The Evolutionarily Conserved Core Design of the Catalytic Activation Step of the Yeast Spliceosome

Molecular Cell

Volumn 36, Issue 4, 2009, Pages 593-608

  Fabrizio, Patrizia ^a   Dannenberg, Julia ^a   Dube, Prakash ^a   Kastner, Berthold ^a   Stark, Holger ^a,b   Urlaub, Henning ^a   Lührmann, Reinhard ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

PROTEINS; RNA

Indexed keywords

MESSENGER RNA PRECURSOR; RIBONUCLEOPROTEIN; RNA; RNA HELICASE; SMALL NUCLEAR RNA;

ARTICLE; ELECTRON MICROSCOPY; EUKARYOTE; EVOLUTION; MASS SPECTROMETRY; NONHUMAN; PROTEIN ANALYSIS; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SPLICEOSOME; YEAST;

BIOCATALYSIS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; HUMANS; KINETICS; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPLICEOSOMES;

EUKARYOTA; METAZOA; SACCHAROMYCES CEREVISIAE;

EID: 70449625597     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.09.040     Document Type: Article

References (43)

1. Abelson J. Is the spliceosome a ribonucleoprotein enzyme?. Nat. Struct. Mol. Biol. 15 (2008) 1235-1237
2. Albers M., Diment A., Muraru M., Russell C.S., and Beggs J.D. Identification and characterization of Prp45p and Prp46p, essential pre-mRNA splicing factors. RNA 9 (2003) 138-150
3. Behzadnia N., Golas M.M., Hartmuth K., Sander B., Kastner B., Deckert J., Dube P., Will C.L., Urlaub H., Stark H., and Lührmann R. Composition and three-dimensional EM structure of double affinity-purified, human prespliceosomal A complexes. EMBO J. 26 (2007) 1737-1748
4. Bessonov S., Anokhina M., Will C.L., Urlaub H., and Lührmann R. Isolation of an active step I spliceosome and composition of its RNP core. Nature 452 (2008) 846-850
5. Boehringer D., Makarov E.M., Sander B., Makarova O.V., Kastner B., Lührmann R., and Stark H. Three-dimensional structure of a pre-catalytic human spliceosomal complex B. Nat. Struct. Mol. Biol. 11 (2004) 463-468
6. Brow D.A. Allosteric cascade of spliceosome activation. Annu. Rev. Genet. 36 (2002) 333-360
7. Caceres J.F., and Kornblihtt A.R. Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet. 18 (2002) 186-193
8. Chan S.P., Kao D.I., Tsai W.Y., and Cheng S.C. The Prp19p-associated complex in spliceosome activation. Science 302 (2003) 279-282
9. Cheng S.C. Formation of the yeast splicing complex A1 and association of the splicing factor PRP19 with the pre-mRNA are independent of the 3′ region of the intron. Nucleic Acids Res. 22 (1994) 1548-1554
10. Cheng S.C., and Abelson J. Spliceosome assembly in yeast. Genes Dev. 1 (1987) 1014-1027
11. Deckert J., Hartmuth K., Boehringer D., Behzadnia N., Will C.L., Kastner B., Stark H., Urlaub H., and Lührmann R. Protein composition and electron microscopy structure of affinity-purified human spliceosomal B complexes isolated under physiological conditions. Mol. Cell. Biol. 26 (2006) 5528-5543
12. Dziembowski A., Ventura A.P., Rutz B., Caspary F., Faux C., Halgand F., Laprevote O., and Seraphin B. Proteomic analysis identifies a new complex required for nuclear pre-mRNA retention and splicing. EMBO J. 23 (2004) 4847-4856
13. Golas M.M., Sander B., Will C.L., Lührmann R., and Stark H. Molecular architecture of the multiprotein splicing factor SF3b. Science 300 (2003) 980-984
14. Gottschalk A., Neubauer G., Banroques J., Mann M., Lührmann R., and Fabrizio P. Identification by mass spectrometry and functional analysis of novel proteins of the yeast [U4/U6.U5] tri-snRNP. EMBO J. 18 (1999) 4535-4548
15. Häcker I., Sander B., Golas M.M., Wolf E., Karagoz E., Kastner B., Stark H., Fabrizio P., and Lührmann R. Localization of Prp8, Brr2, Snu114 and U4/U6 proteins in the yeast tri-snRNP by electron microscopy. Nat. Struct. Mol. Biol. 15 (2008) 1206-1212
16. Herold N., Will C.L., Wolf E., Kastner B., Urlaub H., and Lührmann R. Conservation of the protein composition and electron microscopy structure of Drosophila melanogaster and human spliceosomal complexes. Mol. Cell. Biol. 29 (2009) 281-301
17. Hertel K.J., and Graveley B.R. RS domains contact the pre-mRNA throughout spliceosome assembly. Trends Biochem. Sci. 30 (2005) 115-118
18. Jurica M.S., and Moore M.J. Capturing splicing complexes to study structure and mechanism. Methods 28 (2002) 336-345
19. Kastner B., Fischer N., Golas M.M., Sander B., Dube P., Boehringer D., Hartmuth K., Deckert J., Hauer F., Wolf E., et al. GraFix: sample preparation for single-particle electron cryomicroscopy. Nat. Methods 5 (2008) 53-55
