Advertisement

An Expanded View of the Phagocytic Respiratory Burst

Bacterial Competition for Oxygen and Its Stimulation by Host Factor(s)
  • Myron S. Cohen
  • Bradley E. Britigan

Abstract

Baldridge and Gerard in 19331 made the seminal observation that leukocyte consumption of ambient O2 increases markedly during the early stages of phagocytosis. Over the ensuing 43 years remarkable progress was made in characterizing the mechanisms and ramifications of this phenomenon, identified by Babior as the respiratory burst.2 Consumption of O2 by neutrophils and monocytes during phagocytosis leads to the purposeful formation of superoxide, a unique capacity of phagocytic cells. Production of superoxide and subsequent formation of other reactive oxygen intermediates (e.g., H2O2 and OCl-) is critical to the microbicidal activity of these cells.3 This is graphically demonstrated by the natural history of patients with chronic granulomatous disease (CGD) of childhood, whose phagocytes lack the capacity to develop a respiratory burst.3, 4

Keywords

Phorbol Myristate Acetate Respiratory Burst Chronic Granulomatous Disease Hank Balance Salt Solution Neisseria Gonorrhoeae 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Baldridge CW, Gerard RW: The extra respiration of phagocytosis. Am J Physiol 103: 235–236, 1933.Google Scholar
  2. 2.
    Babior BM: Oxygen-dependent microbial killing. N Engl J Med 298: 659–668, 1978.PubMedCrossRefGoogle Scholar
  3. 3.
    Root RK, Cohen MS: The microbial mechanisms of human neutrophils and eosinophils. Rev Infect Dis 3: 565–598, 1981.PubMedCrossRefGoogle Scholar
  4. 4.
    Tauber AI, Borregaard N, Simons E, et al: Chronic granulomatous disease: A syndrome of phagocyte oxidase deficiencies. Medicine (Baltimore) 62: 286–308, 1983.Google Scholar
  5. 5.
    Densen P, Mandell G: Phagocyte strategy versus microbial tactics. Rev Infect Dis 2: 817–838, 1980.PubMedCrossRefGoogle Scholar
  6. 6.
    Miller RM, Carbus J, Hornick RB: Lack of enhanced oxygen consumption by polymorphonuclear leukocytes on phagocytosis of virulent Salmonella typhi. Science 175: 1010–1011, 1972.PubMedCrossRefGoogle Scholar
  7. 7.
    Kossack RE, Guerrant RL, Densen P, et al: Diminished neutrophil oxidative metabolism after phagocytosis of virulent Salmonella typhi. Infect Immun 31: 674–679, 1981.PubMedGoogle Scholar
  8. 8.
    Wilson CB, Tsai V, Remington JS: Failure to trigger the oxidative metabolic burst by normal macrophages: Possible mechanisms for survival of intracellular pathogens. J Exp Med 151: 328–346, 1980.PubMedCrossRefGoogle Scholar
  9. 9.
    Kreutzer DL, Dreyfus LA, Robertson DC: Interaction of polymorphonuclear leukocytes with smooth and rough strains of Brucella abortus. Infect Immun 23: 737–742, 1979.PubMedGoogle Scholar
  10. 10.
    Mandell GL: Catalase, superoxide dismutase and virulence of Staphylococcus aureus: In vitro and in vivo studies with emphasis on staphylococcal-leukocyte interaction. J Clin Invest 55: 561–566, 1979.CrossRefGoogle Scholar
  11. 11.
    Welch DF, Sword CP, Brehm S, et al: Relationship between superoxide dismutase and pathogenic mechanisms of Listeria monocytogenes. Infect Immun 23: 863–879, 1982.Google Scholar
  12. 12.
    Beaman BL, Scates SM, Moring E, et al: Purification and properties of a unique superoxide dismutase from Nocardia asteroides. J Biol Chem 258: 91–96, 1983.PubMedGoogle Scholar
  13. 13.
    Klebanoff S: Myeloperoxidase, halide-hydrogen peroxide antibacterial system. J Bacteriol 95: 2131–2138, 1968.PubMedGoogle Scholar
  14. 14.
    Jones TC, Hirsch JG: The interaction between Toxoplasma gondii and mammalian cells. II. The absence of lysosomal fusion with phagocytic vacuoles containing living parasites. J Exp Med 136: 1173–1194, 1972.PubMedCrossRefGoogle Scholar
