The flavoprotein Mcap0476 (RlmFO) catalyzes m5U1939 modification in Mycoplasma capricolum 23Ś rRNA

Nucleic Acids Research

Volumn 42, Issue 12, 2014, Pages 8073-8082

  Lartigue, Carole ^a,b   Lebaudy, Anne ^a,b   Blanchard, Alain ^a,b   Yacoubi, Basma El ^c   Rose, Simon ^d   Grosjean, Henri ^e   Douthwaite, Stephen ^d  

^a Univ Bordeaux   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c UNIVERSITY OF FLORIDA   (United States)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^e CENTRE DE GÉNÉTIQUE MOLÉCULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

5,10 METHYLENETETRAHYDROFOLATE REDUCTASE (FADH2); FLAVINE ADENINE NUCLEOTIDE; FLAVOPROTEIN; GENOMIC DNA; METHYL GROUP; RIBOSOME RNA; RNA 23S; S ADENOSYLMETHIONINE; TRANSFER RNA;

ARTICLE; BACTERIAL STRAIN; CATALYSIS; MASS SPECTROMETRY; MYCOPLASMA CAPRICOLUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN SYNTHESIS; RNA METHYLATION; WILD TYPE;

BACTERIAL PROTEINS; BIOCATALYSIS; FLAVOPROTEINS; METHYLATION; METHYLTRANSFERASES; MYCOPLASMA CAPRICOLUM; RNA, RIBOSOMAL, 23S; RNA, TRANSFER; URIDINE;

EID: 84904016412     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku518     Document Type: Article

References (52)

