Interplay of cis- and trans-regulatory mechanisms in the spliceosomal RNA helicase Brr2

References

• Wahl MC, Will CL, Lührmann R. The spliceosome: design principles of a dynamic RNP machine. Cell 2009; 136:701-18; PMID:19239890; http://dx.doi.org/10.1016/j.cell.2009.02.009
   PubMed Web of Science ®Google Scholar
• Will CL, Lührmann R. Spliceosome structure and function. Cold Spring Harb Perspect Biol 2011; 3:1-24; http://dx.doi.org/10.1101/cshperspect.a003707
   Web of Science ®Google Scholar
• Brow DA. Allosteric cascade of spliceosome activation. Annu Rev Genet 2002; 36:333-60; PMID:12429696; http://dx.doi.org/10.1146/annurev.genet.36.043002.091635
   PubMed Web of Science ®Google Scholar
• Staley JP, Guthrie C. Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 1998; 92:315-26; PMID:9476892; http://dx.doi.org/10.1016/S0092-8674(00)80925-3
   PubMed Web of Science ®Google Scholar
• Raghunathan PL, Guthrie C. RNA unwinding in U4/U6 snRNPs requires ATP hydrolysis and the DEIH-box splicing factor Brr2. Curr Biol 1998; 8:847-55; PMID:9705931; http://dx.doi.org/10.1016/S0960-9822(07)00345-4
   PubMed Web of Science ®Google Scholar
• Laggerbauer B, Achsel T, Lührmann R. The human U5-200kD DEXH-box protein unwinds U4/U6 RNA duplices in vitro. Proc Natl Acad Sci USA 1998; 95:4188-92; PMID:9539711; http://dx.doi.org/10.1073/pnas.95.8.4188
   PubMed Web of Science ®Google Scholar
• Agafonov DE, Deckert J, Wolf E, Odenwalder P, Bessonov S, Will CL, Urlaub H, Lührmann R. Semiquantitative proteomic analysis of the human spliceosome via a novel two-dimensional gel electrophoresis method. Mol Cell Biol 2011; 31:2667-82; PMID:21536652; http://dx.doi.org/10.1128/MCB.05266-11
   PubMed Web of Science ®Google Scholar
• Theuser M, Hobartner C, Wahl MC, Santos KF. Substrate-assisted mechanism of RNP disruption by the spliceosomal Brr2 RNA helicase. Proc Natl Acad Sci USA 2016; 113:7798-803; PMID:27354531; http://dx.doi.org/10.1073/pnas.1524616113
   PubMed Web of Science ®Google Scholar
• Sashital DG, Cornilescu G, McManus CJ, Brow DA, Butcher SE. U2-U6 RNA folding reveals a group II intron-like domain and a four-helix junction. Nat Struct Mol Biol 2004; 11:1237-42; PMID:15543154; http://dx.doi.org/10.1038/nsmb863
   PubMed Web of Science ®Google Scholar
• Fica SM, Tuttle N, Novak T, Li NS, Lu J, Koodathingal P, Dai Q, Staley JP, Piccirilli JA. RNA catalyses nuclear pre-mRNA splicing. Nature 2013; 503:229-34; PMID:24196718
   PubMed Web of Science ®Google Scholar
• Hang J, Wan R, Yan C, Shi Y. Structural basis of pre-mRNA splicing. Science 2015; 349:1191-8; PMID:26292705; http://dx.doi.org/10.1126/science.aac8159
   PubMed Web of Science ®Google Scholar
• Kim DH, Rossi JJ. The first ATPase domain of the yeast 246-kDa protein is required for in vivo unwinding of the U4/U6 duplex. RNA 1999; 5:959-71; PMID:10411139; http://dx.doi.org/10.1017/S135583829999012X
   PubMed Web of Science ®Google Scholar
• Santos KF, Mozaffari-Jovin S, Weber G, Pena V, Lührmann R, Wahl MC. Structural basis for functional cooperation between tandem helicase cassettes in Brr2-mediated remodeling of the spliceosome. Proc Natl Acad Sci USA 2012; 109:17418-23; PMID:23045696; http://dx.doi.org/10.1073/pnas.1208098109
   PubMed Web of Science ®Google Scholar
