Link of NTR-Mediated Spliceosome Disassembly with DEAH-Box ATPases Prp2, Prp16, and Prp22

REFERENCES

• Brow DA. 2002. Allosteric cascade of spliceosome activation. Annu. Rev. Genet. 36:333–360.
   PubMed Web of Science ®Google Scholar
• Burge CB, Tuschl TH, Sharp PA. 1999. Splicing of precursors to mRNAs by the spliceosome, p 525–560. InGesteland RF, Cech TR, Atkins JF (ed),The RNA world, 2nd ed.Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Wahl MC, Will CL, Lührmann RL. 2009. The spliceosome: design principles of a dynamic RNP machine. Cell 136:701–718.
   PubMed Web of Science ®Google Scholar
• Will CL, Lührmann R. 2006. Spliceosome structure and function, p 369–400. InGesteland RF, Cech TR, Atkins JF (ed),The RNA world, 3rd ed.Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Chan S-P, Kao D-I, Tsai W-Y, Cheng S-C. 2003. The Prp19p-associated complex in spliceosome activation. Science 302:279–282.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Makarova OV, Makarov EM, Urlaub H, Will CL, Gentzel M, Wilm M, Lührmann R. 2004. A subset of human 35S U5 proteins, including Prp19, function prior to catalytic step 1 of splicing. EMBO J. 23:2381–2391.
   PubMed Web of Science ®Google Scholar
• Campodonico E, Schwer B. 2002. ATP-dependent remodeling of the spliceosome: intragenic suppressors of release-defective mutants of Saccharomyces cerevisiae Prp22. Genetics 160:407–415.
   PubMedGoogle Scholar
• Chen JY-F, Stands L, Staley JP, Jackups RRJr, Latus LJ, Chang T-H. 2001. Specific alterations of U1-C protein or U1 small nuclear RNA can eliminate the requirement of Prp28p, an essential DEAD box splicing factor. Mol. Cell 7:227–232.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Schwer B. 2001. A new twist on RNA helicases: DExH/D box proteins as RNPases. Nat. Struct. Biol. 8:113–116.
   PubMedGoogle Scholar
• Schwer B, Guthrie C. 1992. A conformational rearrangement in the spliceosome is dependent on PRP16 and ATP hydrolysis. EMBO J. 11:5033–5040.
   PubMed Web of Science ®Google Scholar
• Staley JP, Guthrie C. 1999. An RNA switch at the 5′ splice site requires ATP and the DEAD box protein Prp28p. Mol. Cell 3:55–64.
   PubMed Web of Science ®Google Scholar
• Fleckner J, Zhang M, Valcárcel J, Green MR. 1997. U2AF65 recruits a novel human DEAD box protein required for the U2 snRNP-branchpoint interaction. Genes Dev. 11:1864–1872.
   PubMed Web of Science ®Google Scholar
• Kistler AL, Guthrie C. 2001. Deletion of MUD2, the yeast homolog of U2AF65, can bypass the requirement for Sub2, an essential spliceosomal ATPase. Genes Dev. 15:42–49.
   PubMed Web of Science ®Google Scholar
• Ruby SW, Chang T-H, Abelson J. 1993. Four yeast spliceosomal proteins (PRP5, PRP9, PRP11, and PRP21) interact to promote U2 snRNP binding to pre-mRNA. Genes Dev. 7:1909–1925.
   PubMed Web of Science ®Google Scholar
• Jones MH, Frank DN, Guthrie C. 1995. Characterization and functional ordering of Slu7p and Prp17p during the second step of pre-mRNA splicing in yeast. Proc. Natl. Acad. Sci. U. S. A. 92:9687–9691.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Lardelli RM, Thompson JX, Yates JRIII, Stevens SW. 2010. Release of SF3 from the intron branchpoint activates the first step of pre-mRNA splicing. RNA 16:516–528.
   PubMed Web of Science ®Google Scholar
• Ohrt T, Prior M, Dannenberg J, Odenwalder P, Dybkov O, Rasche N, Schmitzova J, Gregor I, Fabrizio P, Enderiein J, Lührmann R. 2012. Prp2-mediated protein rearrangements at the catalytic core of the spliceosome as revealed by dcFCCS. RNA 18:1244–1256.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Arenas JE, Abelson JN. 1997. Prp43: an RNA helicase-like factor involved in spliceosome disassembly. Proc. Natl. Acad. Sci. U. S. A. 94:11798–11802.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Wagner JD, Jankowsky E, Company M, Pyle AM, Abelson JN. 1998. The DEAH-box protein PRP22 is an ATPase that mediates ATP-dependent mRNA release from the spliceosome and unwinds RNA duplexes. EMBO J. 17:2926–2937.
   PubMed Web of Science ®Google Scholar
• Maeder C, Kutach AK, Guthrie C. 2009. ATP-dependent unwinding of U4/U6 snRNAs by the Brr2 helicase requires the C terminus of Prp8. Nat. Struct. Mol. Biol. 16:42–48.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Bellare P, Small EC, Huang X, Wohlschlegel JA, Staley JP, Sontheimer EJ. 2008. A role for ubiquitin in the spliceosome assembly pathway. Nat. Struct. Mol. Biol. 15:444–451.
   PubMed Web of Science ®Google Scholar
• Small EC, Leggett SR, Winans AA, Staley JP. 2006. The EF-G-like GTPase Snu114p regulates spliceosome dynamics mediated by Brr2p, a DExD/H box ATPase. Mol. Cell 23:389–399.
