Abstract
Rat mast cells, pretreated with metabolic inhibitors and permeabilized by streptolysin-O, secrete histamine when provided with Ca2+ (buffered in the micromolar range) and nucleoside triphosphates. We have surveyed the ability of various exogenous nucleotides to support or inhibit secretion. The preferred rank order in support of secretion is ITP greater than XTP greater than GTP much greater than ATP. Pyrimidine nucleotides (UTP and CTP) are without effect. Nucleoside diphosphates included alongside Ca2+ plus ITP inhibit secretion in the order 2'- deoxyGDP greater than GDP greater than o-GDP greater than ADP approximately equal to 2'deoxyADP approximately equal to IDP. Secretion from the metabolically inhibited and permeabilized cells can also be induced by stable analogues of GTP (GTP-gamma-S greater than GppNHp greater than GppCH2p) which synergize with Ca2+ to trigger secretion in the absence of phosphorylating nucleotides. ATP enhances the effective affinity for Ca2+ and GTP analogues in the exocytotic process but does not alter the maximum extent of secretion. The results suggest that the presence of Ca2+ combined with activation of events controlled by a GTP regulatory protein provide a sufficient stimulus to exocytotic secretion from mast cells.
Full Text
The Full Text of this article is available as a PDF (751.0 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ahnert-Hilger G., Bhakdi S., Gratzl M. Minimal requirements for exocytosis. A study using PC 12 cells permeabilized with staphylococcal alpha-toxin. J Biol Chem. 1985 Oct 15;260(23):12730–12734. [PubMed] [Google Scholar]
- Akkerman J. W., Gorter G., Schrama L., Holmsen H. A novel technique for rapid determination of energy consumption in platelets. Demonstration of different energy consumption associated with three secretory responses. Biochem J. 1983 Jan 15;210(1):145–155. doi: 10.1042/bj2100145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barrowman M. M., Cockcroft S., Gomperts B. D. Differential control of azurophilic and specific granule exocytosis in Sendai-virus-permeabilized rabbit neutrophils. J Physiol. 1987 Feb;383:115–124. doi: 10.1113/jphysiol.1987.sp016399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Bennett J. P., Cockcroft S., Caswell A. H., Gomperts B. D. Plasma-membrane location of phosphatidylinositol hydrolysis in rabbit neutrophils stimulated with formylmethionyl-leucylphenylalanine. Biochem J. 1982 Dec 15;208(3):801–808. doi: 10.1042/bj2080801. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bennett J. P., Cockcroft S., Gomperts B. D. Ionomycin stimulates mast cell histamine secretion by forming a lipid-soluble calcium complex. Nature. 1979 Dec 20;282(5741):851–853. doi: 10.1038/282851a0. [DOI] [PubMed] [Google Scholar]
- Bennett J. P., Cockcroft S., Gomperts B. D. Rat mast cells permeabilized with ATP secrete histamine in response to calcium ions buffered in the micromolar range. J Physiol. 1981 Aug;317:335–345. doi: 10.1113/jphysiol.1981.sp013828. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berridge M. J. Inositol trisphosphate and diacylglycerol as second messengers. Biochem J. 1984 Jun 1;220(2):345–360. doi: 10.1042/bj2200345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bilezikian J. P., Aurbach G. D. The effects of nucleotides on the expression of beta-adrenergic adenylate cyclase activity in membranes from turkey erythrocytes. J Biol Chem. 1974 Jan 10;249(1):157–161. [PubMed] [Google Scholar]
- Bittner M. A., Holz R. W., Neubig R. R. Guanine nucleotide effects on catecholamine secretion from digitonin-permeabilized adrenal chromaffin cells. J Biol Chem. 1986 Aug 5;261(22):10182–10188. [PubMed] [Google Scholar]
