Molecular recognition and modification of the 30S ribosome by the aminoglycoside-resistance methyltransferase NpmA

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 17, 2014, Pages 6275-6280

  Dunkle, Jack A ^a   Vinal, Kellie ^a   Desai, Pooja M ^a   Zelinskaya, Natalia ^a   Savic, Miloje ^a   West, Dayne M ^a   Conn, Graeme L ^a   Dunham, Christine M ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antibiotic resistance; Base flipping; RNA modification

Indexed keywords

AMINOGLYCOSIDE; METHYLTRANSFERASE; RIBOSOME RNA; RNA 16S; SINEFUNGIN;

ARTICLE; BIOGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MODIFICATION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; RIBOSOME; RNA METHYLATION; RNA STRUCTURE; SITE DIRECTED MUTAGENESIS;

ANTIBIOTIC RESISTANCE; BASE FLIPPING; RNA MODIFICATION;

ADENOSINE; AMINO ACIDS; AMINOGLYCOSIDES; BIOCATALYSIS; CATALYTIC DOMAIN; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE TRANSFER, HORIZONTAL; METHYLATION; METHYLTRANSFERASES; MODELS, MOLECULAR; NUCLEOTIDES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RNA, RIBOSOMAL, 16S; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84899634018     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1402789111     Document Type: Article

References (39)

