Phosphorylation-dephosphorylation differentially affects activities of splicing factor ASF/SF2

EMBO Journal

Volumn 17, Issue 21, 1998, Pages 6359-6367

  Xiao, Shou Hua ^a,b   Manley, James L ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b MILLENNIUM PHARMACEUTICALS INC   (United States)

Author keywords

Phosphorylation status; Splicing factor ASF SF2 SR proteins

Indexed keywords

RNA BINDING PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ALTERNATIVE RNA SPLICING; ARTICLE; DEPHOSPHORYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SPLICEOSOME; STRUCTURE ACTIVITY RELATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL EXTRACTS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; GENE PRODUCTS, TAT; HELA CELLS; HUMANS; INSECT PROTEINS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; RIBONUCLEOPROTEINS; RNA PRECURSORS; RNA SPLICING; RNA, VIRAL; RNA-BINDING PROTEINS;

EID: 0032476604     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.21.6359     Document Type: Article

References (70)

1. Amrein, H., Hedley, M.L. and Maniatis, T. (1994) The role of specific protein-RNA and protein-protein interactions in positive and negative control of pre-mRNA splicing by transformer 2. Cell, 76, 735-746.
2. Berget, S.M. (1995) Exon recognition in vertebrate splicing. J. Biol. Chem., 270, 2411-2414.
3. Cáceres, J.F., Stamm, S., Helhman, D.M. and Krainer, A. (1994) Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science, 265, 1706-1709.
4. Cao, W., Jamison, S.F. and Garcia-Blanco, M.A. (1997) Both phosphorylation and dephosphorylation of ASF/SF2 are required for premRNA splicing in vitro. RNA, 3, 1456-1467.
5. Champion-Arnaud, P., Gozani, O., Palandjian, L. and Reed, R. (1995) Accumulation of a novel spliceosomal complex on pre-mRNAs containing branch site mutations. Mol. Cell. Biol., 15, 5750-5756.
6. Chandler, S.D., Mayeda, A. Yeakley, J.M. Krainer, A.R. and Fu, X.-D. (1997) RNA splicing specificity determined by the coordinated action of RNA recognition in SR proteins. Proc. Natl Acad. Sci. USA, 94, 3596-3601.
7. 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 intracellular distribution. EMBO J., 15, 265-275.
8. Crispino, J.D. and Sharp, P.A. (1995) A U6 snRNA:pre-mRNA interaction can be rate-limiting for U1-independent splicing. Genes Dev., 9, 2314-2323.
9. Crispino, J.D., Blencowe, B.J. and Sharp, P.A. (1994) Complementation by SR proteins of pre-mRNA splicing reactions depleted of U1 snRNP, Science. 265, 1866-1869.
10. Eperon, I.C. Ireland, D.C., Smith, R.A., Mayeda, A. and Krainer, A.R. (1993) Pathways for selection of 5′ splice sites by U1 snRNPs and SF2/ASF. EMBO J., 12, 3607-3617.
11. Fu, X.-D. (1993) Specific commitment of different pre-mRNAs to splicing by single SR proteins. Nature, 365, 82-85.
12. Fu, X.-D. (1995) The superfamily of arginine/serine-rich splicing factors. RNA, 1, 663-680.
13. Fu, X.-D. and Maniatis, T. (1992) Isolation of a complementary DNA that encodes the mammalian splicing factor SC35. Science, 256, 535-538.
14. Fu, X.-D., Mayeda, A., Maniatis, T. and Krainer, A.R. (1992) General splicing factor SF2 and SC35 have equivalent activities in vitro and both affect alternative 5′ and 3′ splice site selection. Proc. Natl Acad. Sci. USA, 89, 11224-11228.
15. Ge, H. and Manley, J.L. (1990) A protein factor. ASF, controls cell-specific alternative splicing of SV40 early pre-mRNA in vitro. Cell, 62, 25-34.
16. Ge, H., Zuo, P. and Manley, J.L. (1991) Primary structure of the human splicing factor ASF reveals similarities with Drosophila regulators. Cell, 66, 373-382.
17. 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.
18. 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.
19. Huang, S. and Spector, D.L. (1996) Intron-dependent recruitment of pre-mRNA splicing factors to sites of transcription. J. Cell Biol., 133, 719-732.
20. Jamison, S.F. Pasman, Z., Wang, J., Will, C., Lührmann, R., Manley, J.L. and Garcia-Blanco, M.A. (1995) U1 snRNP-ASF/SF2 interaction and 5′ splice site recognition: characterization of required elements. Nucleic Acids Res., 23, 3260-3267.
21. Kohtz, J.D., Jamison, S.F., Will, C.L., Zuo, P., Lührmann, R., Garcia-Blanco, M.A. and Manley, J.L. (1994) Protein-protein interactions and 5′-splice site recognition in mammalian mRNA precursors. Nature, 368, 119-124.
