Noncoding RNAs in eukaryotic ribosome biogenesis and function

Nature Structural and Molecular Biology

Volumn 22, Issue 1, 2015, Pages 11-19

  Lafontaine, Denis L J ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL NUCLEOLAR RIBONUCLEOPROTEIN; UNTRANSLATED RNA;

BIOGENESIS; CELL HETEROGENEITY; EUKARYOTE; HUMAN; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; RNA CLEAVAGE; RNA FOLDING; RNA METHYLATION; RNA PROCESSING; RNA SEQUENCE; RNA SPLICING; RNA SYNTHESIS; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

EUKARYOTA;

EUKARYOTA; GENE EXPRESSION REGULATION; MODELS, BIOLOGICAL; MODELS, MOLECULAR; RIBOSOMES; RNA, UNTRANSLATED;

EID: 84925286904     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2939     Document Type: Review

References (94)

1. Voorhees, R.M. & Ramakrishnan, V. Structural basis of the translational elongation cycle. Annu. Rev. Biochem. 82, 203-236 (2013).
2. Lafontaine, D.L.A. 'Garbage can' for ribosomes: how eukaryotes degrade their ribosomes. Trends Biochem. Sci. 35, 267-277 (2010).
3. Narla, A. & Ebert, B.L. Ribosomopathies: human disorders of ribosome dysfunction. Blood 115, 3196-3205 (2010).
4. Freed, E.F., Bleichert, F., Dutca, L.M. & Baserga, S.J. When ribosomes go bad: diseases of ribosome biogenesis. Mol. Biosyst. 6, 481-493 (2010).
5. Gilbert, W.V. Functional specialization of ribosomes? Trends Biochem. Sci. 36, 127-132 (2011).
6. Xue, S. & Barna, M. Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat. Rev. Mol. Cell Biol. 13, 355-369 (2012).
7. Ramagopal, S. Are eukaryotic ribosomes heterogeneous? Affirmations on the horizon. Biochem. Cell Biol. 70, 269-272 (1992).
8. Oeffinger, M. et al. Rrp17p is a eukaryotic exonuclease required for 5′ end processing of Pre-60S ribosomal RNA. Mol. Cell 36, 768-781 (2009).
9. Schillewaert, S., Wacheul, L., Lhomme, F. & Lafontaine, D.L. The evolutionarily conserved protein Las1 is required for pre-rRNA processing at both ends of ITS2. Mol. Cell. Biol. 32, 430-444 (2012).
10. Woolford, J.L. Jr. & Baserga, S.J. Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 195, 643-681 (2013).
11. Strunk, B.S. & Karbstein, K. Powering through ribosome assembly. RNA 15, 2083-2104 (2009).
12. Kressler, D., Hurt, E. & Bassler, J. Driving ribosome assembly. Biochim. Biophys. Acta 1803, 673-683 (2010).
13. Strunk, B.S. et al. Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science 333, 1449-1453 (2011).
14. Bussiere, C., Hashem, Y., Arora, S., Frank, J. & Johnson, A.W. Integrity of the P-site is probed during maturation of the 60S ribosomal subunit. J. Cell Biol. 197, 747-759 (2012).
15. Bradatsch, B. et al. Structure of the pre-60S ribosomal subunit with nuclear export factor Arx1 bound at the exit tunnel. Nat. Struct. Mol. Biol. 19, 1234-1241 (2012).
16. Matsuo, Y. et al. Coupled GTPase and remodelling ATPase activities form a checkpoint for ribosome export. Nature 505, 112-116 (2014).
17. Tafforeau, L. et al. The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of Pre-rRNA processing factors. Mol. Cell 51, 539-551 (2013).
18. Sloan, K.E. et al. Both endonucleolytic and exonucleolytic cleavage mediate ITS1 removal during human ribosomal RNA processing. J. Cell Biol. 200, 577-588 (2013).
19. Kos, M. & Tollervey, D. Yeast pre-rRNA processing and modification occur cotranscriptionally. Mol. Cell 37, 809-820 (2010).
20. Osheim, Y.N. 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 16, 943-954 (2004).
21. Morrissey, J.P. & Tollervey, D. Birth of the snoRNPs: the evolution of RNase MRP and the eukaryotic pre-rRNA-processing system. Trends Biochem. Sci. 20, 78-82 (1995).
