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. 1983 Apr;48(4):657–665.

The stimulation of superoxide anion production in guinea-pig peritoneal macrophages and neutrophils by phorbol myristate acetate, opsonized zymosan and IgG2-containing soluble immune complexes.

M A Baxter, R G Leslie, W G Reeves
PMCID: PMC1454078  PMID: 6299935

Abstract

The kinetics of superoxide anion production in guinea-pig peritoneal macrophages and neutrophils were determined following in vitro stimulation with phorbol myristate acetate (PMA), opsonized zymosan (OZ) and soluble immune complexes of guinea-pig IgG2 (SIC). Superoxide production was recorded as chemiluminescence (CL) arising from the reductive cleavage of lucigenin. With PMA, both macrophages and neutrophils displayed a two-phase response consisting of a rapid initial burst of CL, which preceded ligand ingestion, followed by a plateau in the CL response which persisted for more than 30 min. By contrast, OZ induced a slow progressive increase in CL in both phagocytes which was consistent with the development of an oxidative burst concomitant with ingestion. The phagocytes differed in their responses to SIC, the macrophages displaying CL kinetics similar to those observed with PMA, whereas the neutrophils responded in the manner observed with OZ. The relationship between disparity in the patterns of macrophage and neutrophil CL responses to SIC and differences in their expression of Fc receptors for IgG2 (Coupland & Leslie, 1983) is discussed.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alexander E. L., Titus J. A., Segal D. M. Human leukocyte Fc (IgG) receptors: quantitation and affinity with radiolabeled affinity cross-linked rabbit IgG. J Immunol. 1979 Jul;123(1):295–302. [PubMed] [Google Scholar]
  2. Alexander M. D., Andrews J. A., Leslie R. G., Wood N. J. The binding of human and guinea-pig IgG subclasses to homologous macrophage and monocyte Fc receptors. Immunology. 1978 Jul;35(1):115–123. [PMC free article] [PubMed] [Google Scholar]
  3. Allred C. D., Margetts J., Hill H. R. Luminol-induced neutrophil chemiluminescence. Biochim Biophys Acta. 1980 Aug 13;631(2):380–385. doi: 10.1016/0304-4165(80)90311-6. [DOI] [PubMed] [Google Scholar]
  4. Andersen B. R., Brendzel A. M. Use of a unique chemiluminescence spectrometer in a study of factors influencing granulocyte light emission. J Immunol Methods. 1978;19(2-3):279–287. doi: 10.1016/0022-1759(78)90187-4. [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. Beall G. D., Repine J. E., Hoidal J. R., Rasp F. L. Chemiluminescence by human alveolar macrophages: stimulation with heat-killed bacteria or phorobol myristate acetate. Infect Immun. 1977 Jul;17(1):117–120. doi: 10.1128/iai.17.1.117-120.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carter S. D., Leslie R. G., Reeves W. G. Human monocyte binding of homologous monomer and complexed IgG. Immunology. 1982 Aug;46(4):793–800. [PMC free article] [PubMed] [Google Scholar]
  8. Connell P. A., Seehra M. S., Leslie R. G., Reeves W. G. Chemiluminescence of guinea pig peritoneal macrophages stimulated by immune precipitates and soluble immune complexes. Eur J Immunol. 1980 Dec;10(12):966–968. doi: 10.1002/eji.1830101214. [DOI] [PubMed] [Google Scholar]
  9. Coupland K., Leslie R. G. The expression of Fc receptors on guinea-pig peritoneal macrophages and neutrophils. Immunology. 1983 Apr;48(4):647–656. [PMC free article] [PubMed] [Google Scholar]
  10. Dower S. K., DeLisi C., Titus J. A., Segal D. M. Mechanism of binding of multivalent immune complexes to Fc receptors. 1. Equilibrium binding. Biochemistry. 1981 Oct 27;20(22):6326–6334. doi: 10.1021/bi00525a007. [DOI] [PubMed] [Google Scholar]
