A novel role for shuttling SR proteins in mRNA translation

Genes and Development

Volumn 18, Issue 7, 2004, Pages 755-768

  Sanford, Jeremy R ^a   Gray, Nicola K ^a   Beckmann, Karsten ^a,b   Cáceres, Javier F ^a  

^a WESTERN GENERAL HOSPITAL   (United Kingdom)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Nucleocytoplasmic shuttling; Pre mRNA splicing; Ribosomes; SR proteins; Translation

Indexed keywords

ARGININE; MESSENGER RNA; PHOSPHOPROTEIN; PROTEIN; SERINE;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; OOCYTE; PRIORITY JOURNAL; RIBOSOME; RNA SPLICING; RNA TRANSLATION; XENOPUS;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BINDING SITES; CELL NUCLEUS; CYTOPLASM; FEMALE; GENE EXPRESSION REGULATION; GENES, REPORTER; HELA CELLS; HUMANS; LUCIFERASES; NUCLEAR PROTEINS; OOCYTES; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOMES; RNA SPLICING; RNA, MESSENGER; RNA-BINDING PROTEINS; XENOPUS LAEVIS;

ANIMALIA; EUKARYOTA;

EID: 1842632326     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.286404     Document Type: Article

References (66)

1. Bergamini, G., Preiss, T., and Hentze, M.W. 2000. Picomavirus IRESes and the poly(A) tail jointly promote cap-independent translation in a mammalian cell-free system. RNA 6: 1781-1790.
2. Blencowe, B.J. 2000. Exonic splicing enhancers: Mechanism of action, diversity and role in human genetic diseases. Trends Biochem. Sci. 25: 106-110.
3. Burge, C.B., Padgett, R.A., and Sharp, P.A. 1998. Evolutionary fates and origins of U12-type introns. Mol. Cell 2: 773-785.
4. Caceres, J.F. and Komblihtt, A.R. 2002. Alternative splicing: Multiple control mechanisms and involvement in human disease. Trends Genet. 18: 186-193.
5. Caceres, J.F. and Krainer, A.R. 1993. Functional analysis of pre-mRNA splicing factor SF2/ASF structural domains. EMBO J. 12: 4715-4726.
6. Caceres, J.F., Stamm, S., Helfman, D.M., and Krainer, A.R. 1994. Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265: 1706-1709.
7. Caceres, J.F., Misteli, T., Screaton, G.R., Spector, D.L., and Krainer, A.R. 1997. Role of the modular domains of SR proteins in subnuclear localization and alternative splicing specificity. J. Cell. Biol. 138: 225-238.
8. Caceres, J.F., Screaton, G.R., and Krainer, A.R. 1998. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes & Dev. 12: 55-66.
9. Caputi, M., Casari, G., Guenzi, S., Tagliabue, R., Sidoli, A., Melo, C.A., and Baralle, F.E. 1994. A novel bipartite splicing enhancer modulates the differential processing of the human fibronectin EDA exon. Nucleic Acids Res. 22: 1018-1022.
10. Cartegni, L., Wang, J., Zhu, Z., Zhang, M.Q., and Krainer, A.R. 2003. ESEfinder: A web resource to identify exonic splicing enhancers. Nucleic Acids Res. 31: 3568-3571.
11. Cavaloc, Y., Bourgeois, C.F., Kister, L., and Stevenin, J. 1999. The splicing factors 9G8 and SRp20 transactivate splicing through different and specific enhancers. RNA 5: 468-483.
12. Cazalla, D., Zhu, J., Manche, L., Huber, E., Krainer, A.R., and Caceres, J.F. 2002. Nuclear export and retention signals in the RS domain of SR proteins. Mol. Cell Biol. 22: 6871-6882.
13. Cramer, P., Caceres, J.F., Cazalla, D., Kadener, S., Muro, A.F., Baralle, F.E., and Kornblihtt, A.R. 1999. Coupling of transcription with alternative splicing: RNA pol II promoters modulate SF2/ASF and 9G8 effects on an exonic splicing enhancer. Mol. Cell 4: 251-258.
14. Dreyfuss, G., Kim, V.N., and Kataoka, N. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell. Biol. 3: 195-205.
15. Fu, X.D. 1995. The superfamily of arginine/serine-rich splicing factors. RNA 1: 663-680.
16. Gorlach, M., Burd, C.G., and Dreyfuss, G. 1994. The mRNA poly(A)-binding protein: Localization, abundance, and RNA-binding specificity. Exp. Cell Res. 211: 400-407.
17. Graveley, B.R. 2000. Sorting out the complexity of SR protein functions. RNA 6: 1197-1211.
18. Graveley, B.R. and Maniatis, T. 1998. Arginine/serine-rich domains of SR proteins can function as activators of pre-mRNA splicing. Mol. Cell 1: 765-771.
