Identification and characterization of the Thermus thermophilus 5-methylcytidine (m 5C) methyltransferase modifying 23 S ribosomal RNA (rRNA) base C1942

Journal of Biological Chemistry

Volumn 287, Issue 33, 2012, Pages 27593-27600

  Larsen, Line H G ^a   Rasmussen, Anette ^a   Giessing, Anders M B ^a   Jogl, Gerwald ^b   Kirpekar, Finn ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; COFACTORS; ENZYMATIC MECHANISMS; KEY RESIDUES; MESOPHILIC BACTERIA; METHYLTRANSFERASES; POST-TRANSCRIPTIONAL; RIBOSOMAL RNA (RRNA); S ADENOSYL L METHIONINES; THERMOPHILUS; THERMUS THERMOPHILUS; X RAY CRYSTAL STRUCTURES;

ALKYLATION; AMINO ACIDS; GENES;

RNA;

5 METHYLCYTIDINE METHYLTRANSFERASE; BACTERIAL RNA; CYTOSINE; METHYLTRANSFERASE; PROTEIN RLMD; PROTEIN RLMO; RNA 23S; RNA 50S; RNA 70S; RNA METHYLTRANSFERASE; S ADENOSYLMETHIONINE COFACTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; C1942 METHYLTRANSFERASE GENE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME STRUCTURE; GENE INACTIVATION; MESOPHILIC BACTERIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN MODIFICATION; PROTEIN RNA BINDING; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY; THERMUS THERMOPHILUS; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; COENZYMES; CRYSTALLOGRAPHY, X-RAY; METHYLATION; METHYLTRANSFERASES; RIBOSOME SUBUNITS, LARGE, BACTERIAL; RNA, BACTERIAL; RNA, RIBOSOMAL, 23S; S-ADENOSYLMETHIONINE; THERMUS THERMOPHILUS;

EID: 84864981568     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.376160     Document Type: Article

References (50)

