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rRNA Biogenesis in Trypanosomes

Chapter
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 28)

Abstract

rRNA processing is a complex and essential process that starts in the nucleolus, continues in the nucleoplasm, and is completed in the cytoplasm. The process involves the concerted action of the small nucleolar RNAs that direct cleavage at distinct sites in the intergenic spaces and modify the rRNA by 2′-O-methylation and pseudouridylation. The process also requires protein factors such as endonucleases, ATPases, GTPases, and helicases that mediate the precise cleavage of the pre-rRNA in the intergenic regions and ensure the correct assembly of the two ribosomal subunits. In this chapter, I describe unique properties of this process in trypanosomes. As opposed to most eukaryotes, the large subunit of the rRNA is cleaved into two large subunits and additional small rRNA fragments. The unique repertoire of small nucleolar RNAs (snoRNAs) is described, emphasizing the lack of conventional snoRNAs involved in rRNA processing and the presence of trypanosome-specific snoRNAs. Finally, the protein factors involved in this process are described, focusing on factors whose function was elucidated in trypanosomes, and on a bioinformatics survey to detect protein factors involved in this process in other eukaryotes.

Keywords

Large subunit rRNA Processosome Small nucleolar RNAs Small rRNA Small subunit rRNA Trypanosomes 

Notes

Acknowledgements

Our work on rRNA processing was supported by a grant from the Israel-US Binational Science Foundation (BSF). S.M. holds the David and Inez Myers Chair in RNA silencing of diseases. I wish to thank Fr. Hiba Asher-Waldman for the bioinformatics analysis of the protein factors involved in rRNA processing and maturation.

References

  1. Asano K, Phan L, Valasek L, Schoenfeld LW, Shalev A, Clayton J, Nielsen K, Donahue TF, Hinnebusch AG (2001) A multifactor complex of eIF1, eIF2, eIF3, eIF5, and tRNA(i)Met promotes initiation complex assembly and couples GTP hydrolysis to AUG recognition. Cold Spring Harb Symp Quant Biol 66:403–415PubMedCrossRefGoogle Scholar
  2. Atzorn V, Fragapane P, Kiss T (2004) U17/snR30 is a ubiquitous snoRNA with two conserved sequence motifs essential for 18S rRNA production. Mol Cell Biol 24:1769–1778PubMedCrossRefGoogle Scholar
  3. Bally M, Hughes J, Cesareni G (1988) SnR30: a new, essential small nuclear RNA from Saccharomyces cerevisiae. Nucleic Acids Res 16:5291–5303PubMedCrossRefGoogle Scholar
  4. Barth S, Hury A, Liang XH, Michaeli S (2005) 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 280:34558–34568PubMedCrossRefGoogle Scholar
  5. Barth S, Shalem B, Hury A, Tkacz ID, Liang XH, Uliel S, Myslyuk I, Doniger T, Salmon-Divon M, Unger R, Michaeli S (2008) Elucidating the role of C/D snoRNA in rRNA processing and modification in Trypanosoma brucei. Eukaryot Cell 7:86–101PubMedCrossRefGoogle Scholar
  6. Beltrame M, Tollervey D (1992) Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO J 11:1531–1542PubMedGoogle Scholar
  7. Bohnsack MT, Kos M, Tollervey D (2008) Quantitative analysis of snoRNA association with pre-ribosomes and release of snR30 by Rok1 helicase. EMBO Rep 9:1230–1236PubMedCrossRefGoogle Scholar
