Remodeling of U2-U6 snRNA helix i during pre-mRNA splicing by Prp16 and the nineteen complex protein Cwc2

Nucleic Acids Research

Volumn 42, Issue 12, 2014, Pages 8008-8023

  Hogg, Rebecca ^a   De Almeida, Rogerio Alves ^a   Ruckshanthi, Jayalath P D ^a   O'Keefe, Raymond T ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CELL PROTEIN; CWC2 PROTEIN; MESSENGER RNA PRECURSOR; NTC30 PROTEIN; PRP16 PROTEIN; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG; YJU2 PROTEIN;

ARTICLE; COLD SENSITIVITY; GENE INTERACTION; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN SECRETION; RNA SPLICING; RNA STABILITY; RNA STRUCTURE; SPLICEOSOME;

ADENOSINE TRIPHOSPHATASES; MUTATION; NUCLEIC ACID CONFORMATION; RNA HELICASES; RNA PRECURSORS; RNA SPLICING; RNA, MESSENGER; RNA, SMALL NUCLEAR; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84904016400     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku431     Document Type: Article

References (49)

1. Wahl, M.C., Will, C.L., Lührmann, R. (2009) The spliceosome: design principles of a dynamic RNP machine. Cell, 136, 701-718.
2. Nilsen, T.W. (1998) In: Simons RW and Grunberg-ManagoM (eds). RNA Structure and Function. Cold Spring Harbor Press, Cold Spring Harbor, NY, pp. 279-307.
3. Keating, K.S., Toor, N., Perlman, P.S., Pyle, A.M. (2010) A structural analysis of the group II intron active site and implications for the spliceosome. RNA, 16, 1-9.
4. Fica, S.M., Tuttle, N., Novak, T., Li, N.S., Lu, J., Koodathingal, P., Dai, Q., Staley, J.P., Piccirilli, J.A. (2013) RNA catalyses nuclear pre-mRNA splicing. Nature, 503, 229-234.
5. Smith, D.J., Query, C.C., Konarska, M.M. (2008) "Nought may endure but mutability": spliceosome dynamics and the regulation of splicing. Mol. Cell, 30, 657-666.
6. Burgess, S.M., Guthrie, C. (1993) A mechanism to enhance mRNA splicing fidelity: the RNA-dependent ATPase Prp16 governs usage of a discard pathway for aberrant lariat intermediates. Cell, 73, 1377-1391.
7. Mayas, R.M., Maita, H., Staley, J.P. (2006) Exon ligation is proofread by the DExD/H-box ATPase Prp22p. Nat. Struct. Mol. Biol., 13, 482-490.
8. Xu, Y.Z., Query, C.C. (2007) Competition between the ATPase Prp5 and branch region-U2 snRNA pairing modulates the fidelity of spliceosome assembly. Mol. Cell, 28, 838-849.
9. Yang, F., Wang, X.Y., Zhang, Z.M., Pu, J., Fan, Y.J., Zhou, J., Query, C.C., Xu, Y.Z. (2013) Splicing proofreading at 5' splice sites by ATPase Prp28p. Nucleic Acids Res., 41, 4660-4670.
10. Kim, S.H., Lin, R.J. (1993) Pre-mRNA splicing within an assembled yeast spliceosome requires an RNA-dependent ATPase and ATP hydrolysis. Proc. Natl. Acad. Sci. U.S.A., 90, 888-892.
11. Kim, S.H., Lin, R.J. (1996) Spliceosome activation by PRP2 ATPase prior to the first transesterification reaction of pre-mRNA splicing. Mol. Cell. Biol., 16, 6810-6819.
12. Liu, H.L., Cheng, S.C. (2012) The interaction of Prp2 with a defined region of the intron is required for the first splicing reaction. Mol. Cell. Biol., 32, 5056-5066.
13. Teigelkamp, S., McGarvey, M., Plumpton, M., Beggs, J.D. (1994) The splicing factor PRP2, a putative RNA helicase, interacts directly with pre-mRNA. EMBO J., 13, 888-897.
