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. 1996 Sep;71(3):1633–1640. doi: 10.1016/S0006-3495(96)79368-2

Exocytotic release from individual granules exhibits similar properties at mast and chromaffin cells.

K Pihel 1, E R Travis 1, R Borges 1, R M Wightman 1
PMCID: PMC1233631  PMID: 8874038

Abstract

The effects of temperature on granular secretion were studied in individual bovine adrenal chromaffin and rat peritoneal mast cells. It was found that more molecules are released from individual granules at physiological temperature than at room temperature, where such experiments are normally performed. In mast cells, there is also a dramatic decrease in the time required for exocytosis to be complete at 37 degrees C compared to room temperature. In the presence of some cations, the amount released from individual granules at room temperature from both types of cells could be altered. The amount of secretion decreased with the divalent cation zinc but increased with the monovalent cation cesium. These experiments used two electrochemical techniques: cyclic voltammetry and amperometry. With amperometry, the concentration gradient created by the electrode near the cell further increased the amount of release. Similar responses to changes in the extracellular environment in chromaffin and mast cells suggest that the mechanism of extrusion of the granule contents is similar in both cell types.

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Selected References

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  1. Alvarez de Toledo G., Fernández-Chacón R., Fernández J. M. Release of secretory products during transient vesicle fusion. Nature. 1993 Jun 10;363(6429):554–558. doi: 10.1038/363554a0. [DOI] [PubMed] [Google Scholar]
  2. Baur J. E., Kristensen E. W., May L. J., Wiedemann D. J., Wightman R. M. Fast-scan voltammetry of biogenic amines. Anal Chem. 1988 Jul 1;60(13):1268–1272. doi: 10.1021/ac00164a006. [DOI] [PubMed] [Google Scholar]
  3. Beaudoin A. R., Mercier M. Exocytosis in mammalian cells. VI. Temperature dependence of pancreatic exocrine secretion. Can J Physiol Pharmacol. 1980 Dec;58(12):1509–1512. doi: 10.1139/y80-228. [DOI] [PubMed] [Google Scholar]
  4. Bittner M. A., Holz R. W. A temperature-sensitive step in exocytosis. J Biol Chem. 1992 Aug 15;267(23):16226–16229. [PubMed] [Google Scholar]
  5. Bruns D., Jahn R. Real-time measurement of transmitter release from single synaptic vesicles. Nature. 1995 Sep 7;377(6544):62–65. doi: 10.1038/377062a0. [DOI] [PubMed] [Google Scholar]
  6. Casey R. P., Njus D., Radda G. K., Sehr P. A. Active proton uptake by chromaffin granules: observation by amine distribution and phosphorus-31 nuclear magnetic resonance techniques. Biochemistry. 1977 Mar 8;16(5):972–977. doi: 10.1021/bi00624a025. [DOI] [PubMed] [Google Scholar]
  7. Chow R. H., von Rüden L., Neher E. Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature. 1992 Mar 5;356(6364):60–63. doi: 10.1038/356060a0. [DOI] [PubMed] [Google Scholar]
  8. Curran M. J., Brodwick M. S. Ionic control of the size of the vesicle matrix of beige mouse mast cells. J Gen Physiol. 1991 Oct;98(4):771–790. doi: 10.1085/jgp.98.4.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Daniels A. J., Williams R. J., Wright P. E. The character of the stored molecules in chromaffin granules of the adrenal medulla: a nuclear magnetic resonance study. Neuroscience. 1978;3(6):573–585. doi: 10.1016/0306-4522(78)90022-2. [DOI] [PubMed] [Google Scholar]
  10. Danscher G., Obel J., Thorlacius-Ussing O. Electron microscopic demonstration of metals in rat mast cells. A cytochemical study based on an improved sulphide silver method. Histochemistry. 1980;66(3):293–300. doi: 10.1007/BF00495742. [DOI] [PubMed] [Google Scholar]
