1887

Abstract

To understand the importance of quorum sensing in chronic lung infection, the pathogenic effects of the wild-type PAO1 and its double mutant, PAO1 , in which the signal-generating parts of the quorum sensing systems are defective were compared. The rat model of lung infection was used in the present study. The rats were killed on days 3, 7, 14 and 28 after infection with the strains. The results showed that during the early stages of infection, the PAO1 double mutant induced a stronger serum antibody response, higher production of pulmonary interferon γ, and more powerful blood polymorphonuclear leukocyte (PMN) chemiluminescence compared to its wild-type counterpart. On days 14 and 28 post-infection, significantly milder lung pathology, a reduction in the number of mast cells present in the lung foci, a reduced number of lung bacteria, and minor serum IgG and IgG1 responses but increased lung interferon γ production were detected in the group infected with the PAO1 double mutant when compared with the PAO1-infected group. Delayed immune responses were observed in the PAO1-infected group and they might be associated with the production of virulence factors that are controlled by the quorum sensing systems. The conclusion of this study is that functional and genes of PAO1 play a significant role during lung infection.

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2001-05-01
2020-03-29
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References

  1. Abraham S. N., Malaviya R. 1996; Role of mast cells in bacterial clearance in the lung. Mucosal Immunology Update4:58–60
    [Google Scholar]
  2. Bainbridge T., Fick R. B. Jr. 1989; Functional importance of cystic fibrosis immunoglobulin G fragments generated by Pseudomonas aeruginosa elastase. J Lab Clin Med114:728–733
    [Google Scholar]
  3. Brint J. M., Ohman D. E. 1995; Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. J Bacteriol177:7155–7163
    [Google Scholar]
  4. Chapon-Herve V., Akrim M., Latifi A., Williams P., Lazdunski A., Bally M. 1997; Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa. Mol Microbiol24:1169–1178[CrossRef]
    [Google Scholar]
  5. Ciofu O., Giwercman B., Pedersen S. S., Høiby N. 1994; Development of antibiotic resistance in Pseudomonas aeruginosa during two decades of antipseudomonal treatment at the Danish CF Center. APMIS102:674–680[CrossRef]
    [Google Scholar]
  6. Doring G. 1994; The role of neutrophil elastase in chronic inflammation. Am J Respir Crit Care Med150:S114–S117[CrossRef]
    [Google Scholar]
  7. Doring G., Dauner H. M. 1988; Clearance of Pseudomonas aeruginosa in different rat lung models. Am Rev Respir Dis138:1249–1253[CrossRef]
    [Google Scholar]
  8. Doring G., Obernesser H. J., Botzenhart K. 1981; Extracellular toxins of Pseudomonas aeruginosa . II. Effect of two proteases on human immunoglobulins IgG, IgA and secretory IgA. Zentbl Bakteriol A249:89–98
    [Google Scholar]
  9. Doring G., Dalhoff A., Vogel O., Brunner H., Droge U., Botzenhart K. 1984; In vivo activity of proteases of Pseudomonas aeruginosa in a rat model. J Infect Dis149:532–537[CrossRef]
    [Google Scholar]
  10. Doring G., Goldstein W., Roll A., Schiotz P. O., Høiby N., Botzenhart K. 1985; Role of Pseudomonas aeruginosa exoenzymes in lung infections of patients with cystic fibrosis. Infect Immun49:557–562
    [Google Scholar]
  11. Doring G., Maier M., Muller E., Bibi Z., Tummler B., Kharazmi A. 1987; Virulence factors of Pseudomonas aeruginosa . Antibiot Chemother39:136–148
    [Google Scholar]
  12. Finch R. G., Pritchard D. I., Bycroft B. W., Williams P., Stewart G. S. 1998; Quorum sensing: a novel target for anti-infective therapy. J Antimicrob Chemother42:569–571[CrossRef]
    [Google Scholar]
  13. Fuqua C., Greenberg E. P. 1998; Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr Opin Microbiol1:183–189[CrossRef]
    [Google Scholar]
  14. Fuqua C., Winans S. C., Greenberg E. P. 1996; Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu Rev Microbiol50:727–751[CrossRef]
    [Google Scholar]
  15. 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
    [Google Scholar]
  16. 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
    [Google Scholar]
  17. Glessner A., Smith R., Iglewski B., Robinson J. 1999; Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of twitching motility. J Bacteriol181:1623–1629
    [Google Scholar]
  18. Govan J. R., Deretic V. 1996; Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia . Microbiol Rev60:539–574
    [Google Scholar]
