A single methyltransferase YefA (RlmCD) catalyses both m 5U747 and m 5U1939 modifications in Bacillus subtilis 23S rRNA

Nucleic Acids Research

Volumn 39, Issue 21, 2011, Pages 9368-9375

  Desmolaize, Benoit ^a   Fabret, Céline ^b,c   Brégeon, Damien ^b   Rose, Simon ^a   Grosjean, Henri ^b   Douthwaite, Stephen ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLURIDINE; BACTERIAL ENZYME; METHYLTRANSFERASE; RECOMBINANT ENZYME; RLMCD PROTEIN; RNA 23S; TRANSFER RNA; TRMFO PROTEIN; UNCLASSIFIED DRUG; URIDINE DERIVATIVE; YEFA PROTEIN;

ARTICLE; BACILLUS SUBTILIS; CONTROLLED STUDY; ENZYME SPECIFICITY; ESCHERICHIA COLI; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA METHYLATION;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BIOCATALYSIS; METHYLTRANSFERASES; MOLECULAR SEQUENCE DATA; RNA, RIBOSOMAL, 23S; SEQUENCE ALIGNMENT; URIDINE;

EID: 82255185627     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr626     Document Type: Article

References (48)

1. Björk, G.R. and Hagervall, T.G. (2005) Transfer RNA modification. In Böck, A., Curtis, R., Kaper, J.B., Neidhardt, T., Nyström, T. and Squires, C. (eds), Escherichia coli and Salmonella. ASM Press, Washington DC, p. 4.6.2.
2. Grosjean, H. (2009) DNA and RNA Modification Enzymes: Structure, Mechanism, Function and Evolution. Landes Biosciences, Austin Texas.
3. Urbonavič ius, J., Auxilien, S., Walbott, H., Trachana, K., Golinelli-Pimpaneau, B., Brochier-Armanet, C. and Grosjean, H. (2008) Acquisition of a bacterial RumA-type tRNA(uracil-54, C5)-methyltransferase by Archaea through an ancient horizontal gene transfer. Mol. Microbiol., 67, 323-335.
4. Ofengand, J. and Del Campo, M. (2005) Modified nucleotides of E. coli ribosomal RNA. In Böck, A., Curtis, R., Kaper, J.B., Neidhardt, T., Nyström, T. and Squires, C. (eds), Escherichia coli and Salmonella. ASM Press, Washington DC, p. 4.6.1.
5. Auxilien, S., Rasmussen, A., Rose, S., Brochier-Armanet, C., Husson, C., Fourmy, D., Grosjean, H. and Douthwaite, S. (2011) Specificity shifts in the rRNA and tRNA nucleotide targets of archaeal and bacterial m5U methyltransferases. RNA, 17, 45-53.
6. Jühling, F., Mörl, M., Hartmann, R.K., Sprinzl, M., Stadler, P.F. and Pütz, J. (2009) tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res., 37, D159-D162.
7. Björk, G.R. (1975) Transductional mapping of gene trmA responsible for the production of 5methyluridine in transfer ribonucleic acid of Escherichia coli. J. Bacteriol., 124, 92-98.
8. Piekna-Przybylska, D., Decatur, W.A. and Fournier, M.J. (2008) The 3D rRNA modification maps database: with interactive tools for ribosome analysis. Nucleic Acids Res., 36, D178-D183. (Pubitemid 351149718)
9. Agarwalla, S., Kealey, J.T., Santi, D.V. and Stroud, R.M. (2002) Characterization of the 23S ribosomal RNA m5U1939 methyltransferase from Escherichia coli. J. Biol. Chem., 277, 8835-8840. (Pubitemid 34952950)
10. Madsen, C.T., Mengel-Jorgensen, J., Kirpekar, F. and Douthwaite, S. (2003) Identifying the methyltransferases for m5U747 and m5U1939 in 23S rRNA using MALDI mass spectrometry. Nucleic Acids Res., 31, 4738-4746. (Pubitemid 37441836)
11. Tatusov, R.L., Fedorova, N.D., Jackson, J.D., Jacobs, A.R., Kiryutin, B., Koonin, E.V., Krylov, D.M., Mazumder, R., Mekhedov, S.L., Nikolskaya, A.N. et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics, 4, 41.
12. Nordlund, M.E., Johansson, J.O., von Pawel-Rammingen, U. and Byström, A.S. (2000) Identification of the TRM2 gene encoding the tRNA(m5U54)methyltransferase of Saccharomyces cerevisiae. RNA, 6, 844-860. (Pubitemid 30396026)
