An evolutionarily conserved U5 snRNP-specific protein is a GTP-binding factor closely related to the ribosomal translocase EF-2

EMBO Journal

Volumn 16, Issue 13, 1997, Pages 4092-4106

  Fabrizio, Patrizia ^a   Laggerbauer, Bernhard ^a   Lauber, Jürgen ^a,c   Lane, William S ^b   Lührmann, Reinhard ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b HARVARD UNIVERSITY   (United States)

^c QIAGEN GMBH   (Germany)

Author keywords

Elongation factor EF 2; GTP binding; GTPase superfamily; Pre mRNA splicing; U5 snRNP

Indexed keywords

CARRIER PROTEIN; ELONGATION FACTOR; GUANINE NUCLEOTIDE BINDING PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; CONFORMATIONAL TRANSITION; CONSENSUS SEQUENCE; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; RNA CONFORMATION; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SPLICEOSOME; ULTRAVIOLET IRRADIATION; YEAST CELL;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CELL SURVIVAL; CONSERVED SEQUENCE; CROSS-LINKING REAGENTS; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; GENES, LETHAL; GTP-BINDING PROTEINS; GUANOSINE TRIPHOSPHATE; HELA CELLS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PEPTIDE ELONGATION FACTOR 2; PEPTIDE ELONGATION FACTOR G; PEPTIDE ELONGATION FACTORS; PHENOTYPE; RIBONUCLEOPROTEIN, U5 SMALL NUCLEAR; RNA PRECURSORS; RNA SPLICING; SUBCELLULAR FRACTIONS; ULTRAVIOLET RAYS;

EID: 0030976931     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.13.4092     Document Type: Article

References (93)

1. Abel, K. and Jurnak, F. (1996) A complex profile of protein elongation: translating chemical energy into molecular movement. Structure, 4, 229-238.
2. Ævarsson, A. (1995) Structure-based sequence alignment of elongation factors Tu and G with related GTPase involved in translation. J. Mol. Evol., 41, 1096-1104.
3. Ævarsson, A., Brazhnikov, E., Garber, M., Zheltonosova, J., Chirgadze, Y., Al-Karadaghi, S., Svensson, L.A. and Liljas, A. (1994) Three-dimensional structure of the ribosomal translocase: elongation factor G from Thermus thermophilus. EMBO J., 13, 3669-3677.
4. Altschul, S.F., Gish, W., Miller, W., Myers, E.M. and Lipman, J. (1990) Basic local alignment search tool. J. Mol. Biol., 215, 403-410.
5. Bach, M., Bringmann, P. and Lührmann, R. (1990) Purification of small nuclear ribonucleoprotein particles with antibodies against modified nucleosides of small nuclear RNAs. Methods Enzymol., 181, 232-257.
6. Beggs, J.D. (1995) Yeast splicing factors and genetics strategies for their analysis. In Lamond,A.I. (ed.), Pre-mRNA Processing. R.G. Landes Co., TX, pp. 79-95.
7. Behrens, S.E. and Lührmann, R. (1991) Immunoaffinity purification of a [U4/U6·U5] tri-snRNP from human cells. Genes Dev., 5, 1439-1452.
8. Bennett, M., Michaud, S., Kingston, J. and Reed, R. (1992) Protein components specifically associated with prespliceosome and spliceosome complexes. Genes Dev., 6, 1986-2000.
9. Berchtold, H., Reshetnikova, L., Reiser, C.O., Schirmer, N.K., Sprinzl, M. and Hilgenfeld, R. (1993) Crystal structure of active elongation factor Tu reveals major domain rearrangements. Nature, 365, 126-132.
10. Bochnig, P., Reuter, R., Bringmann, P. and Lührmann, R. (1987) A monoclonal antibody against 2,2,7-trimethylguanosine that reacts with intact, class U, small nuclear ribonucleoproteins as well as with 7-methylguanosine-capped RNAs. Eur. J. Biochem., 168, 461-467.
11. Boeke, J.D., Trueheart, J., Natsoulis, G. and Fink, G.R. (1987) 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol., 154, 164-175.
12. Bourne, H.R., Sanders, D.A. and McCormick, F. (1990) The GTPase superfamily: a conserved switch for diverse cell functions. Nature, 348, 125-132.
13. Bourne, H.R., Sanders, D.A. and McCormick, F. (1991) The GTPase superfamily: conserved structure and molecular mechanism. Nature, 349, 117-127.
14. Bringmann, P., Appel, B., Rinke, J., Reuter, R., Theissen, H. and Lührmann, R. (1984) Evidence for the existence of snRNAs U4 and U6 in a single ribonucleoprotein complex and for their association by intermolecular base pairing. EMBO J., 3, 1357-1363.
15. Brow, D.A. and Guthrie, C. (1988) Spliceosomal RNA U6 is remarkably conserved from yeast to mammals. Nature, 334, 213-218.
16. Burgess, S.M. and Guthrie, C. (1993) Beat the clock: paradigms for NTPases in the maintenance of biological fidelity. Trends Biochem. Sci., 18, 381-384.
17. Burgess, S., Couto, J.R. and Guthrie, C. (1990) A putative ATP binding protein influences the fidelity of branchpoint recognition in yeast splicing. Cell, 60, 705-717.
18. Chen, J.H. and Lin, R.J. (1990) The yeast PRP2 protein, a putative RNA-dependent ATPase, shares extensive sequence homology with two other pre-mRNA splicing factors. Nucleic Acids Res., 18, 6447.
19. Company, M., Arenas, J. and Abelson, J. (1991) Requirement of the RNA helicase-like protein PRP22 for release of messenger RNA from spliceosomes. Nature, 349, 487-193.
20. Cortes, J.J., Sontheimer, E.J., Seiwert, S.D. and Steitz, J.A. (1993) Mutations in the conserved loop of human U5 snRNA generate use of novel cryptic 5′ splice sites in vivo. EMBO J., 12, 5181-5189.
21. Czworkowski, J., Wang, J., Steitz, T.A. and Moore, P.B. (1994) The crystal structure of the elongation factor G complexed with GDP, at 2.7 Å resolution. EMBO J., 13, 3661-3668.
