Cwc2 and its human homologue RBM22 promote an active conformation of the spliceosome catalytic centre

EMBO Journal

Volumn 31, Issue 6, 2012, Pages 1591-1604

  Rasche, Nicolas ^a   Dybkov, Olexandr ^a   Schmitzová, Jana ^a   Akyildiz, Berktan ^a   Fabrizio, Patrizia ^a   Lührmann, Reinhard ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

catalytic centre; Cwc2; RBM22; spliceosome; U6 ISL

Indexed keywords

MESSENGER RNA PRECURSOR; RIBOZYME; RNA U6; SACCHAROMYCES CEREVISIAE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN CWC2; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME SUBSTRATE COMPLEX; GENE; GENETIC CONSERVATION; INTRON; PRIORITY JOURNAL; PROTEIN FUNCTION; RBM22 GENE; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SPLICEOSOME;

CATALYSIS; DEAD-BOX RNA HELICASES; HUMANS; INTRONS; RNA PRECURSORS; RNA SPLICE SITES; RNA SPLICING; RNA, BACTERIAL; RNA, SMALL NUCLEAR; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPLICEOSOMES;

EID: 84858799296     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.502     Document Type: Article

References (60)

1. Abelson J (2008) Is the spliceosome a ribonucleoprotein enzyme? Nat Struct Mol Biol 15: 1235-1237
2. Agafonov DE, Deckert J, Wolf E, Odenwälder P, Bessonov S, Will CL, 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
3. Bessonov S, Anokhina M, Krasauskas A, Golas MM, Sander B, Will CL, Urlaub H, Stark H, Lührmann R (2010) Characterization of purified human Bact spliceosomal complexes reveals compositional and morphological changes during spliceosome activation and first step catalysis. RNA 16: 2384-2403
4. Bessonov S, Anokhina M, Will CL, Urlaub H, Lührmann R (2008) Isolation of an active step I spliceosome and composition of its RNP core. Nature 452: 846-850 (Pubitemid 351550864)
5. Burgess SM, 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 (Pubitemid 23201150)
6. Butcher SE, Brow DA (2005) Towards understanding the catalytic core structure of the spliceosome. Biochem Soc Trans 33: 447-449 (Pubitemid 40873862)
7. Chan SP, Cheng SC (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
8. Chan SP, Kao DI, Tsai WY, Cheng SC (2003) The Prp19p-associated complex in spliceosome activation. Science 302: 279-282
9. Chen CH, Tsai WY, Chen HR, Wang CH, Cheng SC (2001) Identification and characterization of two novel components of the Prp19p-associated complex, Ntc30p and Ntc20p. J Biol Chem 276: 488-494
10. Chiu YF, Liu YC, Chiang TW, Yeh TC, Tseng CK, Wu NY, Cheng SC (2009) Cwc25 is a novel splicing factor required after Prp2 and Yju2 to facilitate the first catalytic reaction. Mol Cell Biol 29: 5671-5678
11. Ehresmann C, Baudin F, Mougel M, Romby P, Ebel JP, Ehresmann B (1987) Probing the structure of RNAs in solution. Nucleic Acids Res 15: 9109-9128
12. 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
13. Fabrizio P, Abelson J (1992) Thiophosphates in yeast U6 snRNA specifically affect pre-mRNA splicing in vitro. Nucleic Acids Res 20: 3659-3664
14. 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
15. Fortner DM, Troy RG, Brow DA (1994) A stem/loop in U6 RNA defines a conformational switch required for pre-mRNA splicing. Genes Dev 8: 221-233
16. Grainger RJ, Beggs JD (2005) Prp8 protein: at the heart of the spliceosome. RNA 11: 533-557 (Pubitemid 40594322)
17. Hilliker AK, Staley JP (2004) Multiple functions for the invariant AGC triad of U6 snRNA. RNA 10: 921-928 (Pubitemid 38669765)
18. Hogg R, McGrail JC, O'Keefe RT (2010) The function of the NineTeen Complex (NTC) in regulating spliceosome conformations and fidelity during pre-mRNA splicing. Biochem Soc Trans 38: 1110-1115
19. Huppler A, Nikstad LJ, Allmann AM, Brow DA, Butcher SE (2002) Metal binding and base ionization in the U6 RNA intramolecular stem-loop structure. Nat Struct Biol 9: 431-435 (Pubitemid 34568787)
20. Jurica MS, Moore MJ (2003) Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 12: 5-14 (Pubitemid 36945033)
21. Kandels-Lewis S, Séraphin B (1993) Involvement of U6 snRNA in 50 splice site selection. Science 262: 2035-2039
22. Keating KS, Toor N, Perlman PS, Pyle AM (2010) A structural analysis of the group II intron active site and implications for the spliceosome. RNA 16: 1-9
23. Kim SH, Lin RJ (1996) Spliceosome activation by PRP2 ATPase prior to the first transesterification reaction of pre-mRNA splicing. Mol Cell Biol 16: 6810-6819
24. Konarska MM, Query CC (2005) Insights into the mechanisms of splicing: more lessons from the ribosome. Genes Dev 19: 2255-2260 (Pubitemid 41396900)
25. Konarska MM, Vilardell J, Query CC (2006) Repositioning of the reaction intermediate within the catalytic center of the spliceosome. Mol Cell 21: 543-553 (Pubitemid 43228009)
26. Lesser CF, Guthrie C (1993) Mutations in U6 snRNA that alter splice site specificity: implications for the active site. Science 262: 1982-1988 (Pubitemid 24041875)
27. Madhani HD, 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
28. Madhani HD, Guthrie C (1994) Dynamic RNA-RNA interactions in the spliceosome. Annu Rev Genet 28: 1-26
