Abstract
Histamine release induced by the introduction of a nonhydrolyzable analogue of GTP, GTP-gamma-S, into ATP-permeabilized mast cells, is associated with phosphoinositide breakdown, as evidenced by the production of phosphatidic acid (PA) in a neomycin-sensitive process. The dependency of both PA formation and histamine secretion on GTP- gamma-S concentrations is bell shaped. Whereas concentrations of up to 0.1 mM GTP-gamma-S stimulate both processes, at higher concentrations the cells' responsiveness is inhibited. At a concentration of 1 mM, GTP- gamma-S self-inhibits both PA formation and histamine secretion. Inhibition of secretion can, however, be overcome by the basic secretagogues compound 48/80 and mastoparan that in suboptimal doses synergize with 1 mM GTP-gamma-S to potentiate secretion. Secretion under these conditions is not accompanied by PA formation and is resistant both to depletion of Ca2+ from internal stores and to pertussis toxin (PtX) treatment. In addition, 48/80, like mastoparan, is capable of directly stimulating the GTPase activity of G-proteins in a cell-free system. Together, our results are consistent with a model in which the continuous activation of a phosphoinositide-hydrolyzing phospholipase C (PLC) by a stimulatory G-protein suffices to trigger histamine secretion. Basic secretagogues of mast cells, such as compound 48/80 and mastoparan, are capable of inducing secretion in a mechanism that bypasses PLC by directly activating a G-protein that is presumably located downstream from PLC (GE). Thereby, these secretagogues induce histamine secretion in a receptor-independent manner.
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- Barrowman M. M., Cockcroft S., Gomperts B. D. Two roles for guanine nucleotides in the stimulus-secretion sequence of neutrophils. Nature. 1986 Feb 6;319(6053):504–507. doi: 10.1038/319504a0. [DOI] [PubMed] [Google Scholar]
- Bocckino S. B., Blackmore P. F., Wilson P. B., Exton J. H. Phosphatidate accumulation in hormone-treated hepatocytes via a phospholipase D mechanism. J Biol Chem. 1987 Nov 5;262(31):15309–15315. [PubMed] [Google Scholar]
- Cockcroft S. Ca2+-dependent conversion of phosphatidylinositol to phosphatidate in neutrophils stimulated with fMet-Leu-Phe or ionophore A23187. Biochim Biophys Acta. 1984 Aug 15;795(1):37–46. doi: 10.1016/0005-2760(84)90102-4. [DOI] [PubMed] [Google Scholar]
- Cockcroft S., Gomperts B. D. Evidence for a role of phosphatidylinositol turnover in stimulus-secretion coupling. Studies with rat peritoneal mast cells. Biochem J. 1979 Mar 15;178(3):681–687. doi: 10.1042/bj1780681. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cockcroft S., Gomperts B. D. Role of guanine nucleotide binding protein in the activation of polyphosphoinositide phosphodiesterase. Nature. 1985 Apr 11;314(6011):534–536. doi: 10.1038/314534a0. [DOI] [PubMed] [Google Scholar]
- Ennis M., Truneh A., White J. R., Pearce F. L. Calcium pools involved in histamine release from rat mast cells. Int Arch Allergy Appl Immunol. 1980;62(4):467–471. doi: 10.1159/000232551. [DOI] [PubMed] [Google Scholar]
- Fernandez J. M., Lindau M., Eckstein F. Intracellular stimulation of mast cells with guanine nucleotides mimic antigenic stimulation. FEBS Lett. 1987 May 25;216(1):89–93. doi: 10.1016/0014-5793(87)80762-7. [DOI] [PubMed] [Google Scholar]
- 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]
