YccW is the m5C Methyltransferase Specific for 23S rRNA Nucleotide 1962

Journal of Molecular Biology

Volumn 383, Issue 3, 2008, Pages 641-651

  Purta, Elzbieta ^a,b   O'Connor, Michelle ^a,c   Bujnicki, Janusz M ^b,d   Douthwaite, Stephen ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^c UNIVERSITY COLLEGE CORK   (Ireland)

^d INSTITUTE OF MOLECULAR PHYSICS   (Poland)

Author keywords

ribosomal subunit interface; RlmI; RNA mass spectrometry; rRNA methylation

Indexed keywords

PROTEIN YCCW; RECOMBINANT PROTEIN; RNA 23S; RNA METHYLTRANSFERASE; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; M(5)C RRNA METHYLTRANSFERASE; METHYLTRANSFERASE; NUCLEOTIDE;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE INACTIVATION; GROWTH RATE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METHYLATION; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; ENZYMOLOGY; GENETIC COMPLEMENTATION; GENETICS; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

AMINO ACID SEQUENCE; BASE SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENETIC COMPLEMENTATION TEST; METHYLATION; METHYLTRANSFERASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; NUCLEOTIDES; PROTEIN STRUCTURE, TERTIARY; RNA, RIBOSOMAL, 23S; SEQUENCE ALIGNMENT; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUBSTRATE SPECIFICITY;

EID: 52949109757     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.08.061     Document Type: Article

References (57)

