Tissue-specific splicing factor gene expression signatures

Nucleic Acids Research

Volumn 36, Issue 15, 2008, Pages 4823-4832

  Grosso, Ana Rita ^a,b   Gomes, Anita Q ^a   Barbosa Morais, Nuno L ^b   Caldeira, Sandra ^a   Thorne, Natalie P ^b   Grech, Godfrey ^c   von Lindern, Marieke ^c   Carmo Fonseca, Maria ^a  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN L; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN LL; MESSENGER RNA; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN LSM2; PROTEIN LSM4; PROTEIN SF3A3; PROTEIN SNRPA; PROTEIN SNRPA 1; PROTEIN SNRPC; PROTEIN SNRPD2; PROTEIN SNRPG; PROTEIN U5 40D; PROTEIN USP39; RNA BINDING PROTEIN; RNA BINDING PROTEIN RDBP; SMALL NUCLEAR RIBONUCLEOPROTEIN; SPLICING FACTOR 3A SUBUNIT 2; SR PROTEIN KINASE 1; SR PROTEIN KINASE 2; TESTIS DETERMINING FACTOR;

ADIPOGENESIS; ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CELL CULTURE; CELL DIFFERENTIATION; CELL TYPE; CHIMPANZEE; DOWN REGULATION; ERYTHROPOIESIS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; HUMAN; HUMAN TISSUE; MALE; MICROARRAY ANALYSIS; MOUSE; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SPERMATOGENESIS; SPLICEOSOME; TESTIS; UPREGULATION;

PAN;

EID: 50849145126     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn463     Document Type: Article

References (67)

