In vivo evolution to Colistin resistance by PmrB sensor kinase mutation in KPC-producing Klebsiella pneumoniae is associated with low-dosage colistin treatment

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 8, 2014, Pages 4399-4403

  Cannatelli, Antonio ^a   Di Pilato, Vincenzo ^a   Giani, Tommaso ^a   Arena, Fabio ^a   Ambretti, Simone ^b   Gaibani, Paolo ^b   D'Andrea, Marco Maria ^a   Rossolinia, Gian Maria ^a,c,d  

^a UNIVERSITY OF SIENA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF FLORENCE   (Italy)

^d CAREGGI UNIVERSITY HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; BETA LACTAMASE; CARBAPENEMASE; COLISTIN; LIPOPOLYSACCHARIDE; PMRA PROTEIN, BACTERIA; PMRB PROTEIN, BACTERIA; TRANSCRIPTION FACTOR;

AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; CELL CLONE; DOSE CALCULATION; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MUTATION; OPERON;

AMINO ACID SUBSTITUTION; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAM RESISTANCE; BETA-LACTAMASES; CLONE CELLS; COLISTIN; DRUG DOSAGE CALCULATIONS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; LIPOPOLYSACCHARIDES; MICROBIAL SENSITIVITY TESTS; MUTATION; OPERON; TRANSCRIPTION FACTORS;

EID: 84905394181     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02555-14     Document Type: Article

References (31)

