RNA folding and functions of RNA helicases in ribosome biogenesis

References

• Baßler J, Hurt E. Eukaryotic ribosome assembly. Annu Rev Biochem. 2019;1:281–306. DOI:10.1146/annurev-biochem-013118-110817
   PubMedGoogle Scholar
• de la Cruz J, Karbstein K, Woolford JL. Functions of ribosomal proteins in assembly of eukaryotic ribosomes in vivo. Annu Rev Biochem. 2015;84:93–129.
   PubMed Web of Science ®Google Scholar
• Frazier MN, Pillon MC, Kocaman S, et al. Structural overview of macromolecular machines involved in ribosome biogenesis. Curr Opin Struct Biol. 2021;67:51–60.
   PubMed Web of Science ®Google Scholar
• Klinge S, Woolford JL. Ribosome assembly coming into focus. Nat Rev Mol Cell Biol. 2019;20(2):116–131.
   PubMed Web of Science ®Google Scholar
• Kofler L, Prattes M, Bergler H. From snapshots to flipbook-resolving the dynamics of ribosome biogenesis with chemical probes. Int J Mol Sci. 2020;21(8):2998.
   PubMed Web of Science ®Google Scholar
• Kressler D, Hurt E, Baßler J. A puzzle of life: crafting ribosomal subunits. Trends Biochem Sci. 2017;42(8):640–654.
   PubMed Web of Science ®Google Scholar
• Bohnsack KE, Bohnsack MT. Uncovering the assembly pathway of human ribosomes and its emerging links to disease. EMBO J. 2019;38(13). DOI:10.15252/embj.2018100278
   PubMed Web of Science ®Google Scholar
• Woolford JL Jr, Baserga SJ. Ribosome biogenesis in the yeast saccharomyces cerevisiae. Genetics. 2013;195(3):643–681.
   PubMed Web of Science ®Google Scholar
• Dragon F, Gallagher JEG, Compagnone-Post PA, et al. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature. 2002;417(6892):967–970.
   PubMed Web of Science ®Google Scholar
• Grandi P, Rybin V, Baßler J, et al. 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol Cell. 2002;10(1):105–115.
   PubMed Web of Science ®Google Scholar
• Osheim YN, French SL, Keck KM, et al. Pre-18S ribosomal RNA is structurally compacted into the SSU processome prior to being cleaved from nascent transcripts in Saccharomyces cerevisiae. Mol Cell. 2004;16(6):943–954.
   PubMed Web of Science ®Google Scholar
• Pérez-Fernández J, Román A, Rivas J de L, et al. The 90S preribosome is a multimodular structure that is assembled through a hierarchical mechanism. Mol Cell Biol. 2007;27(15):5414–5429.
   PubMed Web of Science ®Google Scholar
• Barandun J, Chaker-Margot M, Hunziker M, et al. The complete structure of the small-subunit processome. Nat Struct Mol Biol. 2017;24(11):944–953.
   PubMed Web of Science ®Google Scholar
• Chaker-Margot M, Barandun J, Hunziker M, et al. Architecture of the yeast small subunit processome. Science. 2017;355(6321):eaal1880.
   PubMed Web of Science ®Google Scholar
• Chaker-Margot M, Hunziker M, Barandun J, et al. Stage-specific assembly events of the 6-MDa small-subunit processome initiate eukaryotic ribosome biogenesis. Nat Struct Mol Biol. 2015;22(11):920–923.
   PubMed Web of Science ®Google Scholar
• Hunziker M, Barandun J, Petfalski E, et al. UtpA and UtpB chaperone nascent pre-ribosomal RNA and U3 snoRNA to initiate eukaryotic ribosome assembly. Nat Commun. 2016;7(1):12090.
   PubMedGoogle Scholar
• Kornprobst M, Turk M, Kellner N, et al. Architecture of the 90S pre-ribosome: a structural view on the birth of the eukaryotic ribosome. Cell. 2016;166(2):380–393.
   PubMed Web of Science ®Google Scholar
• Singh S, Vanden Broeck A, Miller L, et al. Nucleolar maturation of the human small subunit processome. Science. 2021;373(6560):eabj5338.
   PubMed Web of Science ®Google Scholar
• Sun Q, Zhu X, Qi J, et al. Molecular architecture of the 90S small subunit pre-ribosome. Elife. 2017;6:e22086.
   PubMed Web of Science ®Google Scholar
• Zhang L, Wu C, Cai G, et al. Stepwise and dynamic assembly of the earliest precursors of small ribosomal subunits in yeast. Genes Dev. 2016;30(6):718–732.
   PubMed Web of Science ®Google Scholar
• Cheng J, Baßler J, Fischer P, et al. Thermophile 90S pre-ribosome structures reveal the reverse order of co-transcriptional 18S rRNA subdomain integration. Mol Cell. 2019;75(6):1256‐1269.e7.
   Web of Science ®Google Scholar
• Cheng J, Kellner N, Berninghausen O, et al. 3.2-Å-resolution structure of the 90S preribosome before A1 pre-rRNA cleavage. Nat Struct Mol Biol. 2017;24(11):954–964.
   PubMed Web of Science ®Google Scholar
• Cheng J, Lau B, La Venuta G, et al. 90S pre-ribosome transformation into the primordial 40S subunit. Science. 2020;369(6510):1470–1476.
   PubMed Web of Science ®Google Scholar
• Kos M, Tollervey D. Yeast pre-rRNA processing and modification occur cotranscriptionally. Mol Cell. 2010;37(6):809–820.
   PubMed Web of Science ®Google Scholar
• 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(3):397–414.
   PubMed Web of Science ®Google Scholar
• Bleichert F, Granneman S, Osheim YN, et al. The PINc domain protein Utp24, a putative nuclease, is required for the early cleavage steps in 18S rRNA maturation. Proc Natl Acad Sci USA. 2006;103( 25):9464–9469.
   Google Scholar
• Tomecki R, Labno A, Drazkowska K, et al. hUTP24 is essential for processing of the human rRNA precursor at site A1, but not at site A0. RNA Biol. 2015;12(9):1010–1029.
   PubMed Web of Science ®Google Scholar
• Wells GR, Weichmann F, Colvin D, et al. The PIN domain endonuclease Utp24 cleaves pre-ribosomal RNA at two coupled sites in yeast and humans. Nucleic Acids Res. 2016;44(18):9016.
   PubMed Web of Science ®Google Scholar
• Ferreira-Cerca S, Pöll G, Kühn H, et al. Analysis of the in vivo assembly pathway of eukaryotic 40S ribosomal proteins. Mol Cell. 2007;28(3):446–457.
   PubMed Web of Science ®Google Scholar
• Fischer U, Schäuble N, Schütz S, et al. A non-canonical mechanism for Crm1-export cargo complex assembly. Elife. 2015;4:e05745.
   PubMed Web of Science ®Google Scholar
• Moriggi G, Nieto B, Dosil M, et al. Rrp12 and the exportin Crm1 participate in late assembly events in the nucleolus during 40S ribosomal subunit biogenesis. PLoS Genet. 2014;10(12):e1004836.
   PubMed Web of Science ®Google Scholar
• Schäfer T, Strauss D, Petfalski E, et al. The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J. 2003;22(6):1370–1380.
   PubMed Web of Science ®Google Scholar
• Ameismeier M, Cheng J, Berninghausen O, et al. Visualizing late states of human 40S ribosomal subunit maturation. Nature. 2018;558(7709):249–253.
   PubMed Web of Science ®Google Scholar
• Ameismeier M, Zemp I, van den Heuvel J, et al. Structural basis for the final steps of human 40S ribosome maturation. Nature. 2020;587(7835):683–687.
   PubMed Web of Science ®Google Scholar
• Fatica A, Oeffinger M, Dlakić M, et al. Nob1p is required for cleavage of the 3’ end of 18S rRNA. Mol Cell Biol. 2003;23(5):1798–1807.
   PubMed Web of Science ®Google Scholar
• Ferreira-Cerca S, Sagar V, Schäfer T, et al. ATPase-dependent role of the atypical kinase Rio2 on the evolving pre-40S ribosomal subunit. Nat Struct Mol Biol. 2012;19(12):1316–1323.
   PubMed Web of Science ®Google Scholar
• Huang H, Ghalei H, Karbstein K. Quality control of 40S ribosome head assembly ensures scanning competence. J Cell Biol. 2020;219(11). DOI:10.1083/jcb.202004161
   Web of Science ®Google Scholar
• Huang H, Karbstein K. Assembly factors chaperone rRNA folding by isolating helical junctions that are prone to misfolding. [publisher unknown]; 2020.
   Google Scholar
• Mitterer V, Murat G, Réty S, et al. Sequential domain assembly of ribosomal protein S3 drives 40S subunit maturation. Nat Commun. 2016;7(1):10336.
   PubMedGoogle Scholar
• Mitterer V, Shayan R, Ferreira-Cerca S, et al. Conformational proofreading of distant 40S ribosomal subunit maturation events by a long-range communication mechanism. Nat Commun. 2019;10(1):2754.
   PubMedGoogle Scholar
• Parker MD, Collins JC, Korona B, et al. A kinase-dependent checkpoint prevents escape of immature ribosomes into the translating pool. PLoS Biol. 2019;17(12):e3000329.
