1887

Abstract

The role of quorum sensing (QS) in the regulation of virulence factor production in is well established. Increased antibiotic resistance in this bacterium has led to the search for new treatment options, and inhibition of the QS system has been explored for potential therapeutic benefits. If the use of QS inhibitory agents were to lead to a reduction in bacterial virulence, new approaches in the treatment of infections could be further developed. Accordingly, we examined whether human serum paraoxonase 1 (hPON1), which uses lactonase activity to hydrolyse -acyl homoserine lactones, could cleave -derived signalling molecules. hPON1 was purified using ammonium sulfate precipitation and hydrophobic interaction chromatography (Sepharose 4B–-tyrosine-1-naphthylamine). Different concentrations of hPON1 were found to reduce various virulence factors including pyocyanin, rhamnolipid, elastase, staphylolytic LasA protease and alkaline protease. Although treatment with 0.1–10 mg hPON1 ml did not show a highly inhibitory effect on elastase and staphylolytic LasA protease production, it resulted in good inhibitory effects on alkaline protease production at concentrations as low as 0.1 mg ml. hPON1 also reduced the production of pyocyanin and rhamnolipid at a concentration of 1.25 mg ml (within a range of 0.312–5 mg ml). In addition, rhamnolipid, an effective biosurfactant reported to stimulate the biodegradation of hydrocarbons, was able to degrade oil only in the absence of hPON1.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000206
2016-02-01
2020-09-30
Loading full text...

Full text loading...

/deliver/fulltext/jmm/65/2/105.html?itemId=/content/journal/jmm/10.1099/jmm.0.000206&mimeType=html&fmt=ahah

References

  1. Adonizio A. L., Downum K., Bennett B. C., Mathee K.. 2006; Anti-quorum sensing activity of medicinal plants in southern Florida. J Ethnopharmacol105:427–435 [CrossRef][PubMed]
    [Google Scholar]
  2. Bandara M. B. K., Zhu H., Sankaridurg P. R., Willcox M. D. P.. 2006; Salicylic acid reduces the production of several potential virulence factors of Pseudomonas aeruginosa associated with microbial keratitis. Invest Ophthalmol Vis Sci47:4453–4460 [CrossRef][PubMed]
    [Google Scholar]
  3. Barequet I. S., Ben Simon G. J., Safrin M., Ohman D. E., Kessler E.. 2004; Pseudomonas aeruginosa LasA protease in treatment of experimental staphylococcal keratitis. Antimicrob Agents Chemother48:1681–1687 [CrossRef][PubMed]
    [Google Scholar]
  4. Barequet I. S., Habot-Wilner Z., Mann O., Safrin M., Ohman D. E., Kessler E., Rosner M.. 2009; Evaluation of Pseudomonas aeruginosa staphylolysin (LasA protease) in the treatment of methicillin-resistant Staphylococcus aureus endophthalmitis in a rat model. Graefes Arch Clin Exp Ophthalmol247:913–917 [CrossRef][PubMed]
    [Google Scholar]
  5. Beekhof P. K., Gorshunska M., Jansen E. H.. 2012; Long term stability of paraoxonase-1 and high-density lipoprotein in human serum. Lipids Health Dis11:53 [CrossRef][PubMed]
    [Google Scholar]
  6. Boles B. R., Thoendel M., Singh P. K.. 2005; Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol57:1210–1223 [CrossRef][PubMed]
    [Google Scholar]
  7. Caballero A. R., Moreau J. M., Engel L. S., Marquart M. E., Hill J. M., O'Callaghan R. J.. 2001; Pseudomonas aeruginosa protease IV enzyme assays and comparison to other Pseudomonas proteases. Anal Biochem290:330–337 [CrossRef][PubMed]
    [Google Scholar]
  8. Camps J., Pujol I., Ballester F., Joven J., Simó J. M.. 2011; Paraoxonases as potential antibiofilm agents: their relationship with quorum-sensing signals in Gram-negative bacteria. Antimicrob Agents Chemother55:1325–1331 [CrossRef][PubMed]
    [Google Scholar]
