Partial purification of the yeast U2 snRNP reveals a novel yeast pre-mRNA splicing factor required for pre-spliceosome assembly

EMBO Journal

Volumn 18, Issue 12, 1999, Pages 3463-3474

  Caspary, Friederike ^a   Shevchenko, Anna ^a   Wilm, Matthias ^a   Séraphin, Bertrand ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

DNA repair; Polyadenylation; RSE1; Saccharomyces cerevisiae; SF3

Indexed keywords

FUNGAL PROTEIN; MESSENGER RNA PRECURSOR; MUTANT PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DATA BASE; MASS SPECTROMETRY; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE; SPLICEOSOME;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; DNA REPAIR; FUNGAL PROTEINS; GENES, ESSENTIAL; GENES, FUNGAL; HUMANS; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; MUTATION; OPEN READING FRAMES; RIBONUCLEOPROTEIN, U2 SMALL NUCLEAR; RNA SPLICING; RNA, SMALL NUCLEAR; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SALTS; SEQUENCE ALIGNMENT; SPLICEOSOMES;

EID: 0033564206     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.12.3463     Document Type: Article

References (70)

1. Abovich, N. and Rosbash, M. (1997) Cross-intron bridging and interactions in the yeast commitment complex are conserved in mammals. Cell, 89, 403-412.
2. Abovich, N., Liao, X.C. and Rosbash, M. (1994) The yeast MUD2 protein: an interaction with PRP11 defines a bridge between commitment complexes and U2 snRNP addition. Genes Dev., 8, 843-854.
3. Alexander, H., Lee, S.K., Yu, S.L. and Alexander, S. (1996) repE - the Dictyostelium homolog of the human xeroderma pigmentosum group E gene is developmentally regulated and contains a leucine zipper motif. Nucleic Acids Res., 24, 2295-2301.
4. Behrens, S.E., Galisson, F., Legrain, P. and Lührmann, R. (1993a) Evidence that the 60-kDa protein of 17S U2 small nuclear ribonucleoprotein is immunologically and functionally related to the yeast PRP9 splicing factor and is required for the efficient formation of prespliceosomes. Proc. Natl Acad. Sci. USA, 90, 8229-8233.
5. Behrens, S.E., Tyc, K., Kastner, B., Reichelt, J. and Lührmann, R. (1993b) Small nuclear ribonucleoprotein (RNP) U2 contains numerous additional proteins and has a bipartite RNP structure under splicing conditions. Mol. Cell. Biol., 13, 307-319.
6. Bennett, M. and Reed, R. (1993) Correspondence between a mammalian spliceosome component and an essential yeast splicing factor. Science, 262, 105-108.
7. Bennett, M., Michaud, S., Kingston, J. and Reed, R. (1992) Protein components specifically associated with prespliceosome and spliceosome complexes. Genes Dev., 6, 1986-2000.
8. Berglund, J.A., Abovich, N. and Rosbash, M. (1998) A cooperative interaction between U2AF65 and mBBP/SFI facilitates branchpoint region recognition. Genes Dev., 12, 858-867.
9. Brosi, R., Groning, K., Behrens, S.E., Lührmann, R. and Krämer, A. (1993a) Interaction of mammalian splicing factor SF3a with U2 snRNP and relation of its 60-kD subunit to yeast PRP9. Science, 262, 102-105.
10. Brosi, R., Hauri, H.P. and Krämer, A. (1993b) Separation of splicing factor SF3 into two components and purification of SF3a activity. J. Biol. Chem., 268, 17640-17646.
11. Burd, C.G. and Dreyfuss, G. (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science, 265, 615-621.
12. Caspary, F. and Séraphin, B. (1998) The yeast U2A′/U2B″ complex is required for pre-spliceosome formation. EMBO J., 17, 6348-6358.