19. Graveley, B.R., Hertel, K.J., and Maniatis, T. 1998. A systematic analysis of the factors that determine the strength of pre-mRNA splicing enhancers. EMBO J. 17: 6747-6756.
20. Gray, N.K., Coller, J.M., Dickson, K.S., and Wickens, M. 2000. Multiple portions of poly(A)-binding protein stimulate translation in vivo. EMBO J. 19: 4723-4733.
21. Habelhah, H., Shah, K., Huang, L., Ostareck-Lederer, A., Burlingame, A.L., Shokat, K.M., Hentze, M.W., and Ronai, Z. 2001. ERK phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation. Nat. Cell. Biol. 3: 325-330.
22. Hanamura, A., Caceres, J.F., Mayeda, A., Franza, B.R., and Krainer, A.R. 1998. Regulated tissue-specific expression of antagonistic pre-mRNA splicing factors. RNA 4: 430-444.
23. Hastings, M.L. and Krainer, A.R. 2001. Pre-mRNA splicing in the new millennium. Curr. Opin. Cell. Biol. 13: 302-309.
24. Hedley, M.L., Amrein, H., and Maniatis, T. 1995. An amino acid sequence motif sufficient for subnuclear localization of an arginine/serine-rich splicing factor. Proc. Natl. Acad. Sci. 92: 11524-11528.
25. Hoek, K.S., Kidd, G.J., Carson, J.H., and Smith, R. 1998. hnRNP A2 selectively binds the cytoplasmic transport sequence of myelin basic protein mRNA. Biochemistry 37: 7021-7029.
26. Hoffman, B.E. and Lis, J.T. 2000. Pre-mRNA splicing by the essential Drosophila protein B52: Tissue and target specificity. Mol. Cell. Biol. 20: 181-186.
27. Huang, Y. and Steitz, J.A. 2001. Splicing factors SRp20 and 9G8 promote the nucleocytoplasmic export of mRNA. Mol. Cell 7: 899-905.
28. Huang, Y., Gattoni, R., Stevenin, J., and Steitz, J.A. 2003. SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol. Cell 11: 837-843.
29. Jumaa, H. and Nielsen, P.J. 1997. The splicing factor SRp20 modifies splicing of its own mRNA and ASF/SF2 antagonizes this regulation. EMBO J. 16: 5077-5085.
30. Jumaa, H., Wei, G., and Nielsen, P.J. 1999. Blastocyst formation is blocked in mouse embryos lacking the splicing factor SRp20. Curr. Biol. 9: 899-902.
31. Jurica, M.S. and Moore, M.J. 2003. Pre-mRNA splicing. Awash in a sea of proteins. Mol. Cell 12: 5-14.
32. Kaminski, A., Hunt, S.L., Patton, J.G., and Jackson, R.J. 1995. Direct evidence that polypyrimidine tract binding protein (PTB) is essential for internal initiation of translation of encephalomyocarditis virus RNA. RNA 1: 924-938.
33. Kawano, T., Fujita, M., and Sakamoto, H. 2000. Unique and redundant functions of SR proteins, a conserved family of splicing factors, in Caenorhabditis elegans development. Mech. Dev. 95: 67-76.
34. Kollmus, H., Flohe, L., and McCarthy, J.E. 1996. Analysis of eukaryotic mRNA structures directing cotranslational incorporation of selenocysteine. Nucleic Acids Res. 24: 1195-1201.
35. Kramer, A. 1996. The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem. 65: 367-409.
36. Lall, S., Francis-Lang, H., Flament, A., Norvell, A., Schupbach, T., and Ish-Horowicz, D. 1999. Squid hnRNP protein promotes apical cytoplasmic transport and localization of Drosophila pair-rule transcripts. Cell 98: 171-180.
37. Lamond, A.I. and Spector, D.L. 2003. Nuclear speckles: A model for nuclear organelles. Nat. Rev. Mol. Cell. Biol. 4: 605-612.
38. Lavigueur, A., La Branch, H., Kornblihtt, A.R., and Chabot, B. 1993. A splicing enhancer in the human fibronectin alternate ED1 exon interacts with SR proteins and stimulates U2 snRNP binding. Genes & Dev. 7: 2405-2417.
39. Lemaire, R., Prasad, J., Kashima, T., Gustafson, J., Manley, J.L., and Lafyatis, R. 2002. Stability of a PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: A novel function for SR proteins. Genes & Dev. 16: 594-607.
40. Liu, H.X., Chew, S.L., Cartegni, L., Zhang, M.Q., and Krainer, A.R. 2000. Exonic splicing enhancer motif recognized by human SC35 under splicing conditions. Mol. Cell. Biol. 20: 1063-1071.
41. Loflin, P., Chen, C.Y., and Shyu, A.B. 1999. Unraveling a cytoplasmic role for hnRNP D in the in vivo mRNA destabilization directed by the AU-rich element. Genes & Dev. 13: 1884-1897.
