Distinctive Features of Drosophila Alternative Splicing Factor RS Domain: Implication for Specific Phosphorylation, Shuttling, and Splicing Activation

REFERENCES

• Biencowe, B. J.. 2000. Exonic splicing enhancers: mechanism of action, diversity and role in human genetic diseases. Trends Biochem. 25:106–110.
   PubMedGoogle Scholar
• Brand, A. H., A. S. Manoukian, and N. Perrimon. 1994. Ectopic expression in Drosophila. Methods Cell Biol. 44:635–654.
   PubMedGoogle Scholar
• Cáceres, J. F., and A. R. Krainer. 1993. Functional analysis of pre-mRNA splicing factor SF2/ASF structural domains. EMBO J. 12:4715–4726.
   PubMed Web of Science ®Google Scholar
• Cáceres, J. F., T. Misteli, G. R. Screaton, D. L. Spector, and A. R. Krainer. 1997. Role of the modular domains of SR proteins in subnuclear localization and alternative splicing specificity. J. Cell Biol. 138:225–238.
   PubMed Web of Science ®Google Scholar
• Cáceres, J. F., G. R. Screaton, and A. R. Krainer. 1998. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev. 12:55–66.
   PubMed Web of Science ®Google Scholar
• Cavaloc, Y., M. Popielarz, J. P. Fuchs, R. Gattoni, and J. Stevenin. 1994. Characterization and cloning of the human splicing factor 9G8: a novel 35 kDa factor of the serine/arginine protein family. EMBO J. 13:2639–2649.
   PubMed Web of Science ®Google Scholar
• Cavaloc, Y., C. F. Bourgeois, L. Kister, and J. Stevenin. 1999. The splicing factors 9G8 and SRp20 transactivate splicing through different and specific enhancers. RNA 5:468–483.
   PubMed Web of Science ®Google Scholar
• Colwill, K., T. Pawson, B. Andrews, J. Prasad, J. L. Manley, J. C. Bell, and P. I. Duncan. 1996. The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J. 15:265–275.
   PubMed Web of Science ®Google Scholar
• Colwill, K., L. L. Feng, J. M. Yeakley, G. D. Gish, J. F. Cáceres, T. Pawson, and X. D. Fu. 1996. SRPK1 and Clk/Sty protein kinases show distinct substrate specificities for serine/arginine-rich splicing factors. J. Biol. Chem. 271:24569–24575.
   PubMed Web of Science ®Google Scholar
• Flach, J., M. Bossie, J. Vogel, A. Corbett, T. Jinks, D. A. Willins, and P. A. Silver. 1994. A yeast RNA-binding protein shuttles between the nucleus and the cytoplasm. Mol. Cell. Biol. 14:8399–8407.
   PubMedGoogle Scholar
• Freeman, M.. 1996. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87:651–660.
   PubMed Web of Science ®Google Scholar
• Fu, X. D., and T. Maniatis. 1992. Isolation of a complementary DNA that encodes the mammalian splicing factor SC35. Science 256:535–538.
   PubMed Web of Science ®Google Scholar
• Fu, X. D.. 1995. The superfamily of arginine/serine-rich splicing factors. RNA 1:663–680.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ge, H., P. Zuo, and J. L. Manley. 1991. Primary structure of the human splicing factor ASF reveals similarities with Drosophila regulators. Cell 66:373–382.
   PubMedGoogle Scholar
• Graveley, B. R., K. J. Hertel, and T. Maniatis. 1998. A systematic analysis of the factors that determine the strength of pre-mRNA splicing enhancers. EMBO J. 17:6747–6756.
   PubMed Web of Science ®Google Scholar
• Gui, J. F., W. S. Lane, and X. D. Fu. 1994. A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature 369:678–682.
   PubMed Web of Science ®Google Scholar
• Hecht, N. B.. 2000. Intracellular and intercellular transport of many germ cell mRNAs is mediated by the DNA- and RNA-binding protein, testis-brain-RNA-binding protein (TB-RBP). Mol. Reprod. Dev. 56:252–253.