20. Kim S.H., and Lin R.J. Spliceosome activation by PRP2 ATPase prior to the first transesterification reaction of pre-mRNA splicing. Mol. Cell. Biol. 16 (1996) 6810-6819
21. Kosowski T.R., Keys H.R., Quan T.K., and Ruby S.W. DExD/H-box Prp5 protein is in the spliceosome during most of the splicing cycle. RNA 15 (2009) 1345-1362
22. Kress T.L., Krogan N.J., and Guthrie C. A single SR-like protein, Npl3, promotes pre-mRNA splicing in budding yeast. Mol. Cell 32 (2008) 727-734
23. Liu Y.C., Chen H.C., Wu N.Y., and Cheng S.C. A novel splicing factor, Yju2, is associated with NTC and acts after Prp2 in promoting the first catalytic reaction of pre-mRNA splicing. Mol. Cell. Biol. 27 (2007) 5403-5413
24. Makarova O.V., Makarov E.M., Urlaub H., Will C.L., Gentzel M., Wilm M., and Lührmann R. A subset of human 35S U5 proteins, including Prp19, function prior to catalytic step 1 of splicing. EMBO J. 23 (2004) 2381-2391
25. McGrail J.C., Krause A., and O'Keefe R.T. The RNA binding protein Cwc2 interacts directly with the U6 snRNA to link the nineteen complex to the spliceosome during pre-mRNA splicing. Nucleic Acids Res. 37 (2009) 4205-4217
26. Nilsen T.W. RNA-RNA interactions in nuclear pre-mRNA splicing. In: Grundber-Manago M., and Simons R.W. (Eds). RNA Structure and Function (1998), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 279-307
27. Ohi M.D., Link A.J., Ren L., Jennings J.L., McDonald W.H., and Gould K.L. Proteomics analysis reveals stable multiprotein complexes in both fission and budding yeasts containing Myb-related Cdc5p/Cef1p, novel pre-mRNA splicing factors, and snRNAs. Mol. Cell. Biol. 22 (2002) 2011-2024
28. Pandit S., Lynn B., and Rymond B.C. Inhibition of a spliceosome turnover pathway suppresses splicing defects. Proc. Natl. Acad. Sci. USA 103 (2006) 13700-13705
29. Pyle A.M. Translocation and unwinding mechanisms of RNA and DNA helicases. Annu. Rev. Biophys. 37 (2008) 317-336
30. Ruby S.W., Chang T.H., and Abelson J. Four yeast spliceosomal proteins (PRP5, PRP9, PRP11, and PRP21) interact to promote U2 snRNP binding to pre-mRNA. Genes Dev. 7 (1993) 1909-1925
31. Rymond B.C., and Rosbash M. Cleavage of 5′ splice site and lariat formation are independent of 3′ splice site in yeast mRNA splicing. Nature 317 (1985) 735-737
32. Sapra A.K., Khandelia P., and Vijayraghavan U. The splicing factor Prp17 interacts with the U2, U5 and U6 snRNPs and associates with the spliceosome pre- and post-catalysis. Biochem. J. 416 (2008) 365-374
33. Small E.C., Leggett S.R., Winans A.A., and Staley J.P. The EF-G-like GTPase Snu114p regulates spliceosome dynamics mediated by Brr2p, a DExD/H box ATPase. Mol. Cell 23 (2006) 389-399
34. Smith D.J., Query C.C., and Konarska M.M. trans-splicing to spliceosomal U2 snRNA suggests disruption of branch site-U2 pairing during pre-mRNA splicing. Mol. Cell 26 (2007) 883-890
35. Stevens S.W., and Abelson J. Purification of the yeast U4/U6.U5 small nuclear ribonucleoprotein particle and identification of its proteins. Proc. Natl. Acad. Sci. USA 96 (1999) 7226-7231
36. Stevens S.W., Ryan D.E., Ge H.Y., Moore R.E., Young M.K., Lee T.D., and Abelson J. Composition and functional characterization of the yeast spliceosomal penta-snRNP. Mol. Cell 9 (2002) 31-44
37. Tanaka N., Aronova A., and Schwer B. Ntr1 activates the Prp43 helicase to trigger release of lariat-intron from the spliceosome. Genes Dev. 21 (2007) 2312-2325
38. Tarn W.Y., Lee K.R., and Cheng S.C. Yeast precursor mRNA processing protein PRP19 associates with the spliceosome concomitant with or just after dissociation of U4 small nuclear RNA. Proc. Natl. Acad. Sci. USA 90 (1993) 10821-10825
39. Tsai R.T., Tseng C.K., Lee P.J., Chen H.C., Fu R.H., Chang K.J., Yeh F.L., and Cheng S.C. Dynamic interactions of Ntr1-Ntr2 with Prp43 and with U5 govern the recruitment of Prp43 to mediate spliceosome disassembly. Mol. Cell. Biol. 27 (2007) 8027-8037
40. Umen J.G., and Guthrie C. The second catalytic step of pre-mRNA splicing. RNA 1 (1995) 869-885
41. Vijayraghavan U., Parker R., Tamm J., Iimura Y., Rossi J., Abelson J., and Guthrie C. Mutations in conserved intron sequences affect multiple steps in the yeast splicing pathway, particularly assembly of the spliceosome. EMBO J. 5 (1986) 1683-1695
42. Wahl M.C., Will C.L., and Lührmann R. The spliceosome: Design principles of a dynamic RNP machine. Cell 136 (2009) 701-718
43. Xu D., and Friesen J.D. Splicing factor Slt11p and its involvement in formation of U2/U6 helix II in activation of the yeast spliceosome. Mol. Cell. Biol. 21 (2001) 1011-1023