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Cited by 257RNA modifications and cancerRNA and protein synthesis mechanismsRNA regulation and disease

An updated human snoRNAome

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Jorjani, Hadi, Kehr, Stephanie, Jedlinski, Dominik J., Gumienny, Rafal, Hertel, Jana, Stadler, Peter F., Zavolan, Mihaela, Gruber, Andreas R.·2016·Nucleic Acids Research
DOI 10.1093/nar/gkw386PMC PMC4914119
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Abstract

Small nucleolar RNAs (snoRNAs) are a class of non-coding RNAs that guide the post-transcriptional processing of other non-coding RNAs (mostly ribosomal RNAs), but have also been implicated in processes ranging from microRNA-dependent gene silencing to alternative splicing. In order to construct an up-to-date catalog of human snoRNAs we have combined data from various databases, de novo prediction and extensive literature review. In total, we list more than 750 curated genomic loci that give rise to snoRNA and snoRNA-like genes. Utilizing small RNA-seq data from the ENCODE project, our study characterizes the plasticity of snoRNA expression identifying both constitutively as well as cell type specific expressed snoRNAs. Especially, the comparison of malignant to non-malignant tissues and cell types shows a dramatic perturbation of the snoRNA expression profile. Finally, we developed a high-throughput variant of the reverse-transcriptase-based method for identifying 2'-O-methyl modifications in RNAs termed RimSeq. Using the data from this and other high-throughput protocols together with previously reported modification sites and state-of-the-art target prediction methods we re-estimate the snoRNA target RNA interaction network. Our current results assign a reliable modification site to 83% of the canonical snoRNAs, leaving only 76 snoRNA sequences as orphan.

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  • All genes of the SNORD115 cluster are exclusively expressed in brain.

    “All genes of SNORD115 cluster, for example are exclusively expressed in brain (Chamberlain, 2013; Jorjani et al., 2016; Rogelj, 2006).”

    From Small nucleolar RNAs in plasma extracellular vesicles and their discriminatory power as diagnostic biomarkers of Alzheimer's disease (2021) · cites this paper as Jorjani et al., 2016

    In Results, “Expression profiling of human snoRNAs” (page unavailable), the paper calls the SNORD115 family neuron-specific, and Table 4 lists its expression as strongly biased toward neurons. It does not establish that every gene in the cluster is expressed exclusively in brain; the Methods describe averaging expression across snoRNAs grouped into families. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

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  1. [1]Marz M. Gruber A.R. Höner Zu Siederdissen C. Amman F. Badelt S. Bartschat S. Bernhart S.H. Beyer W. Kehr S. Lorenz R. Animal snoRNAs and scaRNAs with exceptional structures RNA Biol. 2011 8 938 946 21955586 PMC3256416
  2. [2]Decatur W.A. Fournier M.J. rRNA modifications and ribosome function Trends Biochem. Sci. 2002 27 344 351 12114023
  3. [3]Darzacq X. Jády B.E. Verheggen C. Kiss A.M. Bertrand E. Kiss T. Cajal body-specific small nuclear RNAs: a novel class of 2′-O-methylation and pseudouridylation guide RNAs EMBO J. 2002 21 2746 2756 12032087 PMC126017
