U2 snRNA-protein contacts in purified human 17S U2 snRNPs and in spliceosomal A and B complexes

Molecular and Cellular Biology

Volumn 26, Issue 7, 2006, Pages 2803-2816

  Dybkov, Olexandr ^a   Will, Cindy L ^a   Deckert, Jochen ^a   Behzadnia, Nastaran ^a   Hartmuth, Klaus ^a   Lührmann, Reinhard ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; LEAD; MESSENGER RNA; MESSENGER RNA PRECURSOR; PROTEIN SM; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA;

ANTIBODY AFFINITY; ARTICLE; CONTROLLED STUDY; CROSS LINKING; HELA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA CLEAVAGE; RNA SPLICING; SPLICEOSOME; ULTRAVIOLET RADIATION;

CROSS-LINKING REAGENTS; HUMANS; LEAD; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RIBONUCLEOPROTEIN, U2 SMALL NUCLEAR; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, SMALL NUCLEAR; RNA, SPLICED LEADER; RNA-BINDING PROTEINS; SPLICEOSOMES; ULTRAVIOLET RAYS;

EID: 33645212088     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.7.2803-2816.2006     Document Type: Article

References (57)

1. Ares, M., Jr., and A. H. Igel. 1990. Lethal and temperature-sensitive mutations and their suppressors identify an essential structural element in U2 small nuclear RNA. Genes Dev. 4:2132-2145.
2. Behrens, S. E., K. Tyc, B. Kastner, J. Reichelt, and R. Lührmann. 1993. Small nuclear ribonucleoprotein (RNP) U2 contains numerous additional proteins and has a bipartite RNP structure under splicing conditions. Mol. Cell. Biol. 13:307-319.
3. Brosi, R., K. Gröning, S. E. Behrens, R. Lührmann, and A. Krämer. 1993. Interaction of mammalian splicing factor SF3a with U2 snRNP and relation of its 60-kD subunit to yeast PRP9. Science 262:102-105.
4. Brunel, C., and P. Romby. 2000. Probing RNA structure and RNA-ligand complexes with chemical probes. Methods Enzymol. 318:3-21.
5. Caspary, F., A. Shevchenko, M. Wilm, and B. Séraphin. 1999. Partial purification of the yeast U2 snRNP reveals a novel yeast pre-mRNA splicing factor required for pre-spliceosome assembly. EMBO J. 18:3463-3474.
6. Champion-Arnaud, P., and R. Reed. 1994. The prespliceosome components SAP 49 and SAP 145 interact in a complex implicated in tethering U2 snRNP to the branch site. Genes Dev. 8:1974-1983.
7. Chiara, M. D., P. Champion-Arnaud, M. Buvoli, B. Nadal-Ginard, and R. Reed. 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.
8. Das, B. K., L. Xia, L. Palandjian, O. Gozani, Y. Chyung, and R. Reed. 1999. Characterization of a protein complex containing spliceosomal proteins SAPs 49, 130, 145, and 155. Mol. Cell. Biol. 19:6796-6802.
9. Das, R., Z. Zhou, and R. Reed. 2000. Functional association of U2 snRNP with the ATP-independent spliceosomal complex E. Mol. Cell 5:779-787.
10. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
11. Dönmez, G., K. Hartmuth, and R. Lührmann. 2004. Modified nucleotides at the 5′ end of human U2 snRNA are required for spliceosomal E-complex formation. RNA 10:1925-1933.
12. Dziembowski, A., A. P. Ventura, B. Rutz, F. Caspary, C. Faux, F. Halgand, O. Laprévote, and B. Séraphin. 2004. Proteomic analysis identifies a new complex required for nuclear pre-mRNA retention and splicing. EMBO J. 23:4847-4856.
13. Golas, M. M., B. Sander, C. L. Will, R. Lührmann, and H. Stark. 2003. Molecular architecture of the multiprotein splicing factor SF3b. Science 300:980-984.
14. Golas, M. M., B. Sander, C. L. Will, R. Lührmann, and H. Stark. 2005. Major conformational change in the complex SF3b upon integration into the spliceosomal U31/U12 di-snRNP as revealed by electron cryomicroscopy. Mol. Cell 17:869-883.
15. Gozani, O., R. Feld, and R. Reed. 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.
16. Gozani, O., J. Potashkin, and R. Reed. 1998. A potential role for U2AF-SAP 155 interactions in recruiting U2 snRNP to the branch site. Mol. Cell. Biol. 18:4752-4760.
