Molecular dissection of step 2 catalysis of yeast pre-mRNA splicing investigated in a purified system

RNA

Volumn 19, Issue 7, 2013, Pages 902-915

  Ohrt, Thomas ^a   Odenwälder, Peter ^a   Dannenberg, Julia ^a   Prior, Mira ^b   Warkocki, Zbigniew ^a   Schmitzová, Jana ^a   Karaduman, Ramazan ^a   Gregor, Ingo ^b   Enderlein, Jörg ^b   Fabrizio, Patrizia ^a   Lührmann, Reinhard ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Prp22; Slu7 Prp18; Spliceosome; Step 2 catalysis; Step 2 factors Prp16

Indexed keywords

ADENOSINE TRIPHOSPHATASE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYSIS; EXON; FLUORESCENCE SPECTROSCOPY; IN VITRO STUDY; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; RNA PURIFICATION; RNA SPLICING; SPLICEOSOME; YEAST;

PRP22; SLU7 PRP18; SPLICEOSOME; STEP 2 CATALYSIS; STEP 2 FACTORS/PRP16;

CATALYSIS; CATALYTIC DOMAIN; DEAD-BOX RNA HELICASES; EXONS; FUNGAL PROTEINS; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; RNA SPLICE SITES; RNA SPLICING; RNA, FUNGAL; RNA, MESSENGER; SPECTROMETRY, FLUORESCENCE; SPLICEOSOMES; YEASTS;

EID: 84879311174     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.039024.113     Document Type: Article

References (50)