  4. [4]d'Orval B.C. Bortolin M.-L. Gaspin C. Bachellerie J.-P. Box C/D RNA guides for the ribose methylation of archaeal tRNAs. The tRNATrp intron guides the formation of two ribose-methylated nucleosides in the mature tRNATrp Nucleic Acids Res. 2001 29 4518 4529 11713301 PMC92551
  5. [5]Kiss T. Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions Cell 2002 109 145 148 12007400
  6. [6]Matera A.G. Terns R.M. Terns M.P. Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs Nat. Rev. Mol. Cell Biol. 2007 8 209 220 17318225
  7. [7]Bratkovič T. Rogelj B. Biology and applications of small nucleolar RNAs Cell. Mol. Life Sci. 2011 68 3843 3851 21748470 PMC11114935
  8. [8]Tollervey D. Kiss T. Function and synthesis of small nucleolar RNAs Curr. Opin. Cell Biol. 1997 9 337 342 9159079
  9. [9]Darzacq X. Kiss T. Processing of intron-encoded box C/D small nucleolar RNAs lacking a 5′, 3′-terminal stem structure Mol. Cell. Biol. 2000 20 4522 4531 10848579 PMC85834
  10. [10]Kiss T. Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs EMBO J. 2001 20 3617 3622 11447102 PMC125535
  11. [11]McKeegan K.S. Debieux C.M. Boulon S. Bertrand E. Watkins N.J. A Dynamic Scaffold of Pre-snoRNP Factors Facilitates Human Box C/D snoRNP Assembly Mol. Cell. Biol. 2007 27 6782 6793 17636026 PMC2099223
  12. [12]Tollervey D. Lehtonen H. Jansen R. Kern H. Hurt E.C. Temperature-sensitive mutations demonstrate roles for yeast fibrillarin in pre-rRNA processing, pre-rRNA methylation, and ribosome assembly Cell 1993 72 443 457 8431947
  13. [13]Nicoloso M. Qu L.H. Michot B. Bachellerie J.P. Intron-encoded, antisense small nucleolar RNAs: the characterization of nine novel species points to their direct role as guides for the 2′-O-ribose methylation of rRNAs J. Mol. Biol. 1996 260 178 195 8764399
  14. [14]Kiss-László Z. Henry Y. Bachellerie J.P. Caizergues-Ferrer M. Kiss T. Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs Cell 1996 85 1077 1088 8674114
  15. [15]Cavaillé J. Nicoloso M. Bachellerie J.P. Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides Nature 1996 383 732 735 8878486
  16. [16]Balakin A.G. Smith L. Fournier M.J. The RNA world of the nucleolus: two major families of small RNAs defined by different box elements with related functions Cell 1996 86 823 834 8797828
  17. [17]Ganot P. Caizergues-Ferrer M. Kiss T. The family of box ACA small nucleolar RNAs is defined by an evolutionarily conserved secondary structure and ubiquitous sequence elements essential for RNA accumulation Genes Dev. 1997 11 941 956 9106664
  18. [18]Lafontaine D.L. Bousquet-Antonelli C. Henry Y. Caizergues-Ferrer M. Tollervey D. The box H+ ACA snoRNAs carry Cbf5p, the putative rRNA pseudouridine synthase Genes Dev 1998 12 527 537 9472021 PMC316522
  19. [19]Ganot P. Bortolin M.L. Kiss T. Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs Cell 1997 89 799 809 9182768
  20. [20]Bortolin M.L. Ganot P. Kiss T. Elements essential for accumulation and function of small nucleolar RNAs directing site-specific pseudouridylation of ribosomal RNAs EMBO J. 1999 18 457 469 9889201 PMC1171139
  21. [21]Richard P. Darzacq X. Bertrand E. Jády B.E. Verheggen C. Kiss T. A common sequence motif determines the Cajal body-specific localization of box H/ACA scaRNAs EMBO J. 2003 22 4283 4293 12912925 PMC175784
