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Volume 2013 (2013), Article ID 614735, 14 pages
http://dx.doi.org/10.1155/2013/614735
Review Article

Ribonucleoproteins in Archaeal Pre-rRNA Processing and Modification

1Department of Molecular Biophysics and Biochemistry, Yale University School of Medicine, New Haven, CT 06510, USA
2Department of Microbial Pathogenesis, Yale University School of Medicine, New Haven, CT 06510, USA
3Department of Therapeutic Radiology, Yale University School of Medicine, New Haven, CT 06510, USA
4Department of Genetics, Yale University School of Medicine, New Haven, CT 06510, USA

Received 12 October 2012; Revised 9 January 2013; Accepted 15 January 2013

Academic Editor: Anita Marchfelder

Copyright © 2013 W. S. Vincent Yip et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. F. Doolittle, “Phylogenetic classification and the universal tree,” Science, vol. 284, no. 5423, pp. 2124–2128, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Yarza, M. Richter, J. Peplies et al., “The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains,” Systematic and Applied Microbiology, vol. 31, no. 4, pp. 241–250, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. G. E. Fox, L. J. Magrum, W. E. Balch, R. S. Wolfe, and C. R. Woese, “Classification of methanogenic bacteria by 16S ribosomal RNA characterization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 74, no. 10, pp. 4537–4541, 1977. View at Scopus
  4. C. R. Woese and G. E. Fox, “Phylogenetic structure of the prokaryotic domain: the primary kingdoms,” Proceedings of the National Academy of Sciences of the United States of America, vol. 74, pp. 5088–5090, 1977. View at Publisher · View at Google Scholar
  5. C. R. Woese, O. Kandler, and M. L. Wheelis, “Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 12, pp. 4576–4579, 1990. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Green and H. F. Noller, “Ribosomes and translation,” Annual Review of Biochemistry, vol. 66, pp. 679–716, 1997. View at Publisher · View at Google Scholar
  7. P. J. Shaw and E. G. Jordan, “The nucleolus,” Annual Review of Cell and Developmental Biology, vol. 11, pp. 93–121, 1995. View at Publisher · View at Google Scholar
  8. J. R. Warner, “The economics of ribosome biosynthesis in yeast,” Trends in Biochemical Sciences, vol. 24, no. 11, pp. 437–440, 1999. View at Publisher · View at Google Scholar · View at Scopus
  9. T. Allers and M. Mevarech, “Archaeal genetics—the third way,” Nature Reviews Genetics, vol. 6, no. 1, pp. 58–73, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. A. E. Hage and D. Tollervey, “A surfeit of factors: why is ribosome assembly so much more complicated in eukaryotes than bacteria?” RNA Biology, vol. 1, no. 1, pp. 10–15, 2004. View at Scopus
  11. G. Klug, E. Evguenieva-Hackenberg, A. D. Omer, et al., RNA Processing, American Society for Microbiology, Washington, DC, USA, 2007.
  12. C. R. Woese, L. J. Magrum, and G. E. Fox, “Archaebacteria,” Journal of Molecular Evolution, vol. 11, no. 3, pp. 245–252, 1978. View at Scopus