13. Champion-Amaud, P. and Reed, R. (1994) The prespliceosome components SAP 49 and SAP 145 interact in a complex implicated in tethering U2 snRNP to the branch site. Genes Dev., 16, 1974-1983.
14. Chen, E.J., Frand, A.R., Chitouras, E. and Kaiser, C.A. (1998) A link between secretion and pre-mRNA processing defects in Saccharomyces cerevisiae and the identification of a novel splicing gene. RSEI. Mol. Cell. Biol., 18, 7139-7146.
15. Chiara, M.D., Champion Arnaud, P., Buvoli, M., Nadal Ginard, B. and Reed, R. (1994) Specific protein-protein interactions between the essential mammalian spliceosome-associated proteins SAP 61 and SAP 114. Proc. Natl Acad. Sci. USA, 91, 6403-6407.
16. Devereux, J., Haeberli, P. and Smithies, O. (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res., 12, 387-395.
17. Dualan, R., Brody, T., Keeney, S., Nichols, A.F., Admon, A. and Linn, S. (1995) Chromosomal localization and cDNA cloning of the genes (DDB1 and DDB2) for the p127 and p48 subunits of a human damage-specific DNA binding protein. Genomics, 29, 62-69.
18. Fabrizio, P., McPheeters, D.S. and Abelson, J. (1989) In vitro assembly of yeast U6 snRNP: a functional assay. Genes Dev., 3, 2137-2150.
19. Fromont-Racine, M., Rain, J.-C. and Legrain, P. (1997) Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nature Genet., 16, 277-282.
20. Gottschalk, A. et al. (1998) A comprehensive biochemical and genetic analysis of the yeast U1 snRNP reveals five novel proteins. RNA, 4, 374-393.
21. Gozani, O., Feld, R. and Reed, R. (1996) Evidence that sequence-independent binding of highly conserved U2 snRNP proteins upstream of the branch site is required for assembly of spliceosomal complex A. Genes Dev., 10, 233-243.
22. Gozani, O., Potashkin, J. and Reed, R. (1998) A potential role for U2AF-SAP 155 interactions in recruiting U2 snRNP to the branch site. Mol. Cell. Biol., 18, 4752-4760.
23. Hodges, P.E. and Beggs, J.D. (1994) RNA splicing. U2 fulfils a commitment. Curr. Biol., 4, 264-267.
24. Igel, H., Wells, S., Perriman, R. and Ares, M., Jr (1998) Conservation of structure and subunit interactions in yeast homologues of splicing factor 3b (SF3b) subunits. RNA, 4, 1-10.
25. Jenny, A. and Keller, W. (1995) Cloning of cDNAs encoding the 160 kDa subunit of the bovine cleavage and polyadenylation specificity factor. Nucleic Acids Res., 23, 2629-2635.
26. Keller, W., Bienroth, S., Lang, K.M. and Christofori, G. (1991) Cleavage and polyadenylation factor CPF specifically interacts with the pre-mRNA 3′ processing signal AAUAAA. EMBO J., 10, 4241-4249.
27. Krámer, A. (1988) Presplicing complex formation requires two proteins and U2 snRNP. Genes Dev., 2, 1155-1167.
28. Krämer, A. (1992) Purification of splicing factor SF1, a heat stable protein that functions in the assembly of a presplicing complex. Mol. Cell. Biol., 12, 4545-4552.
29. Krämer, A. (1996) The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem., 65, 367-409.
30. Krämer, A. and Utans, U. (1991) Three protein factors (SF1, SF3 and U2AF) function in pre-splicing complex formation in addition to snRNPs. EMBO J., 10, 1503-1509.
31. Krämer, A., Mulhauser, F., Wersig, C., Groning, K. and Bilbe, G. (1995) Mammalian splicing factor SF3a120 represents a new member of the SURP family of proteins and is homologous to the essential splicing factor PRP21p of Saccharomyces cerevisiae. RNA, 1, 260-272.
32. Lafontaine, D. and Tollervey, D. (1996) One-step PCR mediated strategy for the construction of conditionally expressed and epitope tagged yeast proteins. Nucleic Acids Res., 24, 3469-3471.