  9. Ceron J. J., Tecles F., Tvarijonaviciute A.. 2014; Serum paraoxonase 1 (PON1) measurement: an update. BMC Vet Res10:74 [CrossRef][PubMed]
    [Google Scholar]
  10. Chan K. G., Wong C. S., Yin W. F., Sam C. K., Koh C. L.. 2010; Rapid degradation of N-3-oxo-acylhomoserine lactones by a Bacillus cereus isolate from Malaysian rainforest soil. Antonie van Leeuwenhoek98:299–305 [CrossRef][PubMed]
    [Google Scholar]
  11. Chan K. G., Atkinson S., Mathee K., Sam C. K., Chhabra S. R., Cámara M., Koh C. L., Williams P.. 2011; Characterization of N-acylhomoserine lactone-degrading bacteria associated with the Zingiber officinale (ginger) rhizosphere: co-existence of quorum quenching and quorum sensing in Acinetobacter and Burkholderia. BMC Microbiol11:51 [CrossRef][PubMed]
    [Google Scholar]
  12. Chun C. K., Ozer E. A., Welsh M. J., Zabner J., Greenberg E. P.. 2004; Inactivation of a Pseudomonas aeruginosa quorum-sensing signal by human airway epithelia. Proc Natl Acad Sci U S A101:3587–3590 [CrossRef][PubMed]
    [Google Scholar]
  13. Demir N., Nadaroglu H., Demir Y.. 2011; Purification of paraoxonase (PON1) from olive (Olea europaea L.) and effect of some chemicals on paraoxonase activity in vitro. Asian J Chem23:2584–2588
    [Google Scholar]
  14. Denning G. M., Railsback M. A., Rasmussen G. T., Cox C. D., Britigan B. E.. 1998; Pseudomonas pyocyanine alters calcium signaling in human airway epithelial cells. Am J Physiol274:L893–L900[PubMed]
    [Google Scholar]
  15. Déziel E., Lépine F., Milot S., Villemur R.. 2003; rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiology149:2005–2013 [CrossRef][PubMed]
    [Google Scholar]
  16. Dulon S., Leduc D., Cottrell G. S., D'Alayer J., Hansen K. K., Bunnett N. W., Hollenberg M. D., Pidard D., Chignard M.. 2005; Pseudomonas aeruginosa elastase disables proteinase-activated receptor 2 in respiratory epithelial cells. Am J Respir Cell Mol Biol32:411–419 [CrossRef][PubMed]
    [Google Scholar]
  17. Essar D. W., Eberly L., Hadero A., Crawford I. P.. 1990; Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J Bacteriol172:884–900[PubMed]
    [Google Scholar]
  18. Fekete A., Kuttler C., Rothballer M., Hense B. A., Fischer D., Buddrus-Schiemann K., Lucio M., Müller J., Schmitt-Kopplin P., Hartmann A.. 2010; Dynamic regulation of N-acyl-homoserine lactone production and degradation in Pseudomonas putida IsoF. FEMS Microbiol Ecol72:22–34 [CrossRef][PubMed]
    [Google Scholar]
  19. Gallagher L. A., McKnight S. L., Kuznetsova M. S., Pesci E. C., Manoil C.. 2002; Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol184:6472–6480 [CrossRef][PubMed]
    [Google Scholar]
  20. Gambello M. J., Iglewski B. H.. 1991; Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J Bacteriol173:3000–3009[PubMed]
    [Google Scholar]
  21. Gambello M. J., Kaye S., Iglewski B. H.. 1993; LasR of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene (apr) and an enhancer of exotoxin A expression. Infect Immun61:1180–1184[PubMed]
    [Google Scholar]
  22. Gan K. N., Smolen A., Eckerson H. W., La Du B. N.. 1991; Purification of human serum paraoxonase/arylesterase. Evidence for one esterase catalyzing both activities. Drug Metab Dispos19:100–106[PubMed]
    [Google Scholar]
  23. Golmanesh L., Mehrani H., Tabei M.. 2008; Simple procedures for purification and stabilization of human serum paraoxonase-1. J Biochem Biophys Methods70:1037–1042 [CrossRef][PubMed]
    [Google Scholar]
  24. Gunther N.W,IV., Nuñez A., Fett W., Solaiman D. K. Y.. 2005; Production of rhamnolipids by Pseudomonas chlororaphis, a nonpathogenic bacterium. Appl Environ Microbiol71:2288–2293 [CrossRef][PubMed]
    [Google Scholar]
