small nucleolar rna


Summary: Small nuclear RNAs that are involved in the processing of pre-ribosomal RNA in the nucleolus. Box C/D containing snoRNAs (U14, U15, U16, U20, U21 and U24-U63) direct site-specific methylation of various ribose moieties. Box H/ACA containing snoRNAs (E2, E3, U19, U23, and U64-U72) direct the conversion of specific uridines to pseudouridine. Site-specific cleavages resulting in the mature ribosomal RNAs are directed by snoRNAs U3, U8, U14, U22 and the snoRNA components of RNase MRP and RNase P.

Top Publications

  1. Allmang C, Kufel J, Chanfreau G, Mitchell P, Petfalski E, Tollervey D. Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J. 1999;18:5399-410 pubmed
    ..We conclude that the exosome is involved in the processing of many RNA substrates and that different components can have distinct functions. ..
  2. Xie J, Zhang M, Zhou T, Hua X, Tang L, Wu W. Sno/scaRNAbase: a curated database for small nucleolar RNAs and cajal body-specific RNAs. Nucleic Acids Res. 2007;35:D183-7 pubmed
    ..Thus our sno/scaRNAbase serves as a more uniform and friendly platform for sno/scaRNA research. The database is free available at ..
  3. Hardin J, Batey R. The bipartite architecture of the sRNA in an archaeal box C/D complex is a primary determinant of specificity. Nucleic Acids Res. 2006;34:5039-51 pubmed
  4. Ding F, Li H, Zhang S, Solomon N, Camper S, Cohen P, et al. SnoRNA Snord116 (Pwcr1/MBII-85) deletion causes growth deficiency and hyperphagia in mice. PLoS ONE. 2008;3:e1709 pubmed publisher
    ..2. Our previous translocation studies predicted a major role for the C/D box small nucleolar RNA cluster SNORD116 (PWCR1/HBII-85) in PWS...
  5. Ballarino M, Morlando M, Pagano F, Fatica A, Bozzoni I. The cotranscriptional assembly of snoRNPs controls the biosynthesis of H/ACA snoRNAs in Saccharomyces cerevisiae. Mol Cell Biol. 2005;25:5396-403 pubmed
    ..connection between phospho-CTD, generated by the Ctk1p kinase, and protein factors having a function in small nucleolar RNA (snoRNA) biogenesis...
  6. Liang X, Uliel S, Hury A, Barth S, Doniger T, Unger R, et al. A genome-wide analysis of C/D and H/ACA-like small nucleolar RNAs in Trypanosoma brucei reveals a trypanosome-specific pattern of rRNA modification. RNA. 2005;11:619-45 pubmed
    ..The large repertoire of modifications and guide RNAs in trypanosomes suggests that these modifications possibly play a central role in these parasites. ..
  7. Jady B, Bertrand E, Kiss T. Human telomerase RNA and box H/ACA scaRNAs share a common Cajal body-specific localization signal. J Cell Biol. 2004;164:647-52 pubmed
    ..CBs may function in post-transcriptional maturation (e.g., cap hypermethylation of hTR), but they may also play a role in the assembly and/or function of telomerase holoenzyme. ..
  8. Michienzi A, Li S, Zaia J, Rossi J. A nucleolar TAR decoy inhibitor of HIV-1 replication. Proc Natl Acad Sci U S A. 2002;99:14047-52 pubmed
    ..Based on the known nucleolar localization properties of Tat, we constructed a chimeric small nucleolar RNA-TAR decoy that localizes to the nucleoli of human cells and colocalizes in the nucleolus with a Tat-..
  9. Terns M, Terns R. Small nucleolar RNAs: versatile trans-acting molecules of ancient evolutionary origin. Gene Expr. 2002;10:17-39 pubmed
    ..The unique properties of snoRNAs are now being harnessed for basic research and therapeutic applications. ..