  22. [22]Marnef A. Richard P. Pinzón N. Kiss T. Targeting vertebrate intron-encoded box C/D 2′-O-methylation guide RNAs into the Cajal body Nucleic Acids Res. 2014 42 6616 6629 24753405 PMC4041459
  23. [24]Jády B.E. Ketele A. Kiss T. Human intron-encoded Alu RNAs are processed and packaged into Wdr79-associated nucleoplasmic box H/ACA RNPs Genes Dev. 2012 26 1897 1910 22892240 PMC3435494
  24. [25]Mitchell J.R. Cheng J. Collins K. A box H/ACA small nucleolar RNA-like domain at the human telomerase RNA 3′ end Mol. Cell. Biol. 1999 19 567 576 9858580 PMC83914
  25. [26]Zhang Q. Kim N.-K. Feigon J. Architecture of human telomerase RNA Proc. Natl. Acad. Sci. U.S.A. 2011 108 20325 20332 21844345 PMC3251123
  26. [27]Li Y. Podlevsky J.D. Marz M. Qi X. Hoffmann S. Stadler P.F. Chen J.J.-L. Identification of purple sea urchin telomerase RNA using a next-generation sequencing based approach RNA 2013 19 852 860 23584428 PMC3683918
  27. [28]Qi X. Li Y. Honda S. Hoffmann S. Marz M. Mosig A. Podlevsky J.D. Stadler P.F. Selker E.U. Chen J.J.-L. The common ancestral core of vertebrate and fungal telomerase RNAs Nucleic Acids Res 2013 41 450 462 23093598 PMC3592445
  28. [29]Ulyanov N.B. Shefer K. James T.L. Tzfati Y. Pseudoknot structures with conserved base triples in telomerase RNAs of ciliates Nucleic Acids Res. 2007 35 6150 6160 17827211 PMC2094054
  29. [30]Jády B.E. Bertrand E. Kiss T. Human telomerase RNA and box H/ACA scaRNAs share a common Cajal body–specific localization signal J. Cell Biol. 2004 164 647 652 14981093 PMC2172171
  30. [31]Bratkovič T. Rogelj B. The many faces of small nucleolar RNAs Biochim. Biophys. Acta 2014 1839 438 443 24735946
  31. [32]Lafontaine D.L. Tollervey D. Birth of the snoRNPs: the evolution of the modification-guide snoRNAs Trends Biochem. Sci. 1998 23 383 388 9810226
  32. [33]Kishore S. Gruber A.R. Jedlinski D.J. Syed A.P. Jorjani H. Zavolan M. Insights into snoRNA biogenesis and processing from PAR-CLIP of snoRNA core proteins and small RNA sequencing Genome Biol. 2013 14 R45 23706177 PMC4053766
  33. [34]Kishore S. Stamm S. The snoRNA HBII-52 regulates alternative splicing of the serotonin receptor 2C Science 2006 311 230 232 16357227
  34. [35]Doe C.M. Relkovic D. Garfield A.S. Dalley J.W. Theobald D.E.H. Humby T. Wilkinson L.S. Isles A.R. Loss of the imprinted snoRNA mbii-52 leads to increased 5htr2c pre-RNA editing and altered 5HT2CR-mediated behaviour Hum. Mol. Genet. 2009 18 2140 2148 19304781 PMC2685753
  35. [36]Yin Q.-F. Yang L. Zhang Y. Xiang J.-F. Wu Y.-W. Carmichael G.G. Chen L.-L. Long noncoding RNAs with snoRNA ends Mol. Cell 2012 48 219 30 22959273
  36. [37]Scott M.S. Ono M. Yamada K. Endo A. Barton G.J. Lamond A.I. Human box C/D snoRNA processing conservation across multiple cell types Nucleic Acids Res. 2012 40 3676 3688 22199253 PMC3333852
  37. [38]Ender C. Krek A. Friedländer M.R. Beitzinger M. Weinmann L. Chen W. Pfeffer S. Rajewsky N. Meister G. A human snoRNA with microRNA-like functions Mol. Cell 2008 32 519 528 19026782
  38. [39]Zhang X.-O. Yin Q.-F. Wang H.-B. Zhang Y. Chen T. Zheng P. Lu X. Chen L.-L. Yang L. Species-specific alternative splicing leads to unique expression of sno-lncRNAs BMC Genomics 2014 15 287 24734784 PMC4234469
  39. [40]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 D187 17099227 PMC1669756