  11. Ehlenberger A. G., Nussenzweig V. The role of membrane receptors for C3b and C3d in phagocytosis. J Exp Med. 1977 Feb 1;145(2):357–371. doi: 10.1084/jem.145.2.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goldstein I. M., Roos D., Kaplan H. B., Weissmann G. Complement and immunoglobulins stimulate superoxide production by human leukocytes independently of phagocytosis. J Clin Invest. 1975 Nov;56(5):1155–1163. doi: 10.1172/JCI108191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Griffin F. M., Jr, Silverstein S. C. Segmental response of the macrophage plasma membrane to a phagocytic stimulus. J Exp Med. 1974 Feb 1;139(2):323–336. doi: 10.1084/jem.139.2.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Henson P. M., Oades Z. G. Stimulation of human neutrophils by soluble and insoluble immunoglobulin aggregates. Secretion of granule constituents and increased oxidation of glucose. J Clin Invest. 1975 Oct;56(4):1053–1061. doi: 10.1172/JCI108152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Henson P. M. The immunologic release of constituents from neutrophil leukocytes. I. The role of antibody and complement on nonphagocytosable surfaces or phagocytosable particles. J Immunol. 1971 Dec;107(6):1535–1546. [PubMed] [Google Scholar]
  16. 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]
  17. Lay W. H., Nussenzweig V. Receptors for complement of leukocytes. J Exp Med. 1968 Nov 1;128(5):991–1009. doi: 10.1084/jem.128.5.991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Leslie R. G., Alexander M. D. Cytophilic antibodies. Curr Top Microbiol Immunol. 1979;88:25–104. doi: 10.1007/978-3-642-67331-3_2. [DOI] [PubMed] [Google Scholar]
  19. Leslie R. G. Macrophage handling of soluble immune complexes. Ingestion and digestion of surface-bound complexes at 4, 20 and 37 degrees C. Eur J Immunol. 1980 May;10(5):323–333. doi: 10.1002/eji.1830100503. [DOI] [PubMed] [Google Scholar]
  20. Leslie R. G. The binding of soluble immune complexes of guinea pig IgG2 to homologous peritoneal macrophages. Determination of the avidity constants at 4 degrees C. Eur J Immunol. 1980 May;10(5):317–322. doi: 10.1002/eji.1830100502. [DOI] [PubMed] [Google Scholar]
  21. Morrison A. D., Pruzanski W., Ranadive N. S. Release of lysosomal enzymes from human polymorphonuclear leukocytes by soluble intermediate immune complexes. Scand J Rheumatol. 1978;7(4):241–246. doi: 10.3109/03009747809095663. [DOI] [PubMed] [Google Scholar]
  22. Newman S. L., Johnston R. B., Jr Role of binding through C3b and IgG in polymorphonuclear neutrophil function: studies with trypsin-generated C3b. J Immunol. 1979 Oct;123(4):1839–1846. [PubMed] [Google Scholar]
  23. Pestel J., Joseph M., Dessaint J. P., Capron A. Macrophage triggering by aggregated immunoglobulins. I. Delayed effect of IgG aggregates or immune complexes. J Immunol. 1981 May;126(5):1887–1891. [PubMed] [Google Scholar]
  24. Repine J. E., White J. G., Clawson C. C., Holmes B. M. The influence of phorbol myristate acetate on oxygen consumption by polymorphonuclear leukocytes. J Lab Clin Med. 1974 Jun;83(6):911–920. [PubMed] [Google Scholar]
  25. Segal D. M., Hurwitz E. Binding of affinity cross-linked oligomers of IgG to cells bearing Fc receptors. J Immunol. 1977 Apr;118(4):1338–1337. [PubMed] [Google Scholar]
  26. Stahl P., Schlesinger P. H., Sigardson E., Rodman J. S., Lee Y. C. Receptor-mediated pinocytosis of mannose glycoconjugates by macrophages: characterization and evidence for receptor recycling. Cell. 1980 Jan;19(1):207–215. doi: 10.1016/0092-8674(80)90402-x. [DOI] [PubMed] [Google Scholar]
  27. Steinman R. M., Brodie S. E., Cohn Z. A. Membrane flow during pinocytosis. A stereologic analysis. J Cell Biol. 1976 Mar;68(3):665–687. doi: 10.1083/jcb.68.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tamoto K., Koyama J. Superoxide anion production from guinea pig macrophages stimulated with immune complexes of different IgG subclasses. J Biochem. 1980 Jun;87(6):1649–1657. doi: 10.1093/oxfordjournals.jbchem.a132909. [DOI] [PubMed] [Google Scholar]
  29. Williams A. J., Cole P. J. In vitro stimulation of alveolar macrophage metabolic activity by polystyrene in the absence of phagocytosis. Br J Exp Pathol. 1981 Feb;62(1):1–7. [PMC free article] [PubMed] [Google Scholar]
  30. Williams A. J., Cole P. J. Polymorphonuclear leucocyte membrane-stimulated oxidative metabolic activity---the effect of divalent cations and cytochalasins. Immunology. 1981 Dec;44(4):847–858. [PMC free article] [PubMed] [Google Scholar]
  31. Ziprin R. L. Phagocytosis by sheep alveolar macrophages: relationship between opsonin concentration and light emission in the presence of luminol. Infect Immun. 1978 Mar;19(3):889–892. doi: 10.1128/iai.19.3.889-892.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]

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