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. 1972 Nov 30;136(6):1356–1377. doi: 10.1084/jem.136.6.1356

LEUKOCYTE-DEPENDENT HISTAMINE RELEASE FROM RABBIT PLATELETS

THE ROLE OF IGE, BASOPHILS, AND A PLATELET-ACTIVATING FACTOR

Jacques Benveniste 1, Peter M Henson 1, Charles G Cochrane 1
PMCID: PMC2139324  PMID: 4118412

Abstract

We have studied the leukocyte-dependent mechanism of histamine release (LDHR) from rabbit platelets, a complement-independent mechanism which has been implicated in the deposition of immune complexes in acute serum sickness of rabbits. It was found by chromatography and passive transfer of serum from immunized rabbits that the antibody responsible for the LDHR was of IgE type. By electron microscope study of the reaction, the leukocyte involved in agglutination of platelets and release of their histamine content was identified as the basophil. Upon addition of antigen, basophils sensitized with IgE degranulated, released their histamine content and a platelet-activating factor (PAF) that caused aggregation of platelets and release of their histamine. Conditions of preparing and preserving PAF activity and some properties of this factor have been elucidated. LDHR must, therefore, be considered as an immediate hypersensitivity-type mechanism which may link allergic reactions with immunologic disease associated with severe structural injury.