1. Noller H.F. RNA structure: reading the ribosome. Science 309 (2005) 1508-1514
2. Grosjean H. Fine-tuning of RNA functions by modification and editing. In: Hohmann S. (Ed). Topics in Current Genetics vol. 12 (2005), Springer Verlag, New York, NY
3. Rozenski J., Crain P., Crain P.F., and McCloskey J.A. The RNA Modification Database: 1999 update. Nucleic Acids Res. 27 (1999) 196-197
4. Dunin-Horkawicz S., Czerwoniec A., Gajda M., Czerwoniec A., Gajda M.J., Feder M., et al. MODOMICS: a database of RNA modification pathways. Nucleic Acids Res. 34 (2006) D145-D149
5. 5C methyltransferase specific for 16S rRNA nucleotide 1407. J. Mol. Biol. 359 (2006) 777-786
6. Lafontaine D.L., and Tollervey D. Birth of the snoRNPs: the evolution of the modification-guide snoRNAs. Trends Biochem. Sci. 23 (1998) 383-388
7. Kiss T. Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs. EMBO J. 20 (2001) 3617-3622
8. Tran E., Brown J., and Maxwell E.S. Evolutionary origins of the RNA-guided nucleotide-modification complexes: from the primitive translation apparatus?. Trends Biochem. Sci. 29 (2004) 343-350
9. Ofengand J., and Del Campo M. Modified nucleotides of Escherichia coli ribosomal RNA. In: Curtiss R. (Ed). EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology (2004), ASM Press, Washington, DC. http://www.ecosal.org http://www.ecosal.org.
10. Sergiev P.V., Bogdanov A.A., and Dontsova O.A. Ribosomal RNA guanine-(N2)-methyltransferases and their targets. Nucleic Acids Res. 35 (2007) 2295-2301
11. 5C967 methyltransferase from Escherichia coli. Biochemistry 38 (1999) 4053-4057
12. 5C967 methyltransferase from Escherichia coli. Biochemistry 38 (1999) 1884-1892
13. 5C methyltransferases from searching genomic and proteomic sequences. Nucleic Acids Res. 27 (1999) 3138-3145
14. Kagan R.M., and Clarke S. Widespread occurrence of three sequence motifs in diverse S-adenosylmethionine-dependent methyltransferases suggests a common structure for these enzymes. Arch. Biochem. Biophys. 310 (1994) 417-427
15. Malone T., Blumenthal R.M., and Cheng X. Structure-guided analysis reveals nine sequence motifs conserved among DNA amino-methyltransferases, and suggests a catalytic mechanism for these enzymes. J. Mol. Biol. 253 (1995) 618-632
16. Fauman E.B., Cheng X., and Blumenthal R.M. Structure and evolution of AdoMet-dependent methyltransferases. In: Cheng X., and Blumenthal R.M. (Eds). S-Adenosylmethionine-Dependent Methyltransferases: Structures and Functions (1999), World Scientific, River Edge, NJ 1-32
17. 5U methyltransferases. Nucleic Acids Res. 32 (2004) 2453-2463
18. Tkaczuk K.L., Dunin-Horkawicz S., Purta E., and Bujnicki J.M. Structural and evolutionary bioinformatics of the SPOUT superfamily of methyltransferases. BMC Bioinformatics 8 (2007) 73
19. Pioszak A.A., Murayama K., Nakagawa N., Ebihara A., Kuramitsu S., Shirouzu M., and Yokoyama S. Structures of a putative RNA 5-methyluridine methyltransferase, Thermus thermophilus TTHA1280, and its complex with S-adenosyl-l-homocysteine. Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun. 61 (2005) 867-874
20. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2 (2006) 2006-2008
21. Kurowski M.A., and Bujnicki J.M. GeneSilico protein structure prediction meta-server. Nucleic Acids Res. 31 (2003) 3305-3307
22. Sun W., Xu X., Pavlova M., Edwards A.M., Joachimiak A., Savchenko A., and Christendat D. The crystal structure of a novel SAM-dependent methyltransferase PH1915 from Pyrococcus horikoshii. Protein Sci. 14 (2005) 3121-3128
23. 2G methyltransferases: I. The ycbY gene encodes a methyltransferase specific for G2445 of the 23S rRNA. J. Mol. Biol. 364 (2006) 20-25
24. Aravind L., and Koonin E.V. THUMP-a predicted RNA-binding domain shared by 4-thiouridine, pseudouridine synthases and RNA methylases. Trends Biochem. Sci. 26 (2001) 215-217
25. Lee T.T., Agarwalla S., and Stroud R.M. A unique RNA fold in the RumA-RNA-cofactor ternary complex contributes to substrate selectivity and enzymatic function. Cell 120 (2005) 599-611
26. 5C DNA methyl transferases use different cysteine residues as catalysts. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 8263-8265
27. 5U1939 methyltransferase from Escherichia coli. J. Biol. Chem. 277 (2002) 8835-8840
28. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., and Cate J.H. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310 (2005) 827-834
29. Selmer M., Dunham C.M., Murphy F.V., Weixlbaumer A., Petry S., Kelley A.C., et al. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313 (2006) 1935-1942
30. Brimacombe R., Mitchell P., Osswald M., Stade K., and Bochkariov D. Clustering of modified nucleotides at the functional center of bacterial ribosomal RNA. FASEB J. 7 (1993) 161-167
