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. 1983 Jun 1;157(6):1981–1991. doi: 10.1084/jem.157.6.1981

Activation of basophil and mast cell histamine release by eosinophil granule major basic protein

PMCID: PMC2187055  PMID: 6854212

Abstract

Major basic protein (MBP) is a primary constituent of eosinophil granules. In this report, we demonstrate that MBP from human eosinophil granules initiates a nonlytic histamine release from human leukocytes. A direct effect of MBP on basophils was confirmed using purified human basophils. The kinetics of release were similar to those reported for poly-L-arginine, although MBP was less potent than poly-L-arginine of similar molecular weight. Reduction and alkylation of MBP diminished both the potency and efficacy of the molecule. Native MBP also stimulated histamine secretion from purified rat peritoneal mast cells in a manner characteristic of other polycations. These results emphasize the bidirectional nature of the basophil/mast cell-eosinophil regulatory axis.

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Selected References

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  1. Ackerman S. J., Weil G. J., Gleich G. J. Formation of Charcot-Leyden crystals by human basophils. J Exp Med. 1982 Jun 1;155(6):1597–1609. doi: 10.1084/jem.155.6.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anwar A. R., McKean J. R., Smithers S. R., Kay A. B. Human eosinophil- and neutrophil-mediated killing of schistosomula of Schistosoma mansoni in vitro. I. Enhancement of complement-dependent damage by mast cell-derived mediators and formyl methionyl peptides. J Immunol. 1980 Mar;124(3):1122–1129. [PubMed] [Google Scholar]
  3. Austen K. F. Homeostasis of effector systems which can also be recruited for immunologic reactions. J Immunol. 1978 Sep;121(3):793–805. [PubMed] [Google Scholar]
  4. Bloom G. D., Fredholm B., Haegermark O. Studies on the time course of histamine release and morphological changes induced by histamine liberators in rat peritoneal mast cells. Acta Physiol Scand. 1967 Dec;71(4):270–282. doi: 10.1111/j.1748-1716.1967.tb03734.x. [DOI] [PubMed] [Google Scholar]
  5. Brown S. J., Galli S. J., Gleich G. J., Askenase P. W. Ablation of immunity to Amblyomma americanum by anti-basophil serum: cooperation between basophils and eosinophils in expression of immunity to ectoparasites (ticks) in guinea pigs. J Immunol. 1982 Aug;129(2):790–796. [PubMed] [Google Scholar]
  6. Butterworth A. E., Sturrock R. F., Houba V., Mahmoud A. A., Sher A., Rees P. H. Eosinophils as mediators of antibody-dependent damage to schistosomula. Nature. 1975 Aug 28;256(5520):727–729. doi: 10.1038/256727a0. [DOI] [PubMed] [Google Scholar]
  7. Butterworth A. E., Wassom D. L., Gleich G. J., Loegering D. A., David J. R. Damage to schistosomula of Schistosoma mansoni induced directly by eosinophil major basic protein. J Immunol. 1979 Jan;122(1):221–229. [PubMed] [Google Scholar]
  8. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl. 1968;97:77–89. [PubMed] [Google Scholar]
  9. Church M. K., Pao G. J., Holgate S. T. Characterization of histamine secretion from mechanically dispersed human lung mast cells: effects of anti-IgE, calcium ionophore A23187, compound 48/80, and basic polypeptides. J Immunol. 1982 Nov;129(5):2116–2121. [PubMed] [Google Scholar]
  10. Douglas W. W. Stimulus-secretion coupling: variations on the theme of calcium-activated exocytosis involving cellular and extracellular sources of calcium. Ciba Found Symp. 1978;(54):61–90. doi: 10.1002/9780470720356.ch4. [DOI] [PubMed] [Google Scholar]
  11. Dvorak A. M., Mihm M. C., Jr, Osage J. E., Kwan T. H., Austen K. F., Wintroub B. U. Bullous pemphigoid, an ultrastructural study of the inflammatory response: eosinophil, basophil and mast cell granule changes in multiple biopsies from one patient. J Invest Dermatol. 1982 Feb;78(2):91–101. doi: 10.1111/1523-1747.ep12505711. [DOI] [PubMed] [Google Scholar]
  12. Filley W. V., Holley K. E., Kephart G. M., Gleich G. J. Identification by immunofluorescence of eosinophil granule major basic protein in lung tissues of patients with bronchial asthma. Lancet. 1982 Jul 3;2(8288):11–16. doi: 10.1016/s0140-6736(82)91152-7. [DOI] [PubMed] [Google Scholar]
  13. Foreman J. C., Lichtenstein L. M. Induction of histamine secretion by polycations. Biochim Biophys Acta. 1980 May 22;629(3):587–603. doi: 10.1016/0304-4165(80)90164-6. [DOI] [PubMed] [Google Scholar]
  14. Frigas E., Loegering D. A., Solley G. O., Farrow G. M., Gleich G. J. Elevated levels of the eosinophil granule major basic protein in the sputum of patients with bronchial asthma. Mayo Clin Proc. 1981 Jun;56(6):345–353. [PubMed] [Google Scholar]
  15. Gilbert H. S., Ornstein L. Basophil counting with a new staining method using alcian blue. Blood. 1975 Aug;46(2):279–286. [PubMed] [Google Scholar]
  16. Gleich G. J., Frigas E., Loegering D. A., Wassom D. L., Steinmuller D. Cytotoxic properties of the eosinophil major basic protein. J Immunol. 1979 Dec;123(6):2925–2927. [PubMed] [Google Scholar]