More Information


  1. Qu L, Meng Q, Zhou H, Chen Y, Liang Hu Q, Qing M, et al. Identification of 10 novel snoRNA gene clusters from Arabidopsis thaliana. Nucleic Acids Res. 2001;29:1623-30 pubmed
    Ten novel small nucleolar RNA (snoRNA) gene clusters, consisting of two or three snoRNA genes, respectively, were identified from Arabidopsis thaliana...
  2. Lukowiak A, Granneman S, Mattox S, Speckmann W, Jones K, Pluk H, et al. Interaction of the U3-55k protein with U3 snoRNA is mediated by the box B/C motif of U3 and the WD repeats of U3-55k. Nucleic Acids Res. 2000;28:3462-71 pubmed
    U3 small nucleolar RNA (snoRNA) is a member of the Box C/D family of snoRNAs which functions in ribosomal RNA processing. U3-55k is a protein that has been found to interact with U3 but not other members of the Box C/D snoRNA family...
  3. Barneche F, Gaspin C, Guyot R, Echeverria M. Identification of 66 box C/D snoRNAs in Arabidopsis thaliana: extensive gene duplications generated multiple isoforms predicting new ribosomal RNA 2'-O-methylation sites. J Mol Biol. 2001;311:57-73 pubmed
    ..The discovery of numerous different snoRNAs, some of them arising from common ancestors, provide new insights to understand snoRNAs evolution and the birth of new rRNA methylation sites in plants and other organisms. ..
  4. Greenwood S, Schnare M, Cook J, Gray M. Analysis of intergenic spacer transcripts suggests 'read-around' transcription of the extrachromosomal circular rDNA in Euglena gracilis. Nucleic Acids Res. 2001;29:2191-8 pubmed imperfect palindrome near site A0 and a sequence near site A' that could potentially base pair with U3 small nucleolar RNA. Our identification of the TIS (verified by mung bean nuclease analysis) is considered tentative because we ..
  5. He H, Cai L, Skogerbø G, Deng W, Liu T, Zhu X, et al. Profiling Caenorhabditis elegans non-coding RNA expression with a combined microarray. Nucleic Acids Res. 2006;34:2976-83 pubmed
    ..Taken together, our microarray analysis presents a more complete and detailed picture of a non-coding transcriptome than hitherto has been presented for any other multicellular organism. ..
  6. Dichtl B, Aasland R, Keller W. Functions for S. cerevisiae Swd2p in 3' end formation of specific mRNAs and snoRNAs and global histone 3 lysine 4 methylation. RNA. 2004;10:965-77 pubmed
    ..We also provide evidence that the roles of Swd2p as component of CPF and SET1C are functionally independent. Taken together, our results establish a dual requirement for Swd2p in 3' end formation and histone tail modification. ..
  7. Thompson M, Haeusler R, Good P, Engelke D. Nucleolar clustering of dispersed tRNA genes. Science. 2003;302:1399-401 pubmed that tRNA genes, though dispersed in the linear genome, colocalize with 5S ribosomal DNA and U14 small nucleolar RNA at the nucleolus...
  8. Mitchell P, Petfalski E, Houalla R, Podtelejnikov A, Mann M, Tollervey D. Rrp47p is an exosome-associated protein required for the 3' processing of stable RNAs. Mol Cell Biol. 2003;23:6982-92 pubmed
    ..Northern analyses demonstrated that Rrp47p is required for the exosome-dependent processing of rRNA and small nucleolar RNA (snoRNA) precursors. Rrp47p also participates in the 3' processing of U4 and U5 small nuclear RNAs (snRNAs)...
  9. Hiley S, Babak T, Hughes T. Global analysis of yeast RNA processing identifies new targets of RNase III and uncovers a link between tRNA 5' end processing and tRNA splicing. Nucleic Acids Res. 2005;33:3048-56 pubmed
    ..This analysis demonstrates the applicability of microarray technology to the study of global analysis of ncRNA synthesis and provides an extensive directory of processing events mediated by yeast ncRNA processing enzymes. ..