22. Konforti, B.B., Koziolkiewicz, M.J. and Konaska, M.M. (1993) Disruption of base pairing between the 5′ splice site and the 5′ end of U1 snRNA is required for spliceosome assembly, Cell, 75, 863-873.
23. Krainer, A.R., Conway, G.C. and Kozak, D. (1990a) Purification and characterization of pre-mRNA splicing factor SF2 from HeLa cells. Genes Dev., 4, 1158-1171.
24. Krainer, A.R., Conway, G.C. and Kozak, D. (1990b) The essential pre-mRNA splicing factor SF2 influences 5′ splice site selection by activating proximal sites. Cell 62, 35-42.
25. Krainer, A.R., Mayeda, A., Kozak, D. and Binns, G. (1991) Functional expression of cloned human splicing factor SF2: homology to RNA-binding proteins, U170K and Drosophila splicing regulators. Cell, 66, 383-394.
26. Kramer, A. (1996) The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem., 65, 367-409.
27. Lynch, K.W. and Maniatis, T. (1995) Synergistic interactions between two distinct elements of a regulated splicing enhancer. Genes Dev., 9, 284-293.
28. Lynch, K.W. and Maniatis, T. (1996) Assembly of specific SR protein complexes on distinct regulatory elements of the Drosophila doublesex splicing enhancer. Genes Dev., 10, 2089-2101.
29. Madhani, H.D. and Guthrie, C. (1994) Dynamic RNA-RNA interactions in the spliceosome. Annu. Rev. Genet., 28, 1-26.
30. Manley, J.L. and Tacke, R. (1996) SR proteins and splicing control. Genes Dev., 10, 1569-1579.
31. Mermoud, J.E., Cohen, P. and Lamond, A.I. (1992) Ser/Thr-specific protein phosphatases are required for both catalytic steps of pre-mRNA splicing. Nucleic Acids Res., 20, 5263-5269.
32. Mermoud, J., Cohen, P.T.W. and Lamond, A.I. (1994) Regulation of mammalian spliceosome assembly by a protein phosphorylation mechanism. EMBO J., 13, 5679-5688.
33. Misteli, T. and Spector, D.L. (1997) Protein phosphorylation and nuclear organization of pre-mRNA splicing. Trends Cell Biol., 7, 135-138.
34. Misteli, T. Caceres J.F. and Spector, D.L. (1997) The dynamics of a pre-mRNA splicing factor in living cells. Nature, 387, 523-527.
35. Moore, M.J., Query, C.C. and Sharp, P.A. (1993) Splicing of precursors to messenger RNAs by the spliceosome. In Gesteland, R.F. and Atkins, J.F. (eds), The RNA World. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. pp. 303-358.
36. Ramchatesingh, J., Zahler, A.M., Neubebauer, K.M., Roth, M.B. and Cooper, T.A, (1995) A subset of SR proteins activates splicing of the cardiac troponin T alternative exon by direct interactions with an exonic enhancer. Mol. Cell. Biol., 15, 4898-1907.
37. Roscigno, R.F. and Garcia-Blanco, M.A. (1995) SR proteins escort U4/ 6.U5 tri-snRNP to the spliceosome. RNA, 1, 692-706.
38. Roth, M.B., Murphy, C. and Gall, J.G. (1990) A monoclonal antibody that recognizes a phosphorylated cpitope stains lampbrush chromosome loops and small granules in the amphibian germinal vesicle. J. Cell Biol., 111, 2217-2223.
39. Roth, M.B., Zahler, A.M. and Stolk, J.A. (1991) A conserved family of nuclear phosphoproteins is localized to sites of polymerase II transcription. J. Cell Biol., 115, 587-596.
40. Si, Z., Amendt, B.A. and Stoltzfus, C.M. (1997) Splicing efficiency of human immunodeficiency virus type 1 tat RNA is determined by both a suboptimal 3′ splice site and a 10 nucleotide exon splicing silencer element located within tat exon 2. Nucleic Acids Res., 25, 861-867.
41. Singer, R.H. and Green, M.R. (1997) Compartmentalization of eukaryotic gene expression: causes and effects. Cell, 91, 291-294.
42. Staffa, A. and Cochrane, A. (1994) The tat rev intron of human immunodeficiency virus type 1 is inefficiently spliced because of suboptimal signals in the 3′ splice site. J. Virol., 68, 3071-3079.
43. Staffa, A. and Cochrane, A. (1995) Identification of positive and negative splicing regulatory elements within the terminal tat-rev exon of human immunodeficiency virus type 1. Mol. Cell. Biol., 15, 4597-4605.
44. Staknis, D. and Reed, R. (1994) SR proteins promote the first specific recognition of pre-mRNA and are present together with the U1 small nuclear ribonucleoprotein particle in a general splicing enhancer complex. Mol. Cell. Biol., 14, 7670-7682.