  40. [41]Lestrade L. Weber M.J. snoRNA-LBME-db, a comprehensive database of human H/ACA and C/D box snoRNAs Nucleic Acids Res. 2006 34 D158 D162 16381836 PMC1347365
  41. [42]Ellis J.C. Brown D.D. Brown J.W. The small nucleolar ribonucleoprotein (snoRNP) database RNA 2010 16 664 666 20197376 PMC2844615
  42. [43]Zhang Y. Liu J. Jia C. Li T. Wu R. Wang J. Chen Y. Zou X. Chen R. Wang X.-J. Systematic identification and evolutionary features of rhesus monkey small nucleolar RNAs BMC Genomics 2010 11 61 20100322 PMC2832892
  43. [44]Liu T.-T. Zhu D. Chen W. Deng W. He H. He G. Bai B. Qi Y. Chen R. Deng X.W. A global identification and analysis of small nucleolar RNAs and possible intermediate-sized non-coding RNAs in Oryza sativa Mol. Plant 2013 6 830 846 22986792 PMC3716300
  44. [45]Gardner P.P. Bateman A. Poole A.M. SnoPatrol: how many snoRNA genes are there? J. Biol. 2010 9 4 20122292 PMC2871523
  45. [46]Kaur D. Gupta A.K. Kumari V. Sharma R. Bhattacharya A. Bhattacharya S. Computational prediction and validation of C/D, H/ACA and Eh_U3 snoRNAs of Entamoeba histolytica BMC Genomics 2012 13 390 22892049 PMC3542256
  46. [47]Makarova J.A. Kramerov D.A. SNOntology: Myriads of novel snoRNAs or just a mirage? BMC Genomics 2011 12 543 22047601 PMC3349704
  47. [49]Yang J.-H. Zhang X.-C. Huang Z.-P. Zhou H. Huang M.-B. Zhang S. Chen Y.-Q. Qu L.-H. snoSeeker: an advanced computational package for screening of guide and orphan snoRNA genes in the human genome Nucleic Acids Res. 2006 34 5112 5123 16990247 PMC1636440
  48. [50]Hertel J. Hofacker I.L. Stadler P.F. SnoReport: computational identification of snoRNAs with unknown targets Bioinformatics 2008 24 158 164 17895272
  49. [51]Marz M. Kirsten T. Stadler P.F. Evolution of spliceosomal snRNA genes in metazoan animals J. Mol. Evol. 2008 67 594 607 19030770
  50. [52]Maden T. Ribosomal RNA. Click here for methylation Nature 1996 383 675 676 8878473
  51. [53]Maden B.E. Identification of the locations of the methyl groups in 18 S ribosomal RNA from Xenopus laevis and man J. Mol. Biol. 1986 189 681 699 3783688
  52. [54]Ofengand J. Bakin A. Mapping to nucleotide resolution of pseudouridine residues in large subunit ribosomal RNAs from representative eukaryotes, prokaryotes, archaebacteria, mitochondria and chloroplasts J. Mol. Biol. 1997 266 246 268 9047361
  53. [55]Cantara W.A. Crain P.F. Rozenski J. McCloskey J.A. Harris K.A. Zhang X. Vendeix F.A.P. Fabris D. Agris P.F. The RNA Modification Database, RNAMDB: 2011 update Nucleic Acids Res. 2011 39 D195 D201 21071406 PMC3013656
  54. [56]McCloskey J.A. Rozenski J. The Small Subunit rRNA Modification Database Nucleic Acids Res. 2005 33 D135 D138 15608163 PMC539969
  55. [57]Dönmez G. Hartmuth K. Lührmann R. Modified nucleotides at the 5′ end of human U2 snRNA are required for spliceosomal E-complex formation RNA 2004 10 1925 1933 15525712 PMC1370681
  56. [58]Yu Y.T. Shu M.D. Steitz J.A. Modifications of U2 snRNA are required for snRNP assembly and pre-mRNA splicing EMBO J. 1998 17 5783 5795 9755178 PMC1170906
  57. [59]Carlile T.M. Rojas-Duran M.F. Zinshteyn B. Shin H. Bartoli K.M. Gilbert W.V. Pseudouridine profiling reveals regulated mRNA pseudouridylation in yeast and human cells Nature 2014 515 143 146 25192136 PMC4224642
  58. [60]Tafer H. Kehr S. Hertel J. Hofacker I.L. Stadler P.F. RNAsnoop: efficient target prediction for H/ACA snoRNAs Bioinformatics 2010 26 610 616 20015949
