Trypanosoma brucei RRP44 is involved in an early stage of large ribosomal subunit RNA maturation

References

• Henras AK, Soudet J, Gérus M, et al. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci. 2008;65(15):2334–2359.
   PubMed Web of Science ®Google Scholar
• Henras AK, Plisson-Chastang C, O’Donohue MF, et al. An overview of pre-ribosomal RNA processing in eukaryotes. Wiley Interdiscip Rev RNA. 2015;6(2):225–242.
   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
• Turowski TW, Tollervey D. Cotranscriptional events in eukaryotic ribosome synthesis. Wiley Interdiscip Rev RNA. 2015;6(1):129–139.
   PubMed Web of Science ®Google 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
• 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
• Kater L, Thoms M, Barrio-Garcia C, et al. Visualizing the assembly pathway of nucleolar pre-60s ribosomes. Cell. 2017;171(7):1599–1610.
   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
• Tomecki R, Sikorski PJ, Zakrzewska-Placzek M. Comparison of preribosomal RNA processing pathways in yeast, plant and human cells - focus on coordinated action of endo- and exoribonucleases. FEBS Lett. 2017;591(13):1801–1850.
   PubMed Web of Science ®Google Scholar
• White TC, Rudenko G, Borst P. Three small RNAs within the 10 kb trypanosome rRNA transcription unit are analogous to domain VII of other eukaryotic 28S rRNAs. Nucleic Acids Res. 1986;14(23):9471–9489.
   PubMed Web of Science ®Google Scholar
• Campbell DA, Kubo K, Clark CG, et al. Precise identification of cleavage sites involved in the unusual processing of trypanosome ribosomal RNA. J Mol Biol. 1987;196(1):113–124.
   PubMed Web of Science ®Google Scholar
• Hartshorne T, Toyofuku W. Two 5ʹ-ETS regions implicated in interactions with U3 snoRNA are required for small subunit rRNA maturation in Trypanosoma brucei. Nucleic Acids Res. 1999;27(16):3300–3309.
   PubMed Web of Science ®Google Scholar
• Hashem Y, Des Georges A, Fu J, et al. High-resolution cryo-electron microscopy structure of the Trypanosoma brucei ribosome. Nature. 2013;494(7437):385–389.
   PubMed Web of Science ®Google Scholar
• Rosenblad MA, López MD, Piccinelli P, et al. Inventory and analysis of the protein subunits of the ribonucleases P and MRP provides further evidence of homology between the yeast and human enzymes. Nucleic Acids Res. 2006;34(18):5145–5156.
   PubMed Web of Science ®Google Scholar
• Piccinelli P, Rosenblad MA, Samuelsson T. Identification and analysis of ribonuclease P and MRP RNA in a broad range of eukaryotes. Nucleic Acids Res. 2005;33(14):4485–4495.
   PubMed Web of Science ®Google Scholar
• Chu S, Archer RH, Zengel JM, et al. The RNA of RNase MRP is required for normal processing of ribosomal RNA. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):659–663.
   PubMed Web of Science ®Google Scholar
• Lindahl L, Bommankanti A, Li X, et al. RNase MRP is required for entry of 35S precursor rRNA into the canonical processing pathway. RNA. 2009;15(7):1407–1416.
   PubMed Web of Science ®Google Scholar
• Goldfarb KC, Cech TR. Targeted CRISPR disruption reveals a role for RNase MRP RNA in human preribosomal RNA processing. Genes Dev. 2017;31(1):59–71.
   PubMed Web of Science ®Google Scholar
• Mitchell P. Exosome substrate targeting: the long and short of it. Biochem Soc Trans. 2014;42(4):1129–1134.
   PubMedGoogle Scholar
• Januszyk K, Lima CD. The eukaryotic RNA exosome. Curr Opin Struct Biol. 2014;24:132–140.
   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
• 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
• Lebreton A, Tomecki R, Dziembowski A, et al. Endonucleolytic RNA cleavage by a eukaryotic exosome. Nature. 2008;456(7224):993–996.
   PubMed Web of Science ®Google Scholar
• Schneider C, Leung E, Brown J, et al. The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res. 2009;37(4):1127–1140.
   PubMed Web of Science ®Google 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
• 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(5):577–588.
   PubMed Web of Science ®Google Scholar
• Estévez AM, Kempf T, Clayton C. The exosome of Trypanosoma brucei. Embo J. 2001;20(14):3831–3839.
   PubMed Web of Science ®Google Scholar
• Estévez AM, Lehner B, Sanderson CM, et al. The roles of intersubunit interactions in exosome stability. J Biol Chem. 2003;278(37):34943–34951.
   PubMed Web of Science ®Google Scholar
• Cristodero M, Böttcher B, Diepholz M, et al. The Leishmania tarentolae exosome: purification and structural analysis by electron microscopy. Mol Biochem Parasitol. 2008;159(1):24–29.
   PubMed Web of Science ®Google Scholar
• Jensen BC, Wang Q, Kifer CT, et al. The NOG1 GTP-binding protein is required for biogenesis of the 60 S ribosomal subunit. J Biol Chem. 2003;278(34):32204–32211.
   PubMed Web of Science ®Google Scholar
• Hartshorne T, Agabian N. RNA B is the major nucleolar trimethylguanosine-capped small nuclear RNA associated with fibrillarin and pre-rRNAs in Trypanosoma brucei. Mol Cell Biol. 1993;13(1):144–154.
   PubMed Web of Science ®Google Scholar
• Umaer K, Ciganda M, Williams N. Ribosome biogenesis in african trypanosomes requires conserved and trypanosome-specific factors. Eukaryot Cell. 2014;13(6):727–737.
