Structural insights into the function of aminoglycoside-resistance A1408 16S rRNA methyltransferases from antibiotic-producing and human pathogenic bacteria

Nucleic Acids Research

Volumn 38, Issue 21, 2010, Pages 7791-7799

  MacMaster, Rachel ^a,b   Zelinskaya, Natalia ^a   Savic, Miloje ^a   Rankin, C Robert ^a   Conn, Graeme L ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGLYCOSIDE; BACTERIAL PROTEIN; METHYLTRANSFERASE; NEBRAMYCIN; PROTEIN KAMB; PROTEIN NPMA; PROTEIN RMTB; PROTEIN SGM; RIBOSOME RNA; RNA 16S; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM; BETA SHEET; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ESCHERICHIA COLI; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN METHYLATION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; STREPTOALLOTEICHUS TENEBRARIUS; STRUCTURE ANALYSIS;

ACTINOMYCETALES; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, MICROBIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; METHYLTRANSFERASES; MODELS, MOLECULAR; PROTEIN BINDING; S-ADENOSYLHOMOCYSTEINE; S-ADENOSYLMETHIONINE; SEQUENCE ANALYSIS, PROTEIN; SUBSTRATE SPECIFICITY; TRNA METHYLTRANSFERASES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; STREPTOALLOTEICHUS;

EID: 78649839859     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq627     Document Type: Article

References (33)

