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Research Paper

Protein cofactor competition regulates the action of a multifunctional RNA helicase in different pathways

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Pages 320-330 | Received 08 Sep 2015, Accepted 07 Jan 2016, Published online: 01 Mar 2016

References

  • Cordin O, Banroques J, Tanner NK, Linder P. The DEAD-box protein family of RNA helicases. Gene 2006; 367:17-37; PMID:16337753; http://dx.doi.org/10.1016/j.gene.2005.10.019
  • Bleichert F, Baserga SJ. The long unwinding road of RNA helicases. Mol. Cell 2007; 27:339-52; PMID: 17679086; http://dx.doi.org/10.1016/j.molcel.2007.07.014
  • Linder P, Jankowsky E. From unwinding to clamping - the DEAD box RNA helicase family. Nature Rev Mol Cell Biol 2011; 12:505-516;PMID: 21779027; http://dx.doi.org/10.1038/nrm3154
  • Martin R, Straub AU, Doebele C, Bohnsack MT. DExD/H-box RNA helicases in ribosome biogenesis. RNA Biol 2013; 10:4-18; PMID:22922795; http://dx.doi.org/10.4161/rna.21879
  • Rodriguez-Galan O, Garcia-Gomez JJ, de la Cruz J. Yeast and human RNA helicases involved in ribosome biogenesis: current status and perspectives. Biochim Biophys Acta 2013; 1829:775-90; PMID:23357782; http://dx.doi.org/10.1016/j.bbagrm.2013.01.007
  • Hilbert M, Kebbel F, Gubaev A, Klostermeier D. eIF4G stimulates the activity of the DEAD box protein eIF4A by a conformational guidance mechanism. Nucleic Acids Res 2011; 39:2260-70; PMID:21062831; http://dx.doi.org/10.1093/nar/gkq1127
  • Nielsen KH, Behrens MA, He Y, Oliveira CL, Jensen LS, Hoffmann SV, Pedersen JS, Andersen GR. Synergistic activation of eIF4A by eIF4B and eIF4G. Nucleic Acids Res 2011; 39:2678-89; PMID:21113024; http://dx.doi.org/10.1093/nar/gkq1206
  • Cordin O, Hahn D, Beggs JD. Structure, function and regulation of spliceosomal RNA helicases. Curr Opin Cell Biol 2012; 24:431-8; PMID:22464735; http://dx.doi.org/10.1016/j.ceb.2012.03.004
  • Granneman S, Lin C, Champion EA, Nandineni MR, Zorca C, Baserga SJ. The nucleolar protein Esf2 interacts directly with the DExD/H box RNA helicase, Dbp8, to stimulate ATP hydrolysis. Nucleic Acids Res 2006; 34:3189-99; PMID:16772403; http://dx.doi.org/10.1093/nar/gkl419
  • Vos HR, Bax R, Faber AW, Vos JC, Raué HA. U3 snoRNP and Rrp5p associate independently with Saccharomyces cerevisiae 35S pre-rRNA, but Rrp5p is essential for association of Rok1p. Nucleic Acids Res 2004; 32:5827-33; PMID:15523097; http://dx.doi.org/10.1093/nar/gkh904
  • Bohnsack MT, Kos M, Tollervey D. Quantitative analysis of snoRNA association with pre-ribosomes and release of snR30 by Rok1 helicase. EMBO Rep 2008; 9:1230-6; PMID:18833290; http://dx.doi.org/10.1038/embor.2008.184
  • Young CL, Khoshnevis S, Karbstein K. Cofactor-dependent specificity of a DEAD-box protein. Proc Natl Acad Sci 2013; 110:2668-76; PMID: 23630256; http://dx.doi.org/10.1073/pnas.1302577110
  • Martin R, Hackert P, Ruprecht M, Simm S, Brüning L, Mirus O, Sloan KE, Kudla G, Schleiff E, Bohnsack MT. A pre-ribosomal RNA interaction network involving snoRNAs and the Rok1 helicase. RNA 2014; 20:1173-82; PMID:24947498; http://dx.doi.org/10.1261/rna.044669.114
  • Aravind L, Koonin EV. G-patch: a new conserved domain in eukaryotic RNA-processing proteins and type D retroviral polyproteins. Trends Biochem Sci 1999; 24:342-4; PMID:10470032; http://dx.doi.org/10.1016/S0968-0004(99)01437-1