  59. [61]Kehr S. Bartschat S. Stadler P.F. Tafer H. PLEXY: efficient target prediction for box C/D snoRNAs Bioinformatics 2011 27 279 280 21076148
  60. [62]Mückstein U. Tafer H. Hackermüller J. Bernhart S.H. Stadler P.F. Hofacker I.L. Thermodynamics of RNA-RNA binding Bioinformatics 2006 22 1177 1182 16446276
  61. [63]Bartschat S. Kehr S. Tafer H. Stadler P.F. Hertel J. snoStrip: a snoRNA annotation pipeline Bioinformatics 2014 30 115 116 24174566
  62. [64]Kehr S. Bartschat S. Tafer H. Stadler P.F. Hertel J. Matching of Soulmates: coevolution of snoRNAs and their targets Mol. Biol. Evol. 2014 31 455 467 24162733
  63. [65]Maden B.E. Corbett M.E. Heeney P.A. Pugh K. Ajuh P.M. Classical and novel approaches to the detection and localization of the numerous modified nucleotides in eukaryotic ribosomal RNA Biochimie 1995 77 22 29 7599273
  64. [66]Maden B.E. Mapping 2′-O-methyl groups in ribosomal RNA Methods 2001 25 374 382 11860292
  65. [67]Taft R.J. Glazov E.A. Lassmann T. Hayashizaki Y. Carninci P. Mattick J.S. Small RNAs derived from snoRNAs RNA 2009 15 1233 1240 19474147 PMC2704076
  66. [68]Falaleeva M. Stamm S. Processing of snoRNAs as a new source of regulatory non-coding RNAs: snoRNA fragments form a new class of functional RNAs Bioessays 2013 35 46 54 23180440 PMC3732821
  67. [69]Deschamps-Francoeur G. Garneau D. Dupuis-Sandoval F. Roy A. Frappier M. Catala M. Couture S. Barbe-Marcoux M. Abou-Elela S. Scott M.S. Identification of discrete classes of small nucleolar RNA featuring different ends and RNA binding protein dependency Nucleic Acids Res. 2014 42 10073 10085 25074380 PMC4150776
  68. [70]Derrien T. Johnson R. Bussotti G. Tanzer A. Djebali S. Tilgner H. Guernec G. Martin D. Merkel A. Knowles D.G. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression Genome Res. 2012 22 1775 1789 22955988 PMC3431493
  69. [71]Yang J.-H. Shao P. Zhou H. Chen Y.-Q. Qu L.-H. deepBase: a database for deeply annotating and mining deep sequencing data Nucleic Acids Res. 2010 38 D123 D130 19966272 PMC2808990
  70. [72]Machyna M. Kehr S. Straube K. Kappei D. Buchholz F. Butter F. Ule J. Hertel J. Stadler P.F. Neugebauer K.M. The coilin interactome identifies hundreds of small noncoding RNAs that traffic through Cajal bodies Mol. Cell 2014 56 389 399 25514182
  71. [73]Griffiths-Jones S. Bateman A. Marshall M. Khanna A. Eddy S.R. Rfam: an RNA family database Nucleic Acids Res. 2003 31 439 441 12520045 PMC165453
  72. [74]Nawrocki E.P. Eddy S.R. Infernal 1.1: 100-fold faster RNA homology searches Bioinformatics 2013 29 2933 2935 24008419 PMC3810854
  73. [75]Kishore S. Khanna A. Zhang Z. Hui J. Balwierz P.J. Stefan M. Beach C. Nicholls R.D. Zavolan M. Stamm S. The snoRNA MBII-52 (SNORD 115) is processed into smaller RNAs and regulates alternative splicing Hum. Mol. Genet. 2010 19 1153 1164 20053671 PMC2838533
  74. [76]Schwartz S. Bernstein D.A. Mumbach M.R. Jovanovic M. Herbst R.H. León-Ricardo B.X. Engreitz J.M. Guttman M. Satija R. Lander E.S. Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA Cell 2014 159 148 162 25219674 PMC4180118
  75. [77]Carey M.F. Peterson C.L. Smale S.T. The primer extension assay Cold Spring Harb. Protoc. 2013 2013 164 173 23378648
  76. [78]Boorstein W.R. Craig E.A. Primer extension analysis of RNA Methods Enzymol. 1989 180 347 369 2482424