• Pena V, Mozaffari-Jovin S, Fabrizio P, Orlowski J, Bujnicki JM, Lührmann R, Wahl MC. Common design principles in the spliceosomal RNA helicase Brr2 and in the Hel308 DNA helicase. Mol Cell 2009; 35:454-66; PMID:19716790; http://dx.doi.org/10.1016/j.molcel.2009.08.006
   PubMed Web of Science ®Google Scholar
• Zhang L, Xu T, Maeder C, Bud LO, Shanks J, Nix J, Guthrie C, Pleiss JA, Zhao R. Structural evidence for consecutive Hel308-like modules in the spliceosomal ATPase Brr2. Nat Struct Mol Biol 2009; 16:731-9; PMID:19525970; http://dx.doi.org/10.1038/nsmb.1625
   PubMed Web of Science ®Google Scholar
• Hahn D, Kudla G, Tollervey D, Beggs JD. Brr2p-mediated conformational rearrangements in the spliceosome during activation and substrate repositioning. Genes Dev 2012; 26:2408-21; PMID:23124065; http://dx.doi.org/10.1101/gad.199307.112
   PubMed Web of Science ®Google Scholar
• Mayerle M, Guthrie C. Prp8 retinitis pigmentosa mutants cause defects in the transition between the catalytic steps of splicing. RNA 2016; 22:793-809; PMID:26968627; http://dx.doi.org/10.1261/rna.055459.115
   PubMed Web of Science ®Google Scholar
• Small EC, Leggett SR, Winans AA, Staley JP. The EF-G-like GTPase Snu114p regulates spliceosome dynamics mediated by Brr2p, a DExD/H box ATPase. Mol Cell 2006; 23:389-99; PMID:16885028; http://dx.doi.org/10.1016/j.molcel.2006.05.043
   PubMed Web of Science ®Google Scholar
• Fourmann JB, Schmitzova J, Christian H, Urlaub H, Ficner R, Boon KL, Fabrizio P, Lührmann R. Dissection of the factor requirements for spliceosome disassembly and the elucidation of its dissociation products using a purified splicing system. Genes Dev 2013; 27:413-28; PMID:23431055; http://dx.doi.org/10.1101/gad.207779.112
   PubMed Web of Science ®Google Scholar
• Absmeier E, Wollenhaupt J, Mozaffari-Jovin S, Becke C, Lee CT, Preussner M, Heyd F, Urlaub H, Lührmann R, Santos KF, et al. The large N-terminal region of the Brr2 RNA helicase guides productive spliceosome activation. Genes Dev 2015; 29:2576-87; PMID:26637280
   PubMed Web of Science ®Google Scholar
• Absmeier E, Rosenberger L, Apelt L, Becke C, Santos KF, Stelzl U, Wahl MC. A noncanonical PWI domain in the N-terminal helicase-associated region of the spliceosomal Brr2 protein. Acta Crystallogr D 2015; 71:762-71; PMID:25849387; http://dx.doi.org/10.1107/S1399004715001005
   PubMedGoogle Scholar
• Mozaffari-Jovin S, Wandersleben T, Santos KF, Will CL, Lührmann R, Wahl MC. Novel regulatory principles of the spliceosomal Brr2 RNA helicase and links to retinal disease in humans. RNA Biol 2014; 11:298-312; PMID:24643059; http://dx.doi.org/10.4161/rna.28353
   PubMed Web of Science ®Google Scholar
• Mozaffari-Jovin S, Wandersleben T, Santos KF, Will CL, Lührmann R, Wahl MC. Inhibition of RNA helicase Brr2 by the C-terminal tail of the spliceosomal protein Prp8. Science 2013; 341:80-4; PMID:23704370; http://dx.doi.org/10.1126/science.1237515
   PubMed Web of Science ®Google Scholar
• Nguyen TH, Li J, Galej WP, Oshikane H, Newman AJ, Nagai K. Structural basis of Brr2-Prp8 interactions and implications for U5 snRNP biogenesis and the spliceosome active site. Structure 2013; 21:910-19; PMID:23727230; http://dx.doi.org/10.1016/j.str.2013.04.017
   PubMed Web of Science ®Google Scholar