1. Decatur, W.A., Fournier, M.J. (2002) rRNA modifications and ribosome function. Trends Biochem. Sci., 27, 344-351.
2. Grosjean, H. (ed.) (2005) Fine-tuning of RNA Functions by Modification and Editing. Springer Verlag, New York.
3. Machnicka, M.A., Milanowska, K., Osman Oglou, O., Purta, E., Kurkowska, M., Olchowik, A., Januszewski, W., Kalinowski, S., Dunin-Horkawicz, S., Rother, K.M. et al. (2013) MODOMICS: a database of RNA modification pathways - 2013 update. Nucleic Acids Res., 41, D262-D267.
4. 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. BMC Bioinformatics, 4, 41.
5. Motorin, Y., Helm, M. (2011) RNA nucleotide methylation. Wiley Interdis. Rev. RNA, 2, 611-631.
6. Madsen, C.T., Mengel-Jorgensen, J., Kirpekar, F., Douthwaite, S. (2003) Identifying the methyltransferases for m5U747 and m5U1939 in 23S rRNA using MALDI mass spectrometry. Nucleic Acids Res., 31, 4738-4746.
7. Agarwalla, S., Kealey, J.T., Santi, D.V., Stroud, R.M. (2002) Characterization of the 23S ribosomal RNA m5U1939 methyltransferase from Escherichia coli. J. Biol. Chem., 277, 8835-8840.
8. Ny, T., Bjrk, G.R. (1980) Cloning and restriction mapping of the trmA gene coding for transfer ribonucleic acid 5-methyluridine methyltransferase in Escherichia coli K-12. J. Bacteriol., 142, 371-379.
9. Desmolaize, B., Fabret, C., Bregeon, D., Rose, S., Grosjean, H., Douthwaite, S. (2011) A single methyltransferase YefA (RlmCD) catalyses both m5U747 and m5U1939 modifications in Bacillus subtilis 23S rRNA. Nucleic Acids Res., 39, 9368-9375.
10. Urbonavicius, J., Skouloubris, S., Myllykallio, H., 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.
11. Urbonavicius, J., Brochier-Armanet, C., Skouloubris, S., Myllykallio, H., Grosjean, H. (2007) In vitro detection of the enzymatic activity of folate-dependent tRNA uracil-54 C5-methyltransferase: evolutionary implications. Methods Enzymol., 425, 103-119.
12. Delk, A.S., Nagle, D.P., Rabinowitz, J.C. (1980) Methylenetetrahydrofolate-dependent biosynthesis of ribothymidine in transfer RNA of Streptococcus faecalis. Evidence for reduction of the 1-carbon unit by FADH2. J. Biol. Chem., 255, 4387-4390.
13. Nishimasu, H., Ishitani, R., Yamashita, K., Iwashita, C., Hirata, A., Hori, H., Nureki, O. (2009) Atomic structure of a folate/ FAD-dependent tRNA T54 methyltransferase. Proc. Natl. Acad. Sci. U.S.A., 106, 8180-8185.
14. Yamagami, R., Yamashita, K., Nishimasu, H., Tomikawa, C., Ochi, A., Iwashita, C., Hirata, A., Ishitani, R., Nureki, O., Hori, H. (2012) The tRNA recognition mechanism of folate/FAD-dependent tRNA methyltransferase (TrmFO). J. Biol. Chem., 287, 42480-42494.
15. de Crcy-Lagard, V., Marck, C., Brochier-Armanet, C., Grosjean, H. (2007) Comparative RNomics and modomics in Mollicutes: prediction of gene function and evolutionary implications. IUBMB Life, 59, 634-658.
16. Woese, C.R., Stackebrandt, E., Ludwig, W. (1984) What are mycoplasmas: the relationship of tempo and mode in bacterial evolution. J. Mol. Evol., 21, 305-316.
17. Sirand-Pugnet, P., Citti, C., Barre, A., Blanchard, A. (2007) Evolution of mollicutes: down a bumpy road with twists and turns. Res. Microbiol., 158, 754-766.
18. Juhas, M., Eberl, L., Glass, J.I. (2011) Essence of life: essential genes of minimal genomes. Trends Cell Biol., 21, 562-568.
19. Lartigue, C., Glass, J.I., Alperovich, N., Pieper, R., Parmar, P.P., Hutchison, C.A., Smith, H.O., Venter, J.C. (2007) Genome transplantation in bacteria: changing one species to another. Science, 317, 632-638.
20. Montague, M.G., Lartigue, C., Vashee, S. (2012) Synthetic genomics: potential and limitations. Curr. Opin. Biotech., 23, 659-665.
21. Lartigue, C., Vashee, S., Algire, M.A., Chuang, R.Y., Benders, G.A., Ma, L., Noskov, V.N., Denisova, E.A., Gibson, D.G., Assad-Garcia, N. et al. (2009) Creating bacterial strains from genomes that have been cloned and engineered in yeast. Science, 325, 1693-1696.
22. Johnson, L., Hayashi, H., Soll, D. (1970) Isolation and properties of a transfer ribonucleic acid deficient in ribothymidine. Biochemistry, 9, 2823-2831.
23. Hsuchen, C.C., Dubin, D.T. (1980) Methylation patterns of mycoplasma transfer and ribosomal ribonucleic acid. J. Bacteriol., 144, 991-998.
24. Andachi, Y., Yamao, F., Muto, A., Osawa, S. (1989) Codon recognition patterns as deduced from sequences of the complete set of transfer RNA species in Mycoplasma capricolum. Resemblance to mitochondria. J. Mol. Biol., 209, 37-54.
25. Benders, G.A., Noskov, V.N., Denisova, E.A., Lartigue, C., Gibson, D.G., Assad-Garcia, N., Chuang, R.Y., Carrera, W., Moodie, M., Algire, M.A. et al. (2010) Cloning whole bacterial genomes in yeast. Nucleic Acids Res., 38, 2558-2569.
26. Tully, J.G., Whitcomb, R.F., Clark, H.F., Williamson, D.L. (1977) Pathogenic mycoplasmas: cultivation and vertebrate pathogenicity of a new spiroplasma. Science, 195, 892-894.
27. Treco, D.A.,Winston, F. (2008) Growth and manipulation of yeast. Curr. Protoc. Mol. Biol. Ausubel, F.M. et al., Chapter 13, Unit 13 12.