45. Staknis, D. and Reed, R. (1995) Members of a family of proteins (the RD family) detected by a U1 70K monoclonal antibody are present in spliceosomal complexes. Nucleic Acids Res., 23, 4081-4086.
46. Sun, Q., Mayeda, A., Hampson, R.K., Krainer, A.R. and Rottman, F.M. (1993) General splicing factor SF2/ASF promotes alternative splicing by binding to an exonic splicing enhancer. Genes Dev, 7, 2598-2608.
47. Tacke, R. and Manley, J.L. (1995) The human splicing factors ASF/SF2 and SC35 possess different, functionally significant RNA binding specificities. EMBO J., 14, 3540-3551.
48. Tacke, R., Chen, Y. and Manley, J.L. (1997) Sequence-specific RNA binding by an SR protein requires RS domain phosphorylation: creation of an SRp40-specific splicing enhancer. Proc. Natl Acad. Sci. USA, 94, 1148-1153.
49. Tacke, R., Tohyama, M., Ogawa, S. and Manley, J.L. (1998) Human Tra2 proteins are sequence-specific activators of pre-mRNA splicing. Cell, 93, 139-148.
50. Tam, W.Y. and Steitz, J.A. (1995) Modulation of 5′ splice site choice in pre-messenger RNA by two distinct steps. Proc. Natl Acad. Sci. USA, 92, 2504-2508.
51. Tazi, J., Daugeron, M.C., Cathala, G., Brunel, C. and Jeanteur, P (1992) Adenosine phosphoruthioates (ATPαS and ATPTS) differentially affect the two steps of mammalian pre-mRNA splicing. J. Biol. Chem., 267, 4322-4326.
52. Tazi, J., Kornstadt, U., Rossi, F., Jeanteur, P., Cathala, G., Brunel.C, and Lührmann, R. (1993) Thiophosphorylation of U1-70K protein inhibits pre-mRNA splicing. Nature, 363, 283-286.
53. Tian, M. and Maniatis, T. (1993) A splicing enhancer complex controls alternative splicing of doublesex pre-mRNA. Cell, 74, 105-114.
54. Valcárcel, J. and Green, M.R. (1996) The SR protein family: pleiotropic functions in pre-mRNA splicing. Trends Biochem. Sci., 21, 296-301.
55. 65 RS region with pre-mRNA branch point and promotion of base pairing with U2 snRNA. Science, 273, 1706-1709.
56. Wang, J. and Manley, J.L. (1995) Overexpression of the SR proteins ASF/ SF2 and SC35 influences alternative splicing in vivo in diverse ways. RNA, 1, 335-346.
57. 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.
58. Wang, Z, Hoffman, H.M. and Grabowski, P.J. (1995) Intrinsic U2AF binding is modulated by exon enhancer signals in parallel with changes in splicing activity. RNA, 1, 21-35.
59. Wu, J.Y. and Maniatis, T. (1993) Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell, 75, 1061-1070.
60. 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.
61. Yeakley, J.M., Morfin, J.P., Rosenfeld, M.G. and Fu, X.-D. (1996) A complex of nuclear proteins mediates SR protein binding to a purine-rich splicing enhancer. Proc. Natl Acad. Sci. USA, 93, 7582-7587.
62. Zahler, A.M., Lane, W.S., Stòlk, J.A. and Roth, M.B. (1992) SR proteins: a conserved family of pre-mRNA splicing factors. Genes Dev., 6, 837-847.
63. Zahler, A.M. and Roth, M.B. (1995) Distinct functions of SR proteins in recruitment of U1 snRNP to alternative 5′ splice sites. Proc. Natl Acad. Sci. USA. 92, 2642-2646.
64. Zahler, A.M., Neugenbauer, K.M., Lane, W.S. and Roth, M.B. (1993) Distinct functions of SR proteins in alternative pre-mRNA splicing. Science. 260, 219-222.
65. Zamore, P.D., Patton, J.G. and Green, M.R. (1992) Cloning and domain structure of the mammalian splicing factor U2AF. Nature, 355, 609-614.
66. Zeng, C., Kim, E., Warren, S.L. and Berget, S.M. (1997) Dynamic relocation of transcription and splicing factors dependent upon transcriptional activity. EMBO J., 16, 1401-1412.
67. Zhang, G., Taneja, K.L., Singer, R.H. and Green, M.R. (1994) Localization of pre-mRNA splicing in mammalian nuclei. Nature, 372, 809-812.
68. Zhang, M., Zamore, P.D., Carmo-Fonseca.M., Lamond.A.I. and Green.M.R. (1992) Cloning and imracellular localization of the U2 small nuclear ribonucleoprotein auxiliary factor small subunit. Proc. Natl Acad. Sci. USA, 89, 8769-8773.
69. 35 mediates critical protein-protein interactions in constitutive and enhancer-dependent splicing. Genes Dev., 10, 1356-1368.
70. Zuo, P. and Manley, J.L. (1994) The human splicing factor ASF/SF2 can specifically recognize pre-mRNA 5′ splice sites. Proc. Natl Acad. Sci. USA, 91, 3363-3367.