1887

Microbiology Society logo

Volume 134, Issue 8

Interaction of Virulence Components with Neutrophils: Effect on Chemiluminescence Induced by a Chemotactic Peptide and by Intact Bacteria Free

Abstract

The effect of secreted virulence components of on chemiluminescence (CL) of rabbit peritoneal neutrophils was determined with the chemotactic peptide ′-formyl--methionyl--leucyl--phenylalanine (fMLP) or intact as the stimulus. Pertussis toxin (PT) inhibited the response to fMLP in a dose-dependent manner, although only after the neutrophils had been exposed to the toxin for >15 min. Both filamentous haemagglutinin (FHA) and lipopolysaccharide (LPS) markedly enhanced the CL response to fMLP after ≥15 min incubation with the neutrophils. Similar effects to those of LPS were also seen with smooth and rough LPS from . With the lowest dose of each component which elicited a maximal effect on CL, the inhibitory effect of PT overrode the enhancing effect of FHA and LPS. Pre-incubation of neutrophils with PT, FHA or B. pertussis LPS caused a slight reduction in the subsequent CL response to virulent Tohama. Virulent (phase I, or X-mode) organisms of 18334 and Tohama induced greater neutrophil CL than their avirulent (C-mode) derivatives. There appeared to be an inverse correlation between bacterial hydrophilicity and the ability to induce neutrophil CL: X-mode bacteria were significantly less hydrophilic than C-mode organisms. Three mutants, the adenylate cyclase (AC)- and haemolysin (HLY)-deficient BP348, the FHA-deficient BP353, and the PT-deficient BP357, generated similar levels of CL and had similar hydrophilicity values. The hydrophilicity value of the avirulent mutant BP347 (deficient in AC, HLY, FHA and PT) and the CL induced by this strain were similar to those of C-mode organisms. Thus, the interaction of with neutrophils appears to be complex, reflecting both the alteration of leucocyte function by secreted virulence components of the organism and, in the absence of opsonins, the surface properties of the bacterium.

  • Received:
  • Revised:
  • Published Online:
© Society for General Microbiology, 1988
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-134-8-2201
1988-08-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/micro/134/8/mic-134-8-2201.html?itemId=/content/journal/micro/10.1099/00221287-134-8-2201&mimeType=html&fmt=ahah