- Foreman J. C., Mongar J. L. The role of the alkaline earth ions in anaphylactic histamine secretion. J Physiol. 1972 Aug;224(3):753–769. doi: 10.1113/jphysiol.1972.sp009921. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilman A. G. G proteins: transducers of receptor-generated signals. Annu Rev Biochem. 1987;56:615–649. doi: 10.1146/annurev.bi.56.070187.003151. [DOI] [PubMed] [Google Scholar]
- 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]
- Herrmann E., Jakobs K. H. Stimulation and inhibition of human platelet membrane high-affinity GTPase by neomycin. FEBS Lett. 1988 Feb 29;229(1):49–53. doi: 10.1016/0014-5793(88)80795-6. [DOI] [PubMed] [Google Scholar]
- Higashijima T., Uzu S., Nakajima T., Ross E. M. Mastoparan, a peptide toxin from wasp venom, mimics receptors by activating GTP-binding regulatory proteins (G proteins). J Biol Chem. 1988 May 15;263(14):6491–6494. [PubMed] [Google Scholar]
- Howell T. W., Cockcroft S., Gomperts B. D. Essential synergy between Ca2+ and guanine nucleotides in exocytotic secretion from permeabilized rat mast cells. J Cell Biol. 1987 Jul;105(1):191–197. doi: 10.1083/jcb.105.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huff R. M., Neer E. J. Subunit interactions of native and ADP-ribosylated alpha 39 and alpha 41, two guanine nucleotide-binding proteins from bovine cerebral cortex. J Biol Chem. 1986 Jan 25;261(3):1105–1110. [PubMed] [Google Scholar]
- Katada T., Oinuma M., Ui M. Two guanine nucleotide-binding proteins in rat brain serving as the specific substrate of islet-activating protein, pertussis toxin. Interaction of the alpha-subunits with beta gamma-subunits in development of their biological activities. J Biol Chem. 1986 Jun 25;261(18):8182–8191. [PubMed] [Google Scholar]
- Katakami Y., Kaibuchi K., Sawamura M., Takai Y., Nishizuka Y. Synergistic action of protein kinase C and calcium for histamine release from rat peritoneal mast cells. Biochem Biophys Res Commun. 1984 Jun 15;121(2):573–578. doi: 10.1016/0006-291x(84)90220-1. [DOI] [PubMed] [Google Scholar]
- Lagunoff D., Martin T. W., Read G. Agents that release histamine from mast cells. Annu Rev Pharmacol Toxicol. 1983;23:331–351. doi: 10.1146/annurev.pa.23.040183.001555. [DOI] [PubMed] [Google Scholar]
- Lawson D. Rat peritoneal mast cells: a model system for studying membrane fusion. Soc Gen Physiol Ser. 1980;34:27–44. [PubMed] [Google Scholar]
- Lindau M., Nüsse O. Pertussis toxin does not affect the time course of exocytosis in mast cells stimulated by intracellular application of GTP-gamma-S. FEBS Lett. 1987 Oct 5;222(2):317–321. doi: 10.1016/0014-5793(87)80393-9. [DOI] [PubMed] [Google Scholar]
- Nakamura T., Ui M. Islet-activating protein, pertussis toxin, inhibits Ca2+-induced and guanine nucleotide-dependent releases of histamine and arachidonic acid from rat mast cells. FEBS Lett. 1984 Aug 6;173(2):414–418. doi: 10.1016/0014-5793(84)80816-9. [DOI] [PubMed] [Google Scholar]
- Oberdisse E., Lapetina E. G. GDP beta S enhances the activation of phospholipase C caused by thrombin in human platelets: evidence for involvement of an inhibitory GTP-binding protein. Biochem Biophys Res Commun. 1987 May 14;144(3):1188–1196. doi: 10.1016/0006-291x(87)91437-9. [DOI] [PubMed] [Google Scholar]
- Okano Y., Takagi H., Tohmatsu T., Nakashima S., Kuroda Y., Saito K., Nozawa Y. A wasp venom mastoparan-induced polyphosphoinositide breakdown in rat peritoneal mast cells. FEBS Lett. 1985 Sep 2;188(2):363–366. doi: 10.1016/0014-5793(85)80403-8. [DOI] [PubMed] [Google Scholar]
