Biology and applications of small nucleolar RNAs

Cellular and Molecular Life Sciences

Volumn 68, Issue 23, 2011, Pages 3843-3851

  Bratkovič, Tomaž ^a   Rogelj, Boris ^b  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Alternative splicing; Biogenesis; Gene silencing; RNA editing; Small nucleolar RNAs

Indexed keywords

RIBOSOME RNA; RNA POLYMERASE II; SEROTONIN 2C RECEPTOR; SEROTONIN UPTAKE INHIBITOR; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA; SMALL NUCLEOLAR RNA; SNORD115 PROTEIN; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; BIOGENESIS; GENE EXPRESSION REGULATION; HUMAN; HUMAN GENOME; ISOMERIZATION; LEARNING; MEMORY CONSOLIDATION; NONHUMAN; NUCLEIC ACID PROBE; NUCLEOTIDE SEQUENCE; PRADER WILLI SYNDROME; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PSEUDORIDYLATION; REVIEW; RIBOSOME; RNA CLEAVAGE; RNA EDITING; RNA GENE; RNA METHYLATION; RNA PROCESSING; RNA SEQUENCE; SEROTONIN METABOLISM;

ANIMALS; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; HUMANS; RNA, MESSENGER; RNA, SMALL NUCLEOLAR;

EID: 82255175105     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-011-0762-y     Document Type: Review

References (76)

1. Kishore S, Stamm S (2006) The snoRNA HBII-52 regulates alternative splicing of the serotonin receptor 2C. Science 311:230-232 (Pubitemid 43108188)
2. Kishore S, Khanna A, Zhang Z, Hui J, Balwierz PJ, Stefan M, Beach C, Nicholls RD, Zavolan M, Stamm S (2010) The snoRNA MBII-52 (SNORD 115) is processed into smaller RNAs and regulates alternative splicing. Hum Mol Genet 19:1153-1164
3. Vitali P, Basyuk E, Le Meur E, Bertrand E, Muscatelli F, Cavaille J, Huttenhofer A (2005) ADAR2-mediated editing of RNA substrates in the nucleolus is inhibited by C/D small nucleolar RNAs. J Cell Biol 169:745-753 (Pubitemid 41002880)
4. Yang JH, Zhang XC, Huang ZP, Zhou H, Huang MB, Zhang S, Chen YQ, Qu LH (2006) snoSeeker: an advanced computational package for screening of guide and orphan snoRNA genes in the human genome. Nucleic Acids Res 34:5112-5123 (Pubitemid 44742476)
5. Omer AD, Lowe TM, Russell AG, Ebhardt H, Eddy SR, Dennis PP (2000) Homologs of small nucleolar RNAs in Archaea. Science 288:517-522 (Pubitemid 30236034)
6. Gaspin C, Cavaille J, Erauso G, Bachellerie JP (2000) Archaeal homologs of eukaryotic methylation guide small nucleolar RNAs: lessons from the Pyrococcus genomes. J Mol Biol 297:895-906
7. Dieci G, Preti M, Montanini B (2009) Eukaryotic snoRNAs: a paradigm for gene expression flexibility. Genomics 94:83-88
8. Tycowski KT, Steitz JA (2001) Non-coding snoRNA host genes in Drosophila: expression strategies for modification guide snoRNAs. Eur J Cell Biol 80:119-125 (Pubitemid 32175497)
9. Richard P, Darzacq X, Bertrand E, Jady BE, Verheggen C, Kiss T (2003) A common sequence motif determines the Cajal bodyspecific localization of box H/ACA scaRNAs. EMBO J 22:4283-4293 (Pubitemid 37021755)
10. Reichow SL, Hamma T, Ferre-D'Amare AR, Varani G (2007) The structure and function of small nucleolar ribonucleoproteins. Nucleic Acids Res 35:1452-1464 (Pubitemid 46592868)
11. Boulon S, Verheggen C, Jady BE, Girard C, Pescia C, Paul C, Ospina JK, Kiss T, Matera AG, Bordonne R, Bertrand E (2004) PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol Cell 16:777-787 (Pubitemid 39586535)
12. Pradet-Balade B, Girard C, Boulon S, Paul C, Azzag K, Bordonne R, Bertrand E, Verheggen C (2011) CRM1 controls the composition of nucleoplasmic pre-snoRNA complexes to licence them for nucleolar transport. EMBO J 30:2205-2218
13. Gonzales FA, Zanchin NI, Luz JS, Oliveira CC (2005) Characterization of Saccharomyces cerevisiae Nop17p, a novel Nop58pinteracting protein that is involved in Pre-rRNA processing. J Mol Biol 346:437-455
14. McKeegan KS, Debieux CM, Boulon S, Bertrand E, Watkins NJ (2007) A dynamic scaffold of pre-snoRNP factors facilitates human box C/D snoRNP assembly. Mol Cell Biol 27:6782-6793 (Pubitemid 47483629)
15. Boulon S, Marmier-Gourrier N, Pradet-Balade B, Wurth L, Verheggen C, Jady BE, Rothe B, Pescia C, Robert MC, Kiss T, Bardoni B, Krol A, Branlant C, Allmang C, Bertrand E, Charpentier B (2008) The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J Cell Biol 180:579-595 (Pubitemid 351240705)
16. Darzacq X, Kittur N, Roy S, Shav-Tal Y, Singer RH, Meier UT (2006) Stepwise RNP assembly at the site of H/ACA RNA transcription in human cells. J Cell Biol 173:207-218
17. Godin KS, Walbott H, Leulliot N, van Tilbeurgh H, Varani G (2009) The box H/ACA snoRNP assembly factor Shq1p is a chaperone protein homologous to Hsp90 cochaperones that binds to the Cbf5p enzyme. J Mol Biol 390:231-244
18. Yang PK, Rotondo G, Porras T, Legrain P, Chanfreau G (2002) The Shq1p. Naf1p complex is required for box H/ACA small nucleolar ribonucleoprotein particle biogenesis. J Biol Chem 277:45235-45242 (Pubitemid 36159128)
19. McKeegan KS, Debieux CM, Watkins NJ (2009) Evidence that the AAA + proteins TIP48 and TIP49 bridge interactions between 15.5 K and the related NOP56 and NOP58 proteins during box C/D snoRNP biogenesis. Mol Cell Biol 29:4971-4981
20. Huen J, Kakihara Y, Ugwu F, Cheung KL, Ortega J, Houry WA (2010) Rvb1-Rvb2: essential ATP-dependent helicases for critical complexes. Biochem Cell Biol 88:29-40
21. Zhao R, Kakihara Y, Gribun A, Huen J, Yang G, Khanna M, Costanzo M, Brost RL, Boone C, Hughes TR, Yip CM, Houry WA (2008) Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation. J Cell Biol 180:563-578 (Pubitemid 351240704)
22. Watkins NJ, Lemm I, Ingelfinger D, Schneider C, Hossbach M, Urlaub H, Luhrmann R (2004) Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex. Mol Cell 16:789-798 (Pubitemid 39586536)
23. Grozdanov PN, Roy S, Kittur N, Meier UT (2009) SHQ1 is required prior to NAF1 for assembly of H/ACA small nucleolar and telomerase RNPs. RNA 15:1188-1197
24. Kiss T, Fayet-Lebaron E, Jady BE (2010) Box H/ACA small ribonucleoproteins. Mol Cell 37:597-606
25. Fatica A, Dlakic M, Tollervey D (2002) Naf1 p is a box H/ACA snoRNP assembly factor. RNA 8:1502-1514 (Pubitemid 36009021)
26. Matera AG, Terns RM, Terns MP (2007) Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs. Nat Rev Mol Cell Biol 8:209-220
27. Bertrand E, Fournier MJ (2004) The snoRNPs and related machines: ancient devices that mediate maturation of rRNA and other RNAs. In: Olson MOJ (ed) The nucleolus. Kluwer, New York, pp 225-261
28. Stanek D, Neugebauer KM (2006) The Cajal body: a meeting place for spliceosomal snRNPs in the nuclear maze. Chromosoma 115:343-354 (Pubitemid 44288793)
29. Lestrade L, Weber MJ (2006) snoRNA-LBME-db, a comprehensive database of human H/ACA and C/D box snoRNAs. Nucleic Acids Res 34:D158-D162
30. Fedorov A, Stombaugh J, Harr MW, Yu S, Nasalean L, Shepelev V (2005) Computer identification of snoRNA genes using a Mammalian Orthologous Intron Database. Nucleic Acids Res 33:4578-4583 (Pubitemid 41222572)
31. Washietl S, Hofacker IL, Lukasser M, Huttenhofer A, Stadler PF (2005) Mapping of conserved RNA secondary structures predicts thousands of functional noncoding RNAs in the human genome. Nat Biotechnol 23:1383-1390 (Pubitemid 41679390)
32. Rearick D, Prakash A, McSweeny A, Shepard SS, Fedorova L, Fedorov A (2010) Critical association of ncRNA with introns. Nucleic Acids Res 39:2357-2366
33. van Nues RW, Granneman S, Kudla G, Sloan KE, Chicken M, Tollervey D, Watkins NJ (2011) Box C/D snoRNP catalysed methylation is aided by additional pre-rRNA base-pairing. EMBO J 30:2420-2430
34. Kiss-Laszlo Z, Henry Y, Kiss T (1998) Sequence and structural elements of methylation guide snoRNAs essential for site-specific ribose methylation of pre-rRNA. EMBO J 17:797-807 (Pubitemid 28062058)
35. Jady BE, Kiss T (2001) A small nucleolar guide RNA functions both in 2'-O-ribose methylation and pseudouridylation of the U5 spliceosomal RNA. EMBO J 20:541-551 (Pubitemid 32126989)
36. Kass S, Tyc K, Steitz JA, Sollner-Webb B (1990) The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell 60:897-908
37. Hughes JM, Ares M Jr (1991) Depletion of U3 small nucleolar RNA inhibits cleavage in the 50 external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA. EMBO J 10:4231-4239 (Pubitemid 21905455)
38. Peculis BA, Steitz JA (1993) Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell 73:1233-1245 (Pubitemid 23180496)
39. Liang WQ, Fournier MJ (1995) U14 base-pairs with 18S rRNA: a novel snoRNA interaction required for rRNA processing. Genes Dev 9:2433-2443
40. Tycowski KT, Shu MD, Steitz JA (1994) Requirement for intronencoded U22 small nucleolar RNA in 18S ribosomal RNA maturation. Science 266:1558-1561
41. Kiss T, Marshallsay C, Filipowicz W (1992) 7-2/MRP RNAs in plant and mammalian cells: association with higher order structures in the nucleolus. EMBO J 11:3737-3746
42. Davila Lopez M, Rosenblad MA, Samuelsson T (2009) Conserved and variable domains of RNase MRP RNA. RNA Biol 6:208-220
43. Theimer CA, Feigon J (2006) Structure and function of telomerase RNA. Curr Opin Struct Biol 16:307-318 (Pubitemid 43831650)
44. Blackburn EH, Collins K (2011) Telomerase: an RNP enzyme synthesizes DNA. Cold Spring Harb Perspect Biol 3:a003558
45. Brimacombe R, Mitchell P, Osswald M, Stade K, Bochkariov D (1993) Clustering of modified nucleotides at the functional center of bacterial ribosomal RNA. FASEB J 7:161-167 (Pubitemid 23034028)
46. Ofengand J, Bakin A (1997) Mapping to nucleotide resolution of pseudouridine residues in large subunit ribosomal RNAs from representative eukaryotes, prokaryotes, archaebacteria, mitochondria and chloroplasts. J Mol Biol 266:246-268 (Pubitemid 27171012)
47. King TH, Liu B, McCully RR, Fournier MJ (2003) Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol Cell 11:425-435 (Pubitemid 36293836)
48. Terns MP, Terns RM (2002) Small nucleolar RNAs: versatile trans-acting molecules of ancient evolutionary origin. Gene Expr 10:17-39 (Pubitemid 34169340)
49. Ofengand J, Rudd KE (2000) Bacterial, archaeal and organellar rRNA pseudouridines and methylated nucleosides and their enzymes. In: Garrett RA, Douthwaite SR, Liljas A, Matheson AT, Moore PB, Noller HF (eds) The ribosome: structure, function, antibiotics, and cellular interactions. ASM Press, Washington, pp 175-189
50. Burns CM, Chu H, Rueter SM, Hutchinson LK, Canton H, Sanders-Bush E, Emeson RB (1997) Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 387:303-308 (Pubitemid 27220768)
