Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1989 Aug;57(8):2529–2533. doi: 10.1128/iai.57.8.2529-2533.1989

Phorbol myristate acetate modulates calcium ion-dependent superoxide anion generation induced by a monoclonal antibody raised against polymorphonuclear leukocytes.

Y Ichinose 1, N Hara 1, M Ohta 1, A Motohiro 1, T Kuda 1, H Aso 1, K Yagawa 1
PMCID: PMC313481  PMID: 2545627

Abstract

We used a monoclonal antibody, YI 51, raised against human polymorphonuclear leukocytes (PMN) to induce superoxide anion (O2-) generation in cells. Although YI 51 alone played only a small part in inducing O2- generation in PMN, the amount of O2- generation induced in 5 X 10(5) PMN was 3.7 to 5.5 nmol/min when F(ab')2 fragments of rabbit anti-mouse immunoglobulin antibody were added as a cross-linking agent. This O2- -inducing activity was high compared with that of wheat germ agglutinin (WGA), insoluble immunoglobulin G immune complexes (IC), or phorbol myristate acetate (PMA). The binding of YI 51 and soluble immunoglobulin G IC to PMN was not reciprocally inhibitory, indicating that YI 51 does not interfere with ligand binding to the Fc receptor-binding site. In the absence of calcium ion (Ca2+), O2- generation induced by YI 51 decreased to 10 to 20% of that in the presence of Ca2+. In contrast, O2- generation in response to WGA, IC, or PMA under Ca2+-free conditions was not affected. When PMN were pretreated with low concentrations of PMA (10(-10) to 10(-9) M), the amount of O2- generation by the cells in response to YI 51 in Ca2+-free buffer was enhanced in a concentration-dependent manner. It also equaled the O2- generated by the cells in buffer containing Ca2+. In cells pretreated with PMA, the amount of O2- induced by WGA was enhanced two- to threefold over that in untreated cells. In contrast, there was no augmentation over untreated cells with stimulation by IC. These results suggest that YI 51, IC, and WGA induce O2- generation in human PMN in different manners.

