Functional importance of individual rRNA 2′-O-ribose methylations revealed by high-resolution phenotyping

RNA

Volumn 14, Issue 4, 2008, Pages 649-656

  Esguerra, Jonathan ^a   Warringer, Jonas ^a   Blomberg, Anders ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

2 O ribose methylation; Box C D snoRNA; Phenotypic profiling; rRNA modification

Indexed keywords

2' O RIBOSE; ANTIBIOTIC AGENT; GROWTH INHIBITOR; RIBOSE; RIBOSOME RNA; SMALL NUCLEOLAR RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE DELETION; GENE MUTATION; METHYLATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ANTI-BACTERIAL AGENTS; GENES, FUNGAL; METHYLATION; NUCLEIC ACID CONFORMATION; PHENOTYPE; RIBOSE; RIBOSOMES; RNA, FUNGAL; RNA, RIBOSOMAL; RNA, SMALL NUCLEOLAR; SACCHAROMYCES CEREVISIAE; SEQUENCE DELETION;

EID: 41649115487     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.845808     Document Type: Article

References (36)

1. Bachellerie, J.P., Cavaille, J., and Huttenhofer, A. 2002. The expanding snoRNA world. Biochimie 84: 775-790.
2. Badis, G., Fromont-Racine, M., and Jacquier, A. 2003. A snoRNA that guides the two most conserved pseudouridine modifications within rRNA confers a growth advantage in yeast. RNA 9: 771-779.
3. Bally, M., Hughes, J., and Cesareni, G. 1988. SnR30: A new, essential small nuclear RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 16: 5291-5303. doi: 10.1093/nar/16.12.5291.
4. Ban, N., Nissen, P., Hansen, J., Moore, P.B., and Steitz, T.A. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289: 905-920.
5. Bashan, A., Zarivach, R., Schluenzen, F., Agmon, I., Harms, J., Auerbach, T., Baram, D., Berisio, R., Bartels, H., Hansen, H.A., et al. 2003. Ribosomal crystallography: Peptide bond formation and its inhibition. Biopolymers 70: 19-41.
6. Baxter-Roshek, J.L., Petrov, A.N., and Dinman, J.D. 2007. Optimization of ribosome structure and function by rRNA base modification. PLoS ONE 2: e174. doi: 10.1371/journal.pone.0000174.
7. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., and Bourne, P.E. 2000. The Protein Data Bank. Nucleic Acids Res. 28: 235-242. doi: 10.1093/nar/28.1.235.
8. Charette, M. and Gray, M.W. 2000. Pseudouridine in RNA: What, where, how, and why. IUBMB Life 49: 341-351.
9. Decatur, W.A. and Fournier, M.J. 2002. rRNA modifications and ribosome function. Trends Biochem. Sci. 27: 344-351.
10. Doi, Y., Yokoyama, K., Yamane, K., Wachino, J., Shibata, N., Yagi, T., Shibayama, K., Kato, H., and Arakawa, Y. 2004. Plasmid-mediated 16S rRNA methylase in Serratia marcescens conferring high-level resistance to aminoglycosides. Antimicrob. Agents Chemother. 48: 491-496.
11. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. 95: 14863-14868.
12. Hansen, J.L., Moore, P.B., and Steitz, T.A. 2003. Structures of five antibiotics bound at the peptidyl transferase center of the large ribosomal subunit. J. Mol. Biol. 330: 1061-1075.
13. Heiss, N.S., Knight, S.W., Vulliamy, T.J., Klauck, S.M., Wiemann, S., Mason, P.J., Poustka, A., and Dokal, I. 1998. X-linked dyskeratosis congenita is caused by mutations in a highly conserved gene with putative nucleolar functions. Nat. Genet. 19: 32-38.
14. Hughes, J.M., Konings, D.A., and Cesareni, G. 1987. The yeast homolog of U3 snRNA. EMBO J. 6: 2145-2155.
15. Hummel, H. and Bock, A. 1987. 23S Ribosomal RNA mutations in halobacteria conferring resistance to the anti-80S ribosome targeted antibiotic anisomycin. Nucleic Acids Res. 15: 2431-2443. doi:10.1093/nar/15.6.2431.
16. King, T.H., Liu, B., McCully, R.R., and Fournier, M.J. 2003. Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol. Cell 11: 425-435.
