Inhibition of quorum sensing-controlled virulence factors in by human serum paraoxonase Free

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
2024-03-29
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 Ethnopharmacol 105:427–435 [View Article][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 Sci 47:4453–4460 [View Article][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 Chemother 48:1681–1687 [View Article][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 Ophthalmol 247:913–917 [View Article][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 Dis 11:53 [View Article][PubMed]
    [Google Scholar]
  6. Boles B. R., Thoendel M., Singh P. K. 2005; Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol Microbiol 57:1210–1223 [View Article][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 Biochem 290:330–337 [View Article][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 Chemother 55:1325–1331 [View Article][PubMed]
    [Google Scholar]
  9. Ceron J. J., Tecles F., Tvarijonaviciute A. 2014; Serum paraoxonase 1 (PON1) measurement: an update. BMC Vet Res 10:74 [View Article][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 Leeuwenhoek 98:299–305 [View Article][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 Microbiol 11:51 [View Article][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 A 101:3587–3590 [View Article][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 Chem 23:2584–2588
    [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 Physiol 274: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. Microbiology 149:2005–2013 [View Article][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 Biol 32:411–419 [View Article][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 Bacteriol 172:884–900[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 Ecol 72:22–34 [View Article][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 Bacteriol 184:6472–6480 [View Article][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 Bacteriol 173:3000–3009[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 Immun 61:1180–1184[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 Dispos 19:100–106[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 Methods 70:1037–1042 [View Article][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 Microbiol 71:2288–2293 [View Article][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 Bacteriol 178:6608–6617[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 Immun 60:328–336[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 J 22:3803–3815 [View Article][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 No 2 pp 383–395 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 Immunopathol 62:133–138 [View Article][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 Acta 402:67–74 [View Article][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 Immun 73:6689–6703 [View Article][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 Immun 47:555–560[PubMed]
    [Google Scholar]
  33. Kessler E., Ohman D. E. 1998; Pseudolysin (Pseudomonas aeruginosa elastase). In Handbook of Proteolytic Enzymes pp 1058–1064 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 Chem 272:9884–9889 [View Article][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 Chem 273:30225–30231 [View Article][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 Bacteriol 182:5990–5996 [View Article][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 Microbiol 17:333–343 [View Article][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 Acta 1622:36–41 [View Article][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 Res 42:528–535[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 Chem 193:265–275[PubMed]
    [Google Scholar]
  41. Maeda H., Yamamoto T. 1996; Pathogenic mechanisms induced by microbial proteases in microbial infections. Biol Chem Hoppe Seyler 377:217–226[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. Microbiology 145:283–291 [View Article][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 Biol 28:528–537 [View Article][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 Pathog 33:127–134 [View Article][PubMed]
    [Google Scholar]
  45. Morikawa M., Hirata Y., Imanaka T. 2000; A study on the structure-function relationship of lipopeptide biosurfactants. Biochim Biophys Acta 1488:211–218 [View Article][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 Microbiol 1:54–61
    [Google Scholar]
  47. Ng W. L., Bassler B. L. 2009; Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222 [View Article][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 Bacteriol 142:836–842[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 Lett 253:29–37 [View Article][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 Chem 275:3057–3064 [View Article][PubMed]
    [Google Scholar]
  51. Parmely M., Gale A., Clabaugh M., Horvat R., Zhou W. W. 1990; Proteolytic inactivation of cytokines by Pseudomonas aeruginosa . Infect Immun 58:3009–3014[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 A 96:4360–4365 [View Article][PubMed]
    [Google Scholar]
  53. Patel R. M., Desai A. J. 1997; Biosurfactant production by Pseudomonas aeruginosa GS3 from molasses. Lett Appl Microbiol 25:91–94 [View Article]
    [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 A 92:1490–1494 [View Article][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 Bacteriol 179:3127–3132[PubMed]
    [Google Scholar]
  56. Pinzon N. M., Ju L. K. 2009; Analysis of rhamnolipid biosurfactants by methylene blue complexation. Appl Microbiol Biotechnol 82:975–981 [View Article][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 Immun 65:3086–3090[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 Immun 73:5319–5328 [View Article][PubMed]
    [Google Scholar]
  59. Rasmussen T. B., Givskov M. 2006; Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 296:149–161 [View Article][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 Med 2:a012427 [View Article][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 Immun 10:128–135[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 Bacteriol 185:2066–2079 [View Article][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 Bacteriol 177:654–659[PubMed]
    [Google Scholar]
  64. Siegmund I., Wagner F. 1991; New method for detecting rhamnolipids excreted by Pseudomonas species during growth in mineral agar. Biotechnol Tech 5:265–268 [View Article]
    [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. Biochimie 88:565–574 [View Article][PubMed]
    [Google Scholar]
  66. Smith R. S., Iglewski B. H. 2003; P. aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol 6:56–60 [View Article][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 Invest 118:3123–3131 [View Article][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 Immun 76:2512–2519 [View Article][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 Microbiol 5:2003–2010 [View Article][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 Sci 34:2699–2712[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 Med 37:1777–1786 [View Article][PubMed]
    [Google Scholar]
  72. Venturi V. 2006; Regulation of quorum sensing in Pseudomonas . FEMS Microbiol Rev 30:274–291 [View Article][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 Lett 579:3713–3717 [View Article][PubMed]
    [Google Scholar]
  74. Zhang L. H., Dong Y. H. 2004; Quorum sensing and signal interference: diverse implications. Mol Microbiol 53:1563–1571 [View Article][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 B 6:725–730 [View Article][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 Most Cited RSS feed