   PubMedGoogle Scholar
• Hedley, M. L., H. Amrein, and T. Maniatis. 1995. An amino acid sequence motif sufficient for subnuclear localization of an arginine/serine-rich splicing factor. Proc. Natl. Acad. Sci. USA 92:11524–11528.
   PubMed Web of Science ®Google Scholar
• Heinrichs, V., and B. S. Baker. 1997. In vivo analysis of the functional domains of the Drosophila splicing regulator RBP1. Proc. Natl. Acad. Sci. USA 94:115–120.
   PubMedGoogle Scholar
• Kim, Y. J., P. Zuo, J. L. Manley, and B. S. Baker. 1992. The Drosophila RNA-binding protein RBP1 is localized to transcriptionally active sites of chromosomes and shows a functional similarity to human splicing factor ASF/SF2. Genes Dev. 6:2569–2579.
   PubMedGoogle Scholar
• Kohtz, J. D., S. F. Jamison, C. L. Will, P. Zuo, R. Luhrmann, M. A. Garcia-Blanco, and J. L. Manley. 1994. Protein-protein interactions and 5′-splice-site recognition in mammalian mRNA precursors. Nature 368:119–124.
   PubMed Web of Science ®Google Scholar
• Koizumi, J., Y. Okamoto, H. Onogi, A. Mayeda, A. R. Krainer, and M. Hagiwara. 1999. The subcellular localization of SF2/ASF is regulated by direct interaction with SR protein kinases (SRPKs). J. Biol. Chem. 274:11125–11131.
   PubMed Web of Science ®Google Scholar
• Krainer, A. R., A. Mayeda, D. Kozak, and G. Binns. 1991. Functional expression of cloned human splicing factor SF2: homology to RNA-binding proteins, U1 70K, and Drosophila splicing regulators. Cell 66:383–394.
   PubMed Web of Science ®Google Scholar
• Krämer, A.. 1996. The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem. 65:367–409.
   PubMed Web of Science ®Google Scholar
• Kraus, M. E., and J. T. Lis. 1994. The concentration of B52, an essential splicing factor and regulator of splice site choice in vitro, is critical for Drosophila development. Mol. Cell. Biol. 14:5360–5370.
   PubMedGoogle Scholar
• Labourier, E., F. Rossi, I. E. Gallouzi, E. Allemand, G. Divita, and J. Tazi. 1998. Interaction between the N-terminal domain of human DNA topoisomerase I and the arginine-serine domain of its substrate determines phosphorylation of SF2/ASF splicing factor. Nucleic Acids Res. 26:2955–2962.
   PubMedGoogle Scholar
• Labourier, E., H. M. Bourbon, I. Gallouzi, M. Fostier, E. Allemand, and J. Tazi. 1999. Antagonism between RSF1 and SR proteins for both splice site recognition in vitro and Drosophila development. Genes Dev. 13:740–753.
   PubMedGoogle Scholar
• Labourier, E., J. F. Riou, M. Prudhomme, C. Carrasco, C. Bailly, and J. Tazi. 1999. Poisoning of topoisomerase I by an antitumor indolocarbazole drug: stabilization of topoisomerase I-DNA covalent complexes and specific inhibition of the protein kinase activity. Cancer Res. 59:52–55.
   PubMed Web of Science ®Google Scholar
• Lai, M. C., R. I. Lin, S. Y. Huang, C. W. Tsai, and W. Y. Tarn. 2000. A human importin-beta family protein, transportin-SR2, interacts with the phosphorylated RS domain of SR proteins. J. Biol. Chem. 275:7950–7957.
   PubMed Web of Science ®Google Scholar
• Lynch, K. W., and T. Maniatis. 1996. Assembly of specific SR protein complexes on distinct regulatory elements of the Drosophila doublesex splicing enhancer. Genes Dev. 10:2089–2101.
   PubMed Web of Science ®Google Scholar
• Manley, J. L., and R. Tacke. 1996. SR proteins and splicing control. Genes Dev. 10:1569–1579.