1. Nordmann P, Naas T, Poirel L. 2011. Global spread of carbapenemaseproducing Enterobacteriaceae. Emerg. Infect. Dis. 17:1791-1798. http://dx.doi.org/10.3201/eid1710.110655.
2. Tzouvelekis LS, Markogiannakis A, Psichogiou M, Tassios PT, Daikos GL. 2012. Carbapenemases in Klebsiella pneumoniae and other Enterobacteriaceae: an evolving crisis of global dimensions. Clin. Microbiol. Rev. 25:682-707. http://dx.doi.org/10.1128/CMR.05035-11.
3. Canton R, Akova M, Carmeli Y, Giske CG, Glupczynski Y, Gniadkowski M, Livermore DM, Miriagou V, Naas T, Rossolini GM, Samuelsen O, Seifert H, Woodford N, Nordmann P, European Network on Carbapenemases. 2012. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin. Microbiol. Infect. 18:413-431. http://dx.doi.org/10.1111/j.1469-0691.2012.03821.x.
4. Munoz-Price LS, Poirel L, Bonomo RA, Schwaber MJ, Daikos GL, Cormican M, Cornaglia G, Garau J, Gniadkowski M, Hayden MK, Kumarasamy K, Livermore DM, Maya JJ, Nordmann P, Patel JB, Paterson DL, Pitout J, Villegas MV, Wang H, Woodford N, Quinn JP. 2013. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect. Dis. 13:785-796. http://dx.doi.org/10. 1016/S1473-3099 (13) 70190-7.
5. Giani T, Pini B, Arena F, Conte V, Bracco S, Migliavacca R, AMCLI-CRE Survey Participants, Pantosti A, Pagani L, Luzzaro F, Rossolini GM. 2013. Epidemic diffusion of KPC carbapenemase-producing Klebsiella pneumoniae in Italy: results of the first countrywide survey, 15 May to 30 June 2011. Euro Surveill. 18
6. Livermore DM, Warner M, Mushtaq S, Doumith M, Zhang J, Woodford N. 2011. What remains against carbapenem-resistant Enterobacteriaceae? Evaluation of chloramphenicol, ciprofloxacin, colistin, fosfomycin, minocycline, nitrofurantoin, temocillin and tigecycline. Int. J. Antimicrob. Agents. 37:415-419. http://dx.doi.org/10.1016/j.ijantimicag.2011.01.012.
7. Petrosillo N, Giannella M, Lewis R, Viale P. 2013. Treatment of carbapenemresistant Klebsiella pneumoniae: the state of the art. Expert Rev. Anti Infect. Ther. 11:159-177. http://dx.doi.org/10.1586/eri.12.162.
8. Ah YM, Kim AJ, Lee JY. 8 April 2014. Colistin resistance in Klebsiella pneumoniae. Int. J. Antimicrob. Agents. http://dx.doi.org/10.1016/j.ijantimicag. 2014.02.016.
9. Zagorianou A, Sianou E, Iosifidis E, Dimou V, Protonotariou E, Miyakis S, Roilides E, Sofianou D. 2012. Microbiological and molecular characteristics of carbapenemase-producing Klebsiella pneumoniae endemic in a tertiary Greek hospital during 2004-2010. Euro Surveill. 17: pii=20088. http://www. eurosurveillance.org/ViewArticle.aspx?ArticleId=20088.
10. Lippa AM, Goulian M. 2009. Feedback inhibition in the PhoQ/PhoP signaling system by a membrane peptide. PLoS Genet. 5:e1000788. http://dx.doi.org/10. 1371/journal.pgen. 1000788.
11. Cannatelli A, D'Andrea MM, Giani T, Di Pilato V, Arena F, Ambretti S, Gaibani P, Rossolini GM. 2013. In vivo emergence of colistin resistance in Klebsiella pneumoniae producing KPC-type carbapenemases mediated by insertional inactivation of the PhoQ/PhoP mgrB regulator. Antimicrob. Agents Chemother. 57:5521-5526. http://dx.doi.org/10.1128/AAC.01480-13.
12. López-Camacho E, Gómez-Gil R, Tobes R, Manrique M, Lorenzo M, Galván B, Salvarelli E, Moatassim Y, Salanueva IJ, Pareja E, Codoñer FM, Alvarez-Tejado M, Garcillán-Barcia MP, De La Cruz F, Mingorance J. 2014. Genomic analysis of the emergence and evolution of multidrug resistance during a Klebsiella pneumoniae outbreak including carbapenem and colistin resistance. J. Antimicrob. Chemother. 69:632-636. http://dx.doi.org/10. 1093/jac/dkt419.
13. Cheng HY, Chen YF, Peng HL. 2010. Molecular characterization of the PhoPQ-PmrD-PmrAB mediated pathway regulating polymyxin B resistance in Klebsiella pneumoniae CG43. J. Biomed. Sci. 17:60-76. http://dx.doi.org/10.1186/ 1423-0127-17-60.
14. Chen HD, Groisman EA. 2013. The biology of the PmrA/PmrB twocomponent system: the major regulator of lipopolysaccharide modifications. Annu. Rev. Microbiol. 67:83-112. http://dx.doi.org/10.1146/annurev-micro-092412-155751.
15. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