  15. 15.
    Mandell G: Bactericidal activity of aerobic and anaerobic polymorphonuclear neutrophils. Infect Immun 9: 337–341, 1974.PubMedGoogle Scholar
  16. 16.
    Harrison DEF: Regulation of respiration rate in growing bacteria. Adv Microbiol Physiol 14: 243–313, 1976.CrossRefGoogle Scholar
  17. 17.
    Cohen MS, Cooney MH: A bacterial respiratory burst: Stimulation of Neisseria gonorrhoeae by human serum. J Infect Dis 150: 49–56, 1984.PubMedCrossRefGoogle Scholar
  18. 18.
    Britigan BE, Cohen MS: Effects of human serum on bacterial competition with neutrophils for molecular oxygen. Infect Immun 52: 657–663, 1986.PubMedGoogle Scholar
  19. 19.
    Britigan BE, Chai Y, Cohen MS: Effects of human serum on the growth and metabolism of Neisseria gonorrhoeae: An alternative view of serum. Infect Immun 50: 738–744, 1985.PubMedGoogle Scholar
  20. 20.
    Root RK, Rosenthal AS, Balestra DJ: Abnormal bactericidal, metabolic and lysosomal fuctions of Chediak-Higashi syndrome leukocytes. J Clin Invest 51: 649–665, 1972.PubMedCrossRefGoogle Scholar
  21. 21.
    Verhoef J, Peterson PR, Sabath DL, et al: Kinetics of staphylococcal opsonization, attachment, ingestion, and killing by human polymorphornuclear leukocytes using [3H]-thymidine labeled bacte-ria. J Immunol Methods 14: 303–311, 1977.PubMedCrossRefGoogle Scholar
  22. 22.
    DeChatelet LR, Shirley PS, Johnston RB: Effect of phorbol myristate acetate on the oxidative metabolism of polymorphonuclear leukocytes. Blood 47: 545–554, 1976.PubMedGoogle Scholar
  23. 23.
    Root RK, Metealf J, Oshino N, et al: H202 release from human granulocytes during phagocytosis. 1. Documentation, quantitation, and some regulating factors. J Clin Invest 55: 945–955, 1975.PubMedCrossRefGoogle Scholar
  24. 24.
    Morse SA: The biology of the gonococcus. CRC Crit Rev Microbiol 7: 93–189, 1978.PubMedCrossRefGoogle Scholar
  25. 25.
    Rotstein OD, Pruett TL, Fiegel VD, et al: Succinic acid, a metabolic by-product of Bacteroides species, inhibits polymorphonuclear leukocyte function. Infect Immun 48: 402–408, 1985.PubMedGoogle Scholar
  26. 26.
    Gabrig TC, Bearman SI, Babior BM: Effects of oxygen tension and pH on the respiratory burst of human neutrophils. 53: 1133–1139, 1979.Google Scholar
  27. 27.
    Edwards SN, Hallett MB, Campbell AK: Oxygen-radical production during inflammation may be limited by oxygen concentration. Biochem J 217: 851–854, 1984.PubMedGoogle Scholar
  28. 28.
    Hays RC, Mandel GL: p02, pH, and redox potential of experimental abscesses. Proc Soc Exp Biol Med 147: 29–30, 1974.PubMedGoogle Scholar
  29. 29.
    Rotstein OD, Pruett TL, Simmons RL: Mechanisms of microbial synergy in polymicrobial surgical infections. Rev Infect Dis 7: 151–170, 1985.PubMedCrossRefGoogle Scholar
  30. 30.
    Edwards SW, Hallett MB, Lloyd D, et al: Decrease in apparent Km for oxygen after stimulation of respiration of rat polymorphonuclear leukocytes. FEBS Lett 161: 60–64, 1983.PubMedCrossRefGoogle Scholar
  31. 31.
    Cohen MS, Black JR, Proctor RA, et al: Host defence and the vaginal mucosa: A réévaluation. Scand J Urol Nephrol (suppl) 86: 13–22, 1985.Google Scholar
  32. 32.
    Britigan BE, Cohen MS, Sparling PF: Gonococcal infection: A model of molecular pathogenesis. N Engl J Med 312: 1683–1694, 1985.PubMedCrossRefGoogle Scholar
  33. 33.
    Cannon JG, Sparling PF: The genetics of the gonococcus. Annu Rev Microbiol 38: 111–133, 1984.PubMedCrossRefGoogle Scholar
  34. 34.
    Kellogg DS, Peacock WL Jr, Deacon WE, et al: Neisseria gonorrhoeae. I. Virulence genetically linked to clonal variation. J Bacteriol 85: 1274–1279, 1963.PubMedGoogle Scholar