   PubMed Web of Science ®Google Scholar
• Mayeda, A., G. R. Screaton, S. D. Chandler, X. D. Fu, and A. R. Krainer. 1999. Substrate specificities of SR proteins in constitutive splicing are determined by their RNA recognition motifs and composite pre-mRNA exonic elements. Mol. Cell. Biol. 19:1853–1863.
   PubMed Web of Science ®Google Scholar
• Mintz, P. J., and D. L. Spector. 2000. Compartmentalization of RNA processing factors within nuclear speckles. J. Struct. Biol. 129:241–251.
   PubMedGoogle Scholar
• Misteli, T., J. F. Cáceres, and D. L. Spector. 1997. The dynamics of a pre-mRNA splicing factor in living cells. Nature 387:523–527.
   PubMed Web of Science ®Google Scholar
• Misteli, T., J. F. Cáceres, J. Q. Clement, A. R. Krainer, M. F. Wilkinson, and D. L. Spector. 1998. Serine phosphorylation of SR proteins is required for their recruitment to sites of transcription in vivo. J. Cell Biol. 143:297–307.
   PubMed Web of Science ®Google Scholar
• Mount, S. M., and H. K. Salz. 2000. Pre-messenger RNA processing factors in the Drosophila genome. J. Cell Biol. 150:F37–F44.
   PubMed Web of Science ®Google Scholar
• Papoutsopoulou, S., E. Nikolakaki, G. Chalepakis, V. Kruft, P. Chevaillier, and T. Giannakouros. 1999. SR protein-specific kinase 1 is highly expressed in testis and phosphorylates protamine 1. Nucleic Acids Res. 27:2972–2980.
   PubMedGoogle Scholar
• Pinol-Roma, S., and G. Dreyfuss. 1992. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355:730–732.
   PubMed Web of Science ®Google Scholar
• Popielarz, M., R. Gattoni, and J. Stevenin. 1993. Contrasted cis-acting effects of downstream 5′ splice sites on the splicing of a retained intron: the adenoviral E1A pre-mRNA model. Nucleic Acids Res. 21:5144–5151.
   PubMedGoogle Scholar
• Prasad, J., K. Colwill, T. Pawson, and J. L. Manley. 1999. The protein kinase Clk/Sty directly modulates SR protein activity: both hyper- and hypophosphorylation inhibit splicing. Mol. Cell. Biol. 19:6991–7000.
   PubMedGoogle Scholar
• Reed, R.. 2000. Mechanisms of fidelity in pre-mRNA splicing. Curr. Opin. Cell Biol. 12:340–345.
   PubMed Web of Science ®Google Scholar
• Reed, R., and T. Maniatis. 1986. A role for exon sequences and splice-site proximity in splice-site selection. Cell 46:681–690.
   PubMed Web of Science ®Google Scholar
• Rio, D. C.. 1988. Accurate and efficient pre-mRNA splicing in Drosophila cell-free extracts. Proc. Natl. Acad. Sci. USA 85:2904–2908.
   PubMedGoogle Scholar
• Rossi, F., E. Labourier, T. Forne, G. Divita, J. Derancourt, J. F. Riou, E. Antoine, G. Cathala, C. Brunel, and J. Tazi. 1996. Specific phosphorylation of SR proteins by mammalian DNA topoisomerase I. Nature 381:80–82.
   PubMed Web of Science ®Google Scholar
• Rossi, F., E. Labourier, I. E. Gallouzi, J. Derancourt, E. Allemand, G. Divita, and J. Tazi. 1998. The C-terminal domain but not the tyrosine 723 of human DNA topoisomerase I active site contributes to kinase activity. Nucleic Acids Res. 26:2963–2970.
   PubMedGoogle Scholar
• Roth, M. B., C. Murphy, and J. G. Gall. 1990. A monoclonal antibody that recognizes a phosphorylated epitope stains lambrush chromosome loops and small granules in the amphibian germinal vesicle. J. Cell Biol. 111:2217–2223.