- Ortner M. J., Chignell C. F. Spectroscopic studies of rat mast cells, mouse mastocytoma cells, and compound 48/80-II. The synthesis and some binding properties of spin-labeled 48/80. Biochem Pharmacol. 1981 Feb 15;30(4):283–288. doi: 10.1016/0006-2952(81)90055-1. [DOI] [PubMed] [Google Scholar]
- Penner R. Multiple signaling pathways control stimulus-secretion coupling in rat peritoneal mast cells. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9856–9860. doi: 10.1073/pnas.85.24.9856. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Penner R., Pusch M., Neher E. Washout phenomena in dialyzed mast cells allow discrimination of different steps in stimulus-secretion coupling. Biosci Rep. 1987 Apr;7(4):313–321. doi: 10.1007/BF01121453. [DOI] [PubMed] [Google Scholar]
- Rana R. S., Sekar M. C., Hokin L. E., MacDonald M. J. A possible role for glucose metabolites in the regulation of inositol-1,4,5-trisphosphate 5-phosphomonoesterase activity in pancreatic islets. J Biol Chem. 1986 Apr 25;261(12):5237–5240. [PubMed] [Google Scholar]
- Reimann E. M., Umfleet R. A. Selective precipitation of 32Pi onto filter papers. Application to ATPase and cyclic AMP phosphodiesterase determination. Biochim Biophys Acta. 1978 Apr 12;523(2):516–521. doi: 10.1016/0005-2744(78)90054-2. [DOI] [PubMed] [Google Scholar]
- Repke H., Bienert M. Mast cell activation--a receptor-independent mode of substance P action? FEBS Lett. 1987 Sep 14;221(2):236–240. doi: 10.1016/0014-5793(87)80932-8. [DOI] [PubMed] [Google Scholar]
- Repke H., Piotrowski W., Bienert M., Foreman J. C. Histamine release induced by Arg-Pro-Lys-Pro(CH2)11CH3 from rat peritoneal mast cells. J Pharmacol Exp Ther. 1987 Oct;243(1):317–321. [PubMed] [Google Scholar]
- Sagi-Eisenberg R., Ben-Neriah Z., Pecht I., Terry S., Blumberg S. Structure-activity relationship in the mast cell degranulating capacity of neurotensin fragments. Neuropharmacology. 1983 Feb;22(2):197–201. doi: 10.1016/0028-3908(83)90009-6. [DOI] [PubMed] [Google Scholar]
- Sagi-Eisenberg R., Foreman J. C., Raval P. J., Cockcroft S. Protein and diacylglycerol phosphorylation in the stimulus-secretion coupling of rat mast cells. Immunology. 1987 Jun;61(2):203–206. [PMC free article] [PubMed] [Google Scholar]
- Sagi-Eisenberg R., Foreman J. C., Shelly R. Histamine release induced by histone and phorbol ester from rat peritoneal mast cells. Eur J Pharmacol. 1985 Jul 11;113(1):11–17. doi: 10.1016/0014-2999(85)90337-1. [DOI] [PubMed] [Google Scholar]
- Sagi-Eisenberg R., Lieman H., Pecht I. Protein kinase C regulation of the receptor-coupled calcium signal in histamine-secreting rat basophilic leukaemia cells. Nature. 1985 Jan 3;313(5997):59–60. doi: 10.1038/313059a0. [DOI] [PubMed] [Google Scholar]
- Sagi-Eisenberg R., Pecht I. Protein kinase C, a coupling element between stimulus and secretion of basophils. Immunol Lett. 1984;8(5):237–241. doi: 10.1016/0165-2478(84)90002-6. [DOI] [PubMed] [Google Scholar]
- 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]
- Segal D. M., Taurog J. D., Metzger H. Dimeric immunoglobulin E serves as a unit signal for mast cell degranulation. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2993–2997. doi: 10.1073/pnas.74.7.2993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Watson S. P., McConnell R. T., Lapetina E. G. The rapid formation of inositol phosphates in human platelets by thrombin is inhibited by prostacyclin. J Biol Chem. 1984 Nov 10;259(21):13199–13203. [PubMed] [Google Scholar]
- 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]