  11. Finnegan J. M., Pihel K., Cahill P. S., Huang L., Zerby S. E., Ewing A. G., Kennedy R. T., Wightman R. M. Vesicular quantal size measured by amperometry at chromaffin, mast, pheochromocytoma, and pancreatic beta-cells. J Neurochem. 1996 May;66(5):1914–1923. doi: 10.1046/j.1471-4159.1996.66051914.x. [DOI] [PubMed] [Google Scholar]
  12. Jankowski J. A., Schroeder T. J., Ciolkowski E. L., Wightman R. M. Temporal characteristics of quantal secretion of catecholamines from adrenal medullary cells. J Biol Chem. 1993 Jul 15;268(20):14694–14700. [PubMed] [Google Scholar]
  13. Johansen T. Mechanism of histamine release from rat mast cells induced by the ionophore A23187: effects of calcium and temperature. Br J Pharmacol. 1978 Aug;63(4):643–649. doi: 10.1111/j.1476-5381.1978.tb17277.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Johnson R. G., Carty S. E., Fingerhood B. J., Scarpa A. The internal pH of mast cell granules. FEBS Lett. 1980 Oct 20;120(1):75–79. doi: 10.1016/0014-5793(80)81050-7. [DOI] [PubMed] [Google Scholar]
  15. Johnson R. G., Scarpa A. Protonmotive force and catecholamine transport in isolated chromaffin granules. J Biol Chem. 1979 May 25;254(10):3750–3760. [PubMed] [Google Scholar]
  16. Kao L. S., Westhead E. W. Temperature dependence of catecholamine secretion from cultured bovine chromaffin cells. J Neurochem. 1984 Aug;43(2):590–592. doi: 10.1111/j.1471-4159.1984.tb00940.x. [DOI] [PubMed] [Google Scholar]
  17. Kawagoe K. T., Zimmerman J. B., Wightman R. M. Principles of voltammetry and microelectrode surface states. J Neurosci Methods. 1993 Jul;48(3):225–240. doi: 10.1016/0165-0270(93)90094-8. [DOI] [PubMed] [Google Scholar]
  18. Khanin R., Parnas H., Segel L. Diffusion cannot govern the discharge of neurotransmitter in fast synapses. Biophys J. 1994 Sep;67(3):966–972. doi: 10.1016/S0006-3495(94)80562-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kopell W. N., Westhead E. W. Osmotic pressures of solutions of ATP and catecholamines relating to storage in chromaffin granules. J Biol Chem. 1982 May 25;257(10):5707–5710. [PubMed] [Google Scholar]
  20. Leszczyszyn D. J., Jankowski J. A., Viveros O. H., Diliberto E. J., Jr, Near J. A., Wightman R. M. Nicotinic receptor-mediated catecholamine secretion from individual chromaffin cells. Chemical evidence for exocytosis. J Biol Chem. 1990 Sep 5;265(25):14736–14737. [PubMed] [Google Scholar]
  21. Leszczyszyn D. J., Jankowski J. A., Viveros O. H., Diliberto E. J., Jr, Near J. A., Wightman R. M. Secretion of catecholamines from individual adrenal medullary chromaffin cells. J Neurochem. 1991 Jun;56(6):1855–1863. doi: 10.1111/j.1471-4159.1991.tb03441.x. [DOI] [PubMed] [Google Scholar]
  22. Moro M. A., López M. G., Gandía L., Michelena P., García A. G. Separation and culture of living adrenaline- and noradrenaline-containing cells from bovine adrenal medullae. Anal Biochem. 1990 Mar;185(2):243–248. doi: 10.1016/0003-2697(90)90287-j. [DOI] [PubMed] [Google Scholar]
  23. Nanavati C., Fernandez J. M. The secretory granule matrix: a fast-acting smart polymer. Science. 1993 Feb 12;259(5097):963–965. doi: 10.1126/science.8438154. [DOI] [PubMed] [Google Scholar]
  24. Oberhauser A. F., Monck J. R., Fernandez J. M. Events leading to the opening and closing of the exocytotic fusion pore have markedly different temperature dependencies. Kinetic analysis of single fusion events in patch-clamped mouse mast cells. Biophys J. 1992 Mar;61(3):800–809. doi: 10.1016/S0006-3495(92)81884-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pihel K., Hsieh S., Jorgenson J. W., Wightman R. M. Electrochemical detection of histamine and 5-hydroxytryptamine at isolated mast cells. Anal Chem. 1995 Dec 15;67(24):4514–4521. doi: 10.1021/ac00120a014. [DOI] [PubMed] [Google Scholar]