   PubMedGoogle 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
• Zinder JC, Wasmuth EV, Lima CD. Nuclear RNA exosome at 3.1 Å reveals substrate specificities, RNA paths, and allosteric inhibition of Rrp44/Dis3. Mol Cell. 2016;64(4):734–745.
   PubMed Web of Science ®Google Scholar
• Liu JJ, Bratkowski MA, Liu X, et al. Visualization of distinct substrate-recruitment pathways in the yeast exosome by EM. Nat Struct Mol Biol. 2014;21(1):95–102.
   PubMed Web of Science ®Google Scholar
• Kala S, Mehta V, Yip CW, et al. The interaction of a Trypanosoma brucei KH-domain protein with a ribonuclease is implicated in ribosome processing. Mol Biochem Parasitol. 2017;211:94–103.
   PubMed Web of Science ®Google Scholar
• Wasmuth EV, Lima CD. Exo- and endoribonucleolytic activities of yeast cytoplasmic and nuclear RNA exosomes are dependent on the noncatalytic core and central channel. Mol Cell. 2012;48(1):133–144.
   PubMed Web of Science ®Google Scholar
• Drazkowska K, Tomecki R, Stodus K, et al. The RNA exosome complex central channel controls both exonuclease and endonuclease Dis3 activities in vivo and in vitro. Nucleic Acids Res. 2013;41(6):3845–3858.
   PubMed Web of Science ®Google Scholar
• Schillewaert S, Wacheul L, Lhomme F, et al. The evolutionarily conserved protein Las1 is required for pre-rRNA processing at both ends of ITS2. Mol Cell Biol. 2012 Jan;32(2):430–444.
   PubMed Web of Science ®Google 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
• Schaeffer D, Reis FP, Johnson SJ, et al. The CR3 motif of Rrp44p is important for interaction with the core exosome and exosome function. Nucleic Acids Res. 2012;40(18):9298–9307.
   PubMed Web of Science ®Google Scholar
• Sakyiama J, Zimmer SL, Ciganda M, et al. Ribosome biogenesis requires a highly diverged XRN family 5ʹ->3ʹ exoribonuclease for rRNA processing in Trypanosoma brucei. Rna. 2013;19(10):1419–1431.
   PubMed Web of Science ®Google Scholar
• Fleming IM, Paris Z, Gaston KW, et al. A tRNA methyltransferase paralog is important for ribosome stability and cell division in Trypanosoma brucei. Sci Rep. 2016;6:21438.
   PubMed Web of Science ®Google Scholar
• Clayton CE. Gene expression in kinetoplastids. Curr Opin Microbiol. 2016;32:46–51.
   PubMed Web of Science ®Google Scholar
• Wickstead B, Ersfeld K, Gull K. Targeting of a tetracycline-inducible expression system to the transcriptionally silent minichromosomes of Trypanosoma brucei. Mol Biochem Parasitol. 2002;125(1–2):211–216.
   PubMed Web of Science ®Google Scholar
• Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29(9):e45.
   PubMed Web of Science ®Google Scholar
• Church GM, Gilbert W. Genomic sequencing. Proc Nat Acad Sci USA. 1984;81:1991–1995.
   PubMed Web of Science ®Google Scholar
• Kabsch W. XDS. Acta Crystallogr D Biol Crystallogr. 2010;66(2):125–132.
   PubMedGoogle Scholar
• Sheldrick GM. Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr D Biol Crystallogr. 2010;66(4):479–485.
   PubMedGoogle Scholar
• McCoy AJ, Grosse-Kunstleve RW, Adams PD, et al. Phaser crystallographic software. J Appl Crystallogr. 2007;40(4):658–674.
   PubMed Web of Science ®Google Scholar
• Cowtan K. Recent developments in classical density modification. Acta Crystallogr D Biol Crystallogr. 2010;66(4):470–478.
   PubMedGoogle Scholar
• Cowtan K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr. 2006;62(9):1002–1011.
   PubMedGoogle Scholar
• Bricogne G, Blanc E, Brandl M, et al. BUSTER version 2.10.2. Cambridge (UK): Global Phasing Ltd; 2017.
   Google Scholar
• Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004;60(Pt12 Pt 1):2126–2132.
   PubMedGoogle Scholar
• Yang J, Yan R, Roy A, et al. The I-TASSER suite: protein structure and function prediction. Nat Methods. 2015;12(1):7–8.
   PubMed Web of Science ®Google Scholar
• Pei J, Kim BH, Grishin NV. PROMALS3D: a tool for multiple protein sequence and structure alignments. Nucleic Acids Res. 2008;36(7):2295–2300.
   PubMed Web of Science ®Google Scholar
• Protein interfaces, surfaces and assemblies service PISA [Internet]. European Bioinformatics Institute. Available from: http://www.ebi.ac.uk/pdbe/prot_int/pistart.html
   Google Scholar
• Krissinel E, Henrick K. Inference of macromolecular assemblies from crystalline state. J Mol Biol. 2007;372(3):774–797.
   PubMed Web of Science ®Google Scholar
• Glaser F, Pupko T, Paz I, et al. ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics. 2003;19(1):163–164.
   PubMed Web of Science ®Google Scholar
• Landau M, Mayrose I, Rosenberg Y, et al. ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 2005;33:W299–W302.
   PubMed Web of Science ®Google Scholar
• Ashkenazy H, Abadi S, Martz E, et al. ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucl Acids Res. 2016;44:W344–W350.
   PubMed Web of Science ®Google Scholar