Characterization of the polymyxin B resistome of Pseudomonas aeruginosa

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 1, 2013, Pages 110-119

  Fernández, Lucía ^a   Álvarez Ortega, Carolina ^b   Wiegand, Irith ^a,d   Olivares, Jorge ^b   Kocíncová, Dana ^c   Lam, Joseph S ^c   Martínez, José Luis ^b   Hancock, Robert E W ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^c UNIVERSITY OF GUELPH   (Canada)

^d AiCuris GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL CATIONIC PEPTIDE; ARABINOSE; BACTERIUM LIPOPOLYSACCHARIDE; BETA LACTAM ANTIBIOTIC; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CIPROFLOXACIN; COLISTIN; INDOLICIDIN; LIPID A; MAGNESIUM; O ANTIGEN; POLYMYXIN B; TOBRAMYCIN;

AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL OUTER MEMBRANE; BACTERIUM MUTANT; CONTROLLED STUDY; GENE IDENTIFICATION; GENE INSERTION; GENE MUTATION; GENETIC SCREENING; MEMBRANE PERMEABILITY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; TRANSPOSON; WESTERN BLOTTING; WILD TYPE;

ANTI-BACTERIAL AGENTS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, BACTERIAL; GENE LIBRARY; GENES, BACTERIAL; LIPOPOLYSACCHARIDES; MUTATION; POLYMYXIN B; PSEUDOMONAS AERUGINOSA; TRANSCRIPTOME;

EID: 84872031103     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01583-12     Document Type: Article

References (50)

