Mutational activation of the AmgRS two-component system in aminoglycoside-resistant pseudomonas aeruginosa

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 5, 2013, Pages 2243-2251

  Ho Fung Lau, Calvin ^a   Fraud, Sebastien ^a   Jones, Marcus ^b   Peterson, Scott N ^b   Poole, Keith ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b J CRAIG VENTER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIKACIN; BACTERIAL RNA; CHLORAMPHENICOL; ERYTHROMYCIN; GENTAMICIN; NEOMYCIN; PAROMOMYCIN; SPECTINOMYCIN; TETRACYCLINE; TOBRAMYCIN;

AGAR GEL ELECTROPHORESIS; AMINOGLYCOSIDE RESISTANT PSEUDOMONAS AERUGINOSA; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL MEMBRANE; BACTERIAL MUTATION; BACTERIAL STRAIN; GAIN OF FUNCTION MUTATION; GENE ACTIVATION; GENE EXPRESSION; GENE SEQUENCE; MINIMUM INHIBITORY CONCENTRATION; MISSENSE MUTATION; NONHUMAN; OPERON; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; SITE DIRECTED MUTAGENESIS; WILD TYPE;

AMINOGLYCOSIDES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; HUMANS; MUTATION; OPERON; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS;

EID: 84876264401     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00170-13     Document Type: Article

References (72)

