Role of the stringent stress response in the antibiotic resistance phenotype of methicillin-resistant staphylococcus aureus

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 4, 2016, Pages 2311-2317

  Aedo, Sandra ^a   Tomasz, Alexander ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; CEFTIZOXIME; CHLORAMPHENICOL; ERYTHROMYCIN; OXACILLIN; PSEUDOMONIC ACID; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; BETA LACTAM; ISOPROTEIN; MECA PROTEIN, STAPHYLOCOCCUS AUREUS; METICILLIN; PENICILLIN BINDING PROTEIN; PENICILLIN DERIVATIVE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIUM ISOLATE; CONTROLLED STUDY; GENE EXPRESSION; ILES GENE; MECA GENE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PBPB GENE; PBPD GENE; PHENOTYPE; PRIORITY JOURNAL; STAPHYLOCOCCUS SCIURI; STRESS; STRINGENT STRESS RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL SENSITIVITY TEST; PHYSIOLOGICAL STRESS; PROTEIN SYNTHESIS; REGULATOR GENE; SPECIES DIFFERENCE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAM RESISTANCE; BETA-LACTAMS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REGULATOR; METHICILLIN; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; OXACILLIN; PENICILLIN-BINDING PROTEINS; PENICILLINS; PHENOTYPE; PROTEIN BIOSYNTHESIS; PROTEIN ISOFORMS; SPECIES SPECIFICITY; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

EID: 84963626651     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02697-15     Document Type: Article

References (33)

