DEAD-Box RNA helicase Dbp4 is required for small-subunit processome formation and function

Molecular and Cellular Biology

Volumn 35, Issue 5, 2015, Pages 816-830

  Soltanieh, Sahar ^a,c   Osheim, Yvonne ^b   Spasov, Krasimir ^a,d   Trahan, Christian ^a,c   Beyer, Ann ^b   Dragon, François ^a  

^a UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

^b UNIVERSITY OF VIRGINIA   (United States)

^c CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEAD BOX RNA HELICASE DBP4; HELICASE; HEMAGGLUTININ; PEPTIDES AND PROTEINS; RIBONUCLEOPROTEIN; RNA 18S; SMALL NUCLEOLAR RIBONUCLEOPROTEIN; SMALL NUCLEOLAR RNA; SMALL SUBUNIT PROCESSOME; UNCLASSIFIED DRUG; CHROMATIN; DEAD BOX PROTEIN; HCA4 PROTEIN, S CEREVISIAE; MPP10 PROTEIN, S CEREVISIAE; PHOSPHOPROTEIN; RNA HELICASE; RNA POLYMERASE; RNA, U3 SMALL NUCLEOLAR; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL GROWTH; COMPLEX FORMATION; CONTROLLED STUDY; DEPLETION; DNA FLANKING REGION; ELECTRON MICROSCOPY; IMMUNOPRECIPITATION; NONHUMAN; POLYSOME; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RIBOSOME; RIBOSOME SUBUNIT; RNA PROCESSING; RNA SYNTHESIS; SEDIMENTATION; YEAST; CHEMISTRY; CHROMATIN; DENSITY GRADIENT CENTRIFUGATION; GENETICS; GENOTYPE; METABOLISM; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

IPS;

CENTRIFUGATION, DENSITY GRADIENT; CHROMATIN; DEAD-BOX RNA HELICASES; GENOTYPE; MICROSCOPY, ELECTRON; PHOSPHOPROTEINS; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOPROTEINS; RIBOSOMES; RNA HELICASES; RNA NUCLEOTIDYLTRANSFERASES; RNA, RIBOSOMAL, 18S; RNA, SMALL NUCLEOLAR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84947899905     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01348-14     Document Type: Article

References (53)

