Dissection of the factor requirements for spliceosome disassembly and the elucidation of its dissociation products using a purified splicing system

Genes and Development

Volumn 27, Issue 4, 2013, Pages 413-428

  Fourmann, Jean Baiste ^a   Schmitzová, Jana ^a   Christian, Henning ^b   Urlaub, Henning ^a   Ficner, Ralf ^b   Boon, Kum Loong ^a   Fabrizio, Patrizia ^a   Lührmann, Reinhard ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Brr2; Disassembly; Intron lariat spliceosome; Prp22; Prp43

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; MESSENGER RNA; RNA HELICASE; SMALL NUCLEAR RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; ENZYME ACTIVITY; IN VITRO STUDY; INTRON; NONHUMAN; PRIORITY JOURNAL; RNA SPLICING; SPLICEOSOME;

DEAD-BOX RNA HELICASES; INTRONS; RNA SPLICING; RNA, MESSENGER; RNA, SMALL NUCLEAR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPLICEOSOMES;

EID: 84874268195     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.207779.112     Document Type: Article

References (46)

1. Arenas JE., Abelson JN. 1997. Prp43: An RNA helicase-like factor involved in spliceosome disassembly. Proc Natl Acad Sci 94: 11798-11802.
2. Barbosa I., Haque N, Fiorini F, Barrandon C, Tomasetto C, Blanchette M., Le Hir H. 2012. Human CWC22 escorts the helicase eIF4AIII to spliceosomes and promotes exon junction complex assembly. Nat Struct Mol Biol 19: 983-990.
3. Bell M., Schreiner S, Damianov A, Reddy R, Bindereif A. 2002. p110, a novel human U6 snRNP protein and U4/U6 snRNP recycling factor. EMBO J 21: 2724-2735.
4. Bohnsack MT., Martin R, Granneman S, Ruprecht M, Schleiff E, Tollervey D. 2009. Prp43 bound at different sites on the prerRNA performs distinct functions in ribosome synthesis. Mol Cell 36: 583-592.
5. Boon KL., Auchynnikava T, Edwalds-Gilbert G, Barrass JD, Droop AP., Dez C, Beggs JD. 2006. Yeast ntr1/spp382 mediates prp43 function in postspliceosomes. Mol Cell Biol 26: 6016-6023.
6. Brys A., Schwer B. 1996. Requirement for SLU7 in yeast premRNA splicing is dictated by the distance between the branchpoint and the 39 splice site. RNA 2: 707-717.
7. Chan SP., Cheng SC. 2005. The Prp19-associated complex is required for specifying interactions of U5 and U6 with premRNA during spliceosome activation. J Biol Chem 280: 31190-31199.
8. Chan SP., Kao DI, Tsai WY, Cheng SC. 2003. The Prp19passociated complex in spliceosome activation. Science 302: 279-282.
9. 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.
10. Company M., Arenas J, Abelson J. 1991. Requirement of the RNA helicase-like protein PRP22 for release of messenger RNA from spliceosomes. Nature 349: 487-493.
11. Cordin O., Hahn D, Beggs JD. 2012. Structure, function and regulation of spliceosomal RNA helicases. Curr Opin Cell Biol 24: 431-438.
12. Dziembowski A., Ventura AP, Rutz B, Caspary F, Faux C, Halgand F., Laprevote O, Seraphin B. 2004. Proteomic analysis identifies a new complex required for nuclear premRNA retention and splicing. EMBO J 23: 4847-4856.
13. 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.
14. Gottschalk A., Neubauer G, Banroques J, Mann M, Lührmann R, Fabrizio P. 1999. Identification by mass spectrometry and functional analysis of novel proteins of the yeast [U4/U6. U5] tri-snRNP. EMBO J 18: 4535-4548.
15. Grainger RJ., Barrass JD, Jacquier A, Rain JC, Beggs JD. 2009. Physical and genetic interactions of yeast Cwc21p, an ortholog of human SRm300/SRRM2, suggest a role at the catalytic center of the spliceosome. RNA 15: 2161-2173.
16. Horowitz DS. 2012. The mechanism of the second step of premRNA splicing. Wiley Interdiscip Rev RNA 3: 331-350.
17. Laggerbauer B., Achsel T, Lührmann R. 1998. The human U5-200kD DEXH-box protein unwinds U4/U6 RNA duplices in vitro. Proc Natl Acad Sci 95: 4188-4192.
18. Lardelli RM., Thompson JX, Yates JR 3rd, Stevens SW. 2010. Release of SF3 from the intron branchpoint activates the first step of pre-mRNA splicing. RNA 16: 516-528.
19. Makarov EM., Makarova OV, Urlaub H, Gentzel M, Will CL, Wilm M., Lührmann R. 2002. Small nuclear ribonucleoprotein remodeling during catalytic activation of the spliceosome. Science 298: 2205-2208.
