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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1988 Apr;85(8):2504–2508. doi: 10.1073/pnas.85.8.2504

Effect of cholera toxin on histamine release from bone marrow-derived mouse mast cells.

H Saito 1, F Okajima 1, T F Molski 1, R I Sha'afi 1, M Ui 1, T Ishizaka 1
PMCID: PMC280025  PMID: 2451825

Abstract

Bone marrow-derived mouse mast cells were sensitized with monoclonal mouse IgE antibody and treated with cholera toxin (CT), which ADP-ribosylated the alpha-subunit of the stimulatory guanine nucleotide-binding regulatory protein Gs, prior to challenge with either antigen or thrombin. The CT treatment increased intracellular cAMP levels, but neither enhanced nor inhibited antigen-induced histamine release or arachidonate release. The same treatment of the sensitized bone marrow-derived mouse mast cells with CT markedly enhanced thrombin-induced histamine release without affecting arachidonate release. The CT treatment failed to affect antigen-induced and thrombin-induced generation of inositol trisphosphate and of diacylglycerol or mobilization of intracellular Ca2+. The results indicate that Gs in bone marrow-derived mouse mast cells is not involved in the transduction of the antigen-induced or thrombin-induced triggering signal to phospholipase C, which initiates the enhancement of phosphatidylinositol turnover. The enhancement of thrombin-induced histamine release by CT treatment with the observations that thrombin-induced histamine release was inhibited by pretreatment of the cells with pertussis toxin suggest that the involvement of a guanine nucleotide-binding regulatory protein in thrombin-induced biochemical events is an event distal to Ca2+ mobilization.

