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PMID: 1314225 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Bordetella pertussis induces respiratory burst activity in human polymorphonuclear leukocytes.

Infection and immunity ·Vol. 60 ·No. 5 ·1992-05-00 ·Pages 2101-5

Steed LL, Akporiaye ET, Friedman RL

Abstract

Virulent Bordetella pertussis strains survive intracellularly within human polymorphonuclear leukocytes (PMN), at least in part because of inhibition of phagosome-lysosome fusion (L. L. Steed, M. Setareh, and R. L. Friedman, J. Leukocyte Biol. 50:321-330, 1991). Further investigations were done to determine if B. pertussis also inhibited respiratory burst activity of PMN as an additional mechanism of intracellular survival. Chemiluminescence and flow cytometry assays showed that B. pertussis induced significant levels of hydrogen peroxide production. In contrast, ferricytochrome c reduction showed that B. pertussis suppressed extracellular release of superoxide. PMN intracellular reduction of nitroblue tetrazolium verified that superoxide was indeed produced intracellularly during B. pertussis phagocytosis. Therefore, B. pertussis does not inhibit production of superoxide but inhibits only its release. Thus, while phagosome-lysosome fusion is inhibited by B. pertussis, respiratory burst activity of PMN occurs at normal levels.

MeSH Terms
Bordetella pertussis/pathogenicity Cell Fusion Humans Hydrogen Peroxide/metabolism Luminescent Measurements Neutrophils/metabolism,microbiology Nitroblue Tetrazolium/metabolism Phagosomes/physiology Respiratory Burst/physiology Superoxide Dismutase/pharmacology Superoxides/metabolism Tetradecanoylphorbol Acetate/pharmacology
Chemicals
Superoxides Nitroblue Tetrazolium Hydrogen Peroxide Superoxide Dismutase Tetradecanoylphorbol Acetate
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Steed L L
Department of Microbiology and Immunology, University of Arizona, Tucson 85724.
Akporiaye E T
Friedman R L
References (49)
49 references, click to expand
  1. Interaction of Bordetella pertussis virulence components with neutrophils: effect on chemiluminescence induced by a chemotactic peptide and by intact bacteria.
    J Gen Microbiol. 1988 Aug;134(8):2201-11 PMID: 2908118
  2. Ingestion and intracellular survival of Brucella abortus in human and bovine polymorphonuclear leukocytes.
    Infect Immun. 1984 Oct;46(1):224-30 PMID: 6090315
  3. Mycobacterium leprae fails to stimulate phagocytic cell superoxide anion generation.
    Infect Immun. 1986 Feb;51(2):514-20 PMID: 3002986
  4. Histoplasma capsulatum fails to trigger release of superoxide from macrophages.
    Infect Immun. 1987 Jan;55(1):29-34 PMID: 3025100
  5. Reduction of ferricytochrome C may underestimate superoxide production by monocytes.
    J Immunol Methods. 1987 Apr 2;98(1):63-9 PMID: 3031166
  6. Role of superoxide dismutase and catalase as determinants of pathogenicity of Nocardia asteroides: importance in resistance to microbicidal activities of human polymorphonuclear neutrophils.
    Infect Immun. 1985 Jan;47(1):135-41 PMID: 3880721
  7. Pattern of formylmethionyl-leucyl-phenylalanine-induced luminol- and lucigenin-dependent chemiluminescence in human neutrophils.
    Infect Immun. 1985 Jan;47(1):326-8 PMID: 3965405
  8. Effect of normal and activated human macrophages on Toxoplasma gondii.
    J Exp Med. 1974 May 1;139(5):1154-74 PMID: 4132992
  9. Macrophage behaviour during the complaisant phase of murine pertussis.
    Immunology. 1969 Dec;17(6):875-87 PMID: 4318529
  10. The steady state in cellular immunity. II. Immunological complaisance in murine pertussis.
    Aust J Exp Biol Med Sci. 1967 Aug;45(4):417-26 PMID: 6070045
  11. Phagocyte impotence caused by an invasive bacterial adenylate cyclase.
    Science. 1982 Sep 3;217(4563):948-50 PMID: 6287574
  12. Opsonic requirements for staphylococcal phagocytosis. Heterogeneity among strains.
    Immunology. 1977 Aug;33(2):191-7 PMID: 415969
  13. Catalase, superoxide dismutase, and virulence of Staphylococcus aureus. In vitro and in vivo studies with emphasis on staphylococcal--leukocyte interaction.
    J Clin Invest. 1975 Mar;55(3):561-6 PMID: 1117067
  14. Genetic analysis of superoxide dismutase, the 23 kilodalton antigen of Mycobacterium tuberculosis.
    Mol Microbiol. 1991 Feb;5(2):381-91 PMID: 1904126
  15. Intracellular survival of virulent Bordetella pertussis in human polymorphonuclear leukocytes.
    J Leukoc Biol. 1991 Oct;50(4):321-30 PMID: 1919361
  16. The respiratory burst response to Histoplasma capsulatum by human neutrophils. Evidence for intracellular trapping of superoxide anion.
    J Immunol. 1990 Jun 15;144(12):4765-72 PMID: 1972167
  17. Integrin-mediated localization of Bordetella pertussis within macrophages: role in pulmonary colonization.
    J Exp Med. 1991 May 1;173(5):1143-9 PMID: 2022924
  18. The human neutrophil respiratory burst oxidase.
    J Infect Dis. 1990 Jun;161(6):1140-7 PMID: 2161041
  19. Bordetella pertussis adenylate cyclase toxin: intoxication of host cells by bacterial invasion.
    Infect Immun. 1990 Nov;58(11):3759-64 PMID: 2172167
