2,952
Views
41
CrossRef citations to date
0
Altmetric
Research Paper

The human RNA helicase DHX37 is required for release of the U3 snoRNP from pre-ribosomal particles

, , , &
Pages 54-68 | Received 01 Oct 2018, Accepted 30 Nov 2018, Published online: 27 Dec 2018

References

  • Anger AM, Armache J-P, Berninghausen O, et al. Structures of the human and Drosophila 80S ribosome. Nature. 2013;497:80–85.
  • Woolford JLJ, Baserga SJ. Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics. 2013;195:643–681.
  • Andersen JS, Lyon CE, Fox AH, et al. Directed proteomic analysis of the human nucleolus. Curr Biol. 2002;12:1–11.
  • Scherl A, Coute Y, Deon C, et al. Functional proteomic analysis of human nucleolus. Mol Biol Cell. 2002;13:4100–4109.
  • Wild T, Horvath P, Wyler E, et al. A protein inventory of human ribosome biogenesis reveals an essential function of exportin 5 in 60S subunit export. PLoS Biol. 2010;8:e1000522.
  • Tafforeau L, Zorbas C, Langhendries J-L, et al. The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of Pre-rRNA processing factors. Mol Cell. 2013;51:539–551.
  • Badertscher L, Wild T, Montellese C, et al. Genome-wide RNAi screening identifies protein modules required for 40S subunit synthesis in human cells. Cell Rep. 2015;13:2879–2891.
  • Farley-Barnes KI, McCann KL, Ogawa LM, et al. Diverse regulators of human ribosome biogenesis discovered by changes in nucleolar number. Cell Rep. 2018;22:1923–1934.
  • Sloan KE, Bohnsack MT, Schneider C, et al. The roles of SSU processome components and surveillance factors in the initial processing of human ribosomal RNA. Rna. 2014;20:540–550.
  • Sloan KE, Mattijssen S, Lebaron S, et al. Both endonucleolytic and exonucleolytic cleavage mediate ITS1 removal during human ribosomal RNA processing. J Cell Biol. 2013;200:577–588.
  • Preti M, O’Donohue M-F, Montel-Lehry N, et al. Gradual processing of the ITS1 from the nucleolus to the cytoplasm during synthesis of the human 18S rRNA. Nucleic Acids Res. 2013;41:4709–4723.
  • Mills EW, Green R. Ribosomopathies: there’s strength in numbers. Science. 2017;358:eaan2755.
  • Pelletier J, Thomas G, Volarevic S. Ribosome biogenesis in cancer: new players and therapeutic avenues. Nat Rev Cancer. 2018;18:51–63.
  • Henras AK, Plisson-Chastang C, O’Donohue M-F, et al. An overview of pre-ribosomal RNA processing in eukaryotes. Wiley Interdiscip Rev RNA. 2015;6:225–242.
  • 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.
  • Sloan KE, Warda AS, Sharma S, et al. Tuning the ribosome: the influence of rRNA modification on eukaryotic ribosome biogenesis and function. RNA Biol. 2017;14:1138–1152.
  • 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;44:5399–5409.
  • Wells GR, Weichmann F, Sloan KE, et al. The ribosome biogenesis factor yUtp23/hUTP23 coordinates key interactions in the yeast and human pre-40S particle and hUTP23 contains an essential PIN domain. Nucleic Acids Res. 2017;45:4796–4809.
  • Warda AS, Freytag B, Haag S, et al. Effects of the Bowen-Conradi syndrome mutation in EMG1 on its nuclear import, stability and nucleolar recruitment. Hum Mol Genet. 2016;25:5353–5364.
  • Kass S, Tyc K, Steitz JA, et al. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell. 1990;60:897–908.
  • Sharma K, Venema J, Tollervey D. The 5ʹ end of the 18S rRNA can be positioned from within the mature rRNA. Rna. 1999;5:678–686.
  • 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;259:645–654.
  • Borovjagin AV, Gerbi SA. The spacing between functional Cis-elements of U3 snoRNA is critical for rRNA processing. J Mol Biol. 2000;300:57–74.
  • Barandun J, Chaker-Margot M, Hunziker M, et al. The complete structure of the small-subunit processome. Nat Struct Mol Biol. 2017;24:944–953.
  • Cheng J, Kellner N, Berninghausen O, et al. 3.2-A-resolution structure of the 90S preribosome before A1 pre-rRNA cleavage. Nat Struct Mol Biol. 2017;24:954–964.
  • 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:e1002083.
  • Sloan KE, Gleizes P-E, Bohnsack MT. Nucleocytoplasmic Transport of RNAs and RNA-Protein Complexes. J Mol Biol. 2016;428:2040–2059.
  • Linder P, Jankowsky E. From unwinding to clamping - the DEAD box RNA helicase family. Nat Rev Mol Cell Biol. 2011;12:505–516.
  • Jarmoskaite I, Russell R. RNA helicase proteins as chaperones and remodelers. Annu Rev Biochem. 2014;83:697–725.
  • Liang X-H, Fournier MJ. The helicase Has1p is required for snoRNA release from pre-rRNA. Mol Cell Biol. 2006;26:7437–7450.
  • Bohnsack MT, Kos M, Tollervey D. Quantitative analysis of snoRNA association with pre-ribosomes and release of snR30 by Rok1 helicase. EMBO Rep. 2008;9:1230–1236.
