Genome-wide analysis of small nucleolar RNAs of leishmania major reveals a rich repertoire of RNAs involved in modification and processing of rRNA

RNA Biology

Volumn 12, Issue 11, 2015, Pages 1222-1255

  Eliaz, Dror ^a   Doniger, Tirza ^a   Tkacz, Itai Dov ^a   Biswas, Viplov Kumar ^a   Gupta, Sachin Kumar ^a   Kolev, Nikolay G ^b   Unger, Ron ^a   Ullu, Elisabetta ^c   Tschudi, Christian ^b   Michaeli, Shulamit ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b YALE UNIVERSITY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

C D; H ACA; Leishmania; Methylation; Pseudouridylation; RRNA processing; SnoRNA

Indexed keywords

CORE PROTEIN; NHP2 PROTEIN; RIBOSOME RNA; SINGLE STRANDED RNA; SMALL NUCLEOLAR RNA; SNU13 PROTEIN; UNCLASSIFIED DRUG; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; COMPARATIVE STUDY; EUKARYOTE; GENE CLUSTER; LEISHMANIA MAJOR; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN MODIFICATION; PROTEIN SECONDARY STRUCTURE; RNA CLEAVAGE; RNA DEGRADATION; RNA PROCESSING; RNA SEQUENCE; RNA STRUCTURE; SEQUENCE ANALYSIS; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE; BASE PAIRING; BINDING SITE; CHEMISTRY; CONFORMATION; GENE LIBRARY; GENETICS; GENOME; GENOME-WIDE ASSOCIATION STUDY; METABOLISM; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE;

BASE PAIRING; BASE SEQUENCE; BINDING SITES; GENE LIBRARY; GENOME, PROTOZOAN; GENOME-WIDE ASSOCIATION STUDY; LEISHMANIA MAJOR; MULTIGENE FAMILY; NUCLEIC ACID CONFORMATION; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, RIBOSOMAL; RNA, SMALL NUCLEOLAR; TRYPANOSOMA;

EID: 84964058471     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.1080/15476286.2015.1038019     Document Type: Article

References (53)