1. Venema J, Tollervey D. 1999. Ribosome synthesis in Saccharomyces cerevisiae. Annu Rev Genet 33:261-311. http://dx.doi.org/10.1146/annurev .genet.33.1.261.
2. Moore PB, Steitz TA. 2002. The involvement of RNA in ribosome function. Nature 418:229-235. http://dx.doi.org/10.1038/418229a.
3. Kressler D, Linder P, de La Cruz J. 1999. Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae. Mol Cell Biol 19:7897-7912.
4. Fromont-Racine M, Senger B, Saveanu C, Fasiolo F. 2003. Ribosome assembly in eukaryotes. Gene 313:17-42. http://dx.doi.org/10.1016 /S0378-1119(03)00629-2.
5. Henras AK, Soudet J, Gerus M, Lebaron S, Caizergues-Ferrer M, Mougin A, Henry Y. 2008. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci 65:2334-2359. http://dx.doi.org/10 .1007/s00018-008-8027-0.
6. Kressler D, Hurt E, Bassler J. 2010. Driving ribosome assembly. Biochim Biophys Acta 1803:673-683. http://dx.doi.org/10.1016/j.bbamcr.2009.10 .009.
7. Henras AK, Dez C, Henry Y. 2004. RNA structure and function in C/D and H/ACA s(no)RNPs. Curr Opin Struct Biol 14:335-343. http://dx.doi .org/10.1016/j.sbi.2004.05.006.
8. Kiss T. 2001. Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs. EMBOJ 20:3617-3622. http://dx.doi.org/10.1093 /emboj/20.14.3617.
9. Decatur WA, Fournier MJ. 2003. RNA-guided nucleotide modification of ribosomal and other RNAs. J Biol Chem 278:695-698. http://dx.doi.org /10.1074/jbc.R200023200.
10. Maxwell ES, Fournier MJ. 1995. The small nucleolar RNAs. Annu Rev Biochem 64:897-934. http://dx.doi.org/10.1146/annurev.bi.64.070195 .004341.
11. King TH, Liu B, McCully RR, Fournier MJ. 2003. Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol Cell 11:425-435. http://dx.doi.org /10.1016/S1097-2765(03)00040-6.
12. Liang XH, Liu Q, King TH, Fournier MJ. 2010. Strong dependence between functional domains in a dual-function snoRNA infers coupling of rRNA processing and modification events. Nucleic Acids Res 38:3376-3387. http://dx.doi.org/10.1093/nar/gkq043.
13. Woolford JL, Jr, Baserga SJ. 2013. Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 195:643-681. http://dx.doi.org/10 .1534/genetics.113.153197.
14. Piekna-Przybylska D, Decatur WA, Fournier MJ. 2007. New bioinformatic tools for analysis of nucleotide modifications in eukaryotic rRNA. RNA 13:305-312. http://dx.doi.org/10.1261/rna.373107.
15. Dragon F, Gallagher JE, Compagnone-Post PA, Mitchell BM, Porwancher KA, Wehner KA, Wormsley S, Settlage RE, Shabanowitz J, Osheim Y, Beyer AL, Hunt DF, Baserga SJ. 2002. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417:967-970. http://dx.doi.org/10.1038/nature00769.
16. Osheim YN, French SL, Keck KM, Champion EA, Spasov K, Dragon F, Baserga SJ, Beyer AL. 2004. Pre-18S ribosomal RNA is structurally compacted into the SSU processome prior to being cleaved from nascent transcripts in Saccharomyces cerevisiae. Mol Cell 16:943-954. http://dx.doi.org /10.1016/j.molcel.2004.11.031.
17. Bernstein KA, Gallagher JE, Mitchell BM, Granneman S, Baserga SJ. 2004. The small-subunit processome is a ribosome assembly intermediate. Eukaryot Cell 3:1619-1626. http://dx.doi.org/10.1128/EC.3.6.1619-1626
18. Phipps KR, Charette J, Baserga SJ. 2011. The small subunit processome in ribosome biogenesis-progress and prospects. Wiley Interdiscip Rev RNA 2:1-21. http://dx.doi.org/10.1002/wrna.57.
19. Lim YH, Charette JM, Baserga SJ. 2011. Assembling a protein-protein interaction map of the SSU processome from existing datasets. PLoS One 6:e17701. http://dx.doi.org/10.1371/journal.pone.0017701.
