Reversible antibiotic tolerance induced in Staphylococcus aureus by concurrent drug exposure

mBio

Volumn 6, Issue 1, 2015, Pages

  Haaber, Jakob ^a,b   Friberg, Cathrine ^b   McCreary, Mark ^a   Lin, Richard ^a   Cohen, Stanley N ^a   Ingmer, Hanne ^b  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; CIPROFLOXACIN; COLISTIN; GENTAMICIN; RIFAMPICIN; TEICOPLANIN; TETRACYCLINE; VANCOMYCIN; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL WALL; BACTERIAL STRAIN; DRUG EXPOSURE; DRUG SCREENING; DRUG TOLERANCE; GENE EXPRESSION; GRAM NEGATIVE INFECTION; MUTATIONAL ANALYSIS; NONHUMAN; OPERON; PHENOTYPE; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; VANCOMYCIN INTERMEDIATE STAPHYLOCOCCUS AUREUS; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; STAPHYLOCOCCAL INFECTIONS;

BACTERIA (MICROORGANISMS); METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NEGIBACTERIA; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; COLISTIN; HUMANS; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VANCOMYCIN; VANCOMYCIN RESISTANCE;

EID: 84924187397     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02268-14     Document Type: Article

References (49)

1. Boucher H, Talbot G, Bradley J, Edwards J, Gilbert D, Rice L, Scheld M, Spellberg B, Bartlett J. 2009. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis 48: 1-12. http://dx. doi. org/10. 1086/595011.
2. Barlow M. 2009. What antimicrobial resistance has taught us about horizontal gene transfer. Methods Mol Biol 532: 397-411. http://dx. doi. org/10. 1007/978-1-60327-853-9_23.
3. Chancey ST, Zähner D, Stephens DS. 2012. Acquired inducible antimicrobial resistance in Gram-positive bacteria. Future Microbiol 7: 959-978. http://dx. doi. org/10. 2217/fmb. 12. 63.
4. Lowy FD. 1998. Staphylococcus aureus infections. N Engl J Med 339: 520-532. http://dx. doi. org/10. 1056/NEJM199808203390806.
5. Kennedy AD, Otto M, Braughton KR, Whitney AR, Chen L, Mathema B, Mediavilla JR, Byrne KA, Parkins LD, Tenover FC, Kreiswirth BN, Musser JM, DeLeo FR. 2008. Epidemic community-associated methicillin-resistant Staphylococcus aureus: recent clonal expansion and diversification. Proc Natl Acad Sci U S A 105: 1327-1332. http://dx. doi. org/10. 1073/pnas. 0710217105.
6. Grundmann H, Aires-de-Sousa M, Boyce J, Tiemersma E. 2006. Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. Lancet 368: 874-885. http://dx. doi. org/10. 1016/S0140-6736(06)68853-3.
7. Chambers HF, DeLeo FR. 2009. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7: 629-641. http://dx. doi. org/10. 1038/nrmicro2200.
8. Greenwood D. 1988. Microbiological properties of teicoplanin. J Antimicrob Chemother 21(Suppl A): 1-13. http://dx. doi. org/10. 1093/jac/21. suppl_A. 1.
9. Howden BP, Davies JK, Johnson PD, Stinear TP, Grayson ML. 2010. Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heterogeneous vancomycin-intermediate strains: resistance mechanisms, laboratory detection, and clinical implications. Clin Microbiol Rev 23: 99-139. http://dx. doi. org/10. 1128/CMR. 00042-09.
10. McAleese F, Wu SW, Sieradzki K, Dunman P, Murphy E, Projan S, Tomasz A. 2006. Overexpression of genes of the cell wall stimulon in clinical isolates of Staphylococcus aureus exhibiting vancomycinintermediate S. aureus-type resistance to vancomycin. J Bacteriol 188: 1120-1133. http://dx. doi. org/10. 1128/JB. 188. 3. 1120-1133. 2006.
