In vivo emergence of colistin resistance in Klebsiella pneumoniae producing KPC-type carbapenemases mediated by insertional inactivation of the PhoQ/PhoP mgrB regulator

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 11, 2013, Pages 5521-5526

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

CARBAPENEMASE; COLISTIN;

ACINETOBACTER BAUMANNII; AEROSOL; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM ISOLATE; CONTROLLED STUDY; DELETION MUTANT; GENE; GENE DELETION; GENE INACTIVATION; GENE INSERTION SEQUENCE; GENETIC COMPLEMENTATION; GENOME ANALYSIS; HUMAN; IN VITRO SELECTION; IN VIVO STUDY; KLEBSIELLA PNEUMONIAE; MGRB GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PRIORITY JOURNAL; REGULATOR GENE; UPREGULATION; WILD TYPE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAMASES; COLISTIN; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REGULATOR; HUMANS; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; MEMBRANE PROTEINS; MUTAGENESIS, INSERTIONAL; OPERON; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84885909781     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01480-13     Document Type: Article

References (35)

1. Yigit H, Queenan AM, Anderson GJ, Domenech-Sanchez A, Biddle JW, Steward CD, Alberti S, Bush K, Tenover FC. 2001. Novel carbapenem-hydrolyzing β-lactamase, KPC-1, from a carbapenem-resistant strain of Klebsiella pneumoniae. Antimicrob. Agents Chemother. 45:1151-1161.
2. Nordmann P, Naas T, Poirel L. 2011. Global spread of carbapenemaseproducing Enterobacteriaceae. Emerg. Infect. Dis. 17:1791-1798.
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. 2012. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin. Microbiol. Infect. 18:413-431.
4. 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.
5. Giani T, Pini B, Arena F, Conte V, Bracco S, Migliavacca R, Pantosti A, Pagani L, Luzzaro F, Rossolini G. 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: pii-20489. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId-20489.
6. Borer A, Saidel-Odes L, Riesenberg K, Eskira S, Peled N, Nativ R, Schlaeffer F, Sherf M. 2009. Attributable mortality rate for carbapenemresistant Klebsiella pneumoniae bacteremia. Infect. Control Hosp. Epidemiol. 30:972-976.
7. Falagas ME, Karageorgopoulos DE, Nordmann P. 2011. Therapeutic options for infections with Enterobacteriaceae producing carbapenemhydrolyzing enzymes. Future Microbiol. 6:653-666.
8. Qureshi ZA, Paterson DL, Potoski BA, Kilayko MC, Sandovsky G, Sordillo E, Polsky B, Adams-Haduch JM, Doi Y. 2012. Treatment outcome of bacteremia due to KPC-producing Klebsiella pneumoniae: superiority of combination antimicrobial regimens. Antimicrob. Agents Chemother. 56:2108-2113.
9. Tumbarello M, Viale P, Viscoli C, Trecarichi EM, Tumietto F, Marchese A, Spanu T, Ambretti S, Ginocchio F, Cristini F, Losito AR, Tedeschi S, Cauda R, Bassetti M. 2012. Predictors of mortality in bloodstream infections caused by Klebsiella pneumoniae carbapenemaseproducing K. pneumoniae: importance of combination therapy. Clin. Infect. Dis. 55:943-950.
10. Bogdanovich T, Adams-Haduch JM, Tian GB, Nguyen MH, Kwak EJ, Muto CA, Doi Y. 2011. Colistin-resistant, Klebsiella pneumoniae carbapenemase (KPC)-producing Klebsiella pneumoniae belonging to the international epidemic clone ST258. Clin. Infect. Dis. 53:373-376.
11. Hrabak J, Niemczykova J, Chudackova E, Fridrichova M, Studentova V, Cervena D, Urbaskova P, Zemlickova H. 2011. KPC-2-producing Klebsiella pneumoniae isolated from a Czech patient previously hospitalized in Greece and in vivo selection of colistin resistance. Folia Microbiol. (Praha) 56:361-365.