Full text

PDF
2529

Selected References

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

  1. Anderson C. L., Guyre P. M., Whitin J. C., Ryan D. H., Looney R. J., Fanger M. W. Monoclonal antibodies to Fc receptors for IgG on human mononuclear phagocytes. Antibody characterization and induction of superoxide production in a monocyte cell line. J Biol Chem. 1986 Sep 25;261(27):12856–12864. [PubMed] [Google Scholar]
  2. Babior B. M. Oxygen-dependent microbial killing by phagocytes (first of two parts). N Engl J Med. 1978 Mar 23;298(12):659–668. doi: 10.1056/NEJM197803232981205. [DOI] [PubMed] [Google Scholar]
  3. Boucek M. M., Snyderman R. Calcium influx requirement for human neutrophil chemotaxis: inhibition by lanthanum chloride. Science. 1976 Sep 3;193(4256):905–907. doi: 10.1126/science.948752. [DOI] [PubMed] [Google Scholar]
  4. Cuatrecasas P., Hollenberg M. D. Membrane receptors and hormone action. Adv Protein Chem. 1976;30:251–451. doi: 10.1016/s0065-3233(08)60481-7. [DOI] [PubMed] [Google Scholar]
  5. Ferrante A., Thong Y. H. Optimal conditions for simultaneous purification of mononuclear and polymorphonuclear leucocytes from human blood by the Hypaque-Ficoll method. J Immunol Methods. 1980;36(2):109–117. doi: 10.1016/0022-1759(80)90036-8. [DOI] [PubMed] [Google Scholar]
  6. Hansen W. P., Hoffman R. A., Ip S. H., Healey K. W. Light scatter as an adjunct to cellular immunofluorescence in flow cytometric systems. J Clin Immunol. 1982 Jul;2(3 Suppl):32S–41S. [PubMed] [Google Scholar]
  7. Hazum E., Cuatrecasas P., Marian J., Conn P. M. Receptor-mediated internalization of fluorescent gonadotropin-releasing hormone by pituitary gonadotropes. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6692–6695. doi: 10.1073/pnas.77.11.6692. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hill H. R., Estensen R. D., Quie P. G., Hogan N. A., Goldberg N. D. Modulation of human neutrophil chemotactic responses by cyclic 3',5'-guanosine monophosphate and cyclic 3',5'-adenosine monophosphate. Metabolism. 1975 Mar;24(3):447–456. doi: 10.1016/0026-0495(75)90124-9. [DOI] [PubMed] [Google Scholar]
  9. Ichinose Y., Yagawa K., Kaku M., Hara N., Ohta M. Phorbol myristate acetate-induced modulation of antibody-dependent cellular cytotoxicity by human polymorphonuclear leukocytes. Infect Immun. 1984 Dec;46(3):682–685. doi: 10.1128/iai.46.3.682-685.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ishizaka K., Ishizaka T., Lee E. H. Biologic function of the Fc fragments of E myeloma protein. Immunochemistry. 1970 Aug;7(8):687–702. doi: 10.1016/0019-2791(70)90175-8. [DOI] [PubMed] [Google Scholar]
  11. Johnston R. B., Jr, Godzik C. A., Cohn Z. A. Increased superoxide anion production by immunologically activated and chemically elicited macrophages. J Exp Med. 1978 Jul 1;148(1):115–127. doi: 10.1084/jem.148.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kaku M., Yagawa K., Nagao S., Tanaka A. Enhanced superoxide anion release from phagocytes by muramyl dipeptide or lipopolysaccharide. Infect Immun. 1983 Feb;39(2):559–564. doi: 10.1128/iai.39.2.559-564.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Krebs E. G., Beavo J. A. Phosphorylation-dephosphorylation of enzymes. Annu Rev Biochem. 1979;48:923–959. doi: 10.1146/annurev.bi.48.070179.004423. [DOI] [PubMed] [Google Scholar]
  14. Köhler G., Milstein C. Continuous cultures of fused cells secreting antibody of predefined specificity. Nature. 1975 Aug 7;256(5517):495–497. doi: 10.1038/256495a0. [DOI] [PubMed] [Google Scholar]
  15. Lawson D., Fewtrell C., Gomperts B., Raff M. Anti-immunoglobulin-induced histamine secretion by rat peritoneal mast cells studied by immunoferritin electron microscopy. J Exp Med. 1975 Aug 1;142(2):391–402. doi: 10.1084/jem.142.2.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lehmeyer J. E., Johnston R. B., Jr Effect of anti-inflammatory drugs and agents that elevate intracellular cyclic AMP on the release of toxic oxygen metabolites by phagocytes: studies in a model of tissue-bound IgG. Clin Immunol Immunopathol. 1978 Apr;9(4):482–490. doi: 10.1016/0090-1229(78)90144-7. [DOI] [PubMed] [Google Scholar]
  17. Lehmeyer J. E., Snyderman R., Johnston R. B., Jr Stimulation of neutrophil oxidative metabolism by chemotactic peptides: influence of calcium ion concentration and cytochalasin B and comparison with stimulation by phorbol myristate acetate. Blood. 1979 Jul;54(1):35–45. [PubMed] [Google Scholar]
  18. Looney R. J., Abraham G. N., Anderson C. L. Human monocytes and U937 cells bear two distinct Fc receptors for IgG. J Immunol. 1986 Mar 1;136(5):1641–1647. [PubMed] [Google Scholar]
  19. NISONOFF A., WISSLER F. C., LIPMAN L. N., WOERNLEY D. L. Separation of univalent fragments from the bivalent rabbit antibody molecule by reduction of disulfide bonds. Arch Biochem Biophys. 1960 Aug;89:230–244. doi: 10.1016/0003-9861(60)90049-7. [DOI] [PubMed] [Google Scholar]
  20. Nathan C. F., Silverstein S. C., Brukner L. H., Cohn Z. A. Extracellular cytolysis by activated macrophages and granulocytes. II. Hydrogen peroxide as a mediator of cytotoxicity. J Exp Med. 1979 Jan 1;149(1):100–113. doi: 10.1084/jem.149.1.100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nishizuka Y. Studies and perspectives of protein kinase C. Science. 1986 Jul 18;233(4761):305–312. doi: 10.1126/science.3014651. [DOI] [PubMed] [Google Scholar]
  22. Rozengurt E. Early signals in the mitogenic response. Science. 1986 Oct 10;234(4773):161–166. doi: 10.1126/science.3018928. [DOI] [PubMed] [Google Scholar]
  23. Schlessinger J., Shechter Y., Willingham M. C., Pastan I. Direct visualization of binding, aggregation, and internalization of insulin and epidermal growth factor on living fibroblastic cells. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2659–2663. doi: 10.1073/pnas.75.6.2659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Simchowitz L., Spilberg I. Generation of superoxide radicals by human peripheral neutrophils activated by chemotactic factor. Evidence for the role of calcium. J Lab Clin Med. 1979 Apr;93(4):583–593. [PubMed] [Google Scholar]
  25. Smolen J. E., Korchak H. M., Weissmann G. The roles of extracellular and intracellular calcium in lysosomal enzyme release and superoxide anion generation by human neutrophils. Biochim Biophys Acta. 1981 Nov 5;677(3-4):512–520. doi: 10.1016/0304-4165(81)90267-1. [DOI] [PubMed] [Google Scholar]
  26. Starkebaum G., Stevens D. L., Henry C., Gavin S. E. Stimulation of human neutrophil chemiluminescence by soluble immune complexes and antibodies to neutrophils. J Lab Clin Med. 1981 Aug;98(2):280–291. [PubMed] [Google Scholar]
  27. Stephens C. G., Snyderman R. Cyclic nucleotides regulate the morphologic alterations required for chemotaxis in monocytes. J Immunol. 1982 Mar;128(3):1192–1197. [PubMed] [Google Scholar]
  28. Stossel T. P. Quantitative studies of phagocytosis. Kinetic effects of cations and heat-labile opsonin. J Cell Biol. 1973 Aug;58(2):346–356. doi: 10.1083/jcb.58.2.346. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Vaughn M., Taylor M., Mohanakumar T. Characterization of human IgG Fc receptors. J Immunol. 1985 Dec;135(6):4059–4065. [PubMed] [Google Scholar]
  30. Willis H. E., Browder B., Feister A. J., Mohanakumar T., Ruddy S. Monoclonal antibody to human IgG Fc receptors. Cross-linking of receptors induces lysosomal enzyme release and superoxide generation by neutrophils. J Immunol. 1988 Jan 1;140(1):234–239. [PubMed] [Google Scholar]
  31. Wolfson M., McPhail L. C., Nasrallah V. N., Snyderman R. Phorbol myristate acetate mediates redistribution of protein kinase C in human neutrophils: potential role in the activation of the respiratory burst enzyme. J Immunol. 1985 Sep;135(3):2057–2062. [PubMed] [Google Scholar]
  32. Yagawa K., Onoue K., Aida Y. Structural studies of Fc receptors. I. Binding properties, solubilization, and partial characterization of fc receptors of macrophages. J Immunol. 1979 Jan;122(1):366–373. [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES