Evidence that U5 snRNP recognizes the 3' splice site for catalytic step II in mammals

EMBO Journal

Volumn 16, Issue 15, 1997, Pages 4746-4759

  Chiara, Maria Dolores ^a,b   Palandjian, Leon ^a   Kramer, Rebecca Feld ^a   Reed, Robin ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

3' splice site; Spliceosome; Splicing; U5 snRNP

Indexed keywords

DINUCLEOTIDE; MESSENGER RNA PRECURSOR; PYRIMIDINE; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DNA BINDING; PROTEIN RNA BINDING; RNA SEQUENCE; RNA SPLICING; SPLICEOSOME;

ANIMALS; BASE SEQUENCE; BINDING SITES; CROSS-LINKING REAGENTS; KINETICS; MAMMALS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RIBONUCLEOPROTEIN, U5 SMALL NUCLEAR; RNA PRECURSORS; RNA SPLICING; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SPLICEOSOMES;

ANIMALIA; MAMMALIA;

EID: 0030750730     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.15.4746     Document Type: Article

References (60)

1. Adams, M.D., Rudner, D.Z. and Rio, D.C. (1996) Biochemistry and regulation of pre-mRNA splicing. Curr. Opin. Cell Biol., 8, 331-339.
2. Bach, M., Winkelmann, G. and Luhrmann, R. (1989) 20S small nuclear ribonucleoprotein U5 shows a surprisingly complex protein composition. Proc. Natl Acad. Sci. USA, 86, 6038-6042.
3. Behrens, S.E. and Luhrmann, R. (1991) Immunoaffinity purification of a [U4/U6.U5] tri-snRNP from human cells. Genes Dev., 5, 1439-1452.
4. Bennett, M., Michaud, S., Kingston, J. and Reed, R. (1992) Protein components specifically associated with prespliceosome and spliceosome complexes. Genes Dev., 6, 1986-2000.
5. Billings, P.B., Allen, R.W., Jensen, F.C. and Hoch, S.O. (1982) Anti-RNP monoclonal antibodies derived from a mouse strain with lupus-like autoimmunity. J. Immunol., 128, 1176-1180.
6. Byrs, A. and Schwer, B. (1996) Requirement for SLU7 in yeast pre-mRNA splicing is dictated by the distance between the branchpoint and 3′ splice site. RNA, 2, 707-717.
7. 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.
8. Chiara, M.D., Gozani, O., Bennett, M., Champion-Arnaud, P., Palandjian, L. and Reed, R. (1996) Identification of proteins that interact with Exon sequences, splice sites, and the branchpoint sequence during each stage of spliceosome assembly. Mol. Cell. Biol., 16, 3317-3326.
9. 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.
10. Frank, D. and Guthrie, C. (1992) An essential splicing factor, SLU7, mediates 3′ splice site choice in yeast. Genes Dev., 6, 2112-2124.
11. Frank, D., Patterson, B. and Guthrie, C. (1992) Synthetic lethal mutations suggest interactions between U5 small nuclear RNA and four proteins required for the second step of splicing. Mol. Cell. Biol., 12, 5197-5205.
12. 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.
13. 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.
14. Horowitz, D.S. and Krainer, A.R. (1997) A human protein required for the second step is functionally related to a yeast splicing factor. Genes Dev., 11, 139-151.
15. Kandels-Lewis, S. and Seraphin, B. (1993) Role of U6 snRNA in 5′ splice site selection. Science, 262, 2035-2039.
16. Kramer, A. (1996) The structure and function of proteins involved in mammalian pre-mRNA splicing. Annu. Rev. Biochem., 65, 367-409.
17. Lamm, G.M., Blencowe, B.J., Sproat, B.S., Iribarren, A.M., Ryder, U. and Lamond, A.I. (1991) Antisense probes containing 2-aminoadenosine allow efficient depletion of U5 snRNP from HeLa splicing extracts. Nucleic Acids Res., 19, 3193-3198.
18. Lauber, J., Fabrizio, P., Teigelkamp, S., Lane, W.S., Hartmann, E. and Luhrmann, R. (1996) The HeLa 200 kDa U5 snRNP-specific protein and its homologue in Saccharomyces cerevisiae are members of the DEXH-box protein family of putative RNA helicases. EMBO J., 15, 4001-4015.
19. 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.
20. Lossky, M., Anderson, G.J., Jackson, S.P. and Beggs, J. (1987) Identification of a yeast snRNP protein and detection of snRNP-snRNP interactions. Cell, 51, 1019-1026.
21. Luukkonen, B.G.M. and Seraphin, B. (1997) The roles of branchpoint-3′ splice site spacing and interaction between intron terminal nucleotides in 3′ splice site selection in Saccharomyces cerevisiae. EMBO J., 16, 779-792.
22. Madhani, H.D. and Guthrie, C. (1994) Dynamic RNA-RNA interactions in the spliceosome. Annu. Rev. Genet., 28, 1-26.
23. Michaud, S. and Reed, R. (1993) A functional association between the 5′ and 3′ splice site is established in the earliest prespliceosome complex (E) in mammals. Genes Dev., 7, 1008-1020.
24. Moore, M.J. and Sharp, P.A. (1992) Site-specific modification of pre-mRNA: the 2′-hydroxyl groups at the splice sites. Science, 256, 992-997.
25. Neugebauer, K.M., Stolk, J.A. and Roth, M.B. (1995) A conserved epitope on a subset of SR proteins defines a larger family of pre-mRNA splicing factors. J. Cell Biol., 129, 899-908.
26. Newman, A.J. (1994) Pre-mRNA splicing. Curr. Opin. Genet. Dev., 4, 298-304.