13. Urbonavič ius, J., Skouloubris, S., Myllykallio, H. and Grosjean, H. (2005) Identification of a novel gene encoding a flavin-dependent tRNA: m5U methyltransferase in bacteria-evolutionary implications. Nucleic Acids Res., 33, 3955-3964. (Pubitemid 41487256)
14. Vagner, V., Dervyn, E. and Ehrlich, S.D. (1998) A vector for systematic gene inactivation in Bacillus subtilis. Microbiology, 144, 3097-3104. (Pubitemid 28515588)
15. Trieu-Cuot, P., de Cespedes, G. and Horaud, T. (1992) Nucleotide sequence of the chloramphenicol resistance determinant of the streptococcal plasmid pIP501. Plasmid, 28, 272-276.
16. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K.A., Tomita, M., Wanner, B.L. and Mori, H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol., 2, 2006 0008.
17. Datsenko, K.A. and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA, 97, 6640-6645. (Pubitemid 30412767)
18. Sambrook, J. and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Press, Cold Spring Harbor, NY.
19. Douthwaite, S., Powers, T., Lee, J.Y. and Noller, H.F. (1989) Defining the structural requirements for a helix in 23S ribosomal RNA that confers erythromycin resistance. J. Mol. Biol., 209, 655-665. (Pubitemid 20046123)
20. Andersen, T.E., Porse, B.T. and Kirpekar, F. (2004) A novel partial modification at C2501 in Escherichia coli 23S ribosomal RNA. RNA, 10, 907-913. (Pubitemid 38669763)
21. Douthwaite, S. and Kirpekar, F. (2007) Identifying modifications in RNA by MALDI mass spectrometry. Methods Enzymol., 425, 1-20.
22. Kirpekar, F., Douthwaite, S. and Roepstorff, P. (2000) Mapping posttranscriptional modifications in 5S ribosomal RNA by MALDI mass spectrometry. RNA, 6, 296-306. (Pubitemid 30091599)
23. Kirpekar, F. and Krogh, T.N. (2001) RNA fragmentation studied in a matrix-assisted laser desorption/ionisation tandem quadropole/orthogonal time-of-flight mass spectrometer. Rapid Commun. Mass Sp., 15, 8-14. (Pubitemid 32094785)
24. Giessing, A.M., Jensen, S.S., Rasmussen, A., Hansen, L.H., Gondela, A., Long, K., Vester, B. and Kirpekar, F. (2009) Identification of 8-methyladenosine as the modification catalyzed by the radical SAM methyltransferase Cfr that confers antibiotic resistance in bacteria. RNA, 15, 327-336.
25. Urbonavič ius, J., Brochier-Armanet, C., Skouloubris, S., Myllykallio, H. and Grosjean, H. (2007) In vitro detection of the enzyme activity of folate-dependent tRNA(U54, C5)methyltransferase. Methods in Enzymology, 425, 103-119.
26. Decatur, W.A. and Fournier, M.J. (2002) rRNA modifications and ribosome function. Trends Biochem. Sci., 27, 344-351. (Pubitemid 34756517)
27. Dennis, P.P., Omer, A. and Lowe, T. (2001) A guided tour: small RNA function in Archaea. Mol Microbiol., 40, 509-519. (Pubitemid 32453106)
28. Tran, E., Brown, J. and Maxwell, E.S. (2004) Evolutionary origins of the RNA-guided nucleotide-modification complexes: from the primitive translation apparatus? Trends Biochem. Sci., 29, 343-350. (Pubitemid 38968750)
29. Bachellerie, J.P. and Cavaille, J. (1997) Guiding ribose methylation of rRNA. Trends Biochem. Sci., 22, 257-261. (Pubitemid 27310946)
30. Kiss, T. (2001) Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs. EMBO J., 20, 3617-3622. (Pubitemid 32691772)
31. Lafontaine, D.L. and Tollervey, D. (1998) Birth of the snoRNPs: the evolution of the modification-guide snoRNAs. Trends Biochem. Sci., 23, 383-388. (Pubitemid 28511378)