• Maeder C, Kutach AK, Guthrie C. ATP-dependent unwinding of U4/U6 snRNAs by the Brr2 helicase requires the C terminus of Prp8. Nat Struct Mol Biol 2009; 16:42-8; PMID:19098916; http://dx.doi.org/10.1038/nsmb.1535
   PubMed Web of Science ®Google Scholar
• Mozaffari-Jovin S, Santos KF, Hsiao HH, Will CL, Urlaub H, Wahl MC, Lührmann R. The Prp8 RNase H-like domain inhibits Brr2-mediated U4/U6 snRNA unwinding by blocking Brr2 loading onto the U4 snRNA. Genes Dev 2012; 26:2422-34; PMID:23124066; http://dx.doi.org/10.1101/gad.200949.112
   PubMed Web of Science ®Google Scholar
• Nguyen TH, Galej WP, Bai XC, Oubridge C, Newman AJ, Scheres SH, Nagai K. Cryo-EM structure of the yeast U4/U6.U5 tri-snRNP at 3.7 A resolution. Nature 2016; 530:298-302; PMID:26829225; http://dx.doi.org/10.1038/nature16940
   PubMed Web of Science ®Google Scholar
• Walbott H, Mouffok S, Capeyrou R, Lebaron S, Humbert O, van Tilbeurgh H, Henry Y, Leulliot N. Prp43p contains a processive helicase structural architecture with a specific regulatory domain. EMBO J 2010; 29:2194-204; PMID:20512115; http://dx.doi.org/10.1038/emboj.2010.102
   PubMed Web of Science ®Google Scholar
• Tanaka N, Aronova A, Schwer B. Ntr1 activates the Prp43 helicase to trigger release of lariat-intron from the spliceosome. Genes Dev 2007; 21:2312-25; PMID:17875666; http://dx.doi.org/10.1101/gad.1580507
   PubMed Web of Science ®Google Scholar
• Christian H, Hofele RV, Urlaub H, Ficner R. Insights into the activation of the helicase Prp43 by biochemical studies and structural mass spectrometry. Nucleic Acids Res 2014; 42:1162-79; PMID:24165877; http://dx.doi.org/10.1093/nar/gkt985
   PubMed Web of Science ®Google Scholar
• Silverman EJ, Maeda A, Wei J, Smith P, Beggs JD, Lin RJ.-- Interaction between a G-patch protein and a spliceosomal DEXD/H-box ATPase that is critical for splicing. Mol Cell Biol 2004; 24:10101-10; PMID:15542821; http://dx.doi.org/10.1128/MCB.24.23.10101-10110.2004
   PubMed Web of Science ®Google Scholar
• Warkocki Z, Schneider C, Mozaffari-Jovin S, Schmitzova J, -Hobartner C, Fabrizio P, Lührmann R. The G-patch protein Spp2 couples the spliceosome-stimulated ATPase activity of the DEAH-box protein Prp2 to catalytic activation of the spliceosome. Genes Dev 2015; 29:94-107; PMID:25561498; http://dx.doi.org/10.1101/gad.253070.114
   PubMed Web of Science ®Google Scholar
• van Nues RW, Beggs JD. 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 2001; 157:1451-67; PMID:11290703
   PubMed Web of Science ®Google Scholar
• Wan RX, Yan CY, Bai R, Wang L, Huang M, Wong CC, Shi Y. The 3.8 Å structure of the U4/U6.U5 tri-snRNP: Insights into spliceosome assembly and catalysis. Science 2016; 351:466-75; PMID:26743623; http://dx.doi.org/10.1126/science.aad6466
   PubMed Web of Science ®Google Scholar
• Agafonov DE, Kastner B, Dybkov O, Hofele RV, Liu WT, Urlaub H, Lührmann R, Stark H. Molecular architecture of the human U4/U6.U5 tri-snRNP. Science 2016; 351:1416-20; PMID:26912367; http://dx.doi.org/10.1126/science.aad2085
   PubMed Web of Science ®Google Scholar
• Galej WP, Wilkinson ME, Fica SM, Oubridge C, Newman AJ, Nagai K. Cryo-EM structure of the spliceosome immediately after branching. Nature 2016; 537:197-201; PMID:27459055; http://dx.doi.org/10.1038/nature19316