29. McGrail JC, Krause A, O'Keefe RT (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. McManus CJ, Schwartz ML, Butcher SE, Brow DA (2007) A dynamic bulge in the U6 RNA internal stem-loop functions in spliceosome assembly and activation. RNA 13: 2252-2265 (Pubitemid 350127565)
31. Mefford MA, Staley JP (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
32. Michel F, Costa M, Westhof E (2009) The ribozyme core of group II introns: a structure in want of partners. Trends Biochem Sci 34: 189-199
33. Moine H, Ehresmann B, Ehresmann C, Romby P (1997) Probing RNA structure and function in solution. In: Simons RW, Grunberg-Manago M (eds). RNA Structure and Function. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY. . pp 77-115
34. Nilsen TW (1998) RNA-RNA interactions in nuclear pre-mRNA splicing. In: Grundber-Manago M, Simons RW (eds). RNA Structure and Function. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, . pp 279-307
35. O'Keefe RT, Newman AJ (1998) Functional analysis of the U5 snRNA loop 1 in the second catalytic step of yeast pre-mRNA splicing. EMBO J 17: 565-574 (Pubitemid 28045496)
36. Ohi MD, Gould KL (2002) Characterization of interactions among the Cef1p-Prp19p-associated splicing complex. RNA 8: 798-815 (Pubitemid 34620456)
37. Pena V, Rozov A, Fabrizio P, Lührmann R, Wahl MC (2008) Structure and function of an RNase H domain at the heart of the spliceosome. EMBO J 27: 2929-2940
38. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, Bragado-Nilsson E, Wilm M, Séraphin B (2001) The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24: 218-229 (Pubitemid 32846428)
39. Query CC, Konarska MM (2006) Splicing fidelity revisited. Nat Struct Mol Biol 13: 472-474 (Pubitemid 43853033)
40. Rhode BM, Hartmuth K, Westhof E, Lührmann R (2006) Proximity of conserved U6 and U2 snRNA elements to the 50 splice site region in activated spliceosomes. EMBO J 25: 2475-2486 (Pubitemid 44012230)
41. Ritchie DB, Schellenberg MJ, Gesner EM, Raithatha SA, Stuart DT, Macmillan AM (2008) Structural elucidation of a PRP8 core domain from the heart of the spliceosome. Nat Struct Mol Biol 15: 1199-1205
42. Shukla GC, Padgett RA (2002) A catalytically active group II intron domain 5 can function in the U12-dependent spliceosome. Mol Cell 9: 1145-1150 (Pubitemid 34626682)
43. Sontheimer EJ, Steitz JA (1993) The U5 and U6 small nuclear RNAs as active site components of the spliceosome. Science 262: 1989-1996 (Pubitemid 24041876)
44. Staley JP, Guthrie C (1998) Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92: 315-326 (Pubitemid 28093010)
45. Steitz TA, Steitz JA (1993) A general two-metal-ion mechanism for catalytic RNA. Proc Natl Acad Sci USA 90: 6498-6502 (Pubitemid 23207240)
46. Tarn WY, Hsu CH, Huang KT, Chen HR, Kao HY, Lee KR, Cheng SC (1994) Functional association of essential splicing factor(s) with PRP19 in a protein complex. EMBO J 13: 2421-2431
47. Toor N, Keating KS, Fedorova O, Rajashankar K, Wang J, Pyle AM (2010) Tertiary architecture of the Oceanobacillus iheyensis group II intron. RNA 16: 57-69
48. Toor N, Keating KS, Taylor SD, Pyle AM (2008) Crystal structure of a self-spliced group II intron. Science 320: 77-82 (Pubitemid 351490756)
49. Urlaub H, Hartmuth K, Lührmann R (2002) A two-tracked approach to analyze RNA-protein crosslinking sites in native, nonlabeled small nuclear ribonucleoprotein particles. Methods 26: 170-181 (Pubitemid 34969579)
50. Valadkhan S (2005) snRNAs as the catalysts of pre-mRNA splicing. Curr Opin Chem Biol 9: 603-608
51. Valadkhan S, Manley JL (2002) Intrinsic metal binding by a spliceosomal RNA. Nat Struct Biol 9: 498-499 (Pubitemid 34693799)
52. Vander Kooi CW, Ren L, Xu P, Ohi MD, Gould KL, Chazin WJ (2010) The Prp19 WD40 domain contains a conserved protein interaction region essential for its function. Structure 18: 584-593
53. Vidal VP, Verdone L, Mayes AE, Beggs JD (1999) Characterization of U6 snRNA-protein interactions. RNA 5: 1470-1481 (Pubitemid 29530491)
54. 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 (Pubitemid 41186990)
55. Warkocki Z, Odenwälder P, Schmitzová 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
56. Will CL, Lührmann R (2011) Spliceosome structure and function. In: Gesteland RF, Cech TR, Atkins JF (eds). RNA World. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, . pp 181-203
57. Wu JA, Manley JL (1991) Base pairing between U2 and U6 snRNAs is necessary for splicing of a mammalian pre-mRNA. Nature 352: 818-821 (Pubitemid 21912439)
58. Xu D, Friesen JD (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 (Pubitemid 32114951)
59. Yang K, Zhang L, Xu T, Heroux A, Zhao R (2008) Crystal structure of the beta-finger domain of Prp8 reveals analogy to ribosomal proteins. Proc Natl Acad Sci USA 105: 13817-13822
60. Yean SL, Wuenschell G, Termini J, Lin RJ (2000) Metal-ion coordination by U6 small nuclear RNA contributes to catalysis in the spliceosome. Nature 408: 881-884 (Pubitemid 32016101)