31. Decatur W.A., and Fournier M.J. rRNA modifications and ribosome function. Trends Biochem. Sci. 27 (2002) 344-351
32. Hansen M.A., Kirpekar F., Ritterbusch W., and Vester B. Posttranscriptional modifications in the A-loop of 23S rRNAs from selected archaea and eubacteria. RNA 8 (2002) 202-213
33. Ban N., Nissen P., Hansen J., Moore P.B., and Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289 (2000) 905-920
34. Harms J., Schluenzen F., Zarivach R., Bashan A., Gat S., Agmon I., et al. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107 (2001) 679-688
35. Korostelev A., Trakhanov S., Laurberg M., and Noller H.F. Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 126 (2006) 1065-1077
36. Leppik M., Peil L., Kipper K., Liiv A., and Remme J. Substrate specificity of the pseudouridine synthase RluD in Escherichia coli. FEBS J. 274 (2007) 5759-5766
37. Vaidyanathan P.P., Deutscher M.P., and Malhotra A. RluD, a highly conserved pseudouridine synthase, modifies 50S subunits more specifically and efficiently than free 23S rRNA. RNA 13 (2007) 1868-1876
38. Sunita S., Purta E., Tkaczuk K.L., Douthwaite S., Bujnicki J.M., and Sivaraman J. Crystal structure of the methyltransferase YccW (RlmI) from Escherichia coli. J. Mol. Biol., (2008) following article, JMB-D-08-00716
39. .Ero, R., Peil, L., Liiv, A. & Remme, J. (2008). Identification of pseudouridine methyltransferase in Escherichia coli. RNA, published on-line ahead of press, August 28, 2008, doi:10.1261/rna.1186608.
40. 3Ψ methyltransferase RlmH that targets nucleotide 1915 in 23S rRNA. RNA, published on-line ahead of press, August 28, 2008, doi:10.1261/rna.1198108.
41. 5C967 by their respective methyltransferases. Nucleic Acids Res. 19 (1991) 7089-7095
42. Schlünzen F., Tocilj A., Zarivach R., Harms J., Gluehmann M., Janell D., et al. Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell 102 (2000) 615-623
43. Wimberly B.T., Brodersen D.E., Clemons W.M.J., Morgan-Warren R.J., Carter A.P., Vonrhein C., et al. Structure of the 30S ribosomal subunit. Nature 407 (2000) 327-339
44. 5C methyltransferase YebU from Escherichia coli reveals a C-terminal RNA-recruiting PUA. J. Mol. Biol. 360 (2006) 774-787
45. Perez-Arellano I., Gallego J., and Cervera J. The PUA domain-a structural and functional overview. FEBS J. 274 (2007) 4972-4984
46. Bujnicki J.M. Phylogenomic analysis of 16S rRNA:(guanine-N2) methyltransferases suggests new family members and reveals highly conserved motifs and a domain structure similar to other nucleic acid amino-methyltransferases. FASEB J. 14 (2000) 2365-2368
47. Das G., Thotala D.K., Kapoor S., Karunanithi S., Thakur S.S., Singh N.S., and Varshney U. Role of 16S ribosomal RNA methylations in translation initiation in Escherichia coli. EMBO J. 27 (2008) 840-851
48. Bujnicki J.M., Droogmans L., Grosjean H., Purushothaman S.K., and Lapeyre B. Bioinformatics-guided identification and experimental characterization of novel RNA methyltransferases. In: Bujnicki J.M. (Ed). Practical Bioinformatics vol. 15 (2004), Springer Verlag, Berlin, Germany 139-168
49. Saka K., Tadenuma M., Nakade S., Tanaka N., Sugawara H., Nishikawa K., et al. A complete set of Escherichia coli open reading frames in mobile plasmids facilitating genetic studies. DNA Res. 12 (2005) 63-68
50. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd edit. (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
51. Gutgsell N., Englund N., Niu L., Kaya Y., Lane B.G., and Ofengand J. Deletion of the Escherichia coli pseudouridine synthase gene truB blocks formation of pseudouridine 55 in tRNA in vivo, does not affect exponential growth, but confers a strong selective disadvantage in competition with wild-type cells. RNA 6 (2000) 1870-1881
52. Toh S.-M., Xiong L., Bae T., and Mankin A.S. The methyltransferase YfgB/RlmN is responsible for modification of adenosine 2503 in 23S rRNA. RNA 14 (2008) 98-106
53. Andersen T.E., Porse B.T., and Kirpekar F. A novel partial modification at C2501 in Escherichia coli 23S ribosomal RNA. RNA 10 (2004) 907-913
54. Douthwaite S., and Kirpekar F. Identifying modifications in RNA by MALDI mass spectrometry. Methods Enzymol. 425 (2007) 1-20
55. Kirpekar F., Douthwaite S., and Roepstorff P. Mapping posttranscriptional modifications in 5S ribosomal RNA by MALDI mass spectrometry. RNA 6 (2000) 296-306
56. Kirpekar F., and Krogh T.N. RNA fragmentation studied in a matrix-assisted laser desorption/ionisation tandem quadropole/orthogonal time-of-flight mass spectrometer. Rapid Commun. Mass Spec. 15 (2001) 8-14
57. Douthwaite S., Powers T., Lee J.Y., and Noller H.F. Defining the structural requirements for a helix in 23S ribosomal RNA that confers erythromycin resistance. J. Mol. Biol. 209 (1989) 655-665