   PubMedGoogle Scholar
• Roth, M. B., A. M. Zahler, and J. A. Stolk. 1991. A conserved family of nuclear phosphoproteins localized to sites of polymerase II transcription. J. Cell Biol. 115:587–596.
   PubMed Web of Science ®Google Scholar
• Rubin, G. M., L. Hong, P. Brokstein, M. Evans-Holm, E. Frise, M. Stapleton, and D. A. Harvey. 2000. A Drosophila complementary DNA resource. Science 287:2222–2224.
   PubMed Web of Science ®Google Scholar
• Siebel, C. W., L. Feng, C. Guthrie, and X. D. Fu. 1999. Conservation in budding yeast of a kinase specific for SR splicing factors. Proc. Natl. Acad. Sci. USA 96:5440–5445.
   PubMedGoogle Scholar
• Spradling, A. C., and G. M. Rubin. 1982. Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218:341–347.
   PubMed Web of Science ®Google Scholar
• Staley, J. P., and C. Guthrie. 1998. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92:315–326.
   PubMed Web of Science ®Google Scholar
• Tacke, R., and J. L. Manley. 1995. The human splicing factors ASF/SF2 and SC35 possess distinct, functionally significant RNA binding specificities. EMBO J. 14:3540–3551.
   PubMed Web of Science ®Google Scholar
• Tacke, R., and J. L. Manley. 1999. Determinants of SR protein specificity. Curr. Opin. Cell Biol. 11:358–362.
   PubMedGoogle Scholar
• Tazi, J., J. Temsamani, C. Alibert, W. Rhead, S. Khellil, G. Cathala, C. Brunel, and P. Jeanteur. 1989. Purified U5 small nuclear ribonucleoprotein can relieve the inhibition of spliceosome assembly and splicing by snRNP-free nuclear proteins. Nucleic Acids Res. 17:5223–5243.
   PubMedGoogle Scholar
• Tazi, J., U. Kornstadt, F. Rossi, P. Jeanteur, G. Cathala, C. Brunel, and R. Lührmann. 1993. Thiophosphorylation of U1–70K protein inhibits pre-mRNA splicing. Nature 363:283–286.
   PubMed Web of Science ®Google Scholar
• Tazi, J., F. Rossi, E. Labourier, I. Gallouzi, C. Brunel, and E. Antoine. 1997. DNA topoisomerase I: customs officer at the border between DNA and RNA worlds?. J. Mol. Med. 75:786–800.
   PubMedGoogle Scholar
• Wu, J. Y., and T. Maniatis. 1993. Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75:1061–1070.
   PubMed Web of Science ®Google Scholar
• Xiao, S. H., and J. L. Manley. 1998. Phosphorylation-dephosphorylation differentially affects activities of splicing factor ASF/SF2. EMBO J. 17:6359–6367.
   PubMedGoogle Scholar
• Yeakley, J. M., H. Tronchere, J. Olesen, J. A. Dyck, H. Y. Wang, and X. D. Fu. 1999. Phosphorylation regulates in vivo interaction and molecular targeting of serine/arginine-rich pre-mRNA splicing factors. J. Cell Biol. 145:447–455.
   PubMed Web of Science ®Google Scholar
• Zahler, A. M., W. S. Lane, J. A. Stolk, and M. B. Roth. 1992. SR proteins: a conserved family of pre-mRNA splicing factors. Genes Dev. 6:837–847.
   PubMed Web of Science ®Google Scholar
• Zillmann, M., M. L. Zapp, and S. M. Berget. 1988. Gel electrophoretic isolation of splicing complexes containing U1 small nuclear ribonucleoprotein particles. Mol. Cell. Biol. 8:814–821.
   PubMedGoogle Scholar
• Zuo, P., and J. L. Manley. 1993. Functional domains of the human splicing factor ASF/SF2. EMBO J. 12:4727–4737.
   PubMed Web of Science ®Google Scholar
• Zuo, P., and T. Maniatis. 1996. The splicing factor U2AF35 mediates critical protein-protein interactions in constitutive and enhancer-dependent splicing. Genes Dev. 10:1356–1368.
   PubMedGoogle Scholar