  77. [79]Raymond C.K. Roberts B.S. Garrett-Engele P. Lim L.P. Johnson J.M. Simple, quantitative primer-extension PCR assay for direct monitoring of microRNAs and short-interfering RNAs RNA 2005 11 1737 1744 16244135 PMC1370860
  78. [80]Cavaillé J. Hadjiolov A.A. Bachellerie J.P. Processing of mammalian rRNA precursors at the 3′ end of 18S rRNA. Identification of cis-acting signals suggests the involvement of U13 small nucleolar RNA Eur. J. Biochem. 1996 242 206 213 8973634
  79. [81]Kass S. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing Cell 1990 60 897 908 2156625
  80. [82]Dupuis-Sandoval F. Poirier M. Scott M.S. The emerging landscape of small nucleolar RNAs in cell biology Wiley Interdiscip. Rev. RNA 2015 6 381 397 25879954 PMC4696412
  81. [83]Fayet-Lebaron E. Atzorn V. Henry Y. Kiss T. 18S rRNA processing requires base pairings of snR30 H/ACA snoRNA to eukaryote-specific 18S sequences EMBO J. 2009 28 1260 1270 19322192 PMC2664660
  82. [84]Mannoor K. Liao J. Jiang F. Small nucleolar RNAs in cancer Biochim. Biophys. Acta 2012 1826 121 128 22498252 PMC3842010
  83. [85]Bortolin-Cavaillé M.-L. Cavaillé J. The SNORD115 (H/MBII-52) and SNORD116 (H/MBII-85) gene clusters at the imprinted Prader–Willi locus generate canonical box C/D snoRNAs Nucleic Acids Res. 2012 40 6800 6807 22495932 PMC3413130
  84. [86]Cavaillé J. Buiting K. Kiefmann M. Lalande M. Brannan C.I. Horsthemke B. Bachellerie J.P. Brosius J. Hüttenhofer A. Identification of brain-specific and imprinted small nucleolar RNA genes exhibiting an unusual genomic organization Proc. Natl. Acad. Sci. U.S.A. 2000 97 14311 14316 11106375 PMC18915
  85. [87]Mannoor K. Shen J. Liao J. Liu Z. Jiang F. Small nucleolar RNA signatures of lung tumor-initiating cells Mol. Cancer 2014 13 104 24886050 PMC4029979
  86. [88]Lin Y. Li Z. Ozsolak F. Kim S.W. Arango-Argoty G. Liu T.T. Tenenbaum S.A. Bailey T. Monaghan A.P. Milos P.M. An in-depth map of polyadenylation sites in cancer Nucleic Acids Res. 2012 40 8460 8471 22753024 PMC3458571
  87. [89]Gao L. Ma J. Mannoor K. Guarnera M.A. Shetty A. Zhan M. Xing L. Stass S.A. Jiang F. Genome-wide small nucleolar RNA expression analysis of lung cancer by next-generation deep sequencing Int. J. Cancer 2014 doi:10.1002/ijc.29169 25159866 · DOI · Paper page
  88. [90]Ronchetti D. Mosca L. Cutrona G. Tuana G. Gentile M. Fabris S. Agnelli L. Ciceri G. Matis S. Massucco C. Small nucleolar RNAs as new biomarkers in chronic lymphocytic leukemia BMC Med. Genomics 2013 6 27 24004562 PMC3766210
  89. [92]Gingold H. Tehler D. Christoffersen N.R. Nielsen M.M. Asmar F. Kooistra S.M. Christophersen N.S. Christensen L.L. Borre M. Sørensen K.D. A dual program for translation regulation in cellular proliferation and differentiation Cell 2014 158 1281 1292 25215487
  90. [93]Abel Y. Clerget G. Bourguignon-Igel V. Salone V. Rederstorff M. [Beyond usual functions of snoRNAs] Med. Sci. 2014 30 297 302 24685221
  91. [94]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. 2009 5 e1000507 19763159 PMC2730528
  92. [95]Ono M. Scott M.S. Yamada K. Avolio F. Barton G.J. Lamond A.I. Identification of human miRNA precursors that resemble box C/D snoRNAs Nucleic Acids Res. 2011 39 3879 3891 21247878 PMC3089480