- Buckingham L., Duncan J. L. Approximate dimensions of membrane lesions produced by streptolysin S and streptolysin O. Biochim Biophys Acta. 1983 Mar 23;729(1):115–122. doi: 10.1016/0005-2736(83)90462-5. [DOI] [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]
- Cooper D. M., Londos C. GTP-dependent stimulation and inhibition of adenylate cyclase. Horiz Biochem Biophys. 1982;6:309–333. [PubMed] [Google Scholar]
- Dangelmaier C. A., Daniel J. L., Smith J. B. Determination of basal and stimulated levels of inositol triphosphate in [32P]orthophosphate-labeled platelets. Anal Biochem. 1986 May 1;154(2):414–419. doi: 10.1016/0003-2697(86)90007-2. [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., Gomperts B. D. Calcium ionophores and movement of calcium ions following the physiological stimulus to a secretory process. Nature. 1973 Oct 5;245(5423):249–251. doi: 10.1038/245249a0. [DOI] [PubMed] [Google Scholar]
- Gomperts B. D., Baldwin J. M., Micklem K. J. Rat mast cells permeabilized with Sendai virus secrete histamine in response to Ca2+ buffered in the micromolar range. Biochem J. 1983 Mar 15;210(3):737–745. doi: 10.1042/bj2100737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gomperts B. D., Barrowman M. M., Cockcroft S. Dual role for guanine nucleotides in stimulus-secretion coupling. Fed Proc. 1986 Jun;45(7):2156–2161. [PubMed] [Google Scholar]
- Haslam R. J., Davidson M. M. Potentiation by thrombin of the secretion of serotonin from permeabilized platelets equilibrated with Ca2+ buffers. Relationship to protein phosphorylation and diacylglycerol formation. Biochem J. 1984 Sep 1;222(2):351–361. doi: 10.1042/bj2220351. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haslam R. J., Davidson M. M. Receptor-induced diacylglycerol formation in permeabilized platelets; possible role for a GTP-binding protein. J Recept Res. 1984;4(1-6):605–629. doi: 10.3109/10799898409042576. [DOI] [PubMed] [Google Scholar]
- Howell T. W., Gomperts B. D. Rat mast cells permeabilised with streptolysin O secrete histamine in response to Ca2+ at concentrations buffered in the micromolar range. Biochim Biophys Acta. 1987 Feb 18;927(2):177–183. doi: 10.1016/0167-4889(87)90132-7. [DOI] [PubMed] [Google Scholar]
- Johansen T. Adenosine triphosphate levels during anaphylactic histamine release in rat mast cells in vitro. Effects of glycolytic and respiratory inhibitors. Eur J Pharmacol. 1979 Sep 15;58(2):107–115. doi: 10.1016/0014-2999(79)90001-3. [DOI] [PubMed] [Google Scholar]
- Johansen T. Dependence of anaphylactic histamine release from rat mast cells on cellular energy metabolism. Eur J Pharmacol. 1981 Jul 10;72(4):281–286. doi: 10.1016/0014-2999(81)90565-3. [DOI] [PubMed] [Google Scholar]
- Johansen T. Utilization of adenosine triphosphate in rat mast cells during histamine release induced by the ionophore A23187. Br J Pharmacol. 1979 Jan;65(1):103–109. doi: 10.1111/j.1476-5381.1979.tb17338.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knight D. E., Baker P. F. Calcium-dependence of catecholamine release from bovine adrenal medullary cells after exposure to intense electric fields. J Membr Biol. 1982;68(2):107–140. doi: 10.1007/BF01872259. [DOI] [PubMed] [Google Scholar]
- Knight D. E., Baker P. F. Guanine nucleotides and Ca-dependent exocytosis. Studies on two adrenal cell preparations. FEBS Lett. 1985 Sep 23;189(2):345–349. doi: 10.1016/0014-5793(85)81053-x. [DOI] [PubMed] [Google Scholar]