  13. R. P. Anitori, Ed., Extremophiles: Microbiology and Biotechnology, Caister Academic Press, Norfolk, UK, 2012.
  14. Z. M. P. Lee, C. Bussema III, and T. M. Schmidt, “rrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea,” Nucleic Acids Research, vol. 37, no. 1, pp. D489–D493, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. J. A. Klappenbach, P. R. Saxman, J. R. Cole, and T. M. Schmidt, “rrndb: the ribosomal RNA operon copy number database,” Nucleic Acids Research, vol. 29, no. 1, pp. 181–184, 2001. View at Scopus
  16. K. R. Bower-Phipps, D. W. Taylor, H. Wang, and S. J. Baserga, “The box C/D sRNP dimeric architecture is conserved across domain Archaea,” RNA, vol. 18, no. 8, pp. 1527–1540, 2012. View at Publisher · View at Google Scholar
  17. J. Lin, S. Lai, R. Jia et al., “Structural basis for site-specific ribose methylation by box C/D RNA protein complexes,” Nature, vol. 469, no. 7331, pp. 559–563, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. A. L. Hartman, C. Norais, J. H. Badger et al., “The complete genome sequence of Haloferax volcanii DS2, a model archaeon,” PloS One, vol. 5, no. 3, article e9605, 2010. View at Scopus
  19. J. Chant and P. Dennis, “Archaebacteria: transcription and processing of ribosomal RNA sequences in Halobacterium cutirubrum,” The EMBO Journal, vol. 5, no. 5, pp. 1091–1097, 1986. View at Scopus
  20. J. Kjems and R. A. Garrett, “An intron in the 23S ribosomal RNA gene of the archaebacterium Desulfurococcus mobilis,” Nature, vol. 318, no. 6047, pp. 675–677, 1985. View at Scopus
  21. J. Kjems and R. A. Garrett, “Ribosomal RNA introns in archaea and evidence for RNA conformational changes associated with splicing,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 2, pp. 439–443, 1991. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Burggraf, N. Larsen, C. R. Woese, and K. O. Stetter, “An intron within the 16S ribosomal RNA gene of the archaeon Pyrobaculum aerophilum,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 6, pp. 2547–2550, 1993. View at Scopus
  23. J. Z. Dalgaard, R. A. Garrett, and M. Belfort, “Purification and characterization of two forms of I-DmoI, a thermophilic site-specific endonuclease encoded by an archaeal intron,” Journal of Biological Chemistry, vol. 269, no. 46, pp. 28885–28892, 1994. View at Scopus
  24. J. Z. Dalgaard, R. A. Garrett, and M. Belfort, “A site-specific endonuclease encoded by a typical archaeal intron,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 12, pp. 5414–5417, 1993. View at Scopus
  25. V. Salman, R. Amann, D. A. Shub, et al., “Multiple self-splicing introns in the 16S rRNA genes of giant sulfur bacteria,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, pp. 4203–4208, 2012.
  26. A. D. Omer, S. Ziesche, H. Ebhardt, and P. P. Dennis, “In vitro reconstitution and activity of a C/D box methylation guide ribonucleoprotein complex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 8, pp. 5289–5294, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. B. Charpentier, S. Muller, and C. Branlant, “Reconstitution of archaeal H/ACA small ribonucleoprotein complexes active in pseudouridylation,” Nucleic Acids Research, vol. 33, no. 10, pp. 3133–3144, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. D. L. Baker, O. A. Youssef, M. I. R. Chastkofsky, D. A. Dy, R. M. Terns, and M. P. Terns, “RNA-guided RNA modification: functional organization of the archaeal H/ACA RNP,” Genes & Development, vol. 19, no. 10, pp. 1238–1248, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Tollervey, “Small nucleolar RNAs guide ribosomal RNA methylation,” Science, vol. 273, no. 5278, pp. 1056–1057, 1996. View at Scopus
  30. P. Ganot, M. L. Bortolin, and T. Kiss, “Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs,” Cell, vol. 89, no. 5, pp. 799–809, 1997. View at Scopus
  31. Z. Kiss-László, Y. Henry, J. P. Bachellerie, M. Caizergues-Ferrer, and T. Kiss, “Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs,” Cell, vol. 85, no. 7, pp. 1077–1088, 1996. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Nicoloso, L. H. Qu, B. Michot, and J. P. Bachellerie, “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,” Journal of Molecular Biology, vol. 260, no. 2, pp. 178–195, 1996. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Cavaillé, M. Nicoloso, and J. P. Bachellerie, “Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides,” Nature, vol. 383, no. 6602, pp. 732–735, 1996. View at Publisher · View at Google Scholar · View at Scopus
  34. B. Lapeyre, “Conserved ribosomal RNA modification and their putative roles in ribosome biogenesis and translation,” in Fine-Tuning of RNA Functions by Modification and Editing, vol. 12, pp. 263–284, Springer, New York, NY, USA, 2005.