1. Ito T, Katayama Y, Hiramatsu K. 1999. Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315. Antimicrob Agents Chemother 43:1449-1458.
2. Garcia-Alvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, Walpole E, Brooks K, Pickard DJ, Teale C, Parkhill J, Bentley SD, Edwards GF, Girvan EK, Kearns AM, Pichon B, Hill RL, Larsen AR, Skov RL, Peacock SJ, Maskell DJ, Holmes MA. 2011. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis 11:595-603. http://dx.doi.org/10.1016/S1473-3099 (11) 70126-8.
3. Hartman BJ, Tomasz A. 1984. Low-affinity penicillin-binding protein associated with beta-lactam resistance in Staphylococcus aureus. J Bacteriol 158:513-516.
4. de Jonge BL, Chang YS, Gage D, Tomasz A. 1992. Peptidoglycan composition in heterogeneous Tn551 mutants of a methicillin-resistant Staphylococcus aureus strain. J Biol Chem 267:11255-11259.
5. Ryffel C, Strassle A, Kayser FH, Berger-Bachi B. 1994. Mechanisms of heteroresistance in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 38:724-728. http://dx.doi.org/10.1128/AAC.38.4.724.
6. Tomasz A, Nachman S, Leaf H. 1991. Stable classes of phenotypic expression in methicillin-resistant clinical isolates of staphylococci. Antimicrob Agents Chemother 35:124-129. http://dx.doi.org/10.1128/AAC.35.1.124.
7. de Lencastre H, Figueiredo AM, Tomasz A. 1993. Genetic control of population structure in heterogeneous strains of methicillin resistant Staphylococcus aureus. Eur J Clin Microbiol Infect Dis 12(Suppl 1):S13-S18. http://dx.doi.org/10.1007/BF02389872.
8. de Lencastre H, de Jonge BL, Matthews PR, Tomasz A. 1994. Molecular aspects of methicillin resistance in Staphylococcus aureus. J Antimicrob Chemother 33:7-24. http://dx.doi.org/10.1093/jac/33.1.7.
9. Dordel J, Kim C, Chung M, Pardos de la Gandara M, Holden MT, Parkhill J, de Lencastre H, Bentley SD, Tomasz A. 2014. Novel determinants of antibiotic resistance: identification of mutated loci in highly methicillin-resistant subpopulationsof methicillin-resistant Staphylococcus aureus. mBio 5:e01000. http://dx.doi.org/10.1128/mBio.01000-13.
10. Mwangi MM, Kim C, Chung M, Tsai J, Vijayadamodar G, Benitez M, Jarvie TP, Du L, Tomasz A. 2013. Whole-genome sequencing reveals a link between beta-lactam resistance and synthetases of the alarmone (p) ppGpp in Staphylococcus aureus. Microb Drug Resist 19:153-159. http://dx.doi.org/10.1089/mdr.2013.0053.
11. Kim C, Mwangi M, Chung M, Milheirco C, de Lencastre H, Tomasz A. 2013. The mechanism of heterogeneous beta-lactam resistance in MRSA: key role of the stringent stress response. PLoS One 8:e82814. http://dx.doi.org/10.1371/journal.pone.0082814.
12. Dengler V, McCallum N, Kiefer P, Christen P, Patrignani A, Vorholt JA, Berger-Bachi B, Senn MM. 2013. Mutation in the C-di-AMP cyclase dacA affects fitness and resistance of methicillin resistant Staphylococcus aureus. PLoS One 8:e73512. http://dx.doi.org/10.1371/journal.pone.0073512.
13. Rosato RR, Fernandez R, Paz LI, Singh CR, Rosato AE. 2014. TCA cycle-mediated generation of ROS is a key mediator for HeR-MRSA survival under beta-lactam antibiotic exposure. PLoS One 9:e99605. http://dx.doi.org/10.1371/journal.pone.0099605.
14. Cuirolo A, Plata K, Rosato AE. 2009. Development of homogeneous expression of resistance in methicillin-resistant Staphylococcus aureus clinical strains is functionally associated with a beta-lactam-mediated SOS response. J Antimicrob Chemother 64:37-45. http://dx.doi.org/10.1093/jac/dkp164.
15. Potrykus K, Cashel M. 2008. (p) ppGpp: still magical? Annu Rev Microbiol 62:35-51. http://dx.doi.org/10.1146/annurev. micro.62.081307.162903.
16. Srivatsan A, Wang JD. 2008. Control of bacterial transcription, translation and replicationby (p) ppGpp. Curr Opin Microbiol 11:100-105. http://dx.doi.org/10.1016/j.mib.2008.02.001.
17. Reiss S, Pane-Farre J, Fuchs S, Francois P, Liebeke M, Schrenzel J, Lindequist U, Lalk M, Wolz C, Hecker M, Engelmann S. 2012. Global analysis of the Staphylococcus aureus response to mupirocin. Antimicrob Agents Chemother 56:787-804. http://dx.doi.org/10.1128/AAC.05363-11.
18. McKinney TK, Sharma VK, Craig WA, Archer GL. 2001. Transcription of the gene mediating methicillin resistance in Staphylococcus aureus (mecA) is corepressed but not coinduced by cognate mecA and betalactamase regulators. J Bacteriol 183:6862-6868. http://dx.doi.org/10.1128/JB.183.23.6862-6868.2001.