17. Kirpekar, F., Hansen, L.H., Rasmussen, A., Poehlsgaard, J., and Vester, B. 2005. The archaeon Haloarcula marismortui has few modifications in the central parts of its 23S ribosomal RNA. J. Mol. Biol. 348: 563-573.
18. Kiss, T. 2002. Small nucleolar RNAs: An abundant group of noncoding RNAs with diverse cellular functions. Cell 109: 145-148.
19. Lowe, T.M. and Eddy, S.R. 1999. A computational screen for methylation guide snoRNAs in yeast. Science 283: 1168-1171.
20. Ofengand, J. and Bakin, A. 1997. Mapping to nucleotide resolution of pseudouridine residues in large subunit ribosomal RNAs from representative eukaryotes, prokaryotes, archaebacteria, mitochondria, and chloroplasts. J. Mol. Biol. 266: 246-268.
21. Osterberg, M., Kim, H., Warringer, J., Melen, K., Blomberg, A., and von Heijne, G. 2006. Phenotypic effects of membrane protein overexpression in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. 103: 11148-11153.
22. Parker, R., Simmons, T., Shuster, E.O., Siliciano, P.G., and Guthrie, C. 1988. Genetic analysis of small nuclear RNAs in Saccharomyces cerevisiae: Viable sextuple mutant. Mol. Cell. Biol. 8: 3150-3159.
23. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., and Ferrin, T.E. 2004. UCSF Chimera - A visualization system for exploratory research and analysis. J. Comput. Chem. 25: 1605-1612.
24. Piekna-Przybylska, D., Decatur, W.A., and Fournier, M.J. 2007. New bioinformatic tools for analysis of nucleotide modifications in eukaryotic rRNA. RNA 13: 305-312.
25. Qu, L.H., Henras, A., Lu, Y.J., Zhou, H., Zhou, W.X., Zhu, Y.Q., Zhao, J., Henry, Y., Caizergues-Ferrer, M., and Bachellerie, J.P. 1999. Seven novel methylation guide small nucleolar RNAs are processed from a common polycistronic transcript by Rat1p and RNase III in yeast. Mol. Cell. Biol. 19: 1144-1158.
26. Ruggero, D., Grisendi, S., Piazza, F., Rego, E., Mari, F., Rao, P.H., Cordon-Cardo, C., and Pandolfi, P.P. 2003. Dyskeratosis congenita and cancer in mice deficient in ribosomal RNA modification. Science 299: 259-262.
27. Schmitt, M.E. and Clayton, D.A. 1993. Nuclear RNase MRP is required for correct processing of pre-5.8S rRNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 13: 7935-7941.
28. Schoemaker, R.J. and Gultyaev, A.P. 2006. Computer simulation of chaperone effects of Archaeal C/D box sRNA binding on rRNA folding. Nucleic Acids Res. 34: 2015-2026. doi: 10.1093/nar/gkl154.
29. Selmer, M., Dunham, C.M., Murphy, F.V.T., Weixlbaumer, A., Petry, S., Kelley, A.C., Weir, J.R., and Ramakrishnan, V. 2006. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313: 1935-1942.
30. Thatcher, J.W., Shaw, J.M., and Dickinson, W.J. 1998. Marginal fitness contributions of nonessential genes in yeast. Proc. Natl. Acad. Sci. 95: 253-257.
31. Tollervey, D. 1987. A yeast small nuclear RNA is required for normal processing of pre-ribosomal RNA. EMBO J. 6: 4169-4175.
32. Tollervey, D. and Guthrie, C. 1985. Deletion of a yeast small nuclear RNA gene impairs growth. EMBO J. 4: 3873-3878.
33. Warringer, J. and Blomberg, A. 2003. Automated screening in environmental arrays allows analysis of quantitative phenotypic profiles in Saccharomyces cerevisiae. Yeast 20: 53-67.
34. Warringer, J., Ericson, E., Fernandez, L., Nerman, O., and Blomberg, A. 2003. High-resolution yeast phenomics resolves different physiological features in the saline response. Proc. Natl. Acad. Sci. 100: 15724-15729.
35. Yoon, A., Peng, G., Brandenburger, Y., Zollo, O., Xu, W., Rego, E., and Ruggero, D. 2006. Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita. Science 312: 902-906.
36. Zagorski, J., Tollervey, D., and Fournier, M.J. 1988. Characterization of an SNR gene locus in Saccharomyces cerevisiae that specifies both dispensible and essential small nuclear RNAs. Mol. Cell. Biol. 8: 3282-3290.