1. Hidron AI, Edwards JR, Patel J, Horan TC, Sievert DM, Pollock DA, Fridkin SK. 2008. NHSN annual update: antimicrobial-resistant pathogens associated with healthcare associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007. Infect. Control Hosp. Epidemiol. 29:996-1011.
2. Zhanel GG, DeCorby M, Adam H, Mulvey MR, McCracken M, Lagacé-Wiens P, Nichol KA, Wierzbowski A, Baudry PJ, Tailor F, Karlowsky JA, Walkty A, Schweizer F, Johnson J, the Canadian Antimicrobial Resistance Alliance, Hoban DJ. 2010. Prevalence of antimicrobialresistant pathogens in Canadian hospitals: results of the Canadian Ward Surveillance Study (CANWARD 2008). Antimicrob. Agents Chemother. 54:4684-4693.
3. Lyczak JB, Cannon CL, Pier GB. 2002. Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15:194-222.
4. Ratjen F, Brockhaus F, Angyalosi G. 2009. Aminoglycoside therapy against Pseudomonas aeruginosa in cystic fibrosis: a review. J. Cyst. Fibros. 8:361-369.
5. Cantón R, Cobos N, De Gracia J, Baquero F, Honorato J, Gartner S, Alvarez A, Salcedo A, Oliver A, García-Quetglas E, the Spanish Consensus Group for Antimicrobial Therapy in the Cystic Fibrosis Patient. 2005. Antimicrobial therapy for pulmonary pathogenic colonisation and infection by Pseudomonas aeruginosa in cystic fibrosis patients. Clin. Microbiol. Infect. 11:690-703.
6. Poole K. 2011. Pseudomonas aeruginosa: resistance to the max. Front. Microbiol. 2:65.
7. Poole K. 2005. Aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 49:479-487.
8. Davis BD. 1987. Mechanism of bactericidal action of aminoglycosides. Microbiol. Rev. 51:341-350.
9. Davis BD, Chen LL, Tai PC. 1986. Misread protein creates membrane channels: an essential step in the bactericidal action of aminoglycosides. Proc. Natl. Acad. Sci. U. S. A. 83:6164-6168.
10. 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.
11. 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.
12. Kohanski MA, Dwyer DJ, Wierzbowski J, Cottarel G, Collins JJ. 2008. Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 135:679-690.
13. Shakil S, Khan R, Zarrilli R, Khan A. 2008. Aminoglycosides versus bacteria-a description of the action, resistance mechanism, and nosocomial battleground. J. Biomed. Sci. 15:5-14.
14. Jana S, Deb JK. 2006. Molecular understanding of aminoglycoside action and resistance. Appl. Microbiol. Biotechnol. 70:140-150.
15. Wachino JI, Arakawa Y. 2012. Exogenously acquired 16S rRNA methyltransferases found in aminoglycoside-resistant pathogenic Gramnegative bacteria: an update. Drug Resist. Updates 15:133-148.
16. Yokoyama K, Doi Y, Yamane K, Kurokawa H, Shibata N, Shibayama K, Yagi T, Kato H, Arakawa Y. 2003. Acquisition of 16S rRNA methylase gene in Pseudomonas aeruginosa. Lancet 362:1888-1893.
17. Ramirez MS, Tolmasky ME. 2010. Aminoglycoside modifying enzymes. Drug Resist. Updates 13:151-171.
18. Islam S, Jalal S, Wretlind B. 2004. Expression of the MexXY efflux pump in amikacin-resistant isolates of Pseudomonas aeruginosa. Clin. Microbiol. Infect. 10:877-883.
19. Islam S, Oh H, Jalal S, Karpati F, Ciofu O, Høiby N, Wretlind B. 2009. Chromosomal mechanisms of aminoglycoside resistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Clin. Microbiol. Infect. 15:60-66.
20. Sobel ML, McKay GA, Poole K. 2003. Contribution of the MexXY multidrug transporter to aminoglycoside resistance in Pseudomonas aeruginosa clinical isolates. Antimicrob. Agents Chemother. 47:3202-3207.
21. Westbrock-Wadman S, Sherman DR, Hickey MJ, Coulter SN, Zhu YQ, Warrener P, Nguyen LY, Shawar RM, Folger KR, Stover CK. 1999. Characterization of a Pseudomonas aeruginosa efflux pump contributing to aminoglycoside impermeability. Antimicrob. Agents Chemother. 43: 2975-2983.
22. Morita Y, Tomida J, Kawamura Y. 2012. MexXY multidrug efflux system of Pseudomonas aeruginosa. Front. Microbiol. 3:408.
23. Vettoretti L, Plésiat P, Muller C, El Garch F, Phan G, Attrée I, Ducruix A, Llanes C. 2009. Efflux unbalance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob. Agents Chemother. 53:1987-1997.
24. El'Garch F, Jeannot K, Hocquet D, Llanes-Barakat C, Plésiat P. 2007. Cumulative effects of several nonenzymatic mechanisms on the resistance of Pseudomonas aeruginosa to aminoglycosides. Antimicrob. Agents Chemother. 51:1016-1021.
25. Gallagher LA, Shendure J, Manoil C. 2011. Genome-scale identification of resistance functions in Pseudomonas aeruginosa using Tn-seq. mBio 2:e00315-10.
26. Krahn T, Gilmour C, Tilak J, Fraud S, Kerr N, Lau CHF, Poole K. 2012. Determinants of intrinsic aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 56:5591-5602.
