Genome-wide Analysis Reveals SR Protein Cooperation and Competition in Regulated Splicing

Molecular Cell

Volumn 50, Issue 2, 2013, Pages 223-235

  Pandit, Shatakshi ^a   Zhou, Yu ^a   Shiue, Lily ^b   Coutinho Mansfield, Gabriela ^a   Li, Hairi ^a   Qiu, Jinsong ^a   Huang, Jie ^c   Yeo, Gene W ^a   Ares, Manuel ^b   Fu, Xiang Dong ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

RNA BINDING PROTEIN; SERINE ARGININE RICH PROTEIN; TRANSCRIPTOME;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; BINDING SITE; BIOGENESIS; CROSS LINKING; EMBRYO; EXON; EXON SKIPPING; FIBROBLAST; GENOME; GENOME ANALYSIS; IMMUNOPRECIPITATION; INTRON; MAMMAL CELL; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; RNA BINDING;

ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; BINDING SITES; CELLS, CULTURED; CONSENSUS SEQUENCE; EXONS; FIBROBLASTS; GENE KNOCKOUT TECHNIQUES; GENOME; INTRONS; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS; PROTEIN BINDING; RIBONUCLEOPROTEINS; RNA SPLICING; RNA-BINDING PROTEINS; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

MAMMALIA;

EID: 84876839218     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.03.001     Document Type: Article

References (55)