  35. W. A. Decatur and M. J. Fournier, “rRNA modifications and ribosome function,” Trends in Biochemical Sciences, vol. 27, no. 7, pp. 344–351, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. K. R. Noon, E. Bruenger, and J. A. McCloskey, “Posttranscriptional modifications in 16S and 23S rRNAs of the archaeal hyperthermophile Sulfolobus solfataricus,” Journal of Bacteriology, vol. 180, no. 11, pp. 2883–2888, 1998. View at Scopus
  37. W. A. Decatur and M. J. Fournier, “RNA-guided nucleotide modification of ribosomal and other RNAs,” Journal of Biological Chemistry, vol. 278, no. 2, pp. 695–698, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Ofengand and A. Bakin, “Mapping to nucleotide resolution of pseudouridine residues in large subunit ribosomal RNAs from representative eukaryotes, prokaryotes, archaebacteria, mitochondria and chloroplasts,” Journal of Molecular Biology, vol. 266, no. 2, pp. 246–268, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. B. E. H. Maden, “The numerous modified nucleotides in eukaryotic ribosomal RNA,” Progress in Nucleic Acid Research and Molecular Biology, vol. 39, pp. 241–303, 1990. View at Publisher · View at Google Scholar · View at Scopus
  40. D. D. Piekna-Przybylska, W. A. Decatur, and M. J. Fournier, “The 3D rRNA modification maps database: with interactive tools for ribosome analysis,” Nucleic Acids Research, vol. 36, no. 1, pp. D178–D183, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Del Campo, Y. Kaya, and J. Ofengand, “Identification and site of action of the remaining four putative pseudouridine synthases in Escherichia coli,” RNA, vol. 7, no. 11, pp. 1603–1615, 2001. View at Scopus
  42. T. H. Tang, N. Polacek, M. Zywicki et al., “Identification of novel non-coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus,” Molecular Microbiology, vol. 55, no. 2, pp. 469–481, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. M. A. Zago, P. P. Dennis, and A. D. Omer, “The expanding world of small RNAs in the hyperthermophilic archaeon Sulfolobus solfataricus,” Molecular Microbiology, vol. 55, no. 6, pp. 1812–1828, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Kjems and R. A. Garrett, “Novel expression of the ribosomal RNA genes in the extreme thermophile and archaebacterium Desulfurococcus mobilis,” The EMBO Journal, vol. 6, pp. 3521–3530, 1987.
  45. J. Kjems, H. Leffers, R. A. Garrett, G. Wich, W. Leinfelder, and A. Böck, “Gene organization, transcription signals and processing of the single ribosomal RNA operon of the archaebacterium Thermoproteus tenax,” Nucleic Acids Research, vol. 15, no. 12, pp. 4821–4835, 1987. View at Publisher · View at Google Scholar · View at Scopus
  46. Q. She, R. K. Singh, F. Confalonieri, et al., “The complete genome of the crenarchaeon Sulfolobus solfataricus P2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 14, pp. 7835–7840, 2001. View at Publisher · View at Google Scholar
  47. R. K. Hartmann, N. Ulbrich, and V. A. Erdmann, “An unusual rRNA operon constellation: in Thermus thermophilus HB8 the 23S/5S rRNA operon is a separate entity from the 16S rRNA operon,” Biochimie, vol. 69, no. 10, pp. 1097–1104, 1987. View at Scopus
  48. C. J. Bult, O. White, G. J. Olsen, et al., “Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii,” Science, vol. 273, no. 5278, pp. 1058–1073, 1996. View at Publisher · View at Google Scholar
  49. H. K. Ree and R. A. Zimmermann, “Organization and expression of the 16S, 23S and 5S ribosomal RNA genes from the archaebacterium Thermoplasma acidophilum,” Nucleic Acids Research, vol. 18, no. 15, pp. 4471–4478, 1990. View at Scopus