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Selected References

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  1. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  2. Beaven M. A., Moore J. P., Smith G. A., Hesketh T. R., Metcalfe J. C. The calcium signal and phosphatidylinositol breakdown in 2H3 cells. J Biol Chem. 1984 Jun 10;259(11):7137–7142. [PubMed] [Google Scholar]
  3. Beaven M. A., Rogers J., Moore J. P., Hesketh T. R., Smith G. A., Metcalfe J. C. The mechanism of the calcium signal and correlation with histamine release in 2H3 cells. J Biol Chem. 1984 Jun 10;259(11):7129–7136. [PubMed] [Google Scholar]
  4. Berridge M. J., Dawson R. M., Downes C. P., Heslop J. P., Irvine R. F. Changes in the levels of inositol phosphates after agonist-dependent hydrolysis of membrane phosphoinositides. Biochem J. 1983 May 15;212(2):473–482. doi: 10.1042/bj2120473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bokoch G. M., Katada T., Northup J. K., Hewlett E. L., Gilman A. G. Identification of the predominant substrate for ADP-ribosylation by islet activating protein. J Biol Chem. 1983 Feb 25;258(4):2072–2075. [PubMed] [Google Scholar]
  6. Cassel D., Pfeuffer T. Mechanism of cholera toxin action: covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2669–2673. doi: 10.1073/pnas.75.6.2669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fernandez J. M., Neher E., Gomperts B. D. Capacitance measurements reveal stepwise fusion events in degranulating mast cells. 1984 Nov 29-Dec 5Nature. 312(5993):453–455. doi: 10.1038/312453a0. [DOI] [PubMed] [Google Scholar]
  8. Garcia-Gil M., Siraganian R. P. Phospholipase A2 stimulation during cell secretion in rat basophilic leukemia cells. J Immunol. 1986 Jan;136(1):259–263. [PubMed] [Google Scholar]
  9. Gill D. M., Meren R. ADP-ribosylation of membrane proteins catalyzed by cholera toxin: basis of the activation of adenylate cyclase. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3050–3054. doi: 10.1073/pnas.75.7.3050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gomperts B. D. Involvement of guanine nucleotide-binding protein in the gating of Ca2+ by receptors. Nature. 1983 Nov 3;306(5938):64–66. doi: 10.1038/306064a0. [DOI] [PubMed] [Google Scholar]
  11. Imboden J. B., Shoback D. M., Pattison G., Stobo J. D. Cholera toxin inhibits the T-cell antigen receptor-mediated increases in inositol trisphosphate and cytoplasmic free calcium. Proc Natl Acad Sci U S A. 1986 Aug;83(15):5673–5677. doi: 10.1073/pnas.83.15.5673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ishizaka T., Hirata F., Sterk A. R., Ishizaka K., Axelrod J. A. Bridging of IgE receptors activates phospholipid methylation and adenylate cyclase in mast cell plasma membranes. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6812–6816. doi: 10.1073/pnas.78.11.6812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ishizaka T., Ishizaka K. Activation of mast cells for mediator release through IgE receptors. Prog Allergy. 1984;34:188–235. [PubMed] [Google Scholar]
  14. Ishizaka T., König W., Kurata M., Mauser L., Ishizaka K. Immunologic properties of mast cells from rats infected with Nippostrongylus brasiliensis. J Immunol. 1975 Oct;115(4):1078–1083. [PubMed] [Google Scholar]
  15. Ishizaka T. The Robert A. Cooke memorial lecture. Analysis of triggering events in mast cells for immunoglobulin E-mediated histamine release. J Allergy Clin Immunol. 1981 Feb;67(2):90–96. doi: 10.1016/0091-6749(81)90002-6. [DOI] [PubMed] [Google Scholar]
  16. Katada T., Ui M. ADP ribosylation of the specific membrane protein of C6 cells by islet-activating protein associated with modification of adenylate cyclase activity. J Biol Chem. 1982 Jun 25;257(12):7210–7216. [PubMed] [Google Scholar]
  17. Katada T., Ui M. Direct modification of the membrane adenylate cyclase system by islet-activating protein due to ADP-ribosylation of a membrane protein. Proc Natl Acad Sci U S A. 1982 May;79(10):3129–3133. doi: 10.1073/pnas.79.10.3129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lichtenstein L. M., Henney C. S., Bourne H. R., Greenough W. B., 3rd Effects of cholera toxin on in vitro models of immediate and delayed hypersensitivity. Further evidence for the role of cyclic adenosine 3',5'-monophosphate. J Clin Invest. 1973 Mar;52(3):691–697. doi: 10.1172/JCI107230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lichtenstein L. M., Margolis S. Histamine release in vitro: inhibition by catecholamines and methylxanthines. Science. 1968 Aug 30;161(3844):902–903. doi: 10.1126/science.161.3844.902. [DOI] [PubMed] [Google Scholar]
  20. Molski T. F., Naccache P. H., Marsh M. L., Kermode J., Becker E. L., Sha'afi R. I. Pertussis toxin inhibits the rise in the intracellular concentration of free calcium that is induced by chemotactic factors in rabbit neutrophils: possible role of the "G proteins" in calcium mobilization. Biochem Biophys Res Commun. 1984 Oct 30;124(2):644–650. doi: 10.1016/0006-291x(84)91603-6. [DOI] [PubMed] [Google Scholar]
  21. Musch M. W., Siegel M. I. Antigenic stimulated release of arachidonic acid, lipoxygenase activity and histamine release in a cloned murine mast cell MC9. Biochem Biophys Res Commun. 1985 Jan 16;126(1):517–525. doi: 10.1016/0006-291x(85)90636-9. [DOI] [PubMed] [Google Scholar]
  22. Nitta T., Suzuki T. Fc gamma 2b receptor-mediated prostaglandin synthesis by a murine macrophage cell line (P388D1). J Immunol. 1982 Jun;128(6):2527–2532. [PubMed] [Google Scholar]
  23. Ogawa M., Nakahata T., Leary A. G., Sterk A. R., Ishizaka K., Ishizaka T. Suspension culture of human mast cells/basophils from umbilical cord blood mononuclear cells. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4494–4498. doi: 10.1073/pnas.80.14.4494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pozzan T., Arslan P., Tsien R. Y., Rink T. J. Anti-immunoglobulin, cytoplasmic free calcium, and capping in B lymphocytes. J Cell Biol. 1982 Aug;94(2):335–340. doi: 10.1083/jcb.94.2.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Saito H., Okajima F., Molski T. F., Sha'afi R. I., Ui M., Ishizaka T. Effects of ADP-ribosylation of GTP-binding protein by pertussis toxin on immunoglobulin E-dependent and -independent histamine release from mast cells and basophils. J Immunol. 1987 Jun 1;138(11):3927–3934. [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. White J. R., Ishizaka T., Ishizaka K., Sha'afi R. Direct demonstration of increased intracellular concentration of free calcium as measured by quin-2 in stimulated rat peritoneal mast cell. Proc Natl Acad Sci U S A. 1984 Jul;81(13):3978–3982. doi: 10.1073/pnas.81.13.3978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. van Heyningen S. Cholera toxin. Biol Rev Camb Philos Soc. 1977 Nov;52(4):509–509. doi: 10.1111/j.1469-185x.1977.tb00858.x. [DOI] [PubMed] [Google Scholar]

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