  25. Gustin J. K., Kessler E., Ohman D. E.. 1996; A substitution at His-120 in the LasA protease of Pseudomonas aeruginosa blocks enzymatic activity without affecting propeptide processing or extracellular secretion. J Bacteriol178:6608–6617[PubMed]
    [Google Scholar]
  26. Hassett D. J., Charniga L., Bean K., Ohman D. E., Cohen M. S.. 1992; Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of a manganese-cofactored superoxide dismutase. Infect Immun60:328–336[PubMed]
    [Google Scholar]
  27. Hentzer M., Wu H., Andersen J. B., Riedel K., Rasmussen T. B., Bagge N., Kumar N., Schembri M. A., Song Z., other authors. 2003; Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J22:3803–3815 [CrossRef][PubMed]
    [Google Scholar]
  28. Hoge R., Pelzer A., Rosenau F., Wilhelm S.. 2010; Weapons of a pathogen: proteases and their role in virulence of Pseudomonas aeruginosa. In Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology No2 pp383–395 Edited by Mendez-Vilas A.. Spain: Formatex Research Center;
    [Google Scholar]
  29. Hong Y. Q., Ghebrehiwet B.. 1992; Effect of Pseudomonas aeruginosa elastase and alkaline protease on serum complement and isolated components C1q and C3. Clin Immunol Immunopathol62:133–138 [CrossRef][PubMed]
    [Google Scholar]
  30. Huen K., Richter R., Furlong C., Eskenazi B., Holland N.. 2009; Validation of PON1 enzyme activity assays for longitudinal studies. Clin Chim Acta402:67–74 [CrossRef][PubMed]
    [Google Scholar]
  31. Hung C. Y., Seshan K. R., Yu J. J., Schaller R., Xue J., Basrur V., Gardner M. J., Cole G. T.. 2005; A metalloproteinase of Coccidioides posadasii contributes to evasion of host detection. Infect Immun73:6689–6703 [CrossRef][PubMed]
    [Google Scholar]
  32. Jacquot J., Tournier J. M., Puchelle E.. 1985; In vitro evidence that human airway lysozyme is cleaved and inactivated by Pseudomonas aeruginosa elastase and not by human leukocyte elastase. Infect Immun47:555–560[PubMed]
    [Google Scholar]
  33. Kessler E., Ohman D. E.. 1998; Pseudolysin (Pseudomonas aeruginosa elastase). In Handbook of Proteolytic Enzymes pp1058–1064 Edited by Barrett A. J., Rawlings N. D., Woessner J. F.. San Diego: Academic Press;
    [Google Scholar]
  34. Kessler E., Safrin M., Abrams W. R., Rosenbloom J., Ohman D. E.. 1997; Inhibitors and specificity of Pseudomonas aeruginosa LasA. J Biol Chem272:9884–9889 [CrossRef][PubMed]
    [Google Scholar]
  35. Kessler E., Safrin M., Gustin J. K., Ohman D. E.. 1998; Elastase and the LasA protease of Pseudomonas aeruginosa are secreted with their propeptides. J Biol Chem273:30225–30231 [CrossRef][PubMed]
    [Google Scholar]
  36. Köhler T., Curty L. K., Barja F., van Delden C., Pechère J. C.. 2000; Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol182:5990–5996 [CrossRef][PubMed]
    [Google Scholar]
  37. Latifi A., Winson M. K., Foglino M., Bycroft B. W., Stewart G.S.A.B., Lazdunski A., Williams P.. 1995; Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol Microbiol17:333–343 [CrossRef][PubMed]
    [Google Scholar]
  38. Lépine F., Déziel E., Milot S., Rahme L. G.. 2003; A stable isotope dilution assay for the quantification of the Pseudomonas quinolone signal in Pseudomonas aeruginosa cultures. Biochim Biophys Acta1622:36–41 [CrossRef][PubMed]
    [Google Scholar]
  39. Leviev I., Deakin S., James R. W.. 2001; Decreased stability of the M54 isoform of paraoxonase as a contributory factor to variations in human serum paraoxonase concentrations. J Lipid Res42:528–535[PubMed]
    [Google Scholar]
  40. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J.. 1951; Protein measurement with the Folin phenol reagent. J Biol Chem193:265–275[PubMed]
    [Google Scholar]
  41. Maeda H., Yamamoto T.. 1996; Pathogenic mechanisms induced by microbial proteases in microbial infections. Biol Chem Hoppe Seyler377:217–226[PubMed]