22. Dalbadie-McFarland, G. and Abelson, J. (1990) PRP5: a helicase-like protein required for mRNA splicing in yeast. Proc. Natl Acad. Sci. USA, 87, 4236-4240.
23. Datta, B. and Weiner, A.M. (1991) Genetic evidence for base pairing between U2 and U6 snRNA in mammalian mRNA splicine. Nature, 352, 821-824.
24. Dever, T.E., Glynias, M.J. and Merrick, W.C. (1987) GTP-binding domain: three consensus sequence elements with distinct spacing. Proc. Natl Acad. Sci. USA, 84, 1814-1818.
25. Dignam, J.D., Lebovitz, R.M. and Roeder, R.G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11, 1475-1489.
26. Dujon, B. et al. (1994) Complete DNA sequence of yeast chromosome XI. Nature, 369, 371-378.
27. 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.
28. Fabrizio, P. and Abelson, J. (1990) Two domains of yeast U6 small nuclear RNA required for both steps of nuclear precursor messenger RNA splicing. Science, 250, 404-409.
29. Fabrizio, R. McPheeters, D.S. and Abelson, J. (1989) In vitro assembly of yeast U6 snRNP: a functional assay. Genes Dev., 3, 2137-2150.
30. Fabrizio, P., Esser, S., Kastner, B. and Lührmann, R. (1994) Isolation of S.cerevisiae snRNPs: comparison of U1 and U4/U6-U5 to their human counterparts. Science, 264, 261-265.
31. Frendewey, D. and Keller, W. (1985) Stepwise assembly of a pre-mRNA splicing complex requires U-snRNPs and specific intron sequences. Cell, 42, 355-367.
32. Fu, X.D. and Maniatis, T. (1992) The 35-kDa mammalian splicing factor SC35 mediates specific interactions between U1 and U2 small nuclear ribonucleoprotein particles at the 3′ splice site. Proc. Natl Acad. Sci. USA, 89, 1725-1729.
33. Gozani, O., Patton, J.G. and Reed, R. (1994) A novel set of spliceosome-associated proteins and the essential splicing factor PSF bind stably to pre-mRNA prior to catalytic step II of the splicing reaction. EMBO J., 13, 3356-3367.
34. Green, M.R. (1991) Biochemical mechanisms of constitutive and regulated pre-mRNA splicing. Annu. Rev. Cell Biol., 7, 559-599.
35. Guthrie, C. (1991) Messenger RNA splicing in yeast: clues to why the spliceosome is a ribonucleoprotein. Science, 253, 157-163.
36. Guthrie, C. and Fink, G.R. (1991) Guide to yeast genetics and molecular biology. Methods Enzymol., 194, 1-863.
37. Hardy, S.F. Grabowski, P.J., Padgett, R.A. and Sharp, P.A. (1984) Cofactor requirements of splicing of purified messenger RNA precursors. Nature, 308, 375-377.
38. Hashimoto, C. and Steitz, J.A. (1984) U4 and U6 RNAs coexist in a single small nuclear ribonucleoprotein particle. Nucleic Acids Res., 12, 3283-3293.
39. Hodges, P.E. and Beggs, J.D. (1994) RNA splicing. U2 fulfils a commitment. Curr. Biol., 4, 264-267.
40. Hughes, J.M., Konings, D.A. and Cesareni, G. (1987) The yeast homologue of U3 snRNA. EMBO J., 6, 2145-2155.
41. Ito, H., Fukuda, Y. Murata, K. and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol., 153, 163-168.
42. Johnston, M. and Davis, R.W. (1984) Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol. Cell. Biol., 4, 1440-1448.
43. Kandels-Lewis, S. and Séraphin, B. (1993) Involvement of U6 snRNA in 5′ splice site selection. Science, 262, 2035-2039.
44. Kaziro, Y. (1978) The role of guanosine 5′-triphosphate in polypeptide chain elongation. Biochim. Biophys. Acta, 505, 95-127.
45. King, D.S. and Beggs, J.D. (1990) Interactions of PRP2 protein with pre-mRNA splicing complexes in Saccharomyces cerevisiae. Nucleic Acids Res., 18, 6559-6564.
46. Kjeldgaard, M., Nissen, P., Thirup, S. and Nyborg, J. (1993) The crystal structure of elongation factor EF-Tu from Thermus aquaticus in the GTP conformation. Structure, 1, 35-50.
47. Krainer, A.R., Maniatis, T., Ruskin, B. and Green, M.R. (1984) Normal and mutant human beta-globin pre-mRNAs are faithfully and efficiently spliced in vitro. Cell, 36, 993-1005.