  50. E. Waters, M. J. Hohn, I. Ahel, et al., “The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 22, pp. 12984–12988, 2003. View at Publisher · View at Google Scholar
  51. G. Wachtershauser, “Towards a reconstruction of ancestral genomes by gene cluster alignment,” Systematic and Applied Microbiology, vol. 21, no. 4, pp. 473–477, 1998. View at Scopus
  52. J. Duan, L. Li, J. Lu, W. Wang, and K. Ye, “Structural mechanism of substrate RNA recruitment in H/ACA RNA-guided pseudouridine synthase,” Molecular Cell, vol. 34, no. 4, pp. 427–439, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Lykke-Andersen, C. Aagaard, M. Semionenkov, and R. A. Garrett, “Archaeal introns: splicing, intercellular mobility and evolution,” Trends in Biochemical Sciences, vol. 22, no. 9, pp. 326–331, 1997. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Belfort, M. E. Reaban, T. Coetzee, and J. Z. Dalgaard, “Prokaryotic introns and inteins: a panoply of form and function,” Journal of Bacteriology, vol. 177, no. 14, pp. 3897–3903, 1995. View at Scopus
  55. T. H. Tang, T. S. Rozhdestvensky, B. C. d'Orval et al., “RNomics in Archaea reveals a further link between splicing of archaeal introns and rRNA processing,” Nucleic Acids Research, vol. 30, no. 4, pp. 921–930, 2002. View at Scopus
  56. P. P. Dennis, A. Omer, and T. Lowe, “A guided tour: small RNA function in Aarchaea,” Molecular Microbiology, vol. 40, no. 3, pp. 509–519, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. S. M. Ziesche, A. D. Omer, and P. P. Dennis, “RNA-guided nucleotide modification of ribosomal and non-ribosomal RNAs in Archaea,” Molecular Microbiology, vol. 54, no. 4, pp. 980–993, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. A. D. Omer, S. Ziesche, W. A. Decatur, M. J. Fournier, and P. P. Dennis, “RNA-modifying machines in archaea,” Molecular Microbiology, vol. 48, no. 3, pp. 617–629, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. P. P. Dennis and A. Omer, “Small non-coding RNAs in Archaea,” Current Opinion in Microbiology, vol. 8, no. 6, pp. 685–694, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Ni, A. L. Tien, and M. J. Fournier, “Small nucleolar RNAs direct site-specific synthesis of pseudouridine in ribosomal RNA,” Cell, vol. 89, no. 4, pp. 565–573, 1997. View at Scopus
  61. A. D. Omer, T. M. Lowe, A. G. Russell, H. Ebhardt, S. R. Eddy, and P. P. Dennis, “Homologs of small nucleolar RNAs in Archaea,” Science, vol. 288, no. 5465, pp. 517–522, 2000. View at Publisher · View at Google Scholar · View at Scopus
  62. R. J. Klein, Z. Misulovin, and S. R. Eddy, “Noncoding RNA genes identified in AT-rich hyperthermophiles,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 11, pp. 7542–7547, 2002. View at Publisher · View at Google Scholar · View at Scopus
  63. C. Gaspin, J. Cavaillé, G. Erauso, et al., “Archaeal homologs of eukaryotic methylation guide small nucleolar RNAs: lessons from the Pyrococcus genomes,” Journal of Molecular Biology, vol. 297, no. 4, pp. 895–906, 2000. View at Publisher · View at Google Scholar
  64. T. H. Tang, J. P. Bachellerie, T. Rozhdestvensky et al., “Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 11, pp. 7536–7541, 2002. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Muller, F. Leclerc, I. Behm-Ansmant, J. B. Fourmann, B. Charpentier, and C. Branlant, “Combined in silico and experimental identification of the Pyrococcus abyssi H/ACA sRNAs and their target sites in ribosomal RNAs,” Nucleic Acids Research, vol. 36, no. 8, pp. 2459–2475, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. L. Randau, “RNA processing in the minimal organism Nanoarchaeum equitans,” Genome Biology, vol. 13, article R63, 2012.