1. Motorin Y, Helm M. RNA nucleotide methylation. Wiley Interdiscip Rev RNA 2011; 2:611-31; PMID:21823225; http://dx.doi.org/10.1002/wrna.79
2. Yu YT, Meier UT. Sf mod: Rna-guided isomerization of uridine to pseudouridine - pseudouridylation. RNA Biol 2015; 11:1483-94.
3. Balakin AG, Smith L, Fournier MJ. The RNA world of the nucleolus: two major families of small RNAs defined by different box elements with related functions. Cell 1996; 86:823-34; PMID:8797828; http://dx.doi.org/10.1016/S0092-8674(00)80156-7
4. Watkins NJ, Bohnsack MT. 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 2011; 3:397-414; PMID:22065625; http://dx.doi.org/10.1002/wrna.117
5. Kiss-Laszlo Z, Henry Y, Bachellerie JP, Caizergues-Ferrer M, Kiss T. Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell 1996; 85:1077-88; PMID:8674114; http://dx.doi.org/10.1016/S0092-8674(00)81308-2
6. Ganot P, Bortolin ML, Kiss T. Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell 1997; 89:799-809; PMID:9182768; http://dx.doi.org/10.1016/S0092-8674(00)80263-9
7. Tollervey D, Kiss T. Function and synthesis of small nucleolar RNAs. Curr Opin Cell Biol 1997; 9:337-42; PMID:9159079; http://dx.doi.org/10.1016/S0955-0674(97)80005-1
8. Aspegren A, Hinas A, Larsson P, Larsson A, Soderbom F. Novel non-coding RNAs in Dictyostelium discoideum and their expression during development. Nucleic Acids Res 2004; 32:4646-56; PMID:15333696; http://dx.doi.org/10.1093/nar/gkh804
9. Luo J, Teng M, Zhang GP, Lun ZR, Zhou H, Qu LH. Evaluating the evolution of G. lamblia based on the small nucleolar RNAs identified from Archaea and unicellular eukaryotes. Parasitol Res 2009; 104:1543-6; PMID:19326145; http://dx.doi.org/10.1007/s00436-009-1403-3
10. Kaur D, Gupta AK, 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; PMID:22892049; http://dx.doi.org/10.1186/ 1471-2164-13-390
11. Mishra PC, Kumar A, Sharma A. Analysis of small nucleolar RNAs reveals unique genetic features in malaria parasites. BMC Genomics 2009; 10:68; PMID:19200392; http://dx.doi.org/10.1186/1471-2164-10-68
12. Huang ZP, Zhou H, He HL, Chen CL, Liang D, Qu LH. Genome-wide analyses of two families of snoRNA genes from Drosophila melanogaster, demonstrating the extensive utilization of introns for coding of snoRNAs. RNA 2005; 11:1303-16; PMID:15987805; http://dx.doi.org/10.1261/rna.2380905
13. Morita K, Saito Y, Sato K, Oka K, Hotta K, Sakakibara Y. Genome-wide searching with base-pairing kernel functions for noncoding RNAs: computational and expression analysis of snoRNA families in Caenorhabditis elegans. Nucleic Acids Res 2009; 37:999-1009; PMID:19129214; http://dx.doi.org/10.1093/nar/gkn1054
14. Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M, Sisk E, Rajandream MA, Adlem E, Aert R, et al. The genome of the kinetoplastid parasite, Leishmania major. Science 2005; 309:436-42; PMID:16020728; http://dx.doi.org/10.1126/science.1112680
15. 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; 14:9471-89; PMID:3797245; http://dx.doi.org/10.1093/nar/14.23.9471
16. Liang XH, Uliel S, Hury A, Barth S, Doniger T, Unger R, Michaeli S. 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; PMID:15840815; http://dx.doi.org/10.1261/rna.7174805
17. Liang XH, Hury A, Hoze E, Uliel S, Myslyuk I, Apatoff A, Unger R, Michaeli S. Genome-wide analysis of C/D and H/ACA-like small nucleolar RNAs in Leishmania major indicates conservation among trypanosomatids in the repertoire and in their rRNA targets. Eukaryot Cell 2007; 6:361-77; PMID:17189491; http://dx.doi.org/10.1128/EC.00296-06
18. Liang XH, Xu YX, Michaeli S. The spliced leader-associated RNA is a trypanosome-specific sn(o) RNA that has the potential to guide pseudouridine formation on the SL RNA. RNA 2002; 8:237-46; PMID:11911368; http://dx.doi.org/10.1017/S1355838202018290
19. Michaeli S. Trans-splicing in trypanosomes: machinery and its impact on the parasite transcriptome. Future Microbiol 2011; 6:459-74; PMID:21526946; http://dx.doi.org/10.2217/fmb.11.20