48. Krämer, A. (1992) Purification of splicing factor SF1, a heat-stable protein that functions in the assembly of a presplicins complex. Mol. Cell. Biol., 12, 4545-4552.
49. Krämer, A. (1995) The biochemistry of pre-mRNA splicing. In Lamond,A.I. (ed.), Pre-mRNA Processing. R.G. Landes Co., TX, pp. 35-64.
50. 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.
51. Laggerbauer, B., Lauber, J. and Lührmann, R. (1996) Identification of an RNA-dependent ATPase activity in mammalian U5 snRNPs. Nucleic Acids Res., 24, 868-875.
52. Lamm, G.M. and Lamond, A.I. (1993) Non-snRNP protein splicing factors. Biochim. Biophys. Acta, 1173, 247-265.
53. Lamond, A.I. and Carmo-Fonseca, M. (1993) Localization of splicing snRNPs in mammalian cells. Mol. Biol. Rep., 18, 127-133.
54. Lauber, J., Fabrizio, P. Teigelkamp, S., Lane, W.S., Hartmann, E. and Lührmann, R. (1996) The HeLa 200 kDa U5 snRNP-specific protein and its homolog in Saccharomyces cerevisiae are members of the DEXH-box protein family of putative RNA helicases. EMBO J., 15, 4001-1015.
55. Lerner, E.A., Lerner, M.R., Janeway, C. and Steitz, J.A. (1981) Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc. Natl Acad. Sci. USA, 78, 2737-2741.
56. Lesser, C.F. and Guthrie, C. (1993) Mutations in U6 snRNA that alter splice site specificity: implications for the active site. Science, 262, 1982-1988.
57. Lin, J. and Rossi, J.J. (1996) Identification and characterization of yeast mutants that overcome an experimentally introduced block to splicing at the 3′ splice site. RNA, 2, 835-848.
58. Madhani, H.D. and Guthrie, C. (1992) A novel base-pairing interaction between U2 and U6 snRNAs suggests a mechanism for the catalytic activation of the spliceosome. Cell, 71, 803-817.
59. Madhani, H.D. and Guthrie, C. (1994) Dynamic RNA-RNA interactions in the spliceosome. Annu. Rev. Genet., 28, 1-26.
60. 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 Arkins,J.F. (eds), The RNA World. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 303-357.
61. Myslinski, E., Segault, V. and Branlant, C. (1990) An intron in the genes for U3 small nucleolar RNAs of the yeast Saccharomyces cerevisiae. Science, 247, 1213-1216.
62. 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.
63. Newman, A. and Norman, C. (1991) Mutations in yeast U5 snRNA alter the specificity of 5′ splice-site cleavage. Cell, 65, 115-123.
64. Nierhaus, K.H., Adlung, R., Hausner, T.-P., Schilling-Bartetzko, S., Twardowski, T. and Triana, F. (1993) The allosteric three sites model and the mechanism of action of both elongation factors EF-Tu and EF-G. In Nierhaus,K.H., Franceschi,F., Subramanian,A.R., Erdmann,V.A. and Wittman-Liebold,B. (eds), The Translational Apparatus. Plenum Press, New York, pp. 273-284.
65. Nilsen, T.W. (1994) RNA-RNA interactions in the spliceosome: unraveling the ties that bind. Cell, 78, 1-4.
66. Nissen, P., Kjeldgaard, M., Thirup, S., Polekhina, G., Reshetnikova, L., Clark, B.F. and Nyborg, J. (1995) Crystal structure of the ternary complex of Phe-tRNAPhe, EF-Tu and a GTP analog. Science, 270, 1464-1472.
67. Noble, S.M. and Guthrie, C. (1996) Identification of novel genes required for yeast pre-mRNA splicing by means of cold-sensitive mutations. Genetics, 143, 67-80.
68. Noller, H.F., Moazed, D., Stern, S., Powers, T., Allen, P.N., Robertson, J.M., Weiser, B. and Triman, K. (1990) Structure of rRNA and its functional interactions in translation. In Hill,W.E., Dahlberg,A., Garrett,R.A., Moore,P.B., Schlessinger,D. and Warner,J.R. (eds), The Ribosome, Structure, Function and Evolution. American Society for Microbiology Press, Washington DC, pp. 73-92.
