SR proteins induce alternative exon skipping through their activities on the flanking constitutive exons

Molecular and Cellular Biology

Volumn 31, Issue 4, 2011, Pages 793-802

  Han, Joonhee ^a   Ding, Jian Hua ^a   Byeon, Cheol W ^b   Kim, Jee H ^b   Hertel, Klemens J ^c   Jeong, Sunjoo ^b   Fu, Xiang Dong ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Dankook University   (South Korea)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IIDELTA; REGULATOR PROTEIN; RNA BINDING FOX FAMILY OF SPLICING REGULATOR PROTEIN; SERINE ARGININE RICH PROTEIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; DNA FLANKING REGION; DOWN REGULATION; EMBRYO; EXON SKIPPING; MOUSE; MUTATIONAL ANALYSIS; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION;

ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL DIFFERENTIATION; CELLS, CULTURED; EXONS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MUTAGENESIS; NEURONS; NUCLEAR PROTEINS; RECOMBINANT PROTEINS; RNA-BINDING PROTEINS;

MAMMALIA; MUS;

EID: 79251584960     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01117-10     Document Type: Article

References (49)

1. Anko, M. L., L. Morales, I. Henry, A. Beyer, and K. M. Neugebauer. 2010. Global analysis reveals SRp20- and SRp75-specific mRNPs in cycling and neural cells. Nat. Struct. Mol. Biol. 17:962-970.
2. Black, D. L. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72:291-336.
3. Buratti, E., C. Stuani, G. De Prato, and F. E. Baralle. 2007. SR protein-mediated inhibition of CFTR exon 9 inclusion: molecular characterization of the intronic splicing silencer. Nucleic Acids Res. 35:4359-4368.
4. Ding, J. H., et al. 2004. Dilated cardiomyopathy caused by tissue-specific ablation of SC35 in the heart. EMBO J. 23:885-896.
5. Eperon, I. C., D. C. Ireland, R. A. Smith, A. Mayeda, and A. R. Krainer. 1993. Pathways for selection of 5′ splice sites by U1 snRNPs and SF2/ASF. EMBO J. 12:3607-3617.
6. Eperon, I. C., et al. 2000. Selection of alternative 5′ splice sites: role of U1 snRNP and models for the antagonistic effects of SF2/ASF and hnRNP A1. Mol. Cell. Biol. 20:8303-8318.
7. Fu, X. D. 1995. The superfamily of arginine/serine-rich splicing factors. RNA 1:663-680.
8. Fu, X. D. 2004. Towards a splicing code. Cell 119:736-738.
9. Gallego, M. E., R. Gattoni, J. Stevenin, J. Marie, and A. Expert-Bezancon. 1997. 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. 16:1772-1784.
10. Ghigna, C., et al. 2005. Cell motility is controlled by SF2/ASF through alternative splicing of the Ron protooncogene. Mol. Cell 20:881-890. (Pubitemid 41814877)
11. Goren, A., et al. 2006. Comparative analysis identifies exonic splicing regulatory sequences: the complex definition of enhancers and silencers. Mol. Cell 22:769-781. (Pubitemid 43912467)
12. Graveley, B. R. 2000. Sorting out the complexity of SR protein functions. RNA 6:1197-1211.
13. Graveley, B. R., and T. Maniatis. 1998. Arginine/serine-rich domains of SR proteins can function as activators of pre-mRNA splicing. Mol. Cell 1:765-771.
14. Hakim, N., T. Kounishi, A. Alam, T. Tsukahara, and H. Suzuki. 2010. Alternative splicing of Mef2c promoted by Fox-1 during neuronal differentiation in P19 cells. Genes Cells 15:255-267.
15. Hanamura, A., J. F. Caceres, A. Mayeda, B. R. Franza, Jr., and A. R. Krainer. 1998. Regulated tissue-specific expression of antagonistic premRNA splicing factors. RNA 4:430-444.
16. Hertel, K. J. 2008. Combinatorial control of exon recognition. J. Biol. Chem. 283:1211-1215.
17. Hertel, K. J., and B. R. Graveley. 2005. RS domains contact the pre-mRNA throughout spliceosome assembly. Trends Biochem. Sci. 30:115-118.
18. Hicks, M. J., B. J. Lam, and K. J. Hertel. 2005. Analyzing mechanisms of alternative pre-mRNA splicing using in vitro splicing assays. Methods 37:306-313.
19. +/calmodulin- dependent protein kinase II: the role of structure and autoregulation in cellular function. Annu. Rev. Biochem. 71:473-510.
20. Ibrahim el, C., T. D. Schaal, K. J. Hertel, R. Reed, and T. Maniatis. 2005. Serine/arginine-rich protein-dependent suppression of exon skipping by exonic splicing enhancers. Proc. Natl. Acad. Sci. U. S. A. 102:5002-5007.
21. Itoh, F., T. Nakane, and S. Chiba. 1997. Expression of MASH-1, MATH-1, neuronD, and NSCL-2, basic helix-loop-helix during neuronal differentiation in p19 embryonal carcinoma cells. J. Exp. Med. 182:327-336.