  93. [96]Brameier M. Herwig A. Reinhardt R. Walter L. Gruber J. Human box C/D snoRNAs with miRNA like functions: expanding the range of regulatory RNAs Nucleic Acids Res. 2011 39 675 686 20846955 PMC3025573
  94. [97]Röther S. Meister G. Small RNAs derived from longer non-coding RNAs Biochimie 2011 93 1905 1915 21843590
  95. [98]Maxwell E.S. Fournier M.J. The small nucleolar RNAs Annu. Rev. Biochem. 1995 64 897 934 7574504
  96. [99]Makarova J.A. Kramerov D.A. Analysis of C/D box snoRNA genes in vertebrates: The number of copies decreases in placental mammals Genomics 2009 94 11 19 19272437
  97. [100]Machnicka M.A. Milanowska K. Osman Oglou O. Purta E. Olchowik A. Januszewski W. Kalinowski S. Dunin-Horkawicz S. Rother K.M. MODOMICS: a database of RNA modification pathways–2013 update Nucleic Acids Res. 2013 41 D262 D267 23118484 PMC3531130
  98. [101]Bleichert F. Gagnon K.T. Brown B.A. 2nd Maxwell E.S. Leschziner A.E. Unger V.M. Baserga S.J. A dimeric structure for archaeal box C/D small ribonucleoproteins Science 2009 325 1384 1387 19745151 PMC2975540
  99. [102]Schattner P. Barberan-Soler S. Lowe T.M.P. A computational screen for mammalian pseudouridylation guide H/ACA RNAs RNA 2006 12 15 25 16373490 PMC1370881
  100. [103]Weinberg Z. Zasha W. Breaker R.R. R2R - software to speed the depiction of aesthetic consensus RNA secondary structures BMC Bioinformatics 2011 12 3 21205310 PMC3023696

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Authors
Jorjani, H., Kehr, S., Jedlinski, D. J., Gumienny, R., Hertel, J., Stadler, P. F., Zavolan, M., & Gruber, A. R.
Affiliations
  • SIB Swiss Institute of Bioinformatics (CH)
  • Leipzig University (DE)
  • University of Vienna (AT)
Corresponding author
  • Zavolan, Mihaela
  • Gruber, Andreas R.
ORCID
Venue
Nucleic Acids Research
Publisher
Oxford University Press (OUP)
Published
2016-05-12
Volume
44
Issue
11
Pages
5068-5082
ISSN
  • 0305-1048 (ISSN-L)
  • 1362-4962
DOI
10.1093/nar/gkw386
PMC
PMC4914119
OpenAlex
W2382893801
Cited by
257
References
3
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15.77
Type
journal article
Language
en
Open access
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  • Nucleic Acids Research (publishedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • edoc (University of Basel) (submittedVersion, other-oa)
  • Phaidra (Universität Wien) (submittedVersion, cc-by-nc-nd)
  • Max Planck Institute for Plasma Physics (submittedVersion)
  • HighWire Press Open Archive (submittedVersion)
  • Fraunhofer-Publica (Fraunhofer-Gesellschaft) (submittedVersion)
  • edoc (University of Basel)
Funders
  • National Science Foundation
  • Marie Curie (28900)
  • European Commission (289007)
  • Deutsche Forschungsgemeinschaft (CRC 1052)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (31003A, 147013)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA modifications and cancer
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
Keywords
small nucleolar RNA, cell type-specific gene expression
MeSH terms
Gene Expression Regulation, Humans, Nucleic Acid Conformation, RNA Processing, Post-Transcriptional, Cluster Analysis, Computational Biology, RNA, Small Nucleolar, Gene Expression Profiling, RNA, Untranslated, Databases, Nucleic Acid, Molecular Sequence Annotation, Transcriptome

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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