  67. D. L. Bernick, P. P. Dennis, M. Höchsmann, et al., “Discovery of Pyrobaculum small RNA families with atypical pseudouridine guide RNA features,” RNA, vol. 18, pp. 402–411, 2012.
  68. F. Bleichert, K. T. Gagnon, B. Brown, et al., “A dimeric structure for archaeal box C/D small ribonucleoproteins,” Science, vol. 325, pp. 1384–1387, 2009.
  69. F. Bleichert and S. J. Baserga, “Ribonucleoprotein multimers and their functions,” Critical Reviews in Biochemistry and Molecular Biology, vol. 45, no. 5, pp. 331–350, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. T. Moore, Y. Zhang, M. O. Fenley, and H. Li, “Molecular basis of box C/D RNA-protein interactions: cocrystal structure of archaeal L7Ae and a box C/D RNA,” Structure, vol. 12, no. 5, pp. 807–818, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. D. J. Klein, T. M. Schmeing, P. B. Moore, and T. A. Steitz, “The kink-turn: a new RNA secondary structure motif,” The EMBO Journal, vol. 20, no. 15, pp. 4214–4221, 2001. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Nolivos, A. J. Carpousis, and B. Clouet-d'Orval, “The K-loop, a general feature of the Pyrococcus C/D guide RNAs, is an RNA structural motif related to the K-turn,” Nucleic Acids Research, vol. 33, no. 20, pp. 6507–6514, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. E. Tran, X. Zhang, L. Lackey, and E. S. Maxwell, “Conserved spacing between the box C/D and C′/D′ RNPs of the archaeal box C/D sRNP complex is required for efficient 2′-O-methylation of target RNAs,” RNA, vol. 11, no. 3, pp. 285–293, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. H. Wang, D. Boisvert, K. K. Kim, R. Kim, and S. H. Kim, “Crystal structure of a fibrillarin homologue from Methanococcus jannaschii, a hyperthermophile, at 1.6 Å resolution,” The EMBO Journal, vol. 19, no. 3, pp. 317–323, 2000. View at Scopus
  75. J. F. Kuhn, E. J. Tran, and E. S. Maxwell, “Archaeal ribosomal protein L7 is a functional homolog of the eukaryotic 15.5kD/Snu13p snoRNP core protein,” Nucleic Acids Research, vol. 30, no. 4, pp. 931–941, 2002. View at Scopus
  76. T. S. Rozhdestvensky, T. H. Tang, I. V. Tchirkova, J. Brosius, J. P. Bachellerie, and A. Hüttenhofer, “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 Research, vol. 31, no. 3, pp. 869–877, 2003. View at Publisher · View at Google Scholar · View at Scopus
  77. M. Aittaleb, R. Rashid, Q. Chen, J. R. Palmer, C. J. Daniels, and H. Li, “Structure and function of archaeal box C/D sRNP core proteins,” Nature Structural Biology, vol. 10, no. 4, pp. 256–263, 2003. View at Publisher · View at Google Scholar · View at Scopus
  78. R. Rashid, M. Aittaleb, Q. Chen, K. Spiegel, B. Demeler, and H. Li, “Functional requirement for symmetric assembly of archaeal box C/D small ribonucleoprotein particles,” Journal of Molecular Biology, vol. 333, no. 2, pp. 295–306, 2003. View at Publisher · View at Google Scholar · View at Scopus
  79. E. J. Tran, X. Zhang, and E. S. Maxwell, “Efficient RNA 2′-O-methylation requires juxtaposed and symmetrically assembled archaeal box C/D and C′/D′ RNPs,” The EMBO Journal, vol. 22, no. 15, pp. 3930–3940, 2003. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Aittaleb, T. Visone, M. O. Fenley, and H. Li, “Structural and thermodynamic evidence for a stabilizing role of Nop5p in S-adenosyl-L-methionine binding to fibrillarin,” Journal of Biological Chemistry, vol. 279, no. 40, pp. 41822–41829, 2004. View at Publisher · View at Google Scholar · View at Scopus