22. Lamaye, F., Galliot, S., Alibardi, L., Lafontaine, D.L. & Thiry, M. Nucleolar structure across evolution: the transition between bi- and tri-compartmentalized nucleoli lies within the class Reptilia. J. Struct. Biol. 174, 352-359 (2011).
23. Thiry, M. & Lafontaine, D.L. Birth of a nucleolus: the evolution of nucleolar compartments. Trends Cell Biol. 15, 194-199 (2005).
24. Watkins, N.J. & Bohnsack, M.T. 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 3, 397-414 (2012).
25. Henry, Y. et al. The 5′ end of yeast 5.8S rRNA is generated by exonucleases from an upstream cleavage site. EMBO J. 13, 2452-2463 (1994).
26. Mullineux, S.T. & Lafontaine, D.L. Mapping the cleavage sites on mammalian pre- rRNAs: where do we stand? Biochimie 94, 1521-1532 (2012).
27. Esakova, O. & Krasilnikov, A.S. Of proteins and RNA: the RNase P/MRP family. RNA 16, 1725-1747 (2010).
28. Dragon, F. et al. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417, 967-970 (2002).
29. Peculis, B.A. & Steitz, J.A. Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell 73, 1233-1245 (1993).
30. 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. 19, 6012-6019 (1999).
31. Peculis, B.A. The sequence of the 5′ end of the U8 small nucleolar RNA is critical for 5.8S and 28S rRNA maturation. Mol. Cell. Biol. 17, 3702-3713 (1997).
32. Peculis, B.A. & Greer, C.L. The structure of the ITS2-proximal stem is required for pre-rRNA processing in yeast. RNA 4, 1610-1622 (1998).
33. Bassler, J. et al. The AAA-ATPase Rea1 drives removal of biogenesis factors during multiple stages of 60S ribosome assembly. Mol. Cell 38, 712-721 (2010).
34. Ulbrich, C. et al. Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunits. Cell 138, 911-922 (2009).
35. Kressler, D., Hurt, E., Bergler, H. & Bassler, J. The power of AAA-ATPases on the road of pre-60S ribosome maturation-molecular machines that strip pre-ribosomal particles. Biochim. Biophys. Acta 1823, 92-100 (2012).
36. Boulon, S., Bertrand, E. & Pradet-Balade, B. HSP90 and the R2TP co-chaperone complex: building multi-protein machineries essential for cell growth and gene expression. RNA Biol. 9, 148-154 (2012).
37. Darzacq, X. et al. Cajal body-specific small nuclear RNAs: a novel class of 2′-O- methylation and pseudouridylation guide RNAs. EMBO J. 21, 2746-2756 (2002).
38. Machado-Pinilla, R., Liger, D., Leulliot, N. & Meier, U.T. Mechanism of the AAA+ ATPases pontin and reptin in the biogenesis of H/ACA RNPs. RNA 18, 1833-1845 (2012).
39. Boulon, S. et al. The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J. Cell Biol. 180, 579-595 (2008).
40. Zhao, R. et al. Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation. J. Cell Biol. 180, 563-578 (2008).
41. Loc'h, J. et al. RNA mimicry by the Fap7 adenylate kinase in ribosome biogenesis. PLoS Biol. 12, e1001860 (2014).
42. Walbott, H. et al. The H/ACA RNP assembly factor SHQ1 functions as an RNA mimic. Genes Dev. 25, 2398-2408 (2011).
43. Li, S., Duan, J., Li, D., Ma, S. & Ye, K. Structure of the Shq1-Cbf5-Nop10-Gar1 complex and implications for H/ACA RNP biogenesis and dyskeratosis congenita. EMBO J. 30, 5010-5020 (2011).
44. Leulliot, N. et al. The box H/ACA RNP assembly factor Naf1p contains a domain homologous to Gar1p mediating its interaction with Cbf5p. J. Mol. Biol. 371, 1338-1353 (2007).
45. Rothé, B. et al. Characterization of the interaction between protein Snu13p/15.5K and the Rsa1p/NUFIP factor and demonstration of its functional importance for snoRNP assembly. Nucleic Acids Res. 42, 2015-2036 (2014).
