Pseudomonas aeruginosa overrides the virulence inducing effect of opioids when it senses an abundance of phosphate

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Zaborin, Alexander ^a   Gerdes, Svetlana ^b   Holbrook, Christopher ^a   Liu, Donald C ^a   Zaborina, Olga Y ^a   Alverdy, John C ^a  

^a UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

^b Fellowship for Interpretation of Genomes   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 HEPTYL 4 QUINOLONE; 3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE; KAPPA OPIATE RECEPTOR; PHOSPHATE; PYOVERDINE; QUINOLONE DERIVATIVE; UNCLASSIFIED DRUG; NARCOTIC ANALGESIC AGENT; OLIGOPEPTIDE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CAENORHABDITIS ELEGANS; CELL DENSITY; CONTROLLED STUDY; ENERGY CONSERVATION; ENERGY CONSUMPTION; EVOLUTIONARY ADAPTATION; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHENOTYPE; PHOSPHATE DEFICIENCY; PQS C GENE; PQSA GENE; PQSB GENE; PQSD GENE; PQSE GENE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; QUORUM SENSING; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; DRUG EFFECT; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VIRULENCE;

BACTERIA (MICROORGANISMS); CAENORHABDITIS ELEGANS; PSEUDOMONAS AERUGINOSA;

ANALGESICS, OPIOID; ANIMALS; CAENORHABDITIS ELEGANS; MICROSCOPY, ELECTRON, TRANSMISSION; OLIGOPEPTIDES; PHOSPHATES; PSEUDOMONAS AERUGINOSA; QUINOLONES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VIRULENCE;

EID: 84859705613     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034883     Document Type: Article

References (39)