   PubMed Web of Science ®Google Scholar
• Schäfer T, Maco B, Petfalski E, et al. Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature. 2006;441(7093):651–655.
   PubMed Web of Science ®Google Scholar
• Strunk BS, Loucks CR, Su M, et al. Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science. 2011;333(6048):1449–1453.
   PubMed Web of Science ®Google Scholar
• Turowski TW, Lebaron S, Zhang E, et al. Rio1 mediates ATP-dependent final maturation of 40S ribosomal subunits. Nucleic Acids Res. 2014;42(19):12189–12199.
   PubMed Web of Science ®Google Scholar
• Zemp I, Wild T, O’Donohue M-F, et al. Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2. J Cell Biol. 2009;185(7):1167–1180.
   PubMed Web of Science ®Google Scholar
• Belhabich-Baumas K, Joret C, Jády BE, et al. The Rio1p ATPase hinders premature entry into translation of late pre-40S pre-ribosomal particles. Nucleic Acids Res. 2017;45(18):10824–10836.
   PubMed Web of Science ®Google Scholar
• Ferreira-Cerca S, Kiburu I, Thomson E, et al. Dominant Rio1 kinase/ATPase catalytic mutant induces trapping of late pre-40S biogenesis factors in 80S-like ribosomes. Nucleic Acids Res. 2014;42(13):8635–8647.
   PubMed Web of Science ®Google Scholar
• Ghalei H, Trepreau J, Collins JC, et al. The ATPase Fap7 tests the ability to carry out translocation-like conformational changes and releases Dim1 during 40S ribosome maturation. Mol Cell. 2017;67(6):990‐1000.e3.
   PubMed Web of Science ®Google Scholar
• Lebaron S, Schneider C, van Nues RW, et al. Proofreading of pre-40S ribosome maturation by a translation initiation factor and 60S subunits. Nat Struct Mol Biol. 2012;19(8):744–753.
   PubMed Web of Science ®Google Scholar
• Strunk BS, Novak MN, Young CL, et al. A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell. 2012;150(1):111–121.
   PubMed Web of Science ®Google Scholar
• García-Gómez JJ, Fernández-Pevida A, Lebaron S, et al. Final pre-40S maturation depends on the functional integrity of the 60S subunit ribosomal protein L3. PLoS Genet. 2014;10(3):e1004205.
   PubMed Web of Science ®Google Scholar
• Joret C, Capeyrou R, Belhabich-Baumas K, et al. The Npa1p complex chaperones the assembly of the earliest eukaryotic large ribosomal subunit precursor. PLoS Genet. 2018;14(8):e1007597.
   PubMedGoogle Scholar
• Kater L, Mitterer V, Thoms M, et al. Construction of the central protuberance and L1 stalk during 60S subunit biogenesis. Mol Cell. 2020;79(4):615–628.e5.
   PubMed Web of Science ®Google Scholar
• Kater L, Thoms M, Barrio-Garcia C, et al. Visualizing the assembly pathway of nucleolar Pre-60S ribosomes. Cell. 2017;171(7):1599‐1610.e14.
   PubMed Web of Science ®Google Scholar
• Sanghai ZA, Miller L, Molloy KR, et al. Modular assembly of the nucleolar pre-60S ribosomal subunit. Nature. 2018;556(7699):126–129.
   PubMed Web of Science ®Google Scholar
• Zhou D, Zhu X, Zheng S, et al. Cryo-EM structure of an early precursor of large ribosomal subunit reveals a half-assembled intermediate. Protein Cell. 2019;10(2):120–130.
   PubMed Web of Science ®Google Scholar
• Dez C, Froment C, Noaillac-Depeyre J, et al. Npa1p, a component of very early pre-60S ribosomal particles, associates with a subset of small nucleolar RNPs required for peptidyl transferase center modification. Mol Cell Biol. 2004;24(14):6324–6337.
   PubMed Web of Science ®Google Scholar
• Kressler D, Bange G, Ogawa Y, et al. Synchronizing nuclear import of ribosomal proteins with ribosome assembly. Science. 2012;338(6107):666–671.
   PubMed Web of Science ®Google Scholar
• Leidig C, Thoms M, Holdermann I, et al. 60S ribosome biogenesis requires rotation of the 5S ribonucleoprotein particle. Nat Commun. 2014;5(1):3491.
   PubMedGoogle Scholar
• Madru C, Lebaron S, Blaud M, et al. Chaperoning 5S RNA assembly. Genes Dev. 2015;29(13):1432–1446.
   PubMed Web of Science ®Google Scholar
• Wu S, Tutuncuoglu B, Yan K, et al. Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes. Nature. 2016;534(7605):133–137.
   PubMed Web of Science ®Google Scholar
• Zhang J, Harnpicharnchai P, Jakovljevic J, et al. Assembly factors Rpf2 and Rrs1 recruit 5S rRNA and ribosomal proteins rpL5 and rpL11 into nascent ribosomes. Genes Dev. 2007;21(20):2580–2592.
   PubMed Web of Science ®Google Scholar
• Baßler J, Kallas M, Pertschy B, et al. The AAA-ATPase Rea1 drives removal of biogenesis factors during multiple stages of 60S ribosome assembly. Mol Cell. 2010;38(5):712–721.
   PubMed Web of Science ®Google Scholar
• Brüning L, Hackert P, Martin R, et al. RNA helicases mediate structural transitions and compositional changes in pre-ribosomal complexes. Nat Commun. 2018;9(1):5383.
   PubMedGoogle Scholar
• Fromm L, Falk S, Flemming D, et al. Reconstitution of the complete pathway of ITS2 processing at the pre-ribosome. Nat Commun. 2017;8(1):1787.
   PubMedGoogle Scholar
• Gasse L, Flemming D, Hurt E. Coordinated ribosomal ITS2 RNA processing by the Las1 complex integrating endonuclease, polynucleotide kinase, and exonuclease activities. Mol Cell. 2015;60(5):808–815.
   PubMed Web of Science ®Google Scholar
• Kressler D, Roser D, Pertschy B, et al. The AAA ATPase Rix7 powers progression of ribosome biogenesis by stripping Nsa1 from pre-60S particles. J Cell Biol. 2008;181(6):935–944.
   PubMed Web of Science ®Google Scholar
• Liang X, Zuo M-Q, Zhang Y, et al. Structural snapshots of human pre-60S ribosomal particles before and after nuclear export. Nat Commun. 2020;11(1):3542.
   PubMed Web of Science ®Google Scholar
• Manikas R-G, Thomson E, Thoms M, et al. The K+-dependent GTPase Nug1 is implicated in the association of the helicase Dbp10 to the immature peptidyl transferase centre during ribosome maturation. Nucleic Acids Res. 2016;44(4):1800–1812.
   PubMed Web of Science ®Google Scholar
• Matsuo Y, Granneman S, Thoms M, et al. Coupled GTPase and remodelling ATPase activities form a checkpoint for ribosome export. Nature. 2014;505(7481):112–116.
   PubMed Web of Science ®Google Scholar
• Sarkar A, Pech M, Thoms M, et al. Ribosome-stalk biogenesis is coupled with recruitment of nuclear-export factor to the nascent 60S subunit. Nat Struct Mol Biol. 2016;23(12):1074–1082.
   PubMed Web of Science ®Google Scholar
• Schuller JM, Falk S, Fromm L, et al. Structure of the nuclear exosome captured on a maturing preribosome. Science. 2018;360(6385):219–222.
   PubMed Web of Science ®Google Scholar
• Ulbrich C, Diepholz M, Baßler J, et al. Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunits. Cell. 2009;138(5):911–922.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Musalgaonkar S, Johnson AW, et al. Tightly-orchestrated rearrangements govern catalytic center assembly of the ribosome. Nat Commun. 2019;10(1):958.
   PubMedGoogle Scholar
• Bussiere C, Hashem Y, Arora S, et al. Integrity of the P-site is probed during maturation of the 60S ribosomal subunit. J Cell Biol. 2012;197(6):747–759.
   PubMed Web of Science ®Google Scholar
• Greber BJ, Gerhardy S, Leitner A, et al. Insertion of the biogenesis factor Rei1 probes the ribosomal tunnel during 60S maturation. Cell. 2016;164(1–2):91–102.
   PubMed Web of Science ®Google Scholar
• Kappel L, Loibl M, Zisser G, et al. Rlp24 activates the AAA-ATPase Drg1 to initiate cytoplasmic pre-60S maturation. J Cell Biol. 2012;199(5):771–782.
   PubMed Web of Science ®Google Scholar
• Kargas V, Castro-Hartmann P, Escudero-Urquijo N, et al. Mechanism of completion of peptidyltransferase centre assembly in eukaryotes. Elife. 2019;8:e44904.
   PubMed Web of Science ®Google Scholar
• Klingauf-Nerurkar P, Gillet LC, Portugal-Calisto D, et al. The GTPase Nog1 co-ordinates the assembly, maturation and quality control of distant ribosomal functional centers. Elife. 2020;9. DOI:10.7554/eLife.52474.
   PubMed Web of Science ®Google Scholar
• K-y L, Li Z, Bussiere C, et al. Defining the pathway of cytoplasmic maturation of the 60S ribosomal subunit. Mol Cell. 2010;39(2):196–208.