20. Barth S, Hury A, Liang XH, Michaeli S. Elucidating the role of H/ACA-like RNAs in trans-splicing and rRNA processing via RNA interference silencing of the Trypanosoma brucei CBF5 pseudouridine synthase. J Biol Chem 2005; 280:34558-68; PMID:16107339; http://dx.doi.org/10.1074/jbc.M503465200
21. Hury A, Goldshmidt H, Tkacz ID, Michaeli S. Trypanosome spliced-leader-associated RNA (SLA1) localization and implications for spliced-leader RNA biogenesis. Eukaryot Cell 2009; 8:56-68; PMID:19028994; http://dx.doi.org/10.1128/EC.00322-08
22. Michaeli S, Doniger T, Gupta SK, Wurtzel O, Romano M, Visnovezky D, Sorek R, Unger R, Ullu E. RNA-seq analysis of small RNPs in Trypanosoma brucei reveals a rich repertoire of non-coding RNAs. Nucleic Acids Res 2012; 40:1282-98; PMID:21976736; http://dx.doi.org/10.1093/nar/gkr786
23. Gupta SK, Hury A, Ziporen Y, Shi H, Ullu E, Michaeli S. Small nucleolar RNA interference in Trypanosoma brucei: mechanism and utilization for elucidating the function of snoRNAs. Nucleic Acids Res 2010; 38:7236-47; PMID:20601683; http://dx.doi.org/10.1093/nar/gkq599
24. Mandelboim M, Barth S, Biton M, Liang XH, Michaeli S. Silencing of Sm proteins in Trypanosoma brucei by RNA interference captured a novel cytoplasmic intermediate in spliced leader RNA biogenesis. J Biol Chem 2003; 278:51469-78; PMID:14532264; http://dx.doi.org/10.1074/jbc.M308997200
25. Liu L, Ben-Shlomo H, Xu YX, Stern MZ, Goncharov I, Zhang Y, Michaeli S. The trypanosomatid signal recognition particle consists of two RNA molecules, a 7SL RNA homologue and a novel tRNA-like molecule. J Biol Chem 2003; 278:18271-80; PMID:12606550; http://dx.doi.org/10.1074/jbc.M209215200
26. Lustig Y, Wachtel C, Safro M, Liu L, Michaeli S.’RNA walk’ a novel approach to study RNA-RNA interactions between a small RNA and its target. Nucleic Acids Res 2010; 38:e5; PMID:19854950; http://dx.doi.org/10.1093/nar/gkp872
27. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. Integrative genomics viewer. Nat Biotechnol 2011; 29:24-6; PMID:21221095; http://dx.doi.org/10.1038/nbt.1754
28. Thorvaldsdottir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 2012; 14:178-92; PMID:22517427; http://dx.doi.org/10.1093/bib/bbs017
29. Tkacz ID, Gupta SK, Volkov V, Romano M, Haham T, Tulinski P, Lebenthal I, Michaeli S. Analysis of spliceosomal proteins in Trypanosomatids reveals novel functions in mRNA processing. J Biol Chem 2010; 285:27982-99; PMID:20592024; http://dx.doi.org/10.1074/jbc.M109.095349
30. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008; 5:621-8; PMID:18516045; http://dx.doi.org/10.1038/nmeth.1226
31. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403-10; PMID:2231712; http://dx.doi.org/10.1016/S0022-2836(05)80360-2
32. Lowe TM, Eddy SR. A computational screen for methylation guide snoRNAs in yeast. Science 1999; 283:1168-71; PMID:10024243; http://dx.doi.org/10.1126/science.283.5405.1168
33. Schattner P, Decatur WA, Davis CA, Ares M, Jr., Fournier MJ, Lowe TM. Genome-wide searching for pseudouridylation guide snoRNAs: analysis of the Saccharomyces cerevisiae genome. Nucleic Acids Res 2004; 32:4281-96; PMID:15306656; http://dx.doi.org/10.1093/nar/gkh768
34. Myslyuk I, Doniger T, Horesh Y, Hury A, Hoffer R, Ziporen Y, Michaeli S, Unger R. Psiscan: a computational approach to identify H/ACA-like and AGA-like non-coding RNA in trypanosomatid genomes. BMC Bioinformatics 2008; 9:471; PMID:18986541; http://dx.doi.org/10.1186/1471-2105-9-471
35. Mathews DH, Sabina J, Zuker M, Turner DH. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 1999; 288:911-40; PMID:10329189; http://dx.doi.org/10.1006/jmbi.1999.2700
36. Doniger T, Michaeli S, Unger R. Families of H/ACA ncRNA molecules in trypanosomatids. RNA Biol 2009; 6; PMID:19652533; http://dx.doi.org/10.4161/rna.6.4.9270
37. Rice P, Longden I, Bleasby A. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 2000; 16:276-7; PMID:10827456; http://dx.doi.org/10.1016/S0168-9525(00)02024-2