  17. Gleich G. J., Loegering D. A., Kueppers F., Bajaj S. P., Mann K. G. Physiochemical and biological properties of the major basic protein from guinea pig eosinophil granules. J Exp Med. 1974 Aug 1;140(2):313–332. doi: 10.1084/jem.140.2.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gleich G. J., Loegering D. A., Maldonado J. E. Identification of a major basic protein in guinea pig eosinophil granules. J Exp Med. 1973 Jun 1;137(6):1459–1471. doi: 10.1084/jem.137.6.1459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gleich G. J., Loegering D. A., Mann K. G., Maldonado J. E. Comparative properties of the Charcot-Leyden crystal protein and the major basic protein from human eosinophils. J Clin Invest. 1976 Mar;57(3):633–640. doi: 10.1172/JCI108319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Goetzl E. J., Austen K. F. Purification and synthesis of eosinophilotactic tetrapeptides of human lung tissue: identification as eosinophil chemotactic factor of anaphylaxis. Proc Natl Acad Sci U S A. 1975 Oct;72(10):4123–4127. doi: 10.1073/pnas.72.10.4123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Goth A., Adams H. R., Knoohuizen M. Phosphatidylserine: selective enhancer of histamine release. Science. 1971 Sep 10;173(4001):1034–1035. doi: 10.1126/science.173.4001.1034. [DOI] [PubMed] [Google Scholar]
  22. Henderson W. R., Chi E. Y., Jong E. C., Klebanoff S. J. Mast cell-mediated tumor-cell cytotoxicity. Role of the peroxidase system. J Exp Med. 1981 Mar 1;153(3):520–533. doi: 10.1084/jem.153.3.520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Henderson W. R., Chi E. Y., Klebanoff S. J. Eosinophil peroxidase-induced mast cell secretion. J Exp Med. 1980 Aug 1;152(2):265–279. doi: 10.1084/jem.152.2.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Johnson A. R., Erdös E. G. Release of histamine from mast cells by vasoactive peptides. Proc Soc Exp Biol Med. 1973 Apr;142(4):1252–1256. doi: 10.3181/00379727-142-37219. [DOI] [PubMed] [Google Scholar]
  25. Jong E. C., Henderson W. R., Klebanoff S. J. Bactericidal activity of eosinophil peroxidase. J Immunol. 1980 Mar;124(3):1378–1382. [PubMed] [Google Scholar]
  26. Jong E. C., Klebanoff S. J. Eosinophil-mediated mammalian tumor cell cytotoxicity: role of the peroxidase system. J Immunol. 1980 Apr;124(4):1949–1953. [PubMed] [Google Scholar]
  27. Kay A. B., Stechschulte D. J., Austen K. F. An eosinophil leukocyte chemotactic factor of anaphylaxis. J Exp Med. 1971 Mar 1;133(3):602–619. doi: 10.1084/jem.133.3.602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. LICHTENSTEIN L. M., OSLER A. G. STUDIES ON THE MECHANISMS OF HYPERSENSITIVITY PHENOMENA. IX. HISTAMINE RELEASE FROM HUMAN LEUKOCYTES BY RAGWEED POLLEN ANTIGEN. J Exp Med. 1964 Oct 1;120:507–530. doi: 10.1084/jem.120.4.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lewis D. M., Lewis J. C., Loegering D. A., Gleich G. J. Localization of the guinea pig eosinophil major basic protein to the core of the granule. J Cell Biol. 1978 Jun;77(3):702–713. doi: 10.1083/jcb.77.3.702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lewis R. A., Goetzl E. J., Wasserman S. I., Valone F. H., Rubin R. H., Austen K. F. The release of four mediators of immediate hypersensitivity from human leukemic basophils. J Immunol. 1975 Jan;114(1 Pt 1):87–92. [PubMed] [Google Scholar]
  31. Lichtenstein L. M. The immediate allergic response: in vitro separation of antigen activation, decay and histamine release. J Immunol. 1971 Oct;107(4):1122–1130. [PubMed] [Google Scholar]
  32. Mickenberg I. D., Root R. K., Wolff S. M. Bactericidal and metabolic properties of human eosinophils. Blood. 1972 Jan;39(1):67–80. [PubMed] [Google Scholar]
  33. Siraganian R. P. An automated continuous-flow system for the extraction and fluorometric analysis of histamine. Anal Biochem. 1974 Feb;57(2):383–394. doi: 10.1016/0003-2697(74)90093-1. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Wassom D. L., Gleich G. J. Damage to Trichinella spiralis newborn larvae by eosinophil major basic protein. Am J Trop Med Hyg. 1979 Sep;28(5):860–863. [PubMed] [Google Scholar]
  36. Wassom D. L., Loegering D. A., Solley G. O., Moore S. B., Schooley R. T., Fauci A. S., Gleich G. J. Elevated serum levels of the eosinophil granule major basic protein in patients with eosinophilia. J Clin Invest. 1981 Mar;67(3):651–661. doi: 10.1172/JCI110080. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Weller P. F., Goetzl E. J. The regulatory and effector roles of eosinophils. Adv Immunol. 1979;27:339–371. doi: 10.1016/s0065-2776(08)60264-3. [DOI] [PubMed] [Google Scholar]
  38. Yam L. T., Li C. Y., Crosby W. H. Cytochemical identification of monocytes and granulocytes. Am J Clin Pathol. 1971 Mar;55(3):283–290. doi: 10.1093/ajcp/55.3.283. [DOI] [PubMed] [Google Scholar]
  39. Zeiger R. S., Colten H. R. Histaminase release from human eosinophils. J Immunol. 1977 Feb;118(2):540–543. [PubMed] [Google Scholar]

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