1. Sirum-Connolly, K., Peltier, J. M., Crain, P. F., McCloskey, J. A., and Mason, T. L. (1995) Implications of a functional large ribosomal RNA with only three modified nucleotides. Biochimie 77, 30-39
2. Cantara, W. A., Crain, P. F., Rozenski, J., McCloskey, J. A., Harris, K. A., Zhang, X., Vendeix, F. A., Fabris, D., and Agris, P. F. (2011) The RNA Modification Database, RNAMDB: 2011 update. Nucleic Acids Res. 39, D195-D201
3. Havelund, J. F., Giessing, A. M., Hansen, T., Rasmussen, A., Scott, L. G., and Kirpekar, F. (2011) Identification of 5-hydroxycytidine at position 2501 concludes characterization of modified nucleotides in E. coli 23 S rRNA. J. Mol. Biol. 411, 529-536
4. Maden, B. E. (1988) Locations of methyl groups in 28 S rRNA of Xenopus laevis and man: clustering in the conserved core of molecule. J. Mol. Biol. 201, 289-314
5. Maden, B. E. (1990) The numerous modified nucleotides in eukaryotic ribosomal RNA. Prog. Nucleic Acid Res. Mol. Biol. 39, 241-303
6. 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
7. Raué, H. A., Klootwijk, J., and Musters, W. (1988) Evolutionary conservation of structure and function of high molecular weight ribosomal RNA. Prog. Biophys. Mol. Biol. 51, 77-129
8. Cavaillé, J., Nicoloso, M., and Bachellerie, J. P. (1996) Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides. Nature 383, 732-735
9. Ganot, P., Bortolin, M. L., and Kiss, T. (1997) Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell 89, 799-809
10. Kiss-László, Z., Henry, Y., Bachellerie, J. P., Caizergues-Ferrer, M., and Kiss, T. (1996) Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell 85, 1077-1088
11. Tycowski, K. T., Smith, C. M., Shu, M. D., and Steitz, J. A. (1996) A small nucleolar RNA requirement for site-specific ribose methylation of rRNA in Xenopus. Proc. Natl. Acad. Sci. U.S.A. 93, 14480-14485
12. Gaspin, C., Cavaillé, J., Erauso, G., and Bachellerie, J. P. (2000) Archaeal homologs of eukaryotic methylation guide small nucleolar RNAs: lessons from the Pyrococcus genomes. J. Mol. Biol. 297, 895-906
13. Omer, A. D., Lowe, T. M., Russell, A. G., Ebhardt, H., Eddy, S. R., and Dennis, P. P. (2000) Homologs of small nucleolar RNAs in Archaea. Science 288, 517-522
14. Del Campo, M., Recinos, C., Yanez, G., Pomerantz, S. C., Guymon, R., Crain, P. F., McCloskey, J. A., and Ofengand, J. (2005) Number, position, and significance of the pseudouridines in the large subunit ribosomal RNA of Haloarcula marismortui and Deinococcus radiodurans. RNA 11, 210-219
15. Massenet, S., Ansmant, I., Motorin, Y., and Branlant, C. (1999) The first determination of pseudouridine residues in 23 S ribosomal RNA from hyperthermophilic Archaea Sulfolobus acidocaldarius. FEBS Lett. 462, 94-100
16. Mengel-Jørgensen, J., Jensen, S. S., Rasmussen, A., Poehlsgaard, J., Iversen, J. J., and Kirpekar, F. (2006) Modifications in Thermus thermophilus 23 S ribosomal RNA are centered in regions of RNA-RNA contact. J. Biol. Chem. 281, 22108-22117
17. O'Connor, M., and Gregory, S. T. (2011) Inactivation of the RluD pseudouridine synthase has minimal effects on growth and ribosome function in wild-type Escherichia coli and Salmonella enterica. J. Bacteriol. 193, 154-162
18. Baudin-Baillieu, A., Fabret, C., Liang, X. H., Piekna-Przybylska, D., Fournier, M. J., and Rousset, J. P. (2009) Nucleotide modifications in three functionally important regions of the Saccharomyces cerevisiae ribosome affect translation accuracy. Nucleic Acids Res. 37, 7665-7677
19. Toh, S. M., Xiong, L., Bae, T., and Mankin, A. S. (2008) The methyltransferase YfgB/RlmN is responsible for modification of adenosine 2503 in 23 S rRNA. RNA 14, 98-106
20. Gustafsson, C., and Persson, B. C. (1998) Identification of the rrmA gene encoding the 23 S rRNA m1G745 methyltransferase in Escherichia coli and characterization of an m1G745-deficient mutant. J. Bacteriol. 180, 359-365
21. Kimura, S., Ikeuchi, Y., Kitahara, K., Sakaguchi, Y., and Suzuki, T. (2012) Base methylations in the double-stranded RNA by a fused methyltransferase bearing unwinding activity. Nucleic Acids Res. 40, 4071-4085
22. Vázquez-Laslop, N., Ramu, H., Klepacki, D., Kannan, K., and Mankin, A. S. (2010) The key function of a conserved and modified rRNA residue in the ribosomal response to the nascent peptide. EMBO J. 29, 3108-3117
23. Motorin, Y., Lyko, F., and Helm, M. (2010) 5-methylcytosine in RNA: detection, enzymatic formation, and biological functions. Nucleic Acids Res. 38, 1415-1430
24. Purta, E., O'Connor, M., Bujnicki, J. M., and Douthwaite, S. (2008) YccW is the m5C methyltransferase specific for 23 S rRNA nucleotide 1962. J. Mol. Biol. 383, 641-651
