Structure of yeast U6 snRNPs: Arrangement of Prp24p and the LSm complex as revealed by electron microscopy

RNA

Volumn 14, Issue 12, 2008, Pages 2528-2537

  Karaduman, Ramazan ^a   Dube, Prakash ^a   Stark, Holger ^a,b   Fabrizio, Patrizia ^a   Kastner, Berthold ^a   Lührmann, Reinhard ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Cross linking; Electron microscopy; LSm tagging; U6 snRNP

Indexed keywords

LSM PROTEIN; PROTEIN TAG; PRP24P PROTEIN; RNA; SMALL NUCLEAR RIBONUCLEOPROTEIN; U6 SMALL NUCLEAR RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ARTICLE; CENTRIFUGATION; CROSS LINKING; ELECTRON MICROSCOPY; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; YEAST;

BASE SEQUENCE; MOLECULAR SEQUENCE DATA; RIBONUCLEOPROTEIN, U4-U6 SMALL NUCLEAR; RNA, FUNGAL; RNA, SMALL NUCLEAR; SACCHAROMYCES CEREVISIAE;

EID: 57049106296     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1369808     Document Type: Article

References (37)

1. Achsel, T., Brahms, H., Kastner, B., Bachi, A., Wilm, M., and Luhrmann, R. 1999. A doughnut-shaped heteromer of human Sm-like proteins binds to the 3′-end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro. EMBO J. 18: 5789-5802.
2. Bae, E., Reiter, N.J., Bingman, C.A., Kwan, S.S., Lee, D., Phillips Jr., G.N., Butcher, S.E., and Brow, D.A. 2007. Structure and interactions of the first three RNA recognition motifs of splicing factor prp24. J. Mol. Biol. 367: 1447-1458.
3. Bell, M., Schreiner, S., Damianov, A., Reddy, R., and Bindereif, A. 2002. p110, a novel human U6 snRNP protein and U4/U6 snRNP recycling factor. EMBO J. 21: 2724-2735.
4. Brow, D.A. 2002. Allosteric cascade of spliceosome activation. Annu. Rev. Genet. 36: 333-360.
5. Brow, D.A. and Guthrie, C. 1988. Spliceosomal RNA U6 is remarkably conserved from yeast to mammals. Nature 334: 213-218.
6. Brow, D.A. and Vidaver, R.M. 1995. An element in human U6 RNA destabilizes the U4/U6 spliceosomal RNA complex. RNA 1: 122-131.
7. Burge, C.B., Tuschl, T., and Sharp, P.A. 1999. Splicing of precursors to mRNAs by the spliceosomes. In The RNA world II (eds. R.F. Gesteland et al.), pp. 525-560. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
8. Dube, P., Tavares, P., Lurz, R., and van Heel, M. 1993. The portal protein of bacteriophage SPP1: A DNA pump with 13-fold symmetry. EMBO J. 12: 1303-1309.
9. Fortner, D.M., Troy, R.G., and Brow, D.A. 1994. A stem/loop in U6 RNA defines a conformational switch required for pre-mRNA splicing. Genes & Dev. 8: 221-233.
10. Fromont-Racine, M., Mayes, A.E., Brunet-Simon, A., Rain, J.C., Colley, A., Dix, I., Decourty, L., Joly, N., Ricard, F., Beggs, J.D., et al. 2000. Genome-wide protein interaction screens reveal functional networks involving Sm-like proteins. Yeast 17: 95-110.
11. Ghetti, A., Company, M., and Abelson, J. 1995. Specificity of Prp24 binding to RNA: A role for Prp24 in the dynamic interaction of U4 and U6 snRNAs. RNA 1: 132-145.
12. Hermann, H., Fabrizio, P., Raker, V.A., Foulaki, K., Hornig, H., Brahms, H., and Luhrmann, R. 1995. snRNP Sm proteins share two evolutionarily conserved sequence motifs which are involved in Sm protein-protein interactions. EMBO J. 14: 2076-2088.
13. Jurica, M.S. and Moore, M.J. 2003. Pre-mRNA splicing: Awash in a sea of proteins. Mol. Cell 12: 5-14.
14. Kambach, C., Walke, S., Young, R., Avis, J.M., de la Fortelle, E., Raker, V.A., Luhrmann, R., Li, J., and Nagai, K. 1999. Crystal structures of two Sm protein complexes and their implications for the assembly of the spliceosomal snRNPs. Cell 96: 375-387.
15. Karaduman, R., Fabrizio, P., Hartmuth, K., Urlaub, H., and Luhrmann, R. 2006. RNA structure and RNA-protein interactions in purified yeast U6 snRNPs. J. Mol. Biol. 356: 1248-1262.
