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Oxygen radical production by neutrophils from patients with bacterial infection and rheumatoid arthritis

Measurement of hydrogen peroxide may most accurately represent enhancement of oxygen radical production during infection

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Abstract

The production of three kinds of oxygen radicals (superoxide, hydrogen peroxide, and hydroxyl radicals) by neutrophils from patients with bacterial infection or rheumatoid arthritis was measured. The stimulators used in this study were opsonized zymosan (1 mg/ml), phorbol myristate acetate (20 ng/ml), A23187 (1μM, and platelet activating factor (1μM). Oxygen radical production by neutrophils from patients with rheumatoid arthritis was not significantly different from that of the control group. Hydrogen peroxide production by the neutrophils from patients with bacterial infection was significantly enhanced by only opsonized zymosan, but the production of the other kinds of oxygen radicals was not. Cytochalasin B reduced the production of hydrogen peroxide induced by opsonized zymosan more markedly than that of any other kind of oxygen radical. The measurement of hydrogen peroxide is suggested to be the most accurate indicator of the enhancement of intracellular production of oxygen radicals by neutrophils during infection.

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References

  1. Solberg, C. O., andK. B. Hellum. 1972. Neutrophil granulocyte function in bacterial infections.Lancet 2:727–730.

    Google Scholar 

  2. Koch, C. 1974. Acquired defect in the bactericidal function of neutrophil granuloctes during bacterial infections.Acta Pathol. Microbiol Scand. (B) 82:439–447.

    Google Scholar 

  3. McCall, C. E., L. R. DeChatelet, R. Butler, andD. Brown. 1974. The biologic basis for the elevated histochemical nitroblue tetrazolium reaction,J. Clin. Invest. 54:1227–1234.

    Google Scholar 

  4. Hill, H. R., W. J. Warwick, B. S. Dettloff, andP. G. Quie. 1974. Neutrophil granulocyte function in patients with pulmonary infection.J. Pediatr. 84:55–58.

    Google Scholar 

  5. Hill, H. R., J. M. Gerrard, N. A. Hogan, andP. G. Quie. 1974. Hyperactivity of neutrophil leukotactic responses during active bacterial infection.J. Clin. Invest. 53:996–1002.

    Google Scholar 

  6. McCall, C. E., L. R. DeChatelet, M. R. Cooper, C. Shannon. 1973. Human toxic neutrophils. III Metabolic characteristics.J. Infect. Dis. 127:26–33.

    Google Scholar 

  7. Barbour, A. G., C. D. Allred, C. O. Solberg, andH. R. Hill. 1980. Chemiluminescence by polymorphonuclear leukocytes from patients with active bacterial infection.J. Infect. Dis. 141:14–26.

    Google Scholar 

  8. Weissmann, G. 1972. Lysosomal mechanisms of tissue injury in arthritis.N. Engl. J. Med. 286: 141–147.

    Google Scholar 

  9. Janoff, A. 1975. At least three human neutrophil lysosomal proteases are capable of degrading joint connective tissues.Ann. N.Y. Acad. Sci. 256:402–408.

    Google Scholar 

  10. O'Flaherty, J. T., J. D. Schmitt, C. E. McCall, andR. L. Wykle. 1984. Diacylglycerols enhance human neutrophil degranulation responses: Relevancy to a multiple mediator hypothesis of cell function.Biochem. Biophys. Res. Commun. 123(1):64–70.

    Google Scholar 

  11. Rasmussen, H. andP. Q. Barrett. 1984. Calcium messenger system: An integrated view.Physiol. Rev. 64(3):938–984.

    Google Scholar 

  12. Bender, J. G. andD. E. Van Epps. 1985. Stimulus interactions in release of superoxide anion from human neutrophils. Further evidence for multiple pathways of activation.Inflammation 9(1):67–79.

    Google Scholar 

  13. Ozaki, Y., S. Kume, andT. Ohashi. 1984. Effect of histamine agonists and antagonists on luminol-dependent chemiluminescence of granulocytes.Agents Actions 15(3-4):182–189.