1. Black,D.L. (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem., 72, 291-336.
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. Jurica,M.S. and Moore,M.J. (2003) Pre-mRNA splicing: Awash in a sea of proteins. Mol. Cell, 12, 5-14.
4. Nilsen,T.W. (2003) The spliceosome: The most complex macromolecular machine in the cell? Bioessays, 25, 1147-1149.
5. Maniatis,T. and Tasic,B. (2002) Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature, 418, 236-243.
6. Shin,C. and Manley,J.L. (2004) Cell signalling and the control of pre-mRNA splicing. Nat. Rev. Mol. Cell Biol., 5, 727-738.
7. Jensen,K.B., Dredge,B.K., Stefani,G., Zhong,R., Buckanovich,R.J., Okano,H.J., Yang,Y.Y. and Darnell,R.B. (2000) Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability. Neuron, 25, 359-371.
8. Singh,R. and Valcarcel,J. (2005) Building specificity with nonspecific RNA-binding proteins. Nat. Struct. Mol. Biol., 12, 645-653.
9. Barbosa-Morais,N.L., Carmo-Fonseca,M. and Aparicio,S. (2006) Systematic genome-wide annotation of spliceosomal proteins reveals differential gene family expansion. Genome Res., 16, 66-77.
10. Hubbard,T.J., Aken,B.L., Beal,K., Ballester,B., Caccamo,M., Chen,Y., Clarke,L., Coates,G., Cunningham,F., Cutts,T. et al. (2007) Ensembl 2007. Nucleic Acids Res., 35, D610-617.
11. Altschul,S.F., Gish,W., Miller,W., Myers,E.W. and Lipman,D.J. (1990) Basic local alignment search tool. J. Mol. Biol., 215, 403-410.
12. Bairoch,A., Apweiler,R., Wu,C.H., Barker,W.C., Boeckmann,B., Ferro,S., Gasteiger,E., Huang,H., Lopez,R., Magrane,M. et al. (2005) The Universal Protein Resource (UniProt). Nucleic Acids Res., 33 D154-159.
13. Stajich,J.E., Block,D., Boulez,K., Brenner,S.E., Chervitz,S.A., Dagdigian,C., Fuellen,G., Gilbert,J.G., Korf,I., Lapp,H. et al. (2002) The Bioperl toolkit: Perl modules for the life sciences. Genome Res., 12, 1611-1618.
14. Stabenau,A., McVicker,G., Melsopp,C., Proctor,G., Clamp,M. and Birney,E. (2004) The Ensembl core software libraries. Genome Res., 14, 929-933.
15. Kent,W.J. (2002) BLAT - the BLAST-like alignment tool. Genome Res. 12, 656-664.
16. 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, D61-65.
17. Benson,D.A., Karsch-Mizrachi,I., Lipman,D.J., Ostell,J. and Wheeler,D.L. (2007) GenBank. Nucleic Acids Res., 35, D21-25.
18. Kuhn,R.M., Karolchik,D., Zweig,A.S., Trumbower,H., Thomas,D.J., Thakkapallayil,A., Sugnet,C.W., Stanke,M., Smith,K.E., Siepel,A. et al. (2007) The UCSC genome browser database: Update 2007. Nucleic Acids Res., 35, D668-673.
19. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
20. Gentleman,R.C., Carey,V.J., Bates,D.M., Bolstad,B., Dettling,M., Dudoit,S., Ellis,B., Gautier,L., Ge,Y., Gentry,J. et al. (2004) Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol., 5, R80.
21. Gautier,L., Cope,L., Bolstad,B.M. and Irizarry,R.A. (2004) affy - analysis of Affymetrix GeneChip data at the probe level. Bioinformatics, 20, 307-315.
22. Drissen,R., von Lindern,M., Kolbus,A., Driegen,S., Steinlein,P., Beug,H., Grosveld,F. and Philipsen,S. (2005) The erythroid phenotype of EKLF-null mice: Defects in hemoglobin metabolism and membrane stability. Mol. Cell. Biol., 25, 5205-5214.
23. Barrett,T., Suzek,T.O., Troup,D.B., Wilhite,S.E., Ngau,W.C., Ledoux,P., Rudnev,D., Lash,A.E., Fujibuchi,W. and Edgar,R. (2005) NCBI GEO: Mining millions of expression profiles - database and tools. Nucleic Acids Res., 33, D562-566.
24. Tomczak,K.K., Marinescu,V.D., Ramoni,M.F., Sanoudou,D., Montanaro,F., Han,M., Kunkel,L.M., Kohane,I.S. and Beggs,A.H. (2004) Expression profiling and identification of novel genes involved in myogenic differentiation. FASEB J., 18, 403-405.
25. Zhao,P., Caretti,G., Mitchell,S., McKeehan,W.L., Boskey,A.L., Pachman,L.M., Sartorelli,V. and Hoffman,E.P. (2006) Fgfr4 is required for effective muscle regeneration in vivo. Delineation of a MyoD-Tead2-Fgfr4 transcriptional pathway. J. Biol. Chem., 281 429-438.