1. Bonomo RA, Szabo D. 2006. Mechanisms of multidrug resistance in Acinetobacter species and Pseudomonas aeruginosa. Clin. Infect. Dis. 43:SS49-SS56.
2. Lyczak JB, Cannon CL, Pier GB. 2000. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2:1051-1060.
3. Rowe SM, Miller S, Sorscher EJ. 2005. Cystic fibrosis. N. Engl. J. Med. 352:1992-2001.
4. Hancock REW, Speert DP. 2000. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and impact on treatment. Drug Resist. Updat. 3:247-255.
5. Falagas ME, Kasiakou SK. 2005. Colistin: the revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections. Clin. Infect. Dis. 40:1333-1341.
6. Zhang L, Dhillon P, Yan H, Farmer S, Hancock REW. 2000. Interactions of bacterial cationic peptide antibiotics with outer and cytoplasmic membranes of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 44:3317-3321.
7. Falagas ME, Rafailidis PI, Matthaiou DK. 2010. Resistance to polymyxins: mechanisms, frequency and treatment options. Drug Resist. Updat. 13:132-138.
8. Miller AK, Brannon MK, Stevens L, Johansen HK, Selgrade SE, Miller SI, Høiby N, Moskowitz SM. 2011. PhoQ mutations promote lipid A modification and polymyxin resistance of Pseudomonas aeruginosa found in colistin-treated cystic fibrosis patients. Antimicrob. Agents Chemother. 55:5761-5779.
9. 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.
10. Muller C, Plésiat P, Jeannot K. 2011. A two-component regulatory system interconnects resistance to polymyxins, aminoglycosides, fluoroquinolones, and β-lactams in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 55:1211-1221.
11. Fernández L, Gooderham WJ, Bains M, McPhee JB, Wiegand I, Hancock REW. 2010. Adaptive resistance to the "last hope" antibiotics polymyxin B and colistin in Pseudomonas aeruginosa is mediated by the novel two-component regulatory system ParR-ParS. Antimicrob. Agents Chemother. 54:3372-3382.
12. Macfarlane ELA, Kwasnicka A, Ochs MM, Hancock REW. 1999. PhoP-PhoQ homologues in Pseudomonas aeruginosa regulate expression of the outer-membrane protein OprH and polymyxin B resistance. Mol. Microbiol. 34:305-316.
13. McPhee JB, Lewenza S, Hancock REW. 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.
14. Alvarez-Ortega C, Wiegand I, Olivares J, Hancock REW, Martínez JL. 2010. Genetic determinants involved in the susceptibility of Pseudomonas aeruginosa to beta-lactam antibiotics. Antimicrob. Agents Chemother. 54:4159-4167.
15. Breidenstein EBM, Khaira BK, Wiegand I, Overhage J, Hancock REW. 2008. Complex ciprofloxacin resistome revealed by screening a Pseudomonas aeruginosa mutant library for altered susceptibility. Antimicrob. Agents Chemother. 52:4486-4491.
16. De Groote VN, Verstraeten N, Fauvart M, Kint CI, Verbeeck AM, Beullens S, Cornelis P, Michiels J. 2009. Novel persistence genes in Pseudomonas aeruginosa identified by high-throughput screening. FEMS Microbiol. Lett. 297:73-79.
17. Dötsch A, Becker T, Pommerenke C, Magnowska Z, Jänsch Häussler LS. 2009. Genomewide identification of genetic determinants of antimicrobial drug resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 53:2522-2531.
18. Gallagher LA, Shendure J, Manoil C. 2011. Genome-scale identification of resistance functions in Pseudomonas aeruginosa using Tn-seq. mBio 2(1):e00315-10. doi:10.1128/mBio.00315-10.
19. Schurek KN, Marr AK, Taylor PK, Wiegand I, Semenec L, Khaira BK, Hancock REW. 2008. Novel genetic determinants of low-level aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 52:4213-4219.
20. Fernández L, Breidenstein EBM, Hancock REW. 2011. Creeping baselines and adaptive resistance to antibiotics. Drug Resist. Updat. 14:1-21.
21. Liberati NT, Urbach JM, Miyata S, Lee DG, Drenkard E, Wu G, Villanueva J, Wei T, Ausubel FM. 2006. An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc. Natl. Acad. Sci. U. S. A. 103:2833-2838.
22. Fajardo A, Martínez-MartíN N, Mercadillo M, Galán JC, Ghysels B, Matthijs S, Cornelis P, Wiehlmann L, Tümmler B, Baquero F, Martínez JL. 2008. The neglected intrinsic resistome of bacterial pathogens. PLoS One 3:e1619. doi:10.1371/journal.pone.0001619.
23. Wiegand I, Hilpert K, Hancock REW. 2008. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3:163-175.
24. 2+-induced gene regulation in Pseudomonas aeruginosa. J. Bacteriol. 188:3995-4006.
25. Hitchcock PJ, Brown TM. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154:269-277.
26. Fomsgaard A, Freudenberg MA, Galanos C. 1990. Modification of the silver staining technique to detect lipopolysaccharide in polyacrylamide gels. J. Clin. Microbiol. 28:2627-2631.
27. Zhou Z, Lin S, Cotter RJ, Raetz CR. 1999. Lipid A modifications characteristic of Salmonella typhimurium are induced by NH4VO3 in Escherichia coli K12. Detection of 4-amino-4-deoxy-L-arabinose, phosphoethanolamine and palmitate J. Biol. Chem. 274:18503-18514.