16. Kastner, B., Bach, M., and Luhrmann, R. 1990. Electron microscopy of small nuclear ribonucleoprotein (snRNP) particles U2 and U5: Evidence for a common structure-determining principle in the major U snRNP family. Proc. Natl. Acad. Sci. 87: 1710-1714.
17. Kastner, B., Fischer, N., Golas, M.M., Sander, B., Dube, P., Boehringer, D., Hartmuth, K., Deckert, J., Hauer, F., Wolf, E., et al. 2008. GraFix: Sample preparation for single-particle electron cryomicroscopy. Nat. Methods 5: 53-55.
18. Kwan, S.S. and Brow, D.A. 2005. The N- and C-terminal RNA recognition motifs of splicing factor Prp24 have distinct functions in U6 RNA binding. RNA 11: 808-820.
19. Mura, C., Cascio, D., Sawaya, M.R., and Eisenberg, D.S. 2001. The crystal structure of a heptameric archaeal Sm protein: Implications for the eukaryotic snRNP core. Proc. Natl. Acad. Sci. 98: 5532-5537.
20. Nilsen, T.W. 2003. The spliceosome: The most complex macromolecular machine in the cell? Bioessays 25: 1147-1149.
21. Pannone, B.K., Do Kim, S., Noe, D.A., and Wolin, S.L. 2001. Multiple functional interactions between components of the Lsm2-Lsm8 complex, U6 snRNA, and the yeast La protein. Genetics 158: 187-196.
22. Puig, O., Caspary, F., Rigaut, G., Rutz, B., Bouveret, E., Bragado-Nilsson, E., Wilm, M., and Seraphin, B. 2001. The tandem affinity purification (TAP) method: A general procedure of protein complex purification. Methods 24: 218-229.
23. Rader, S.D. and Guthrie, C. 2002. A conserved Lsm-interaction motif in Prp24 required for efficient U4/U6 di-snRNP formation. RNA 8: 1378-1392.
24. Ryan, D.E., Stevens, S.W., and Abelson, J. 2002. The 5′ and 3′ domains of yeast U6 snRNA: Lsm proteins facilitate binding of Prp24 protein to the U6 telestem region. RNA 8: 1011-1033.
25. 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.
26. Shannon, K.W. and Guthrie, C. 1991. Suppressors of a U4 snRNA mutation define a novel U6 snRNP protein with RNA-binding motifs. Genes & Dev. 5: 773-785.
27. Sheff, M.A. and Thorn, K.S. 2004. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21: 661-670.
28. Staley, J.P. and Guthrie, C. 1998. Mechanical devices of the spliceosome: Motors, clocks, springs, and things. Cell 92: 315-326.
29. Stevens, S.W., Barta, I., Ge, H.Y., Moore, R.E., Young, M.K., Lee, T.D., and Abelson, J. 2001. Biochemical and genetic analyses of the U5, U6, and U4/U6 x U5 small nuclear ribonucleoproteins from Saccharomyces cerevisiae. RNA 7: 1543-1553.
30. van Heel, M. 1984. Multivariate statistical classification of noisy images (randomly oriented biological macromolecules). Ultramicroscopy 13: 165-183.
31. van Heel, M., Harauz, G., Orlova, E.V., Schmidt, R., and Schatz, M. 1996. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116: 17-24.
32. Verdone, L., Galardi, S., Page, D., and Beggs, J.D. 2004. Lsm proteins promote regeneration of pre-mRNA splicing activity. Curr. Biol. 14: 1487-1491.
33. Vidal, V.P., Verdone, L., Mayes, A.E., and Beggs, J.D. 1999. Characterization of U6 snRNA-protein interactions. RNA 5: 1470-1481.
34. Vidaver, R.M., Fortner, D.M., Loos-Austin, L.S., and Brow, D.A. 1999. Multiple functions of Saccharomyces cerevisiae splicing protein Prp24 in U6 RNA structural rearrangements. Genetics 153: 1205-1218.
35. Will, C.L. and Lührmann, R. 2006. Spliceosome structure and function. In RNA world III (eds. R.F. Gesteland et al.), pp. 369-400. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Wolff, T. and Bindereif, A. 1993. Conformational changes of U6 RNA during the spliceosome cycle: An intramolecular helix is essential both for initiating the U4-U6 interaction and for the first step of slicing. Genes & Dev. 7: 1377-1389.
37. Zaric, B., Chami, M., Remigy, H., Engel, A., Ballmer-Hofer, K., Winkler, F.K., and Kambach, C. 2005. Reconstitution of two recombinant LSm protein complexes reveals aspects of their architecture, assembly, and function. J. Biol. Chem. 280: 16066-16075.