  81. X. Zhang, E. A. Champion, E. J. Tran, B. A. Brown, S. J. Baserga, and E. Stuart Maxwell, “The coiled-coil domain of the Nop56/58 core protein is dispensable for sRNP assembly but is critical for archaeal box C/D sRNP-guided nucleotide methylation,” RNA, vol. 12, no. 6, pp. 1092–1103, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. J. W. Hardin and R. T. Batey, “The bipartite architecture of the sRNA in an archaeal box C/D complex is a primary determinant of specificity,” Nucleic Acids Research, vol. 34, no. 18, pp. 5039–5051, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. A. D. Omer, M. Zago, A. Chang, and P. P. Dennis, “Probing the structure and function of an archaeal C/D-box methylation guide sRNA,” RNA, vol. 12, no. 9, pp. 1708–1720, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Oruganti, Y. Zhang, H. Li et al., “Alternative conformations of the archaeal Nop56/58-fibrillarin complex imply flexibility in box C/D RNPs,” Journal of Molecular Biology, vol. 371, no. 5, pp. 1141–1150, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. C. D. Appel and E. S. Maxwell, “Structural features of the guide:target RNA duplex required for archaeal box C/D sRNA-guided nucleotide 2′-O-methylation,” RNA, vol. 13, no. 6, pp. 899–911, 2007. View at Publisher · View at Google Scholar · View at Scopus
  86. K. Ye, R. Jia, J. Lin et al., “Structural organization of box C/D RNA-guided RNA methyltransferase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 33, pp. 13808–13813, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. S. Xue, R. Wang, F. Yang et al., “Structural basis for substrate placement by an archaeal box C/D ribonucleoprotein particle,” Molecular Cell, vol. 39, no. 6, pp. 939–949, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. K. T. Gagnon, X. Zhang, G. Qu et al., “Signature amino acids enable the archaeal L7Ae box C/D RNP core protein to recognize and bind the K-loop RNA motif,” RNA, vol. 16, no. 1, pp. 79–90, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. F. Bleichert and S. J. Baserga, “Dissecting the role of conserved box C/D sRNA sequences in di-sRNP assembly and function,” Nucleic Acids Research, vol. 38, no. 22, pp. 8295–8305, 2010. View at Publisher · View at Google Scholar · View at Scopus
  90. K. T. Gagnon, S. Biswas, X. Zhang, et al., “Structurally conserved Nop56/58 N-terminal domain facilitates archaeal box C/D ribonucleoprotein-guided methyltransferase activity,” The Journal of Biological Chemistry, vol. 287, no. 23, pp. 19418–19428, 2012. View at Publisher · View at Google Scholar
  91. J. L. Martin and F. M. McMillan, “SAM (dependent) I AM: the S-adenosylmethionine-dependent methyltransferase fold,” Current Opinion in Structural Biology, vol. 12, no. 6, pp. 783–793, 2002. View at Publisher · View at Google Scholar · View at Scopus
  92. D. Tollervey, H. Lehtonen, R. Jansen, H. Kern, and E. C. Hurt, “Temperature-sensitive mutations demonstrate roles for yeast fibrillarin in pre-rRNA processing, pre-rRNA methylation, and ribosome assembly,” Cell, vol. 72, no. 3, pp. 443–457, 1993. View at Publisher · View at Google Scholar · View at Scopus