  • Robert-Paganin J, Réty S, Leulliot N. Regulation of DEAH/RHA helicases by G-patch proteins. Biomed Res Int 2015; 2015:931857; PMID:25692149; http://dx.doi.org/10.1155/2015/931857
  • Roy J, Kim K, Maddock JR, Anthony JG, Woolford JL. Jr The final stages of spliceosome maturation require Spp2p that can interact with the DEAH box protein Prp2p and promote step 1 of splicing. RNA 1995; 1:375-90; PMID:7493316
  • Edwalds-Gilbert G, Kim DH, Silverman E, Lin RJ. Definition of a spliceosome interaction domain in yeast Prp2 ATPase. RNA 2004; 10:210-20; PMID:14730020; http://dx.doi.org/10.1261/rna.5151404
  • 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
  • Tsai R T, Fu RH, Yeh FL, Tseng CK, Lin YC, Huang YH, Cheng SC. Spliceosome disassembly catalyzed by Prp43 and its associated components Ntr1 and Ntr2. Genes Dev 2005; 19:2991-3003; PMID:16357217; http://dx.doi.org/10.1101/gad.1377405
  • Boon KL, Auchynnikava T, Edwalds-Gilbert G, Barrass JD, Droop AP, Dez C, Beggs JD. Yeast ntr1/spp382 mediates prp43 function in postspliceosomes. Mol Cell Biol 2006; 26:6016-23; PMID:16880513; http://dx.doi.org/10.1128/MCB.02347-05
  • Arenas JE, Abelson JN. Prp43: An RNA helicase-like factor involved in spliceosome disassembly. Proc. Natl. Acad. Sci. 1997; 94:11798-802; PMID:9342317; http://dx.doi.org/10.1073/pnas.94.22.11798
  • Martin A, Schneider S, Schwer B. Prp43 is an essential RNA-dependent ATPase required for release of lariat-intron from the spliceosome. J Biol Chem 2002; 277:17743-50; PMID:11886864; http://dx.doi.org/10.1074/jbc.M200762200
  • Ebersberger I, Simm S, Leisegang MS, Schmitzberger P, Mirus O, von Haeseler A, Bohnsack MT, Schleiff E. The evolution of the ribosome biogenesis pathway from a yeast perspective. Nucleic Acids Res 2014; 42:1509-23; PMID:24234440; http://dx.doi.org/10.1093/nar/gkt1137
  • Gee S, Krauss SW, Miller E, Aoyagi K, Arenas J, Conboy J G. Cloning of mDEAH9, a putative RNA helicase and mammalian homologue of Saccharomyces cerevisiae splicing factor Prp43. Proc Natl Acad Sci 1997; 94:11803-7; PMID:9342318; http://dx.doi.org/10.1073/pnas.94.22.11803
  • Wen X, Lei YP, Zhou YL, Okamoto CT, Snead ML, Paine, M.L. Structural organization and cellular localization of tuftelin-interacting protein 11 (TFIP11). Cell Mol Life Sci 2005; 62:1038-46; PMID:15868102; http://dx.doi.org/10.1007/s00018-005-4547-z
  • Guglielmi B, Werner M. The yeast homolog of human PinX1 is involved in rRNA and small nucleolar RNA maturation, not in telomere elongation inhibition. J Biol Chem 2002; 277:35712-9; PMID:12107183; http://dx.doi.org/10.1074/jbc.M205526200
  • Lebaron S, Papin C, Capeyrou R, Chen YL, Froment C, Monsarrat B, Caizergues-Ferrer M, Grigoriev M, Henry Y. The ATPase and helicase activities of Prp43p are stimulated by the G-patch protein Pfa1p during yeast ribosome biogenesis. EMBO J 2009; 28:3808-19; PMID:19927118; http://dx.doi.org/10.1038/emboj.2009.335
  • Lebaron S, Froment C, Fromont-Racine M, Rain JC, Monsarrat B, Caizergues-Ferrer M, Henry Y. The splicing ATPase prp43p is a component of multiple preribosomal particles. Mol Cell Biol 2005; 25:9269-82; PMID:16227579; http://dx.doi.org/10.1128/MCB.25.21.9269-9282.2005
  • Chen YL, Capeyrou R, Humbert O, Mouffok S, Kadri YA, Lebaron S, Henras AK, Henry Y. The telomerase inhibitor Gno1p/PINX1 activates the helicase Prp43p during ribosome biogenesis. Nucleic Acids Res 2014; 42:7330-45; PMID:24823796; http://dx.doi.org/10.1093/nar/gku357