References

  1. Ashworth L. A. E., Fitzgeorge R. B., Irons L. I., Morgan C. P., Robinson A. 1982; Rabbit nasopharyngeal colonization by Bordetella pertussis: the effects of immunization on clearance and on serum and nasal antibody levels. Journal of Hygiene 88:475–486
     [Google Scholar]
  2. Ayme G., Caroff M., Chaby R., Haeffner-Cavaillon N., Ledur A., Moreau M., Muset M., Mynard M.-C., Roumiantzeff M., Schulz D., Szabo L. 1980; Biological activities of fragments derived from Bordetella pertussis endotoxin: isolation of a non-toxic, Schwartzman-nega- tive lipid A possessing high adjuvant properties. Infection and Immunity 27:739–745
     [Google Scholar]
  3. Becker E. L., Kermode J. C., Naccache P. H., Yassin R., Marsh M. L., Munoz J. J., Sha’Afi R. I. 1985; The inhibition of neutrophil granule enzyme secretion and chemotaxis by pertussis toxin. Journal of Cell Biology 100:1641–1646
     [Google Scholar]
  4. Becker E. L., Kermode J. C., Naccache P. H., Yassin R., Munoz J. J., Marsh M. L., Huang C.-K., Sha’Afi R. I. 1986; Pertussis toxin as a probe of neutrophil activation. Federation Proceedings 45:2151–2155
     [Google Scholar]
  5. Bender J. G., Van Epps D. E. 1983; Analysis of the bimodal chemiluminescence pattern stimulated in human neutrophils by chemotactic factors. Infection and Immunity 41:1062–1070
     [Google Scholar]
  6. Brownlie R. M., Parton R., Coote J. G. 1985; The effect of growth conditions on adenylate cyclase activity and virulence-related properties of Bordetella pertussis . Journal of General Microbiology 131:17–25
     [Google Scholar]
  7. Campbell R. C. 1981 Statistics for Biologists. Cambridge: Cambridge University Press;
     [Google Scholar]
  8. Confer D. L., Eaton J. W. 1982; Phagocyte impotence caused by an invasive bacterial adenylate cyclase. Science 217:948–950
     [Google Scholar]
  9. Craig F. F., Christodoulides M., Parton R., Stewart-Tull D. E. S., Freer J. H., Lackie J. M. 1988; A sensitive, chemiluminescence assay for pertussis toxin and for evaluation of cell-free pertussis toxoids. FEMS Microbiology Immunology (in the Press)
    [Google Scholar]
  10. Dahlgren C., Stendahl O. 1983; Role Ot myeloperoxidase in luminol-dependent chemiluminescence of polymorphonuclear leukocytes. Infection and Immunity 39:736–741
     [Google Scholar]
  11. Dechatelet L. R., Long G. D., Shirley P. S., Bass D. A., Thomas M. J., Henderson F. W., Cohen M. S. 1982; Mechanism of the luminol-dependent chemiluminescence of human neutrophils. Journal of Immunology 129:1589–1593
     [Google Scholar]
  12. Friedman R. L., Fiederlein R. L., Glasser L., Galgiani J. N. 1987; Bordetella pertussis adenylate cyclase: effects of affinity-purified adenylate cyclase on human polymorphonuclear leukocyte functions. Infection and Immunity 55:135–140
     [Google Scholar]
  13. Gallin J. I., Wright D. G., Malech H. L., Davis J. M., Klempner M. S., Kirkpatrick C. H. 1980; Disorders of phagocyte chemotaxis. Annals of Internal Medicine 92:520–538
     [Google Scholar]
  14. Henricks P. A. J., Van Der Tol M. E., Thyssen R.M.W.M., Van Asbeck B. S., Verhoef J. 1983; Escherichia coli lipopolysaccharides diminish and enhance cell function of human polymorphonuclear leukocytes. Infection and Immunity 41:294–301
     [Google Scholar]
  15. Hewlett E. L., Gordon V. M. 1988; Adenylate cyclase toxin of Bordetella pertussis . In Pathogenesis and Immunity in Pertussis pp 193–209 Wardlaw A. C., Parton R. Edited by London: John Wiley (in the Press);
     [Google Scholar]
  16. Horan T. D., English D., Mcpherson T. A. 1982; Association of neutrophil chemiluminescence with microbicidal activity. Clinical Immunology and Immunopathology 22:259–269
     [Google Scholar]
  17. Imaizumi A., Suzuki Y., Ono S., Sato H., Sato Y. 1983; Effect of heptakis(2,6-O-dimethyl)β-cyclodextrin on the production of pertussis toxin by Bordetella pertussis . Infection and Immunity 41:1138–1143
     [Google Scholar]
  18. Jamieson W. M. 1973; Whooping cough. British Medical Journal 1:223–225
     [Google Scholar]
  19. Lacey B. W. 1960; Antigenic modulation of Bordetella pertussis . Journal of Hygiene 58:57–93
     [Google Scholar]
  20. Lackie J. M. 1977; The aggregation of rabbit polymorphonuclear leukocytes (PMN’s): effects of agents which affect the acute inflammatory response and correlation with secretory activity. Inflammation 2:1–15
     [Google Scholar]
  21. Lad P. M., Olson C. V., Smiley P. A. 1985; Association of the jV-formyl-Met-Leu-Phe receptor in human neutrophils with a GTP-binding protein sensitive to pertussis toxin. Proceedings of the National Academy of Sciences of the United States of America 82:869–873