27. Lee S, Hinz A, Bauerle E, Angermeyer A, Juhaszova K, Kaneko Y, Singh PK, Manoil C. 2009. Targeting a bacterial stress response to enhance antibiotic action. Proc. Natl. Acad. Sci. U. S. A. 106:14570-14575.
28. Hancock RE, Farmer SW, Li ZS, Poole K. 1991. Interaction of aminoglycosides with the outer membranes and purified lipopolysaccharide and OmpF porin of Escherichia coli. Antimicrob. Agents Chemother. 35: 1309-1314.
29. Kadurugamuwa JL, Lam JS, Beveridge TJ. 1993. Interaction of gentamicin with the A band and B band lipopolysaccharides of Pseudomonas aeruginosa and its possible lethal effect. Antimicrob. Agents Chemother. 37:715-721.
30. Taber HW, Mueller JP, Miller PF, Arrow AS. 1987. Bacterial uptake of aminoglycoside antibiotics. Microbiol. Rev. 51:439-457.
31. Hinz A, Lee S, Jacoby K, Manoil C. 2011. Membrane proteases and aminoglycoside antibiotic resistance. J. Bacteriol. 193:4790-4797.
32. Fraud S, Poole K. 2011. Oxidative stress induction of the mexXY multidrug efflux genes and promotion of aminoglycoside resistance development in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 55: 1068-1074.
33. Edelheit O, Hanukoglu A, Hanukoglu I. 2009. Simple and efficient site-directed mutagenesis using two single-primer reactions in parallel to generate mutants for protein structure-function studies. BMC Biotechnol. 9:61.
34. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
35. Inoue H, Nojima H, Okayama H. 1990. High efficiency transformation of Escherichia coli with plasmids. Gene 96:23-28.
36. Boyle-Vavra S, Jones M, Gourley BL, Holmes M, Ruf R, Balsam AR, Boulware DR, Kline S, Jawahir S, DeVries A, Peterson SN, Daum RS. 2011. Comparative genome sequencing of an isogenic pair of USA800 clinical methicillin-resistant Staphylococcus aureus isolates obtained before and after daptomycin treatment failure. Antimicrob. Agents Chemother. 55:2018-2025.
37. Lau CHF, Fraud S, Jones M, Peterson SN, Poole K. 2012. Reduced expression of the rplU-rpmA ribosomal protein operon in mexXYexpressing pan-aminoglycoside-resistant mutants of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 56:5171-5179.
38. Jo JTH, Brinkman FSL, Hancock REW. 2003. Aminoglycoside efflux in Pseudomonas aeruginosa: involvement of novel outer membrane proteins. Antimicrob. Agents Chemother. 47:1101-1111.
39. Morita Y, Sobel ML, Poole K. 2006. Antibiotic inducibility of the MexXY multidrug efflux system of Pseudomonas aeruginosa: involvement of the antibiotic-inducible PA5471 gene product. J. Bacteriol. 188:1847-1855.
40. Carter AP, Clemons WM, Brodersen DE, Morgan-Warren RJ, Wimberly BT, Ramakrishnan V. 2000. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407:340-348.
41. Francois B, Russell RJ, Murray JB, Aboul-ela F, Masquida B, Vicens Q, Westhof E. 2005. Crystal structures of complexes between aminoglycosides and decoding A site oligonucleotides: role of the number of rings and positive charges in the specific binding leading to miscoding. Nucleic Acids Res. 33:5677-5690.
42. Mehta R, Champney WS. 2002. 30S ribosomal subunit assembly is a target for inhibition by aminoglycosides in Escherichia coli. Antimicrob. Agents Chemother. 46:1546-1549.
43. Salian S, Matt T, Akbergenov R, Harish S, Meyer M, Duscha S, Shcherbakov D, Bernet BB, Vasella A, Westhof E, Bottger EC. 2012. Structure-activity relationships among the kanamycin aminoglycosides: role of ring I hydroxyl and amino groups. Antimicrob. Agents Chemother. 56:6104-6108.
44. Appleman JA, Stewart V. 2003. Mutational analysis of a conserved signaltransducing element: the HAMP linker of the Escherichia coli nitrate sensor NarX. J. Bacteriol. 185:89-97.
45. Giraud A, Arous S, De Paepe M, Gaboriau-Routhiau V, Bambou JC, Rakotobe S, Lindner AB, Taddei F, Cerf-Bensussan N. 2008. Dissecting the genetic components of adaptation of Escherichia coli to the mouse gut. PLoS Genet. 4:e2. doi:10.1371/journal.pgen.0040002.
46. Harlocker SL, Rampersaud A, Yang WP, Inouye M. 1993. Phenotypic revertant mutations of a new OmpR2 mutant (V203Q) of Escherichia coli lie in the envZ gene, which encodes the OmpR kinase. J. Bacteriol. 175: 1956-1960.
47. Park H, Inouye M. 1997. Mutational analysis of the linker region of EnvZ, an osmosensor in Escherichia coli. J. Bacteriol. 179:4382-4390.
48. Tokishita S, Kojima A, Mizuno T. 1992. Transmembrane signal transduction and osmoregulation in Escherichia coli: functional importance of the transmembrane regions of membrane-located protein kinase, EnvZ. J. Biochem. 111:707-713.
