Expansion of the aminoglycoside-resistance 16S rRNA (m1A1408) methyltransferase family: Expression and functional characterization of four hypothetical enzymes of diverse bacterial origin

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1844, Issue 9, 2014, Pages 1648-1655

  Witek, Marta A ^a   Conn, Graeme L ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antibiotic resistance; Bacteria; Methylation; Ribosomal RNA; S Adenosyl L methionine; S Adenosylhomocysteine

Indexed keywords

AMINOGLYCOSIDE; ANTIINFECTIVE AGENT; RNA 16S; RNA METHYLTRANSFERASE; S ADENOSYLHOMOCYSTEINE; S ADENOSYLMETHIONINE;

ARTICLE; BACTERIAL STRAIN; BACTERIUM; BINDING AFFINITY; CANDIDATUS ARTHROMITUS; CATENULISPORA ACIDIPHILA; CIRCULAR DICHROISM; CLONING; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MODIFICATION; GENE SEQUENCE; METHYLATION; MINIMUM INHIBITORY CONCENTRATION; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION; THERMOMONOSPORA CURVATA;

ANTIBIOTIC RESISTANCE; BACTERIA; METHYLATION; RIBOSOMAL RNA; S-ADENOSYL-L-METHIONINE; S-ADENOSYLHOMOCYSTEINE;

ACTINOBACTERIA; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CLOSTRIDIUM; ESCHERICHIA COLI; GENE EXPRESSION; GENES, RRNA; METHYLTRANSFERASES; MICROBIAL SENSITIVITY TESTS; MULTIGENE FAMILY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; RNA, RIBOSOMAL, 16S;

EID: 84904016062     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2014.06.012     Document Type: Article

References (33)