  8. Brown JW, Echeverria M, Qu LH (2003) Plant snoRNAs: functional evolution and new modes of gene expression. Trends Plant Sci 8:42–49PubMedCrossRefGoogle Scholar
  9. Campbell DA, Kubo K, Clark CG, Boothroyd JC (1987) Precise identification of cleavage sites involved in the unusual processing of trypanosome ribosomal RNA. J Mol Biol 196:113–124PubMedCrossRefGoogle Scholar
  10. Chanfreau G, Gouyette C, Schwer B, Jacquier A (1999) Trans-complementation of the second step of pre-mRNA splicing by exogenous 5′ exons. RNA 5:876–882PubMedCrossRefGoogle Scholar
  11. Chekanova JA, Dutko JA, Mian IS, Belostotsky DA (2002) Arabidopsis thaliana exosome subunit AtRrp4p is a hydrolytic 3′→5′ exonuclease containing S1 and KH RNA-binding domains. Nucleic Acids Res 30:695–700PubMedCrossRefGoogle Scholar
  12. Cordingley JS, Turner MJ (1980) 6.5S RNA; preliminary characterisation of unusual small RNAs in Trypanosoma brucei. Mol Biochem Parasitol 1:91–96PubMedCrossRefGoogle Scholar
  13. Darzacq X, Kiss T (2000) Processing of intron-encoded box C/D small nucleolar RNAs lacking a 5′,3′-terminal stem structure. Mol Cell Biol 20:4522–4531PubMedCrossRefGoogle Scholar
  14. Decatur WA, Fournier MJ (2003) RNA-guided nucleotide modification of ribosomal and other RNAs. J Biol Chem 278:695–698PubMedCrossRefGoogle Scholar
  15. Dennis PP, Omer A, Lowe T (2001) A guided tour: small RNA function in Archaea. Mol Microbiol 40:509–519PubMedCrossRefGoogle Scholar
  16. Dez C, Noaillac-Depeyre J, Caizergues-Ferrer M, Henry Y (2002) Naf1p, an essential nucleoplasmic factor specifically required for accumulation of box H/ACA small nucleolar RNPs. Mol Cell Biol 22:7053–7065PubMedCrossRefGoogle Scholar
  17. Dieci G, Preti M, Montanini B (2009) Eukaryotic snoRNAs: a paradigm for gene expression flexibility. Genomics 94:83–88PubMedCrossRefGoogle Scholar
  18. Dragon F, Gallagher JE, Compagnone-Post PA, Mitchell BM, Porwancher KA, Wehner KA, Wormsley S, Settlage RE, Shabanowitz J, Osheim Y, Beyer AL, Hunt DF, Baserga SJ (2002) A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417:967–970PubMedCrossRefGoogle Scholar
  19. Droll D, Archer S, Fenn K, Delhi P, Matthews K, Clayton C (2010) The trypanosome Pumilio-domain protein PUF7 associates with a nuclear cyclophilin and is involved in ribosomal RNA maturation. FEBS Lett 584:1156–1162PubMedCrossRefGoogle Scholar
  20. Dunbar DA, Chen AA, Wormsley S, Baserga SJ (2000a) The genes for small nucleolar RNAs in Trypanosoma brucei are organized in clusters and are transcribed as a polycistronic RNA. Nucleic Acids Res 28:2855–2861PubMedCrossRefGoogle Scholar
  21. Dunbar DA, Wormsley S, Lowe TM, Baserga SJ (2000b) Fibrillarin-associated box C/D small nucleolar RNAs in Trypanosoma brucei. Sequence conservation and implications for 2′-O-ribose methylation of rRNA. J Biol Chem 275:14767–14776PubMedCrossRefGoogle Scholar
  22. Eichler DC, Craig N (1994) Processing of eukaryotic ribosomal RNA. Prog Nucleic Acid Res Mol Biol 49:197–239PubMedCrossRefGoogle Scholar
  23. Fatica A, Oeffinger M, Dlakic M, Tollervey D (2003) Nob1p is required for cleavage of the 3′ end of 18S rRNA. Mol Cell Biol 23:1798–1807PubMedCrossRefGoogle Scholar