22. Jiang, Z. H., W. J. Zhang, Y. Rao, and J. Y. Wu. 1998. Regulation of Ich-1 pre-mRNA alternative splicing and apoptosis by mammalian splicing factors. Proc. Natl. Acad. Sci. U. S. A. 95:9155-9160.
23. Jumaa, H., and P. J. Nielsen. 1997. The splicing factor SRp20 modifies splicing of its own mRNA and ASF/SF2 antagonizes this regulation. EMBO J. 16:5077-5085.
24. Karni, R., et al. 2007. The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nat. Struct. Mol. Biol. 14:185-193.
25. Kornblihtt, A. R., M. de la Mata, J. P. Fededa, M. J. Munoz, and G. Nogues. 2004. Multiple links between transcription and splicing. RNA 10:1489-1498.
26. Lareau, L. F., M. Inada, R. E. Green, J. C. Wengrod, and S. E. Brenner. 2007. Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature 446:926-929.
27. Lemaire, R., A. Winne, M. Sarkissian, and R. Lafyatis. 1999. SF2 and SRp55 regulation of CD45 exon 4 skipping during T cell activation. Eur. J. Immunol. 29:823-837.
28. Lin, S., G. Coutinho-Mansfield, D. Wang, S. Pandit, and X. D. Fu. 2008. The splicing factor SC35 has an active role in transcriptional elongation. Nat. Struct. Mol. Biol. 15:819-826.
29. Lin, S., and X. D. Fu. 2007. SR proteins and related factors in alternative splicing. Adv. Exp. Med. Biol. 623:107-122.
30. Lin, S., R. Xiao, P. Sun, X. Xu, and X. D. Fu. 2005. Dephosphorylation- dependent sorting of SR splicing factors during mRNP maturation. Mol. Cell 20:413-425.
31. Long, J. C., and J. F. Caceres. 2009. The SR protein family of splicing factors: master regulators of gene expression. Biochem. J. 417:15-27.
32. Modafferi, E. F., and D. L. Black. 1997. A complex intronic splicing enhancer from the c-src pre-mRNA activates inclusion of a heterologous exon. Mol. Cell. Biol. 17:6537-6545.
33. Modafferi, E. F., and D. L. Black. 1999. Combinatorial control of a neuron-specific exon. RNA 5:687-706.
34. Nakahata, S., and S. Kawamoto. 2005. Tissue-dependent isoforms of mammalian Fox-1 homologs are associated with tissue-specific splicing activities. Nucleic Acids Res. 33:2078-2089.
35. Sanford, J. R., et al. 2008. Identification of nuclear and cytoplasmic mRNA targets for the shuttling protein SF2/ASF. PLoS One 3:e3369.
36. Sanford, J. R., et al. 2009. Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts. Genome Res. 19:381-394.
37. Schaal, T. D., and T. Maniatis. 1999. Multiple distinct splicing enhancers in the protein-coding sequences of a constitutively spliced pre-mRNA. Mol. Cell. Biol. 19:261-273.
38. 2+/calmodulin-dependent protein kinase II. Differential expression in rat brain and aorta. J. Biol. Chem. 268:14443-14449.
39. Shen, H., J. L. Kan, and M. R. Green. 2004. Arginine-serine-rich domains bound at splicing enhancers contact the branchpoint to promote prespliceosome assembly. Mol. Cell 13:367-376.
40. Solis, A. S., R. Peng, J. B. Crawford, J. A. Phillips III, and J. G. Patton. 2008. Growth hormone deficiency and splicing fidelity: two serine/arginine-rich proteins, ASF/SF2 and SC35, act antagonistically. J. Biol. Chem. 283:23619-23626.
41. ten Dam, G. B., et al. 2000. Regulation of alternative splicing of CD45 by antagonistic effects of SR protein splicing factors. J. Immunol. 164:5287-5295.
42. Underwood, J. G., P. L. Boutz, J. D. Dougherty, P. Stoilov, and D. L. Black. 2005. Homologues of the Caenorhabditis elegans Fox-1 protein are neuronal splicing regulators in mammals. Mol. Cell. Biol. 25:10005-10016.
43. Wang, E. T., et al. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456:470-476.
44. Xiao, R., et al. 2007. Splicing regulator SC35 is essential for genomic stability and cell proliferation during mammalian organogenesis. Mol. Cell. Biol. 27:5393-5402.
45. Xu, X., et al. 2005. ASF/SF2-regulated CaMKIIδ alternative splicing temporally reprograms excitation-contraction coupling in cardiac muscle. Cell 120:59-72.
46. Yeo, G. W., et al. 2009. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat. Struct. Mol. Biol. 16:130-137.
47. Zhang, C., et al. 2008. Defining the regulatory network of the tissue-specific splicing factors Fox-1 and Fox-2. Genes Dev. 22:2550-2563.
48. Zhong, X. Y., P. Wang, J. Han, M. G. Rosenfeld, and X. D. Fu. 2009. SR proteins in vertical integration of gene expression from transcription to RNA processing to translation. Mol. Cell 35:1-10.
49. Zhou, H. L., and H. Lou. 2008. Repression of prespliceosome complex formation at two distinct steps by Fox-1/Fox-2 proteins. Mol. Cell. Biol. 28:5507-5516.