12. Mammina C, Bonura C, Di BF, Aleo A, Fasciana T, Sodano C, Saporito MA, Verde MS, Tetamo R, Palma DM. 2012. Ongoing spread of colistinresistant Klebsiella pneumoniae in different wards of an acute general hospital, Italy, June to December 2011. Euro Surveill. 17:pii-20248. http://www.eurosurveillance. org/ViewArticle.aspx?ArticleId-20248.
13. 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.
14. Helander IM, Kato Y, Kilpelainen I, Kostiainen R, Lindner B, Nummila K, Sugiyama T, Yokochi T. 1996. Characterization of lipopolysaccharides of polymyxin-resistant and polymyxin-sensitive Klebsiella pneumoniae O3. Eur. J. Biochem. 237:272-278.
15. 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.
16. Mitrophanov AY, Jewett MW, Hadley TJ, Groisman EA. 2008. Evolution and dynamics of regulatory architectures controlling polymyxin B resistance in enteric bacteria. PLoS Genet. 4:e1000233. doi:10.1371/journal.pgen.1000233.
17. Groisman EA. 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183:1835-1842.
18. Bader MW, Sanowar S, Daley ME, Schneider AR, Cho U, Xu W, Klevit RE, Le MH, Miller SI. 2005. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122:461-472.
19. Prost LR, Daley ME, Le SV, Bader MW, Le MH, Klevit RE, Miller SI. 2007. Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol. Cell 26:165-174.
20. Gunn JS. 2008. The Salmonella PmrAB regulon: lipopolysaccharide modifications, antimicrobial peptide resistance and more. Trends Microbiol. 16:284-290.
21. Chen HD, Groisman EA. 17 June 2013. The biology of the PmrA/PmrB two-component system: the major regulator of lipolysaccharide modifications. Annu. Rev. Microbiol. [Epub ahead of print.] doi:10.1146/annurev-micro-092412- 155751.
22. Lippa AM, Goulian M. 2009. Feedback inhibition in the PhoQ/PhoP signaling system by a membrane peptide. PLoS Genet. 5:e1000788. doi:10.1371/journal.pgen. 1000788.
23. Diancourt L, Passet V, Verhoef J, Grimont PA, Brisse S. 2005. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J. Clin. Microbiol. 43:4178-4182.
24. Yuan M, Aucken H, Hall LM, Pitt TL, Livermore DM. 1998. Epidemiological typing of klebsiellae with extended-spectrum β-lactamases from European intensive care units. J. Antimicrob. Chemother. 41:527-539.
25. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
26. 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.
27. D'Andrea MM, Giani T, D'Arezzo S, Capone A, Petrosillo N, Visca P, Luzzaro F, Rossolini GM. 2009. Characterization of pABVA01, a plasmid encoding the OXA-24 carbapenemase from Italian isolates of Acinetobacter baumannii. Antimicrob. Agents Chemother. 53:3528-3533.
28. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I. 2009. ABySS: a parallel assembler for short read sequence data. Genome Res. 19:1117-1123.
29. Auch AF, Klenk HP, Goker M. 2010. Standard operating procedure for calculating genome-to-genome distances based on high-scoring segment pairs. Stand. Genomic Sci. 2:142-148.
30. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75. doi:10.1186/1471- 2164-9-75.
31. Liu P, Li P, Jiang X, Bi D, Xie Y, Tai C, Deng Z, Rajakumar K, Ou HY. 2012. Complete genome sequence of Klebsiella pneumoniae subsp. pneumoniae HS11286, a multidrug-resistant strain isolated from human sputum. J. Bacteriol. 194:1841-1842.
32. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421. doi:10.1186/1471-2105-10-421.
33. Snitkin ES, Zelazny AM, Thomas PJ, Stock F, Henderson DK, Palmore TN, Segre JA. 2012. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci. Transl. Med. 4:148ra116.
34. CT method. Methods 25: 402-408.
35. Kroger M, Hobom G. 1982. Structural analysis of insertion sequence IS5. Nature 297:159-162.