46. Ben-Shem, A. et al. The structure of the eukaryotic ribosome at 3.0 A resolution. Science 334, 1524-1529 (2011).
47. Gunderson, J.H. et al. Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science 238, 933-937 (1987).
48. Velichutina, I.V., Rogers, M.J., McCutchan, T.F. & Liebman, S.W. Chimeric rRNAs containing the GTPase centers of the developmentally regulated ribosomal rRNAs of Plasmodium falciparum are functionally distinct. RNA 4, 594-602 (1998).
49. Azpurua, J. et al. Naked mole-rat has increased translational fidelity compared with the mouse, as well as a unique 28S ribosomal RNA cleavage. Proc. Natl. Acad. Sci. USA 110, 17350-17355 (2013).
50. Birkedal, U. et al. Profiling of ribose methylations in RNA by high-throughput sequencing. Angew. Chem. Int. Ed. Engl. doi:10.1002/anie.201408362 (21 November 2014).
51. Belin, S. et al. Dysregulation of ribosome biogenesis and translational capacity is associated with tumor progression of human breast cancer cells. PLoS ONE 4, e7147 (2009).
52. Buchhaupt, M. et al. Partial methylation at Am100 in 18S rRNA of baker's yeast reveals ribosome heterogeneity on the level of eukaryotic rRNA modification. PLoS ONE 9, e89640 (2014).
53. Decatur, W.A. & Fournier, M.J. rRNA modifications and ribosome function. Trends Biochem. Sci. 27, 344-351 (2002).
54. Bellodi, C. et al. H/ACA small RNA dysfunctions in disease reveal key roles for noncoding RNA modifications in hematopoietic stem cell differentiation. Cell Reports 3, 1493-1502 (2013).
55. Yoon, A. et al. Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita. Science 312, 902-906 (2006).
56. Jack, K. et al. rRNA pseudouridylation defects affect ribosomal ligand binding and translational fidelity from yeast to human cells. Mol. Cell 44, 660-666 (2011).
57. Castle, J.C. et al. Digital genome-wide ncRNA expression, including SnoRNAs, across 11 human tissues using polyA-neutral amplification. PLoS ONE 5, e11779 (2010).
58. Hughes, M.E., Grant, G.R., Paquin, C., Qian, J. & Nitabach, M.N. Deep sequencing the circadian and diurnal transcriptome of Drosophila brain. Genome Res. 22, 1266-1281 (2012).
59. Jouffe, C. et al. The circadian clock coordinates ribosome biogenesis. PLoS Biol. 11, e1001455 (2013).
60. Su, H. et al. Elevated snoRNA biogenesis is essential in breast cancer. Oncogene 33, 1348-1358 (2014).
61. Martens-Uzunova, E.S. et al. Diagnostic and prognostic signatures from the small non-coding RNA transcriptome in prostate cancer. Oncogene 31, 978-991 (2012).
62. Mei, Y.P. et al. Small nucleolar RNA 42 acts as an oncogene in lung tumorigenesis. Oncogene 31, 2794-2804 (2012).
63. Marcel, V. et al. p53 acts as a safeguard of translational control by regulating fibrillarin and rRNA methylation in cancer. Cancer Cell 24, 318-330 (2013).
64. Krastev, D.B. et al. A systematic RNAi synthetic interaction screen reveals a link between p53 and snoRNP assembly. Nat. Cell Biol. 13, 809-818 (2011).
65. Liao, J. et al. Small nucleolar RNA signatures as biomarkers for non-small-cell lung cancer. Mol. Cancer 9, 198 (2010).
66. Gee, H.E. et al. The small-nucleolar RNAs commonly used for microRNA normalisation correlate with tumour pathology and prognosis. Br. J. Cancer 104, 1168-1177 (2011).
67. Appaiah, H.N. et al. Persistent upregulation of U6:SNORD44 small RNA ratio in the serum of breast cancer patients. Breast Cancer Res. 13, R86 (2011).
68. Mannoor, K., Liao, J. & Jiang, F. Small nucleolar RNAs in cancer. Biochim. Biophys. Acta 1826, 121-128 (2012).
69. Houseley, J., Kotovic, K., El Hage, A. & Tollervey, D. Trf4 targets ncRNAs from telomeric and rDNA spacer regions and functions in rDNA copy number control. EMBO J. 26, 4996-5006 (2007).