32. Bonnerot, C., Pintard, L. and Lutfalla, G. (2003) Functional redundancy of Spb1p and a snR52dependent mechanism for the 20-O-ribose methylation of a conserved rRNA position in yeast. Mol. Cell., 12, 1309-1315. (Pubitemid 37487937)
33. Decatur, W.A. and Schnare, M.N. (2008) Different mechanisms for pseudouridine formation in yeast 5S and 5.8S rRNAs. Mol. Cell Biol., 28, 3089-3100. (Pubitemid 351657076)
34. Purta, E., O'Connor, M., Bujnicki, J.M. and Douthwaite, S. (2009) YgdE is the 2'-O-ribose methyltransferase RlmM specific for nucleotide C2498 in bacterial 23S rRNA. Mol. Microbiol., 72, 1147-1158.
35. 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.
36. Ero, R., Leppik, M., Liiv, A. and Remme, J. (2010) Specificity and kinetics of 23S rRNA modification enzymes RlmH and RluD. RNA, 16, 2075-2084.
37. Helser, T.L., Davies, J.E. and Dahlberg, J.E. (1972) Mechanism of kasugamycin resistance in Escherichia coli. Nat. New Biol., 235, 6-9.
38. Demirci, H., Murphy, F.t., Belardinelli, R., Kelley, A.C., Ramakrishnan, V., Gregory, S.T., Dahlberg, A.E. and Jogl, G. (2010) Modification of 16S ribosomal RNA by the KsgA methyltransferase restructures the 30S subunit to optimize ribosome function. RNA, 16, 2319-2324.
39. Desai, P.M., Culver, G.M. and Rife, J.P. (2011) Site-directed mutants of 16S rRNA reveal important RNA domains for KsgA function and 30S subunit assembly. Biochemistry, 50, 854-863.
40. Demirci, H., Larsen, L.H., Hansen, T., Rasmussen, A., Cadambi, A., Gregory, S.T., Kirpekar, F. and Jogl, G. (2010) Multi-site-specific 16S rRNA methyltransferase RsmF from Thermus thermophilus. RNA, 16, 1584-1596.
41. Johansen, S.K., Maus, C.E., Plikaytis, B.B. and Douthwaite, S. (2006) Capreomycin binds across the ribosomal subunit interface using tlyA-encoded 2'-O-methylations in 16S and 23S rRNAs. Mol. Cell., 23, 173-182. (Pubitemid 44081881)
42. Conrad, J., Sun, D., Englund, N. and Ofengand, J. (1998) The rluC gene of Escherichia coli codes for a pseudouridine synthase that is solely responsible for synthesis of pseudouridine at positions 955, 2504, and 2580 in 23S ribosomal RNA. J. Biol, Chem., 273, 18562-18566. (Pubitemid 28334786)
43. Wrzesinski, J., Nurse, K., Bakin, A., Lane, B.G. and Ofengand, J. (1995) A dual-specificity pseudouridine synthase: an Escherichia coli synthase purified and cloned on the basis of its specificity forψ 746 in 23S RNA is also specific forψ32 in tRNAPhe. RNA, 1, 437-448.
44. Persaud, C., Lu, Y., Vila-Sanjurjo, A., Campbell, J.L., Finley, J. and O'Connor, M. (2010) Mutagenesis of the modified bases, m5U1939 andψ2504, in Escherichia coli 23S rRNA. Biochem. Biophys. Res. Commun., 392, 223-227.
45. Kovaleva, G.Y., Kovaleva, G.Y., Kazanov, M.D., Malko, D.B., Vitreschak, A.G., Sernova, N.V., Gelfand, M.S., Lazarev, V.N., Levitskii, S.A., Basovskii, Y.I. et al. (2007) Acholeplasma laidlawii complete genome. EMBL accession number CP000896.
46. Hsuchen, C.C. and Dubin, D.T. (1980) Methylation patterns of mycoplasma transfer and ribosomal ribonucleic acid. J. Bacteriol., 144, 991-998. (Pubitemid 11219117)
47. Purta, E., O'Connor, M., Bujnicki, J. and Douthwaite, S. (2008) YccW is the m5C methyltransferase specific for 23S rRNA nucleotide 1962. J. Mol. Biol., 383, 641-651.
48. Ny, T., Lindstrom, H.R., Hagervall, T.G. and Björk, G.R. (1988) Purification of transfer RNA m5U54-methyltransferase from Escherichia coli. Association with RNA. Eur. J. Biochem., 177, 467-475.