  • 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;36:583–592.
  • Dembowski JA, Kuo B, Woolford JL. Has1 regulates consecutive maturation and processing steps for assembly of 60S ribosomal subunits. Nucleic Acids Res. 2013;41:7889–7904.
  • Pertschy B, Schneider C, Gnadig M, et al. RNA helicase Prp43 and its co-factor Pfa1 promote 20 to 18 S rRNA processing catalyzed by the endonuclease Nob1. J Biol Chem. 2009;284:35079–35091.
  • Martin R, Straub AU, Doebele C, et al. DExD/H-box RNA helicases in ribosome biogenesis. RNA Biol. 2013;10:4–18.
  • Srivastava L, Lapik YR, Wang M, et al. Mammalian DEAD box protein Ddx51 acts in 3ʹ end maturation of 28S rRNA by promoting the release of U8 snoRNA. Mol Cell Biol. 2010;30:2947–2956.
  • Kellner M, Rohrmoser M, Forne I, et al. DEAD-box helicase DDX27 regulates 3ʹ end formation of ribosomal 47S RNA and stably associates with the PeBoW-complex. Exp Cell Res. 2015;334:146–159.
  • Memet I, Doebele C, Sloan KE, et al. The G-patch protein NF-kappaB-repressing factor mediates the recruitment of the exonuclease XRN2 and activation of the RNA helicase DHX15 in human ribosome biogenesis. Nucleic Acids Res. 2017;45:5359–5374.
  • Calo E, Flynn RA, Martin L, et al. RNA helicase DDX21 coordinates transcription and ribosomal RNA processing. Nature. 2015;518:249–253.
  • Sloan KE, Leisegang MS, Doebele C, et al. The association of late-acting snoRNPs with human pre-ribosomal complexes requires the RNA helicase DDX21. Nucleic Acids Res. 2015;43:553–564.
  • Larburu N, Montellese C, O’Donohue M-F, et al. Structure of a human pre-40S particle points to a role for RACK1 in the final steps of 18S rRNA processing. Nucleic Acids Res. 2016;44:8465–8478.
  • Ameismeier M, Cheng J, Berninghausen O, et al. Visualizing late states of human 40S ribosomal subunit maturation. Nature. 2018;558:249–253.
  • Wang M, Pestov DG. 5ʹ-end surveillance by Xrn2 acts as a shared mechanism for mammalian pre-rRNA maturation and decay. Nucleic Acids Res. 2011;39:1811–1822.
  • Zorbas C, Nicolas E, Wacheul L, et al. The human 18S rRNA base methyltransferases DIMT1L and WBSCR22-TRMT112 but not rRNA modification are required for ribosome biogenesis. Mol Biol Cell. 2015;26:2080–2095.
  • Carron C, O’Donohue MF, Choesmel V, et al. Analysis of two human pre-ribosomal factors, bystin and hTsr1, highlights differences in evolution of ribosome biogenesis between yeast and mammals. Nucleic Acids Res. 2011;39:280–291.
  • McCaughan UM, Jayachandran U, Shchepachev V, et al. Pre-40S ribosome biogenesis factor Tsr1 is an inactive structural mimic of translational GTPases. Nat Commun. 2016;7:11789.
  • Leulliot N, Bohnsack MT, Graille M, et al. The yeast ribosome synthesis factor Emg1 is a novel member of the superfamily of alpha/beta knot fold methyltransferases. Nucleic Acids Res. 2008;36:629–639.
  • Meyer B, Wurm JP, Kotter P, et al. The Bowen-Conradi syndrome protein Nep1 (Emg1) has a dual role in eukaryotic ribosome biogenesis, as an essential assembly factor and in the methylation of Psi1191 in yeast 18S rRNA. Nucleic Acids Res. 2011;39:1526–1537.
  • Haag S, Kretschmer J, Bohnsack MT. WBSCR22/Merm1 is required for late nuclear pre-ribosomal RNA processing and mediates N7-methylation of G1639 in human 18S rRNA. Rna. 2015;21:180–187.
  • Bohnsack MT, Tollervey D, Granneman S. Identification of RNA helicase target sites by UV cross-linking and analysis of cDNA [Internet]. 1st ed. Elsevier Inc.; 2012. DOI:10.1016/B978-0-12-396546-2.00013-9.
  • Haag S, Kretschmer J, Sloan KE, et al. Crosslinking methods to identify RNA methyltransferase targets in vivo. Methods Mol Biol. 2017;1562:269–281.
  • Sloan KE, Bohnsack MT. Unravelling the mechanisms of RNA helicase regulation. Trends Biochem Sci. 2018;43:237–250.
  • 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;34:2208–2220.
  • 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:E5518–26.
  • 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;36:965–978.
  • Ounap K, Kasper L, Kurg A, et al. The human WBSCR22 protein is involved in the biogenesis of the 40S ribosomal subunits in mammalian cells. PLoS One. 2013;8:e75686.
  • Choque E, Schneider C, Gadal O, et al. Turnover of aberrant pre-40S pre-ribosomal particles is initiated by a novel endonucleolytic decay pathway. Nucleic Acids Res. 2018;46:4699–4714.
  • White J, Li Z, Sardana R, et al. Bud23 methylates G1575 of 18S rRNA and is required for efficient nuclear export of pre-40S subunits. Mol Cell Biol. 2008;28:3151–3161.
  • 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;13:320–330.