33. Legrain, P. and Chapon, C. (1993) Interaction between PRP11 and SPP91 yeast splicing factors and characterization of a PRP9-PRP11-SPP91 complex. Science, 262, 108-110.
34. Liao, X.C., Colot, H.V., Wang, Y. and Rosbash, M. (1992) Requirements for U2 snRNP addition to yeast pre-mRNA. Nucleic Acids Res., 20, 4237-4245.
35. Mann, M. (1996) A shortcut to interesting human genes: peptide sequence tags, expressed-sequence tags and computers. Trends Biol. Sci., 21, 494-495.
36. Michaud, S. and Reed, R. (1991) An ATP-independent complex commits pre-mRNA to the mammalian spliceosome assembly pathway. Genes Dev., 5, 2534-2546.
37. Moore, M., Query, C. and Sharp, P. (1993) Splicing of precursors to mRNA by the spliceosome. In Gesteland, R. and Atkins, J. (eds), The RNA World. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 303-357.
38. Murthy, K.G. and Manley, J.L. (1995) The 160-kD subunit of human cleavage-polyadenylation specificity factor coordinates pre-mRNA 3′-end formation. Genes Dev., 9, 2672-2683.
39. Neubauer, G., Gottschalk, A., Fabrizio, P., Séraphin, B., Lührmann, R. and Mann, M. (1997) Identification of the proteins of the yeast U1 small nuclear ribonucleoprotein complex by mass spectrometry. Proc. Natl Acad. Sci. USA, 94, 385-390.
40. Newman, A. (1994) Analysis of pre-mRNA splicing in yeast. In Higgins, S.J. and Hames, B.D. (eds), RNA Processing. Vol. I. Oxford University Press, Oxford, UK, pp. 179-196.
41. Pikielny, C.W. and Rosbash, M. (1985) mRNA splicing efficiency in yeast and the contribution of nonconserved sequences. Cell, 41, 119-126.
42. Polycarpou-Schwarz, M., Gunderson, S., Kandels-Lewis, S., Séraphin, B. and Mattaj, I. (1996) Drosophila SNF/D25 combines the function of the two snRNP proteins U1A and U2B″ that are encoded separately in human, potato and yeast. RNA, 2, 11-23.
43. Puig, O., Rutz, B., Luukkonen, B.G.M., Kandels-Lewis, S., Bragado-Nilsson, E. and Séraphin, B. (1998) New constructs and strategies for efficient PCR-based gene manipulations in yeast. Yeast, 14, 1139-1146.
44. Rain, J.C., Tartakoff, A.M., Krämer, A. and Legrain, P. (1996) Essential domains of the RP21 splicing factor are implicated in the binding to PRP9 and PRP11 proteins and are conserved through evolution. RNA, 2, 535-550.
45. Reardon, J.T., Nichols, A.F., Keeney, S., Smith, C.A., Taylor, J.S., Linn, S. and Sancar, A. (1993) Comparative analysis of binding of human damaged DNA-binding protein (XPE) and Escherichia coli damage recognition protein (UvrA) to the major ultraviolet photoproducts: T[c,s]T, T[t,s]T, T[6-4]T and T[Dewar]T. J. Biol. Chem., 268, 21301-21308.
46. Reed, R. (1996) Initial splice-site recognition and pairing during pre-mRNA splicing. Curr. Opin. Genet. Dev., 6, 215-220.
47. Rosbash, M. and Séraphin, B. (1991) Who's on first? The U1 snRNP-5′ splice site interaction and splicing. Trends Biochem. Sci., 16, 187-190.
48. Ruby, S.W., Chang, T.H. and Abelson, J. (1993) Four yeast spliceosomal proteins (PRP5, PRP9, PRP11 and PRP21) interact to promote U2 snRNP binding to pre-mRNA. Genes Dev., 7, 1909-1925.
49. Salgado-Garrido, J., Bragado-Nilsson, E., Kandels-Lewis, S. and Séraphin, B. (1999) Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin. EMBO J., 18, 3451-3462.
50. Schmidt-Zachmann, M.S., Knecht, S. and Kramer, A. (1998) Molecular characterization of a novel, widespread nuclear protein that colocalizes with spliceosome components. Mol. Biol. Cell, 9, 143-160.