  24. Filipowicz W, Pogacic V (2002) Biogenesis of small nucleolar ribonucleoproteins. Curr Opin Cell Biol 14:319–327PubMedCrossRefGoogle Scholar
  25. Fromont-Racine M, Senger B, Saveanu C, Fasiolo F (2003) Ribosome assembly in eukaryotes. Gene 313:17–42PubMedCrossRefGoogle Scholar
  26. Ganot P, Bortolin ML, Kiss T (1997) Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell 89:799–809PubMedCrossRefGoogle Scholar
  27. Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, Remor M, Hofert C, Schelder M, Brajenovic M, Ruffner H, Merino A, Klein K, Hudak M, Dickson D, Rudi T, Gnau V, Bauch A, Bastuck S, Huhse B, Leutwein C, Heurtier MA, Copley RR, Edelmann A, Querfurth E, Rybin V, Drewes G, Raida M, Bouwmeester T, Bork P, Seraphin B, Kuster B, Neubauer G, Superti-Furga G (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141–147PubMedCrossRefGoogle Scholar
  28. Grandi P, Rybin V, Bassler J, Petfalski E, Strauss D, Marzioch M, Schafer T, Kuster B, Tschochner H, Tollervey D, Gavin AC, Hurt E (2002) 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol Cell 10:105–115PubMedCrossRefGoogle Scholar
  29. Gray MW (1979) The ribosomal RNA of the trypanosomatid protozoan Crithidia fasciculata: physical characteristics and methylated sequences. Can J Biochem 57:914–926PubMedCrossRefGoogle Scholar
  30. Gupta SK, Hury A, Ziporen Y, Shi H, Ullu E, Michaeli S (2010) Small nucleolar RNA interference in Trypanosoma brucei: mechanism and utilization for elucidating the function of snoRNAs. Nucleic Acids Res 38:7236–7247PubMedCrossRefGoogle Scholar
  31. Hartshorne T (1998) Distinct regions of U3 snoRNA interact at two sites within the 5′ external transcribed spacer of pre-rRNAs in Trypanosoma brucei cells. Nucleic Acids Res 26:2541–2553PubMedCrossRefGoogle Scholar
  32. Hartshorne T, Agabian N (1993) RNA B is the major nucleolar trimethylguanosine-capped small nuclear RNA associated with fibrillarin and pre-rRNAs in Trypanosoma brucei. Mol Cell Biol 13:144–154PubMedGoogle Scholar
  33. Hartshorne T, Toyofuku W (1999) Two 5′-ETS regions implicated in interactions with U3 snoRNA are required for small subunit rRNA maturation in Trypanosoma brucei. Nucleic Acids Res 27:3300–3309PubMedCrossRefGoogle Scholar
  34. Hartshorne T, Toyofuku W, Hollenbaugh J (2001) Trypanosoma brucei 5′ETS A’-cleavage is directed by 3′-adjacent sequences, but not two U3 snoRNA-binding elements, which are all required for subsequent pre-small subunit rRNA processing events. J Mol Biol 313:733–749PubMedCrossRefGoogle Scholar
  35. Huang GM, Jarmolowski A, Struck JC, Fournier MJ (1992) Accumulation of U14 small nuclear RNA in Saccharomyces cerevisiae requires box C, box D, and a 5′, 3′ terminal stem. Mol Cell Biol 12:4456–4463PubMedGoogle Scholar
  36. Hury A, Goldshmidt H, Tkacz ID, Michaeli S (2009) Trypanosome spliced-leader-associated RNA (SLA1) localization and implications for spliced-leader RNA biogenesis. Eukaryot Cell 8:56–68PubMedCrossRefGoogle Scholar
  37. Jarmolowski A, Zagorski J, Li HV, Fournier MJ (1990) Identification of essential elements in U14 RNA of Saccharomyces cerevisiae. EMBO J 9:4503–4509PubMedGoogle Scholar
  38. Jensen BC, Wang Q, Kifer CT, Parsons M (2003) The NOG1 GTP-binding protein is required for biogenesis of the 60 S ribosomal subunit. J Biol Chem 278:32204–32211PubMedCrossRefGoogle Scholar
