Aminoglycoside resistance 16S rRNA methyltransferases block endogenous methylation, affect translation efficiency and fitness of the host

RNA

Volumn 20, Issue 3, 2014, Pages 382-391

  Lioy, Virginia S ^a,b   Goussard, Sylvie ^a   Guerineau, Vincent ^b   Yoon, Eun Jeong ^a   Courvalin, Patrice ^a   Galimand, Marc ^a   Grillot Courvalin, Catherine ^a  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

Author keywords

16S rRNA methyltransferase; Aminoglycoside resistance; Fitness; Translation

Indexed keywords

16S RRNA METHYLTRANSFERASE; AMINOGLYCOSIDE RESISTANCE; FITNESS; TRANSLATION;

AMINOGLYCOSIDES; ANTI-BACTERIAL AGENTS; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENETIC FITNESS; METHYLATION; METHYLTRANSFERASES; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, RIBOSOMAL, 16S; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84894283875     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.042572.113     Document Type: Article

References (35)

1. Andersen NM, Douthwaite S. 2006. YebU is a m5C methyltransferase specific for 16 S rRNA nucleotide 1407. J Mol Biol 359: 777-786.
2. Andersen TE, Porse BT, Kirpekar F. 2004. A novel partial modification at C2501 in Escherichia coli 23S ribosomal RNA. RNA 10: 907-913.
3. Andersson DI, Hughes D. 2010. Antibiotic resistance and its cost: Is it possible to reverse resistance? Nat Rev Microbiol 8: 260-271.
4. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol Syst Biol 2: 2006.0008.
5. Bachmann BJ. 1972. Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol Rev 36: 525-557.
6. Basturea GN, Rudd KE, Deutscher MP. 2006. Identification and characterization of RsmE, the founding member of a new RNA base methyltransferase family. RNA 12: 426-434.
7. Basturea GN, Dague DR, Deutscher MP, Rudd KE. 2012. YhiQ is RsmJ, the methyltransferase responsible for methylation of G1516 in 16S rRNA of E. Coli. J Mol Biol 415: 16-21.
8. Chaveroche MK, Ghigo JM, d'Enfert C. 2000. A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res 28: e97.
9. Cherepanov PP, Wackernagel W. 1995. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158: 9-14.
10. Churchward G, Belin D, Nagamine Y. 1984. A pSC101-derived plasmid which shows no sequence homology to other commonly used cloning vectors. Gene 31: 165-171.
11. Cubrilo S, Babic F, Douthwaite S, Maravic Vlahovicek G. 2009. The aminoglycoside resistance methyltransferase Sgm impedes RsmF methylation at an adjacent rRNA nucleotide in the ribosomal A site. RNA 15: 1492-1497.
12. Foucault ML, Courvalin P, Grillot-Courvalin C. 2009. Fitness cost of VanA-type vancomycin resistance in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 53: 2354-2359.
13. Galimand M, Courvalin P, Lambert T. 2003. Plasmid-mediated high-level resistance to aminoglycosides in Enterobacteriaceae due to 16S rRNA methylation. Antimicrob Agents Chemother 47: 2565-2571.
14. 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: 2949-2953.
15. Grillot-Courvalin C, Goussard S, Huetz F, Ojcius DM, Courvalin P. 1998. Functional gene transfer from intracellular bacteria to mammalian cells. Nat Biotechnol 16: 862-866.
16. Gutierrez B, Escudero JA, San Millan A, Hidalgo L, Carrilero L, Ovejero CM, Santos-Lopez A, Thomas-Lopez D, Gonzalez-Zorn B. 2012. Fitness cost and interference of Arm/Rmt aminoglycoside resistance with the RsmF housekeeping methyltransferases. Antimicrob Agents Chemother 56: 2335-2341.
17. Gutierrez B, Douthwaite S, Gonzalez-Zorn B. 2013. Indigenous and acquired modifications in the aminoglycoside binding sites of Pseudomonas aeruginosa rRNAs. RNA Biol 10: 1324-1332.
18. Husain N, Tkaczuk KL, Tulsidas SR, Kaminska KH, Cubrilo S, Maravic-Vlahovicek G, Bujnicki JM, 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 38: 4120-4132.
19. Husain N, Obranic S, Koscinski L, Seetharaman J, Babic F, Bujnicki JM, Maravic-Vlahovicek G, Sivaraman J. 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: 1903-1918.
20. Kimura S, Suzuki T. 2010. Fine-tuning of the ribosomal decoding center by conserved methyl-modifications in the Escherichia coli 16S rRNA. Nucleic Acids Res 38: 1341-1352.
21. LaMarre JM, Locke JB, Shaw KJ, Mankin AS. 2011. Low fitness cost of the multidrug resistance gene cfr. Antimicrob Agents Chemother 55: 3714-3719.
22. Liou GF, Yoshizawa S, Courvalin P, Galimand M. 2006. Aminoglycoside resistance by ArmA-mediated ribosomal 16S methylation in human bacterial pathogens. J Mol Biol 359: 358-364.
23. Magnet S, Blanchard JS. 2005. Molecular insights into aminoglycoside action and resistance. Chem Rev 105: 477-498.
24. Marcusson LL, Frimodt-Moller N, Hughes D. 2009. Interplay in the selection of fluoroquinolone resistance and bacterial fitness. PLoS Pathog 5: e1000541.
25. McLuckey SA, Van Berkel GJ, Glish GL. 1992. Tandem mass spectrometry of small multiply charged oligonucleotides. J Am Soc Mass Spectrom 3: 60-70.
26. O'Connor M, Thomas CL, Zimmermann RA, Dahlberg AE. 1997. Decoding fidelity at the ribosomal A and P sites: Influence of mutations in three different regions of the decoding domain in 16S rRNA. Nucleic Acids Res 25: 1185-1193.
27. Périchon B, Courvalin P, Galimand M. 2007. Transferable resistance to aminoglycosides by methylation of G1405 in 16S rRNA and to hydrophilic fluoroquinolones by QepA-mediated efflux in Escherichia coli. Antimicrob Agents Chemother 51: 2464-2469.
28. Pfister P, Hobbie S, Vicens Q, Bottger EC, Westhof E. 2003. The molecular basis for A-site mutations conferring aminoglycoside resistance: Relationship between ribosomal susceptibility and X-ray crystal structures. Chembiochem 4: 1078-1088.
29. Qin D, Liu Q, Devaraj A, Fredrick K. 2012. Role of helix 44 of 16S rRNA in the fidelity of translation initiation. RNA 18: 485-495.
30. Roy-Chaudhuri B, Kirthi N, Culver GM. 2010. Appropriate maturation and folding of 16S rRNA during 30S subunit biogenesis are critical for translational fidelity. Proc Natl Acad Sci 107: 4567-4572.
31. 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: 570-582.
32. Wachino J, Arakawa Y. 2012. Exogenously acquired 16S rRNA methyltransferases found in aminoglycoside-resistant pathogenic Gramnegative bacteria: An update. Drug Resist Updat 15: 133-148.
33. Wachino J, Shibayama K, Kurokawa H, Kimura K, Yamane K, Suzuki S, Shibata N, Ike Y, 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.
34. Wei Y, Zhang H, Gao ZQ, Wang WJ, Shtykova EV, Xu JH, Liu QS, Dong YH. 2012. Crystal and solution structures of methyltransferase RsmH provide basis for methylation of C1402 in 16S rRNA. J Struct Biol 179: 29-40.
35. 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: 346-355.