospisil,H., Valcarcel,J., Reich,J. and Bork,P. (2002) Alternative splicing and genome complexity. Nat. Genet., 30, 29-30.
45. Harrington,E.D., Boue,S., Valcarcel,J., Reich,J.G. and Bork,P. (2004) Estimating rates of alternative splicing in mammals and invertebrates. Nat. Genet., 36, 916-917, author reply.
46. Kim,H., Klein,R., Majewski,J. and Ott,J. (2004) Estimating rates of alternative splicing in mammals and invertebrates. Nature Genet., 36, 915-916.
47. Takeda,J., Suzuki,Y., Sakate,R., Sato,Y., Seki,M., Irie,T., Takeuchi,N., Ueda,T., Nakao,M., Sugano,S. et al. (2008) Low conservation and species-specific evolution of alternative splicing in humans and mice: comparative genomics analysis using well-annotated full-length cDNAs. Nucleic Acids Res., 36, 6386-6395.
48. Bainbridge,M.N., Warren,R.L., Hirst,M., Romanuik,T., Zeng,T., Go,A., Delaney,A., Griffith,M., Hickenbotham,M., Magrini,V. et al. (2006) Analysis of the prostate cancer cell line LNCaP transcriptome using a sequencing-by-synthesis approach. BMC Genomics, 7, 246.
49. 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.
50. Cloonan,N., Forrest,A.R., Kolle,G., Gardiner,B.B., Faulkner,G.J., Brown,M.K., Taylor,D.F., Steptoe,A.L., Wani,S., Bethel,G. et al. (2008) Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat. Methods, 5, 613-619.
51. Carninci,P., Sandelin,A., Lenhard,B., Katayama,S., Shimokawa,K., Ponjavic,J., Semple,C.A., Taylor,M.S., Engström,P.G., Frith,M.C. et al. (2006) Genome-wide analysis of mammalian promoter architecture and evolution. Nat. Genet., 38, 626-635.
52. Sandelin,A., Carninci,P., Lenhard,B., Ponjavic,J., Hayashizaki,Y. and Hume,D.A. (2007) Mammalian RNA polymerase II core promoters: insights from genome-wide studies. Nat. Rev. Genet., 8, 424-436.
53. Listerman,I., Bledau,A.S., Grishina,I. and Neugebauer,K.M. (2007) Extragenic accumulation of RNA polymerase II enhances transcription by RNA polymerase III. PLoS Genet., 3, e212.
54. Smith,A.D., Sumazin,P., Das,D. and Zhang,M.Q. (2005) Mining ChIP-chip data for transcription factor and cofactor binding sites. Bioinformatics., 21(Suppl 1), i403-i412.
55. Ji,H., Jiang,H., Ma,W., Johnson,D.S., Myers,R.M. and Wong,W.H. (2008) An integrated software system for analyzing ChIP-chip and ChIP-seq data. Nat. Biotechnol., 26, 1293-1300.
56. Forrest,S.T., Barringhaus,K.G., Perlegas,D., Hammarskjold,M.L. and McNamara,C.A. (2004) Intron retention generates a novel Id3 isoform that inhibits vascular lesion formation. J. Biol. Chem., 279, 32897-32903.
57. Lejeune,F., Cavaloc,Y. and Stevenin,J. (2001) Alternative splicing of intron 3 of the serine/arginine-rich protein 9G8 gene. Identification of flanking exonic splicing enhancers and involvement of 9G8 as a trans-acting factor. J. Biol. Chem., 276, 7850-7858.
58. Mansilla,A., López-Sánchez,C., de la Rosa,E.J., García-Martínez,V., Martínez-Salas,E., de Pablo,F. and Hernández-Sánchez,C. (2005) Developmental regulation of a proinsulin messenger RNA generated by intron retention. EMBO Rep., 6, 1182-1187.
59. Zhong,X., Liu,J.R., Kyle,J.W., Hanck,D.A. and Agnew,W.S. (2006) A profile of alternative RNA splicing and transcript variation of CACNA1H, a human T-channel gene candidate for idiopathic generalized epilepsies. Hum. Mol. Genet., 15, 1497-1512.
60. Bell,T.J., Miyashiro,K.Y., Sul,J.Y., McCullough,R., Buckley,P.T., Jochems,J., Meaney,D.F., Haydon,P., Cantor,C., Parsons,T.D. et al. (2008) Cytoplasmic BK(Ca) channel intron-containing mRNAs contribute to the intrinsic excitability of hippocampal neurons. Proc. Natl Acad. Sci. USA, 105, 1901-1906.