   PubMed Web of Science ®Google Scholar
• Jäkel S. Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J. 1998;17(15):4491–4502.
   PubMed Web of Science ®Google Scholar
• Ma C, Wu S, Li N, et al. Structural snapshot of cytoplasmic pre-60S ribosomal particles bound by Nmd3, Lsg1, Tif6 and Reh1. Nat Struct Mol Biol. 2017; (3):214–220. DOI:10.1038/nsmb.3364.
   PubMed Web of Science ®Google Scholar
• Malyutin AG, Musalgaonkar S, Patchett S, et al. Nmd3 is a structural mimic of eIF5A, and activates the cpGTPase Lsg1 during 60S ribosome biogenesis. EMBO J. 2017;36(7):854–868.
   PubMed Web of Science ®Google Scholar
• Weis F, Giudice E, Churcher M, et al. Mechanism of eIF6 release from the nascent 60S ribosomal subunit. Nat Struct Mol Biol. 2015;22(11):914–919.
   PubMed Web of Science ®Google Scholar
• Petrov AS, Bernier CR, Gulen B, et al. Secondary structures of rRNAs from all three domains of life. PloS One. 2014;9(2):e88222.
   PubMed Web of Science ®Google Scholar
• Du Y, An W, Zhu X, et al. Cryo-EM structure of 90S small ribosomal subunit precursors in transition states. Science. 2020;369(6510):1477–1481.
   PubMed Web of Science ®Google Scholar
• Heuer A, Thomson E, Schmidt C, et al. Cryo-EM structure of a late pre-40S ribosomal subunit from Saccharomyces cerevisiae. Elife. 2017;6:e30189.
   PubMed Web of Science ®Google Scholar
• Hunziker M, Barandun J, Buzovetsky O, et al. Conformational switches control early maturation of the eukaryotic small ribosomal subunit. Elife. 2019;8:e45185.
   PubMed Web of Science ®Google Scholar
• Micic J, Li Y, Wu S, et al. Coupling of 5S RNP rotation with maturation of functional centers during large ribosomal subunit assembly. Nat Commun. 2020;11(1):3751.
   PubMed Web of Science ®Google Scholar
• Scaiola A, Peña C, Weisser M, et al. Structure of a eukaryotic cytoplasmic pre-40S ribosomal subunit. EMBO J. 2018;37(7). DOI:10.15252/embj.201798499.
   PubMed Web of Science ®Google Scholar
• Shayan R, Rinaldi D, Larburu N, et al. Good vibrations: structural remodeling of maturing yeast Pre-40S ribosomal particles followed by cryo-electron microscopy. Molecules. 2020;25(5):1125.
   PubMed Web of Science ®Google Scholar
• Adilakshmi T, Bellur DL, Woodson SA. Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly. Nature. 2008;455(7217):1268–1272.
   PubMed Web of Science ®Google Scholar
• Agalarov SC, Williamson JR. A hierarchy of RNA subdomains in assembly of the central domain of the 30S ribosomal subunit. RNA. 2000;6(3):402–408.
   PubMed Web of Science ®Google Scholar
• Held WA, Ballou B, Mizushima S, et al. Assembly mapping of 30S ribosomal proteins from Escherichia coli. Journal of Biological Chemistry. 1974;249(10):3103–3111.
   PubMed Web of Science ®Google Scholar
• Kim H, Abeysirigunawarden SC, Chen K, et al. Protein-guided RNA dynamics during early ribosome assembly. Nature. 2014;506(7488):334–338.
   PubMed Web of Science ®Google Scholar
• Powers T, Daubresse G, Noller HF. Dynamics of in vitro assembly of 16S rRNA into 30S ribosomal subunits. J Mol Biol. 1993;232(2):362–374.
   PubMed Web of Science ®Google Scholar
• Stern S, Powers T, Changchien LM, et al. RNA-protein interactions in 30S ribosomal subunits: folding and function of 16S rRNA. Science. 1989;244(4906):783–790.
   PubMed Web of Science ®Google Scholar
• Sykes MT, Williamson JR. A complex assembly landscape for the 30S ribosomal subunit. Annu Rev Biophys. 2009;38(1):197–215.
   PubMed Web of Science ®Google Scholar
• Rodgers ML, Woodson SA. A roadmap for rRNA folding and assembly during transcription. Trends Biochem Sci. 2021;46(11):889–901.
   PubMed Web of Science ®Google Scholar
• Andersen CBF, Ballut L, Johansen JS, et al. Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA. Science. 2006;313(5795):1968–1972.
   PubMed Web of Science ®Google Scholar
• Lau B, Cheng J, Flemming D, et al. Structure of the maturing 90S pre-ribosome in association with the RNA exosome. Mol Cell. 2021;81(2):293–303.e4.
   PubMed Web of Science ®Google Scholar
• Sardana R, Liu X, Granneman S, et al. The DEAH-box helicase Dhr1 dissociates U3 from the pre-rRNA to promote formation of the central pseudoknot. PLoS Biol. 2015;13(2):e1002083.
   PubMed Web of Science ®Google Scholar
• Herold M, Nierhaus KH. Incorporation of six additional proteins to complete the assembly map of the 50S subunit from Escherichia coli ribosomes. J Biol Chem. 1987;262(18):8826–8833.
   PubMed Web of Science ®Google Scholar
• Nierhaus KH. The assembly of prokaryotic ribosomes. Biochimie. 1991;73(6):739–755.
   PubMed Web of Science ®Google Scholar
• Davis JH, Tan YZ, Carragher B, et al. Modular assembly of the bacterial large ribosomal subunit. Cell. 2016;167(6):1610–1622.e15.
   PubMed Web of Science ®Google Scholar
• Gamalinda M, Ohmayer U, Jakovljevic J, et al. A hierarchical model for assembly of eukaryotic 60S ribosomal subunit domains. Genes Dev. 2014;28(2):198–210.
   PubMed Web of Science ®Google Scholar
• Ohmayer U, Gamalinda M, Sauert M, et al. Studies on the assembly characteristics of large subunit ribosomal proteins in S. cerevisae. PloS One. 2013;8(7):e68412.
   PubMed Web of Science ®Google Scholar
• Burlacu E, Lackmann F, Aguilar L-C, et al. High-throughput RNA structure probing reveals critical folding events during early 60S ribosome assembly in yeast. Nat Commun. 2017;8(1):714.
   PubMedGoogle Scholar
• Moazed D, Stern S, Noller HF. Rapid chemical probing of conformation in 16S ribosomal RNA and 30S ribosomal subunits using primer extension. J Mol Biol. 1986;187(3):399–416.
   PubMed Web of Science ®Google Scholar
• Clatterbuck Soper SF, Dator RP, Limbach PA, et al. In vivo X-ray footprinting of pre-30S ribosomes reveals chaperone-dependent remodeling of late assembly intermediates. Mol Cell. 2013;52(4):506–516.
   PubMed Web of Science ®Google Scholar
• Duss O, Stepanyuk GA, Puglisi JD, et al. Transient protein-RNA interactions guide nascent ribosomal RNA folding. Cell. 2019;179(6):1357‐1369.e16.
   PubMed Web of Science ®Google Scholar
• Woodson SA, Panja S, Santiago-Frangos A. Proteins that chaperone RNA regulation. Microbiol Spectr. 2018;6(4). DOI:10.1128/microbiolspec.RWR-0026-2018
   PubMedGoogle Scholar
• Rodgers ML, Woodson SA. Transcription increases the cooperativity of ribonucleoprotein assembly. Cell. 2019;179(6):1370‐1381.e12.
   PubMed Web of Science ®Google Scholar
• Piekna-Przybylska D, Decatur WA, Fournier MJ. The 3D rRNA modification maps database: with interactive tools for ribosome analysis. Nucleic Acids Res. 2008;36( Database issue):D178–83.
   PubMed Web of Science ®Google Scholar
• Helm M. Post-transcriptional nucleotide modification and alternative folding of RNA. Nucleic Acids Res. 2006;34(2):721–733.
   PubMed Web of Science ®Google Scholar
• Seelam PP, Sharma P, Mitra A. Structural landscape of base pairs containing post-transcriptional modifications in RNA. RNA. 2017;23(6):847–859.
   PubMed Web of Science ®Google Scholar
• Abou Assi H, Rangadurai AK, Shi H, et al. 2’-O-Methylation can increase the abundance and lifetime of alternative RNA conformational states. Nucleic Acids Res. 2020;48(21):12365–12379.
   PubMed Web of Science ®Google Scholar
• Kawai G, Yamamoto Y, Kamimura T, et al. Conformational rigidity of specific pyrimidine residues in tRNA arises from posttranscriptional modifications that enhance steric interaction between the base and the 2’-hydroxyl group. Biochemistry. 1992;31(4):1040–1046.
   PubMed Web of Science ®Google Scholar
• Baxter-Roshek JL, Petrov AN, Dinman JD. Optimization of ribosome structure and function by rRNA base modification. PloS One. 2007;2(1):e174.
   PubMed Web of Science ®Google Scholar
• Dudnakova T, Dunn-Davies H, Peters R, et al. Mapping targets for small nucleolar RNAs in yeast. Wellcome Open Res. 2018;3:120.