11. 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. 1365-2958. 2003. 03599. x.
12. Falord M, Mäder U, Hiron A, Débarbouillé M, Msadek T. 2011. Investigation of the Staphylococcus aureus GraSR regulon reveals novel links to virulence, stress response and cell wall signal transduction pathways. PLoS One 6: e21323. http://dx. doi. org/10. 1371/journal. pone. 0021323.
13. Falord M, Karimova G, Hiron A, Msadek T. 2012. GraXSR interact with the VraFG ABC transporter to form a five-component system required for cationic antimicrobial peptide sensing and resistance in Staphylococcus aureus. Antimicrob Agents Chemother 56: 1047-1058. http://dx. doi. org/10. 1128/AAC. 05054-11.
14. Kuroda M, Kuwahara-Arai K, Hiramatsu K. 2000. Identification of the up-and down-regulated genes in vancomycin-resistant Staphylococcus aureus strains Mu3 and Mu50 by cDNA differential hybridization method. Biochem Biophys Res Commun 269: 485-490. http://dx. doi. org/10. 1006/bbrc. 2000. 2277.
15. Watanakunakorn C. 1984. Mode of action and in-vitro activity of vancomycin. J Antimicrob Chemother 14(Suppl D): 7-18. http://dx. doi. org/10. 1093/jac/14. suppl_D. 7.
16. Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, Götz F. 1999. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274: 8405-8410. http://dx. doi. org/10. 1074/jbc. 274. 13. 8405.
17. Peschel A, Jack RW, Otto M, Collins LV, Staubitz P, Nicholson G, Kalbacher H, Nieuwenhuizen WF, Jung G, Tarkowski A, Van Kessel KP, Van Strijp JA. 2001. Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with l-lysine. J Exp Med 193: 1067-1076. http://dx. doi. org/10. 1084/jem. 193. 9. 1067.
18. Rogasch K, Rühmling V, Pané-Farré J, Höper D, Weinberg C, Fuchs S, Schmudde M, Bröker BM, Wolz C, Hecker M, Engelmann S. 2006. Influence of the two-component system SaeRS on global gene expression in two different Staphylococcus aureus strains. J Bacteriol 188: 7742-7758. http://dx. doi. org/10. 1128/JB. 00555-06.
19. Novick RP, Jiang D. 2003. The staphylococcal saeRS system coordinates environmental signals with agr quorum sensing. Microbiology 149: 2709-2717. http://dx. doi. org/10. 1099/mic. 0. 26575-0.
20. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, Moghazeh S. 1993. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12: 3967-3975.
21. Gardete S, Kim C, Hartmann BM, Mwangi M, Roux CM, Dunman PM, Chambers HF, Tomasz A. 2012. Genetic pathway in acquisition and loss of vancomycin resistance in a methicillin resistant Staphylococcus aureus (MRSA) strain of clonal type USA300. PLoS Pathog. 8: e1002505. http://dx. doi. org/10. 1371/journal. ppat. 1002505.
22. Peleg AY, Monga D, Pillai S, Mylonakis E, Moellering RC, Jr., Eliopoulos GM. 2009. Reduced susceptibility to vancomycin influences pathogenicity in Staphylococcus aureus infection. J Infect Dis 199: 532-536. http://dx. doi. org/10. 1086/596511.
23. Mwangi MM, Wu SW, Zhou Y, Sieradzki K, de Lencastre H, Richardson P, Bruce D, Rubin E, Myers E, Siggia ED, Tomasz A. 2007. Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc Natl Acad Sci U S A 104: 9451-9456. http://dx. doi. org/10. 1073/pnas. 0609839104.
24. Cui L, Neoh HM, Shoji M, Hiramatsu K. 2009. Contribution of vraSR and graSR point mutations to vancomycin resistance in vancomycinintermediate Staphylococcus aureus. Antimicrob Agents Chemother 53: 1231-1234. http://dx. doi. org/10. 1128/AAC. 01173-08.