1. Ansari A, Schwer B. 1995. SLU7 and a novel activity, SSF1, act during the PRP16-dependent step of yeast pre-mRNA splicing. EMBO J 14: 4001-4009.
2. Aronova A, Bacikova D, Crotti LB, Horowitz DS, Schwer B. 2007. Functional interactions between Prp8, Prp18, Slu7, and U5 snRNA during the second step of pre-mRNA splicing. RNA 13: 1437-1444.
3. Brys A, Schwer B. 1996. Requirement for SLU7 in yeast pre-mRNA splicing is dictated by the distance between the branchpoint and the 3′ splice site. RNA 2: 707-717. (Pubitemid 26374222)
4. 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)
5. Burgess S, Couto JR, Guthrie C. 1990. A putative ATP binding protein influences the fidelity of branchpoint recognition in yeast splicing. Cell 60: 705-717.
6. Chen C-H, Yu W-C, Tsao TY, Wang L-Y, Chen H-R, Lin J-Y, Tsai W-Y, Cheng S-C. 2002. Functional and physical interactions between components of the Prp19p-associated complex. Nucleic Acids Res 30: 1029-1037. (Pubitemid 34679672)
7. 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.
8. Collins CA, Guthrie C. 1999. Allele-specific genetic interactions between Prp8 and RNA active site residues suggest a function for Prp8 at the catalytic core of the spliceosome. Genes Dev 13: 1970-1982. (Pubitemid 29407364)
9. 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. (Pubitemid 21912085)
10. Cordin O, Hahn D, Beggs JD. 2012. Structure, function and regulation of spliceosomal RNA helicases. Curr Opin Cell Biol 24: 431-438.
11. Crotti LB, Bacikova D, Horowitz DS. 2007. The Prp18 protein stabilizes the interaction of both exons with the U5 snRNA during the second step of pre-mRNA splicing. Genes Dev 21: 1204-1216. (Pubitemid 46789878)
12. 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.
13. Földes-Papp Z. 2005. How the molecule number is correctly quantified in two-color fluorescence cross-correlation spectroscopy: Corrections for cross-talk and quenching in experiments. Curr Pharm Biotechnol 6: 437-444. (Pubitemid 43137064)
14. Földes-Papp Z, Rigler R. 2001. Quantitative two-color fluorescence cross-correlation spectroscopy in the analysis of polymerase chain reaction. Biol Chem 382: 473-478. (Pubitemid 32372491)
15. Fourmann JB, Schmitzová J, Christian H, Urlaub H, Ficner R, Boon KL, Fabrizio P, Lührmann R. 2013. Dissection of the factor requirements for spliceosome disassembly and the elucidation of its dissociation products using a purified splicing system. Genes Dev 27:413-428.
16. Frank D, Patterson B, Guthrie C. 1992. Synthetic lethal mutations suggest interactions between U5 small nuclear RNA and four proteins required for the second step of splicing. Mol Cell Biol 12:5197-5205.
17. Grainger RJ, Beggs JD. 2005. Prp8 protein: At the heart of the spliceosome. RNA 11: 533-557. (Pubitemid 40594322)
18. Horowitz DS. 2011. The splice is right: Guarantors of fidelity in premRNA splicing. RNA 17: 551-554.
19. Horowitz DS. 2012. The mechanism of the second step of pre-mRNA splicing. Wiley Interdiscip Rev RNA 3: 331-350.
20. Ilagan JO, Chalkley RJ, Burlingame AL, Jurica MS. 2013. Rearrangements within human spliceosomes captured after exon ligation. RNA 19: 400-412.
21. James SA, TurnerW, Schwer B. 2002. How Slu7 and Prp18 cooperate in the second step of yeast pre-mRNA splicing. RNA 8: 1068-1077.
22. Kettling U, Koltermann A, Schwille P, Eigen M. 1998. Real-time enzyme kinetics monitored by dual-color fluorescence cross-correlation spectroscopy. Proc Natl Acad Sci 95: 1416-1420.
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. Koodathingal P, Novak T, Piccirilli JA, Staley JP. 2010. The DEAH box ATPases Prp16 and Prp43 cooperate to proofread 5′ splice site cleavage during pre-mRNA splicing. Mol Cell 39: 385-395.
27. Lardelli RM, Thompson JX, Yates JR III, Stevens SW. 2010. Release of SF3 from the intron branchpoint activates the first step of pre-mRNA splicing. RNA 16: 516-528.
28. Liu YC, Chen HC, Wu NY, Cheng SC. 2007. 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: 5403-5413.
29. McPheeters DS, Schwer B, Muhlenkamp P. 2000. Interaction of the yeast DExH-box RNA helicase prp22p with the 3′ splice site during the second step of nuclear pre-mRNA splicing. Nucleic Acids Res 28: 1313-1321. (Pubitemid 30142673)
30. Meyer M, Plass M, Pérez-Valle J, Eyras E, Vilardell J. 2011. Deciphering 3′ ss selection in the yeast genome reveals an RNA thermosensor that mediates alternative splicing. Mol Cell 43: 1033-1039.
31. Mütze J, Ohrt T, Schwille P. 2011. Fluorescence correlation spectroscopy in vivo. Laser Photon Rev 5: 52-67.
32. Ohrt T, Mütze J, Staroske W, Weinmann L, Hock J, Crell K, Meister G, Schwille P. 2008. Fluorescence correlation spectroscopy and fluorescence cross-correlation spectroscopy reveal the cytoplasmic origination of loaded nuclear RISC in vivo in human cells. Nucleic Acids Res 36: 6439-6449.
33. Ohrt T, Staroske W, Mütze J, Crell K, Landthaler M, Schwille P. 2011. Fluorescence cross-correlation spectroscopy reveals mechanistic insights into the effect of 2′-O-methyl modified siRNAs in living cells. Biophys J 100: 2981-2990.
34. 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.
35. Ricka J, Binkert T. 1989. Direct measurement of a distinct correlation-function by fluorescence cross-correlation. Phys Rev A 39: 2646-2652.
36. 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.
37. Schwer B. 2008. A conformational rearrangement in the spliceosome sets the stage for Prp22-dependent mRNA release. Mol Cell 30: 743-754. (Pubitemid 351815129)
38. 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. (Pubitemid 28154537)
39. Schwer B, Guthrie C. 1992. A conformational rearrangement in the spliceosome is dependent on PRP16 and ATP hydrolysis. EMBO J 11: 5033-5039. (Pubitemid 23023447)
40. Schwille P, Meyer-Almes FJ, Rigler R. 1997. Dual-color fluorescence cross-correlation spectroscopy for multicomponent diffusional analysis in solution. Biophys J 72: 1878-1886. (Pubitemid 27133126)
41. 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. (Pubitemid 39507850)
42. 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)
43. Staley JP, Guthrie C. 1998. Mechanical devices of the spliceosome: Motors, clocks, springs, and things. Cell 92: 315-326. (Pubitemid 28093010)
44. Steitz TA, Steitz JA. 1993. A general two-metal-ion mechanism for catalytic RNA. Proc Natl Acad Sci 90: 6498-6502. (Pubitemid 23207240)
45. Teigelkamp S, Newman AJ, Beggs JD. 1995. Extensive interactions of PRP8 protein with the 5′ and 3′ splice sites during splicing suggest a role in stabilization of exon alignment by U5 snRNA. EMBO J 14: 2602-2612.
46. Tseng CK, Liu HL, Cheng SC. 2011. DEAH-box ATPase Prp16 has dual roles in remodeling of the spliceosome in catalytic steps. RNA 17: 145-154.
47. Umen JG, Guthrie C. 1995. Prp16p, Slu7p, and Prp8p interact with the 3′ splice site in two distinct stages during the second catalytic step of pre-mRNA splicing. RNA 1: 584-597.
48. 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.
49. Will CL, Lührmann R. 2011. Spliceosome structure and function. In RNA Worlds (ed. Gesteland RF, Cech TR, Atkins JF), pp. 181-203. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
50. Zhang X, Schwer B. 1997. Functional and physical interaction between the yeast splicing factors Slu7 and Prp18. Nucleic Acids Res 25: 2146-2152. (Pubitemid 27307011)