  39. Jensen BC, Brekken DL, Randall AC, Kifer CT, Parsons M (2005) Species specificity in ribosome biogenesis: a nonconserved phosphoprotein is required for formation of the large ribosomal subunit in Trypanosoma brucei. Eukaryot Cell 4:30–35PubMedCrossRefGoogle Scholar
  40. Kass S, Sollner-Webb B (1990) The first pre-rRNA-processing event occurs in a large complex: analysis by gel retardation, sedimentation, and UV cross-linking. Mol Cell Biol 10:4920–4931PubMedGoogle Scholar
  41. Kiss-Laszlo Z, Henry Y, Bachellerie JP, Caizergues-Ferrer M, Kiss T (1996) Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell 85:1077–1088PubMedCrossRefGoogle Scholar
  42. Kolev NG, Franklin JB, Carmi S, Shi H, Michaeli S, Tschudi C (2010) The transcriptome of the human pathogen Trypanosoma brucei at single-nucleotide resolution. PLoS Pathog 6:e1001090PubMedCrossRefGoogle Scholar
  43. Levitan A, Xu YX, Ben Dov C, Ben Shlomo H, Zhang YF, Michaeli S (1998) Characterization of a novel trypanosomatid small nucleolar RNA. Nucleic Acids Res 26:1775–1783PubMedCrossRefGoogle Scholar
  44. Li L, Ye K (2006) Crystal structure of an H/ACA box ribonucleoprotein particle. Nature 443:302–307PubMedCrossRefGoogle Scholar
  45. Li HD, Zagorski J, Fournier MJ (1990) Depletion of U14 small nuclear RNA (snR128) disrupts production of 18S rRNA in Saccharomyces cerevisiae. Mol Cell Biol 10:1145–1152PubMedGoogle Scholar
  46. Liang WQ, Fournier MJ (1995) U14 base-pairs with 18S rRNA: a novel snoRNA interaction required for rRNA processing. Genes Dev 9:2433–2443PubMedCrossRefGoogle Scholar
  47. Liang WQ, Clark JA, Fournier MJ (1997) The rRNA-processing function of the yeast U14 small nucleolar RNA can be rescued by a conserved RNA helicase-like protein. Mol Cell Biol 17:4124–4132PubMedGoogle Scholar
  48. Liang XH, Liu L, Michaeli S (2001) Identification of the first trypanosome H/ACA RNA that guides pseudouridine formation on rRNA. J Biol Chem 276:40313–40318PubMedGoogle Scholar
  49. Liang XH, Xu YX, Michaeli S (2002) 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 8:237–246PubMedCrossRefGoogle Scholar
  50. Liang XH, Liu Q, Michaeli S (2003) Small nucleolar RNA interference induced by antisense or double-stranded RNA in trypanosomatids. Proc Natl Acad Sci USA 100:7521–7526PubMedCrossRefGoogle Scholar
  51. Liang XH, Uliel S, Hury A, Barth S, Doniger T, Unger R, Michaeli S (2005) 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 11:619–645PubMedCrossRefGoogle Scholar
  52. Liang XH, Hury A, Hoze E, Uliel S, Myslyuk I, Apatoff A, Unger R, Michaeli S (2007a) 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 6:361–377PubMedCrossRefGoogle Scholar
  53. Liang XH, Liu Q, Fournier MJ (2007b) rRNA modifications in an intersubunit bridge of the ribosome strongly affect both ribosome biogenesis and activity. Mol Cell 28:965–977PubMedCrossRefGoogle Scholar
  54. Lustig Y, Wachtel C, Safro M, Liu L, Michaeli S (2010) ‘RNA walk’ a novel approach to study RNA-RNA interactions between a small RNA and its target. Nucleic Acids Res 38:e5PubMedCrossRefGoogle Scholar
  55. Matera AG, Terns RM, Terns MP (2007) Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs. Nat Rev Mol Cell Biol 8:209–220PubMedCrossRefGoogle Scholar