    [Google Scholar]
  42. Manefield M., de Nys R., Naresh K., Roger R., Givskov M., Peter S., Kjelleberg S.. 1999; Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology145:283–291 [CrossRef][PubMed]
    [Google Scholar]
  43. Mariencheck W. I., Alcorn J. F., Palmer S. M., Wright J. R.. 2003; Pseudomonas aeruginosa elastase degrades surfactant proteins A and D. Am J Respir Cell Mol Biol28:528–537 [CrossRef][PubMed]
    [Google Scholar]
  44. Miyoshi S., Sonoda Y., Wakiyama H., Rahman M. M., Tomochika K., Shinoda S., Yamamoto S., Tobe K.. 2002; An exocellular thermolysin-like metalloprotease produced by Vibrio fluvialis: purification, characterization, and gene cloning. Microb Pathog33:127–134 [CrossRef][PubMed]
    [Google Scholar]
  45. Morikawa M., Hirata Y., Imanaka T.. 2000; A study on the structure-function relationship of lipopeptide biosurfactants. Biochim Biophys Acta1488:211–218 [CrossRef][PubMed]
    [Google Scholar]
  46. Nasr S., Soudi M. R., Mehrnia M. R., Sarrafzadeh M. H.. 2009; Characterization of novel biosurfactant producing strains of Bacillus spp. isolated from petroleum contaminated soil. Iran J Microbiol1:54–61
    [Google Scholar]
  47. Ng W. L., Bassler B. L.. 2009; Bacterial quorum-sensing network architectures. Annu Rev Genet43:197–222 [CrossRef][PubMed]
    [Google Scholar]
  48. Ohman D. E., Cryz S. J., Iglewski B. H.. 1980; Isolation and characterization of Pseudomonas aeruginosa PAO mutant that produces altered elastase. J Bacteriol142:836–842[PubMed]
    [Google Scholar]
  49. Ozer E. A., Pezzulo A., Shih D. M., Chun C., Furlong C., Lusis A. J., Greenberg E. P., Zabner J.. 2005; Human and murine paraoxonase 1 are host modulators of Pseudomonas aeruginosa quorum-sensing. FEMS Microbiol Lett253:29–37 [CrossRef][PubMed]
    [Google Scholar]
  50. Park P. W., Pier G. B., Preston M. J., Goldberger O., Fitzgerald M. L., Bernfield M.. 2000; Syndecan-1 shedding is enhanced by LasA, a secreted virulence factor of Pseudomonas aeruginosa. J Biol Chem275:3057–3064 [CrossRef][PubMed]
    [Google Scholar]
  51. Parmely M., Gale A., Clabaugh M., Horvat R., Zhou W. W.. 1990; Proteolytic inactivation of cytokines by Pseudomonas aeruginosa. Infect Immun58:3009–3014[PubMed]
    [Google Scholar]
  52. Parsek M. R., Val D. L., Hanzelka B. L., Cronan J. E. Jr., Greenberg E. P.. 1999; Acyl homoserine-lactone quorum-sensing signal generation. Proc Natl Acad Sci U S A96:4360–4365 [CrossRef][PubMed]
    [Google Scholar]
  53. Patel R. M., Desai A. J.. 1997; Biosurfactant production by Pseudomonas aeruginosa GS3 from molasses. Lett Appl Microbiol25:91–94 [CrossRef]
    [Google Scholar]
  54. Pearson J. P., Passador L., Iglewski B. H., Greenberg E. P.. 1995; A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc Natl Acad Sci U S A92:1490–1494 [CrossRef][PubMed]
    [Google Scholar]
  55. Pesci E. C., Pearson J. P., Seed P. C., Iglewski B. H.. 1997; Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol179:3127–3132[PubMed]
    [Google Scholar]
  56. Pinzon N. M., Ju L. K.. 2009; Analysis of rhamnolipid biosurfactants by methylene blue complexation. Appl Microbiol Biotechnol82:975–981 [CrossRef][PubMed]
    [Google Scholar]
  57. Preston M. J., Seed P. C., Toder D. S., Iglewski B. H., Ohman D. E., Gustin J. K., Goldberg J. B., Pier G. B.. 1997; Contribution of proteases and LasR to the virulence of Pseudomonas aeruginosa during corneal infections. Infect Immun65:3086–3090[PubMed]
    [Google Scholar]
  58. Prithiviraj B., Bais H. P., Weir T., Suresh B., Najarro E. H., Dayakar B. V., Schweizer H. P., Vivanco J. M.. 2005; Down regulation of virulence factors of Pseudomonas aeruginosa by salicylic acid attenuates its virulence on Arabidopsis thaliana and Caenorhabditis elegans. Infect Immun73:5319–5328 [CrossRef][PubMed]