   PubMed Web of Science ®Google Scholar
• Maeder C, Guthrie C. 2008. Modifications target spliceosome dynamics. Nat. Struct. Mol. Biol. 15:426–428.
   PubMedGoogle Scholar
• Mathew R, Hartmuth K, Möhlmann S, Urlaub H, Ficner R, Lührmann R. 2008. Phosphorylation of human PRP28 by SRPK2 is required for integration of the U4/U6-U5 tri-snRNP into the spliceosome. Nat. Struct. Mol. Biol. 15:435–443.
   PubMed Web of Science ®Google Scholar
• Song EJ, Werner SL, Neubauer J, Stegmeier F, Aspden J, Rio D, Harper JW, Elledge SJ, Kirschner MW, Rape M. 2010. The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev. 24:1434–1447.
   PubMed Web of Science ®Google Scholar
• Tsai R-T, Fu R-H, Yeh F-L, Tseng C-K, Lin Y-C, Huang Y-H, Cheng S-C. 2005. Spliceosome disassembly catalyzed by Prp43 and its associated components Ntr1 and Ntr2. Genes Dev. 19:2991–3003.
   PubMed Web of Science ®Google Scholar
• Tsai R-T, Tseng C-K, Lee P-J, Chen H-C, Fu R-H, Chang K-J, Yeh F-L, Cheng S-C. 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Mayas RM, Maita H, Semlow DR, Staley JP. 2010. Spliceosome discards intermediates via the DEAH box ATPase Prp43p. Proc. Natl. Acad. Sci. U. S. A. 107:10020–10025.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Liu Y-C, Chen H-C, Wu N-Y, Cheng S-C. 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.
   PubMed Web of Science ®Google Scholar
• Tseng C-K, Cheng S-C. 2008. Both catalytic steps of nuclear pre-mRNA splicing are reversible. Science 320:1782–1784.
   PubMedGoogle Scholar
• Chen C-H, Tsai W-Y, Chen H-R, Wang C-H, Cheng S-C. 2001. Identification and characterization of two novel components of the Prp19p-associated complex, Ntc30p and Ntc20p. J. Biol. Chem. 276:488–494.
   PubMedGoogle Scholar
• Schwer B, Meszaros T. 2000. RNA helicase dynamics in pre-mRNA splicing. EMBO J. 19:6582–6591.
   PubMedGoogle Scholar
• Vijayraghavan U, Parker R, Tamm J, Iimura Y, Rossi J, Abelson J, Guthrie C. 1986. Mutations in conserved intron sequences affect multiple steps in the yeast splicing pathway, particularly assembly of the spliceosome. EMBO J. 5:1683–1695.
   PubMed Web of Science ®Google Scholar
• James S, Tirmer W, Schwer B. 2002. How Slu7 and Prp18 cooperate in the second step of yeast pre-mRNA splicing. RNA 8:1068–1077.
   PubMedGoogle Scholar
• Chiu Y-F, Liu Y-C, Chiang T-W, Yeh T-C, Tseng C-K, Wu NY, Cheng S-C. 2009. Cwc25 is a novel splicing factor required after Prp2 and Yju2 to facilitate the first catalytic reaction. Mol. Cell. Biol. 29:5671–5678.
   PubMed Web of Science ®Google Scholar
• Horowitz DS, Abelson J. 1993. Stages in the second reaction of pre-mRNA splicing: the final step is ATP independent. Genes Dev. 7:320–329.
   PubMedGoogle Scholar
• Hotz H-R, Schwer B. 1998. Mutational analysis of the yeast DEAH-box splicing factor Prp16. Genetics 149:807–815.
   PubMedGoogle Scholar
• Plumpton M, McGarvey M, Beggs JD. 1994. A dominant negative mutation in the conserved RNA helicase motif ‘SAT’ causes splicing factor PRP2 to stall in spliceosomes. EMBO J. 13:879–887.
   PubMed Web of Science ®Google Scholar
• van Nues RW, Beggs JD. 2001. Functional contacts with a range of splicing proteins suggest a central role for Brr2p in the dynamic control of the order of events in spliceosomes of Saccharomyces cerevisiae. Genetics 157:1451–1467.
   PubMed Web of Science ®Google Scholar
• Xie J, Beickman K, Otte E, Rymond BC. 1998. Progression through the spliceosome cycle requires Prp38p function for U4/U6 snRNA dissociation. EMBO J. 17:2938–2946.
   PubMedGoogle Scholar
• Pandit S, Lynn B, Rymond BC. 2006. Inhibition of a spliceosome turnover pathway suppresses splicing defects. Proc. Natl. Acad. Sci. U. S. A. 103:13700–13705.
   PubMed Web of Science ®Google Scholar
• 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 73:1377–1392.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Xu Y-Z, Query CC. 2007. Competition between the ATPase Prp5 and branch region-U2 snRNA pairing modulates the fidelity of spliceosome assembly. Mol. Cell 28:838–849.
   PubMed Web of Science ®Google Scholar
• Burgess SM, Guthrie C. 1993. Beat the clock: paradigms for NTPases in the maintenance of biological fidelity. Trends Biochem. Sci. 18:381–384.
   PubMedGoogle Scholar
• Horowitz DS. 2011. The splice is right: guarantors of fidelity in pre-mRNA splicing. RNA 17:551–554.
   PubMed Web of Science ®Google Scholar
• Yean S-L, Wuenschell G, Termini J, Lin R- J. 2000. Metal-ion coordination by U6 small nuclear RNA contributes to catalysis in the spliceosome. Nature 408:881–884.
   PubMed Web of Science ®Google Scholar