17. Hartmuth, K., V. A. Raker, J. Huber, C. Branlant, and R. Lührmann. 1999. An unusual chemical reactivity of Sm site adenosines strongly correlates with proper assembly of core U snRNP particles. J. Mol. Biol. 285:133-147.
18. Hartmuth, K., H. Urlaub, H.-P. Vornlocher, C. L. Will, M. Gentzel, M. Wilm, and R. Lührmann. 2002. Protein composition of human prespliceosomes isolated by a tobramycin affinity-selection method. Proc. Natl. Acad. Sci. USA 99:16719-16724.
19. Hausner, T. P., L. M. Giglio, and A. M. Weiner. 1990. Evidence for base-pairing between mammalian U2 and U6 small nuclear ribonucleoprotein particles. Genes Dev. 4:2146-2156.
20. Heinrichs, V., W. Hackl, and R. Lührmann. 1992. Direct binding of small nuclear ribonucleoprotein G to the Sm site of small nuclear RNA. Ultraviolet light cross-linking of protein G to the AAU stretch within the Sm site (AAUUUGUGG) of U1 small nuclear ribonucleoprotein reconstituted in vitro. J. Mol. Biol. 227:15-28.
21. Hermann, H., P. Fabrizio, V. A. Raker, K. Foulaki, H. Hornig, H. Brahms, and R. Lührmann. 1995. snRNP Sm proteins share two evolutionary conserved sequence motifs which are involved in Sm protein-protein interactions. EMBO J. 14:2076-2088.
22. Igel, H., S. Wells, R. Perriman, and M. Ares, Jr. 1998. Conservation of structure and subunit interactions in yeast homologues of splicing factor 3b (SF3b) subunits. RNA 4:1-10.
23. Kambach, C., S. Walke, R. Young, J. M. Avis, E. de la Fortelle, V. A. Raker, R. Lührmann, J. Li, and K. Nagai. 1999. Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs. Cell 96:375-387.
24. Krämer, A., F. Mulhauser, C. Wersig, K. Gröning, and G. Bilbe. 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.
25. Krämer, A., P. Grüter, K. Gröning, and B. Kastner. 1999. Combined biochemical and electron microscopic analyses reveal the architecture of the mammalian U2 snRNP. J. Cell Biol. 145:1355-1368.
26. MacMillan, A. M., C. C. Query, C. R. Allerson, S. Chen, G. L. Verdine, and P. A. Sharp. 1994. Dynamic association of proteins with the pre-mRNA branch region. Genes Dev. 8:3008-3020.
27. Madhani, H. D., and C. Guthrie. 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.
28. Makarova, O. V., E. M. Makarov, H. Urlaub, C. L. Will, M. Gentzel, M. Wilm, and R. Lührmann. 2004. A subset of human 35S U5 proteins, including Prp19, function prior to catalytic step 1 of splicing. EMBO J. 23:2381-2391.
29. Moore, M. J., and P. A. Sharp. 1992. Site-specific modification of pre-mRNA: the 2′-hydroxyl groups at the splice sites. Science 256:992-997.
30. Nesic, D., and A. Krämer. 2001. Domains in human splicing factors SF3a60 and SF3a66 required for binding to SF3a120, assembly of the 17S U2 snRNP, and prespliceosome formation. Mol. Cell. Biol. 21:6406-6417.
31. Nilsen, T. W. 1998. RNA-RNA interactions in nuclear pre-mRNA splicing, p. 279-307. In R. W. Simons and M. Grunberg-Manago (ed.), RNA structure and function. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
32. Patel, A. A., and J. A. Steitz. 2003. Splicing double: insights from the second spliceosome. Nat. Rev. Mol. Cell Biol. 4:960-970.
33. Price, S. R., P. R. Evans, and K. Nagai. 1998. Crystal structure of the spliceosomal U2B″-U2A′ protein complex bound to a fragment of U2 small nuclear RNA. Nature 394:645-650.
34. Pruijn, G. J. M., F. Scheute, J. P. H. Thijssen, R. J. T. Smeenk, and W. J. van Venrooij. 1997. Mapping of SLE-specific Sm B cell epitopes using murine monoclonal antibodies. J. Autoimmun. 10:127-136.
35. Query, C. C., M. J. Moore, and P. A. Sharp. 1994. Branch nucleophile selection in pre-mRNA splicing: evidence for the bulged duplex model. Genes Dev. 8:587-597.
36. Query, C. C., S. A. Strobel, and P. A. Sharp. 1996. Three recognition events at the branch-site adenine. EMBO J. 15:1392-1402.
37. Ruby, S. W., T. H. Chang, and J. Abelson. 1993. Four yeast spliceosomal proteins (PRP5, PRP9, PRP11, and PRP21) interact to promote U2 snRNP binding to pre-mRNA. Genes Dev. 7:1909-1925.