49. Hsing W, Russo FD, Bernd KK, Silhavy TJ. 1998. Mutations that alter the kinase and phosphatase activities of the two-component sensor EnvZ. J. Bacteriol. 180:4538-4546.
50. Mizuno T, Mizushima S. 1990. Signal transduction and gene regulation through the phosphorylation of two regulatory components: the molecular basis for the osmotic regulation of the porin genes. Mol. Microbiol. 4:1077-1082.
51. Forst S, Comeau D, Norioka S, Inouye M. 1987. Localization and membrane topology of EnvZ, a protein involved in osmoregulation of OmpF and OmpC in Escherichia coli. J. Biol. Chem. 262:16433-16438.
52. Park H, Saha SK, Inouye M. 1998. Two-domain reconstitution of a functional protein histidine kinase. Proc. Natl. Acad. Sci. U. S. A. 95:6728-6732.
53. Ames P, Parkinson JS. 1988. Transmembrane signaling by bacterial chemoreceptors: E. coli transducers with locked signal output. Cell 55: 817-826.
54. del Carmen Burón-Barral M, Gosink KK, Parkinson JS. 2006. Loss-and gain-of-function mutations in the F1-HAMP region of the Escherichia coli aerotaxis transducer Aer. J. Bacteriol. 188:3477-3486.
55. Dunin-Horkawicz S, Lupas AN. 2010. Comprehensive analysis of HAMP domains: implications for transmembrane signal transduction. J. Mol. Biol. 397:1156-1174.
56. Leatham-Jensen MP, Frimodt-Moller J, Adediran J, Mokszycki ME, Banner ME, Caughron JE, Krogfelt KA, Conway T, Cohen PS. 2012. The streptomycin-treated mouse intestine selects Escherichia coli envZ mis-sense mutants that interact with dense and diverse intestinal microbiota. Infect. Immun. 80:1716-1727.
57. Rainwater S, Silverman PM. 1990. The Cpx proteins of Escherichia coli K-12: evidence that cpxA, ecfB, ssd, and eup mutations all identify the same gene. J. Bacteriol. 172:2456-2461.
58. Sun S, Berg OG, Roth JR, Andersson DI. 2009. Contribution of gene amplification to evolution of increased antibiotic resistance in Salmonella typhimurium. Genetics 182:1183-1195.
59. Kato Y, Suzuki T, Ida T, Maebashi K. 2010. Genetic changes associated with glycopeptide resistance in Staphylococcus aureus: predominance of amino acid substitutions in YvqF/VraSR. J. Antimicrob. Chemother. 65: 37-45.
60. Kato Y, Suzuki T, Ida T, Maebashi K, Sakurai M, Shiotani J, Hayashi I. 2008. Microbiological and clinical study of methicillin-resistant Staphylococcus aureus (MRSA) carrying VraS mutation: changes in susceptibility to glycopeptides and clinical significance. Int. J. Antimicrob. Agents 31:64-70.
61. Howden BP, Stinear TP, Allen DL, Johnson PD, Ward PB, Davies JK. 2008. Genomic analysis reveals a point mutation in the two-component sensor gene graS that leads to intermediate vancomycin resistance in clinical Staphylococcus aureus. Antimicrob. Agents Chemother. 52:3755-3762.
62. Macfarlane EL, Kwasnicka A, Hancock RE. 2000. Role of Pseudomonas aeruginosa PhoP-PhoQ in resistance to antimicrobial cationic peptides and aminoglycosides. Microbiology 146:2543-2554.
63. McPhee JB, Lewenza S, Hancock RE. 2003. Cationic antimicrobial peptides activate a two-component regulatory system, PmrA-PmrB, that regulates resistance to polymyxin B and cationic antimicrobial peptides in Pseudomonas aeruginosa. Mol. Microbiol. 50:205-217.
64. Richards SM, Strandberg KL, Gunn JS. 2010. Salmonella-regulated lipopolysaccharide modifications. Subcell. Biochem. 53:101-122.
65. Sun S, Negrea A, Rhen M, Andersson DI. 2009. Genetic analysis of colistin resistance in Salmonella enterica serovar Typhimurium. Antimicrob. Agents Chemother. 53:2298-2305.
66. Moskowitz SM, Brannon MK, Dasgupta N, Pier M, Sgambati N, Miller AK, Selgrade SE, Miller SI, Denton M, Conway SP, Johansen HK, Hoiby N. 2012. PmrB mutations promote polymyxin resistance of Pseudomonas aeruginosa isolated from colistin-treated cystic fibrosis patients. Antimicrob. Agents Chemother. 56:1019-1030.
67. Lee JY, Lim MH, Heo ST, Ko KS. 2012. Repeated isolation of Pseudomonas aeruginosa isolates resistant to both polymyxins and carbapenems from 1 patient. Diagn. Microbiol. Infect. Dis. 72:267-271.
68. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. 1992. Short protocols in molecular biology, 2nd ed. John Wiley & Sons, Inc., New York, NY.
69. Simon R, Priefer U, Puhler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gramnegative bacteria. Nat. Biotechnol. 1:784-791.
70. Masuda N, Ohya S. 1992. Cross-resistance to meropenem, cephems, and quinolones in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 36:1847-1851.
71. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
72. Notredame C, Higgins DG, Heringa J. 2000. T-coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302:205-217.