  20. A new assay for invasion of HeLa 229 cells by Bordetella pertussis: effects of inhibitors, phenotypic modulation, and genetic alterations.
    Infect Immun. 1990 Aug;58(8):2516-22 PMID: 2370104
  21. Regulation of human neutrophil type 3 complement receptor (iC3b receptor) expression during phagocytosis of Staphylococcus aureus and Escherichia coli.
    Immunology. 1989 Aug;67(4):460-5 PMID: 2527804
  22. Invasion of HeLa 229 cells by virulent Bordetella pertussis.
    Infect Immun. 1989 Sep;57(9):2698-704 PMID: 2547718
  23. Polymorphonuclear leukocyte function during hemodialysis: relationship to complement activation.
    Nephron. 1989;52(2):119-24 PMID: 2739846
  24. Bordetella pertussis adenylate cyclase: effects of affinity-purified adenylate cyclase on human polymorphonuclear leukocyte functions.
    Infect Immun. 1987 Jan;55(1):135-40 PMID: 2878884
  25. The respiratory burst of phagocytes.
    J Clin Invest. 1984 Mar;73(3):599-601 PMID: 6323522
  26. Flow cytometric quantitation of oxidative product formation by polymorphonuclear leukocytes during phagocytosis.
    J Immunol. 1984 Dec;133(6):3303-7 PMID: 6491287
  27. Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation.
    J Immunol. 1983 Apr;130(4):1910-7 PMID: 6833755
  28. The effects of Legionella pneumophila toxin on oxidative processes and bacterial killing of human polymorphonuclear leukocytes.
    J Infect Dis. 1982 Sep;146(3):328-34 PMID: 7050255
  29. Diminished neutrophil oxidative metabolism after phagocytosis of virulent Salmonella typhi.
    Infect Immun. 1981 Feb;31(2):674-8 PMID: 7216467
  30. The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes.
    J Exp Med. 1983 Dec 1;158(6):2108-26 PMID: 6644240
  31. Influence of the Escherichia coli capsule on complement fixation and on phagocytosis and killing by human phagocytes.
    J Clin Invest. 1980 Jan;65(1):82-94 PMID: 6985617
  32. Intra- and extracellular events in luminol-dependent chemiluminescence of polymorphonuclear leukocytes.
    Infect Immun. 1984 Jul;45(1):1-5 PMID: 6329953
  33. Interaction of polymorphonuclear leukocytes with smooth and rough strains of Brucella abortus.
    Infect Immun. 1979 Mar;23(3):737-42 PMID: 110680
  34. Stimulation of human neutrophil oxidative metabolism by nonopsonized Neisseria gonorrhoeae.
    Infect Immun. 1991 Dec;59(12):4383-90 PMID: 1657785
  35. Detection of Bordetella pertussis associated with the alveolar macrophages of children with human immunodeficiency virus infection.
    Infect Immun. 1991 Dec;59(12):4715-9 PMID: 1937833
  36. Coxiella burnetii fails to stimulate human neutrophil superoxide anion production.
    Acta Virol. 1990 Feb;34(1):64-70 PMID: 1975727
  37. Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2',7'-dichlorofluorescin.
    J Leukoc Biol. 1990 May;47(5):440-8 PMID: 2159514
  38. Adenylate cyclase toxin of Bordetella pertussis: production, purification, and partial characterization.
    Infect Immun. 1990 Nov;58(11):3621-6 PMID: 2228232
  39. Contribution of superoxide dismutase and catalase activities to Shigella flexneri pathogenesis.
    Infect Immun. 1990 Feb;58(2):529-35 PMID: 2404874
  40. Altered polymorphonuclear neutrophilic granulocyte functions in patients with large burns.
    J Trauma. 1989 Jun;29(6):847-55 PMID: 2661844
  41. Virulence factors of Bordetella pertussis.
    Annu Rev Microbiol. 1986;40:661-86 PMID: 2877614
  42. Effects of adenylate cyclase toxin from Bordetella pertussis on human neutrophil interactions with Coccidioides immitis and Staphylococcus aureus.
    Infect Immun. 1988 Apr;56(4):751-5 PMID: 2894360
  43. Inhibition of lymphocyte and neutrophil chemotaxis by pertussis toxin.
    J Immunol. 1985 Dec;135(6):4135-43 PMID: 2999238
  44. Pertussis toxin as a probe of neutrophil activation.
    Fed Proc. 1986 Jun;45(7):2151-5 PMID: 3011523
  45. Evidence for activation of a respiratory burst in the interaction of human neutrophils with Mycobacterium tuberculosis.
    Infect Immun. 1987 Sep;55(9):2304-7 PMID: 3040594
  46. Survival and growth of Yersinia pestis within macrophages and an effect of the loss of the 47-megadalton plasmid on growth in macrophages.
    Infect Immun. 1985 Jan;47(1):234-41 PMID: 3965398
  47. The effect of Chlamydia trachomatis on luminol-dependent chemiluminescence of human polymorphonuclear leukocytes: requirements for opsonization.
    J Infect Dis. 1985 Jun;151(6):1045-51 PMID: 3998506
  48. An electron-microscope study of intracerebral infection of mice with low-virulence Bordetella pertussis.
    J Med Microbiol. 1972 Feb;5(1):154-7 PMID: 4336736
  49. Bordetella parapertussis invasion of HeLa 229 cells and human respiratory epithelial cells in primary culture.
    Infect Immun. 1989 Apr;57(4):1240-7 PMID: 2925250
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
DOI
10.1128/iai.60.5.2101-2105.1992
Published
1992-05-00
Pages
2101-5
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC257121
Subset
IM
Grants
NCI NIH HHS · CA 39827 · United States
PHS HHS · R01-A1 22822 · United States
External Links
PubMed source DOI: 10.1128/iai.60.5.2101-2105.1992 PMC Full Text View journal details
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