  56. Mereau A, Fournier R, Gregoire A, Mougin A, Fabrizio P, Lührmann R, Branlant C (1997) An in vivo and in vitro structure-function analysis of the Saccharomyces cerevisiae U3A snoRNP: protein-RNA contacts and base-pair interaction with the pre-ribosomal RNA. J Mol Biol 273:552–571PubMedCrossRefGoogle Scholar
  57. Michaeli S, Doniger T, Gupta SK, Wurtzel O, Romano M, Visnovezky D, Sorek R, Unger R, Ullu E (2012) RNA-seq analysis of small RNPs in Trypanosoma brucei reveals a rich repertoire of non-coding RNAs. Nucleic Acids Res 40(3):1282–1298PubMedCrossRefGoogle Scholar
  58. Morrissey JP, Tollervey D (1993) Yeast snR30 is a small nucleolar RNA required for 18S rRNA synthesis. Mol Cell Biol 13:2469–2477PubMedGoogle Scholar
  59. Morrissey JP, Tollervey D (1997) U14 small nucleolar RNA makes multiple contacts with the pre-ribosomal RNA. Chromosoma 105:515–522PubMedCrossRefGoogle Scholar
  60. Myslyuk I, Doniger T, Horesh Y, Hury A, Hoffer R, Ziporen Y, Michaeli S, Unger R (2008) Psiscan: a computational approach to identify H/ACA-like and AGA-like non-coding RNA in trypanosomatid genomes. BMC Bioinformatics 9:471PubMedCrossRefGoogle Scholar
  61. Nakaar V, Dare AO, Hong D, Ullu E, Tschudi C (1994) Upstream tRNA genes are essential for expression of small nuclear and cytoplasmic RNA genes in trypanosomes. Mol Cell Biol 14:6736–6742PubMedGoogle Scholar
  62. Nissan TA, Bassler J, Petfalski E, Tollervey D, Hurt E (2002) 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J 21:5539–5547PubMedCrossRefGoogle Scholar
  63. Nizami Z, Deryusheva S, Gall JG (2010) The Cajal body and histone locus body. Cold Spring Harb Perspect Biol 2:a000653PubMedCrossRefGoogle Scholar
  64. Peculis BA (1997) The sequence of the 5′ end of the U8 small nucleolar RNA is critical for 5.8S and 28S rRNA maturation. Mol Cell Biol 17:3702–3713PubMedGoogle Scholar
  65. Peculis BA, Steitz JA (1994) Sequence and structural elements critical for U8 snRNP function in Xenopus oocytes are evolutionarily conserved. Genes Dev 8:2241–2255PubMedCrossRefGoogle Scholar
  66. Prohaska K, Williams N (2009) Assembly of the Trypanosoma brucei 60S ribosomal subunit nuclear export complex requires trypanosome-specific proteins P34 and P37. Eukaryot Cell 8:77–87PubMedCrossRefGoogle Scholar
  67. Puvion-Dutilleul F, Bachellerie JP, Puvion E (1991) Nucleolar organization of HeLa cells as studied by in situ hybridization. Chromosoma 100:395–409PubMedCrossRefGoogle Scholar
  68. Rashid R, Aittaleb M, Chen Q, Spiegel K, Demeler B, Li H (2003) Functional requirement for symmetric assembly of archaeal box C/D small ribonucleoprotein particles. J Mol Biol 333:295–306PubMedCrossRefGoogle Scholar
  69. Rashid R, Liang B, Baker DL, Youssef OA, He Y, Phipps K, Terns RM, Terns MP, Li H (2006) Crystal structure of a Cbf5-Nop10-Gar1 complex and implications in RNA-guided pseudouridylation and dyskeratosis congenita. Mol Cell 21:249–260PubMedCrossRefGoogle Scholar
  70. Roberts TG, Dungan JM, Watkins KP, Agabian N (1996) The SLA RNA gene of Trypanosoma brucei is organized in a tandem array which encodes several small RNAs. Mol Biochem Parasitol 83:163–174PubMedCrossRefGoogle Scholar