    Google Scholar 

  14. Cohen, P. P. 1957. Suspending media for normal tissues.In Monometric Techniques and Tissue Metabolism, 3rd ed.W. W. Umbreit, R. H. Burris, andJ. F. Stauffer, editors. Burgess Publishing, Minneapolis, 149–150.

    Google Scholar 

  15. Johnston, R. B., Jr., andJ. E. Lehmeyer. 1976. Elaboration of toxic oxygen byproducts by neutrophils in a model of immune complex diseases.J. Clin. Invest. 57:836.

    Google Scholar 

  16. Root, R. K., andJ. A. Metcalf. 1977. H2O2 release from human granulocytes during phagocytosis. Relationship to superoxide anion formation and cellular catabolism of H2O3: Studies with normal and cytochalasin B-treated cells.J. Clin. Invest. 60:1266–1279.

    Google Scholar 

  17. Klebanoff, S. J., andH. Rosen. 1978. Ethylene formation by polymorphonuclear leukocytes. Role of myeloperoxidase.J. Exp. Med. 147:490–505.

    Google Scholar 

  18. Winston, G. W., andA. I. Cederbaum. 1983. NADPH-dependent production of oxygen radicals by purified components of the rat liver mixed function oxidase system.J. Biol. Chem. 258:1508–1513.

    Google Scholar 

  19. Wenger, M. E. 1972. Nitroblue tetrazolium dye reduction by peripheral leukocytes from patients with rheumatoid arthritis and systemic lupus erythematosus.Arthritis Rheum. 15(4):459–460.

    Google Scholar 

  20. Niwa, Y., T. Sakane, M. Shingu, andM. Yokoyama. 1983. Effect of stimulated neutrophils from the synovial fluid of patients with rheumatoid arthritis on lymphocytes. A possible role of increased oxygen radicals generated by the neutrophils.J. Clin. Immunol. 3(3):228–240.

    Google Scholar 

  21. Boxer, L. A., M. Yoder, S. Bonsib, M. Schmidt, P. Ho, R. Jersild, andR. L. Baehner. 1979. Effects of a chemotactic factor,N-formylmethionyl peptide, on adherence, superoxide anion generation, phagocytosis and microtubule assembly of human polymorphonuclear leukocytes.J. Lab. Clin. Med. 93:506–514.

    Google Scholar 

  22. Smith, C. W., J. C. Hollers, R. A. Patrick, andC. Hassett. 1979. Motility and adhesiveness in human neutrophils, effects of chemotactic factors.J. Clin. Invest. 63:221–229.

    Google Scholar 

  23. Gallin, J. I., D. G., Wright, andE. Schiffmann. 1978. Role of secretory events in modulating human neutrophil chemotaxis.J. Clin. Invest. 62:1364–1374.

    Google Scholar 

  24. Issekutz, A. C., K. Lee, andW. D. Biggar. 1979. Enhancement of human neutrophil bactericidal activity by chemotactic factors.Infect Immun. 24:295–301.

    Google Scholar 

  25. Link, A. S., D. A. Bass, andC. E. McCall. 1978. Altered neutrophil migration in bacterial infection associated with a serum modulator of cellular motility.Clin. Res. 26:524A (abstract).

    Google Scholar 

  26. Lentnek, A. L., A. D., Schreiber, andR. R. MacGregor. 1976. The induction of augmented granulocyte adherence by inflammation.J. Clin. Invest. 57:1098–1103.

    Google Scholar 

  27. Dreidger, P. E., andP. M. Blumberg. 1980. Specific binding of phorbol ester tumor promoters.Proc. Natl. Acad. Sci. U.S.A. 77:567–571.

    Google Scholar 

  28. Tauber, A. I., D. B. Brettler, E. A. Kennington, andP. M. Blumberg. 1982. Relation of human neutrophil phorbol ester receptor occupancy and NADPH-oxidase activity.Blood 60:333–339.

    Google Scholar 

  29. Terashita, Z., S. Tsushima, Y. Yoshioka, H. Nomura, Y. Inada, andK. Nishikawa. 1983. CV-3988—a specific antagonist of platelet activating factor (PAF).Life Sci. 32:1975–1982.

