Unusual intron conservation near tissue-regulated exons found by splicing microarrays

PLoS Computational Biology

Volumn 2, Issue 1, 2006, Pages

  Sugnet, Charles W ^a   Srinivasan, Karpagam ^b   Clark, Tyson A ^c   O'Brien, Georgeann ^b   Cline, Melissa S ^c,d   Wang, Hui ^c   Williams, Alan ^c   Kulp, David ^c,e   Blume, John E ^c   Haussler, David ^a   Ares, Manuel ^b  

^a University of California Santa Cruz   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Thermo Fisher Scientific   (United States)

^d INSTITUT PASTEUR   (France)

^e Biologically Inspired Neural and Dynamical Systems Laboratory   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; HISTOLOGY; MAMMALS; OLIGONUCLEOTIDES; PROTEINS;

ALTERNATIVE SPLICING; GENE-REGULATION; MOUSE GENOME; OLIGONUCLEOTIDE MICROARRAY; PROTEIN-CODING; REGULATORY PATTERNS; SEQUENCE CONSERVATION; SPLICE JUNCTIONS; STATISTICAL COMPARISONS; SYSTEMS APPROACH;

MUSCLE;

GUANYLATE KINASE; ISOPROTEIN; MEMBRANE PROTEIN; NEUROPEPTIDE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONSENSUS; CONTROLLED STUDY; DOWNSTREAM PROCESSING; EXON; FEMALE; GENE SEQUENCE; GENOME; INTRON; MALE; MAMMAL; MICROARRAY ANALYSIS; MOLECULAR EVOLUTION; MOUSE; MULTIGENE FAMILY; MUSCLE TISSUE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PROTEIN EXPRESSION; PROTEIN MOTIF; RNA SPLICING; VERTEBRATE; ALTERNATIVE RNA SPLICING; ANIMAL; ANTIBODY SPECIFICITY; BRAIN; CLASSIFICATION; DNA MICROARRAY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUSCLE; SEQUENCE ALIGNMENT;

ANIMALIA; MAMMALIA; VERTEBRATA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; BRAIN; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; EXONS; HUMANS; INTRONS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUSCLES; NEUROPEPTIDES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; PROTEIN ISOFORMS; SEQUENCE ALIGNMENT;

EID: 33645760966     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.0020004     Document Type: Article

References (86)

1. Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72: 291-336.
2. Lejeune F, Maquat LE (2005) Mechanistic links between nonsense-mediated mRNA decay and pre-mRNA splicing in mammalian cells. Curr Opin Cell Biol 17: 309-315.
3. Lewis BP, Green RE, Brenner SE (2003) Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc Natl Acad Sci U S A 100: 189-192.
4. Green RE, Lewis BP, Hillman RT, Blanchette M, Lareau LF, et al. (2003) Widespread predicted nonsense-mediated mRNA decay of alternativelyspliced transcripts of human normal and disease genes. Bioinformatics 19 (Suppl 1): i118-i121.
5. Morrison M, Harris KS, Roth MB (1997) smg mutants affect the expression of alternatively spliced SR protein mRNAs in Caenorhabditis elegans. Proc Natl Acad Sci U S A 94: 9782-9785.
6. Black DL, Grabowski PJ (2003) Alternative pre-mRNA splicing and neuronal function. Prog Mol Subcell Biol 31: 187-216.
7. Grabowski PJ, Black DL (2001) Alternative RNA splicing in the nervous system. Prog Neurobiol 65: 289-308.
8. Kopelman NM, Lancet D, Yanai I (2005) Alternative splicing and gene duplication are inversely correlated evolutionary mechanisms. Nat Genet 37: 588-589.
9. Smith CW, Valcarcel J (2000) Alternative pre-mRNA splicing: The logic of combinatorial control. Trends Biochem Sci 25: 381-388.
10. Dredge BK, Stefani G, Engelhard CC, Darnell RB (2005) Nova autoregulation reveals dual functions in neuronal splicing. EMBO J 24: 1608-1620.
11. Han J, Cooper TA (2005) Identification of CELF splicing activation and repression domains in vivo. Nucleic Acids Res 33: 2769-2780.
12. Ladd AN, Cooper TA (2002) Finding signals that regulate alternative splicing in the post-genomic era. Genome Biol 3: reviews0008.
13. Underwood JG, Boutz PL, Dougherty JD, Stoilov P, Black DL (2005) Homologues of the Caenorhabditis elegans Fox-1 protein are neuronal splicing regulators in mammals. Mol Cell Biol 25: 10005-10016.
14. Nakahata S, Kawamoto S (2005) Tissue-dependent isoforms of mammalian Fox-1 homologs are associated with tissue-specific splicing activities. Nucleic Acids Res 33: 2078-2089.
15. Ryder SP, Williamson JR (2004) Specificity of the STAR/GSG domain protein Qk1: Implications for the regulation of myelination. RNA 10: 1449-1458.
16. Ryder SP, Frater LA, Abramovitz DL, Goodwin EB, Williamson JR (2004) RNA target specificity of the STAR/GSG domain post-transcriptional regulatory protein GLD-1. Nat Struct Mol Biol 11: 20-28.
17. Liu Z, Luyten I, Bottomley MJ, Messias AC, Houngninou-Molango S, et al. (2001) Structural basis for recognition of the intron branch site RNA by splicing factor 1. Science 294: 1098-1102.
18. Wu JI, Reed RB, Grabowski PJ, Artzt K (2002) Function of quaking in myelination: Regulation of alternative splicing. Proc Natl Acad Sci U S A 99: 4233-4238.
19. Wu J, Zhou L, Tonissen K, Tee R, Artzt K (1999) The quaking I-5 protein (QKI-5) has a novel nuclear localization signal and shuttles between the nucleus and the cytoplasm. J Biol Chem 274: 29202-29210.
20. Kondo T, Furuta T, Mitsunaga K, Ebersole TA, Shichiri M, et al. (1999) Genomic organization and expression analysis of the mouse qkI locus. Mamm Genome 10: 662-669.
21. Karolchik D, Baertsch R, Diekhans M, Furey TS, Hinrichs A, et al. (2003) The UCSC Genome Browser Database. Nucleic Acids Res 31: 51-54.
22. Thanaraj TA, Clark F, Muilu J (2003) Conservation of human alternative splice events in mouse. Nucleic Acids Res 31: 2544-2552.
23. Brudno M, Gelfand MS, Spengler S, Zorn M, Dubchak I, et al. (2001) Computational analysis of candidate intron regulatory elements for tissue-specific alternative pre-mRNA splicing. Nucleic Acids Res 29: 2338-2348.
24. Sugnet CW, Kent WJ, Ares M Jr, Haussler D (2004) Transcriptome and genome conservation of alternative splicing events in humans and mice. Pac Symp Biocomput 66-77.
25. Sorek R, Ast G (2003) Intronic sequences flanking alternatively spliced exons are conserved between human and mouse. Genome Res 13: 1631-1637.
26. Yeo GW, Van Nostrand E, Holste D, Poggio T, Burge CB (2005) Identification and analysis of alternative splicing events conserved in human and mouse. Proc Natl Acad Sci U S A 102: 2850-2855.
27. Modrek B, Lee CJ (2003) Alternative splicing in the human, mouse and rat genomes is associated with an increased frequency of exon creation and/or loss. Nat Genet 34: 177-180.
28. Modrek B, Resch A, Grasso C, Lee C (2001) Genome-wide detection of alternative splicing in expressed sequences of human genes. Nucleic Acids Res 29: 2850-2859.
29. Sorek R, Shemesh R, Cohen Y, Basechess O, Ast G, et al. (2004) A non-ESTbased method for exon-skipping prediction. Genome Res 14: 1617-1623.