  93. H. Ghalei, H. H. Hsiao, H. Urlaub, M. C. Wahl, and N. J. Watkins, “A novel Nop5-sRNA interaction that is required for efficient archaeal box C/D sRNP formation,” RNA, vol. 16, no. 12, pp. 2341–2348, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. M. Terns and R. Terns, “Noncoding RNAs of the H/ACA family,” Cold Spring Harbor Symposia on Quantitative Biology, vol. 71, pp. 395–405, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. N. J. Watkins and M. T. Bohnsack, “The box C/D and H/ACA snoRNPs: key players in the modification, processing and the dynamic folding of ribosomal RNA,” Wiley Interdisciplinary Reviews. RNA, vol. 3, no. 3, pp. 397–414, 2012. View at Publisher · View at Google Scholar
  96. T. Hamma and A. R. Ferré-D'Amaré, “Structure of protein L7Ae bound to a K-turn derived from an archaeal box H/ACA sRNA at 1.8 Å resolution,” Structure, vol. 12, no. 5, pp. 893–903, 2004. View at Publisher · View at Google Scholar · View at Scopus
  97. E. V. Koonin, “Pseudouridine syntheses: four families of enzymes containing a putative uridine-binding motif also conserved in dUTPases and dCTP deaminases,” Nucleic Acids Research, vol. 24, no. 12, pp. 2411–2415, 1996. View at Scopus
  98. I. K. Blaby, M. Majumder, K. Chatterjee et al., “Pseudouridine formation in archaeal RNAs: the case of Haloferax volcanii,” RNA, vol. 17, no. 7, pp. 1367–1380, 2011. View at Publisher · View at Google Scholar · View at Scopus
  99. D. L. J. Lafontaine, C. Bousquet-Antonelli, Y. Henry, M. Caizergues-Ferrer, and D. Tollervey, “The box H + ACA snoRNAs carry Cbf5p, the putative rRNA pseudouridine synthase,” Genes & Development, vol. 12, no. 4, pp. 527–537, 1998. View at Scopus
  100. T. Hamma, S. L. Reichow, G. Varani, and A. R. Ferré-D'Amaré, “The Cbf5-Nop10 complex is a molecular bracket that organizes box H/ACA RNPs,” Nature Structural and Molecular Biology, vol. 12, no. 12, pp. 1101–1107, 2005. View at Publisher · View at Google Scholar · View at Scopus
  101. L. Li and K. Ye, “Crystal structure of an H/ACA box ribonucleoprotein particle,” Nature, vol. 443, no. 7109, pp. 302–307, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. X. Manival, C. Charron, J. B. Fourmann, F. Godard, B. Charpentier, and C. Branlant, “Crystal structure determination and site-directed mutagenesis of the Pyrococcus abyssi aCBF5-aNOP10 complex reveal crucial roles of the C-terminal domains of both proteins in H/ACA sRNP activity,” Nucleic Acids Research, vol. 34, no. 3, pp. 826–839, 2006. View at Publisher · View at Google Scholar · View at Scopus
  103. R. Rashid, B. Liang, D. L. Baker et al., “Crystal structure of a Cbf5-Nop10-Gar1 complex and implications in RNA-guided pseudouridylation and dyskeratosis congenita,” Molecular Cell, vol. 21, no. 2, pp. 249–260, 2006. View at Publisher · View at Google Scholar · View at Scopus
  104. B. Liang, J. Zhou, E. Kahen, R. M. Terns, M. P. Terns, and H. Li, “Structure of a functional ribonucleoprotein pseudouridine synthase bound to a substrate RNA,” Nature Structural and Molecular Biology, vol. 16, no. 7, pp. 740–746, 2009. View at Publisher · View at Google Scholar · View at Scopus
  105. B. Liang, S. Xue, R. M. Terns, M. P. Terns, and H. Li, “Substrate RNA positioning in the archaeal H/ACA ribonucleoprotein complex,” Nature Structural and Molecular Biology, vol. 14, no. 12, pp. 1189–1195, 2007. View at Publisher · View at Google Scholar · View at Scopus
  106. A. K. Henras, J. Soudet, M. Gérus et al., “The post-transcriptional steps of eukaryotic ribosome biogenesis,” Cellular and Molecular Life Sciences, vol. 65, no. 15, pp. 2334–2359, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. K. R. Phipps, J. M. Charette, and S. J. Baserga, “The small subunit processome in ribosome biogenesis—progress and prospects,” WIREs RNA, vol. 2, no. 1, pp. 1–21, 2011. View at Publisher · View at Google Scholar