  35. 35.
    Diam K: Documenta Geigy Scientific Tables. Ardsley, New York, Geigy Pharmaceuticals, 1962.Google Scholar
  36. 36.
    Hughes DE, Wimpenny JWT: Oxygen metabolism by micro-organisms. Adv Microbiol Physiol 3: 197–232, 1969.CrossRefGoogle Scholar
  37. 37.
    Rest, RF, Fischer SH, Ingham ZZ, et al: Interaction of Neisseria gonorrhoeae with human neutrophils: Effects of serum and gonococcal opacity on phagocyte killing and chemiluminescence. Infect Immun 36: 737–744, 1982.PubMedGoogle Scholar
  38. 38.
    Rest RF, Lee N, Bowden C: Stimulation of human leukocytes by protein 11+ gonococci is mediated by lectin-like gonococcal components. Infect Immun 50: 116–122, 1985.PubMedGoogle Scholar
  39. 39.
    DeChatelet LR, Mullikin DS, Shirley PS, et al: Phagocytosis of live versus heat-killed bacteria by human polymorphonuclear leukocytes. Infect Immun 10: 25–29, 1974.PubMedGoogle Scholar
  40. 40.
    Britigan BE, Klapper D, Svendsen T, Cohen MS: Phagocyte-derived lactate stimulates oxygen consumption by Neisseria gonorrhoeae: An unrecognized aspect of the oxygen metabolism of phagocytosis. J Clin Invest 81: 318–324, 1988.PubMedCrossRefGoogle Scholar
  41. 41.
    Harris P, Ralph P: Human leukemic models of myelomonocytic development: A review of the HL-60 and U937 cell lines. J Leukocyte Biol 37: 407–422, 1985.PubMedGoogle Scholar
  42. 42.
    Munroe JF, Shipp JC: Glucose metabolism in leucocytes from patients with diabetes mellitus, with and without hypercholesterolemia. Diabetes 14: 584–590, 1965.PubMedGoogle Scholar
  43. 43.
    Garvie, EI: Bacterial lactate dehydrogenase. Microbiol Rev 44: 106–139, 1980.PubMedGoogle Scholar
  44. 44.
    Johnston KH, Gotschlich EC: Isolation and characterization of the outer membrane of Neisseria gonorrhoeae. J Bacteriol 119: 250–257, 1974.PubMedGoogle Scholar
  45. 45.
    Barron ESG, Hastings AB: Studies on biological oxidations II. The oxidation of lactic acid by a- hydroxyoxidase and its metabolism. J Biol Chem 100: 155–182, 1933.Google Scholar
  46. 46.
    Van Zwieten RR, Wever MN, Hamers RS, et al: Extracellular proton release by stimulated neutrophils. J Clin Invest 63: 310–313, 1981.CrossRefGoogle Scholar
  47. 47.
    Elsbach P, Weiss J: A réévaluation of the roles of 02-dependent and 02-independent microbicidal systems of phagocytes. Rev Infect Dis 5: 843–853, 1983.PubMedCrossRefGoogle Scholar
  48. 48.
    Ganz T, Selsted ME, Harwig SL, et al: Defensins. Natural peptide antibiotics of human neutrophils. J Clin Invest 76: 1427–1435, 1985.PubMedCrossRefGoogle Scholar
  49. 49.
    Rest RF: Killing of Neisseria gonorrhoeae by human polymorphonuclear neutrophil granule extracts. Infect Immun 25: 574–579, 1979.PubMedGoogle Scholar
  50. 50.
    Modrzakowski MC, Spitznagel JK: Bactericidal activity of fractionated granule contents from human polymorphonuclear leukocytes: Antagonism of granule cationic proteins by lipopolysac- charide. Infect Immun 25: 597–602, 1979.PubMedGoogle Scholar
  51. 51.
    Casey SG, Shafer WM, Spitznagel JK: Anaerobiosis increases resistance of Neisseria gonorrhoeae to 02-independent antimicrobial proteins from human polymorphonuclear granulocytes. Infect Immun 47: 401–407, 1985.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1988

Authors and Affiliations

  • Myron S. Cohen
    • 1
  • Bradley E. Britigan
    • 2
  1. 1.Departments of Medicine and Microbiology and Immunology, Division of Infectious DiseasesUniversity of North CarolinaChapel HillUSA
  2. 2.Department of MedicineUniversity of North CarolinaChapel HillUSA

Personalised recommendations