  10. Chen C, Chen C, Vallon O, Huang Z, Zhou H, Qu L. Genomewide analysis of box C/D and box H/ACA snoRNAs in Chlamydomonas reinhardtii reveals an extensive organization into intronic gene clusters. Genetics. 2008;179:21-30 pubmed publisher
    ..Using the powerful small nucleolar RNA (snoRNA) mining platform to screen the C...
  11. Nabavi S, Nellimarla S, Nazar R. Post-transcriptional regulation of the U3 small nucleolar RNA. J Biol Chem. 2008;283:21404-10 pubmed publisher
    A high copy shuttle vector was used to express a "tagged" U3 small nucleolar RNA (snoRNA) gene in Schizosaccharomyces pombe to examine regulatory responses to a high gene dosage...
  12. Dragon F, Pogacic V, Filipowicz W. In vitro assembly of human H/ACA small nucleolar RNPs reveals unique features of U17 and telomerase RNAs. Mol Cell Biol. 2000;20:3037-48 pubmed
    ..Moreover, we show that in vitro-reconstituted RNPs contain hGAR1 and that binding of hGAR1 does not appear to be a prerequisite for the assembly of the other H/ACA proteins. ..
  13. Yang J, Zhang X, Huang Z, Zhou H, Huang M, Zhang S, et al. snoSeeker: an advanced computational package for screening of guide and orphan snoRNA genes in the human genome. Nucleic Acids Res. 2006;34:5112-23 pubmed
    ..The results of this study provide the most comprehensive listing of two families of snoRNA genes in the human genome till date. ..
  14. Aspegren A, Hinas A, Larsson P, Larsson A, Söderbom F. Novel non-coding RNAs in Dictyostelium discoideum and their expression during development. Nucleic Acids Res. 2004;32:4646-56 pubmed
    ..g. 18 small nucleolar RNA candidates (17 box C/D, of which a few are developmentally regulated, and one box H/ACA)...
  15. Zhou H, Chen Y, Du Y, Qu L. The Schizosaccharomyces pombe mgU6-47 gene is required for 2'-O-methylation of U6 snRNA at A41. Nucleic Acids Res. 2002;30:894-902 pubmed
    ..The timing of S.pombe U6 pre-RNA transport in the nucleus for splicing and methylation was also analyzed and is described. ..
  16. Lestrade L, Weber M. snoRNA-LBME-db, a comprehensive database of human H/ACA and C/D box snoRNAs. Nucleic Acids Res. 2006;34:D158-62 pubmed
    ..The database is available online at It can also be accessed from the human UCSC Genome Browser via the sno/miRNA track. ..
  17. Hoang T, Peng W, Vanrobays E, Krogan N, Hiley S, Beyer A, et al. Esf2p, a U3-associated factor required for small-subunit processome assembly and compaction. Mol Cell Biol. 2005;25:5523-34 pubmed
    ..The identification of ABT1 in a large-scale analysis of the human nucleolar proteome indicates that its role may also be conserved in mammals. ..
  18. Meier U. The many facets of H/ACA ribonucleoproteins. Chromosoma. 2005;114:1-14 pubmed
    ..The multiple functions of H/ACA RNPs appear to be reflected in the complex phenotype of dyskeratosis congenita. ..
  19. Weischenfeldt J, Lykke Andersen J, Porse B. Messenger RNA surveillance: neutralizing natural nonsense. Curr Biol. 2005;15:R559-62 pubmed
  20. Bernstein K, Baserga S. The small subunit processome is required for cell cycle progression at G1. Mol Biol Cell. 2004;15:5038-46 pubmed
    ..results indicate that the small subunit (SSU) processome, a complex consisting of 40 proteins and the U3 small nucleolar RNA necessary for ribosome biogenesis, is not mitotically regulated...
  21. Clery A, Senty Ségault V, Leclerc F, Raué H, Branlant C. Analysis of sequence and structural features that identify the B/C motif of U3 small nucleolar RNA as the recognition site for the Snu13p-Rrp9p protein pair. Mol Cell Biol. 2007;27:1191-206 pubmed
    ..They bring important information to understand how different K-turn motifs can recruit different sets of proteins after Snu13p association. ..