   PubMedGoogle Scholar
• Kudla G, Granneman S, Hahn D, et al. Cross-linking, ligation, and sequencing of hybrids reveals RNA-RNA interactions in yeast. Proc Natl Acad Sci USA. 2011;108( 24):10010–10015.
   Google Scholar
• Hughes JM, Ares M. Depletion of U3 small nucleolar RNA inhibits cleavage in the 5’ external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA. EMBO J. 1991;10(13):4231–4239.
   PubMed Web of Science ®Google Scholar
• Watkins NJ, Ségault V, Charpentier B, et al. A common core RNP structure shared between the small nucleoar box C/D RNPs and the spliceosomal U4 snRNP. Cell. 2000;103(3):457–466.
   PubMed Web of Science ®Google Scholar
• Gérczei T, Correll CC. Imp3p and Imp4p mediate formation of essential U3-precursor rRNA (pre-rRNA) duplexes, possibly to recruit the small subunit processome to the pre-rRNA. Proceedings of the National Academy of Sciences of the United States of America. 2004;101( 43):15301–15306.
   Google Scholar
• Beltrame M, Henry Y, Tollervey D. Mutational analysis of an essential binding site for the U3 snoRNA in the 5’ external transcribed spacer of yeast pre-rRNA. Nucleic Acids Res. 1994;22(23):5139–5147.
   PubMed Web of Science ®Google Scholar
• Beltrame M, Tollervey D. Base pairing between U3 and the pre-ribosomal RNA is required for 18S rRNA synthesis. EMBO J. 1995;14(17):4350–4356.
   PubMed Web of Science ®Google Scholar
• Beltrame M, Tollervey D. Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO J. 1992;11(4):1531–1542.
   PubMed Web of Science ®Google Scholar
• Dutca LM, Gallagher JEG, Baserga SJ. The initial U3 snoRNA:pre-rRNA base pairing interaction required for pre-18S rRNA folding revealed by in vivo chemical probing. Nucleic Acids Res. 2011;39(12):5164–5180.
   PubMed Web of Science ®Google Scholar
• Hughes JM. Functional base-pairing interaction between highly conserved elements of U3 small nucleolar RNA and the small ribosomal subunit RNA. J Mol Biol. 1996;259(4):645–654.
   PubMed Web of Science ®Google Scholar
• Marz M, Stadler PF. Comparative analysis of eukaryotic U3 snoRNA. RNA Biol. 2009;6(5):503–507.
   PubMed Web of Science ®Google Scholar
• Marmier-Gourrier N, Cléry A, Schlotter F, et al. A second base pair interaction between U3 small nucleolar RNA and the 5’-ETS region is required for early cleavage of the yeast pre-ribosomal RNA. Nucleic Acids Res. 2011;39(22):9731–9745.
   PubMed Web of Science ®Google Scholar
• Sharma K, Tollervey D. Base pairing between U3 small nucleolar RNA and the 5’ end of 18S rRNA is required for pre-rRNA processing. Mol Cell Biol. 1999;19(9):6012–6019.
   PubMed Web of Science ®Google Scholar
• Vos TJ, Kothe U. Small nucleolar ribonucleoprotein: a critical player during ribosome biogenesis. Cells. 2020;9(10):2195. snR30/U17
   PubMed Web of Science ®Google Scholar
• Atzorn V, Fragapane P, Kiss T. U17/snR30 is a ubiquitous snoRNA with two conserved sequence motifs essential for 18S rRNA production. Mol Cell Biol. 2004;24(4):1769–1778.
   PubMed Web of Science ®Google Scholar
• Martin R, Hackert P, Ruprecht M, et al. A pre-ribosomal RNA interaction network involving snoRNAs and the Rok1 helicase. RNA. 2014;20(8):1173–1182.
   PubMed Web of Science ®Google Scholar
• Tollervey D, Guthrie C. Deletion of a yeast small nuclear RNA gene impairs growth. EMBO J. 1985;4(13B):3873–3878.
   PubMed Web of Science ®Google Scholar
• Liang X, Liu Q, Liu Q, et al. Strong dependence between functional domains in a dual-function snoRNA infers coupling of rRNA processing and modification events. Nucleic Acids Res. 2010;38(10):3376–3387.
   PubMed Web of Science ®Google Scholar
• Tollervey D. A yeast small nuclear RNA is required for normal processing of pre-ribosomal RNA. EMBO J. 1987;6(13):4169–4175.
   PubMed Web of Science ®Google Scholar
• Li HD, Zagorski J, Fournier MJ. Depletion of U14 small nuclear RNA (snR128) disrupts production of 18S rRNA in Saccharomyces cerevisiae. Mol Cell Biol. 1990;10(3):1145–1152.
   PubMed Web of Science ®Google Scholar
• Liang WQ, Fournier MJ. U14 base-pairs with 18S rRNA: a novel snoRNA interaction required for rRNA processing. Genes Dev. 1995;9(19):2433–2443.
   PubMed Web of Science ®Google Scholar
• Morrissey JP, Tollervey D. U14 small nucleolar RNA makes multiple contacts with the pre-ribosomal RNA. Chromosoma. 1997;105(7–8):515–522.
   PubMed Web of Science ®Google Scholar
• Jaafar M, Contreras J, Dominique C, et al. Association of snR190 snoRNA chaperone with early pre-60S particles is regulated by the RNA helicase Dbp7 in yeast. Nat Commun. 2021;12(1):6153.
   PubMed Web of Science ®Google Scholar
• Jankowsky E. RNA helicases at work: binding and rearranging. Trends Biochem Sci. 2011;36(1):19–29.
   PubMed Web of Science ®Google Scholar
• Valentini M, P L. Happy birthday: 30 Years of RNA helicases. Methods Mol Biol. 2021;2209:17–34.
   PubMedGoogle Scholar
• Saraste M, Sibbald PR, Wittinghofer A. The P-loop — a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci. 1990;15(11):430–434.
   PubMed Web of Science ®Google Scholar
• Walker JE, Saraste M, Runswick MJ, et al. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982;1(8):945–951.
   PubMed Web of Science ®Google Scholar
• Fairman-Williams ME, Guenther U-P, Jankowsky E. SF1 and SF2 helicases: family matters. Curr Opin Struct Biol. 2010;20(3):313–324.
   PubMed Web of Science ®Google Scholar
• Singleton MR, Dillingham MS, Wigley DB. Structure and mechanism of helicases and nucleic acid translocases. Annu Rev Biochem. 2007;76(1):23–50.
   PubMedGoogle Scholar
• Byrd AK, Raney KD. Superfamily 2 helicases. Front Biosci (Landmark Ed). 2012;17(6):2070–2088.
   PubMedGoogle Scholar
• Bono F, Ebert J, Lorentzen E, et al. The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. Cell. 2006;126(4):713–725.
   PubMed Web of Science ®Google Scholar
• Caruthers JM, Johnson ER, McKay DB. Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase. Proc Natl Acad Sci USA. 2000;97( 24):13080–13085.
   Google Scholar
• Ozgur S, Buchwald G, Falk S, et al. The conformational plasticity of eukaryotic RNA-dependent ATPases. FEBS J. 2015;282(5):850–863.
   PubMed Web of Science ®Google Scholar
• Subramanya HS, Bird LE, Brannigan JA, et al. Crystal structure of a DExx box DNA helicase. Nature. 1996;384(6607):379–383.
   PubMed Web of Science ®Google Scholar
• Collins R, Karlberg T, Lehtiö L, et al. The DEXD/H-box RNA helicase DDX19 is regulated by an {alpha}-helical switch. J Biol Chem. 2009;284(16):10296–10300.
   PubMed Web of Science ®Google Scholar
• Gilman B, Tijerina P, Russell R. Distinct RNA-unwinding mechanisms of DEAD-box and DEAH-box RNA helicase proteins in remodeling structured RNAs and RNPs. Biochem Soc Trans. 2017;45(6):1313–1321.
   PubMedGoogle Scholar
• Jarmoskaite I, Russell R. RNA helicase proteins as chaperones and remodelers. Annu Rev Biochem. 2014;83(1):697–725.
   PubMedGoogle Scholar
• Linder P, Lasko PF, Ashburner M, et al. Birth of the D-E-A-D box. Nature. 1989;337(6203):121–122.
   PubMed Web of Science ®Google Scholar
• Linder P, Jankowsky E. From unwinding to clamping - the DEAD box RNA helicase family. Nat Rev Mol Cell Biol. 2011;12(8):505–516.
   PubMed Web of Science ®Google Scholar
• Del Campo M, Lambowitz AM. Structure of the Yeast DEAD box protein Mss116p reveals two wedges that crimp RNA. Mol Cell. 2009;35(5):598–609.
   PubMed Web of Science ®Google Scholar
• Hardin JW, Hu YX, McKay DB. Structure of the RNA binding domain of a DEAD-box helicase bound to its ribosomal RNA target reveals a novel mode of recognition by an RNA recognition motif. J Mol Biol. 2010;402(2):412–427.
   PubMed Web of Science ®Google Scholar
• Mallam AL, Jarmoskaite I, Tijerina P, et al. Solution structures of DEAD-box RNA chaperones reveal conformational changes and nucleic acid tethering by a basic tail. Proc Natl Acad Sci USA. 2011;108( 30):12254–12259.