16. Clinical and Laboratory Standards Institute. 2012. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard-9th ed. CLSI document M07-A9. Clinical and Laboratory Standards Institute, Wayne, PA.
17. Simpson JT, Wong K, Jackman SD, Schein JE, Jones S J M, Birol I. 2009. ABySS: a parallel assembler for short read sequence data. Genome Res. 19:1117-1123. http://dx.doi.org/10.1101/gr.089532.108.
18. Chang AC, Cohen SN. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134:1141-1156.
19. ΔΔCT method. Methods 25:402-408. http://dx.doi.org/10.1006/meth.2001.1262.
20. Beceiro A, Moreno A, Fernández N, Vallejo JA, Aranda J, Adler B, Harper M, Boyce JD, Bou G. 2014. Biological cost of different mechanisms of colistin resistance and their impact on virulence in Acinetobacter baumannii. Antimicrob. Agents Chemother. 58:518-526. http://dx.doi.org/10.1128/AAC.01597- 13.
21. López-Rojas R, McConnell MJ, Jiménez-Mejías ME, Domínguez-Herrera J, Fernández-Cuenca F, Pachón J. 2013. Colistin resistance in a clinical Acinetobacter baumannii strain appearing after colistin treatment: effect on virulence and bacterial fitness. Antimicrob. Agents Chemother. 57:4587-4589. http://dx.doi.org/10.1128/AAC.00543-13.
22. Lacour S, Doublet P, Obadia B, Cozzone AJ, Grangeasse C. 2006. A novel role for protein-tyrosine kinase Etk from Escherichia coli K-12 related to polymyxin resistance. Res. Microbiol. 157:637-641. http://dx.doi.org/10.1016/j. resmic.2006.01.003.
23. Lacour S, Bechet E, Cozzone AJ, Mijakovic I, Grangeasse C. 2008. Tyrosine phosphorylation of the UDP-glucose dehydrogenase of Escherichia coli is at the crossroads of colanic acid synthesis and polymyxin resistance. PLoS One 3:e3053. http://dx.doi.org/10.1371/journal.pone.0003053.
24. Adams MD, Nickel GC, Bajaksouzian S, Lavender H, Murthy AR, Jacobs MR, Bonomo RA. 2009. Resistance to colistin in Acinetobacter baumannii associated with mutations in the PmrAB two-component system. Antimicrob. Agents Chemother. 53:3628-3634. http://dx.doi.org/10.1128/AAC.00284-09.
25. Lesho E, Yoon EJ, McGann P, Snesrud E, Kwak Y, Milillo M, Onmus-Leone F, Preston L, St Clair K, Nikolich M, Viscount H, Wortmann G, Zapor M, Grillot-Courvalin C, Courvalin P, Clifford R, Waterman PE. 2013. Emergence of colistin-resistance in extremely drug-resistant Acinetobacter baumannii containing a novel pmrCAB operon during colistin therapy of wound infections. J. Infect. Dis. 208:1142-1151. http://dx.doi.org/10.1093/infdis/jit293.
26. Beceiro A, Llobet E, Aranda J, Bengoechea JA, Doumith M, Hornsey M, Dhanji H, Chart H, Bou G, Livermore DM, Woodford N. 2011. Phosphoethanolamine modification of lipid A in colistin-resistant variants of Acinetobacter baumannii mediated by the pmrAB two-component regulatory system. Antimicrob. Agents Chemother. 55:3370-3379. http://dx.doi.org/10.1128/AAC.00079-11.
27. Moskowitz SM, Brannon MK, Dasgupta N, Pier M, Sgambati N, Miller AK, Selgrade SE, Miller SI, Denton M, Conway SP, Johansen HK, Høiby N. 2012. PmrB mutations promote polymyxin resistance of Pseudomonas aeruginosa isolated from colistin-treated cystic fibrosis patients. Antimicrob. Agents Chemother. 56:1019-1030. http://dx.doi.org/10.1128/AAC.05829-11.
28. Choi MJ, Ko KS. 2014. Mutant prevention concentrations of colistin for Acinetobacter baumannii, Pseudomonas aeruginosa and Klebsiella pneumoniae clinical isolates. J. Antimicrob. Chemother. 69:275-277. http://dx.doi.org/10. 1093/jac/dkt315.
29. Wösten MM, Kox LF, Chamnongpol S, Soncini FC, Groisman EA. 2000. Asignal transduction system that responds to extracellular iron. Cell 103:113-125. http://dx.doi.org/10.1016/S0092-8674 (00) 00092-1.
30. López-Rojas R, Domínguez-Herrera J, McConnell MJ, Docobo-Peréz F, Smani Y, Fernández-Reyes M, Rivas L, Pachón J. 2011. Impaired virulence and in vivo fitness of colistin-resistant Acinetobacter baumannii J. Infect. Dis. 203:545-548. http://dx.doi.org/10.1093/ infdis/jiq086.
31. Llobet E, Campos MA, Giménez P, Moranta D, Bengoechea JA. 2011. Analysis of the networks controlling the antimicrobial-peptidedependent induction of Klebsiella pneumoniae virulence factors. Infect. Immun. 79:3718-3732. http://dx.doi.org/10.1128/IAI.05226-11.