38. Ségault, V., C. L. Will, B. S. Sproat, and R. Lührmann. 1995. In vitro reconstitution of mammalian U2 and U5 snRNPs active in splicing: Sm proteins are functionally interchangeable and are essential for the formation of functional U2 and U5 snRNPs. EMBO J. 14:4010-4021.
39. Spadaccini, R., U. Reidt, O. Dybkov, C. L. Will, R. Frank, G. Stier, L. Corsini, M.C. Wahl, R. Lührmann, and M. Sattler. Biochemical and NMR analyses of an SF3b155-p14-U2AF-RNA interaction network involved in branch point definition during pre-mRNA splicing. RNA, in press.
40. Staknis, D., and R. Reed. 1994. Direct interactions between pre-mRNA and six U2 small nuclear ribonucleoproteins during spliceosome assembly. Mol. Cell. Biol. 14:2994-3005.
41. Staley, J. P., and C. Guthrie. 1998. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92:315-326.
42. Sun, J. S., and J. L. Manley. 1995. A novel U2-U6 snRNA structure is necessary for mammalian mRNA splicing. Genes Dev. 9:843-854.
43. Tanaka, Y., A. Ohta, K. Terashima, and H. Sakamoto. 1997. Polycistronic expression and RNA-binding specificity of the C. elegans homologue of the spliceosome-associated protein SAP49. J. Biochem. (Tokyo) 121:739-745.
44. Urlaub, H., K. Hartmuth, S. Kostka, G. Grelle, and R. Lührmann. 2000. A general approach for identification of RNA-protein cross-linking sites within native human spliceosomal small nuclear ribonucleoproteins (snRNPs). Analysis of RNA-protein contacts in native U1 and U4/U6-U5 snRNPs. J. Biol. Chem. 275:41458-41468.
45. Urlaub, H., V. A. Raker, S. Kostka, and R. Lührmann. 2001. Sm protein-Sm site RNA interactions within the inner ring of the spliceosomal snRNP core structure. EMBO J. 20:187-196.
46. Varani, G., and K. Nagai. 1998. RNA recognition by RNP proteins during RNA processing. Annu. Rev. Biophys. Biomol. Struct. 27:407-445.
47. Wang, Q., and B. C. Rymond. 2003. Rds3p is required for stable U2 snRNP recruitment to the splicing apparatus. Mol. Cell. Biol. 23:7339-7349.
48. Wells, S. E., and M. Ares, Jr. 1994. Interactions between highly conserved U2 small nuclear RNA structures and Prp5p, Prp9p, Prp11p, and Prp21p proteins are required to ensure integrity of the U2 small nuclear ribonucleoprotein in Saccharomyces cerevisiae. Mol. Cell. Biol. 14:6337-6349.
49. Wells, S. E., M. Neville, M. Haynes, J. Wang, H. Igel, and M. Ares, 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.
50. Will, C. L., and R. Lührmann. 2001. Spliceosomal UsnRNP biogenesis, structure and function. Curr. Opin. Cell Biol. 13:290-301.
51. rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
52. Will, C. L., B. Kastner, and R. Lührmann. 1994. Analysis of ribonucleoprotein interactions, p. 141-177. In S. J. Higgins and B. D. Harnes (ed.), RNA processing: a practical approach, vol. 1. IRL Press, Oxford, United Kingdom.
53. Will, C. L., C. Schneider, A. M. MacMillan, N. F. Katopodis, G. Neubauer, M. Wilm, R. Lührmann, and C. C. Query. 2001. A novel U2 and U11/U12 snRNP protein that associates with the pre-mRNA branch site. EMBO J. 20:4536-4546.
54. Will, C. L., C. Schneider, R. Reed, and R. Luhrmann. 1999. Identification of both shared and distinct proteins in the major and minor spliceosomes. Science 284:2003-2005.
55. Will, C. L., H. Urlaub, T. Achsel, M. Gentzel, M. Wilm, and R. Lührmann. 2002. Characterization of novel SF3b and 17S U2 snRNP proteins, including a human Prp5p homologue and an SF3b DEAD-box protein. EMBO J. 21:4978.
56. Wu, J., and J. L. Manley. 1992. Multiple functional domains of human U2 small nuclear RNA: strengthening conserved stem I can block splicing. Mol. Cell. Biol. 12:5464-5473.
57. Yan, D. and M. Ares, Jr. 1996. Invariant U2 RNA sequences bordering the branchpoint recognition region are essential for interaction with yeast SF3a and SF3b subunits. Mol. Cell. Biol. 16:818-828.