   Google Scholar
• Chen Y, Potratz JP, Tijerina P, et al. DEAD-box proteins can completely separate an RNA duplex using a single ATP. Proc Natl Acad Sci USA. 2008;105( 51):20203–20208.
   Google Scholar
• Hilbert M, Karow AR, Klostermeier D. The mechanism of ATP-dependent RNA unwinding by DEAD box proteins. Biol Chem. 2009;390(12):1237–1250.
   PubMed Web of Science ®Google Scholar
• Liu F, Putnam A, Jankowsky E. ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding. Proc Natl Acad Sci USA. 2008;105( 51):20209–20214.
   Google Scholar
• Mallam AL, Del Campo M, Gilman B, et al. Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p. Nature. 2012;490(7418):121–125.
   PubMed Web of Science ®Google Scholar
• Sengoku T, Nureki O, Nakamura A, et al. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell. 2006;125(2):287–300.
   PubMed Web of Science ®Google Scholar
• Theissen B, Karow AR, Köhler J, et al. Cooperative binding of ATP and RNA induces a closed conformation in a DEAD box RNA helicase. Proc Natl Acad Sci USA. 2008;105( 2):548–553.
   Google Scholar
• Yang Q, Del Campo M, Lambowitz AM, et al. DEAD-box proteins unwind duplexes by local strand separation. Mol Cell. 2007;28(2):253–263.
   PubMed Web of Science ®Google Scholar
• Murakami K, Nakano K, Shimizu T, et al. The crystal structure of human DEAH-box RNA helicase 15 reveals a domain organization of the mammalian DEAH/RHA family. Acta Crystallogr F Struct Biol Commun. 2017;73(Pt 6):347–355.
   PubMedGoogle Scholar
• Tauchert MJ, Fourmann J-B, Lührmann R, et al. Structural insights into the mechanism of the DEAH-box RNA helicase Prp43. Elife. 2017;6:e21510.
   PubMed Web of Science ®Google Scholar
• Walbott H, Mouffok S, Capeyrou R, et al. Prp43p contains a processive helicase structural architecture with a specific regulatory domain. EMBO J. 2010;29(13):2194–2204.
   PubMed Web of Science ®Google Scholar
• He Y, Andersen GR, Nielsen KH. Structural basis for the function of DEAH helicases. EMBO Rep. 2010;11(3):180–186.
   PubMed Web of Science ®Google Scholar
• Gu M, Rice CM. Three conformational snapshots of the hepatitis C virus NS3 helicase reveal a ratchet translocation mechanism. Proc Natl Acad Sci USA. 2010;107( 2):521–528.
   Google Scholar
• Hamann F, Enders M, Ficner R. Structural basis for RNA translocation by DEAH-box ATPases. Nucleic Acids Res. 2019;47(8):4349–4362.
   PubMed Web of Science ®Google Scholar
• Prabu JR, Müller M, Thomae AW, et al. Structure of the RNA helicase MLE reveals the molecular mechanisms for uridine specificity and RNA-ATP coupling. Mol Cell. 2015;60(3):487–499.
   PubMed Web of Science ®Google Scholar
• Semlow DR, Blanco MR, Walter NG, et al. Spliceosomal DEAH-Box ATPases remodel Pre-mRNA to activate alternative splice sites. Cell. 2016;164(5):985–998.
   PubMed Web of Science ®Google Scholar
• Black JJ, Wang Z, Goering LM, et al. Utp14 interaction with the small subunit processome. RNA. 2018;24(9):1214–1228.
   PubMed Web of Science ®Google Scholar
• Davila Gallesio J, Hackert P, Bohnsack KE, et al. Sgd1 is an MIF4G domain-containing cofactor of the RNA helicase Fal1 and associates with the 5’ domain of the 18S rRNA sequence. RNA Biol. 2020;17(4):539–553.
   PubMed Web of Science ®Google Scholar
• Granneman S, Bernstein KA, Bleichert F, et al. Comprehensive mutational analysis of yeast DEXD/H box RNA helicases required for small ribosomal subunit synthesis. Mol Cell Biol. 2006;26(4):1183–1194.
   PubMed Web of Science ®Google Scholar
• Kressler D, de la Cruz J, De, Rojo M, et al. Fal1p is an essential DEAD-box protein involved in 40S-ribosomal-subunit biogenesis in Saccharomyces cerevisiae. Mol Cell Biol. 1997;17(12):7283–7294.
   PubMed Web of Science ®Google Scholar
• Shu S, Ye K. Structural and functional analysis of ribosome assembly factor Efg1. Nucleic Acids Res. 2018;46(4):2096–2106.
   PubMed Web of Science ®Google Scholar
• Sturm M, Cheng J, Baßler J, et al. Interdependent action of KH domain proteins Krr1 and Dim2 drive the 40S platform assembly. Nat Commun. 2017;8(1):2213.
   PubMedGoogle Scholar
• Daugeron MC, Kressler D, Linder P. Dbp9p, a putative ATP-dependent RNA helicase involved in 60S-ribosomal-subunit biogenesis, functionally interacts with Dbp6p. RNA. 2001;7(9):1317–1334.
   PubMed Web of Science ®Google Scholar
• Granneman S, Lin C, Champion EA, et al. The nucleolar protein Esf2 interacts directly with the DExD/H box RNA helicase, Dbp8, to stimulate ATP hydrolysis. Nucleic Acids Res. 2006;34(10):3189–3199.
   PubMed Web of Science ®Google Scholar
• Daugeron MC, Linder P. Characterization and mutational analysis of yeast Dbp8p, a putative RNA helicase involved in ribosome biogenesis. Nucleic Acids Res. 2001;29(5):1144–1155.
   PubMed Web of Science ®Google Scholar
• Kos M, Tollervey D. The putative RNA Helicase Dbp4p is required for release of the U14 snoRNA from preribosomes in saccharomyces cerevisiae. Mol Cell. 2005;20(1):53–64.
   PubMed Web of Science ®Google Scholar
• Soltanieh S, Osheim YN, Spasov K, et al. DEAD-box RNA helicase Dbp4 is required for small-subunit processome formation and function. Mol Cell Biol. 2015;35(5):816–830.
   PubMed Web of Science ®Google Scholar
• Garcia I, Uhlenbeck OC. Differential RNA-dependent ATPase activities of four rRNA processing yeast DEAD-box proteins. Biochemistry. 2008;47(47):12562–12573.
   PubMed Web of Science ®Google Scholar
• Garcia I, Albring MJ, Uhlenbeck OC. Duplex destabilization by four ribosomal DEAD-box proteins. Biochemistry. 2012;51(50):10109–10118.
   PubMed Web of Science ®Google Scholar
• Liang WQ, Clark JA, Fournier MJ. The rRNA-processing function of the yeast U14 small nucleolar RNA can be rescued by a conserved RNA helicase-like protein. Mol Cell Biol. 1997;17(7):4124–4132.
   PubMed Web of Science ®Google Scholar
• 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(12):1230–1236.
   PubMed Web of Science ®Google Scholar
• Turner AJ, Knox AA, Prieto J-L, et al. A novel small-subunit processome assembly intermediate that contains the U3 snoRNP, nucleolin, RRP5, and DBP4. Mol Cell Biol. 2009;29(11):3007–3017.
   PubMed Web of Science ®Google Scholar
• Soltanieh S, Lapensée M, Dragon F. Nucleolar proteins Bfr2 and Enp2 interact with DEAD-box RNA helicase Dbp4 in two different complexes. Nucleic Acids Res. 2014;42(5):3194–3206.
   PubMed Web of Science ®Google Scholar
• O’Day CL, Chavanikamannil F, Abelson J. 18S rRNA processing requires the RNA helicase-like protein Rrp3. Nucleic Acids Res. 1996;24(16):3201–3207.
   PubMed Web of Science ®Google Scholar
• Oh JY, Kim J. ATP hydrolysis activity of the DEAD box protein Rok1p is required for in vivo ROK1 function. Nucleic Acids Res. 1999;27(13):2753–2759.
   PubMed Web of Science ®Google Scholar
• Young CL, Khoshnevis S, Karbstein K. Cofactor-dependent specificity of a DEAD-box protein. Proc Natl Acad Sci USA. 2013;110( 29):E2668–76.
   Google Scholar
• Venema J, Bousquet-Antonelli C, Gelugne JP, et al. Rok1p is a putative RNA helicase required for rRNA processing. Mol Cell Biol. 1997;17(6):3398–3407.
   PubMed Web of Science ®Google Scholar
• Torchet C, Jacq C, Hermann-Le Denmat S. Two mutant forms of the S1/TPR-containing protein Rrp5p affect the 18S rRNA synthesis in Saccharomyces cerevisiae. RNA. 1998;4(12):1636–1652.
   PubMed Web of Science ®Google Scholar
• Eppens NA, Rensen S, Granneman S, et al. The roles of Rrp5p in the synthesis of yeast 18S and 5.8S rRNA can be functionally and physically separated. RNA (New York, N.Y.) 1999;5( 6):779–793.
   Google Scholar
• Hierlmeier T, Merl J, Sauert M, et al. Rrp5p, Noc1p and Noc2p form a protein module which is part of early large ribosomal subunit precursors in S. cerevisiae. Nucleic Acids Res. 2013;41(2):1191–1210.