  19. Haczku A., Macary P., Haddad E. B., Huang T. J., Kemeny D. M., Moqbel R., Chung K. F. 1996; Expression of Th-2 cytokines interleukin-4 and -5 and of Th-1 cytokine interferon-gamma in ovalbumin-exposed sensitized Brown-Norway rats. Immunology88:247–251[CrossRef]
    [Google Scholar]
  20. Hartman G., Wise R. 1998; Quorum sensing: potential means of treating gram-negative infections?. Lancet351:848–849[CrossRef]
    [Google Scholar]
  21. Høiby N. 1993; Cystic fibrosis and endobronchial Pseudomonas infection. Curr Opin Pediatr5:247–254
    [Google Scholar]
  22. Høiby N., Doring G., Schiotz P. O. 1986; The role of immune complexes in the pathogenesis of bacterial infections. Annu Rev Microbiol40:29–53[CrossRef]
    [Google Scholar]
  23. Høiby N., Pedersen S. S., Jensen E. T., Pressler T., Shand G. H., Kharazmi A., Doring G. 1990; Immunology of Pseudomonas aeruginosa infection in cystic fibrosis. Acta Univ Carol Med Praha36:16–21
    [Google Scholar]
  24. Hokland P., Berg K. 1981; Interferon enhances the antibody-dependent cellular cytotoxicity (ADCC) of human polymorphonuclear leukocytes. J Immunol127:1585–1588
    [Google Scholar]
  25. Horvat R. T., Clabaugh M., Duval J. C., Parmely M. J. 1989; Inactivation of human gamma interferon by Pseudomonas aeruginosa proteases: elastase augments the effects of alkaline protease despite the presence of alpha 2-macroglobulin. Infect Immun57:1668–1674
    [Google Scholar]
  26. Jaeger K. E. 1994; Extracellular enzymes of Pseudomonas aeruginosa as virulence factors. Immun Infekt22:177–180
    [Google Scholar]
  27. Johansen H. K., Høiby N. 1992; Local IgA and IgG response to intratracheal immunization with Pseudomonas aeruginosa antigens. APMIS100:87–90[CrossRef]
    [Google Scholar]
  28. Johansen H. K., Espersen F., Pedersen S. S., Hougen H. P., Rygaard J., Høiby N. 1993; Chronic Pseudomonas aeruginosa lung infection in normal and athymic rats. APMIS101:207–225[CrossRef]
    [Google Scholar]
  29. Johansen H. K., Espersen F., Cryz S. J., Hougen H. P., Fomsgaard A., Rygaard J., Høiby N. 1994; Immunization with Pseudomonas aeruginosa vaccines and adjuvant can modulate the type of inflammatory response subsequent to infection. Infect Immun62:3146–3155
    [Google Scholar]
  30. Johansen H. K., Hougen H. P., Rygaard J., Høiby N. 1996; Interferon-gamma (IFN-gamma) treatment decreases the inflammatory response in chronic Pseudomonas aeruginosa pneumonia in rats. Clin Exp Immunol103:212–218[CrossRef]
    [Google Scholar]
  31. Kharazmi A., Høiby N., Doring G., Valerius N. H. 1984a; Pseudomonas aeruginosa exoproteases inhibit human neutrophil chemiluminescence. Infect Immun44:587–591
    [Google Scholar]
  32. Kharazmi A., Doring G., Høiby N., Valerius N. H. 1984b; Interaction of Pseudomonas aeruginosa alkaline protease and elastase with human polymorphonuclear leukocytes in vitro. Infect Immun43:161–165
    [Google Scholar]
  33. Kharazmi A., Eriksen H. O., Doring G., Goldstein W., Høiby N. 1986; Effect of Pseudomonas aeruginosa proteases on human leukocyte phagocytosis and bactericidal activity. Acta Pathol Microbiol Immunol Scand C94:175–179
    [Google Scholar]
  34. Kharazmi A., Bibi Z., Nielsen H., Høiby N., Doring G. 1989; Effect of Pseudomonas aeruginosa rhamnolipid on human neutrophil and monocyte function. APMIS97:1068–1072[CrossRef]
    [Google Scholar]
  35. Kiernan J. A. editor 1981; Histological and Histochemical Methods: Theory and Practice Oxford: Pergamon Press;
    [Google Scholar]
  36. Krishnan L., Guilbert L. J., Russell A. S., Wegmann T. G., Mosmann T. R., Belosevic M. 1996; Pregnancy impairs resistance of C57BL/6 mice to Leishmania major infection and causes decreased antigen-specific IFN-gamma response and increased production of T helper 2 cytokines. J Immunol156:644–652
    [Google Scholar]
  37. Latifi A., Foglino M., Tanaka K., Williams P., Lazdunski A. 1996; A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol21:1137–1146[CrossRef]
    [Google Scholar]
  38. May T. B., Shinabarger D., Maharaj R.. 7 other authors 1991; Alginate synthesis by Pseudomonas aeruginosa : a key pathogenic factor in chronic pulmonary infections of cystic fibrosis patients. Clin Microbiol Rev4:191–206
    [Google Scholar]
  39. Moser C., Johansen H. K., Song Z., Hougen H. P., Rygaard J., Høiby N. 1997; Chronic Pseudomonas aeruginosa lung infection is more severe in Th2 responding BALB/c mice compared to Th1 responding C3H/HeN mice. APMIS105:838–842[CrossRef]
    [Google Scholar]
  40. Mosmann T. R., Coffman R. L. 1989; TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol7:145–173[CrossRef]
    [Google Scholar]