25. Hafer C, Lin Y, Kornblum J, Lowy FD, Uhlemann AC. 2012. Contribution of selected gene mutations to resistance in clinical isolates of vancomycin-intermediate Staphylococcus aureus. Antimicrob Agents Chemother 56: 5845-5851. http://dx. doi. org/10. 1128/AAC. 01139-12.
26. Koehl JL, Muthaiyan A, Jayaswal RK, Ehlert K, Labischinski H, Wilkinson BJ. 2004. Cell wall composition and decreased autolytic activity and lysostaphin susceptibility of glycopeptide-intermediate Staphylococcus aureus. Antimicrob Agents Chemother 48: 3749-3757. http://dx. doi. org/10. 1128/AAC. 48. 10. 3749-3757. 2004.
27. Meehl M, Herbert S, Götz F, Cheung A. 2007. Interaction of the GraRS two-component system with the VraFG ABC transporter to support vancomycin-intermediate resistance in Staphylococcus aureus. Antimicrob Agents Chemother 51: 2679-2689. http://dx. doi. org/10. 1128/AAC. 00209-07.
28. Sieradzki K, Tomasz A. 2003. Alterations of cell wall structure and metabolism accompany reduced susceptibility to vancomycin in an isogenic series of clinical isolates of Staphylococcus aureus. J Bacteriol 185: 7103-7110. http://dx. doi. org/10. 1128/JB. 185. 24. 7103-7110. 2003.
29. 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 149: 2719-2732. http://dx. doi. org/10. 1099/mic. 0. 26426-0.
30. Sakoulas G, Eliopoulos GM, Moellering RC, Jr., Wennersten C, Venkataraman L, Novick RP, Gold HS. 2002. Accessory gene regulator (agr) locus in geographically diverse Staphylococcus aureus isolates with reduced susceptibility to vancomycin. Antimicrob Agents Chemother 46: 1492-1502. http://dx. doi. org/10. 1128/AAC. 46. 5. 1492-1502. 2002.
31. Van Hal SJ, Lodise TP, Paterson DL. 2012. The clinical significance of vancomycin minimum inhibitory concentration in Staphylococcus aureus infections: a systematic review and meta-analysis. Clin Infect Dis 54: 755-771. http://dx. doi. org/10. 1093/cid/cir935.
32. Wi YM, Kim JM, Joo EJ, Ha YE, Kang CI, Ko KS, Chung DR, Song JH, Peck KR. 2012. High vancomycin minimum inhibitory concentration is a predictor of mortality in meticillin-resistant Staphylococcus aureus bacteraemia. Int J Antimicrob Agents 40: 108-113. http://dx. doi. org/10. 1016/j. ijantimicag. 2012. 04. 003.
33. Chang FY, Peacock JE, Jr, Musher DM, Triplett P, MacDonald BB, Mylotte JM, O'Donnell A, Wagener MM, Yu VL. 2003. Staphylococcus aureus bacteremia: recurrence and the impact of antibiotic treatment in a prospective multicenter study. Medicine (Baltimore) 82: 333-339. http://dx. doi. org/10. 1097/01. md. 0000091184. 93122. 09.
34. Dombrowski JC, Winston LG. 2008. Clinical failures of appropriately treated methicillin-resistant Staphylococcus aureus infections. J Infect 57: 110-115. http://dx. doi. org/10. 1016/j. jinf. 2008. 04. 003.
35. Woods CJ, Chowdhury A, Patel VM, Shorr AF. 2012. Impact of vancomycin minimum inhibitory concentration on mortality among critically ill patients with methicillin-resistant Staphylococcus aureus bacteremia. Infect Control Hosp Epidemiol 33: 1246-1249. http://dx. doi. org/10. 1086/668433.
36. Mavros MN, Tansarli GS, Vardakas KZ, Rafailidis PI, Karageorgopoulos DE, Falagas ME. 2012. Impact of vancomycin minimum inhibitory concentration on clinical outcomes of patients with vancomycinsusceptible Staphylococcus aureus infections: a meta-analysis and metaregression. Int J Antimicrob Agents 40: 496-509. http://dx. doi. org/10. 1016/j. ijantimicag. 2012. 07. 023.
