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. 1978 Jan;61(1):187–196. doi: 10.1172/JCI108917

Immunologic and Nonimmunologic Generation of Superoxide from Mast Cells and Basophils

William R Henderson 1, Michael Kaliner 1
PMCID: PMC372527  PMID: 73548

Abstract

Mediator release from rat peritoneal and human lung mast cells as well as human leukemic basophils was examined to determine whether super-oxide (O−2) was concomitantly generated. Immunologic or nonimmunologic stimulation of each preparation induced parallel release of histamine and O−2 within 2 min. O−2 production was quantitated by superoxide dismutase (SOD)-inhibitable chemiluminescence and cytochrome c reduction. SOD was detected in basophil and mast cell lysates and was also released by rat mast cells stimulated by anti-IgE. Secretory granules isolated from purified rat mast cells released histamine, O−2, and SOD upon exposure to cations. Thus, both superoxide radicals and SOD may play a role in host defenses involved in immediate hypersensitivity reactions.

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Selected References

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  1. Allen R. C., Stjernholm R. L., Steele R. H. Evidence for the generation of an electronic excitation state(s) in human polymorphonuclear leukocytes and its participation in bactericidal activity. Biochem Biophys Res Commun. 1972 May 26;47(4):679–684. doi: 10.1016/0006-291x(72)90545-1. [DOI] [PubMed] [Google Scholar]
  2. Anderson P., Röhlich P., Slorach S. A., Uvnäs B. Morphology and storage properties of rat mast cell granules isolated by different methods. Acta Physiol Scand. 1974 Jun;91(2):145–153. doi: 10.1111/j.1748-1716.1974.tb05670.x. [DOI] [PubMed] [Google Scholar]
  3. Askenase P. W., Haynes J. D., Hayden B. J. Antibody-mediated basophil accumulations in cutaneous hypersensitivity reactions of guinea pigs. J Immunol. 1976 Jul;117(1):216–224. [PubMed] [Google Scholar]
  4. Austen K. F., Orange R. P. Bronchial asthma: the possible role of the chemical mediators of immediate hypersensitivity in the pathogenesis of subacute chronic disease. Am Rev Respir Dis. 1975 Sep;112(3):423–436. doi: 10.1164/arrd.1975.112.3.423. [DOI] [PubMed] [Google Scholar]
  5. Babior B. M., Kipnes R. S., Curnutte J. T. Biological defense mechanisms. The production by leukocytes of superoxide, a potential bactericidal agent. J Clin Invest. 1973 Mar;52(3):741–744. doi: 10.1172/JCI107236. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Beauchamp C., Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem. 1971 Nov;44(1):276–287. doi: 10.1016/0003-2697(71)90370-8. [DOI] [PubMed] [Google Scholar]
  7. Becker E. L., Henson P. M. In vitro studies of immunologically induced secretion of mediators from cells and related phenomena. Adv Immunol. 1973;17:93–193. doi: 10.1016/s0065-2776(08)60732-4. [DOI] [PubMed] [Google Scholar]
  8. Bors W., Saran M., Lengfelder E., Spöttl R., Michel C. The relevance of the superoxide anion radical in biological systems. Curr Top Radiat Res Q. 1974 May;9(3):247–309. [PubMed] [Google Scholar]
  9. Cheson B. D., Christensen R. L., Sperling R., Kohler B. E., Babior B. M. The origin of the chemiluminescence of phagocytosing granulocytes. J Clin Invest. 1976 Oct;58(4):789–796. doi: 10.1172/JCI108530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Curnutte J. T., Babior B. M. Biological defense mechanisms. The effect of bacteria and serum on superoxide production by granulocytes. J Clin Invest. 1974 Jun;53(6):1662–1672. doi: 10.1172/JCI107717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Curnutte J. T., Whitten D. M., Babior B. M. Defective superoxide production by granulocytes from patients with chronic granulomatous disease. N Engl J Med. 1974 Mar 14;290(11):593–597. doi: 10.1056/NEJM197403142901104. [DOI] [PubMed] [Google Scholar]