28. Boeke, J.D., LaCroute, F., Fink, G.R. (1984) A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet., 197, 345-346.
29. Kouprina, N., Larionov, V. (2008) Selective isolation of genomic loci from complex genomes by transformation-associated recombination cloning in the yeast Saccharomyces cerevisiae. Nat. Protoc., 3, 371-377.
30. Noskov, V.N., Segall-Shapiro, T.H., Chuang, R.Y. (2010) Tandem repeat coupled with endonuclease cleavage (TREC): a seamless modification tool for genome engineering in yeast. Nucleic Acids Res., 38, 2570-2576.
31. Sikorski, R.S., Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics, 122, 19-27.
32. Gietz, R.D., Schiestl, R.H., Willems, A.R., Woods, R.A. (1995) Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast, 11, 355-360.
33. King, K.W., Dybvig, K. (1994) Transformation of Mycoplasma capricolum and examination of DNA restriction modification in M. capricolum and Mycoplasma mycoides subsp mycoides. Plasmid, 31, 308-311.
34. Andersen, T.E., Porse, B.T., Kirpekar, F. (2004) A novel partial modification at 2501 in Escherichia coli 23S ribosomal RNA. RNA, 10, 907-913.
35. Douthwaite, S., Kirpekar, F. (2007) Identifying modifications in RNA by MALDI mass spectrometry. Methods Enzymol., 425, 3-20.
36. Kirpekar, F., Douthwaite, S., Roepstorff, P. (2000) Mapping posttranscriptional modifications in 5S ribosomal RNA by MALDI mass spectrometry. RNA, 6, 296-306.
37. Giessing, A.M., Jensen, S.S., Rasmussen, A., Hansen, L.H., Gondela, A., Long, K., Vester, B., Kirpekar, F. (2009) Identification of 8-methyladenosine as the modification catalyzed by the radical SAM methyltranferase Cfr that confers antibiotic resistance in bacteria. RNA, 15, 327-336.
38. Hamdane, D., Argentini, M., Cornu, D., Golinelli-Pimpaneau, B., Fontecave, M. (2012) FAD/folate-dependent tRNA methyltransferase: flavin as a new methyl-transfer agent. J. Am. Chem. Soc., 134, 19739-19745.
39. Hamdane, D., Argentini, M., Cornu, D., Myllykallio, H., Skouloubris, S., Hui-Bon-Hoa, G., Golinelli-Pimpaneau, B. (2011) Insights into folate/FAD-dependent tRNA methyltransferase mechanism: role of two highly conserved cysteines in catalysis. J. Biol. Chem., 286, 36268-36280.
40. Purta, E., Kaminska, K.H., Kasprzak, J.M., Bujnicki, J.M., Douthwaite, S. (2008) YbeA is the m3' methyltransferase RlmH that targets nucleotide 1915 in 23S rRNA. RNA, 14, 2234-2244.
41. Bjrk, G.R., Neidhardt, F.C. (1975) Physiological and biochemical studies on the function of 5-methyluridine in the transfer ribonucleic acid of Escherichia coli. J. Bacteriol., 124, 99-111.
42. Bujnicki, J.M., Feder, M., Ayres, C.L., Redman, K.L. (2004) Sequence-structure-function studies of tRNA:m5C methyltransferase Trm4p and its relationship to DNA:m5C and RNA:m5U methyltransferases. Nucleic Acids Res., 32, 2453-2463.
43. Hur, S., Stroud, R.M., Finer-Moore, J. (2006) Substrate recognition by RNA 5-methyluridine methyltransferases and pseudouridine synthases: a structural perspective. J. Biol. Chem., 281, 38969-38973.
44. Persaud, C., Lu, Y., Vila-Sanjurjo, A., Campbell, J.L., Finley, J., O'Connor, M. (2010) Mutagenesis of the modified bases, m5U1939 and-2504, in Escherichia coli 23S rRNA. Biochem. Biophys. Res. Comm., 392, 223-227.
45. Chan, C.T., Dyavaiah, M., DeMott, M.S., Taghizadeh, K., Dedon, P.C., Begley, T.J. (2010) A quantitative systems approach reveals dynamic control of tRNA modifications during cellular stress. PLoS Genet., 6, e1001247.
46. Helm, M., Alfonzo, J.D. (2014) Posttranscriptional RNA modifications: playing metabolic games in a cell's chemical Legoland. Chem. Biol., 21, 174-185.
47. Armengod, M.E., Moukadiri, I., Prado, S., Ruiz-Partida, R., Benitez-Paez, A., Villarroya, M., Lomas, R., Garzon, M.J., Martinez-Zamora, A., Meseguer, S. et al. (2012) Enzymology of tRNA modification in the bacterial MnmEG pathway. Biochimie, 94, 1510-1520.
48. Grosjean, H., Breton, M., Sirand-Pugnet, P., Tardy, F., Thiaucourt, F., Citti, C., Barre, A., Yoshizawa, S., Fourmy, D., de Crcy-Lagard, V. et al. (2014) Predicting the minimal translation apparatus: lessons from the reductive evolution of mollicutes. PLoS Genet., 10, e1004363.
49. Larsen, L.H., Rasmussen, A., Giessing, A.M., Jogl, G., Kirpekar, F. (2012) Identification and characterization of the Thermus thermophilus 5-methylcytidine (m5C) methyltransferase modifying 23S rRNA base C1942. J. Biol. Chem., 287, 27593-27600.
50. Purta, E., O'Connor, M., Bujnicki, J., Douthwaite, S. (2008) YccW is the m5C methyltransferase specific for 23S rRNA nucleotide 1962. J. Mol. Biol., 383, 641-651.
51. Ofengand, J., Del Campo, M. (2005) In: Bck, A, Curtis, R, Kaper, JB, Neidhardt, T, Nystrm, T and Squires, C (eds.). Escherichia coli and Salmonella. ASM Press, Washington, DC. http://www.ecosal.org, pp. 4.6.1.
52. Purta, E., O'Connor, M., Bujnicki, J.M., Douthwaite, S. (2009) YgdE is the 2'-O-ribose methyltransferase RlmM specific for nucleotide C2498 in bacterial 23S rRNA. Mol. Microbiol., 72, 1147-1158.