25. Sunita, S., Tkaczuk, K. L., Purta, E., Kasprzak, J. M., Douthwaite, S., Bujnicki, J. M., and Sivaraman, J. (2008) Crystal structure of the Escherichia coli 23 S rRNA:m5C methyltransferase RlmI (YccW) reveals evolutionary links between RNA modification enzymes. J. Mol. Biol. 383, 652-666
26. Pioszak, A. A., Murayama, K., Nakagawa, N., Ebihara, A., Kuramitsu, S., Shirouzu, M., and Yokoyama, S. (2005) Structures of a putative RNA 5-methyluridine methyltransferase, Thermus thermophilus TTHA1280, and its complex with S-adenosyl-L-homocysteine. Acta Crystallogr. F Struct. Biol. Cryst. Commun. 61, 867-874
27. Foster, P. G., Nunes, C. R., Greene, P., Moustakas, D., and Stroud, R. M. (2003) The first structure of an RNA m5C methyltransferase, Fmu, provides insight into catalytic mechanism and specific binding of RNA substrate. Structure 11, 1609-1620
28. Hallberg, B. M., Ericsson, U. B., Johnson, K. A., Andersen, N. M., Douthwaite, S., Nordlund, P., Beuscher, A. E., 4th, and Erlandsen, H. (2006) The structure of the RNA m5C methyltransferase YebU from Escherichia coli reveals a C-terminal RNA-recruiting PUA domain. J. Mol. Biol. 360, 774-787
29. Demirci, H., Larsen, L. H., Hansen, T., Rasmussen, A., Cadambi, A., Gregory, S. T., Kirpekar, F., and Jogl, G. (2010) Multisite-specific 16 S rRNA methyltransferase RsmF from Thermus thermophilus. RNA 16, 1584-1596
30. Lee, T. T., Agarwalla, S., and Stroud, R. M. (2005) A unique RNA fold in the RumA-RNA-cofactor ternary complex contributes to substrate selectivity and enzymatic function. Cell 120, 599-611
31. Alian, A., Lee, T. T., Griner, S. L., Stroud, R. M., and Finer-Moore, J. (2008) Structure of a TrmA-RNA complex: a consensus RNA fold contributes to substrate selectivity and catalysis in m5U methyltransferases. Proc. Natl. Acad. Sci. U.S.A. 105, 6876-6881
32. Andersen, T. E., Porse, B. T., and Kirpekar, F. (2004) A novel partial modification at C2501 in Escherichia coli 23 S ribosomal RNA. RNA 10, 907-913
33. Douthwaite, S., and Kirpekar, F. (2007) Identifying modifications in RNA by MALDI mass spectrometry. Methods Enzymol. 425, 1-20
34. Giessing, A. M., Scott, L. G., and Kirpekar, F. (2011) A nano-Chip-LC/MSn based strategy for characterization of modified ribonucleic acids using reduced porous graphitic carbon as a stationary phase. J. Am. Soc. Mass. Spectrom. 22, 1242-1251
35. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
36. Long, F., Vagin, A. A., Young, P., and Murshudov, G. N. (2008) BALBES: a molecular replacement pipeline. Acta Crystallogr. D. Biol. Crystallogr. 64, 125-132
37. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D. Biol. Crystallogr. 50, 760-763
38. Sun, W., Xu, X., Pavlova, M., Edwards, A. M., Joachimiak, A., Savchenko, A., and Christendat, D. (2005) The crystal structure of a novel SAM-dependent methyltransferase PH1915 from Pyrococcus horikoshii. Protein Sci. 14, 3121-3128
39. Langer, G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3, 1171-1179
40. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D. Biol. Crystallogr. 60, 2126-2132
41. Painter, J., and Merritt, E. A. (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D. Biol. Crystallogr. 62, 439-450
42. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D. Biol. Crystallogr. 66, 213-221
43. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D. Biol. Crystallogr. 66, 12-21
44. Andersen, N. M., and Douthwaite, S. (2006) YebU is a m5C methyltransferase specific for 16 S rRNA nucleotide 1407. J. Mol. Biol. 359, 777-786
45. Hashimoto, Y., Yano, T., Kuramitsu, S., and Kagamiyama, H. (2001) Disruption of Thermus thermophilus genes by homologous recombination using a thermostable kanamycin-resistant marker. FEBS Lett. 506, 231-234
46. Pérez-Arellano, I., Gallego, J., and Cervera, J. (2007) The PUA domain: a structural and functional overview. FEBS J. 274, 4972-4984
47. Holm, L., Kääriäinen, S., Rosenström, P., and Schenkel, A. (2008) Searching protein structure databases with DaliLite v.3. Bioinformatics 24, 2780-2781
48. Stanley, R. E., Blaha, G., Grodzicki, R. L., Strickler, M. D., and Steitz, T. A. (2010) The structures of the anti-tuberculosis antibiotics viomycin and capreomycin bound to the 70 S ribosome. Nat. Struct. Mol. Biol. 17, 289-293
49. Barneche, F., Gaspin, C., Guyot, R., and Echeverría, M. (2001) Identification of 66 box C/D snoRNAs in Arabidopsis thaliana: extensive gene duplications generated multiple isoforms predicting new ribosomal RNA 2′-O-methylation sites. J. Mol. Biol. 311, 57-73
50. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, version 1.3r1, Schrödinger, LLC, New York