  • Combs DJ, Nagel RJ, Ares M, Stevens SW. Prp43p is a DEAH-box spliceosome disassembly factor essential for ribosome biogenesis. Mol Cell Biol 2006; 26:523-34; PMID:16382144; http://dx.doi.org/10.1128/MCB.26.2.523-534.2006
  • Leeds NB, Small EC, Hiley SL, Hughes TR, Staley JP. The splicing factor Prp43p, a DEAH box ATPase, functions in ribosome biogenesis. Mol Cell Biol 2006; 26:513-22; PMID:16382143; http://dx.doi.org/10.1128/MCB.26.2.513-522.2006
  • Granneman S, Kudla G, Petfalski E, Tollervey D. Identification of protein binding sites on U3 snoRNA and pre-rRNA by UV cross-linking and high-throughput analysis of cDNAs. Proc Natl Acad Sci 2009; 106:9613-8; http://dx.doi.org/10.1073/pnas.0901997106
  • Bohnsack MT, Tollervey D, Granneman S. Identification of RNA helicase target sites by UV cross-linking and analysis of cDNA. Methods Enzymol. 2012; 511:275-88; PMID:22713325; http://dx.doi.org/10.1016/B978-0-12-396546-2.00013-9
  • Bohnsack MT, Martin R, Granneman S, Ruprecht M, Schleiff E, Tollervey D. Prp43 bound at different sites on the pre-rRNA performs distinct functions in ribosome synthesis. Mol Cell 2009; 36:583-92; PMID: 19941819; http://dx.doi.org/10.1016/j.molcel.2009.09.039
  • Pertschy B, Schneider C, Gnädig M, Schäfer T, Tollervey D, Hurt E. RNA helicase Prp43 and its co-factor Pfa1 promote 20 to 18 S rRNA processing catalyzed by the endonuclease Nob1. J Biol Chem 2009; 284:35079-91; PMID:19801658; http://dx.doi.org/10.1074/jbc.M109.040774
  • Watkins NJ, Bohnsack MT. The box C/D and H/ACA snoRNPs: key players in the modification, processing and the dynamic folding of ribosomal RNA. Wiley Interdiscip Rev RNA 2012; 3:397-414; PMID:22065625; http://dx.doi.org/10.1002/wrna.117
  • Tanaka N, Aronova A, Schwer B. Ntr1 activates the Prp43 helicase to trigger release of intron-lariat from the spliceosome. Genes Dev 2007; 21:2312-25; PMID:17875666; http://dx.doi.org/10.1101/gad.1580507
  • 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; http://dx.doi.org/10.1038/emboj.2010.102
  • 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
  • Warkocki Z, Schneider C, Mozaffari-Jovin S, Schmitzová J, Höbartner 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
  • Mick DU, Wagner K, van der Laan M, Frazier AE, Perschil I, Pawlas M, Meyer HE, Warscheid B, Rehling P. Shy1 couples Cox1 translational regulation to cytochrome c oxidase assembly. EMBO J 2007; 26:4347-58; PMID:17882259; http://dx.doi.org/10.1038/sj.emboj.7601862
  • Pandit S, Paul S, Zhang L, Chen M, Durbin N, Harrison SM, Rymond BC. Spp382p interacts with multiple yeast splicing factors, including possible regulators of Prp43 DExD/H-Box protein function. Genetics 2009; 183:195-206; PMID:19581443; http://dx.doi.org/10.1534/genetics.109.106955
  • Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS. Global analysis of protein expression in yeast. Nature 2003; 425:737-41; PMID:14562106; http://dx.doi.org/10.1038/nature02046
  • Mayas RM, Maita H, Semlow DR, Staley JP. Spliceosome discards intermediates via the DEAH box ATPase Prp43p. Proc. Natl. Acad. Sci. 2010; 107:10020-5; PMID:20463285; http://dx.doi.org/10.1073/pnas.0906022107
  • Fourmann JB, Schmitzová 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