  22. Luo Y, Li S. Genome-wide analyses of retrogenes derived from the human box H/ACA snoRNAs. Nucleic Acids Res. 2007;35:559-71 pubmed
  23. Kuhn J, Tran E, Maxwell E. Archaeal ribosomal protein L7 is a functional homolog of the eukaryotic 15.5kD/Snu13p snoRNP core protein. Nucleic Acids Res. 2002;30:931-41 pubmed
    ..L7 functioning as both an sRNP core protein and a ribosomal protein could potentially regulate and coordinate sRNP assembly with ribosome biogenesis...
  24. Cavaille J, Seitz H, Paulsen M, Ferguson Smith A, Bachellerie J. Identification of tandemly-repeated C/D snoRNA genes at the imprinted human 14q32 domain reminiscent of those at the Prader-Willi/Angelman syndrome region. Hum Mol Genet. 2002;11:1527-38 pubmed
    ..shown that another imprinted locus, on human 15q11-q13, contains a large number of tandemly repeated C/D small nucleolar RNA genes (or C/D snoRNAs) only expressed from the paternal allele...
  25. Wachi M, Ogawa T, Yokoyama K, Hokii Y, Shimoyama M, Muto A, et al. Isolation of eight novel Caenorhabditis elegans small RNAs. Gene. 2004;335:47-56 pubmed
    ..The results of our study suggest that there are more as-yet-unidentified small ncRNAs of which genes are located in the intron regions of protein-coding genes in C. elegans. ..
  26. Liang X, Ochaion A, Xu Y, Liu Q, Michaeli S. Small nucleolar RNA clusters in trypanosomatid Leptomonas collosoma. Genome organization, expression studies, and the potential role of sequences present upstream from the first repeated cluster. J Biol Chem. 2004;279:5100-9 pubmed
    Trypanosomatid small nucleolar RNA (snoRNA) genes are clustered in the genome. snoRNAs are transcribed polycistronically and processed into mature RNAs. In this study, we characterized four snoRNA clusters in Leptomonas collosoma...
  27. Nedea E, Nalbant D, Xia D, Theoharis N, Suter B, Richardson C, et al. The Glc7 phosphatase subunit of the cleavage and polyadenylation factor is essential for transcription termination on snoRNA genes. Mol Cell. 2008;29:577-87 pubmed publisher
    ..Swd2 is also a subunit of the Set1c histone H3K4 methyltransferase complex and is required for its stability and optimal methyltransferase activity. ..
  28. Lukowiak A, Narayanan A, Li Z, Terns R, Terns M. The snoRNA domain of vertebrate telomerase RNA functions to localize the RNA within the nucleus. RNA. 2001;7:1833-44 pubmed
    ..Our results identify the Cajal body as a potential site of telomerase RNP biogenesis. ..
  29. Runte M, Varon R, Horn D, Horsthemke B, Buiting K. Exclusion of the C/D box snoRNA gene cluster HBII-52 from a major role in Prader-Willi syndrome. Hum Genet. 2005;116:228-30 pubmed
    ..However, we cannot exclude the possibility that the loss of HBII-52 has a phenotypic effect when accompanied by the loss of function of other genes in 15q11-q13. ..
  30. Bazeley P, Shepelev V, Talebizadeh Z, Butler M, Fedorova L, Filatov V, et al. snoTARGET shows that human orphan snoRNA targets locate close to alternative splice junctions. Gene. 2008;408:172-9 pubmed
    ..The snoTARGET resource is freely available at: ( ..
  31. Tremblay A, Lamontagne B, Catala M, Yam Y, Larose S, Good L, et al. A physical interaction between Gar1p and Rnt1pi is required for the nuclear import of H/ACA small nucleolar RNA-associated proteins. Mol Cell Biol. 2002;22:4792-802 pubmed
    ..These results demonstrate colocalization of various components of the rRNA maturation complex and suggest a mechanism that links rRNA pseudouridylation and cleavage factors. ..