     [Google Scholar]
  22. Manclark C. R., Cowell J. L. 1984; Pertussis. In Bacterial Vaccines, pp 69–106 Germanier R. Edited by London: Academic Press;
     [Google Scholar]
  23. Meade B. D., Kind P. D., Ewell J. B., Mcgrath P. P., Manclark C. R. 1984; In vitro inhibition of murine macrophage migration by Bordetella pertussis lymphocytosis-promoting factor. Infection and Immunity 45:718–725
     [Google Scholar]
  24. Nakase Y., Tateishi M., Sekiya K., Kasuga T. 1970; Chemical and biological properties of the purified O antigen of Bordetella pertussis . Japanese Journal of Microbiology 14:1–8
     [Google Scholar]
  25. Peppler M. S. 1984; Two physically and serologically distinct lipopolysaccharide profiles in strains of Bordetella pertussis and their phenotype variants. Infection and Immunity 43:224–232
     [Google Scholar]
  26. Perera V. Y., Rogers H., Freer J. H. 1985; Onedimensional peptide mapping of the subunits of pertussis toxin. Journal of General Microbiology 131:1897–1901
     [Google Scholar]
  27. Preston N. W., Timewell R. M., Carter E. J. 1980; Experimental pertussis infection in the rabbit: similarities with infection in primates. Journal of Infection 2:227–235
     [Google Scholar]
  28. Robinson A., Gorringe A. R., Irons L. I., Keevil C. W. 1983; Antigenic modulation of Bordetella pertussis in continuous culture. FEMS Microbiology Letters 19:105–109
     [Google Scholar]
  29. Robinson A., Duggleby C. J., Gorringe A. R., Livey I. 1986; Antigenic variation in Bordetella pertussis . In Antigenic Variation in Infectious Diseases, pp. 147–161 Birkbeck T. H., Penn C. W. Edited by Oxford: IRL Press;
     [Google Scholar]
  30. Scheffer J., Konig W., Hacker J., Goebel W. 1985; Bacterial adherence and hemolysin production from Escherichia coli induces histamine and leukotriene release from various cells. Infection and Immunity 50:271–278
     [Google Scholar]
  31. Smith C. W., Hollers J. C., Dupree E., Goldman A. S., Lord R. A. 1972; A serum inhibitor of leukotaxis in a child with recurrent infections. Journal of Laboratory and Clinical Medicine 79:878–885
     [Google Scholar]
  32. Spangrude G. J., Sacchi F., Hill H. R., Van Epps D. E., Daynes R. A. 1985; Inhibition of lymphocyte and neutrophil chemotaxis by pertussis toxin. Journal of Immunology 135:4135–4143
     [Google Scholar]
  33. Stainer D. W., Scholte M. J. 1971; A simple chemically defined medium for the production of phase I Bordetella pertussis . Journal of General Microbiology 63:211–220
     [Google Scholar]
  34. Stendahl O. 1983; The physicochemical basis of surface interaction between bacteria and phagocytic cells. In Medical Microbiology 3, Role of the Envelope in the Survival of Bacterial Infection, pp 137–152 Easmon C. S. F., Jeljaszewicz J., Brown M. R., Lambert P. A. Edited by London: Academic Press;
     [Google Scholar]
  35. Topley N., Harber M. J., Asscher A. W. 1984; Influence of bacterial surface components on the stimulation of phagocyte chemiluminescence. In Analytical Applications of Bioluminescence and Chemiluminescence, pp. 409–410 Kricka L. J., Stanley P. E., Thorpe G. H., Whitehead T. P. Edited by London: Academic Press;
     [Google Scholar]
  36. Tuomanen E., Weiss A. 1985; Characterization of two adhesins of Bordetella pertussis for human ciliated respiratory-epithelial cells. Journal of Infectious Diseases 152:118–125
     [Google Scholar]
  37. Wardlaw A. C., Parton R. 1983; Bordetella pertussis toxins. Pharmacology and Therapeutics 19:1–53
     [Google Scholar]
  38. Weiss A. A., Hewlett E. L. 1986; Virulence factors of Bordetella pertussis . Annual Review of Microbiology 40:661–686
     [Google Scholar]
  39. Weiss A. A., Hewlett E. L., Myers G. A., Falkow S. 1983; Tn5-induced mutations affecting virulence factors of Bordetella pertussis . Infection and Immunity 42:33–41
     [Google Scholar]
  40. Wilkinson P. C. 1982 Chemotaxis and Inflammation,, 2nd edn.. Edinburgh: Churchill-Livingstone;
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-134-8-2201
Loading
Interaction of Bordetella pertussis Virulence Components with Neutrophils: Effect on Chemiluminescence Induced by a Chemotactic Peptide and by Intact Bacteria
Microbiology 134, 2201 (1988); https://doi.org/10.1099/00221287-134-8-2201
/content/journal/micro/10.1099/00221287-134-8-2201
/content/journal/micro/10.1099/00221287-134-8-2201
Loading

Data & Media loading...

Most cited 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