37. Wang JL, Lai CH, Lin HH, Chen WF, Shih YC, Hung CH. 2013. High vancomycin minimum inhibitory concentrations with heteroresistant vancomycin-intermediate Staphylococcus aureus in meticillin-resistant S. aureus bacteraemia patients. Int J Antimicrob Agents 42: 390-394. http://dx. doi. org/10. 1016/j. ijantimicag. 2013. 07. 010.
38. Howden BP, Ward PB, Charles PG, Korman TM, Fuller A, du Cros P, Grabsch EA, Roberts SA, Robson J, Read K, Bak N, Hurley J, Johnson PD, Morris AJ, Mayall BC, Grayson ML. 2004. Treatment outcomes for serious infections caused by methicillin-resistant Staphylococcus aureus with reduced vancomycin susceptibility. Clin Infect Dis 38: 521-528. http://dx. doi. org/10. 1086/381202.
39. Moore MR, Perdreau-Remington F, Chambers HF. 2003. Vancomycin treatment failure associated with heterogeneous vancomycinintermediate Staphylococcus aureus in a patient with endocarditis and in the rabbit model of endocarditis. Antimicrob Agents Chemother 47: 1262-1266. http://dx. doi. org/10. 1128/AAC. 47. 4. 1262-1266. 2003.
40. Deresinski S. 2007. Counterpoint: vancomycin and Staphylococcus aureus-an antibiotic enters obsolescence. Clin Infect Dis 44: 1543-1548. http://dx. doi. org/10. 1086/518452.
41. Lodise TP, Graves J, Evans A, Graffunder E, Helmecke M, Lomaestro BM, Stellrecht K. 2008. Relationship between vancomycin MIC and failure among patients with methicillin-resistant Staphylococcus aureus bacteremia treated with vancomycin. Antimicrob Agents Chemother 52: 3315-3320. http://dx. doi. org/10. 1128/AAC. 00113-08.
42. Rybak MJ, Vidaillac C, Sader HS, Rhomberg PR, Salimnia H, Briski LE, Wanger A, Jones RN. 2013. Evaluation of vancomycin susceptibility testing for methicillin-resistant Staphylococcus aureus: comparison of Etest and three automated testing methods. J Clin Microbiol 51: 2077-2081. http://dx. doi. org/10. 1128/JCM. 00448-13.
43. Yang SJ, Nast CC, Mishra NN, Yeaman MR, Fey PD, Bayer AS. 2010. Cell wall thickening is not a universal accompaniment of the daptomycin nonsusceptibility phenotype in Staphylococcus aureus: evidence for multiple resistance mechanisms. Antimicrob Agents Chemother 54: 3079-3085. http://dx. doi. org/10. 1128/AAC. 00122-10.
44. Huang J, Lih CJ, Pan KH, Cohen SN. 2001. Global analysis of growth phase responsive gene expression and regulation of antibiotic biosynthetic pathways in Streptomyces coelicolor using DNA microarrays. Genes Dev 15: 3183-3192. http://dx. doi. org/10. 1101/gad. 943401.
45. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A, Smyth GK. 2007. A comparison of background correction methods for two-colour microarrays. BioInformatics 23: 2700-2707. http://dx. doi. org/10. 1093/bioinformatics/btm412.
46. Smyth GK, Speed T. 2003. Normalization of cDNA microarray data. Methods 31: 265-273. http://dx. doi. org/10. 1016/S1046-2023(03)00155-5.
47. Smyth GK. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3. http://dx. doi. org/10. 2202/1544-6115. 1027.
48. Eisen MB, Spellman PT, Brown PO, Botstein D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad SciUSA 95: 14863-14868. http://dx. doi. org/10. 1073/pnas. 95. 25. 14863.
49. Saldanha AJ. 2004. Java TreeView-extensible visualization of microarray data. BioInformatics 20: 3246-3248. http://dx. doi. org/10. 1093/bioinformatics/bth349.