    Google Scholar 

  30. Fletcher, M. P., andJ. I. Gallin. 1980. Degranulating stimuli increase the availability of receptors on human neutrophils for the chemoattractant f-Met-Leu-Phe.J. Immunol. 124:1585.

    Google Scholar 

  31. Fletcher, M. P., B. E. Seligmann, andJ. I. Gallin. 1982. Correlation of human neutrophil secretion, chemoattractant receptor mobilization, and enhanced functional capacity.J. Immunol. 128:941–948.

    Google Scholar 

  32. Niedel, J. E., L. J. Kuhn, andG. R. Vandenbark. 1983. Phorbol diester receptor copurifies with protein kinase C.Proc. Natl. Acad. Sci. U.S.A. 80:36–40.

    Google Scholar 

  33. DiVirgilio, F., D. P. Lew, andT. Pozzan. 1984. Protein kinase C activation of physiological processes in human neutrophils at vanishingly small cytosolic Ca levels.Nature 310:691–693.

    Google Scholar 

  34. Hallet, M. B., andA. K. Campbell. 1984. Is intracellular Ca the trigger for oxygen radical production by polymorphonuclear leukocytes?Cell Calcium 5:1–19.

    Google Scholar 

  35. O'Flaherty, J. T., R. L. Wykle, M. J. Thomas, andC. E. McCall. 1984. Neutrophil degranulation responses to combinations of arachidonte metabolites and platelet-activating factor.Res. Commun. Chem. Pathol. Pharmacol. 43:3–23.

    Google Scholar 

  36. Takenawa, T., Y. Homma, andY. Nagai. 1983. Role of Ca2+ in phosphatidylinositol response and arachidonic acid release in formylated tripeptideor Ca2+ ionophore A23187-stimulated guinea pig neutrophils.Immunology 130:2849–2855.

    Google Scholar 

  37. Matsumoto, T., K. Takeshige, andS. Minakami. 1984. Inhibition of phagocytotic metabolic changes of leukocytes by an intracellular calcium-antagonist 8-(n,n-diethyamino)-octyl-3,4,5 trimethoxygenzoate.Biochim. Biophys. Acta 803:271–277.

    Google Scholar 

  38. Lotner, G. Z., J. M. Lynch, S. J. Betz, andP. M. Henson. 1980. A platelet-activating factor derived from human neutrophils.J. Immunol. 124:676.

    Google Scholar 

  39. Takahashi, M., andK. Asada. 1983. Superoxide anion permeability of phospholipid membranes and chloroplast thylakoids.Arch. Biochem. Biophys. 226:558–566.

    Google Scholar 

  40. Malawista, S. E., J. B. L. Gee, andK. G. Bensch. 1971. Cytochalasin B reversibly inhibits phagocytosis: Functional, metabolic, and ultrastructural effects in human blood leukocytes and rabbit alveolar macrophages.Yale J. Biol. Med. 44:286.

    Google Scholar 

  41. Hartwig, J. H., andT. P. Stossel. 1976. Interaction of actin, myosin, and an actin-binding protein of rabbit pulmonary macrophages. III. Effects of Cytochalasin B.J. Cell Biol. 71:295.

    Google Scholar 

  42. Roos, D., W. T. Homan-Muller, andR. S. Weening. 1976. Effect of cytochalasin B on the oxidative metabolism of human peripheral blood granulocytes.Biochem. Biophys. Res. Commun. 68:43–50.

    Google Scholar 

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Authors and Affiliations

  1. First Department of Internal Medicine, School of Medicine, University of Tokyo, Tokyo, Japan

    Yukio Ozaki & Tatsuya Ōhashi

  2. Niwa Institute of Immunology, Tosashimizu, Kochi, Japan

    Yukie Niwa

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  1. Yukio Ozaki
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  2. Tatsuya Ōhashi
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Ozaki, Y., Ōhashi, T. & Niwa, Y. Oxygen radical production by neutrophils from patients with bacterial infection and rheumatoid arthritis. Inflammation 10, 119–130 (1986). https://doi.org/10.1007/BF00915994

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