30. Dror G, Sorek R, Shamir R (2004) Accurate identification of alternatively spliced exons using support vector machine. Bioinformatics 21: 897-901.
31. Clark TA, Sugnet CW, Ares M Jr (2002) Genomewide analysis of mRNA processing in yeast using splicing-specific microarrays. Science 296: 907-910.
32. Johnson JM, Castle J, Garrett-Engele P, Kan Z, Loerch PM, et al. (2003) Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302: 2141-2144.
33. Relogio A, Ben-Dov C, Baum M, Ruggiu M, Gemund C, et al. (2005) Alternative splicing microarrays reveal functional expression of neuron-specific regulators in Hodgkin lymphoma cells. J Biol Chem 280: 4779-4784.
34. Castle J, Garrett-Engele P, Armour CD, Duenwald SJ, Loerch PM, et al. (2003) Optimization of oligonucleotide arrays and RNA amplification protocols for analysis of transcript structure and alternative splicing. Genome Biol 4: R66.
35. Wang H, Hubbell E, Hu JS, Mei G, Cline M, et al. (2003) Gene structure-based splice variant deconvolution using a microarray platform. Bioinformatics 19 (Suppl 1): i315-i322.
36. Yeakley JM, Fan JB, Doucet D, Luo L, Wickham E, et al. (2002) Profiling alternative splicing on fiber-optic arrays. Nat Biotechnol 20: 353-358.
37. Le K, Mitsouras K, Roy M, Wang Q, Xu Q, et al. (2004) Detecting tissue-specific regulation of alternative splicing as a qualitative change in microarray data. Nucleic Acids Res 32: e180.
38. Pan Q, Shai O, Misquitta C, Zhang W, Saltzman AL, et al. (2004) Revealing global regulatory features of mammalian alternative splicing using a quantitative microarray platform. Mol Cell 16: 929-941.
39. Burckin T, Nagel R, Mandel-Gutfreund Y, Shiue L, Clark TA, et al. (2005) Exploring functional relationships between components of the gene expression machinery. Nat Struct Mol Biol 12: 175-182.
40. Fehlbaum P, Guihal C, Bracco L, Cochet O (2005) A microarray con.guration to quantify expression levels and relative abundance of splice variants. Nucleic Acids Res 33: e47.
41. Blanchette M, Green RE, Brenner SE, Rio DC (2005) Global analysis of positive and negative pre-mRNA splicing regulators in Drosophila. Genes Dev 19: 1306-1314.
42. Liu WM, Mei R, Di X, Ryder TB, Hubbell E, et al. (2002) Analysis of high density expression microarrays with signed-rank call algorithms. Bioinformatics 18: 1593-1599.
43. Fodor SP, Read JL, Pirrung MC, Stryer L, Lu AT, et al. (1991) Light-directed, spatially addressable parallel chemical synthesis. Science 251: 767-773.
44. Pease AC, Solas D, Sullivan EJ, Cronin MT, Holmes CP, et al. (1994) Light-generated oligonucleotide arrays for rapid DNA sequence analysis. Proc Natl Acad Sci U S A 91: 5022-5026.
45. Rahman L, Bliskovski V, Kaye FJ, Zajac-Kaye M (2004) Evolutionary conservation of a 2-kb intronic sequence flanking a tissue-specific alternative exon in the PTBP2 gene. Genomics 83: 76-84.
46. Mistry N, Harrington W, Lasda E, Wagner EJ, Garcia-Blanco MA (2003) Of urchins and men: Evolution of an alternative splicing unit in fibroblast growth factor receptor genes. RNA 9: 209-217.
47. Wagner EJ, Baraniak AP, Sessions OM, Mauger D, Moskowitz E, et al. (2005) Characterization of the intronic splicing silencers flanking FGFR2 exon IIIb. J Biol Chem 280: 14017-14027.
48. Siepel A, Haussler D (2004) Combining phylogenetic and hidden Markov models in biosequence analysis. J Comput Biol 11: 413-428.
49. Siepel A, Haussler D (2004) Phylogenetic estimation of context-dependent substitution rates by maximum likelihood. Mol Biol Evol 21: 468-488.
50. Rivas E, Eddy SR (2001) Noncoding RNA gene detection using comparative sequence analysis. BMC Bioinformatics 2: 8.
51. Chou MY, Underwood JG, Nikolic J, Luu MH, Black DL (2000) Multisite RNA binding and release of polypyrimidine tract binding protein during the regulation of c-src neural-specific splicing. Mol Cell 5: 949-957.
52. Markovtsov V, Nikolic JM, Goldman JA, Turck CW, Chou MY, et al. (2000) Cooperative assembly of an hnRNP complex induced by a tissue-specific homolog of polypyrimidine tract binding protein. Mol Cell Biol 20: 7463-7479.
53. Jin Y, Suzuki H, Maegawa S, Endo H, Sugano S, et al. (2003) A vertebrate RNA-binding protein Fox-1 regulates tissue-specific splicing via the pentanucleotide GCAUG. EMBO J 22: 905-912.
54. Buckanovich RJ, Darnell RB (1997) The neuronal RNA binding protein Nova-1 recognizes specific RNA targets in vitro and in vivo. Mol Cell Biol 17: 3194-3201.
55. Burd CG, Dreyfuss G (1994) RNA binding specificity of hnRNP A1: Significance of hnRNP A1 high-affinity binding sites in pre-mRNA splicing. EMBO J 13: 1197-1204.
56. Dredge BK, Darnell RB (2003) Nova regulates GABA(A) receptor gamma2 alternative splicing via a distal downstream UCAU-rich intronic splicing enhancer. Mol Cell Biol 23: 4687-4700.
57. Kumar DV, Nighorn A, St John PA (2002) Role of Nova-1 in regulating alpha2N, a novel glycine receptor splice variant, in developing spinal cord neurons. J Neurobiol 52: 156-165.
58. Jensen KB, Dredge BK, Stefani G, Zhong R, Buckanovich RJ, et al. (2000) Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability. Neuron 25: 359-371.
59. Minovitsky S, Gee SL, Schokrpur S, Dubchak I, Conboy JG (2005) The splicing regulatory element, UGCAUG, is phylogenetically and spatially conserved in introns that flank tissue-specific alternative exons. Nucleic Acids Res 33: 714-724.
60. Lim LP, Sharp PA (1998) Alternative splicing of the fibronectin EIIIB exon depends on specific TGCATG repeats. Mol Cell Biol 18: 3900-3906.
61. Hedjran F, Yeakley JM, Huh GS, Hynes RO, Rosenfeld MG (1997) Control of alternative pre-mRNA splicing by distributed pentameric repeats. Proc Natl Acad Sci U S A 94: 12343-12347.
62. Huh GS, Hynes RO (1994) Regulation of alternative pre-mRNA splicing by a novel repeated hexanucleotide element. Genes Dev 8: 1561-1574.
63. Ao W, Gaudet J, Kent WJ, Muttumu S, Mango SE (2004) Environmentally induced foregut remodeling by PHA-4/FoxA and DAF-12/NHR. Science 305: 1743-1746.
64. Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
65. Grundy WN, Bailey TL, Elkan CP (1996) ParaMEME: A parallel implementation and a web interface for a DNA and protein motif discovery tool. Comput Appl Biosci 12: 303-310.
66. Montgomery JM, Zamorano PL, Garner CC (2004) MAGUKs in synapse assembly and function: An emerging view. Cell Mol Life Sci 61: 911-929.
67. Ponting CP, Phillips C, Davies KE, Blake DJ (1997) PDZ domains: targeting signalling molecules to sub-membranous sites. Bioessays 19: 469-479.
68. Cline MS, Blume J, Cawley S, Clark TA, Hu JS, et al. (2005) ANOSVA: A statistical method for detecting splice variation from expression data. Bioinformatics 21 (Suppl 1): i107-i115.
69. Black DL (1998) Splicing in the inner ear: A familiar tune, but what are the instruments? Neuron 20: 165-168.
70. Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, et al. (2003) CLIP identifies Nova-regulated RNA networks in the brain. Science 302: 1212-1215.
71. Modafferi EF, Black DL (1997) A complex intronic splicing enhancer from the c-src pre-mRNA activates inclusion of a heterologous exon. Mol Cell Biol 17: 6537-6545.
72. Deguillien M, Huang SC, Moriniere M, Dreumont N, Benz EJ Jr, et al. (2001) Multiple cis elements regulate an alternative splicing event at 4.1R premRNA during erythroid differentiation. Blood 98: 3809-3816.
73. Kramer A (1992) Purification of splicing factor SF1, a heat-stable protein that functions in the assembly of a presplicing complex. Mol Cell Biol 12: 4545-4552.
74. Peled-Zehavi H, Berglund JA, Rosbash M, Frankel AD (2001) Recognition of RNA branch point sequences by the KH domain of splicing factor 1 (mammalian branch point binding protein) in a splicing factor complex. Mol Cell Biol 21: 5232-5241.
75. Tanackovic G, Kramer A (2005) Human splicing factor SF3a, but not SF1, is essential for pre-mRNA splicing in vivo. Mol Biol Cell 16: 1366-1377.
76. Guth S, Valcarcel J (2000) Kinetic role for mammalian SF1/BBP in spliceosome assembly and function after polypyrimidine tract recognition by U2AF. J Biol Chem 275: 38059-38066.
77. Maguire ML, Guler-Gane G, Nietlispach D, Raine AR, Zorn AM, et al. (2005) Solution structure and backbone dynamics of the KH-QUA2 region of the Xenopus STAR/GSG quaking protein. J Mol Biol 348: 265-279.
78. Pilotte J, Larocque D, Richard S (2001) Nuclear translocation controlled by alternatively spliced isoforms inactivates the QUAKING apoptotic inducer. Genes Dev 15: 845-858.
79. Kent WJ (2002) BLAT - The BLAST-like alignment tool. Genome Res 12: 656-664.
80. Wheeler R (2002) A method of consolidating and combining EST and mRNA alignments to a genome to enumerate supported splice variants. In: Guigo R, Gusfield D, editors. Algorithms in Bioinformatics: Second International Workshop, WABI 2002, Rome, Italy, September 17-21, 2002, Proceedings. Berlin/New York: Springer. pp. 201-209.
81. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
82. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, et al. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15.
83. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
84. Fisher RA (1970) Statistical Methods for Research Workers. Darien (Colorado): Hafner Press. 362 p.
85. Wilcox RR (2003) Applying Contemporary Statistical Techniques. Amsterdam/ Boston: Academic Press.
86. R Development Core Team (2005) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available: http://www.r-project.org. Accessed: 21 December 2005.