  12. DAVIS B. J. DISC ELECTROPHORESIS. II. METHOD AND APPLICATION TO HUMAN SERUM PROTEINS. Ann N Y Acad Sci. 1964 Dec 28;121:404–427. doi: 10.1111/j.1749-6632.1964.tb14213.x. [DOI] [PubMed] [Google Scholar]
  13. Diamant B. Energy production in rat mast cells and its role for histamine release. Int Arch Allergy Appl Immunol. 1975;49(1-2):155–171. doi: 10.1159/000231391. [DOI] [PubMed] [Google Scholar]
  14. Dolovich J., Hargreave F. E., Chalmers R., Shier K. J., Gauldie J., Bienenstock J. Late cutaneous allergic responses in isolated IgE-dependent reactions. J Allergy Clin Immunol. 1973 Jul;52(1):38–46. doi: 10.1016/0091-6749(73)90119-x. [DOI] [PubMed] [Google Scholar]
  15. Drath D. B., Karnovsky M. L. Superoxide production by phagocytic leukocytes. J Exp Med. 1975 Jan 1;141(1):257–262. doi: 10.1084/jem.141.1.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dvorak H. F. Cutaneous basophil hypersensitivity. J Allergy Clin Immunol. 1976 Jul;58(1 Pt 2):229–240. doi: 10.1016/0091-6749(76)90159-7. [DOI] [PubMed] [Google Scholar]
  17. FAWCETT D. W. An experimental study of mast cell degranulation and regeneration. Anat Rec. 1955 Jan;121(1):29–51. doi: 10.1002/ar.1091210104. [DOI] [PubMed] [Google Scholar]
  18. Fairshter R. D., Wilson A. F. Paraquat poisoning: manifestations and therapy. Am J Med. 1975 Dec;59(6):751–753. doi: 10.1016/0002-9343(75)90459-3. [DOI] [PubMed] [Google Scholar]
  19. Fridovich I. Quantitative aspects of the production of superoxide anion radical by milk xanthine oxidase. J Biol Chem. 1970 Aug 25;245(16):4053–4057. [PubMed] [Google Scholar]
  20. Grosman N., Diamant B. Studies on histamine-retaining granules obtained from isolated rat mast cells. Agents Actions. 1976 Jul;6(4):394–401. doi: 10.1007/BF01973209. [DOI] [PubMed] [Google Scholar]
  21. Ishizaka T., Ishizaka K., Johansson S. G., Bennich H. Histamine release from human leukocytes by anti-gamma E antibodies. J Immunol. 1969 Apr;102(4):884–892. [PubMed] [Google Scholar]
  22. Johnston R. B., Jr, Keele B. B., Jr, Misra H. P., Lehmeyer J. E., Webb L. S., Baehner R. L., RaJagopalan K. V. The role of superoxide anion generation in phagocytic bactericidal activity. Studies with normal and chronic granulomatous disease leukocytes. J Clin Invest. 1975 Jun;55(6):1357–1372. doi: 10.1172/JCI108055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Johnston R. B., Jr, Lehmeyer J. E., Guthrie L. A. Generation of superoxide anion and chemiluminescence by human monocytes during phagocytosis and on contact with surface-bound immunoglobulin G. J Exp Med. 1976 Jun 1;143(6):1551–1556. doi: 10.1084/jem.143.6.1551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kaliner M., Orange R. P., Austen K. F. Immunological release of histamine and slow reacting substance of anaphylaxis from human lung. J Exp Med. 1972 Sep 1;136(3):556–567. doi: 10.1084/jem.136.3.556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Klebanoff S. J. Antimicrobial mechanisms in neutrophilic polymorphonuclear leukocytes. Semin Hematol. 1975 Apr;12(2):117–142. [PubMed] [Google Scholar]
  26. LAGUNOFF D., PHILLIPS M. T., ISERI O. A., BENDITT E. P. ISOLATION AND PRELIMINARY CHARACTERIZATION OF RAT MAST CELL GRANULES. Lab Invest. 1964 Nov;13:1331–1344. [PubMed] [Google Scholar]
  27. McCord J. M., Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969 Nov 25;244(22):6049–6055. [PubMed] [Google Scholar]