26. Burton,G.R., Nagarajan,R., Peterson,C.A. and McGehee,R.E.Jr (2004) Microarray analysis of differentiation-specific gene expression during 3T3-L1 adipogenesis. Gene, 329, 167-185.
27. Akerblad,P., Månsson,R., Lagergren,A., Westerlund,S., Basta,B., Lind,U., Thelin,A., Gisler,R., Liberg,D., Nelander,S. et al. (2005) Gene expression analysis suggests that EBF-1 and PPARgamma2 induce adipogenesis of NIH-3T3 cells with similar efficiency and kinetics. Physiol. Genomics, 23, 206-216.
28. Welch,J.J., Watts,J.A., Vakoc,C.R., Yao,Y., Wang,H., Hardison,R.C., Blobel,G.A., Chodosh,L.A. and Weiss,M.J. (2004) Global regulation of erythroid gene expression by transcription factor GATA-1. Blood, 104, 3136-3147.
29. Schultz,N., Hamra,F.K. and Garbers,D.L. (2003) A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets. Proc. Natl Acad. Sci. USA, 100 12201-12206.
30. Shima,J.E., McLean,D.J., McCarrey,J.R. and Griswold,M.D. (2004) The murine testicular transcriptome: Characterizing gene expression in the testis during the progression of spermatogenesis. Biol. Reprod., 71, 319-330.
31. Hastings,K.E. and Emerson,C.P.Jr (1982) cDNA clone analysis of six co-regulated mRNAs encoding skeletal muscle contractile proteins. Proc. Natl Acad. Sci. USA, 79, 1553-1557.
32. MacLennan,D.H., Duff,C., Zorzato,F., Fujii,J., Phillips,M., Korneluk,R.G., Frodis,W., Britt,B.A. and Wortont,R.G. (1990) Ryanodine receptor gene is a candidate for predisposition to malignant hyperthermia. Nature, 343, 559-561.
33. Djian,P., Phillips,M. and Green,H. (1985) The activation of specific gene transcription in the adipose conversion of 3T3 cells. J. Cell Physiol., 124, 554-556.
34. Lahlil,R., Lecuyer,E., Herblot,S. and Hoang,T. (2004) SCL assembles a multifactorial complex that determines glycophorin A expression. Mol. Cell Biol., 24, 1439-1452.
35. Paw,B.H., Davidson,A.J., Zhou,Y., Li,R., Pratt,S.J., Lee,C., Trede,N.S., Brownlie,A., Donovan,A., Liao,E.C. et al. (2003) Cell-specific mitotic defect and dyserythropoiesis associated with erythroid band 3 deficiency. Nat. Genet., 34, 59-64.
36. Bonny,C., Cooker,L.A. and Goldberg,E. (1998) Deoxyribonucleic acid-protein interactions and expression of the human testis-specific lactate dehydrogenase promoter: Transcription factor Sp1 plays a major role. Biol. Reprod., 58, 754-759.
37. McCarrey,J.R., Kumari,M., Aivaliotis,M.J., Wang,Z., Zhang,P., Marshall,F. and Vandeberg,J.L. (1996) Analysis of the cDNA and encoded protein of the human testis-specific PGK-2 gene. Dev. Genet., 19, 321-332.
38. Benjamini,Y. and Hochberg,Y. (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. B, 57, 289-300.
39. Hastie, T.J. and Pregibon, D. (1992) Generalized linear models. In Chambers,J.M. and Hastie,T.J. (eds), Chapter 6 of Statistical Models Wadsworth & Brooks/Cole.
40. Smyth,G.K, (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol., 3, Article 3.
41. Smyth,G.K. (2005) Limma: Linear models for microarray data. In Gentleman,R., Carey,V., Dudoit,S., Irizarry,R. and Huber,W. (eds), Bioinformatics and Computational Biology Solutions using R and Bioconductor. Springer. New York. pp. 397-420.
42. Jin,W., Riley,R.M., Wolfinger,R.D., White,K.P., Passador-Gurgel,G. and Gibson,G. (2001) The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster. Nat. Genet., 29, 389-395.
43. Conboy,C.M., Spyrou,C., Thorne,N.P., Wade,E.J., Barbosa-Morais,N.L., Wilson,M.D., Bhattacharjec,A., Young,R.A., Tavare,S., Lees,J.A. et al. (2007) Cell cycle genes are the evolutionarily conserved targets of the E2F4 transcription factor. PLoS ONE, 2, e1061.
44. Kuyumcu-Martinez.N.M., Wang,G.S. and Cooper,T.A. (2007) Increased steady-state levels of CUGBP1 in myotonic dystrophy 1 are due to PKC-mcdiated hyperphosphorylation. Mol. Cell, 28, 68-78.
45. Khaitovich,P., Hellmann,I., Enard,W., Nowick,K., Leinweber.M., Franz,H.. Weiss,G., Lachmann,M. and Paabo,S. (2005) Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309, 1850-1854.