  108. M. Beltrame and D. Tollervey, “Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA,” The EMBO Journal, vol. 11, no. 4, pp. 1531–1542, 1992. View at Scopus
  109. M. Beltrame and D. Tollervey, “Base pairing between U3 and the pre-ribosomal RNA is required for 18S rRNA synthesis,” The EMBO Journal, vol. 14, no. 17, pp. 4350–4356, 1995. View at Scopus
  110. A. Méreau, R. Fournier, A. Grégoire et al., “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,” Journal of Molecular Biology, vol. 273, no. 3, pp. 552–571, 1997. View at Publisher · View at Google Scholar · View at Scopus
  111. A. V. Borovjagin and S. A. Gerbi, “The spacing between functional Cis-elements of U3 snoRNA is critical for rRNA processing,” Journal of Molecular Biology, vol. 300, no. 1, pp. 57–74, 2000. View at Publisher · View at Google Scholar · View at Scopus
  112. A. V. Borovjagin and S. A. Gerbi, “Xenopus U3 snoRNA GAC-box A′ and box A sequences play distinct functional roles in rRNA processing,” Molecular and Cellular Biology, vol. 21, no. 18, pp. 6210–6221, 2001. View at Publisher · View at Google Scholar · View at Scopus
  113. D. A. Samarsky and M. J. Fournier, “Functional mapping of the U3 small nucleolar RNA from the yeast Saccharomyces cerevisiae,” Molecular and Cellular Biology, vol. 18, no. 6, pp. 3431–3444, 1998. View at Scopus
  114. P. P. Dennis, A. G. Russell, and M. Moniz De Sá, “Formation of the 5′ end pseudoknot in small subunit ribosomal RNA: involvement of U3-like sequences,” RNA, vol. 3, no. 4, pp. 337–343, 1997. View at Scopus
  115. R. J. W. Schoemaker and A. P. Gultyaev, “Computer simulation of chaperone effects of Archaeal C/D box sRNA binding on rRNA folding,” Nucleic Acids Research, vol. 34, no. 7, pp. 2015–2026, 2006. View at Publisher · View at Google Scholar · View at Scopus
  116. X. H. Liang, Q. Liu, and M. J. Fournier, “Loss of rRNA modifications in the decoding center of the ribosome impairs translation and strongly delays pre-rRNA processing,” RNA, vol. 15, no. 9, pp. 1716–1728, 2009. View at Publisher · View at Google Scholar · View at Scopus
  117. Y. Zebarjadian, T. King, M. J. Fournier, L. Clarke, and J. Carbon, “Point mutations in yeast CBF5 can abolish in vivo pseudouridylation of rRNA,” Molecular and Cellular Biology, vol. 19, no. 11, pp. 7461–7472, 1999. View at Scopus
  118. S. Higa-Nakamine, T. Suzuki, T. Uechi, et al., “Loss of ribosomal RNA modification causes developmental defects in zebrafish,” Nucleic Acids Research, pp. 1–8, 2011. View at Publisher · View at Google Scholar
  119. X. H. Liang, Q. Liu, and M. J. Fournier, “rRNA modifications in an intersubunit bridge of the ribosome strongly affect both ribosome biogenesis and activity,” Molecular Cell, vol. 28, no. 6, pp. 965–977, 2007. View at Publisher · View at Google Scholar · View at Scopus
  120. B. Liu, X. H. Liang, D. Piekna-Przybylska, Q. Liu, and M. J. Fournier, “Mis-targeted methylation in rRNA can severely impair ribosome synthesis and activity,” RNA Biology, vol. 5, no. 4, pp. 249–254, 2008. View at Scopus
  121. S. C. Blanchard and J. D. Puglisi, “Solution structure of the A loop of 23S ribosomal RNA,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 7, pp. 3720–3725, 2001. View at Publisher · View at Google Scholar · View at Scopus