1. Jana, S. and Deb, J. K. (2006) Molecular understanding of aminoglycoside action and resistance. Appl. Microbiol. Biotechnol., 70, 140-150.
2. Noller, H. F. (1991) Ribosomal RNA and translation. Annu. Rev. Biochem., 60, 191-227.
3. Savic, M., Lovric, J., Tomic, T. I., Vasiljevic, B. and Conn, G. L. (2009) Determination of the target nucleosides for members of two families of 16S rRNA methyltransferases that confer resistance to partially overlapping groups of aminoglycoside antibiotics. Nucleic Acids Res., 37, 5420-5431.
4. Cundliffe, E. (1989) How antibiotic-producing organisms avoid suicide. Annu. Rev. Microbiol., 43, 207-233.
5. Long, K. S. and Vester, B. (2009) Antibiotic resistance in bacteria caused by modified nucleosides in 23S ribosomal RNA. In Grosjean, H. (ed. ), DNA and RNA Modification Enzymes: Comparative Structure, Mechanism, Functions, Cellular Interactions and Evolution. Landes Bioscience, Austin, TX, pp. 537-549.
6. Conn, G. L., Savic, M. and Macmaster, R. (2009) Antibiotic resistance in bacteria through modification of nucleosides in 16S ribosomal RNA. In Grosjean, H. (ed. ), DNA and RNA Modification Enzymes: Comparative Structure, Mechanism, Functions, Cellular Interactions and Evolution. Landes Bioscience, Austin, TX, pp. 524-536.
7. Gaynor, M. and Mankin, A. S. (2003) Macrolide antibiotics: binding site, mechanism of action, resistance. Curr. Top. Med. Chem., 3, 949-960.
8. Doi, Y. and Arakawa, Y. (2007) 16S ribosomal RNA methylation: emerging resistance mechanism against aminoglycosides. Clin. Infect. Dis., 45, 88-94.
9. Wachino, J., Shibayama, K., Kurokawa, H., Kimura, K., Yamane, K., Suzuki, S., Shibata, N., Ike, Y. and Arakawa, Y. (2007) Novel plasmid-mediated 16S rRNA m1A1408 methyltransferase, NpmA, found in a clinically isolated Escherichia coli strain resistant to structurally diverse aminoglycosides. Antimicrob. Agents Chemother., 51, 4401-4409.
10. Koscinski, L., Feder, M. and Bujnicki, J. M. (2007) Identification of a missing sequence and functionally important residues of 16S rRNA: m(1)A1408 methyltransferase KamB that causes bacterial resistance to aminoglycoside antibiotics. Cell Cycle, 6, 1268-1271.
11. Schubert, H. L., Blumenthal, R. M. and Cheng, X. D. (2003) Many paths to methyltransfer: a chronicle of convergence. Trends Biochem. Sci., 28, 329-335.
12. Felnagle, E. A., Rondon, M. R., Berti, A. D., Crosby, H. A. and Thomas, M. G. (2007) Identification of the biosynthetic gene cluster and an additional gene for resistance to the antituberculosis drug capreomycin. Appl. Environ. Microbiol., 73, 4162-4170.
13. Zhao, J. Y., Xia, Z. J., Sun, X., Zhong, L., Jiang, D. M., Liu, H., Wang, J., Qin, Z. J. and Li, Y. Z. (2008) Cloning and characterization of an rRNA methyltransferase from Sorangium cellulosum. Biochem. Biophys. Res. Comm., 370, 140-144.
14. Holmes, D. J., Drocourt, D., Tiraby, G. and Cundliffe, E. (1991) Cloning of an aminoglycoside-resistance-encoding gene, kamC, from Saccharopolyspora hirsuta: comparison with kamB from Streptomyces tenebrarius. Gene, 102, 19-26.
15. Tamura, T., Ishida, Y., Otoguro, M., Hatano, K. and Suzuki, K. (2008) Classification of 'Streptomyces tenebrarius' Higgins and Kastner as Streptoalloteichus tenebrarius nom. rev., comb. nov., and emended description of the genus Streptoalloteichus. Int. J. Syst. Evol. Microbiol., 58, 688-691.
16. Schmitt, E., Galimand, M., Panvert, M., Courvalin, P. and Mechulam, Y. (2009) Structural bases for 16S rRNA methylation catalyzed by ArmA and RmtB methyltransferases. J. Mol. Biol., 388, 570-582.
17. Husain, N., Tkaczuk, K. L., Tulsidas, S. R., Kaminska, K. H., Cubrilo, S., Maravic-Vlahovicek, G., Bujnicki, J. M. and Sivaraman, J. (2010) Structural basis for the methylation of G1405 in 16S rRNA by aminoglycoside resistance methyltransferase Sgm from an antibiotic producer: a diversity of active sites in m7G methyltransferases. Nucleic Acids Res., doi:10. 1093/nar/gkq1122.
18. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods in Enzymology, 276, 307-326.
19. Zwart, P. H., Afonine, P. V., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., McKee, E., Moriarty, N. W., Read, R. J., Sacchettini, J. C. et al. (2008) Automated structure solution with the PHENIX suite. Methods Mol. Biol., 426, 419-435.
20. 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.
21. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr., D60, 2126-2132.
22. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C. and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr., 40, 658-674.
23. Adams, P. D., Gopal, K., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Pai, R. K., Read, R. J., Romo, T. D. et al. (2004) Recent developments in the PHENIX software for automated crystallographic structure determination. J. Synchrotron. Radiat., 11, 53-55.
24. Painter, J. and Merritt, E. A. (2006) TLSMD web server for the generation of multi-group TLS models. J. Appl. Crystallogr., 39, 109-111.
25. Holm, L. and Sander, C. (1995) Dali: a network tool for protein structure comparison. Trends Biochem Sci, 20, 478-480.
26. De Vries, S. J., van Dijk, A. D., Krzeminski, M., van Dijk, M., Thureau, A., Hsu, V., Wassenaar, T. and Bonvin, A. M. (2007) HADDOCK versus HADDOCK: new features and performance of HADDOCK2. 0 on the CAPRI targets. Proteins, 69, 726-733.
27. Dunstan, M. S., Hang, P. C., Zelinskaya, N. V., Honek, J. F. and Conn, G. L. (2009) Structure of the thiostrepton resistance methyltransferase-S- adenosyl-L-methionine complex and its interaction with ribosomal RNA. J. Biol. Chem., 284, 17013-17020.
28. Douthwaite, S., Fourmy, D. and Yoshizawa, S. (2005) In Grosjean, H. (ed. ), Fine-Tuning of RNA Funtions by Modification and Editing, Vol. 12. Springer-Verlag, Berlin, pp. 285-307.
29. Krishnamurthy, N., Brown, D. and Sjolander, K. (2007) FlowerPower: clustering proteins into domain architecture classes for phylogenomic inference of protein function. BMC Evol. Biol., 7(Suppl. 1), S12.
30. Savic, M., Ilic-Tomic, T., Macmaster, R., Vasiljevic, B. and Conn, G. L. (2008) Critical residues for cofactor binding and catalytic activity in the aminoglycoside resistance methyltransferase Sgm. J. Bacteriol., 190, 5855-5861.
31. Vlahovicek, G. M., Cubrilo, S., Tkaczuk, K. L. and Bujnicki, J. M. (2008) Modeling and experimental analyses reveal a two-domain structure and amino acids important for the activity of aminoglycoside resistance methyltransferase Sgm. Biochim. Biophys. Acta, Proteins Proteomics, 1784, 582-590.
32. Cheng, X. and Blumenthal, R. M. (2002) Cytosines do it, thymines do it, even pseudouridines do it - base flipping by an enzyme that acts on RNA. Structure, 10, 127-129.
33. O'gara, M., Horton, J. R., Roberts, R. J. and Cheng, X. D. (1998) Structures of Hhal methyltransferase complexed with substrates containing mismatches at the target base. Nat. Struct. Biol., 5, 872-877.