1. Trillis F 3rd, Eckstein EC, Budavich R, Pultz MJ, Donskey CJ, (2008) Contamination of hospital curtains with healthcare-associated pathogens. Infect Control Hosp Epidemiol 29: 1074-1076.
2. Falcone M, Venditti M, Corrao S, Serra P, (2011) Role of multidrug-resistant pathogens in health-care-associated pneumonia. Lancet Infect Dis 11: 11-12; author reply 12-13.
3. Hirsch EB, Tam VH, (2010) Impact of multidrug-resistant Pseudomonas aeruginosa infection on patient outcomes. Expert Rev Pharmacoecon Outcomes Res 10: 441-451.
4. Zaborina O, Lepine F, Xiao G, Valuckaite V, Chen Y, et al. (2007) Dynorphin activates quorum sensing quinolone signaling in Pseudomonas aeruginosa. PLoS Pathog 3: e35.
5. Babrowski T, Holbrook C, Moss J, Gottlieb L, Valuckaite V, et al. (2012) Pseudomonas aeruginosa virulence expression is directly activated by morphine and is capable of causing lethal gut-derived sepsis in mice during chronic morphine administration. Ann Surg 255: 386-393.
6. Patel NJ, Zaborina O, Wu L, Wang Y, Wolfgeher DJ, et al. (2007) Recognition of intestinal epithelial HIF-1alpha activation by Pseudomonas aeruginosa. Am J Physiol Gastrointest Liver Physiol 292: G134-142.
7. Wu L, Estrada O, Zaborina O, Bains M, Shen L, et al. (2005) Recognition of host immune activation by Pseudomonas aeruginosa. Science 309: 774-777.
8. Romanowski K, Zaborin A, Fernandez H, Poroyko V, Valuckaite V, et al. (2011) Prevention of siderophore- mediated gut-derived sepsis due to P. aeruginosa can be achieved without iron provision by maintaining local phosphate abundance: role of pH. BMC Microbiol 11: 212.
9. Zaborin A, Romanowski K, Gerdes S, Holbrook C, Lepine F, et al. (2009) Red death in Caenorhabditis elegans caused by Pseudomonas aeruginosa PAO1. Proc Natl Acad Sci U S A 106: 6327-6332.
10. Long J, Zaborina O, Holbrook C, Zaborin A, Alverdy J, (2008) Depletion of intestinal phosphate after operative injury activates the virulence of P aeruginosa causing lethal gut-derived sepsis. Surgery 144: 189-197.
11. Hernandez ME, Kappler A, Newman DK, (2004) Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl Environ Microbiol 70: 921-928.
12. Coleman JP, Hudson LL, McKnight SL, Farrow JM 3rd, Calfee MW, et al. (2008) Pseudomonas aeruginosa PqsA is an anthranilate-coenzyme A ligase. J Bacteriol 190: 1247-1255.
13. Lepine F, Dekimpe V, Lesic B, Milot S, Lesimple A, et al. (2007) PqsA is required for the biosynthesis of 2,4-dihydroxyquinoline (DHQ), a newly identified metabolite produced by Pseudomonas aeruginosa and Burkholderia thailandensis. Biol Chem 388: 839-845.
14. Xiao G, He J, Rahme LG, (2006) Mutation analysis of the Pseudomonas aeruginosa mvfR and pqsABCDE gene promoters demonstrates complex quorum-sensing circuitry. Microbiology 152: 1679-1686.
15. Zhang YM, Frank MW, Zhu K, Mayasundari A, Rock CO, (2008) PqsD is responsible for the synthesis of 2,4-dihydroxyquinoline, an extracellular metabolite produced by Pseudomonas aeruginosa. J Biol Chem 283: 28788-28794.
16. Deziel E, Lepine F, Milot S, He J, Mindrinos MN, et al. (2004) Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. Proc Natl Acad Sci U S A 101: 1339-1344.
17. Lamarche MG, Deziel E, (2011) MexEF-OprN efflux pump exports the Pseudomonas quinolone signal (PQS) precursor HHQ (4-hydroxy-2-heptylquinoline). PLoS One 6: e24310.
18. Deziel E, Gopalan S, Tampakaki AP, Lepine F, Padfield KE, et al. (2005) The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol Microbiol 55: 998-1014.
19. Xiao G, Deziel E, He J, Lepine F, Lesic B, et al. (2006) MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol 62: 1689-1699.
20. Fletcher MP, Diggle SP, Crusz SA, Chhabra SR, Camara M, et al. (2007) A dual biosensor for 2-alkyl-4-quinolone quorum-sensing signal molecules. Environ Microbiol 9: 2683-2693.
21. Fletcher MP, Diggle SP, Camara M, Williams P, (2007) Biosensor-based assays for PQS, HHQ and related 2-alkyl-4-quinolone quorum sensing signal molecules. Nat Protoc 2: 1254-1262.
22. Rampioni G, Pustelny C, Fletcher MP, Wright VJ, Bruce M, et al. (2010) Transcriptomic analysis reveals a global alkyl-quinolone-independent regulatory role for PqsE in facilitating the environmental adaptation of Pseudomonas aeruginosa to plant and animal hosts. Environ Microbiol 12: 1659-1673.
23. Diggle SP, Matthijs S, Wright VJ, Fletcher MP, Chhabra SR, et al. (2007) The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol 14: 87-96.
24. Chakraborty S, Sivaraman J, Leung KY, Mok YK, (2011) Two-component PhoB-PhoR regulatory system and ferric uptake regulator sense phosphate and iron to control virulence genes in type III and VI secretion systems of Edwardsiella tarda. J Biol Chem 286: 39417-39430.
25. Sommer MO, Dantas G, Church GM, (2009) Functional characterization of the antibiotic resistance reservoir in the human microflora. Science 325: 1128-1131.
26. Sommer MO, Church GM, Dantas G, (2010) The human microbiome harbors a diverse reservoir of antibiotic resistance genes. Virulence 1: 299-303.
27. Glattard E, Welters ID, Lavaux T, Muller AH, Laux A, et al. (2010) Endogenous morphine levels are increased in sepsis: a partial implication of neutrophils. PLoS One 5: e8791.
28. Moss J, Rosow CE, (2008) Development of peripheral opioid antagonists' new insights into opioid effects. Mayo Clin Proc 83: 1116-1130.
29. Shor R, Halabe A, Rishver S, Tilis Y, Matas Z, et al. (2006) Severe hypophosphatemia in sepsis as a mortality predictor. Ann Clin Lab Sci 36: 67-72.
30. Hazan R, He J, Xiao G, Dekimpe V, Apidianakis Y, et al. (2010) Homeostatic interplay between bacterial cell-cell signaling and iron in virulence. PLoS Pathog 6: e1000810.
31. Lepine F, Milot S, Deziel E, He J, Rahme LG, (2004) Electrospray/mass spectrometric identification and analysis of 4-hydroxy-2-alkylquinolines (HAQs) produced by Pseudomonas aeruginosa. J Am Soc Mass Spectrom 15: 862-869.
32. Farrow JM 3rd, Sund ZM, Ellison ML, Wade DS, Coleman JP, et al. (2008) PqsE functions independently of PqsR-Pseudomonas quinolone signal and enhances the rhl quorum-sensing system. J Bacteriol 190: 7043-7051.
33. Chugani S, Greenberg EP, (2010) LuxR homolog-independent gene regulation by acyl-homoserine lactones in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 107: 10673-10678.
34. Oglesby AG, Farrow JM 3rd, Lee JH, Tomaras AP, Greenberg EP, et al. (2008) The influence of iron on Pseudomonas aeruginosa physiology: a regulatory link between iron and quorum sensing. J Biol Chem 283: 15558-15567.
35. Dietrich LE, Price-Whelan A, Petersen A, Whiteley M, Newman DK, (2006) The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol Microbiol 61: 1308-1321.
36. Lamarche MG, Wanner BL, Crepin S, Harel J, (2008) The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol Rev 32: 461-473.
37. Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E, et al. (2003) Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 100: 14339-14344.
38. Diggle SP, Winzer K, Chhabra SR, Worrall KE, Camara M, et al. (2003) The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50: 29-43.
39. Zaborina O, Holbrook C, Chen Y, Long J, Zaborin A, et al. (2008) Structure-function aspects of PstS in multi-drug-resistant Pseudomonas aeruginosa. PLoS Pathog 4: e43.