38. Aphasizhev R, Aphasizheva I, Nelson RE, Gao G, Simpson AM, Kang X, Falick AM, Sbicego S, Simpson L. Isolation of a U-insertion/deletion editing complex from Leishmania tarentolae mitochondria. EMBO J 2003; 22:913-24; PMID:12574127; http://dx.doi.org/10.1093/emboj/cdg083
39. Uliel S, Liang XH, Unger R, Michaeli S. Small nucleolar RNAs that guide modification in trypanosomatids: repertoire, targets, genome organisation, and unique functions. Int J Parasitol 2004; 34:445-54; PMID:15013734; http://dx.doi.org/10.1016/j.ijpara.2003.10.014
40. Barth S, Shalem B, Hury A, Tkacz ID, Liang XH, Uliel S, Myslyuk I, Doniger T, Salmon-Divon M, Unger R, et al. Elucidating the role of C/D snoRNA in rRNA processing and modification in Trypanosoma brucei. Eukaryot Cell 2008; 7:86-101; PMID:17981991; http://dx.doi.org/10.1128/EC.00215-07
41. Hashem Y, des Georges A, Dhote V, Langlois R, Liao HY, Grassucci RA, Pestova TV, Hellen CU, Frank J. Hepatitis-C-virus-like internal ribosome entry sites displace eIF3 to gain access to the 40S subunit. Nature 2013; 503:539-43; PMID:24185006; http://dx.doi.org/10.1038/nature12658
42. Schnare MN, Gray MW. Sixteen discrete RNA components in the cytoplasmic ribosome of Euglena gracilis. J Mol Biol 1990; 215:73-83; PMID:2118960; http://dx.doi.org/10.1016/S0022-2836(05)80096-8
43. Moore AN, Russell AG. Clustered organization, polycistronic transcription, and evolution of modificationguide snoRNA genes in Euglena gracilis. Mol Genet Genomics 2011; 287:55-66; PMID:22134850; http://dx.doi.org/10.1007/s00438-011-0662-8
44. Michaeli S. rRNA Biogenesis in Trypanosomes. In: Bindereif A, ed. RNA Metabolism in Trypanosomes. Belin, Heidelberg: Springer-Verlag, 2012:123-48.
45. Turowski TW, Tollervey D. Cotranscriptional events in eukaryotic ribosome synthesis. Wiley Interdiscip Rev RNA 2014; 6:129-39; PMID:25176256; http://dx.doi.org/10.1002/wrna.1263
46. McMahon M, Contreras A, Ruggero D. Small RNAs with big implications: new insights into H/ACA snoRNA function and their role in human disease. Wiley Interdiscip Rev RNA 2014; 6:173-89.
47. Schwartz S, Bernstein DA, Mumbach MR, Jovanovic M, Herbst RH, Leon-Ricardo BX, Engreitz JM, Guttman M, Satija R, Lander ES, et al. Transcriptome-wide mapping reveals widespread dynamic-regulated pseudouridylation of ncRNA and mRNA. Cell 2014; 159:148-62; PMID:25219674; http://dx.doi.org/10.1016/j.cell.2014.08.028
48. Tang TH, Rozhdestvensky TS, d’Orval BC, Bortolin ML, Huber H, Charpentier B, Branlant C, Bachellerie JP, Brosius J, Huttenhofer A. RNomics in Archaea reveals a further link between splicing of archaeal introns and rRNA processing. Nucleic Acids Res 2002; 30:921-30; PMID:11842103; http://dx.doi.org/10.1093/nar/30.4.921
49. Charette M, Gray MW. Pseudouridine in RNA: what, where, how, and why. IUBMB Life 2000; 49:341-51; PMID:10902565; http://dx.doi.org/10.1080/152165400410182
50. Kawai G, Yamamoto Y, Kamimura T, Masegi T, Sekine M, Hata T, Iimori T, Watanabe T, Miyazawa T, Yokoyama S. Conformational rigidity of specific pyrimidine residues in tRNA arises from posttranscriptional modifications that enhance steric interaction between the base and the 20-hydroxyl group. Biochemistry 1992; 31:1040-6; PMID:1310418; http://dx.doi.org/10.1021/bi00119a012
51. Schnare MN, Gray MW. Complete modification maps for the cytosolic small and large subunit rRNAs of Euglena gracilis: functional and evolutionary implications of contrasting patterns between the two rRNA components. J Mol Biol 2011; 413:66-83; PMID:21875598; http://dx.doi.org/10.1016/j.jmb.2011.08.037
52. Zamudio JR, Mittra B, Chattopadhyay A, Wohlschlegel JA, Sturm NR, Campbell DA. Trypanosoma brucei spliced leader RNA maturation by the cap 1 20-Oribose methyltransferase and SLA1 H/ACA snoRNA pseudouridine synthase complex. Mol Cell Biol 2009; 29:1202-11; PMID:19103757;http://dx.doi.org/10.1128/MCB.01496-08
53. Tycowski KT, Shu MD, Kukoyi A, Steitz JA. A conserved WD40 protein binds the Cajal body localization signal of scaRNP particles. Mol Cell 2009; 34:47-57; PMID:19285445; http://dx.doi.org/10.1016/j.molcel.2009.02.020