   PubMed Web of Science ®Google Scholar
• Lebaron S, Segerstolpe A, French SL, et al. Rrp5 binding at multiple sites coordinates pre-rRNA processing and assembly. Mol Cell. 2013;52(5):707–719.
   PubMed Web of Science ®Google Scholar
• Vos HR, Bax R, Faber AW, et al. 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(19):5827–5833.
   PubMed Web of Science ®Google Scholar
• Khoshnevis S, Askenasy I, Johnson MC, et al. The DEAD-box protein Rok1 Orchestrates 40S and 60S ribosome assembly by promoting the release of Rrp5 from Pre-40S ribosomes to allow for 60S maturation. PLoS Biol. 2016;14(6):e1002480.
   PubMed Web of Science ®Google Scholar
• Colley A, Beggs JD, Tollervey D, et al. Dhr1p, a putative DEAH-box RNA helicase, is associated with the box C+D snoRNP U3. Mol Cell Biol. 2000;20(19):7238–7246.
   PubMed Web of Science ®Google Scholar
• Choque E, Marcellin M, Burlet-Schiltz O, et al. The nucleolar protein Nop19p interacts preferentially with Utp25p and Dhr2p and is essential for the production of the 40S ribosomal subunit in Saccharomyces cerevisiae. RNA Biol. 2011;8(6):1158–1172.
   PubMed Web of Science ®Google Scholar
• Vincent NG, Charette JM, Baserga SJ. The SSU processome interactome in Saccharomyces cerevisiae reveals novel protein subcomplexes. RNA. 2018;24(1):77–89.
   PubMed Web of Science ®Google Scholar
• Reed BJ, Locke MN, Gardner RG. A conserved deubiquitinating enzyme uses intrinsically disordered regions to scaffold multiple protein interaction sites. J Biol Chem. 2015;290(33):20601–20612.
   PubMed Web of Science ®Google Scholar
• Richardson LA, Reed BJ, Charette JM, et al. A conserved deubiquitinating enzyme controls cell growth by regulating RNA polymerase I stability. Cell Rep. 2012;2(2):372–385.
   PubMed Web of Science ®Google Scholar
• Boneberg FM, Brandmann T, Kobel L, et al. Molecular mechanism of the RNA helicase DHX37 and its activation by UTP14A in ribosome biogenesis. RNA. 2019;25(6):685–701.
   PubMed Web of Science ®Google Scholar
• Zhu J, Liu X, Anjos M, et al. Utp14 Recruits and activates the RNA helicase Dhr1 to undock U3 snoRNA from the Preribosome. Mol Cell Biol. 2016;36(6):965–978.
   PubMed Web of Science ®Google Scholar
• Choudhury P, Hackert P, Memet I, et al. The human RNA helicase DHX37 is required for release of the U3 snoRNP from pre-ribosomal particles. RNA Biol. 2019;16(1):54–68.
   PubMed Web of Science ®Google Scholar
• Roychowdhury A, Joret C, Bourgeois G, et al. The DEAH-box RNA helicase Dhr1 contains a remarkable carboxyl terminal domain essential for small ribosomal subunit biogenesis. Nucleic Acids Res. 2019;47(14):7548–7563.
   PubMed Web of Science ®Google Scholar
• Sardana R, Zhu J, Gill M, et al. Physical and functional interaction between the methyltransferase Bud23 and the essential DEAH-box RNA helicase Ecm16. Mol Cell Biol. 2014;34(12):2208–2220.
   PubMed Web of Science ®Google Scholar
• Létoquart J, Huvelle E, Wacheul L, et al. Structural and functional studies of Bud23-Trm112 reveal 18S rRNA N7-G1575 methylation occurs on late 40S precursor ribosomes. Proc Natl Acad Sci USA. 2014;111( 51):E5518‐5526.
   Google Scholar
• Black JJ, Sardana R, Elmir EW, et al. Bud23 promotes the final disassembly of the small subunit Processome in Saccharomyces cerevisiae. PLoS Genet. 2020;16(12):e1009215.
   PubMed Web of Science ®Google Scholar
• Vanden Broeck A, Klinge S. An emerging mechanism for the maturation of the small subunit processome. Curr Opin Struct Biol. 2022;73:102331.
   PubMed Web of Science ®Google Scholar
• 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(20):17743–17750.
   PubMed Web of Science ®Google Scholar
• Tanaka N, Schwer B. Mutations in PRP43 that uncouple RNA-dependent NTPase activity and pre-mRNA splicing function. Biochemistry. 2006;45(20):6510–6521.
   PubMed Web of Science ®Google Scholar
• He Y, Staley JP, Andersen GR, et al. Structure of the DEAH/RHA ATPase Prp43p bound to RNA implicates a pair of hairpins and motif Va in translocation along RNA. RNA. 2017;23(7):1110–1124.
   PubMed Web of Science ®Google Scholar
• Bohnsack KE, Ficner R, Bohnsack MT, et al. Regulation of DEAH-box RNA helicases by G-patch proteins. Biol Chem. 2021;402(5):561–579.
   PubMed Web of Science ®Google Scholar
• Robert-Paganin J, Réty S, Leulliot N. Regulation of DEAH/RHA helicases by G-patch proteins. Biomed Res Int. 2015;2015:931857.
   PubMed Web of Science ®Google Scholar
• 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(1):135–147.
   PubMed Web of Science ®Google Scholar
• Mouffok S, Capeyrou R, Belhabich-Baumas K, et al. The G-patch activators Pfa1 and PINX1 exhibit different modes of interaction with the Prp43 RNA helicase. RNA Biol. 2021;18(4):510–522.
   PubMed Web of Science ®Google Scholar
• Chen Y-L, Capeyrou R, Humbert O, et al. The telomerase inhibitor Gno1p/PINX1 activates the helicase Prp43p during ribosome biogenesis. Nucleic Acids Res. 2014;42(11):7330–7345.
   PubMed Web of Science ®Google Scholar
• Heininger AU, Hackert P, Andreou AZ, et al. Protein cofactor competition regulates the action of a multifunctional RNA helicase in different pathways. RNA Biol. 2016;13(3):320–330.
   PubMed Web of Science ®Google Scholar
• Lebaron S, Papin C, Capeyrou R, et al. The ATPase and helicase activities of Prp43p are stimulated by the G-patch protein Pfa1p during yeast ribosome biogenesis. EMBO J. 2009;28(24):3808–3819.
   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(18):2312–2325.
   PubMed Web of Science ®Google Scholar
• Combs DJ, Nagel RJ, Ares M, et al. Prp43p is a DEAH-box spliceosome disassembly factor essential for ribosome biogenesis. Mol Cell Biol. 2006;26(2):523–534.
   PubMed Web of Science ®Google Scholar
• Lebaron S, Froment C, Fromont-Racine M, et al. The splicing ATPase prp43p is a component of multiple preribosomal particles. Mol Cell Biol. 2005;25(21):9269–9282.
   PubMed Web of Science ®Google Scholar
• Leeds NB, Small EC, Hiley SL, et al. The splicing factor Prp43p, a DEAH box ATPase, functions in ribosome biogenesis. Mol Cell Biol. 2006;26(2):513–522.
   PubMed Web of Science ®Google Scholar
• 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(38):35712–35719.
   PubMed Web of Science ®Google Scholar
• Bohnsack MT, Martin R, Granneman S, et al. Prp43 bound at different sites on the pre-rRNA performs distinct functions in ribosome synthesis. Mol Cell. 2009;36(4):583–592.
   PubMed Web of Science ®Google Scholar
• Pertschy B, Schneider C, Gnädig M, et al. RNA helicase Prp43 and its co-factor Pfa1 promote 20 to 18S rRNA processing catalyzed by the endonuclease Nob1. J Biol Chem. 2009;284(50):35079–35091.
   PubMed Web of Science ®Google Scholar
• Tauchert MJ, Fourmann J-B, Christian H, et al. Structural and functional analysis of the RNA helicase Prp43 from the thermophilic eukaryote Chaetomium thermophilum. Acta Crystallographica. Section F, Struct Biol Commun. 2016;72(Pt 2):112–120.
   PubMedGoogle Scholar
• Studer MK, Ivanović L, Weber ME, et al. Structural basis for DEAH-helicase activation by G-patch proteins. Proc Natl Acad Sci USA. 2020;117( 13):7159–7170.
   Google Scholar
• Nissan TA, Baßler J, Petfalski E, et al. 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J. 2002;21(20):5539–5547.
   PubMed Web of Science ®Google Scholar
• Rocak S, Emery B, Tanner NK, et al. Characterization of the ATPase and unwinding activities of the yeast DEAD-box protein Has1p and the analysis of the roles of the conserved motifs. Nucleic Acids Res. 2005;33(3):999–1009.
   PubMed Web of Science ®Google Scholar
• Gnanasundram SV, Kos-Braun IC, Koš M. At least two molecules of the RNA helicase Has1 are simultaneously present in pre-ribosomes during ribosome biogenesis. Nucleic Acids Res. 2019;47(20):10852–10864.
   PubMed Web of Science ®Google Scholar
• Emery B, de la Cruz J, Rocak S, et al. Has1p, a member of the DEAD-box family, is required for 40S ribosomal subunit biogenesis in Saccharomyces cerevisiae. Mol Microbiol. 2004;52(1):141–158.