1. Ankö M.L., Morales L., Henry I., Beyer A., Neugebauer K.M. Global analysis reveals SRp20- and SRp75-specific mRNPs in cycling and neural cells. Nat. Struct. Mol. Biol. 2010, 17:962-970.
2. Änkö M.L., Müller-McNicoll M., Brandl H., Curk T., Gorup C., Henry I., Ule J., Neugebauer K.M. The RNA-binding landscapes of two SR proteins reveal unique functions and binding to diverse RNA classes. Genome Biol. 2012, 13:R17.
3. Bailey T.L., Boden M., Buske F.A., Frith M., Grant C.E., Clementi L., Ren J., Li W.W., Noble W.S. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009, 37(Web Server issue):W202-W208.
4. Buratti E., Stuani C., De Prato G., Baralle F.E. SR protein-mediated inhibition of CFTR exon 9 inclusion: molecular characterization of the intronic splicing silencer. Nucleic Acids Res. 2007, 35:4359-4368.
5. Cáceres J.F., Screaton G.R., Krainer A.R. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev. 1998, 12:55-66.
6. Cartegni L., Wang J., Zhu Z., Zhang M.Q., Krainer A.R. ESEfinder: A web resource to identify exonic splicing enhancers. Nucleic Acids Res. 2003, 31:3568-3571.
7. Cavaloc Y., Bourgeois C.F., Kister L., Stévenin J. The splicing factors 9G8 and SRp20 transactivate splicing through different and specific enhancers. RNA 1999, 5:468-483.
8. Daubner G.M., Cléry A., Jayne S., Stevenin J., Allain F.H. A syn-anti conformational difference allows SRSF2 to recognize guanines and cytosines equally well. EMBO J. 2012, 31:162-174.
9. Du H., Cline M.S., Osborne R.J., Tuttle D.L., Clark T.A., Donohue J.P., Hall M.P., Shiue L., Swanson M.S., Thornton C.A., Ares M. Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy. Nat. Struct. Mol. Biol. 2010, 17:187-193.
10. Erkelenz S., Mueller W.F., Evans M.S., Busch A., Schöneweis K., Hertel K.J., Schaal H. Position-dependent splicing activation and repression by SR and hnRNP proteins rely on common mechanisms. RNA 2013, 19:96-102. Published online November 21, 2012. 10.1261/rna.037044.112.
11. Fairbrother W.G., Yeh R.F., Sharp P.A., Burge C.B. Predictive identification of exonic splicing enhancers in human genes. Science 2002, 297:1007-1013.
12. Fox-Walsh K.L., Dou Y., Lam B.J., Hung S.P., Baldi P.F., Hertel K.J. The architecture of pre-mRNAs affects mechanisms of splice-site pairing. Proc. Natl. Acad. Sci. USA 2005, 102:16176-16181.
13. Gabut M., Dejardin J., Tazi J., Soret J. The SR family proteins B52 and dASF/SF2 modulate development of the Drosophila visual system by regulating specific RNA targets. Mol. Cell. Biol. 2007, 27:3087-3097.
14. Gallego M.E., Gattoni R., Stévenin J., Marie J., Expert-Bezançon A. The SR splicing factors ASF/SF2 and SC35 have antagonistic effects on intronic enhancer-dependent splicing of the beta-tropomyosin alternative exon 6A. EMBO J. 1997, 16:1772-1784.
15. Ghigna C., Giordano S., Shen H., Benvenuto F., Castiglioni F., Comoglio P.M., Green M.R., Riva S., Biamonti G. Cell motility is controlled by SF2/ASF through alternative splicing of the Ron protooncogene. Mol. Cell 2005, 20:881-890.
16. Graveley B.R., Maniatis T. Arginine/serine-rich domains of SR proteins can function as activators of pre-mRNA splicing. Mol. Cell 1998, 1:765-771.
17. Han J., Ding J.H., Byeon C.W., Kim J.H., Hertel K.J., Jeong S., Fu X.D. SR proteins induce alternative exon skipping through their activities on the flanking constitutive exons. Mol. Cell. Biol. 2011, 31:793-802.
18. Han J., Xiong J., Wang D., Fu X.D. Pre-mRNA splicing: where and when in the nucleus. Trends Cell Biol. 2011, 21:336-343.
19. Havlioglu N., Wang J., Fushimi K., Vibranovski M.D., Kan Z., Gish W., Fedorov A., Long M., Wu J.Y. An intronic signal for alternative splicing in the human genome. PLoS ONE 2007, 2:e1246.
20. Heinz S., Benner C., Spann N., Bertolino E., Lin Y.C., Laslo P., Cheng J.X., Murre C., Singh H., Glass C.K. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 2010, 38:576-589.
21. Hertel K.J., Graveley B.R. RS domains contact the pre-mRNA throughout spliceosome assembly. Trends Biochem. Sci. 2005, 30:115-118.
22. Huelga S.C., Vu A.Q., Arnold J.D., Liang T.Y., Liu P.P., Yan B.Y., Donohue J.P., Shiue L., Hoon S., Brenner S., et al. Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell Rep 2012, 1:167-178.
23. Itoh H., Washio T., Tomita M. Computational comparative analyses of alternative splicing regulation using full-length cDNA of various eukaryotes. RNA 2004, 10:1005-1018.
24. Kent W.J., Sugnet C.W., Furey T.S., Roskin K.M., Pringle T.H., Zahler A.M., Haussler D. The human genome browser at UCSC. Genome Res. 2002, 12:996-1006.
25. Lemaire R., Winne A., Sarkissian M., Lafyatis R. SF2 and SRp55 regulation of CD45 exon 4 skipping during T cell activation. Eur. J. Immunol. 1999, 29:823-837.
26. Li H., Qiu J., Fu X.D. RASL-seq for massively parallel and quantitative analysis of gene expression. Curr. Protoc. Mol. Biol. 2012, 98. 4.13.1-4.13.9.