  71. Roberts TG, Sturm NR, Yee BK, Yu MC, Hartshorne T, Agabian N, Campbell DA (1998) Three small nucleolar RNAs identified from the spliced leader-associated RNA locus in kinetoplastid protozoans. Mol Cell Biol 18:4409–4417PubMedGoogle Scholar
  72. Rozhdestvensky TS, Tang TH, Tchirkova IV, Brosius J, Bachellerie JP, Hüttenhofer A (2003) Binding of L7Ae protein to the K-turn of archaeal snoRNAs: a shared RNA binding motif for C/D and H/ACA box snoRNAs in Archaea. Nucleic Acids Res 31:869–877PubMedCrossRefGoogle Scholar
  73. Russell AG, Schnare MN, Gray MW (2004) Pseudouridine-guide RNAs and other Cbf5p-associated RNAs in Euglena gracilis. RNA 10:1034–1046PubMedCrossRefGoogle Scholar
  74. Russell AG, Schnare MN, Gray MW (2006) A large collection of compact box C/D snoRNAs and their isoforms in Euglena gracilis: structural, functional and evolutionary insights. J Mol Biol 357:1548–1565PubMedCrossRefGoogle Scholar
  75. Sanvito F, Piatti S, Villa A, Bossi M, Lucchini G, Marchisio PC, Biffo S (1999) The beta4 integrin interactor p27(BBP/eIF6) is an essential nuclear matrix protein involved in 60S ribosomal subunit assembly. J Cell Biol 144:823–837PubMedCrossRefGoogle Scholar
  76. Saveanu C, Bienvenu D, Namane A, Gleizes PE, Gas N, Jacquier A, Fromont-Racine M (2001) Nog2p, a putative GTPase associated with pre-60S subunits and required for late 60S maturation steps. EMBO J 20:6475–6484PubMedCrossRefGoogle Scholar
  77. Saveanu C, Namane A, Gleizes PE, Lebreton A, Rousselle JC, Noaillac-Depeyre J, Gas N, Jacquier A, Fromont-Racine M (2003) Sequential protein association with nascent 60S ribosomal particles. Mol Cell Biol 23:4449–4460PubMedCrossRefGoogle Scholar
  78. Savino R, Gerbi SA (1990) In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing. EMBO J 9:2299–2308PubMedGoogle Scholar
  79. Schnare MN, Gray MW (1990) Sixteen discrete RNA components in the cytoplasmic ribosome of Euglena gracilis. J Mol Biol 215:73–83PubMedCrossRefGoogle Scholar
  80. Schnare MN, Spencer DF, Gray MW (1983) Primary structures of four novel small ribosomal RNAs from Crithidia fasciculata. Can J Biochem Cell Biol 61:38–45PubMedCrossRefGoogle Scholar
  81. Shi H, Tschudi C, Ullu E (2006) An unusual Dicer-like1 protein fuels the RNA interference pathway in Trypanosoma brucei. RNA 12:2063–2072PubMedCrossRefGoogle Scholar
  82. Sun C, Woolford JL Jr (1997) The yeast nucleolar protein Nop4p contains four RNA recognition motifs necessary for ribosome biogenesis. J Biol Chem 272:25345–25352PubMedCrossRefGoogle Scholar
  83. Tang TH, Bachellerie JP, Rozhdestvensky T, Bortolin ML, Huber H, Drungowski M, Elge T, Brosius J, Hüttenhofer A (2002) Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proc Natl Acad Sci USA 99:7536–7541PubMedCrossRefGoogle Scholar
  84. Tollervey D (1987) A yeast small nuclear RNA is required for normal processing of pre-ribosomal RNA. EMBO J 6:4169–4175PubMedGoogle Scholar
  85. Tollervey D, Kiss T (1997) Function and synthesis of small nucleolar RNAs. Curr Opin Cell Biol 9:337–342PubMedCrossRefGoogle Scholar
  86. Tschochner H, Hurt E (2003) Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol 13:255–263PubMedCrossRefGoogle Scholar