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Selected References

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  1. ALKSNE J. F. The passage of colloidal particles across the dermal capillary wall under the influence of histamine. Q J Exp Physiol Cogn Med Sci. 1959 Jan;44(1):51–66. doi: 10.1113/expphysiol.1959.sp001376. [DOI] [PubMed] [Google Scholar]
  2. ASTER R. H., JANDL J. H. PLATELET SEQUESTRATION IN MAN. I. METHODS. J Clin Invest. 1964 May;43:843–855. doi: 10.1172/JCI104970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aikawa M., Schoenbechler M. J., Barbaro J. F., Sadun E. H. Interaction of rabbit platelets and leukocytes in the release of histamine. Electron microscopic observations. Am J Pathol. 1971 Apr;63(1):85–98. [PMC free article] [PubMed] [Google Scholar]
  4. BENACERRAF B., McCLUSKEY R. T., PATRAS D. Localization of colloidal substances in vascular endothelium: a mechanism of tissue damage. I. Factors causing the pathologic deposition of colloidal carbon. Am J Pathol. 1959 Jan-Feb;35(1):75–91. [PMC free article] [PubMed] [Google Scholar]
  5. Barbaro J. F., Schoenbechler M. J. The nature of the reaction of antigen with lymphocytes from rabbits infected with Schistosoma mansoni on the release of histamine from rabbit platelets. J Immunol. 1970 May;104(5):1124–1131. [PubMed] [Google Scholar]
  6. Barbaro J. F., Zvaifler N. J. Antigen induced histamine release from platelets of rabbits producing homologous PCA antibody. Proc Soc Exp Biol Med. 1966 Aug-Sep;122(4):1245–1247. doi: 10.3181/00379727-122-31371. [DOI] [PubMed] [Google Scholar]
  7. COCHRANE C. G. STUDIES ON THE LOCALIZATION OF CIRCULATING ANTIGEN-ANTIBODY COMPLEXES AND OTHER MACROMOLECULES IN VESSELS. I. STRUCTURAL STUDIES. J Exp Med. 1963 Oct 1;118:489–502. doi: 10.1084/jem.118.4.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. COCHRANE C. G. STUDIES ON THE LOCALIZATION OF CIRCULATING ANTIGEN-ANTIBODY COMPLEXES AND OTHER MACROMOLECULES IN VESSELS. II. PATHOGENETIC AND PHARMACODYNAMIC STUDIES. J Exp Med. 1963 Oct 1;118:503–513. doi: 10.1084/jem.118.4.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cochrane C. G., Hawkins D. Studies on circulating immune complexes. 3. Factors governing the ability of circulating complexes to localize in blood vessels. J Exp Med. 1968 Jan 1;127(1):137–154. doi: 10.1084/jem.127.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Colwell E. J., Ortaldo J. R., Schoenbechler M. J., Barbaro J. F. In vivo passive sensitization of normal rabbit leukocytes with sera demonstrating homocytotropic antibody activity. Int Arch Allergy Appl Immunol. 1971;41(5):754–764. doi: 10.1159/000230566. [DOI] [PubMed] [Google Scholar]
  11. FALLON H. J., FREI E., 3rd, DAVIDSON J. D., TRIER J. S., BURK D. Leukocyte preparations from human blood: evaluation of their morphologic and metabolic state. J Lab Clin Med. 1962 May;59:779–791. [PubMed] [Google Scholar]
  12. Graham R. C., Jr, Karnovsky M. J. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem. 1966 Apr;14(4):291–302. doi: 10.1177/14.4.291. [DOI] [PubMed] [Google Scholar]
  13. Henson P. M., Cochrane C. G. Acute immune complex disease in rabbits. The role of complement and of a leukocyte-dependent release of vasoactive amines from platelets. J Exp Med. 1971 Mar 1;133(3):554–571. doi: 10.1084/jem.133.3.554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Henson P. M., Cochrane C. G. Immunological induction of increased vascular permeability. II. Two mechanisms of histamine release from rabbit platelets involving complement. J Exp Med. 1969 Jan 1;129(1):167–184. doi: 10.1084/jem.129.1.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Henson P. M. Mechanisms of release of constituents from rabbit platelets by antigen-antibody complexes and complement. II. Interaction of platelets with neutrophils. J Immunol. 1970 Aug;105(2):490–501. [PubMed] [Google Scholar]
  16. Henson P. M. Release of vasoactive amines from rabbit platelets induced by sensitized mononuclear leukocytes and antigen. J Exp Med. 1970 Feb;131(2):287–306. doi: 10.1084/jem.131.2.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ishizaka K., Ishizaka T. Mechanisms of reaginic hypersensitivity: a review. Clin Allergy. 1971 Mar;1(1):9–24. doi: 10.1111/j.1365-2222.1971.tb02444.x. [DOI] [PubMed] [Google Scholar]
  18. Ishizaka K., Tomioka H., Ishizaka T. Mechanisms of passive sensitization. I. Presence of IgE and IgG molecules on human leukocytes. J Immunol. 1970 Dec;105(6):1459–1467. [PubMed] [Google Scholar]
  19. Kniker W. T., Cochrane C. G. The localization of circulating immune complexes in experimental serum sickness. The role of vasoactive amines and hydrodynamic forces. J Exp Med. 1968 Jan 1;127(1):119–136. doi: 10.1084/jem.127.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. MAJNO G., PALADE G. E. Studies on inflammation. 1. The effect of histamine and serotonin on vascular permeability: an electron microscopic study. J Biophys Biochem Cytol. 1961 Dec;11:571–605. doi: 10.1083/jcb.11.3.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. OVARY Z. Immediate reactions in the skin of experimental animals provoked by antibody-antigen interaction. Prog Allergy. 1958;5:459–508. [PubMed] [Google Scholar]
  22. Orange R. P., Austen K. F. Slow reacting substance of anaphylaxis. Adv Immunol. 1969;10:105–144. doi: 10.1016/s0065-2776(08)60416-2. [DOI] [PubMed] [Google Scholar]
  23. RHYNE M. B., GERMUTH F. G., Jr The relationships between serum complement activity and the development of allergic lesions in rabbits. J Exp Med. 1961 Nov 1;114:633–646. doi: 10.1084/jem.114.5.633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. STRAUS W. Colorimetric investigation of the uptake of an intravenously injected protein (horseradish peroxidase) by rat kidney and effects of competition by egg white. J Cell Biol. 1962 Feb;12:231–246. doi: 10.1083/jcb.12.2.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schoenbechler M. J., Sadun E. H. In vitro histamine release from blood cellular elements of rabbits infected with Schistosoma mansoni. Proc Soc Exp Biol Med. 1968 Feb;127(2):601–606. doi: 10.3181/00379727-127-32752. [DOI] [PubMed] [Google Scholar]
  26. Siraganian R. P., Osler A. G. Destruction of rabbit platelets in the allergic response of sensitized leukocytes. I. Demonstration of a fluid phase intermediate. J Immunol. 1971 May;106(5):1244–1251. [PubMed] [Google Scholar]
  27. Siraganian R. P., Osler A. G. Destruction of rabbit platelets in the allergic response of sensitized leukocytes. II. Evidence for basophil involvement. J Immunol. 1971 May;106(5):1252–1259. [PubMed] [Google Scholar]
  28. Zvaifler N. J., Becker E. L. Rabbit anaphylactic antibody. J Exp Med. 1966 May 1;123(5):935–950. doi: 10.1084/jem.123.5.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Zvaifler N. J., Robinson J. O. Rabbit homocytotropic antibody. A unique rabbit immunoglobulin analogous to human IgE. J Exp Med. 1969 Oct 1;130(4):907–929. doi: 10.1084/jem.130.4.907. [DOI] [PMC free article] [PubMed] [Google Scholar]

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