51. Doe CM, Relkovic D, Garfield AS, Dalley JW, Theobald DE, Humby T, Wilkinson LS, Isles AR (2009) Loss of the imprinted snoRNA mbii-52 leads to increased 5htr2c pre-RNA editing and altered 5HT2CR-mediated behaviour. Hum Mol Genet 18:2140-2148
52. Duker AL, Ballif BC, Bawle EV, Person RE, Mahadevan S, Alliman S, Thompson R, Traylor R, Bejjani BA, Shaffer LG, Rosenfeld JA, Lamb AN, Sahoo T (2010) Paternally inherited microdeletion at 15q11.2 confirms a significant role for the SNORD116 C/D box snoRNA cluster in Prader-Willi syndrome. Eur J Hum Genet 18:1196-1201
53. Sahoo T, del Gaudio D, German JR, Shinawi M, Peters SU, Person RE, Garnica A, Cheung SW, Beaudet AL (2008) Prader-Willi phenotype caused by paternal deficiency for the HBII-85 C/D box small nucleolar RNA cluster. Nat Genet 40:719-721 (Pubitemid 351748873)
54. de Smith AJ, Purmann C, Walters RG, Ellis RJ, Holder SE, Van Haelst MM, Brady AF, Fairbrother UL, Dattani M, Keogh JM, Henning E, Yeo GS, O'Rahilly S, Froguel P, Farooqi IS, Blakemore AI (2009) A deletion of the HBII-85 class of small nucleolar RNAs (snoRNAs) is associated with hyperphagia, obesity and hypogonadism. Hum Mol Genet 18:3257-3265
55. Ding F, Li HH, Zhang S, Solomon NM, Camper SA, Cohen P, Francke U (2008) SnoRNA Snord116 (Pwcr1/MBII-85) deletion causes growth deficiency and hyperphagia in mice. PLoS One 3:e1709
56. Martinez-Contreras R, Cloutier P, Shkreta L, Fisette JF, Revil T, Chabot B (2007) hnRNP proteins and splicing control. Adv Exp Med Biol 623:123-147
57. Ono M, Yamada K, Avolio F, Scott MS, van Koningsbruggen S, Barton GJ, Lamond AI (2010) Analysis of human small nucleolar RNAs (snoRNA) and the development of snoRNA modulator of gene expression vectors. Mol Biol Cell 21:1569-1584
58. Ono M, Scott MS, Yamada K, Avolio F, Barton GJ, Lamond AI (2011) Identification of human miRNA precursors that resemble box C/D snoRNAs. Nucleic Acids Res 39:3879-3891
59. Ender C, Krek A, Friedlander MR, Beitzinger M, Weinmann L, Chen W, Pfeffer S, Rajewsky N, Meister G (2008) A human snoRNA with microRNA-like functions. Mol Cell 32:519-528
60. Saraiya AA, Wang CC (2008) snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 4:e1000224
61. Taft RJ, Glazov EA, Lassmann T, Hayashizaki Y, Carninci P, Mattick JS (2009) Small RNAs derived from snoRNAs. RNA 15:1233-1240
62. Scott MS, Avolio F, Ono M, Lamond AI, Barton GJ (2009) Human miRNA precursors with box H/ACA snoRNA features. PLoS Comput Biol 5:e1000507
63. Politz JC, Hogan EM, Pederson T (2009) MicroRNAs with a nucleolar location. RNA 15:1705-1715
64. Brameier M, Herwig A, Reinhardt R, Walter L, Gruber J (2011) Human box C/D snoRNAs with miRNA like functions: expanding the range of regulatory RNAs. Nucleic Acids Res 39:675-686
65. Weber MJ (2006) Mammalian small nucleolar RNAs are mobile genetic elements. PLoS Genet 2:e205
66. Burroughs AM, Ando Y, de Hoon ML, Tomaru Y, Suzuki H, Hayashizaki Y, Daub CO (2011) Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin. RNA Biol 8:158-177
67. Rogelj B (2006) Brain-specific small nucleolar RNAs. J Mol Neurosci 28:103-109
68. Rogelj B, Hartmann CE, Yeo CH, Hunt SP, Giese KP (2003) Contextual fear conditioning regulates the expression of brainspecific small nucleolar RNAs in hippocampus. Eur J Neurosci 18:3089-3096 (Pubitemid 38021550)
69. Cavaille J, Nicoloso M, Bachellerie JP (1996) Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides. Nature 383:732-735 (Pubitemid 26360652)
70. Bortolin ML, Ganot P, Kiss T (1999) Elements essential for accumulation and function of small nucleolar RNAs directing site-specific pseudouridylation of ribosomal RNAs. EMBO J 18:457-469 (Pubitemid 29041953)
71. Ploner A, Ploner C, Lukasser M, Niederegger H, Huttenhofer A (2009) Methodological obstacles in knocking down small noncoding RNAs. RNA 15:1797-1804
72. Liang XH, Vickers TA, Guo S, Crooke ST (2011) Efficient and specific knockdown of small non-coding RNAs in mammalian cells and in mice. Nucleic Acids Res 39:e13
73. Bazeley PS, Shepelev V, Talebizadeh Z, Butler MG, Fedorova L, Filatov V, Fedorov A (2008) snoTARGET shows that human orphan snoRNA targets locate close to alternative splice junctions. Gene 408:172-179
74. Kehr S, Bartschat S, Stadler PF, Tafer H (2011) PLEXY: efficient target prediction for Box C/D snoRNAs. Bioinformatics 27:279-280
75. Tafer H, Kehr S, Hertel J, Hofacker IL, Stadler PF (2010) RNAsnoop: efficient target prediction for H/ACA snoRNAs. Bioinformatics 26:610-616
76. Hertel J, Hofacker IL, Stadler PF (2008) SnoReport: computational identification of snoRNAs with unknown targets. Bioinformatics 24:158-164