27. Newman, A. and Norman, C. (1991) Mutations in yeast U5 snRNA alter the specificity of 5′ splice-site cleavage. Cell, 65, 115-123.
28. Newman, A.J. and Norman, C. (1992) U5 snRNA interacts with exon sequences at 5′ and 3′ splice sites. Cell, 68, 743-754.
29. Newman, A.J., Teigelkamp, S. and Beggs, J.D. (1995) snRNA interactions at 5′ and 3′ splice sites monitored by photoactivated crosslinking in yeast spliceosomes. RNA, 1, 968-980.
30. Nilsen, T.W. (1994) RNA-RNA interactions in the spliceosome: unraveling the ties that bind. Cell, 78, 1-4.
31. 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.
32. O'Keefe, R.T., Norman, C. and Newman, A.J. (1996) The invariant U5 snRNA loop I sequence is dispensable for the first catalytic step of pre-mRNA splicing in yeast. Cell, 86, 679-689.
33. Parker, R., Siliciano, P.G. and Guthrie, C. (1987) Recognition of the TACTAAC box during mRNA splicing in yeast involves base pairing to the U2-like snRNA. Cell, 49, 229-239.
34. Patterson, B. and Guthrie, C. (1991) A U-rich tract enhances usage of an alternative 3′ splice site in yeast. Cell, 64, 181-187.
35. Patton, J.G, Porro, E.B., Galceran, J., Tempst, P. and Nadal-Ginard, B. (1993) Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes Dev., 7, 393-406.
36. Reed, R. (1989) The organization of 3′ splice-site sequences in mammalian introns. Genes Dev., 3, 2113-2123.
37. Reed, R. (1996) Initial splice-site recognition and pairing during premRNA splicing. Curr. Opin. Genet. Dev., 6, 215-220.
38. 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.
39. Sawa, H. and Shimura, Y. (1992) Association of U6 snRNA with the 5′-splice site region of pre-mRNA in the spliceosome. Genes Dev., 6, 244-254.
40. Scadden, A.D.J. and Smith, C.W.J. (1995) Interactions between the terminal bases of mammalian introns are retained in inosine-containing pre-mRNAs. EMBO J., 14, 3236-3246.
41. Seraphin, B., Abovich, N. and Rosbash, M. (1991) Genetic depletion indicates a late role for U5 snRNP during in vitro spliceosome assembly. Nucleic Acids Res., 19, 3857-3860.
42. Smith, C.W., Porro, E.B., Patton, J.G. and Nadal-Ginard, B. (1989) Scanning from an independently specified branch point defines the 3′ splice site of mammalian introns. Nature, 342, 243-247.
43. Smith, C.W., Chu, T.T. and Nadal-Ginard, B. (1993) Scanning and competition between AGs are involved in 3′ splice site selection in mammalian introns. Mol. Cell. Biol., 13, 4939-4952.
44. 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.
45. Spritz, R.A., Strunk, K., Surowy, C.S., Hoch, S.O., Barton, D.E. and Franke, U. (1987) The human U1-70K snRNP protein: cDNA cloning, chromosomal localization, expression, alternative splicing and RNA-binding. Nucleic Acids Res., 15, 10373-10390.
46. 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.
47. 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.
48. Teigelkamp, S., Newman, A.J. and Beggs, J.D. (1995) Extensive interactions of PRP8 protein with the 5′ and 3′ splice sites during splicing suggest a role in stabilization of exon alignment by U5 snRNA. EMBO J., 14, 2602-2612.
49. Umen, J.G. and Guthrie, C. (1995a) The second catalytic step of pre-mRNA splicing. RNA, 1, 869-885.
50. Umen, J.G. and Guthrie, C. (1995b) A novel role for a U5 snRNP protein in 3′ splice site selection. Genes Dev., 9, 855-868.
51. Umen, J.G. and Guthrie, C. (1995c) Prp16p, Slu7p, and Prp8p interact with the 3′ splice site in two distinct stages during the second catalytic step of pre-mRNA splicing. RNA, 1, 584-597.
52. Umen, J.G. and Guthrie, C. (1996) Mutagenesis of the yeast gene PRP8 reveals domains governing the specificity and fidelity of 3′ splice site selection. Genetics, 143, 723-739.
53. Wassarman, D.A. and Steitz, J.A. (1992) Interactions of small nuclear RNAs with precursor messenger RNA during in vitro splicing. Science, 257, 1918-1925.
54. Whittaker, E., Lossky, M. and Beggs, J.D. (1990) Affinity purification of spliceosomes reveals that the precursor RNA processing protein PRP8, a protein in the U5 small nuclear ribonucleoprotein particle, is a component of yeast spliceosome. Proc. Natl Acad. Sci. USA, 87, 2216-2219.
55. Winkelmann, G., Bach, M. and Luhrmann, R. (1989) Evidence from complementation assays in vitro that U5 snRNP is required for both steps of mRNA splicing. EMBO J., 8, 3105-3112.
56. Wu, J. and Manley, J.L. (1989) Mammalian pre-mRNA branch site selection by U2 snRNP involves base pairing. Genes Dev., 3, 1553-1561.
57. 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.
58. Xu, D., Nouraini, S., Field, D., Tang, S. and Friesen, J.D. (1996) An RNA-dependent ATPase associated with U2/U6 snRNAs in pre-mRNA splicing. Nature, 381, 709-713.
59. Zamore, P.D. and Green, M.R. (1989) Identification, purification, and biochemical characterization of U2 small nuclear ribonucleoprotein auxiliary factor. Proc. Natl Acad. Sci. USA, 86, 9243-9247.
60. Zhuang, Y. and Weiner, A.M. (1989) A compensatory base change in human U2 snRNA can suppress a branch site mutation. Genes Dev., 3, 1545-1552.