46. Zapala,M.A., Hovatta,I., Ellison,J.A., Wodicka,L., Del Rio,J.A., Tennant,R., Tynan,W., Broide,R.S., Helton,R., Stoveken,B.S. et al. (2005) Adult mouse brain gene expression patterns bear an embryologic imprint. Proc. Natl Acad. Sci. USA, 102, 10357-10362.
47. Stickeler,E., Fraser,S.D., Honig,A., Chen,A.L., Berget,S.M. and Cooper,T.A. (2001) The RNA binding protein YB-1 binds A/C-rich exon enhancers and stimulates splicing of the CD44 alternative exon v4. EMBO J., 20, 3821-3830.
48. Grimaldi,K., Horn,D.A., Hudson,L.D., Terenghi,G., Barton,R., Polak,J.M. and Latchman,D.S. (1993) Expression of the SmN splicing protein is developmentally regulated in the rodent brain but not in the rodent heart. Dev. Biol., 156, 319-323.
49. Blencowe,B.J. (2006) Alternative splicing: New insights from global analyses. Cell, 126, 37-47.
50. 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.
51. Boutz,P.L., Chawla,G., Stoilov,P. and Black,D.L. (2007) MicroRNAs regulate the expression of the alternative splicing factor nPTB during muscle development. Genes Dev., 21, 71-84.
52. Makeyev,E.V., Zhang,J., Carrasco,M.A. and Maniatis,T. (2007) The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell, 27, 435-448.
53. Yeo,G., Holste,D., Kreiman,G. and Burge,C.B. (2004) Variation in alternative splicing across human tissues. Genome Biol., 5, R74.
54. Pan,Q., Shai,O., Misquitta,C., Zhang,W., Saltzman,A.L., Mohammad,N., Babak,T., Siu,H., Hughes,T.R., Morris,Q.D. et al. (2004) Revealing global regulatory features of mammalian alternative splicing using a quantitative microarray platform. Mol. Cell, 16, 929-941.
55. Clark,T.A., Schweitzer,A,C., Chen,T.X., Staples,M.K., Lu,G., Wang,H., Williams,A. and Blume,J.E. (2007) Discovery of tissue-specific exons using comprehensive human exon microarrays. Genome Biol., 8, R64.
56. Prasad,J., Colwill,K., Pawson,T. and Manley,J.L. (1999) The protein kinase Clk/Sty directly modulates SR protein activity: Both hyper- and hypophosphorylation inhibit splicing. Mol. Cell Biol., 19, 6991-7000.
57. Prasad,J. and Manley,J.L. (2003) Regulation and substrate specificity of the SR protein kinase Clk/Sty. Mol. Cell Biol., 23, 4139-4149.
58. Xiao,S.H. and Manley,J.L. (1997) Phosphorylation of the ASF/SF2 RS domain affects both protein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev., 11, 334-344.
59. Gui,J.F., Lane,W.S. and Fu,X.D. (1994) A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature, 369, 678-682.
60. Colwill,K., Pawson,T., Andrews,B., Prasad,J., Manley,J.L., Bell,J.C. and Duncan,P.I. (1996) The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J., 15, 265-275.
61. Park,J.W., Parisky,K., Celotto,A.M., Reenan,R.A. and Graveley,B.R. (2004) Identification of alternative splicing regulators by RNA interference in Drosophila. Proc. Natl Acad. Sci. USA, 101, 15974-15979.
62. 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 3′ splice site. Mol. Cell Biol., 26, 8183-8190.
63. Pacheco,T.R., Moita,L.F., Gomes,A.Q., Hacohen,N. and Carmo-Fonseca,M. (2006) RNA interference knockdown of bU2AF35 impairs cell cycle progression and modulates alternative splicing of Cdc25 transcripts. Mol. Biol. Cell, 17, 4187-4199.
64. Massiello,A., Roesser,J.R. and Chalfant,C.E. (2006) SAP155 Binds to ceramide-responsive RNA cis-element 1 and regulates the alternative 5′ splice site selection of Bcl-x pre-mRNA. FASEB J., 20, 1680-1682.
65. Query,C.C. and Konarska,M.M. (2004) Suppression of multiple substrate mutations by spliceosomal prp8 alleles suggests functional correlations with ribosomal ambiguity mutants. Mol. Cell, 14, 343-354.
66. Gabanella,F., Carissimi,C., Usiello,A. and Pellizzoni,L. (2005) The activity of the spinal muscular atrophy protein is regulated during development-and cellular differentiation. Hum. Mol. Genet., 14 3629-3642.
67. Mollet,I., Barbosa-Morais,N.L., Andrade,J. and Carmo-Fonseca, M. (2006) Diversity of human U2AF splicing factors. FEBS J., 273, 4807-4816.