  • Gornicka A, Bragoszewski P, Chroscicki P, Wenz LS, Schulz C, Rehling P, Chacinska A A discrete pathway for the transfer of intermembrane space proteins across the outer membrane of mitochondria. Mol. Biol. Cell 2014; 25:3999-4009; PMID:25318675; http://dx.doi.org/10.1091/mbc.E14-06-1155
  • Zhou XZ, Lu KP. The Pin2/TRF1-interacting protein PinX1 is a potent telomerase inhibitor. Cell 2001; 107:347-59; PMID:11701125; http://dx.doi.org/10.1016/S0092-8674(01)00538-4
  • Lin J, Blackburn EH. Nucleolar protein PinX1p regulates telomerase by sequestering its protein catalytic subunit in an inactive complex lacking telomerase RNA. Genes Dev. 2004; 18:387-96; PMID:14977919; http://dx.doi.org/10.1101/gad.1171804
  • Banerjee D, McDaniel PM, Rymond BC. Limited Portability of G-Patch Domains in Regulators of the Prp43 RNA Helicase Required for Pre-mRNA Splicing and Ribosomal RNA Maturation in Saccharomyces cerevisiae. Genetics 2015; 200:135-417; PMID:25808954; http://dx.doi.org/10.1534/genetics.115.176461
  • Swaney DL, Beltrao P, Starita L, Guo A, Rush J, Fields S, Krogan NJ, Villen J. Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation. Nat Methods 2013; 10:676-82; PMID: 23749301; http://dx.doi.org/10.1038/nmeth.2519
  • Niu Z, Jin W, Zhang L, Li X. Tumor suppressor RBM5 directly interacts with the DExD/H-box protein DHX15 and stimulates its helicase activity. FEBS Lett. 2012; 586:977-83; PMID:22569250; http://dx.doi.org/10.1016/j.febslet.2012.02.052
  • Hu FY, Wu C, Li Y, Xu K, Wang WJ, Cao H, Tian XL. AGGF1 is a novel anti-inflammatory factor associated with TNF-α-induced endothelial activation. Cell Signal. 2013; 25:1645-53; PMID:23628701; http://dx.doi.org/10.1016/j.cellsig.2013.04.007
  • Steimer L, Klostermeier D. RNA helicases in infection and disease. RNA Biol. 2012; 9:751-71; PMID:22699555; http://dx.doi.org/10.4161/rna.20090
  • Leulliot N, Bohnsack MT, Graille M, Tollervey D, Van Tilbeurgh H. The yeast ribosome synthesis factor Emg1 is a novel member of the superfamily of α/β knot fold methyltransferases. Nucleic Acids Res. 2008; 36:629-39; PMID:18063569; http://dx.doi.org/10.1093/nar/gkm1074
  • Lehmann P, Bohnsack MT, Schleiff E. The functional domains of the unusual chloroplast positioning protein 1. Plant Science 2011; 180:650-4; PMID:21421414; http://dx.doi.org/10.1016/j.plantsci.2011.01.006
  • Adam H. Adenosin-5′diphosphat und Adenosin-5′monophosphat. In Methoden der enzymatischen Analyse Bergmeyer HU (ed.) 1962; Weinheim: Verlag Chemie:573-7
  • James P, Halladay J, Craig EA. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 1996; 144:1425-36; PMID:8978031
  • Boon KL, Kos M. Deletion of Swm2p selectively impairs trimethylation of snRNAs by trimethylguanosine synthase (Tgs1p). FEBS Lett 2010; 584:3299-304; PMID:20621096; http://dx.doi.org/10.1016/j.febslet.2010.07.001
  • Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998; 14:953-61; PMID:9717241; http://dx.doi.org/10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U
  • Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, Maekawa H, Moreno-Borchart A, Doenges G, Schwob E, Schiebel E, Knop M. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassetes. Yeast 2004; 21:947-62; PMID:15334558; http://dx.doi.org/10.1002/yea.1142
  • Teng X, Hardwick JM. Reliable method for detection of programmed cell death in yeast. Methods Mol Biol 2009; 559:335-42; PMID:19609767; http://dx.doi.org/10.1007/978-1-60327-017-5_23