42. Longman, D., Johnstone, I.L., and Caceres, J.F. 2000. Functional characterization of SR and SR-related genes in Caenorhabditis elegans. EMBO J. 19: 1625-1637.
43. Lu, S. and Cullen, B.R. 2003. Analysis of the stimulatory effect of splicing on mRNA production and utilization in mammalian cells. RNA 9: 618-630.
44. Mayeda, A. and Krainer, A.R. 1992. Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell 68: 365-375.
45. Neugebauer, K.M. and Roth, M.B. 1997. Distribution of pre-mRNA splicing factors at sites of RNA polymerase II transcription. Genes & Dev. 11: 1148-1159.
46. Nott, A., Meislin, S.H., and Moore, M.J. 2003. A quantitative analysis of intron effects on mammalian gene expression. RNA 9: 607-617.
47. Nott, A., Le Hir, H., and Moore, M.J. 2004. Splicing enhances translation in mammalian cells: An additional function of the exon junction complex. Genes & Dev. 18: 210-222.
48. Ostareck, D.H., Ostareck-Lederer, A., Wilm, M., Thiele, B.J., Mann, M., and Hentze, M.W. 1997. mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3′ end. Cell 89: 597-606.
49. Peng, X. and Mount, S.M. 1995. Genetic enhancement of RNA-processing defects by a dominant mutation in B52, the Drosophila gene for an SR protein splicing factor. Mol. Cell. Biol. 15: 6273-6282.
50. Pinol-Roma, S. and Dreyfuss, G. 1992. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355: 730-732.
51. Ring, H.Z. and Lis, J.T. 1994. The SR protein B52/SRp55 is essential for Drosophila development. Mol. Cell. Biol. 14: 7499-7506.
52. Sanford, J.R., Longman, D., and Caceres, J.F. 2003. Multiple roles of the SR protein family in splicing regulation. Prog. Mol. Subcell. Biol. 31: 33-58.
53. Shyu, A.B. and Wilkinson, M.F. 2000. The double lives of shuttling mRNA binding proteins. Cell 102: 135-138.
54. Snow, B.E., Heng, H.H., Shi, X.M., Zhou, Y., Du, K., Taub, R., Tsui, L.C., and McInnes, R.R. 1997. Expression analysis and chromosomal assignment of the human SFRS5/SRp40 gene. Genomics 43: 165-170.
55. Spector, D.L., Fu, X.D., and Maniatis, T. 1991. Associations between distinct pre-mRNA splicing components and the cell nucleus. EMBO J. 10: 3467-3481.
56. Tacke, R. and Manley, J.L. 1999. Determinants of SR protein specificity. Curr. Opin. Cell. Biol. 11: 358-362.
57. Valcarcel, J. and Green, M.R. 1996. The SR protein family: Pleiotropic functions in pre-mRNA splicing. Trends Biochem. Sci. 21: 296-301.
58. Wang, J., Takagaki, Y., and Manley, J.L. 1996. Targeted disruption of an essential vertebrate gene: ASF/SF2 is required for cell viability. Genes & Dev. 10: 2588-2599.
59. Wang, J., Xiao, S.H., and Manley, J.L. 1998. Genetic analysis of the SR protein ASF/SF2: Interchangeability of RS domains and negative control of splicing. Genes & Dev. 12: 2222-2233.
60. Wang, H.Y., Xu, X., Ding, J.H., Bermingham Jr., J.R., and Fu, X.D. 2001. SC35 plays a role in T cell development and alternative splicing of CD45. Mol. Cell 7: 331-342.
61. Wiegand, H.L., Lu, S., and Cullen, B.R. 2003. Exon junction complexes mediate the enhancing effect of splicing on mRNA expression. Proc. Natl. Acad. Sci. 100: 11327-11332.
62. Will, C.L. and Luhrmann, R. 1997. Protein functions in pre-mRNA splicing. Curr. Opin. Cell. Biol. 9: 320-328.
63. Wu, J.Y. and Maniatis, T. 1993. Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75: 1061-1070.
64. Xu, N., Chen, C.Y., and Shyu, A.B. 2001. Versatile role for hnRNP D isoforms in the differential regulation of cytoplasmic mRNA turnover. Mol. Cell. Biol. 21: 6960-6971.
65. Yang, X., Bani, M.R., Lu, S.J., Rowan, S., Ben David, Y., and Chabot, B. 1994. The A1 and A1B proteins of heterogeneous nuclear ribonucleoparticles modulate 5′ splice site selection in vivo. Proc. Natl. Acad. Sci. 91: 6924-6928.
66. Zuo, P. and Maniatis, T. 1996. The splicing factor U2AF35 mediates critical protein-protein interactions in constitutive and enhancer-dependent splicing. Genes & Dev. 10: 1356-1368.