   PubMed Web of Science ®Google Scholar
• Dembowski JA, Kuo B, Woolford JL. Has1 regulates consecutive maturation and processing steps for assembly of 60S ribosomal subunits. Nucleic Acids Res. 2013;41(16):7889–7904.
   PubMed Web of Science ®Google Scholar
• Liang X, Fournier MJ. The helicase Has1p is required for snoRNA release from pre-rRNA. Mol Cell Biol. 2006;26(20):7437–7450.
   PubMed Web of Science ®Google Scholar
• Liu X, Huang H, Karbstein K. Blocking a dead-end assembly pathway creates a point of regulation for the DEAD-box ATPase Has1 and prevents platform misassembly. preprint at bioRxiv; 2021.
   Google Scholar
• Thoms M, Ahmed YL, Maddi K, et al. Concerted removal of the Erb1-Ytm1 complex in ribosome biogenesis relies on an elaborate interface. Nucleic Acids Res. 2016;44(2):926–939.
   PubMed Web of Science ®Google Scholar
• Bernstein J, Patterson DN, Wilson GM, et al. Characterization of the essential activities of Saccharomyces cerevisiae Mtr4p, a 3’-5’ helicase partner of the nuclear exosome. J Biol Chem. 2008;283(8):4930–4942.
   PubMed Web of Science ®Google Scholar
• Allmang C, Kufel J, Chanfreau G, et al. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J. 1999;18(19):5399–5410.
   PubMed Web of Science ®Google Scholar
• Delan-Forino C, Spanos C, Rappsilber J, et al. Substrate specificity of the TRAMP nuclear surveillance complexes. Nat Commun. 2020;11(1):3122.
   PubMed Web of Science ®Google Scholar
• Jia H, Wang X, Anderson JT, et al. RNA unwinding by the Trf4/Air2/Mtr4 polyadenylation (TRAMP) complex. Proceedings of the National Academy of Sciences of the United States of America. 2012;109( 19):7292–7297.
   Google Scholar
• Jia H, Wang X, Liu F, et al. The RNA helicase Mtr4p modulates polyadenylation in the TRAMP complex. Cell. 2011;145(6):890–901.
   PubMed Web of Science ®Google Scholar
• LaCava J, Houseley J, Saveanu C, et al. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell. 2005;121(5):713–724.
   PubMed Web of Science ®Google Scholar
• Vanácová S, Wolf J, Martin G, et al. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biol. 2005;3(6):e189.
   PubMed Web of Science ®Google Scholar
• Wyers F, Rougemaille M, Badis G, et al. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell. 2005;121(5):725–737.
   PubMed Web of Science ®Google Scholar
• Allmang C, Mitchell P, Petfalski E, et al. Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res. 2000;28(8):1684–1691.
   PubMed Web of Science ®Google Scholar
• de la Cruz J, Kressler D, et al. Dob1p (Mtr4p) is a putative ATP-dependent RNA helicase required for the 3’ end formation of 5.8S rRNA in Saccharomyces cerevisiae. EMBO J. 1998;17(4):1128–1140.
   PubMed Web of Science ®Google Scholar
• Thoms M, Thomson E, Baßler J, et al. The Exosome Is Recruited to RNA Substrates through Specific Adaptor Proteins. Cell. 2015;162(5):1029–1038.
   PubMed Web of Science ®Google Scholar
• Jackson RN, Klauer AA, Hintze BJ, et al. The crystal structure of Mtr4 reveals a novel arch domain required for rRNA processing. EMBO J. 2010;29(13):2205–2216.
   PubMed Web of Science ®Google Scholar
• Weir JR, Bonneau F, Hentschel J, et al. Structural analysis reveals the characteristic features of Mtr4, a DExH helicase involved in nuclear RNA processing and surveillance. Proc Natl Acad Sci USA. 2010;107( 27):12139–12144.
   Google Scholar
• Halbach F, Rode M, Conti E. The crystal structure of S. cerevisiae Ski2, a DExH helicase associated with the cytoplasmic functions of the exosome. RNA. 2012;18(1):124–134.
   PubMed Web of Science ®Google Scholar
• Bonneau F, Basquin J, Ebert J, et al. The yeast exosome functions as a macromolecular cage to channel RNA substrates for degradation. Cell. 2009;139(3):547–559.
   PubMed Web of Science ®Google Scholar
• Makino DL, Baumgärtner M, Conti E. Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex. Nature. 2013;495(7439):70–75.
   PubMed Web of Science ®Google Scholar
• Makino DL, Schuch B, Stegmann E, et al. RNA degradation paths in a 12-subunit nuclear exosome complex. Nature. 2015;524(7563):54–58.
   PubMed Web of Science ®Google Scholar
• Wasmuth EV, Lima CD. The Rrp6 C-terminal domain binds RNA and activates the nuclear RNA exosome. Nucleic Acids Res. 2017;45(2):846–860.
   PubMed Web of Science ®Google Scholar
• Barrio-Garcia C, Thoms M, Flemming D, et al. Architecture of the Rix1-Rea1 checkpoint machinery during pre-60S-ribosome remodeling. Nat Struct Mol Biol. 2016;23(1):37–44.
   PubMed Web of Science ®Google Scholar
• Lingaraju M, Johnsen D, Schlundt A, et al. The MTR4 helicase recruits nuclear adaptors of the human RNA exosome using distinct arch-interacting motifs. Nat Commun. 2019;10(1):3393.
   PubMed Web of Science ®Google Scholar
• Kikuma T, Ohtsu M, Utsugi T, et al. Dbp9p, a member of the DEAD box protein family, exhibits DNA helicase activity. J Biol Chem. 2004;279(20):20692–20698.
   PubMed Web of Science ®Google Scholar
• Aquino GRR, Hackert P, Krogh N, et al. The RNA helicase Dbp7 promotes domain V/VI compaction and stabilization of inter-domain interactions during early 60S assembly. Nat Commun. 2021;12(1):6152.
   PubMed Web of Science ®Google Scholar
• Bernstein KA, Granneman S, Lee AV, et al. Comprehensive mutational analysis of yeast DEXD/H box RNA helicases involved in large ribosomal subunit biogenesis. Mol Cell Biol. 2006;26(4):1195–1208.
   PubMed Web of Science ®Google Scholar
• Daugeron MC, Linder P. Dbp7p, a putative ATP-dependent RNA helicase from Saccharomyces cerevisiae, is required for 60S ribosomal subunit assembly. RNA. 1998;4(5):566–581.
   PubMed Web of Science ®Google Scholar
• de la Cruz J, Lacombe T, Deloche O, et al. The putative RNA helicase Dbp6p functionally interacts with Rpl3p, Nop8p and the novel trans-acting factor Rsa3p during biogenesis of 60S ribosomal subunits in Saccharomyces cerevisiae. Genetics. 2004;166(4):1687–1699.
   PubMed Web of Science ®Google Scholar
• Kressler D, de la Cruz J, Rojo M, et al. Dbp6p is an essential putative ATP-dependent RNA helicase required for 60S-ribosomal-subunit assembly in Saccharomyces cerevisiae. Mol Cell Biol. 1998;18(4):1855–1865.
   PubMed Web of Science ®Google Scholar
• Kressler D, Doère M, Rojo M, et al. Synthetic lethality with conditional dbp6 alleles identifies Rsa1p, a nucleoplasmic protein involved in the assembly of 60S ribosomal subunits. Mol Cell Biol. 1999;19(12):8633–8645.
   PubMed Web of Science ®Google Scholar
• Rosado D IV, Lebaron CS, et al. Characterization of Saccharomyces cerevisiae Npa2p (Urb2p) reveals a low-molecular-mass complex containing Dbp6p, Npa1p (Urb1p. Nop8p, and Rsa3p Involved in Early Steps of 60S Ribosomal Subunit Biogenesis Mol Cell Biol. 2007;27(4):1207–1221.
   Google Scholar
• Aquino GRR, Krogh N, Hackert P, et al. RNA helicase-mediated regulation of snoRNP dynamics on pre-ribosomes and rRNA 2’-O-methylation. Nucleic Acids Res. 2021;49(7):4066–4084.
   PubMed Web of Science ®Google Scholar
• Lygerou Z, Allmang C, Tollervey D, et al. Accurate processing of a eukaryotic precursor ribosomal RNA by ribonuclease MRP in vitro. Science. 1996;272(5259):268–270.
   PubMed Web of Science ®Google Scholar
• Weaver PL, Sun C, Chang TH. Dbp3p, a putative RNA helicase in Saccharomyces cerevisiae, is required for efficient pre-rRNA processing predominantly at site A3. Mol Cell Biol. 1997;17(3):1354–1365.
   PubMed Web of Science ®Google Scholar
• Talkish J, Biedka S, Jakovljevic J, et al. Disruption of ribosome assembly in yeast blocks cotranscriptional pre-rRNA processing and affects the global hierarchy of ribosome biogenesis. RNA. 2016;22(6):852–866.
   PubMed Web of Science ®Google Scholar
• Adams CC, Jakovljevic J, Roman J, et al. Saccharomyces cerevisiae nucleolar protein Nop7p is necessary for biogenesis of 60S ribosomal subunits. RNA. 2002;8(2):150–165.