  41. Mosmann T. R., Sad S. 1996; The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol Today17:138–146[CrossRef]
    [Google Scholar]
  42. Ochsner U. A., Reiser J. 1995; Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa . Proc Natl Acad Sci USA92:6424–6428[CrossRef]
    [Google Scholar]
  43. Passador L., Cook J. M., Gambello M. J., Rust L., Iglewski B. H. 1993; Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science260:1127–1130[CrossRef]
    [Google Scholar]
  44. Pearson J. P., Gray K. M., Passador L., Tucker K. D., Eberhard A., Iglewski B. H., Greenberg E. P. 1994; Structure of the autoinducer required for the expression of Pseudomonas aeruginosa virulence genes. Proc Natl Acad Sci USA91:197–201[CrossRef]
    [Google Scholar]
  45. 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 USA92:1490–1494[CrossRef]
    [Google Scholar]
  46. Pearson J., Pesci E., Iglewski B. 1997; Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol179:5756–5767
    [Google Scholar]
  47. Pedersen S. S. 1992; Lung infection with alginate-producing, mucoid Pseudomonas aeruginosa in cystic fibrosis. APMIS Suppl28:1–79
    [Google Scholar]
  48. Pedersen S. S., Shand G. H., Hansen B. L., Hansen G. N. 1990; Induction of experimental chronic Pseudomonas aeruginosa lung infection with P. aeruginosa entrapped in alginate microspheres. APMIS98:203–211[CrossRef]
    [Google Scholar]
  49. Pesci E. C., Iglewski B. H. 1997; The chain of command in Pseudomonas quorum sensing. Trends Microbiol5:132–135[CrossRef]
    [Google Scholar]
  50. 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
    [Google Scholar]
  51. Petroni K. C., Shen L., Guyre P. M. 1988; Modulation of human polymorphonuclear leukocyte IgG Fc receptors and Fc receptor-mediated functions by IFN-gamma and glucocorticoids. J Immunol140:3467–3472
    [Google Scholar]
  52. Pollack M. 1984; The virulence of Pseudomonas aeruginosa . Rev Infect Dis6 Suppl 3:S617–S626[CrossRef]
    [Google Scholar]
  53. Roilides E., Uhlig K., Venzon D., Pizzo P. A., Walsh T. J. 1992; Neutrophil oxidative burst in response to blastoconidia and pseudohyphae of Candida albicans : augmentation by granulocyte colony-stimulating factor and interferon-gamma. J Infect Dis166:668–673[CrossRef]
    [Google Scholar]
  54. Rumbaugh K. P., Griswold J. A., Iglewski B. H., Hamood A. N. 1999; Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infect Immun67:5854–5862
    [Google Scholar]
  55. Salmond G. P., Bycroft B. W., Stewart G. S., Williams P. 1995; The bacterial ‘enigma’: cracking the code of cell-cell communication. Mol Microbiol16:615–624[CrossRef]
    [Google Scholar]
  56. 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
    [Google Scholar]
  57. Solberg C. O., Kalager T., Hill H. R., Glette J. 1982; Polymorphonuclear leukocyte function in bacterial and viral infections. Scand J Infect Dis14:11–18[CrossRef]
    [Google Scholar]
  58. Song Z., Johansen H. K., Faber V., Moser C., Kharazmi A., Rygaard J., Høiby N. 1997; Ginseng treatment reduces bacterial load and lung pathology in chronic Pseudomonas aeruginosa pneumonia in rats. Antimicrob Agents Chemother41:961–964
    [Google Scholar]
  59. Song Z., Kharazmi A., Wu H., Faber V., Moser C., Krogh H. K., Rygaard J., Høiby N. 1998; Effects of ginseng treatment on neutrophil chemiluminescence and immunoglobulin G subclasses in a rat model of chronic Pseudomonas aeruginosa pneumonia. Clin Diagn Lab Immunol5:882–887
    [Google Scholar]
  60. Tang H. B., DiMango D., Bryan R., Gambello M., Iglewski B. H., Goldberg J. B., Prince A. 1996; Contribution of specific Pseudomonas aeruginosa virulence factors to pathogenesis of pneumonia in a neonatal mouse model of infection. Infect Immun64:37–43
    [Google Scholar]
  61. Telford G., Wheeler D., Williams P., Tomkins P. T., Appleby P., Sewell H., Stewart G. S., Bycroft B. W., Pritchard D. I. 1998; The Pseudomonas aeruginosa quorum-sensing signal molecule N -(3-oxododecanoyl)-l-homoserine lactone has immunomodulatory activity. Infect Immun66:36–42
    [Google Scholar]
  62. Van Delden C., Iglewski B. H. 1998; Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg Infect Dis4:551–560[CrossRef]
    [Google Scholar]
  63. Winson M., Camara M., Latifi A.. 10 other authors 1995; Multiple N -acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa . Proc Natl Acad Sci USA92:9427–9431[CrossRef]
    [Google Scholar]
  64. Wu H., Song Z., Hentzer M.. 8 other authors 2000; Detection of N -acylhomoserine lactones in lung tissues of mice infected with Pseudomonas aeruginosa. Microbiology146:2481–2493
    [Google Scholar]
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