  32. Hirose T, Ideue T, Nagai M, Hagiwara M, Shu M, Steitz J. A spliceosomal intron binding protein, IBP160, links position-dependent assembly of intron-encoded box C/D snoRNP to pre-mRNA splicing. Mol Cell. 2006;23:673-84 pubmed
    ..IBP160 binding directly to a snoRNA located too close to the intron branch site interferes with snoRNP assembly. Thus, IBP160 is the key factor linking snoRNP biogenesis and perhaps other postsplicing events to pre-mRNA splicing. ..
  33. Normand C, Capeyrou R, Quevillon Cheruel S, Mougin A, Henry Y, Caizergues Ferrer M. Analysis of the binding of the N-terminal conserved domain of yeast Cbf5p to a box H/ACA snoRNA. RNA. 2006;12:1868-82 pubmed
  34. Royo H, Cavaille J. Non-coding RNAs in imprinted gene clusters. Biol Cell. 2008;100:149-66 pubmed publisher
  35. Bonnerot C, Pintard L, Lutfalla G. Functional redundancy of Spb1p and a snR52-dependent mechanism for the 2'-O-ribose methylation of a conserved rRNA position in yeast. Mol Cell. 2003;12:1309-15 pubmed
    ..In vitro, Spb1p is able to methylate U2918 on 60S subunits. Our results reveal the importance of this methylation for which two mechanisms coexist: a site-specific methyltransferase (Spb1p) and a snoRNA-dependent mechanism. ..
  36. Vasiljeva L, Kim M, Mutschler H, Buratowski S, Meinhart A. The Nrd1-Nab3-Sen1 termination complex interacts with the Ser5-phosphorylated RNA polymerase II C-terminal domain. Nat Struct Mol Biol. 2008;15:795-804 pubmed publisher
    ..Nrd1 recruitment to genes involves a combination of interactions with CTD and Nab3. ..
  37. Schule B, Albalwi M, Northrop E, Francis D, Rowell M, Slater H, et al. Molecular breakpoint cloning and gene expression studies of a novel translocation t(4;15)(q27;q11.2) associated with Prader-Willi syndrome. BMC Med Genet. 2005;6:18 pubmed
    ..As part of the PWCR1/HBII-85 snoRNA cluster is highly conserved between human and mice, while no copy of HBII-438 has been found in mouse, we conclude that PWCR1/HBII-85 snoRNAs is likely to play a major role in the PWS- phenotype. ..
  38. Watkins N, Ségault V, Charpentier B, Nottrott S, Fabrizio P, Bachi A, et al. A common core RNP structure shared between the small nucleoar box C/D RNPs and the spliceosomal U4 snRNP. Cell. 2000;103:457-66 pubmed
    ..5 kD in vitro. The similarities in structure and function observed between the U4 snRNP (chaperone for U6) and the box C/D snoRNPs raises the interesting possibility that these particles may have evolved from a common ancestral RNP. ..
  39. Hirose T, Steitz J. Position within the host intron is critical for efficient processing of box C/D snoRNAs in mammalian cells. Proc Natl Acad Sci U S A. 2001;98:12914-9 pubmed
  40. Sahoo T, del Gaudio D, German J, Shinawi M, Peters S, Person R, et al. Prader-Willi phenotype caused by paternal deficiency for the HBII-85 C/D box small nucleolar RNA cluster. Nat Genet. 2008;40:719-21 pubmed publisher
  41. Decatur W, Schnare M. Different mechanisms for pseudouridine formation in yeast 5S and 5.8S rRNAs. Mol Cell Biol. 2008;28:3089-100 pubmed publisher
    ..8S rRNA pseudouridylation, as well as the multiple specificities of the individual trans factors concerned, suggest possible roles in linking ribosome production to other processes, such as splicing and tRNA synthesis. ..
