Targeting a bacterial stress response to enhance antibiotic action

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 34, 2009, Pages 14570-14575

  Lee, Samuel ^a   Hinz, Aaron ^a   Bauerle, Elizabeth ^a   Angermeyer, Angus ^a   Juhaszova, Katy ^a   Kaneko, Yukihiro ^a   Singh, Pradeep K ^a   Manoil, Colin ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

2 component regulator; AmgRS; Aminoglycoside; CpxRA; Pseudomonas aeruginosa

Indexed keywords

AMGRS; AMINOGLYCOSIDE ANTIBIOTIC AGENT; REGULATOR PROTEIN; TOBRAMYCIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM; BIOFILM; DRUG EFFICACY; DRUG TARGETING; GENE CONTROL; GENE FUNCTION; GENE INACTIVATION; GENE MUTATION; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; STRESS; TRANSCRIPTION INITIATION; TRANSPOSON; VIRULENCE;

AMINOGLYCOSIDES; ANIMALS; ANTI-BACTERIAL AGENTS; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; MICE; MICE, INBRED C57BL; MICROBIAL SENSITIVITY TESTS; MUTAGENESIS, INSERTIONAL; MUTATION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; TOBRAMYCIN; VIRULENCE;

BACTERIA (MICROORGANISMS); MUS; PSEUDOMONAS AERUGINOSA;

EID: 70149120111     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0903619106     Document Type: Article

References (53)