20. Perez-Fernandez J, Martin-Marcos P, Dosil M. 2011. Elucidation of the assembly events required for the recruitment of Utp20, Imp4 and Bms1 onto nascent pre-ribosomes. Nucleic Acids Res 39:8105-8121. http://dx .doi.org/10.1093/nar/gkr508.
21. Liang WQ, Clark JA, Fournier MJ. 1997. The rRNA-processing function of the yeast U14 small nucleolar RNA can be rescued by a conserved RNA helicase-like protein. Mol Cell Biol 17:4124-4132.
22. Garcia I, Albring MJ, Uhlenbeck OC. 2012. Duplex destabilization by four ribosomal DEAD-box proteins. Biochemistry 51:10109-10118. http: //dx.doi.org/10.1021/bi301172s.
23. Jankowsky E. 2011. RNA helicases at work: binding and rearranging. Trends Biochem Sci 36:19-29. http://dx.doi.org/10.1016/j.tibs.2010.07 .008.
24. Silverman E, Edwalds-Gilbert G, Lin RJ. 2003. DExD/H-box proteins and their partners: helping RNA helicases unwind. Gene 312:1-16. http: //dx.doi.org/10.1016/S0378-1119(03)00626-7.
25. Cordin O, Banroques J, Tanner NK, Linder P. 2006. The DEAD-box protein family of RNA helicases. Gene 367:17-37. http://dx.doi.org/10 .1016/j.gene.2005.10.019.
26. de la Cruz J, Kressler D, Linder P. 1999. Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem Sci 24:192-198. http://dx.doi.org/10.1016/S0968-0004(99)01376-6.
27. Bleichert F, Baserga SJ. 2007. The long unwinding road of RNA helicases. Mol Cell 27:339-352. http://dx.doi.org/10.1016/j.molcel.2007.07.014.
28. Rodriguez-Galan O, Garcia-Gomez JJ, de la Cruz J. 2013. Yeast and human RNA helicases involved in ribosome biogenesis: current status and perspectives. Biochim Biophys Acta 1829:775-790. http://dx.doi.org/10 .1016/j.bbagrm.2013.01.007.
29. Kos M, Tollervey D. 2005. The putative RNA helicase Dbp4p is required for release of the U14 snoRNA from preribosomes in Saccharomyces cerevisiae. Mol Cell 20:53-64. http://dx.doi.org/10.1016/j.molcel.2005.08 .022.
30. Granneman S, Baserga SJ. 2004. Ribosome biogenesis: of knobs and RNA processing. Exp Cell Res 296:43-50. http://dx.doi.org/10.1016/j.yexcr .2004.03.016.
31. Soltanieh S, Lapensée M, Dragon F. 2014. Nucleolar proteins Bfr2 and Enp2 interact with DEAD-box RNA helicase Dbp4 in two different complexes. Nucleic Acids Res 42:3194-3206. http://dx.doi.org/10.1093/nar /gkt1293.
32. Turner AJ, Knox AA, Prieto JL, McStay B, Watkins NJ. 2009. A novel small-subunit processome assembly intermediate that contains the U3 snoRNP, nucleolin, RRP5, and DBP4. Mol Cell Biol 29:3007-3017. http: //dx.doi.org/10.1128/MCB.00029-09.
33. Knop M, Siegers K, Pereira G, Zachariae W, Winsor B, Nasmyth K, Schiebel E. 1999. Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15:963-972. http: //dx.doi.org/10.1002/(SICI)1097-0061(199907)15:10B 963::AID -YEA399 3.0.CO;2-W.
34. Longtine MS, McKenzie A, III, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961. http://dx.doi.org/10.1002/(SICI) 1097-0061(199807)14:10 953::AID-YEA293 3.0.CO;2-U.
35. Gari E, Piedrafita L, Aldea M, Herrero E. 1997. A set of vectors with a tetracycline-regulatable promoter system for modulated gene expression in Saccharomyces cerevisiae. Yeast 13:837-848. http://dx.doi.org/10.1002 /(SICI)1097-0061(199707)13:9 837::AID-YEA145 3.0.CO;2-T.
36. Dragon F, Pogacic V, Filipowicz W. 2000. In vitro assembly of human H/ACA small nucleolar RNPs reveals unique features of U17 and telomerase RNAs. Mol Cell Biol 20:3037-3048. http://dx.doi.org/10.1128/MCB .20.9.3037-3048.2000.
37. Dunbar DA, Wormsley S, Agentis TM, Baserga SJ. 1997. Mpp10p, a U3 small nucleolar ribonucleoprotein component required for pre-18S rRNA processing in yeast. Mol Cell Biol 17:5803-5812.