14. Agafonov, D.E., Deckert, J., Wolf, E., Odenwalder, P., Bessonov, S., Will, C.L., Urlaub, H., Lührmann, R. (2011) Semiquantitative proteomic analysis of the human spliceosome via a novel two-dimensional gel electrophoresis method. Mol. Cell. Biol., 31, 2667-2682.
15. Bessonov, S., Anokhina, M., Will, C.L., Urlaub, H., Lührmann, R. (2008) Isolation of an active step I spliceosome and composition of its RNP core. Nature, 452, 846-850.
16. Fabrizio, P., Dannenberg, J., Dube, P., Kastner, B., Stark, H., Urlaub, H., Lührmann, R. (2009) The evolutionarily conserved core design of the catalytic activation step of the yeast spliceosome. Mol. Cell, 36, 593-608.
17. Lardelli, R.M., Thompson, J.X., Yates, J.R. III and Stevens, S.W. (2010) Release of SF3 from the intron branchpoint activates the first step of pre-mRNA splicing. RNA, 16, 516-528.
18. Ohrt, T., Prior, M., Dannenberg, J., Odenwalder, P., Dybkov, O., Rasche, N., Schmitzova, J., Gregor, I., Fabrizio, P., Enderlein, J. et al. (2012) Prp2-mediated protein rearrangements at the catalytic core of the spliceosome as revealed by dcFCCS. RNA, 18, 1244-1256.
19. Warkocki, Z., Odenwalder, P., Schmitzova, J., Platzmann, F., Stark, H., Urlaub, H., Ficner, R., Fabrizio, P., Lührmann, R. (2009) Reconstitution of both steps of Saccharomyces cerevisiae splicing with purified spliceosomal components. Nat. Struct. Mol. Biol., 16, 1237-1243.
20. Yeh, T.C., Liu, H.L., Chung, C.S., Wu, N.Y., Liu, Y.C., Cheng, S.C. (2011) Splicing factor Cwc22 is required for the function of Prp2 and for the spliceosome to escape from a futile pathway. Mol. Cell. Biol., 31, 43-53.
21. Wlodaver, A.M., Staley, J.P. (2014) The DExD/H-box ATPase Prp2p destabilizes and proofreads the catalytic RNA core of the spliceosome. RNA, 20, 282-294.
22. Koodathingal, P., Novak, T., Piccirilli, J.A., Staley, J.P. (2010) The DEAH box ATPases Prp16 and Prp43 cooperate to proofread 5' splice site cleavage during pre-mRNA splicing. Mol. Cell, 39, 385-395.
23. Mefford, M.A., Staley, J.P. (2009) Evidence that U2/U6 helix I promotes both catalytic steps of pre-mRNA splicing and rearranges in between these steps. RNA, 15, 1386-1397.
24. Tseng, C.K., Liu, H.L., Cheng, S.C. (2011) DEAH-box ATPase Prp16 has dual roles in remodeling of the spliceosome in catalytic steps. RNA, 17, 145-154.
25. Schwer, B., Guthrie, C. (1991) PRP16 is an RNA-dependent ATPase that interacts transiently with the spliceosome. Nature, 349, 494-499.
26. Schwer, B., Guthrie, C. (1992) A conformational rearrangement in the spliceosome is dependent on PRP16 and ATP hydrolysis. EMBO J., 11, 5033-5039.
27. Hogg, R., McGrail, J.C., O'Keefe, R.T. (2010) The function of the NineTeen Complex (NTC) in regulating spliceosome conformations and fidelity during pre-mRNA splicing. Biochem. Soc. Trans., 38, 1110-1115.
28. Chan, S.P., Cheng, S.C. (2005) The Prp19-associated complex is required for specifying interactions of U5 and U6 with pre-mRNA during spliceosome activation. J. Biol. Chem., 280, 31190-31199.
29. McGrail, J.C., Krause, A., O'Keefe, R.T. (2009) 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, 4205-4217.
30. Lu, P., Lu, G., Yan, C., Wang, L., Li, W., Yin, P. (2012) Structure of the mRNA splicing complex component Cwc2: insights into RNA recognition. Biochem. J., 441, 591-597.