19. Peacock SJ, Paterson GK. 2015. Mechanisms of methicillin resistance in Staphylococcus aureus. Annu Rev biochemistry 84:577-601. http://dx.doi.org/10.1146/annurev-biochem-060614-034516.
20. Leski TA, Tomasz A. 2005. Role of penicillin-binding protein 2 (PBP2) in the antibiotic susceptibility and cell wall cross-linking of Staphylococcus aureus: evidence for the cooperative functioning of PBP2, PBP4, and PBP2A. J Bacteriol 187:1815-1824. http://dx.doi.org/10.1128/JB.187.5.1815-1824.2005.
21. Pinho MG, Filipe SR, de Lencastre H, Tomasz A. 2001. Complementation of the essential peptidoglycan transpeptidase function of penicillinbinding protein 2 (PBP2) by the drug resistance protein PBP2A in Staphylococcus aureus. J Bacteriol 183:6525-6531. http://dx.doi.org/10.1128/JB.183.22.6525-6531.2001.
22. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45. http://dx.doi.org/10.1093/nar/29.9.e45.
23. Kim C, Milheirico C, Gardete S, Holmes MA, Holden MT, de Lencastre H, Tomasz A. 2012. Properties of a novel PBP2A protein homolog from Staphylococcus aureus strain LGA251 and its contribution to the betalactam-resistant phenotype. J Biol Chem 287:36854-36863. http://dx.doi.org/10.1074/jbc. M112.395962.
24. Kuwahara-Arai K, Kondo N, Hori S, Tateda-Suzuki E, Hiramatsu K. 1996. Suppression of methicillin resistance in a mecA-containing premethicillin-resistant Staphylococcus aureus strain is caused by the mecI-mediated repression of PBP 2= production. Antimicrob Agents Chemother 40:2680-2685.
25. Pinho MG, de Lencastre H, Tomasz A. 2001. An acquired and a native penicillin-binding protein cooperate in building the cell wall of drugresistant staphylococci. Proc Natl Acad Sci U S A 98:10886-10891. http://dx.doi.org/10.1073/pnas.191260798.
26. Memmi G, Filipe SR, Pinho MG, Fu Z, Cheung A. 2008. Staphylococcus aureus PBP4 is essential for beta-lactam resistance in communityacquired methicillin-resistant strains. Antimicrob Agents Chemother 52:3955-3966. http://dx.doi.org/10.1128/AAC.00049-08.
27. Wu SW, de Lencastre H, Tomasz A. 2001. Recruitment of the mecA gene homologue of Staphylococcus sciuri into a resistance determinant and expression of the resistant phenotype in Staphylococcus aureus. J Bacteriol 183:2417-2424. http://dx.doi.org/10.1128/JB.183.8.2417-2424.2001.
28. Gardete S, de Lencastre H, Tomasz A. 2006. A link in transcription between the native pbpB and the acquired mecA gene in a strain of Staphylococcus aureus. Microbiology 152:2549-2558. http://dx.doi.org/10.1099/mic.0.29078-0.
29. Fuda C, Suvorov M, Shi Q, Hesek D, Lee M, Mobashery S. 2007. Shared functional attributes between the mecA gene product of Staphylococcus sciuri and penicillin-binding protein 2a of methicillin-resistant Staphylococcus aureus. Biochemistry 46:8050-8057. http://dx.doi.org/10.1021/bi7004587.
30. Couto I, de Lencastre H, Severina E, Kloos W, Webster JA, Hubner RJ, Sanches IS, Tomasz A. 1996. Ubiquitous presence of a mecA homologue in natural isolates of Staphylococcus sciuri. Microb Drug Resist 2:377-391. http://dx.doi.org/10.1089/mdr.1996.2.377.
31. Couto I, Wu SW, Tomasz A, de Lencastre H. 2003. Development of methicillin resistance in clinical isolates of Staphylococcus sciuri by transcriptional activation of the mecA homologue native to the species. J Bacteriol 185:645-653. http://dx.doi.org/10.1128/JB.185.2.645-653.2003.
32. Holden MT, Feil EJ, Lindsay JA, Peacock SJ, Day NP, Enright MC, Foster TJ, Moore CE, Hurst L, Atkin R, Barron A, Bason N, Bentley SD, Chillingworth C, Chillingworth T, Churcher C, Clark L, Corton C, Cronin A, Doggett J, Dowd L, Feltwell T, Hance Z, Harris B, Hauser H, Holroyd S, Jagels K, James KD, Lennard N, Line A, Mayes R, Moule S, Mungall K, Ormond D, Quail MA, Rabbinowitsch E, Rutherford K, Sanders M, Sharp S, Simmonds M, Stevens K, Whitehead S, Barrell BG, Spratt BG, Parkhill J. 2004. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci U S A 101:9786-9791. http://dx.doi.org/10.1073/pnas.0402521101.
33. Zhou Y, Antignac A, Wu SW, Tomasz A. 2008. Penicillin-binding proteins and cell wall composition in beta-lactam-sensitive and-resistant strains of Staphylococcus sciuri. J Bacteriol 190:508-514. http://dx.doi.org/10.1128/JB.01549-07.