1. Wilson DN (2014) Ribosome-targeting antibiotics and mechanisms of bacterial resistance. Nat Rev Microbiol 12(1):35-48.
2. Franceschi F (2007) Back to the future: The ribosome as an antibiotic target. Future Microbiol 2(6):571-574.
3. Moazed D, Noller HF (1987) Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature 327(6121):389-394.
4. Davies J, Gorini L, Davis BD (1965) Misreading of RNA codewords induced by aminoglycoside antibiotics. Mol Pharmacol 1(1):93-106.
5. Fourmy D, Recht MI, Blanchard SC, Puglisi JD (1996) Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic. Science 274(5291):1367-1371.
6. Carter AP, et al. (2000) Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407(6802):340-348.
7. Vicens Q, Westhof E (2002) Crystal structure of a complex between the aminoglycoside tobramycin and an oligonucleotide containing the ribosomal decoding a site. Chem Biol 9(6):747-755.
8. Ogle JM, et al. (2001) Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292(5518):897-902.
9. Falagas ME, Grammatikos AP, Michalopoulos A (2008) Potential of old-generation antibiotics to address current need for new antibiotics. Expert Rev Anti Infect Ther 6(5):593-600.
10. Jackson J, Chen C, Buising K (2013) Aminoglycosides: How should we use them in the 21st century? Curr Opin Infect Dis 26(6):516-525.
11. Ramirez MS, Tolmasky ME (2010) Aminoglycoside modifying enzymes. Drug Resist Updat 13(6):151-171.
12. Conn GL, Savic M, Macmaster R (2009) Resistance to antibiotics in bacteria through modification of nucleosides in 16S ribosomal RNA. DNA and RNA Modification Enzymes: Comparative Structure, Mechanism, Functions, Cellular Interactions and Evolution, ed Grosjean H (Landes Bioscience, Austin, TX).
13. Wachino J, Arakawa Y (2012) Exogenously acquired 16S rRNA methyltransferases found in aminoglycoside-resistant pathogenic Gram-negative bacteria: An update. Drug Resist Updat 15(3):133-148.
14. Schmitt E, Galimand M, Panvert M, Courvalin P, Mechulam Y (2009) Structural bases for 16 S rRNA methylation catalyzed by ArmA and RmtB methyltransferases. J Mol Biol 388(3):570-582.
15. Macmaster R, Zelinskaya N, Savic M, Rankin CR, Conn GL (2010) Structural insights into the function of aminoglycoside-resistance A1408 16S rRNA methyltransferases from antibioticproducing and human pathogenic bacteria. Nucleic Acids Res 38(21):7791-7799.
16. Husain N, et al. (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 38(12):4120-4132.
17. Husain N, et al. (2011) 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(5):1903-1918.
18. Zarubica T, Baker MR, Wright HT, Rife JP (2011) The aminoglycoside resistance methyltransferases from the ArmA/Rmt family operate late in the 30S ribosomal biogenesis pathway. RNA 17(2):346-355.
19. Wachino J, et al. (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(12):4401-4409.
20. Clemons WM, Jr., et al. (2001) Crystal structure of the 30 S ribosomal subunit from Thermus thermophilus: Purification, crystallization and structure determination. J Mol Biol 310(4):827-843.
21. Matje DM, Krivacic CT, Dahlquist FW, Reich NO (2013) Distal structural elements coordinate a conserved base flipping network. Biochemistry 52(10):1669-1676.
22. Huang N, Banavali NK, MacKerell AD, Jr. (2003) Protein-facilitated base flipping in DNA by cytosine-5-methyltransferase. Proc Natl Acad Sci USA 100(1):68-73.
23. Decatur WA, Fournier MJ (2002) rRNA modifications and ribosome function. Trends Biochem Sci 27(7):344-351.
24. Dunin-Horkawicz S, et al. (2006) MODOMICS: A database of RNA modification pathways. Nucleic Acids Res 34(Database issue):D145-D149.
25. Machnicka MA, et al. (2013) MODOMICS: A database of RNA modification pathways-2013 update. Nucleic Acids Res 41(Database issue):D262-D267.
26. Boehringer D, O'Farrell HC, Rife JP, Ban N (2012) Structural insights into methyltransferase KsgA function in 30S ribosomal subunit biogenesis. J Biol Chem 287(13):10453-10459.
27. Xu Z, O'Farrell HC, Rife JP, Culver GM (2008) A conserved rRNA methyltransferase regulates ribosome biogenesis. Nat Struct Mol Biol 15(5):534-536.
28. Allen HK, et al. (2010) Call of the wild: Antibiotic resistance genes in natural environments. Nat Rev Microbiol 8(4):251-259.
29. D'Costa VM, et al. (2011) Antibiotic resistance is ancient. Nature 477(7365):457-461.
30. Pruden A, Arabi M, Storteboom HN (2012) Correlation between upstream human activities and riverine antibiotic resistance genes. Environ Sci Technol 46(21):11541-11549.
31. Holmes DJ, Drocourt D, Tiraby G, Cundliffe E (1991) Cloning of an aminoglycosideresistance-encoding gene, kamC, from Saccharopolyspora hirsuta: Comparison with kamB from Streptomyces tenebrarius. Gene 102(1):19-26.
32. Galimand M, Sabtcheva S, Courvalin P, Lambert T (2005) Worldwide disseminated armA aminoglycoside resistance methylase gene is borne by composite transposon Tn1548. Antimicrob Agents Chemother 49(7):2949-2953.
33. Savic M, Lovric J, Tomic TI, Vasiljevic B, Conn GL (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(16):5420-5431.
34. Culver GM, Noller HF (2000) Directed hydroxyl radical probing of RNA from iron(II) tethered to proteins in ribonucleoprotein complexes. Methods Enzymol 318:461-475.
35. Zelinskaya N, Rankin CR, Macmaster R, Savic M, Conn GL (2011) Expression, purification and crystallization of adenosine 1408 aminoglycoside-resistance rRNA methyltransferases for structural studies. Protein Expr Purif 75(1):89-94.
36. Kabsch W (2010) Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr D Biol Crystallogr 66(Pt 2):133-144.
37. Echols N, et al. (2012) Graphical tools for macromolecular crystallography in PHENIX. J Appl Cryst 45(Pt 3):581-586.
38. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.
39. Schrodinger LLC (2010) The PyMOL Molecular Graphics System, Version 1.3r1.