31. Schmitzova, J., Rasche, N., Dybkov, O., Kramer, K., Fabrizio, P., Urlaub, H., Lührmann, R., Pena, V. (2012) Crystal structure of Cwc2 reveals a novel architecture of a multipartite RNA-binding protein. EMBO J., 31, 2222-2234.
32. Rasche, N., Dybkov, O., Schmitzova, J., Akyildiz, B., Fabrizio, P., Lührmann, R. (2012) Cwc2 and its human homologue RBM22 promote an active conformation of the spliceosome catalytic centre. EMBO J., 31, 1591-1604.
33. Frazer, L.N., Lovell, S.C., O'Keefe, R.T. (2009) Analysis of synthetic lethality reveals genetic interactions between the GTPase Snu114p and snRNAs in the catalytic core of the Saccharomyces cerevisiae spliceosome. Genetics, 183, 497-515.
34. McGrail, J.C., O'Keefe, R.T. (2008) The U1, U2 and U5 snRNAs crosslink to the 5' exon during yeast pre-mRNA splicing. Nucleic Acids Res., 36, 814-825.
35. Villa, T., Guthrie, C. (2005) The Isy1p component of the NineTeen complex interacts with the ATPase Prp16p to regulate the fidelity of pre-mRNA splicing. Genes Dev., 19, 1894-1904.
36. Xu, D.M., Friesen, J.D. (2001) Splicing factor Slt11p and its involvement in formation of U2/U6 helix II in activation of the yeast spliceosome. Mol. Cell. Biol., 21, 1011-1023.
37. Lesser, C.F., Guthrie, C. (1993) Mutational analysis of pre-mRNA splicing in Saccharomyces cerevisiae using a sensitive new reporter gene, CUP1. Genetics, 133, 851-863.
38. Madhani, H.D., Guthrie, C. (1994) Genetic interactions between the yeast RNA helicase homolog Prp16 and spliceosomal snRNAs identify candidate ligands for the Prp16 RNA-dependent ATPase. Genetics, 137, 677-687.
39. Noble, S.M., Guthrie, C. (1996) Identification of novel genes required for yeast pre-mRNA splicing by means of cold-sensitive mutations. Genetics, 143, 67-80.
40. Rasche, N., Dybkov, O., Schmitzova, J., Akyildiz, B., Fabrizio, P., Lührmann, R. (2012) Cwc2 and its human homologue RBM22 promote an active conformation of the spliceosome catalytic centre. EMBO J., 31, 1591-1604.
41. Hudson, B.P., Martinez-Yamout, M.A., Dyson, H.J., Wright, P.E. (2004) Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d.Nat. Struct. Mol. Biol., 11, 257-264.
42. Ohi, M.D., Gould, K.L. (2002) Characterization of interactions among the Cef1p-Prp19p-associated splicing complex. RNA, 8, 798-815.
43. Ohrt, T., Odenwalder, P., Dannenberg, J., Prior, M., Warkocki, Z., Schmitzova, J., Karaduman, R., Gregor, I., Enderlein, J., Fabrizio, P. et al. (2013) Molecular dissection of step 2 catalysis of yeast pre-mRNA splicing investigated in a purified system. RNA, 19, 902-915.
44. Hilliker, A.K., Staley, J.P. (2004) Multiple functions for the invariant AGC triad of U6 snRNA. RNA, 10, 921-928.
45. Madhani, H.D., 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.
46. Madhani, H.D., Guthrie, C. (1994) Randomization-selection analysis of snRNAs in vivo: Evidence for a tertiary interaction in the spliceosome. Genes Dev., 8, 1071-1086.
47. Madhani, H.D., Bordonné, R., Guthrie, C. (1990) Multiple roles for U6 snRNA in the splicing pathway. Genes Dev., 4, 2264-2277.
48. Fabrizio, P., 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.
49. Toor, N., Keating, K.S., Taylor, S.D., Pyle, A.M. (2008) Crystal structure of a self-spliced group II intron. Science, 320, 77-82.