38. Strunk BS, Novak MN, Young CL, Karbstein K. 2012. A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 150:111-121. http://dx.doi.org/10.1016/j.cell.2012.04.044.
39. Vilardell J, Warner JR. 1997. Ribosomal protein L32 of Saccharomyces cerevisiae influences both the splicing of its own transcript and the processing of rRNA. Mol Cell Biol 17:1959-1965.
40. Sikorski RS, Hieter P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
41. Lemay V, Hossain A, Osheim YN, Beyer AL, Dragon F. 2011. Identification of novel proteins associated with yeast snR30 small nucleolar RNA. Nucleic Acids Res 39:9659-9670. http://dx.doi.org/10.1093/nar/gkr659.
42. Fabrizio P, Esser S, Kastner B, Luhrmann R. 1994. Isolation of S. cerevisiae snRNPs: comparison of U1 and U4/U6.U5 to their human counterparts. Science 264:261-265. http://dx.doi.org/10.1126/science .8146658.
43. Billy E, Wegierski T, Nasr F, Filipowicz W. 2000. Rcl1p, the yeast protein similar to the RNA 3=-phosphate cyclase, associates with U3 snoRNP and is required for 18S rRNA biogenesis. EMBO J 19:2115-2126. http://dx.doi .org/10.1093/emboj/19.9.2115.
44. Wehner KA, Gallagher JE, Baserga SJ. 2002. Components of an interdependent unit within the SSU processome regulate and mediate its activity. Mol Cell Biol 22:7258-7267. http://dx.doi.org/10.1128/MCB.22.20.7258 -7267.2002.
45. Perez-Fernandez J, Roman A, De Las Rivas J, Bustelo XR, Dosil M. 2007. The 90S preribosome is a multimodular structure that is assembled through a hierarchical mechanism. Mol Cell Biol 27:5414-5429. http://dx.doi.org/10.1128/MCB.00380-07.
46. Dutca LM, Gallagher JE, Baserga SJ. 2011. The initial U3 snoRNA:prerRNA base pairing interaction required for pre-18S rRNA folding revealed by in vivo chemical probing. Nucleic Acids Res 39:5164-5180. http://dx .doi.org/10.1093/nar/gkr044.
47. Samarsky DA, Fournier MJ. 1998. Functional mapping of the U3 small nucleolar RNA from the yeast Saccharomyces cerevisiae. Mol Cell Biol 18: 3431-3444.
48. Gallagher JE, Dunbar DA, Granneman S, Mitchell BM, Osheim Y, Beyer AL, Baserga SJ. 2004. RNA polymerase I transcription and prerRNA processing are linked by specific SSU processome components. Genes Dev 18:2506-2517. http://dx.doi.org/10.1101/gad.1226604.
49. Ban N, Beckmann R, Cate JH, Dinman JD, Dragon F, Ellis SR, Lafontaine DL, Lindahl L, Liljas A, Lipton JM, McAlear MA, Moore PB, Noller HF, Ortega J, Panse VG, Ramakrishnan V, Spahn CM, Steitz TA, Tchorzewski M, Tollervey D, Warren AJ, Williamson JR, Wilson D, Yonath A, Yusupov M. 2014. A new system for naming ribosomal proteins. Curr Opin Struct Biol 24:165-169. http://dx.doi.org/10.1016/j.sbi .2014.01.002.
50. Ferreira-Cerca S, Kiburu I, Thomson E, LaRonde N, Hurt E. 2014. Dominant Rio1 kinase/ATPase catalytic mutant induces trapping of late pre-40S biogenesis factors in 80S-like ribosomes. Nucleic Acids Res 42: 8635-8647. http://dx.doi.org/10.1093/nar/gku542.
51. Katsamba PS, Myszka DG, Laird-Offringa IA. 2001. Two functionally distinct steps mediate high affinity binding of U1A protein to U1 hairpin II RNA. J Biol Chem 276:21476-21481. http://dx.doi.org/10.1074/jbc .M101624200.
52. Doetsch M, Schroeder R, Furtig B. 2011. Transient RNA-protein interactions in RNA folding. FEBS J 278:1634-1642. http://dx.doi.org/10.1111 /j.1742-4658.2011.08094.x.
53. Grandi P, Rybin V, Bassler J, Petfalski E, Strauss D, Marzioch M, Schafer T, Kuster B, Tschochner H, Tollervey D, Gavin AC, Hurt E. 2002. 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol Cell 10: 105-115. http://dx.doi.org/10.1016/S1097-2765(02)00579-8.