27. Lim K.H., Ferraris L., Filloux M.E., Raphael B.J., Fairbrother W.G. Using positional distribution to identify splicing elements and predict pre-mRNA processing defects in human genes. Proc. Natl. Acad. Sci. USA 2011, 108:11093-11098.
28. Lin S., Fu X.D. SR proteins and related factors in alternative splicing. Adv. Exp. Med. Biol. 2007, 623:107-122.
29. Lin S., Xiao R., Sun P., Xu X., Fu X.D. Dephosphorylation-dependent sorting of SR splicing factors during mRNP maturation. Mol. Cell 2005, 20:413-425.
30. Liu H.X., Zhang M., Krainer A.R. Identification of functional exonic splicing enhancer motifs recognized by individual SR proteins. Genes Dev. 1998, 12:1998-2012.
31. Liu H.X., Chew S.L., Cartegni L., Zhang M.Q., Krainer A.R. Exonic splicing enhancer motif recognized by human SC35 under splicing conditions. Mol. Cell. Biol. 2000, 20:1063-1071.
32. Long J.C., Caceres J.F. The SR protein family of splicing factors: master regulators of gene expression. Biochem. J. 2009, 417:15-27.
33. Mayeda A., Krainer A.R. Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell 1992, 68:365-375.
34. Mayeda A., Munroe S.H., Cáceres J.F., Krainer A.R. Function of conserved domains of hnRNP A1 and other hnRNP A/B proteins. EMBO J. 1994, 13:5483-5495.
35. Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
36. Sakharkar M.K., Chow V.T., Kangueane P. Distributions of exons and introns in the human genome. In Silico Biol. (Gedrukt) 2004, 4:387-393.
37. Sanford J.R., Coutinho P., Hackett J.A., Wang X., Ranahan W., Caceres J.F. Identification of nuclear and cytoplasmic mRNA targets for the shuttling protein SF2/ASF. PLoS ONE 2008, 3:e3369.
38. Sanford J.R., Wang X., Mort M., Vanduyn N., Cooper D.N., Mooney S.D., Edenberg H.J., Liu Y. Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts. Genome Res. 2009, 19:381-394.
39. Schaal T.D., Maniatis T. Selection and characterization of pre-mRNA splicing enhancers: identification of novel SR protein-specific enhancer sequences. Mol. Cell. Biol. 1999, 19:1705-1719.
40. Shen H., Green M.R. RS domains contact splicing signals and promote splicing by a common mechanism in yeast through humans. Genes Dev. 2006, 20:1755-1765.
41. Shen H., Kan J.L., Green M.R. Arginine-serine-rich domains bound at splicing enhancers contact the branchpoint to promote prespliceosome assembly. Mol. Cell 2004, 13:367-376.
42. Solis A.S., Peng R., Crawford J.B., Phillips J.A., Patton J.G. Growth hormone deficiency and splicing fidelity: two serine/arginine-rich proteins, ASF/SF2 and SC35, act antagonistically. J. Biol. Chem. 2008, 283:23619-23626.
43. Tacke R., Manley J.L. The human splicing factors ASF/SF2 and SC35 possess distinct, functionally significant RNA binding specificities. EMBO J. 1995, 14:3540-3551.
44. Ule J., Jensen K., Mele A., Darnell R.B. CLIP: a method for identifying protein-RNA interaction sites in living cells. Methods 2005, 37:376-386.
45. Wang J., Smith P.J., Krainer A.R., Zhang M.Q. Distribution of SR protein exonic splicing enhancer motifs in human protein-coding genes. Nucleic Acids Res. 2005, 33:5053-5062.
46. Witten J.T., Ule J. Understanding splicing regulation through RNA splicing maps. Trends Genet. 2011, 27:89-97.
47. Wu H., Sun S., Tu K., Gao Y., Xie B., Krainer A.R., Zhu J. A splicing-independent function of SF2/ASF in microRNA processing. Mol. Cell 2010, 38:67-77.
48. Xiao R., Tang P., Yang B., Huang J., Zhou Y., Shao C., Li H., Sun H., Zhang Y., Fu X.D. Nuclear matrix factor hnRNP U/SAF-A exerts a global control of alternative splicing by regulating U2 snRNP maturation. Mol. Cell 2012, 45:656-668.
49. Xue Y., Zhou Y., Wu T., Zhu T., Ji X., Kwon Y.S., Zhang C., Yeo G., Black D.L., Sun H., et al. Genome-wide analysis of PTB-RNA interactions reveals a strategy used by the general splicing repressor to modulate exon inclusion or skipping. Mol. Cell 2009, 36:996-1006.
50. Yeo G., Burge C.B. Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J. Comput. Biol. 2004, 11:377-394.
51. Yeo G.W., Coufal N.G., Liang T.Y., Peng G.E., Fu X.D., Gage F.H. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat. Struct. Mol. Biol. 2009, 16:130-137.
52. Zhang X.H., Chasin L.A. Computational definition of sequence motifs governing constitutive exon splicing. Genes Dev. 2004, 18:1241-1250.
53. Zhang C., Darnell R.B. Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nat. Biotechnol. 2011, 29:607-614.
54. Zhong X.Y., Wang P., Han J., Rosenfeld M.G., Fu X.D. SR proteins in vertical integration of gene expression from transcription to RNA processing to translation. Mol. Cell 2009, 35:1-10.
55. Zhou Z., Qiu J., Liu W., Zhou Y., Plocinik R.M., Li H., Hu Q., Ghosh G., Adams J.A., Rosenfeld M.G., Fu X.D. The Akt-SRPK-SR axis constitutes a major pathway in transducing EGF signaling to regulate alternative splicing in the nucleus. Mol. Cell 2012, 47:422-433.