  26. Rabenstein D. L., Ludowyke R., Lagunoff D. Proton nuclear magnetic resonance studies of mast cell histamine. Biochemistry. 1987 Nov 3;26(22):6923–6926. doi: 10.1021/bi00396a010. [DOI] [PubMed] [Google Scholar]
  27. Schroeder T. J., Borges R., Finnegan J. M., Pihel K., Amatore C., Wightman R. M. Temporally resolved, independent stages of individual exocytotic secretion events. Biophys J. 1996 Feb;70(2):1061–1068. doi: 10.1016/S0006-3495(96)79652-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schroeder T. J., Jankowski J. A., Kawagoe K. T., Wightman R. M., Lefrou C., Amatore C. Analysis of diffusional broadening of vesicular packets of catecholamines released from biological cells during exocytosis. Anal Chem. 1992 Dec 15;64(24):3077–3083. doi: 10.1021/ac00048a003. [DOI] [PubMed] [Google Scholar]
  29. Svendstrup F., Chakravarty N. Glucose metabolism in rat mast cells during histamine release. Exp Cell Res. 1977 Apr;106(1):223–231. doi: 10.1016/0014-4827(77)90259-2. [DOI] [PubMed] [Google Scholar]
  30. Südhof T. C., Morris S. J. Temperature-induced lysis of chromaffin granules provides evidence against the two-pool hypothesis of catecholamine storage. Biochim Biophys Acta. 1983 May 25;757(2):176–181. doi: 10.1016/0304-4165(83)90106-x. [DOI] [PubMed] [Google Scholar]
  31. Takayama I., Fujii Y., Ohno S., Fujino M. A. Morphological study of rat mast cells stimulated with compound 48/80 at different temperatures. Histochemistry. 1994 Aug;102(2):83–87. doi: 10.1007/BF00269010. [DOI] [PubMed] [Google Scholar]
  32. Thorlacius-Ussing O., Rasmussen B. L. Light and electron microscopical visualization of selenium in adrenal glands from rats exposed to sodium selenite. Exp Mol Pathol. 1986 Aug;45(1):59–67. doi: 10.1016/0014-4800(86)90006-7. [DOI] [PubMed] [Google Scholar]
  33. Uvnäs B., Aborg C. H. Cation exchange--a common mechanism in the storage and release of biogenic amines stored in granules (vesicles)? II. Comparative studies on sodium-induced release of biogenic amines from the synthetic weak cation-exchangers Amberlite IRC-50 and duolite CS-100 and from biogenic (granule-enriched) materials. Acta Physiol Scand. 1984 Jan;120(1):87–97. doi: 10.1111/j.1748-1716.1984.tb07377.x. [DOI] [PubMed] [Google Scholar]
  34. Verdugo P. Goblet cells secretion and mucogenesis. Annu Rev Physiol. 1990;52:157–176. doi: 10.1146/annurev.ph.52.030190.001105. [DOI] [PubMed] [Google Scholar]
  35. Videen J. S., Mezger M. S., Chang Y. M., O'Connor D. T. Calcium and catecholamine interactions with adrenal chromogranins. Comparison of driving forces in binding and aggregation. J Biol Chem. 1992 Feb 15;267(5):3066–3073. [PubMed] [Google Scholar]
  36. Wightman R. M., Jankowski J. A., Kennedy R. T., Kawagoe K. T., Schroeder T. J., Leszczyszyn D. J., Near J. A., Diliberto E. J., Jr, Viveros O. H. Temporally resolved catecholamine spikes correspond to single vesicle release from individual chromaffin cells. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10754–10758. doi: 10.1073/pnas.88.23.10754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wightman R. M., Schroeder T. J., Finnegan J. M., Ciolkowski E. L., Pihel K. Time course of release of catecholamines from individual vesicles during exocytosis at adrenal medullary cells. Biophys J. 1995 Jan;68(1):383–390. doi: 10.1016/S0006-3495(95)80199-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wilson S. P., Kirshner N. Calcium-evoked secretion from digitonin-permeabilized adrenal medullary chromaffin cells. J Biol Chem. 1983 Apr 25;258(8):4994–5000. [PubMed] [Google Scholar]
  39. Wilson S. P. Purification of adrenal chromaffin cells on Renografin gradients. J Neurosci Methods. 1987 Feb;19(2):163–171. doi: 10.1016/0165-0270(87)90031-8. [DOI] [PubMed] [Google Scholar]

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