  28. McCord J. M., Fridovich I. The utility of superoxide dismutase in studying free radical reactions. I. Radicals generated by the interaction of sulfite, dimethyl sulfoxide, and oxygen. J Biol Chem. 1969 Nov 25;244(22):6056–6063. [PubMed] [Google Scholar]
  29. Nelson R. D., Mills E. L., Simmons R. L., Quie P. G. Chemiluminescence response of phagocytizing human monocytes. Infect Immun. 1976 Jul;14(1):129–134. doi: 10.1128/iai.14.1.129-134.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ogilvie B. M., Jones V. E. Immunity in the parasitic relationship between helminths and hosts. Prog Allergy. 1973;17:93–144. [PubMed] [Google Scholar]
  31. PADAWER J., GORDON A. S. Cellular elements in the peritoneal fluid of some mammals. Anat Rec. 1956 Feb;124(2):209–222. doi: 10.1002/ar.1091240206. [DOI] [PubMed] [Google Scholar]
  32. Pepys J., Hargreave F. E., Chan M., McCarthy D. S. Inhibitory effects of disodium cromoglycate on allergen-inhalation tests. Lancet. 1968 Jul 20;2(7560):134–137. doi: 10.1016/s0140-6736(68)90419-4. [DOI] [PubMed] [Google Scholar]
  33. Peterson C. Role of energy metabolism in histamine release. A study on isolated rat mast cells. Acta Physiol Scand Suppl. 1974;413:1–34. [PubMed] [Google Scholar]
  34. Rosen H., Klebanoff S. J. Chemiluminescence and superoxide production by myeloperoxidase-deficient leukocytes. J Clin Invest. 1976 Jul;58(1):50–60. doi: 10.1172/JCI108458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sagone A. L., Jr, King G. W., Metz E. N. A comparison of the metabolic response to phagocytosis in human granulocytes and monocytes. J Clin Invest. 1976 May;57(5):1352–1358. doi: 10.1172/JCI108403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sher A. Complement-dependent adherence of mast cells to schistosomula. Nature. 1976 Sep 23;263(5575):334–336. doi: 10.1038/263334a0. [DOI] [PubMed] [Google Scholar]
  37. Solley G. O., Gleich G. J., Jordon R. E., Schroeter A. L. The late phase of the immediate wheal and flare skin reaction. Its dependence upon IgE antibodies. J Clin Invest. 1976 Aug;58(2):408–420. doi: 10.1172/JCI108485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Stechschulte D. J., Austen K. F., Bloch K. J. Antibodies involved in antigen-induced release of slow reacting substance of anaphylaxis (SRS-A) in the guinea pig and rat. J Exp Med. 1967 Jan 1;125(1):127–147. doi: 10.1084/jem.125.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sullivan T. J., Parker C. W. Pharmacologic modulation of inflammatory mediator release by rat mast cells. Am J Pathol. 1976 Nov;85(2):437–464. [PMC free article] [PubMed] [Google Scholar]
  40. Sullivan T. J., Parker K. L., Stenson W., Parker C. W. Modulation of cyclic AMP in purified rat mast cells. I. Responses to pharmacologic, metabolic, and physical stimuli. J Immunol. 1975 May;114(5):1473–1479. [PubMed] [Google Scholar]
  41. Tada T., Ishizaka K. Distribution of gamma E-forming cells in lymphoid tissues of the human and monkey. J Immunol. 1970 Feb;104(2):377–387. [PubMed] [Google Scholar]
  42. Uvnäs B., Aborg C. H., Bergendorff A. Storage of histamine in mast cells. Evidence for an ionic binding of histamine to protein carboxyls in the granule heparin-protein complex. Acta Physiol Scand Suppl. 1970;336:1–26. [PubMed] [Google Scholar]
  43. Wasserman S. I., Goetzl E. J., Austen K. F. Preformed eosinophil chemotactic factor of anaphylaxis (ECF-A). J Immunol. 1974 Jan;112(1):351–358. [PubMed] [Google Scholar]
  44. Weening R. S., Wever R., Roos D. Quantitative aspects of the production of superoxide radicals by phagocytizing human granulocytes. J Lab Clin Med. 1975 Feb;85(2):245–252. [PubMed] [Google Scholar]

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