   PubMed Web of Science ®Google Scholar
• Yan C, Wan R, Bai R, Huang G, Shi Y. Structure of a yeast activated spliceosome at 3.5 A resolution. Science 2016; 353:904-11; PMID:27445306; http://dx.doi.org/10.1126/science.aag0291
   PubMed Web of Science ®Google Scholar
• Rauhut R, Fabrizio P, Dybkov O, Hartmuth K, Pena V, Chari A, Kumar V, Lee CT, Urlaub H, Kastner B, et al. Molecular architecture of the Saccharomyces cerevisiae activated spliceosome. Science 2016; 353:1399-1405; PMID:27562955
   PubMed Web of Science ®Google Scholar
• Wan R, Yan C, Bai R, Huang G, Shi Y. Structure of a yeast catalytic step I spliceosome at 3.4 Å resolution. Science 2016; 353:895-904; PMID:27445308; http://dx.doi.org/10.1126/science.aag2235
   PubMed Web of Science ®Google Scholar
• Yan C, Hang J, Wan R, Huang M, Wong CC, Shi Y. Structure of a yeast spliceosome at 3.6-Å resolution. Science 2015; 349:1182-91; PMID:26292707; http://dx.doi.org/10.1126/science.aac7629
   PubMed Web of Science ®Google Scholar
• Studier FW. Protein production by auto-induction in high-density shaking cultures. Protein Express Purif 2005; 41:207-34; http://dx.doi.org/10.1016/j.pep.2005.01.016
   PubMed Web of Science ®Google Scholar
• Mueller U, Forster R, Hellmig M, Huschmann FU, Kastner A, Malecki P, Pühringer S, Röwer M, Sparta K, Steffien M, Ühlein M, Wilk P, Weiss MS. The macromolecular crystallography beamlines at BESSY II of the Helmholtz-Zentrum Berlin: Current status and perspectives. Eur Phys J Plus 2015; 130:141; http://dx.doi.org/10.1140/epjp/i2015-15141-2
   Web of Science ®Google Scholar
• Kabsch W. XDS. Acta Crystallogr D 2010; 66:125-32.
   PubMed Web of Science ®Google Scholar
• McCoy AJ. Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D 2007; 63:32-41; PMID:17164524; http://dx.doi.org/10.1107/S0907444906045975
   PubMedGoogle Scholar
• Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D 2004; 60:2126-32; PMID:15572765; http://dx.doi.org/10.1107/S0907444904019158
   PubMed Web of Science ®Google Scholar
• Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Nicholls RA, Winn MD, Long F, Vagin AA. Refmac5 for the refinement of macromolecular crystal structures. Acta Crystallogr D 2011; 67:355-67; PMID:21460454; http://dx.doi.org/10.1107/S0907444911001314
   PubMed Web of Science ®Google Scholar
• Schroder GF, Levitt M, Brunger AT. Deformable elastic network refinement for low-resolution macromolecular crystallography. Acta Crystallogr D 2014; 70:2241-55; PMID:25195739; http://dx.doi.org/10.1107/S1399004714016496
   PubMedGoogle Scholar
• Afonine PV, Grosse-Kunstleve RW, Echols N, Headd JJ, Moriarty NW, Mustyakimov M, Terwilliger TC, Urzhumtsev A, Zwart PH, Adams PD. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr D 2012; 68:352-67; PMID:22505256; http://dx.doi.org/10.1107/S0907444912001308
   PubMedGoogle Scholar
• Bunkoczi G, Read RJ. Improvement of molecular-replacement models with Sculptor. Acta Crystallogr D 2011; 67:303-12; PMID:21460448; http://dx.doi.org/10.1107/S0907444910051218
   PubMedGoogle Scholar
• Ryder SP, Recht MI, Williamson JR. Quantitative analysis of protein-RNA interactions by gel mobility shift. Methods Mol Biol 2008; 488:99-115; PMID:18982286; http://dx.doi.org/10.1007/978-1-60327-475-3_7
   PubMedGoogle Scholar