    [Google Scholar]
  59. Rasmussen T. B., Givskov M.. 2006; Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol296:149–161 [CrossRef][PubMed]
    [Google Scholar]
  60. Rutherford S. T., Bassler B. L.. 2012; Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med2:a012427 [CrossRef][PubMed]
    [Google Scholar]
  61. Schultz D. R., Miller K. D.. 1974; Elastase of Pseudomonas aeruginosa: inactivation of complement components and complement-derived chemotactic and phagocytic factors. Infect Immun10:128–135[PubMed]
    [Google Scholar]
  62. Schuster M., Lostroh C. P., Ogi T., Greenberg E. P.. 2003; Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol185:2066–2079 [CrossRef][PubMed]
    [Google Scholar]
  63. Seed P. C., Passador L., Iglewski B. H.. 1995; Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI: an autoinduction regulatory hierarchy. J Bacteriol177:654–659[PubMed]
    [Google Scholar]
  64. Siegmund I., Wagner F.. 1991; New method for detecting rhamnolipids excreted by Pseudomonas species during growth in mineral agar. Biotechnol Tech5:265–268 [CrossRef]
    [Google Scholar]
  65. Sinan S., Kockar F., Arslan O.. 2006; Novel purification strategy for human PON1 and inhibition of the activity by cephalosporin and aminoglikozide derived antibiotics. Biochimie88:565–574 [CrossRef][PubMed]
    [Google Scholar]
  66. Smith R. S., Iglewski B. H.. 2003; P. aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol6:56–60 [CrossRef][PubMed]
    [Google Scholar]
  67. Stoltz D. A., Ozer E. A., Taft P. J., Barry M., Liu L., Kiss P. J., Moninger T. O., Parsek M. R., Zabner J.. 2008; Drosophila are protected from Pseudomonas aeruginosa lethality by transgenic expression of paraoxonase-1. J Clin Invest118:3123–3131 [CrossRef][PubMed]
    [Google Scholar]
  68. Teiber J. F., Horke S., Haines D. C., Chowdhary P. K., Xiao J., Kramer G. L., Haley R. W., Draganov D. I.. 2008; Dominant role of paraoxonases in inactivation of the Pseudomonas aeruginosa quorum-sensing signal N-(3-oxododecanoyl)-l-homoserine lactone. Infect Immun76:2512–2519 [CrossRef][PubMed]
    [Google Scholar]
  69. Toder D. S., Gambello M. J., Iglewski B. H.. 1991; Pseudomonas aeruginosa LasA: a second elastase under the transcriptional control of lasR. Mol Microbiol5:2003–2010 [CrossRef][PubMed]
    [Google Scholar]
  70. Twining S. S., Kirschner S. E., Mahnke L. A., Frank D. W.. 1993; Effect of Pseudomonas aeruginosa elastase, alkaline protease, and exotoxin A on corneal proteinases and proteins. Invest Ophthalmol Vis Sci34:2699–2712[PubMed]
    [Google Scholar]
  71. Veesenmeyer J. L., Hauser A. R., Lisboa T., Rello J.. 2009; Pseudomonas aeruginosa virulence and therapy: evolving translational strategies. Crit Care Med37:1777–1786 [CrossRef][PubMed]
    [Google Scholar]
  72. Venturi V.. 2006; Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev30:274–291 [CrossRef][PubMed]
    [Google Scholar]
  73. Yang F., Wang L. H., Wang J., Dong Y. H., Hu J. Y., Zhang L. H.. 2005; Quorum quenching enzyme activity is widely conserved in the sera of mammalian species. FEBS Lett579:3713–3717 [CrossRef][PubMed]
    [Google Scholar]
  74. Zhang L. H., Dong Y. H.. 2004; Quorum sensing and signal interference: diverse implications. Mol Microbiol53:1563–1571 [CrossRef][PubMed]
    [Google Scholar]
  75. Zhang G. L., Wu Y. T., Qian X. P., Meng Q.. 2005; Biodegradation of crude oil by Pseudomonas aeruginosa in the presence of rhamnolipids. J Zhejiang Univ Sci B6:725–730 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000206
Loading
/content/journal/jmm/10.1099/jmm.0.000206
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error