  87. Tyc K, Steitz JA (1992) A new interaction between the mouse 5′ external transcribed spacer of pre-rRNA and U3 snRNA detected by psoralen crosslinking. Nucleic Acids Res 20:5375–5382PubMedCrossRefGoogle Scholar
  88. Tycowski KT, Shu MD, Steitz JA (1994) Requirement for intron-encoded U22 small nucleolar RNA in 18S ribosomal RNA maturation. Science 266:1558–1561PubMedCrossRefGoogle Scholar
  89. Tycowski KT, Shu MD, Kukoyi A, Steitz JA (2009) A conserved WD40 protein binds the Cajal body localization signal of scaRNP particles. Mol Cell 34:47–57PubMedCrossRefGoogle Scholar
  90. Uliel S, Liang XH, Unger R, Michaeli S (2004) Small nucleolar RNAs that guide modification in trypanosomatids: repertoire, targets, genome organisation, and unique functions. Int J Parasitol 34:445–454PubMedCrossRefGoogle Scholar
  91. Vanrobays E, Gleizes PE, Bousquet-Antonelli C, Noaillac-Depeyre J, Caizergues-Ferrer M, Gelugne JP (2001) Processing of 20S pre-rRNA to 18S ribosomal RNA in yeast requires Rrp10p, an essential non-ribosomal cytoplasmic protein. EMBO J 20:4204–4213PubMedCrossRefGoogle Scholar
  92. Venema J, Tollervey D (1996) RRP5 is required for formation of both 18S and 5.8S rRNA in yeast. EMBO J 15:5701–5714PubMedGoogle Scholar
  93. Venema J, Tollervey D (1999) Ribosome synthesis in Saccharomyces cerevisiae. Annu Rev Genet 33:261–311PubMedCrossRefGoogle Scholar
  94. Venema J, Vos HR, Faber AW, van Venrooij WJ, Raue HA (2000) Yeast Rrp9p is an evolutionarily conserved U3 snoRNP protein essential for early pre-rRNA processing cleavages and requires box C for its association. RNA 6:1660–1671PubMedCrossRefGoogle Scholar
  95. Watkins NJ, Dickmanns A, Lührmann R (2002) Conserved stem II of the box C/D motif is essential for nucleolar localization and is required, along with the 15.5K protein, for the hierarchical assembly of the box C/D snoRNP. Mol Cell Biol 22:8342–8352PubMedCrossRefGoogle Scholar
  96. Wehner KA, Gallagher JE, Baserga SJ (2002) Components of an interdependent unit within the SSU processome regulate and mediate its activity. Mol Cell Biol 22:7258–7267PubMedCrossRefGoogle Scholar
  97. White TC, Rudenko G, Borst P (1986) Three small RNAs within the 10 kb trypanosome rRNA transcription unit are analogous to domain VII of other eukaryotic 28S rRNAs. Nucleic Acids Res 14:9471–9489PubMedCrossRefGoogle Scholar
  98. Xu Y, Liu L, Lopez-Estrano C, Michaeli S (2001) Expression studies on clustered trypanosomatid box C/D small nucleolar RNAs. J Biol Chem 276:14289–14298PubMedGoogle Scholar
  99. Yang CY, Zhou H, Luo J, Qu LH (2005) Identification of 20 snoRNA-like RNAs from the primitive eukaryote, Giardia lamblia. Biochem Biophys Res Commun 328:1224–1231PubMedCrossRefGoogle Scholar
  100. Zamudio JR, Mittra B, Chattopadhyay A, Wohlschlegel JA, Sturm NR, Campbell DA (2009) Trypanosoma brucei spliced leader RNA maturation by the cap 1 2′-O-ribose methyltransferase and SLA1 H/ACA snoRNA pseudouridine synthase complex. Mol Cell Biol 29:1202–1211PubMedCrossRefGoogle Scholar

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© Springer-Verlag GmbH Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.The Mina and Everard Goodman Faculty of Life Sciences, and Advanced Materials and Nanotechnology InstituteBar-Ilan UniversityRamat-GanIsrael

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