Mutations in mmpL and in the cell wall stress stimulon contribute to resistance to oxadiazole antibiotics in methicillin-resistant Staphylococcus aureus

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 10, 2014, Pages 5841-5847

  Xiao, Qiaobin ^a   Vakulenko, Sergei ^a   Chang, Mayland ^a   Mobashery, Shahriar ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; CEFTAZIDIME; IMIPENEM; LINEZOLID; OXADIAZOLE DERIVATIVE; THIOREDOXIN; VANCOMYCIN; ANTIINFECTIVE AGENT;

ANTIBIOTIC BIOSYNTHESIS; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; GENE DELETION; GENE MUTATION; IN VITRO STUDY; IN VIVO STUDY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; MMPL GENE; NONHUMAN; PROMOTER REGION; STIMULON; STRUCTURAL GENE; DRUG EFFECTS; GENETICS; MICROBIAL SENSITIVITY TEST; MUTATION;

ANTI-BACTERIAL AGENTS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; MUTATION; OXADIAZOLES; PROMOTER REGIONS, GENETIC; THIOREDOXINS;

EID: 84907274701     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.03501-14     Document Type: Article

References (35)

1. Centers for Disease Control and Prevention. 2013. Antibiotic resistance threats in the United States, 2013. Centers for Disease Control and Prevention, Atlanta, GA.
2. DeLeo FR, Otto M, Kreiswirth BN, Chambers HF. 2010. Community associated methicillin-resistant Staphylococcus aureus. Lancet 375:15571568. http://dx.doi.org/10.1016/S0140-6736(09)61999-1.
3. Diekema DJ, Pfaller MA, Schmitz FJ, Smayevsky J, Bell J, Jones RN, Beach M, SENTRY Participants Group. 2001. Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997-1999. Clin. Infect. Dis. 32:S114-S132. http: //dx.doi.org/10.1086/320184.
4. Fuda CC, Fisher JF, Mobashery S. 2005. Beta-lactam resistance in Staphylococcus aureus: the adaptive resistance of a plastic genome. Cell Mol. Life Sci. 62:2617-2633. http://dx.doi.org/10.1007/s00018-005-5148-6.
5. The University of Chicago Medical Center. 2010. MRSA history timeline: the first half-century, 1959-2009. MRSA Research Center, The University of Chicago Medical Center, Chicago, IL.
6. Bozdogan BÜ, Esel D, Whitener C, Browne FA, Appelbaum PC. 2003. Antibacterial susceptibility of a vancomycin-resistant Staphylococcus aureus strain isolated at the Hershey Medical Center. J. Antimicrob. Chemother. 52:864-868. http://dx.doi.org/10.1093/jac/dkg457.
7. Tsiodras S, Gold HS, Sakoulas G, Eliopoulos GM, Wennersten C, Venkataraman L, Moellering RC, Ferraro MJ. 2001. Linezolid resistance in a clinical isolate of Staphylococcus aureus. Lancet 358:207-208. http://dx.doi.org/10.10166/S0140-6736(01)05410-l.
8. Boyle-Vavra S, Daum RS. 2007. Community-acquired methicillinresistant Staphylococcus aureus: the role of Panton-Valentine leukocidin. Lab. Invest. 87:3-9. http://dx.doi.org/10.1038/labinvest.3700501.
9. Maree CL, Daum RS, Boyle-Vavra S, Matayoshi K, Miller LG. 2007. Community-associated methicillin-resistant Staphylococcus aureus isolates and healthcare-associated infections. Emerg. Infect. Dis. 13:236-242. http://dx.doi.org/10.3201/eidl302.060781.
10. O'Daniel PI, Peng Z, Pi H, Testero SA, Ding D, Spink EE, Leemans E, Boudreau MA, Yamaguchi T, Schroeder VA, Wolter WR, Llarrull LI, Song W, Lastochkin E, Kumarasiri M, Antunes NT, Espahbodi M, Lichtenwalter K, Suckow MA, Vakulenko SB, Mobashery S, Chang M. 2014. Discovery of a new class of non-ß-lactam inhibitors of penicillinbinding proteins with Gram-positive antibacterial activity. J. Am. Chem. Soc. 136:3664-3672. http://dx.doi.org/10.1021/ja500053x.
11. Domenech P, Reed MB, Barry CE, III. 2005. Contribution of the Mycobacterium tuberculosis mmpL protein family to virulence and drug resistance. Infect. Immun. 73:3492-3501. http://dx.doi.Org/10.1128/IAI.73.6.3492 3501.2005.
12. Cuaron JA, Dulal S, Song Y, Singh AK, Montelongo CE, Yu W, Nagarajan V, Jayaswal RK, Wilkinson BJ, Gustafson JE. 2013. Tea tree oil-induced transcriptional alterations in Staphylococcus aureus. Phytother. Res. 27:390-396. http://dx.doi.org/T0.1002/ptr.4738.
13. Truong-Bolduc QC, Dunman PM, Eidem T, Hooper DC. 2011. Transcriptional profiling analysis of the global regulator NorG, a GntR-like protein of Staphylococcus aureus. J. Bacteriol. 193:6207-6214. http://dx.doi.org/10.1128/JB.05847 11.
14. Clinical and Laboratory Standards Institute. 2006. Methods for dilution antimicrobial susceptibility rests for bacteria that grow aerobically; approved standard, 7th ed. Clinical and Laboratory Standards Institute, Wayne, PA.
15. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. http://dx.doi.org/10.1093/bioinformatic/btp324.
16. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078-2079. http://dx.doi.org/10.1093/bioinformatics/btp352.
17. Arnaud M, Chastanet A, Débarbouillé M. 2004. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl. Environ. Microbiol. 70:6887-6891. http: //dx.doi.org/10.1128/AEM.70.11.6887-689 L2004.
18. Sobral RG, Jones AE, Des Etages SG, Dougherty TJ, Peitzsch RM, Gaasterland T, Ludovice AM, de Lencastre H, Tomasz A. 2007. Extensive and genome-wide changes in the transcription profile of Staphylococcus aureus induced by modulating the transcription of the cell wall synthesis gene murF. J. Bacteriol. 189:2376-2391. http://dx.doi.Org/10.l128/JB.01439-06.
19. Utaida S, Dunman PM, Macapagal D, Murphy E, Projan SJ, Singh VK, Jayaswal RK, Wilkinson BJ. 2003. Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology 49:2719-2732. http://dx.doi.org/10.1099/mic.0.26426-0.
20. Kuroda M, Kuroda H, Oshima T, Takeuchi F, Mori H, Hiramatsu K. 2003. Two-component system VraSR positively modulates the regulation of cell wall biosynthesis pathway in Staphylococcus aureus. Mol. Microbiol. 49:807-821. http://dx.doi.Org/10.1046/j.13652958.2003.03599.x.
21. Jusko M, Potempa J, Kantyka T, Bieíecka E, Miller HK, Kalinska M, Dubin G, Garred P, Shaw LN, Blom AM. 2014. Staphylococcal proteasesaid in evasion of the human complement system. J. Innate Immun. 6:3146. http://dx.doi.org/10.1159/000351458.
22. Varela C, Rittmann D, Singh A, Krumbach K, Bhatt K, Eggeling L, Besra GS, Bhatt A. 2012. MmpL genes are associated with mycolic acid metabolism in mycobacteria and corynebacteria. Chem. Biol. 19:498506. http://dx.doi.Org/10.1016/j.chembiol.2012.03.006.
23. Sondén B, Kocíncová D, Deshayes C, Euphrasie D, Rhayat L, Laval F, Frehel C, Daffé M, Etienne G, Reyrat JM. 2005. Gap, a mycobacterial specific integral membrane protein, is required for glycolipid transport to the cell surface. Mol. Microbiol. 58:426-440. http://dx.doi.Org/10.1111/j.1365-2958.2005.04847.x.
24. Domenech P, Reed MB, Barry CE, III. 2005. Contribution of the Mycobacterium tuberculosis MmpL protein family to virulence and drug resistance. Infect. Immun. 73:3492-501. http://dx.doi.Org/10.1128/IAI73.6.3492-3501.2005.
25. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ. 2007. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:797-810. http://dx.doi.Org/10.1016/j.cell.2007.06.049.
26. Foti JJ, Devadoss B, Winkler JA, Collins JJ, Walker GC. 2012. Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science 336:315-319. http://dx.doi.org/10.1126/science1219192.
27. Wang X, Zhao X, Malik M, Drlica K. 2010. Contribution of reactive oxygen species to pathways of quinolone-mediated bacterial cell death. J. Antimicrob. Chemother. 65:520-524. http://dx.doi.org/10.1093/jac /dkp486.
28. Dhamdhere G, Krishnamoorthy G, Zgurskaya HI. 2010. Interplay between drug efflux and antioxidants in Escherichia coli resistance to antibiotics. Antimicrob. Agents Chemother. 54:5366-5368. http://dx.doi.org/10.1128/AAC.00719-10.
29. Lu J, Vlamis-Gardikas A, Kandasamy K, Zhao R, Gustafsson TN, Engstrand L, Hoffner S, Engman L, Holmgren A. 2013. Inhibition of bacterial thioredoxin reductase: an antibiotic mechanism targeting bacteria lacking glutathione. FASEBJ. 27:1394-1403. http://dx.doi.org/10.1096/fj.12-223305.
30. Arnér E, Holmgren A. 2000. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267:6102-6109. http://dx.doi.org/10.1046/j.1432-1327.2000.01701.x.
31. Holmgren A. 1989. Thioredoxin and glutaredoxin systems. J. Biol. Chem.264:13963-13966.
32. Gon S, Faulkner MJ, Beckwith J. 2006. In vivo requirement for glutaredoxins and thioredoxins in the reduction of the ribonucleotide reductases of Escherichia coli. Antioxid. Redox Signal. 8:735-742. http://dx.doi.org/10.1089/ars.2006.8.735.
33. Charpentier E, Anton AI, Barry P, Alfonso B, Fang Y, Novick RP. 2004. Novel cassette-based shuttle vector system for gram-positive bacteria. Appl. Environ. Microbiol. 70:6076-6085. http://dx.doi.org/10.1128/AEM.70.10.6076-6085.2004.
34. Kreiswirth BN, Lofdahl S, Betley MJ, O'Reilly M, Schlievert PM, Bergdoll MS, Novick RP. 1983. The toxic shock syndrome exotoxin structural gene is not delectably transmitted by a prophage. Nature 305:709-712. http://dx.doi.org/10.1038/305709a0.
35. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580. http://dx.doi.org/10.1016/S0022-2836(83)80284-8.