70. Mayer, C., Schmitz, K.M., Li, J., Grummt, I. & Santoro, R. Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol. Cell 22, 351-361 (2006).
71. Schmitz, K.M., Mayer, C., Postepska, A. & Grummt, I. Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev. 24, 2264-2269 (2010).
72. Manelyte, L., Strohner, R., Gross, T. & Langst, G. Chromatin targeting signals, nucleosome positioning mechanism and non-coding RNA-mediated regulation of the chromatin remodeling complex NoRC. PLoS Genet. 10, e1004157 (2014).
73. Audas, T.E., Jacob, M.D. & Lee, S. Immobilization of proteins in the nucleolus by ribosomal intergenic spacer noncoding RNA. Mol. Cell 45, 147-157 (2012).
74. Taft, R.J. et al. Small RNAs derived from snoRNAs. RNA 15, 1233-1240 (2009).
75. Scott, M.S., Avolio, F., Ono, M., Lamond, A.I. & Barton, G.J. Human miRNA precursors with box H/ACA snoRNA features. PLoS Comput. Biol. 5, e1000507 (2009).
76. Ono, M. et al. Identification of human miRNA precursors that resemble box C/D snoRNAs. Nucleic Acids Res. 39, 3879-3891 (2011).
77. Scott, M.S. et al. Human box C/D snoRNA processing conservation across multiple cell types. Nucleic Acids Res. 40, 3676-3688 (2012).
78. Ender, C. et al. A human snoRNA with microRNA-like functions. Mol. Cell 32, 519-528 (2008).
79. Saraiya, A.A. & Wang, C.C. snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog. 4, e1000224 (2008).
80. Rogler, L.E. et al. Small RNAs derived from lncRNA RNase MRP have gene-silencing activity relevant to human cartilage-hair hypoplasia. Hum. Mol. Genet. 23, 368-382 (2014).
81. Xiao, J., Lin, H., Luo, X., Luo, X. & Wang, Z. miR-605 joins p53 network to form a p53:miR-605:Mdm2 positive feedback loop in response to stress. EMBO J. 30, 524-532 (2011).
82. Kishore, S. & Stamm, S. The snoRNA HBII-52 regulates alternative splicing of the serotonin receptor 2C. Science 311, 230-232 (2006).
83. Kishore, S. et al. The snoRNA MBII-52 (SNORD 115) is processed into smaller RNAs and regulates alternative splicing. Hum. Mol. Genet. 19, 1153-1164 (2010).
84. Yin, Q.F. et al. Long noncoding RNAs with snoRNA ends. Mol. Cell 48, 219-230 (2012).
85. Tessarz, P. et al. Glutamine methylation in histone H2A is an RNA-polymerase-I- dedicated modification. Nature 505, 564-568 (2014).
86. Jobert, L. et al. The human base excision repair enzyme SMUG1 directly interacts with DKC1 and contributes to RNA quality control. Mol. Cell 49, 339-345 (2013).
87. Panse, V.G. & Johnson, A.W. Maturation of eukaryotic ribosomes: acquisition of functionality. Trends Biochem. Sci. 35, 260-266 (2010).
88. Schäfer, T. et al. Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 441, 651-655 (2006).
89. Lo, K.Y. et al. Defining the pathway of cytoplasmic maturation of the 60S ribosomal subunit. Mol. Cell 39, 196-208 (2010).
90. Strunk, B.S., Novak, M.N., Young, C.L. & Karbstein, K. A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 150, 111-121 (2012).
91. Lebaron, S. et al. Proofreading of pre-40S ribosome maturation by a translation initiation factor and 60S subunits. Nat. Struct. Mol. Biol. 19, 744-753 (2012).
92. García-Gómez, J.J. et al. Final pre-40S maturation depends on the functional integrity of the 60S subunit ribosomal protein L3. PLoS Genet. 10, e1004205 (2014).
93. Duan, J., Li, L., Lu, J., Wang, W. & Ye, K. Structural mechanism of substrate RNA recruitment in H/ACA RNA-guided pseudouridine synthase. Mol. Cell 34, 427-439 (2009).
94. Grummt, I. Wisely chosen paths: regulation of rRNA synthesis. FEBS J. 277, 4626-4639 (2010).