- Knight D. E., Niggli V., Scrutton M. C. Thrombin and activators of protein kinase C modulate secretory responses of permeabilised human platelets induced by Ca2+. Eur J Biochem. 1984 Sep 3;143(2):437–446. doi: 10.1111/j.1432-1033.1984.tb08391.x. [DOI] [PubMed] [Google Scholar]
- Knight D. E., Scrutton M. C. Effects of guanine nucleotides on the properties of 5-hydroxytryptamine secretion from electropermeabilised human platelets. Eur J Biochem. 1986 Oct 1;160(1):183–190. doi: 10.1111/j.1432-1033.1986.tb09956.x. [DOI] [PubMed] [Google Scholar]
- Knight D. E., Scrutton M. C. Gaining access to the cytosol: the technique and some applications of electropermeabilization. Biochem J. 1986 Mar 15;234(3):497–506. doi: 10.1042/bj2340497. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ko L., Lagunoff D. Depletion of mast cell ATP inhibits complement-dependent cytotoxic histamine release. Exp Cell Res. 1976 Jul;100(2):313–321. doi: 10.1016/0014-4827(76)90154-3. [DOI] [PubMed] [Google Scholar]
- Nishizuka Y. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature. 1984 Apr 19;308(5961):693–698. doi: 10.1038/308693a0. [DOI] [PubMed] [Google Scholar]
- Palmer S., Hawkins P. T., Michell R. H., Kirk C. J. The labelling of polyphosphoinositides with [32P]Pi and the accumulation of inositol phosphates in vasopressin-stimulated hepatocytes. Biochem J. 1986 Sep 1;238(2):491–499. doi: 10.1042/bj2380491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parker R. B., Waud D. R. Pharmacological estimation of drug-receptor dissociation constants. Statistical evaluation. I. Agonists. J Pharmacol Exp Ther. 1971 Apr;177(1):1–12. [PubMed] [Google Scholar]
- Pfeuffer T., Eckstein F. Topology of the GTP-binding site of adenylyl cyclase from pigeon erythrocytes. FEBS Lett. 1976 Sep 1;67(3):354–358. doi: 10.1016/0014-5793(76)80563-7. [DOI] [PubMed] [Google Scholar]
- Ronning S. A., Martin T. F. Prolactin secretion in permeable GH3 pituitary cells is stimulated by Ca2+ and protein kinase C activators. Biochem Biophys Res Commun. 1985 Jul 31;130(2):524–532. doi: 10.1016/0006-291x(85)90448-6. [DOI] [PubMed] [Google Scholar]
- Ross E. M., Maguire M. E., Sturgill T. W., Biltonen R. L., Gilman A. G. Relationship between the beta-adrenergic receptor and adenylate cyclase. J Biol Chem. 1977 Aug 25;252(16):5761–5775. [PubMed] [Google Scholar]
- Verhoeven A. J., Mommersteeg M. E., Akkerman J. W. Metabolic energy is required in human platelets at any stage during optical aggregation and secretion. Biochim Biophys Acta. 1984 Aug 21;800(3):242–250. doi: 10.1016/0304-4165(84)90402-1. [DOI] [PubMed] [Google Scholar]
- Verhoeven A. J., Mommersteeg M. E., Akkerman J. W. Quantification of energy consumption in platelets during thrombin-induced aggregation and secretion. Tight coupling between platelet responses and the increment in energy consumption. Biochem J. 1984 Aug 1;221(3):777–787. doi: 10.1042/bj2210777. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vilmart-Seuwen J., Kersken H., Stürzl R., Plattner H. ATP keeps exocytosis sites in a primed state but is not required for membrane fusion: an analysis with Paramecium cells in vivo and in vitro. J Cell Biol. 1986 Oct;103(4):1279–1288. doi: 10.1083/jcb.103.4.1279. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wolff J., Cook G. H. Activation of thyroid membrane adenylate cyclase by purine nucleotides. J Biol Chem. 1973 Jan 10;248(1):350–355. [PubMed] [Google Scholar]
- Yamanaka G., Eckstein F., Stryer L. Interaction of retinal transducin with guanosine triphosphate analogues: specificity of the gamma-phosphate binding region. Biochemistry. 1986 Oct 7;25(20):6149–6153. doi: 10.1021/bi00368a048. [DOI] [PubMed] [Google Scholar]