20. Martin A., Schneider S, Schwer B. 2002. Prp43 is an essential RNA-dependent ATPase required for release of lariat-intron from the spliceosome. J Biol Chem 277: 17743-17750.
21. Mayas RM., Maita H, Staley JP. 2006. Exon ligation is proofread by the DExD/H-box ATPase Prp22p. Nat Struct Mol Biol 13: 482-490.
22. 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.
23. Nilsen TW. 1998. RNA-RNA interactions in nuclear pre-mRNA splicing. In RNA structure and function (ed. M Grundber-Manago and RW Simons), pp. 279-307. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Ohi MD., Gould KL. 2002. Characterization of interactions among the Cef1p-Prp19p-associated splicing complex. RNA 8: 798-815.
25. Ohrt T., Prior M, Dannenberg J, Odenwälder P, Dybkov O, Rasche N., Schmitzová 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.
26. Pandit S., Lynn B, Rymond BC. 2006. Inhibition of a spliceosome turnover pathway suppresses splicing defects. Proc Natl Acad Sci 103: 13700-13705.
27. Pandit S., Paul S, Zhang L, Chen M, Durbin N, Harrison SM, Rymond BC. 2009. Spp382p interacts with multiple yeast splicing factors, including possible regulators of Prp43 DExD/ H-box protein function. Genetics 183: 195-206.
28. Rader SD., Guthrie C. 2002. A conserved Lsm-interaction motif in Prp24 required for efficient U4/U6 di-snRNP formation. RNA 8: 1378-1392.
29. Raghunathan PL., Guthrie C. 1998. RNA unwinding in U4/U6 snRNPs requires ATP hydrolysis and the DEIH-box splicing factor Brr2. Curr Biol 8: 847-855.
30. Rasche N., Dybkov O, Schmitzová 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.
31. Roy J., Kim K, Maddock JR, Anthony JG, Woolford JL Jr. 1995. The final stages of spliceosome maturation require Spp2p that can interact with the DEAH box protein Prp2p and promote step 1 of splicing. RNA 1: 375-390.
32. Santos KF., Jovin SM, Weber G, Pena V, Lührmann R, Wahl MC. 2012. Structural basis for functional cooperation between tandem helicase cassettes in Brr2-mediated remodeling of the spliceosome. Proc Natl Acad Sci 109: 17418-17423.
33. Schwer B. 2008. A conformational rearrangement in the spliceosome sets the stage for Prp22-dependent mRNA release. Mol Cell 30: 743-754.
34. Schwer B., Gross CH. 1998. Prp22, a DExH-box RNA helicase, plays two distinct roles in yeast pre-mRNA splicing. EMBO J 17: 2086-2094.
35. Silverman EJ., Maeda A, Wei J, Smith P, Beggs JD, Lin RJ. 2004. Interaction between a G-patch protein and a spliceosomal DEXD/H-box ATPase that is critical for splicing. Mol Cell Biol 24: 10101-10110.
36. Small EC., Leggett SR, Winans AA, Staley JP. 2006. The EFG-like GTPase Snu114p regulates spliceosome dynamics mediated by Brr2p, a DExD/H box ATPase. Mol Cell 23: 389-399.
37. Staley JP., Guthrie C. 1998. Mechanical devices of the spliceosome: Motors, clocks, springs, and things. Cell 92: 315-326.
38. Staley JP., Guthrie C. 1999. An RNA switch at the 59 splice site requires ATP and the DEAD box protein Prp28p. Mol Cell 3: 55-64.
39. Steckelberg AL., Boehm V, Gromadzka AM, Gehring NH. 2012. CWC22 connects pre-mRNA splicing and exon junction complex assembly. Cell Rep 2: 454-461.
40. Stevens SW., Barta I, Ge HY, Moore RE, Young MK, Lee TD, Abelson J. 2001. Biochemical and genetic analyses of the U5, U6, and U4/U6 3 U5 small nuclear ribonucleoproteins from Saccharomyces cerevisiae. RNA 7: 1543-1553.
41. Tanaka N., Aronova A, Schwer B. 2007. Ntr1 activates the Prp43 helicase to trigger release of lariat-intron from the spliceosome. Genes Dev 21: 2312-2325.
42. Tsai RT., Fu RH, Yeh FL, Tseng CK, Lin YC, Huang YH, Cheng SC. 2005. Spliceosome disassembly catalyzed by Prp43 and its associated components Ntr1 and Ntr2. Genes Dev 19: 2991-3003.
43. Tsai RT., Tseng CK, Lee PJ, Chen HC, Fu RH, Chang KJ, Yeh FL, Cheng SC. 2007. Dynamic interactions of Ntr1-Ntr2 with Prp43 and with U5 govern the recruitment of Prp43 to mediate spliceosome disassembly. Mol Cell Biol 27: 8027-8037.
44. 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.
45. Will CL., Lührmann R. 2011. Spliceosome structure and function. In RNA worlds (ed. RF Gesteland, et al.), pp. 181-203.
46. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. Yeh TC., Liu HL, Chung CS, Wu NY, Liu YC, Cheng SC. 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.