28. Moore RA, Bates NC, Hancock REW. 1986. Interaction of polycationic antibiotics with Pseudomonas aeruginosa lipopolysaccharide and lipid A studied by using dansyl-polymyxin. Antimicrob. Agents Chemother. 29:496-500.
29. Loh B, Grant C, Hancock REW. 1984. Use of the fluorescent probe 1-N-phenylnaphthylamine to study the interactions of aminoglycoside antibiotics with the outer membrane of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 26:546-551.
30. Rozen S, Skaletsky HJ. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132:365-386.
31. Winsor GL, Lam DK, Fleming L, Lo R, Whiteside MD, Yu NY, Hancock RE, Brinkman FS. 2011. Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 39:D596-D600.
32. Elzer PH, Kovach ME, Phillips RW, Robertson GT, Peterson KM, Roop II RM. 1995. In vivo and in vitro stability of the broad host-range cloning vector pBBR1MCS in six Brucella species. Plasmid 33:51-57.
33. Baquero F. 2001. Low-level antibacterial resistance: a gateway to clinical resistance. Drug Resist. Updat. 4:93-105.
34. Gooderham WJ, Gellatly SL, Sanschagrin F, McPhee JB, Bains M, Cosseau C, Levesque RC, Hancock REW. 2009. The sensor kinase PhoQ mediates virulence in Pseudomonas aeruginosa. Microbiology 155:699-711.
35. Barrow K, Kwon DH. 2009. Alterations in two-component regulatory systems of phoPQ and pmrAB are associated with polymyxin B resistance in clinical isolates of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 53:5150-5154.
36. Masoud H, Altman E, Richards JC, Lam JS. 1994. A general strategy for structual analysis of the oligosaccharide region of lipopolysaccharides. Structure of oligosaccharide component of Pseudomonas aeruginosa IATS serotype O6 mutant R5 rough-type lipopolysaccharide. Biochem. 33:10568-10578.
37. Priebe GP, Dean CR, Zaidi T, Meluleni GJ, Coleman FT, Coutinho YS, Noto MJ, Urban TA, Pier GB, Goldberg JB. 2004. The galU Gene of Pseudomonas aeruginosa is required for corneal infection and efficient systemic spread following pneumonia but not for infection confined to the lung. Infect. Immun. 72:4224-4232.
38. Lin J, Wang Y, Hoang KV. 2009. Systematic identification of genetic loci required for polymyxin resistance in Campylobacter jejuni using an efficient in vivo transposon mutagenesis system. Foodborne Pathog. Dis. 6:173-185.
39. Jiang SS, Lin TY, Wang WB, Liu MC, Hsueh PR, Liaw SJ. 2010. Characterization of UDP-glucose dehydrogenase and UDP-glucose pyrophosphorylase mutants of Proteus mirabilis: defectiveness in polymyxin B resistance, swarming, and virulence. Antimicrob. Agents Chemother. 54:2000-2009.
40. Klein KA, Fukuto HS, Pelletier M, Romanov G, Grabenstein JP, Palmer LE, Ernst R, Bliska JB. 2012. A transposon site hybridization screen identifies galU and wecBC as important for survival of Yersinia pestis in murine macrophages. J. Bacteriol. 194:653-662.
41. Kocíncová D, Ostler SL, Anderson EM, Lam JS. 2012. Rhamnosyltransferase genes migA and wapR are regulated in a differential manner to modulate the quantities of core oligosaccharide glycoforms produced by Pseudomonas aeruginosa. J. Bacteriol. 194:4295-4300.
42. Poon KK, Westman EL, Vinogradov E, Jin S, Lam JS. 2008. Functional characterization of MigA and WapR: putative rhamnosyltransferases involved in outer core oligosaccharide biosynthesis of Pseudomonas aeruginosa. J. Bacteriol. 190:1857-1865.
43. Veeranagouda Y, Lee K, Cho AR, Cho K, Anderson EM, Lam JS. 2011. Ssg, a putative glycosyltransferase, functions in lipo- and exopolysaccharide biosynthesis and cell surface-related properties in Pseudomonas alkylphenolia. FEMS Microbiol. Lett. 315:38-45.
44. Sperandeo P, Lau FK, Carpentieri A, De Castro C, Molinaro A, Dehò G, Silhavy TJ, Polissi A. 2008. Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J. Bacteriol. 190:4460-4469.
45. Rahim R, Burrows LL, Monteiro MA, Perry MB, Lam JS. 2000. Involvement of the rml locus in core oligosaccharide and Opolysaccharide assembly in Pseudomonas aeruginosa. Microbiology 146:2803-2814.
46. Choudhury B, Carlson RW, Goldberg JB. 2005. The structure of the lipopolysaccharide from a galU mutant of Pseudomonas aeruginosa serogroup-O11. Carbohydr. Res. 340:2761-2772.
47. Dean CR, Goldberg JB. 2002. Pseudomonas aeruginosa galU is required for a complete lipopolysaccharide core and repairs a secondary mutation in a PA103 (serogroup O11) wbpM mutant. FEMS Microbiol. Lett. 210:277-283.
48. Yokota S, Fujii N. 2007. Contributions of the lipopolysaccharide outer core oligosaccharide region on the cell surface properties of Pseudomonas aeruginosa. Comp. Immunol. Microbiol. Infect. Dis. 30:97-109.
49. Nesper J, Lauriano CM, Klose KE, Kapfhammer D, Kraiss A, Reidl J. 2001. Characterization of Vibrio cholerae O1 El tor galU and galE mutants: influence on lipopolysaccharide structure, colonization, and biofilm formation. Infect. Immun. 69:435-445.
50. Lam JS, Taylor VL, Islam ST, Hao Hao Y, Kocíncová D. 2011. Genetics and functional diversity of Pseudomonas aeruginosa lipopolysaccharide. Front. Microbiol. 2:118.