1. Norrby SR, Nord CE, Finch R (2005) Lack of development of new antimicrobial drugs: a potential serious threat to public health. Lancet Infect Dis 5:115-119.
2. Flamm RK, et al. (2004) Factors associated with relative rates of antibiotic resistance in Pseudomonas aeruginosa isolates tested in clinical laboratories in the United States from 1999 to 2002. Antimicrob Agents Chemother 48:2431-2436.
3. Prince AS (2002) Biofilms, antimicrobial resistance, and airway infection. N Engl JMed 347:1110-1111.
4. Parsek MR, Singh PK (2003) Bacterial biofilms: An emerging link to disease pathogenesis. Annu Rev Microbiol 57:677-701.
5. Mackenzie I, Lever A (2007) Management of sepsis. BMJ 335:929-932.
6. Monaghan RL, Barrett JF (2006) Antibacterial drug discovery-then, now and the genomics future. Biochem Pharmacol 71(7):901-909.
7. Dougherty TJ, Barrett JF, Pucci M (2003) Genomics-based approaches to novel antimicrobial target discovery. Microbial Genomics and Drug Discovery, ed Dougherty TJaP, S. J. (Marcel Dekker, Inc, New York), pp 71-96.
8. Silver LL (2007) Multi-targeting by monotherapeutic antibacterials. Nat Rev Drug Discov 6:41-55.
9. Projan SJ, Bradford PA (2007) Late stage antibacterial drugs in the clinical pipeline. Curr Opin Microbiol 10:441-446.
10. Payne DJ, Gwynn MN, Holmes DJ, Pompliano DL (2007) Drugs for bad bugs: Confronting the challenges of antibacterial discovery. Nat Rev Drug Discov 6:29-40.
11. Bumann D (2008) Has nature already identified all useful antibacterial targets? Curr Opin Microbiol 11:387-392.
12. Cottarel G, Wierzbowski J (2007) Combination drugs, an emerging option for antibacterial therapy. Trends Biotechnol 25:547-555. (Pubitemid 350138177)
13. Lomovskaya O, Bostian KA (2006) Practical applications and feasibility of efflux pump inhibitors in the clinic - a vision for applied use. Biochem Pharmacol 71:910-918. (Pubitemid 43306783)
14. Tamae C, et al. (2008) Determination of antibiotic hypersensitivity among 4,000 single-gene-knockout mutants of Escherichia coli. J Bacteriol 190:5981-5988.
15. Breidenstein EB, Khaira BK, Wiegand I, Overhage J, Hancock RE (2008) Complex ciprofloxacin resistome revealed by screening a Pseudomonas aeruginosa mutant library for altered susceptibility. Antimicrob Agents Chemother 52:4486-4491.
16. Fajardo A, et al. (2008) The neglected intrinsic resistome of bacterial pathogens. PLoS ONE 3:e1619. (Pubitemid 351865272)
17. Merlo CA, et al. (2007) Incidence and risk factors for multiple antibiotic-resistant Pseudomonas aeruginosa in cystic fibrosis. Chest 132:562-568.
18. Gibson RL, Burns JL, Ramsey BW (2003) Pathophysiology and management of pulmonary infections in cystic fibrosis. Am J Respir Crit Care Med 168:918-951. (Pubitemid 37267172)
19. Jacobs MA, et al. (2003) Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 100:14339-14344. (Pubitemid 37499238)
20. 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. (Pubitemid 43346863)
21. Poole K (2005) Aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 49:479-487.
22. 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.
23. Kaneko Y, Thoendel M, Olakanmi O, Britigan BE, Singh PK (2007) The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest 117:877-888. (Pubitemid 46556744)
24. Walters MC, III, Roe F, Bugnicourt A, Franklin MJ, Stewart PS (2003) Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother 47:317-323. (Pubitemid 36070381)
25. Smith EE, et al. (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103:8487-8492. (Pubitemid 43838482)
26. Doi Y, Ghilardi AC, Adams J, de Oliveira Garcia D, Paterson DL (2007) High prevalence of metallo-beta-lactamase and 16S rRNA methylase coproduction among imipenem-resistant Pseudomonas aeruginosa isolates in Brazil. Antimicrob Agents Chemother 51:3388-3390. (Pubitemid 350067560)
27. Oshima T, et al. (2002) Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Mol Microbiol 46:281-291. (Pubitemid 35231964)
28. Yamamoto K, Ishihama A (2006) Characterization of copper-inducible promoters regulated by CpxA/CpxR in Escherichia coli. Biosci Biotechnol Biochem 70:1688-1695. (Pubitemid 44124928)
29. De Wulf P, McGuire AM, Liu X, Lin EC (2002) Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P in Escherichia coli. J Biol Chem 277:26652-26661. (Pubitemid 34967164)
30. Shimohata N, Chiba S, Saikawa N, Ito K, Akiyama Y (2002) The Cpx stress response system of Escherichia coli senses plasma membrane proteins and controls HtpX, a membrane protease with a cytosolic active site. Genes Cells 7:653-662. (Pubitemid 34814757)
31. Danese PN, Silhavy TJ (1998) CpxP, a stress-combative member of the Cpx regulon. J Bacteriol 180:831-839.
32. Dorel C, Lejeune P, Rodrigue A (2006) The Cpx system of Escherichia coli, a strategic signaling pathway for confronting adverse conditions and for settling biofilm communities? Res Microbiol 157:306-314.
33. Duguay AR, Silhavy TJ (2004) Quality control in the bacterial periplasm. Biochim Biophys Acta 1694:121-134.
34. Ruiz N, Silhavy TJ (2005) Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol 8:122-126. (Pubitemid 40417951)
35. Zhou L, Lei XH, Bochner BR, Wanner BL (2003) Phenotype microarray analysis of Escherichia coli K-12 mutants with deletions of all two-component systems. J Bacteriol 185:4956-4972. (Pubitemid 36962304)
36. Price NL, Raivio TL (2009) Characterization of the Cpx regulon in Escherichia coli strain MC4100. J Bacteriol 191:1798-1815.
37. Maseda H, Yoneyama H, Nakae T (2000) Assignment of the substrate-selective subunits of the MexEF-OprN multidrug efflux pump of Pseudomonas aeruginosa. Antimicrob Agents Chemother 44:658-664. (Pubitemid 30117958)
38. Kohler T, et al. (1997) Characterization of MexE-MexF-OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa. Mol Microbiol 23:345-354. (Pubitemid 27049187)
39. Calamia J, Manoil C (1990) lac permease of Escherichia coli: Topology and sequence elements promoting membrane insertion. Proc Natl Acad Sci USA 87:4937-4941. (Pubitemid 20224247)
40. Fozo EM, et al. (2008) Repression of small toxic protein synthesis by the Sib and OhsC small RNAs. Mol Microbiol 70:1076-1093.
41. Schurek KN, et al. (2008) Novel genetic determinants of low-level aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 52:4213-4219.
42. 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 USA 83:6164-6168.
43. Busse HJ, Wostmann C, Bakker EP (1992) The bactericidal action of streptomycin: Membrane permeabilization caused by the insertion of mistranslated proteins into the cytoplasmic membrane of Escherichia coli and subsequent caging of the antibiotic inside the cells due to degradation of these proteins. J Gen Microbiol 138:551-561.
44. Kihara A, Akiyama Y, Ito K (1998) Different pathways for protein degradation by the FtsH/HflKC membrane-embedded protease complex: An implication from the interference by a mutant form of a new substrate protein, YccA. J Mol Biol 279:175-188. (Pubitemid 28252137)
45. Ito K, Akiyama Y (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59:211-231. (Pubitemid 41507430)
46. Davis BD (1987) Mechanism of bactericidal action of aminoglycosides. Microbiol Rev 51:341-350.
47. 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. (Pubitemid 47332566)
48. Watanabe T, Okada A, Gotoh Y, Utsumi R (2008) Inhibitors targeting two-component signal transduction. Adv Exp Med Biol 631:229-236.
49. Matsushita M, Janda KD (2002) Histidine kinases as targets for new antimicrobial agents. Bioorg Med Chem 10:855-867. (Pubitemid 34139899)
50. Brazas MD, Hancock RE (2005) Using microarray gene signatures to elucidate mechanisms of antibiotic action and resistance. Drug Discov Today 10:1245-1252.
51. Davies J, Spiegelman GB, Yim G (2006) The world of subinhibitory antibiotic concentrations. Curr Opin Microbiol 9:445-453.
52. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomallylocated DNA sequences: Application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
53. Gallagher LA, McKnight SL, Kuznetsova MS, Pesci EC, Manoil C (2002) Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 184:6472-6480.