69. Nomura, N. et al. (1994) Prediction of the coding sequences of unidentified human genes. I. The coding sequences of 40 new genes (KIAA0001-KIAA0040) deduced by analysis of randomly sampled cDNA clones from human immature myeloid cell line KG-1. DNA Res., 1, 27-35.
70. Reed, R. (1996) Initial splice-site recognition and pairing during pre-mRNA splicing. Curr. Opin. Genet. Dev., 6, 215-220.
71. Rinke, J., Appel, B., Digweed, M. and Lührmann, R. (1985) Localization of a base-paired interaction between small nuclear RNAs U4 and U6 in intact U4/U6 ribonucleoprotein particles by psoralen cross-linking. J. Mol. Biol., 185, 721-731.
72. Rodnina, M.V., Savelsbergh, A., Katunin, V.I. and Wintermeyer, W. (1997) Hydrolysis of GTP by elongation factor G drives tRNA movement on the ribosome. Nature, 385, 37-41.
73. Rymond, B.C. and Rosbash, M. (1992) Yeast pre-mRNA splicing. In Jones,E.W., Pringle,J.R. and Broach, J.R. (eds), The Molecular and Cellular Biology of the Yeast Saccharomyces. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 143-192.
74. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
75. Saraste, M., Sibbald, P.R. and Wittinghofer, A. (1990) The P-loop a common motif in ATP- and GTP-binding proteins. Trends Biochem. Sci., 15, 430-434.
76. Sawa, H. and Abelson, J. (1992) Evidence for a base-pairing interaction between U6 small nuclear RNA and 5′ splice site during the splicing reaction in yeast. Proc. Natl Acad. Sci. USA, 89, 11269-11273.
77. Scherer, S. and Davis, R.W. (1979) Replacement of chromosome segments with altered DNA sequences costructed in vitro. Proc. Natl Acad. Sci. USA, 76, 4951-4955.
78. Schmid, S.R. and Linder, P. (1992) D-E-A-D protein family of putative RNA helicases. Mol. Microbiol. 6, 283-291.
79. Sikorski, R.S. and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics, 122, 19-27.
80. Sontheimer, E.J. and Steitz, J.A. (1993) The U5 and U6 small nuclear RNAs as active site components of the spliceosome. Science, 262, 1989-1996.
81. Strauss, E.J. and Guthrie, C. (1991) A cold-sensitive mRNA splicing mutant is a member of the RNA helicase gene family. Genes Dev., 5, 629-641.
82. Sun, J.S. and Manley, J.L. (1995) A novel U2-U6 snRNA structure is necessary for mammalian mRNA splicing. Genes Dev., 9, 843-854.
83. Utans, U., Behrens, S.E., Lührmann, R., Kole, R. and Krämer, A. (1992) A splicing factor that is inactivated during in vivo heat shock is functionally equivalent to the [U4/U6·U5] triple snRNP-specific proteins. Genes Dev., 6, 631-641.
84. Vijayraghavan, U., Company, M. and Abelson, J. (1989) Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae. Genes Dev., 3, 1206-1216.
85. Walker, J.E., Saraste, M., Runswick, M.J. and Gay, N.J. (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J., 1, 945-951.
86. Wassarman, D.A. and Steitz, J.A. (1991) RNA splicing. Alive with DEAD proteins. Nature, 349, 463-464.
87. Will, C.L., Fabrizio, P. and Lührmann, R. (1995) Nuclear pre-mRNA splicing. In Eckstein,F. and Lilley,D.M.J. (eds), Nucleic Acids and Molecular Biology. Springer Verlag, Berlin, pp. 342-372.
88. Wilson, R. et al. (1994) 2.2 Mb of contiguous nucleotide sequence from chromosome III of C.elegans. Nature, 368, 32-38.
89. Wu, J.A. and Manley, J.L. (1991) Base pairing between U2 and U6 snRNAs is necessary for splicing of a mammalian pre-mRNA. Nature, 352, 818-821.
90. Wyatt, J.R., Sontheimer, E.J. and Steitz, J.A. (1992) Site-specific cross-linking of mammalian U5 snRNP to the 5′ splice site before the first step of pre-mRNA splicing. Genes Dev., 6, 2542-2553.
91. Xu, D., Nouraini, S., Field, D., Tang, S.-J. and Friesen, J.D. (1996) An RNA-dependent ATPase associated with U2/U6 snRNAs in pre-mRNA splicing. Nature, 381, 709-713.
92. 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.
93. 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.