   PubMed Web of Science ®Google Scholar
• Ripmaster TL, Vaughn GP, Woolford JL. A putative ATP-dependent RNA helicase involved in Saccharomyces cerevisiae ribosome assembly. Proc Natl Acad Sci USA. 1992;89( 23):11131–11135.
   Google Scholar
• Merl J, Jakob S, Ridinger K, et al. Analysis of ribosome biogenesis factor-modules in yeast cells depleted from pre-ribosomes. Nucleic Acids Res. 2010;38(9):3068–3080.
   PubMed Web of Science ®Google Scholar
• Kellner M, Rohrmoser M, Forné I, et al. DEAD-box helicase DDX27 regulates 3’ end formation of ribosomal 47S RNA and stably associates with the PeBoW-complex. Exp Cell Res. 2015;334(1):146–159.
   PubMed Web of Science ®Google Scholar
• Zagulski M, Kressler D, Bécam A-M, et al. Mak5p, which is required for the maintenance of the M1 dsRNA virus, is encoded by the yeast ORF YBR142w and is involved in the biogenesis of the 60S subunit of the ribosome. Mol Genet Genomics. 2003;270(3):216–224.
   PubMed Web of Science ®Google Scholar
• Pratte D, Singh U, Murat G, et al. Mak5 and Ebp2 act together on early pre-60S particles and their reduced functionality bypasses the requirement for the essential pre-60S factor Nsa1. PloS One. 2013;8(12):e82741.
   PubMed Web of Science ®Google Scholar
• Bond AT, Mangus DA, He F, et al. Absence of Dbp2p alters both nonsense-mediated mRNA decay and rRNA processing. Mol Cell Biol. 2001;21(21):7366–7379.
   PubMed Web of Science ®Google Scholar
• Cloutier SC, Ma WK, Nguyen LT, et al. The DEAD-box RNA helicase Dbp2 connects RNA quality control with repression of aberrant transcription. J Biol Chem. 2012;287(31):26155–26166.
   PubMed Web of Science ®Google Scholar
• Ma WK, Paudel BP, Xing Z, et al. Recruitment, duplex unwinding and protein-mediated inhibition of the dead-box RNA Helicase Dbp2 at actively transcribed chromatin. J Mol Biol. 2016;428(6):1091–1106.
   PubMed Web of Science ®Google Scholar
• Tedeschi FA, Cloutier SC, Tran EJ, et al. The DEAD-box protein Dbp2p is linked to noncoding RNAs, the helicase Sen1p, and R-loops. RNA. 2018;24(12):1693–1705.
   PubMed Web of Science ®Google Scholar
• Wery M, Descrimes M, Vogt N, et al. Nonsense-mediated decay restricts LncRNA levels in yeast unless blocked by double-stranded RNA structure. Mol Cell. 2016;61(3):379–392.
   PubMed Web of Science ®Google Scholar
• Hirling H, Scheffner M, Restle T, et al. RNA helicase activity associated with the human p68 protein. Nature. 1989;339(6225):562–564.
   PubMed Web of Science ®Google Scholar
• Xing Z, Wang S, Tran EJ. Characterization of the mammalian DEAD-box protein DDX5 reveals functional conservation with S. cerevisiae ortholog Dbp2 in transcriptional control and glucose metabolism. RNA. 2017;23(7):1125–1138.
   PubMed Web of Science ®Google Scholar
• Saveanu C, Namane A, Gleizes P-E, et al. Sequential protein association with nascent 60S ribosomal particles. Mol Cell Biol. 2003;23(13):4449–4460.
   PubMed Web of Science ®Google Scholar
• Jalal C, Uhlmann-Schiffler H, Stahl H. Redundant role of DEAD box proteins p68 (Ddx5) and p72/p82 (Ddx17) in ribosome biogenesis and cell proliferation. Nucleic Acids Res. 2007;35(11):3590–3601.
   PubMed Web of Science ®Google Scholar
• Peculis BA. The sequence of the 5’ end of the U8 small nucleolar RNA is critical for 5.8S and 28S rRNA maturation. Mol Cell Biol. 1997;17(7):3702–3713.
   PubMed Web of Science ®Google Scholar
• Peculis BA, Steitz JA. Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell. 1993;73(6):1233–1245.
   PubMed Web of Science ®Google Scholar
• Srivastava L, Lapik YR, Wang M, et al. Mammalian DEAD box protein Ddx51 acts in 3’ end maturation of 28S rRNA by promoting the release of U8 snoRNA. Mol Cell Biol. 2010;30(12):2947–2956.
   PubMed Web of Science ®Google Scholar
• Peculis BA, Greer CL. The structure of the ITS2-proximal stem is required for pre-rRNA processing in yeast. RNA. 1998;4(12):1610–1622.
   PubMed Web of Science ®Google Scholar
• Côté CA, Greer CL, Peculis BA. Dynamic conformational model for the role of ITS2 in pre-rRNA processing in yeast. RNA. 2002;8(6):786–797.
   PubMed Web of Science ®Google Scholar
• Burger F, Daugeron MC, Linder P. Dbp10p, a putative RNA helicase from Saccharomyces cerevisiae, is required for ribosome biogenesis. Nucleic Acids Res. 2000;28(12):2315–2323.
   PubMed Web of Science ®Google Scholar
• Baßler J, Kallas M, Hurt E. The NUG1 GTPase reveals and N-terminal RNA-binding domain that is essential for association with 60S pre-ribosomal particles. J Biol Chem. 2006;281(34):24737–24744.
   PubMed Web of Science ®Google Scholar
• Babiano R, de la Cruz J. Ribosomal protein L35 is required for 27SB pre-rRNA processing in Saccharomyces cerevisiae. Nucleic Acids Res. 2010;38(15):5177–5192.
   PubMed Web of Science ®Google Scholar
• Gamalinda M, Jakovljevic J, Babiano R, et al. Yeast polypeptide exit tunnel ribosomal proteins L17, L35 and L37 are necessary to recruit late-assembling factors required for 27SB pre-rRNA processing. Nucleic Acids Res. 2013;41(3):1965–1983.
   PubMed Web of Science ®Google Scholar
• Pöll G, Braun T, Jakovljevic J, et al. rRNA maturation in yeast cells depleted of large ribosomal subunit proteins. PloS One. 2009;4(12):e8249.
   PubMed Web of Science ®Google Scholar
• Talkish J, Zhang J, Jakovljevic J, et al. Hierarchical recruitment into nascent ribosomes of assembly factors required for 27SB pre-rRNA processing in Saccharomyces cerevisiae. Nucleic Acids Res. 2012;40(17):8646–8661.
   PubMed Web of Science ®Google Scholar
• Diges CM, Uhlenbeck OC. Escherichia coli DbpA is an RNA helicase that requires hairpin 92 of 23S rRNA. EMBO J. 2001;20(19):5503–5512.
   PubMed Web of Science ®Google Scholar
• Nicol SM, Fuller-Pace FV. The “DEAD box” protein DbpA interacts specifically with the peptidyltransferase center in 23S rRNA. Proc Natl Acad Sci USA. 1995;92( 25):11681–11685.
   Google Scholar
• Tsu CA, Kossen K, Uhlenbeck OC. The Escherichia coli DEAD protein DbpA recognizes a small RNA hairpin in 23S rRNA. RNA. 2001;7(5):702–709.
   PubMed Web of Science ®Google Scholar
• Wurm JP, Glowacz K-A, Sprangers R. Structural basis for the activation of the DEAD-box RNA helicase DbpA by the nascent ribosome. Proc Natl Acad Sci USA. 2021;118( 35).
   Google Scholar
• Karginov FV, Uhlenbeck OC. Interaction of Escherichia coli DbpA with 23S rRNA in different functional states of the enzyme. Nucleic Acids Res. 2004;32(10):3028–3032.
   PubMed Web of Science ®Google Scholar
• Lapeyre B, Purushothaman SK. Spb1p-directed formation of Gm2922 in the ribosome catalytic center occurs at a late processing stage. Mol Cell. 2004;16(4):663–669.
   PubMed Web of Science ®Google Scholar
• Sharma S, Yang J, Watzinger P, et al. Yeast Nop2 and Rcm1 methylate C2870 and C2278 of the 25S rRNA, respectively. Nucleic Acids Res. 2013;41(19):9062–9076.
   PubMed Web of Science ®Google Scholar
• de la Cruz J, Kressler D, Rojo M, et al. Spb4p, an essential putative RNA helicase, is required for a late step in the assembly of 60S ribosomal subunits in Saccharomyces cerevisiae. RNA. 1998;4(10):1268–1281.
   PubMed Web of Science ®Google Scholar
• García-Gómez JJ, Lebaron S, Froment C, et al. Dynamics of the putative RNA helicase Spb4 during ribosome assembly in Saccharomyces cerevisiae. Mol Cell Biol. 2011;31(20):4156–4164.
   PubMed Web of Science ®Google Scholar
• Choudhury P, Kretschmer J, Hackert P, et al. The DExD box ATPase DDX55 is recruited to domain IV of the 28S ribosomal RNA by its C-terminal region. RNA Biol. 2021;18(8):1124–1135.
   PubMed Web of Science ®Google Scholar