61. Chen,Z., Gore,B.B., Long,H., Ma,L. and Tessier-Lavigne,M. (2008) Alternative splicing of the Robo3 axon guidance receptor governs the midline switch from attraction to repulsion. Neuron, 58, 325-332.
62. Kan,Z., States,D. and Gish,W. (2002) Selecting for functional alternative splices in ESTs. Genome Res., 12, 1837-1845.
63. Carninci,P., Kasukawa,T., Katayama,S., Gough,J., Frith,M.C., Maeda,N., Oyama,R., Ravasi,T., Lenhard,B., Wells,C. et al. (2005) The transcriptional landscape of the mammalian genome. Science, 309, 1559-1563.
64. Galante,P.A., Sakabe,N.J., Kirschbaum-Slager,N. and de Souza,S.J. (2004) Detection and evaluation of intron retention events in the human transcriptome. RNA, 10, 757-765.
65. Cullen,B.R. (2003) Nuclear mRNA export: insights from virology. Trends. Biochem. Sci., 28, 419-424.
66. Li,Y., Bor,Y.C., Misawa,Y., Xue,Y., Rekosh,D. and Hammarskjöld,M.L. (2006) An intron with a constitutive transport element is retained in a Tap messenger RNA. Nature, 443, 234-237.
67. Bor,Y.C., Swartz,J., Morrison,A., Rekosh,D., Ladomery,M. and Hammarskjöld,M.L. (2006) The Wilms' tumor 1 (WT1) gene (+KTS isoform) functions with a CTE to enhance translation from an unspliced RNA with a retained intron. Genes Dev., 20, 1597-1608.
68. Wang,Z., Xiao,X., Van Nostrand,E. and Burge,C.B. (2006) General and specific functions of exonic splicing silencers in splicing control. Mol. Cell., 23, 61-70.
69. Marcucci,R., Baralle,F.E. and Romano,M. (2007) Complex splicing control of the human Thrombopoietin gene by intronic G runs. Nucleic Acids Res., 35, 132-142.
70. Schwartz,S.H., Silva,J., Burstein,D., Pupko,T., Eyras,E. and Ast,G. (2008) Large-scale comparative analysis of splicing signals and their corresponding splicing factors in eukaryotes. Genome Res., 18, 88-103.
71. Ner-Gaon,H., Leviatan,N., Rubin,E. and Fluhr,R. (2007) Comparative cross-species alternative splicing in plants. Plant Physiol., 144, 1632-1641.
72. Iida,K., Seki,M., Sakurai,T., Satou,M., Akiyama,K., Toyoda,T., Konagaya,A. and Shinozaki,K. (2004) Genome-wide analysis of alternative pre-mRNA splicing in Arabidopsis thaliana based on full-length cDNA sequences. Nucleic Acids Res., 32, 5096-5103.
73. Ner-Gaon,H., Halachmi,R., Savaldi-Goldstein,S., Rubin,E., Ophir,R. and Fluhr,R. (2004) Intron retention is a major phenomenon in alternative splicing in Arabidopsis. Plant J., 39, 877-885.
74. Wang,B.B. and Brendel,V. (2006) Genomewide comparative analysis of alternative splicing in plants. Proc. Natl Acad. Sci. USA., 103, 7175-7180.
75. Murphy,W.J., Eizirik,E., Johnson,W.E., Zhang,Y.P., Ryder,O.A. and O'Brien,S.J. (2001) Molecular phylogenetics and the origins of placental mammals. Nature, 409, 614-618.
76. Cannarozzi,G., Schneider,A. and Gonnet,G. (2007) A phylogenomic study of human, dog, and mouse. PLoS Comput. Biol., 3, e2.
77. Hiller,M., Findeiss,S., Lein,S., Marz,M., Nickel,C., Rose,D., Schulz,C., Backofen,R., Prohaska,S.J., Reuter,G. et al. (2009) Conserved introns reveal novel transcripts in Drosophila melanogaster. Genome Res., 19, 1289-1300.
78. Shovlin,C.L., Angus,G., Manning,R.A., Okoli,G.N., Govani,F.S., Elderfield,K., Birdsey,G.M., Laffan,M.A., Mollet,I.G. and Mauri,F.A. (2010) Endothelial cell processing and alternatively spliced transcripts of Factor VIII. Potential implications for coagulation cascades and pulmonary hypertension. PLoS ONE, 5, e9154.