1. H.K. Allen, J. Donato, H.H. Wang, K.A. Cloud-Hansen, J. Davies, and J. Handelsman Call of the wild: antibiotic resistance genes in natural environments Nat. Rev. Microbiol. 8 2010 251 259
2. D.N. Wilson Ribosome-targeting antibiotics and mechanisms of bacterial resistance Nat. Rev. Microbiol. 12 2014 35 48
3. J. Poehlsgaard, and S. Douthwaite The bacterial ribosome as a target for antibiotics Nat. Rev. Microbiol. 3 2005 870 881
4. E. Durante-Mangoni, A. Grammatikos, R. Utili, and M.E. Falagas Do we still need the aminoglycosides? Int. J. Antimicrob. Agents 33 2009 201 205
5. G.D. Wright Aminoglycoside-modifying enzymes Curr. Opin. Microbiol. 2 1999 499 503
6. M.S. Ramirez, and M.E. Tolmasky Aminoglycoside modifying enzymes Drug Resist. Updat. 13 2010 151 171
7. J. Wachino, and Y. Arakawa Exogenously acquired 16S rRNA methyltransferases found in aminoglycoside-resistant pathogenic Gram-negative bacteria: an update Drug Resist. Updat. 15 2012 133 148
8. J. Jackson, C. Chen, and K. Buising Aminoglycosides: how should we use them in the 21st century? Curr. Opin. Infect. Dis. 26 2013 516 525
9. E. Cundliffe How antibiotic-producing organisms avoid suicide Annu. Rev. Microbiol. 43 1989 207 233
10. A.A. Beauclerk, and E. Cundliffe Sites of action of two ribosomal RNA methylases responsible for resistance to aminoglycosides J. Mol. Biol. 193 1987 661 671
11. E. Cundliffe Resistance to macrolides and lincosamides in Streptomyces lividans and to aminoglycosides in Micromonospora purpurea Gene 115 1992 75 84
12. S. Magnet, and J.S. Blanchard Molecular insights into aminoglycoside action and resistance Chem. Rev. 105 2005 477 498
13. G.L. Conn, M. Savic, and R. Macmaster Antibiotic resistance in bacteria through modification of nucleosides in 16S ribosomal RNA H. Grojean, DNA and RNA Modification Enzymes: Comparative Structure, Mechanism, Functions, Cellular Interactions and Evolution 2009 Landes Bioscience Austin, TX 524 536
14. M. Savic, J. Lovric, T.I. Tomic, B. Vasiljevic, and G.L. Conn 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 2009 5420 5431
15. H. Ochman, J.G. Lawrence, and E.A. Groisman Lateral gene transfer and the nature of bacterial innovation Nature 405 2000 299 304
16. R. Benveniste, and J. Davies Mechanisms of antibiotic resistance in bacteria Annu. Rev. Biochem. 42 1973 471 506
17. G.D. Wright Antibiotic resistance in the environment: a link to the clinic? Curr. Opin. Microbiol. 13 2010 589 594
18. V.M. D'Costa, C.E. King, L. Kalan, M. Morar, W.W. Sung, C. Schwarz, D. Froese, G. Zazula, F. Calmels, R. Debruyne, G.B. Golding, H.N. Poinar, and G.D. Wright Antibiotic resistance is ancient Nature 477 2011 457 461
19. N. Husain, S. Obranic, L. Koscinski, J. Seetharaman, F. Babic, J.M. Bujnicki, G. Maravic-Vlahovicek, and J. Sivaraman Structural basis for the methylation of A1408 in 16S rRNA by a panaminoglycoside resistance methyltransferase NpmA from a clinical isolate and analysis of the NpmA interactions with the 30S ribosomal subunit Nucleic Acids Res. 39 2011 1903 1918
20. R. Macmaster, N. Zelinskaya, M. Savic, C.R. Rankin, and G.L. Conn Structural insights into the function of aminoglycoside-resistance A1408 16S rRNA methyltransferases from antibiotic-producing and human pathogenic bacteria Nucleic Acids Res. 38 2010 7791 7799
21. J.A. Dunkle, K. Vinal, P.M. Desai, N. Zelinskaya, M. Savic, D.M. West, G.L. Conn, and C.M. Dunham Molecular recognition and modification of the 30S ribosome by the aminoglycoside-resistance methyltransferase NpmA Proc. Natl. Acad. Sci. U. S. A. 111 2014 6275 6280
22. J.L. Martin, and F.M. McMillan SAM (dependent) I AM: the S-adenosylmethionine-dependent methyltransferase fold Curr. Opin. Struct. Biol. 12 2002 783 793
23. N. Zelinskaya, C.R. Rankin, R. Macmaster, M. Savic, and G.L. Conn Expression, purification and crystallization of adenosine 1408 aminoglycoside-resistance rRNA methyltransferases for structural studies Protein Expr. Purif. 75 2011 89 94
24. W.M. Clemons Jr., D.E. Brodersen, J.P. McCutcheon, J.L. May, A.P. Carter, R.J. Morgan-Warren, B.T. Wimberly, and V. Ramakrishnan Crystal structure of the 30 S ribosomal subunit from Thermus thermophilus: purification, crystallization and structure determination J. Mol. Biol. 310 2001 827 843
25. L. Whitmore, and B.A. Wallace Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases Biopolymers 89 2008 392 400
26. S.M. Kelly, T.J. Jess, and N.C. Price How to study proteins by circular dichroism Biochim. Biophys. Acta 1751 2005 119 139
27. D.J. Holmes, D. Drocourt, G. Tiraby, and E. Cundliffe Cloning of an aminoglycoside-resistance-encoding gene, kamC, from Saccharopolyspora hirsuta: comparison with kamB from Streptomyces tenebrarius Gene 102 1991 19 26
28. E.A. Felnagle, M.R. Rondon, A.D. Berti, H.A. Crosby, and M.G. Thomas Identification of the biosynthetic gene cluster and an additional gene for resistance to the antituberculosis drug capreomycin Appl. Environ. Microbiol. 73 2007 4162 4170
29. J. Wachino, K. Shibayama, H. Kurokawa, K. Kimura, K. Yamane, S. Suzuki, N. Shibata, Y. Ike, and Y. Arakawa 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 2007 4401 4409
30. J.Y. Zhao, Z.J. Xia, X. Sun, L. Zhong, D.M. Jiang, H. Liu, J. Wang, Z.J. Qin, and Y.Z. Li Cloning and characterization of an rRNA methyltransferase from Sorangium cellulosum Biochem. Biophys. Res. Commun. 370 2008 140 144
31. N.J. Greenfield Methods to estimate the conformation of proteins and polypeptides from circular dichroism data Anal. Biochem. 235 1996 1 10
32. H. McWilliam, W. Li, M. Uludag, S. Squizzato, Y.M. Park, N. Buso, A.P. Cowley, and R. Lopez Analysis tool web services from the EMBL-EBI Nucleic Acids Res. 41 2013 W597 W600
33. K. Katoh, and H. Toh Recent developments in the MAFFT multiple sequence alignment program Brief. Bioinform. 9 2008 286 298