51. Séraphin, B. (1995) Sm and Sm-like proteins belong to a large family: identification of proteins of the U6 as well as the U1, U2, U4 and U5 snRNPs. EMBO J., 14, 2089-2098.
52. Séraphin, B. and Rosbash, M. (1989a) Identification of functional U1 snRNA-pre-mRNA complexes committed to spliceosome assembly and splicing. Cell, 59, 349-358.
53. Séraphin, B. and Rosbash, M. (1989b) Mutational analysis of the interactions between U1 small nuclear RNA and pre-mRNA of yeast. Gene, 82, 145-151.
54. Séraphin, B. and Rosbash, M. (1991) The yeast branchpoint sequence is not required for the formation of a stable U1 snRNA-pre-mRNA complex and is recognized in the absence of U2 snRNA. EMBO J., 10, 1209-1216.
55. Séraphin, B., Kretzner, L. and Rosbash, M. (1988) A U1 snRNA:pre-mRNA base pairing interaction is required early in yeast spliceosome assembly but does not uniquely define the 5′ cleavage site. EMBO J., 7, 2533-2538.
56. Shevchenko, A., Wilm, M., Vorm, O. and Mann, M. (1996) Mass spectrometric sequencing of proteins on silver-stained polyacrylamide gels. Anal. Chem., 68, 850-858.
57. Soni, R. and Carmichael, J.P. (1993) Parameters affecting lithium acetate-mediated transformation of S.cerevisiae and development of a rapid and simplified procedure. Curr. Genet., 24, 455-459.
58. Staknis, D. and Reed, R. (1994) Direct interactions between pre-mRNA and six U2 small nuclear ribonucleoproteins during spliceosome assembly. Mol. Cell. Biol., 14, 2994-3005.
59. Staley, J.P. and Guthrie, C. (1998) Mechanical devices of the spliceosome: motors, clocks, springs and things. Cell, 92, 315-326.
60. Stumpf, G. and Domdey, H. (1996) Dependence of yeast pre-mRNA 3′-end processing on CFT1: a sequence homolog of the mammalian AAUAAA binding factor. Science, 274, 1517-1520.
61. Takao, M., Abramic, M., Moos, M., Jr, Otrin, V.R., Wootton, J.C., McLenigan, M., Levine, A.S. and Protic, M. (1993) A 127 kDa component of a UV-damaged DNA-binding complex, which is defective in some xeroderma pigmentosum group E patients, is homologous to a slime mold protein. Nucleic Acids Res., 21, 4111-4118.
62. Tang, J., Abovich, N. and Rosbash, M. (1996) Identification and characterization of a yeast gene encoding the U2 small nuclear ribonucleoprotein particle B″ protein. Mol. Cell Biol., 16, 2787-2795.
63. Teem, J.L. and Rosbash, M. (1983) Expression of a β-galactosidase gene containing the ribosomal protein 51 intron is sensitive to the rna2 mutation of yeast. Proc. Natl Acad. Sci. USA, 80, 4403-4407.
64. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25, 4876-4882.
65. Wang, C., Chua, K., Seghezzi, W., Lees, E., Gozani, O. and Reed, R. (1998) Phosphorylation of spliceosomal protein SAP 155 coupled with splicing catalysis. Genes Dev., 12, 1409-1414.
66. Wells, S.E., Neville, M., Haynes, M., Wang, J., Igel, H. and Ares, M., Jr (1996) CUS1, a suppressor of cold-sensitive U2 snRNA mutations, is a novel yeast splicing factor homologous to human SAP 145. Genes Dev., 10, 220-232.
67. Will, C. and Lührmann, R. (1997) Protein functions in pre-mRNA splicing. Curr. Opin. Cell Biol., 9, 320-328.
68. Wilm, M. and Mann, M. (1996) Analytical properties of the nanoelectrospray ion source. Anal. Chem., 68, 1-8.
69. 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.
70. Zavanelli, M.I. and Ares, M., Jr (1991) Efficient association of U2 snRNPs with pre-mRNA requires an essential U2 RNA structural element. Genes Dev., 5, 2521-2533.