  42. Hertel J, de Jong D, Marz M, Rose D, Tafer H, Tanzer A, et al. Non-coding RNA annotation of the genome of Trichoplax adhaerens. Nucleic Acids Res. 2009;37:1602-15 pubmed publisher
    ..We did not find any microRNA candidates homologous to known eumetazoan sequences. Interestingly, most ncRNAs, including the pol-III transcripts, appear as single-copy genes or with very small copy numbers in the Trichoplax genome. ..
  43. Decatur W, Liang X, Piekna Przybylska D, Fournier M. Identifying effects of snoRNA-guided modifications on the synthesis and function of the yeast ribosome. Methods Enzymol. 2007;425:283-316 pubmed
    ..Methods are also included for characterizing modification effects on cell growth, antibiotic sensitivity, rRNA processing, formation of various rRNP complexes, translation activity, and rRNA structure within the ribosome. ..
  44. Kishore S, Stamm S. The snoRNA HBII-52 regulates alternative splicing of the serotonin receptor 2C. Science. 2006;311:230-2 pubmed
    ..This region contains a small nucleolar RNA (snoRNA), HBII-52, that exhibits sequence complementarity to the alternatively spliced exon Vb of the ..
  45. Eo H, Jo K, Lee S, Kim C, Kim W. A combined approach for locating box H/ACA snoRNAs in the human genome. Mol Cells. 2005;20:35-42 pubmed
    ..With our novel method 12 known box H/ACA snoRNAs, and one strong candidate were identified in 30 nucleolar protein genomic sequences. ..
  46. Landers M, Bancescu D, Le Meur E, Rougeulle C, Glatt Deeley H, Brannan C, et al. Regulation of the large (approximately 1000 kb) imprinted murine Ube3a antisense transcript by alternative exons upstream of Snurf/Snrpn. Nucleic Acids Res. 2004;32:3480-92 pubmed
  47. Badis G, Fromont Racine M, Jacquier A. A snoRNA that guides the two most conserved pseudouridine modifications within rRNA confers a growth advantage in yeast. RNA. 2003;9:771-9 pubmed
    ..We show here that, in yeast, the presence of this snoRNA, and hence, most likely, of the conserved pseudouridines it specifies, is not essential for viability but provides a growth advantage to the cell. ..
  48. Fu D, Collins K. Distinct biogenesis pathways for human telomerase RNA and H/ACA small nucleolar RNAs. Mol Cell. 2003;11:1361-72 pubmed
    ..the human telomerase RNA (hTR) suggested that telomerase might utilize the biogenesis pathway of an H/ACA small nucleolar RNA. Here, we have investigated the requirements for processing, stability, and function of hTR...
  49. Pogacic V, Dragon F, Filipowicz W. Human H/ACA small nucleolar RNPs and telomerase share evolutionarily conserved proteins NHP2 and NOP10. Mol Cell Biol. 2000;20:9028-40 pubmed
  50. van Hoof A, Lennertz P, Parker R. Yeast exosome mutants accumulate 3'-extended polyadenylated forms of U4 small nuclear RNA and small nucleolar RNAs. Mol Cell Biol. 2000;20:441-52 pubmed
    ..This finding suggests that the cytoplasmic and nuclear forms of the exosome represent two functionally different complexes involved in distinct 3'-to-5' processing and degradation reactions. ..
  51. Lykke Andersen S, Jensen T. CUT it out: silencing of noise in the transcriptome. Nat Struct Mol Biol. 2006;13:860-1 pubmed
  52. Mouaikel J, Bujnicki J, Tazi J, Bordonné R. Sequence-structure-function relationships of Tgs1, the yeast snRNA/snoRNA cap hypermethylase. Nucleic Acids Res. 2003;31:4899-909 pubmed
    ..Site- directed mutagenesis of Tgs1 allowed also the identification of the residues likely to be involved in the formation of the m7G-binding site and the catalytic center. ..
  53. Fatica A, Dlakic M, Tollervey D. Naf1 p is a box H/ACA snoRNP assembly factor. RNA. 2002;8:1502-14 pubmed
    ..We propose that Naf1 p is recruited to the CTD of RNA polymerase II and binds to nascent box H/ACA snoRNAs promoting snoRNP assembly. ..