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. 1993 Oct;183(Pt 2):309–314.

Exocytosis in adrenal chromaffin cells.

R D Burgoyne 1, A Morgan 1, I Robinson 1, N Pender 1, T R Cheek 1
PMCID: PMC1259910  PMID: 8300418

Abstract

Recent advances have led to an increased understanding of the Ca(2+)-signalling pathway leading to exocytosis in bovine adrenal chromaffin cells. Video-imaging studies have allowed the temporal and spatial aspects of the Ca2+ signal to be investigated in detail. Ca2+ entry at the plasma membrane appears to be crucial for the activation of exocytosis. Ca2+ can enter through the nicotinic channel or characterised voltage-activated channels, or through other poorly defined pathways due to a variety of agonists. Emptying of internal Ca2+ stores is sufficient to activate a Ca2+ entry pathway. The elevation of cytosolic Ca2+ concentration leads to a reorganisation of the cortical actin network and to the triggering of exocytosis. Studies on permeabilised chromaffin cells have resulted in the identification of some of the proteins that control Ca(2+)-dependent exocytosis. These include the peripheral plasma membrane protein annexin II and the cytosolic proteins, protein kinase C and 14-3-3 proteins (Exo1).

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Selected References

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  1. Ahnert-Hilger G., Bader M. F., Bhakdi S., Gratzl M. Introduction of macromolecules into bovine adrenal medullary chromaffin cells and rat pheochromocytoma cells (PC12) by permeabilization with streptolysin O: inhibitory effect of tetanus toxin on catecholamine secretion. J Neurochem. 1989 Jun;52(6):1751–1758. doi: 10.1111/j.1471-4159.1989.tb07253.x. [DOI] [PubMed] [Google Scholar]
  2. Aitken A., Ellis C. A., Harris A., Sellers L. A., Toker A. Kinase and neurotransmitters. Nature. 1990 Apr 12;344(6267):594–594. doi: 10.1038/344594a0. [DOI] [PubMed] [Google Scholar]
  3. Ali S. M., Geisow M. J., Burgoyne R. D. A role for calpactin in calcium-dependent exocytosis in adrenal chromaffin cells. Nature. 1989 Jul 27;340(6231):313–315. doi: 10.1038/340313a0. [DOI] [PubMed] [Google Scholar]
  4. Artalejo C. R., García A. G., Aunis D. Chromaffin cell calcium channel kinetics measured isotopically through fast calcium, strontium, and barium fluxes. J Biol Chem. 1987 Jan 15;262(2):915–926. [PubMed] [Google Scholar]
  5. Burgoyne R. D., Cheek T. R., Morgan A., O'Sullivan A. J., Moreton R. B., Berridge M. J., Mata A. M., Colyer J., Lee A. G., East J. M. Distribution of two distinct Ca2+-ATPase-like proteins and their relationships to the agonist-sensitive calcium store in adrenal chromaffin cells. Nature. 1989 Nov 2;342(6245):72–74. doi: 10.1038/342072a0. [DOI] [PubMed] [Google Scholar]
  6. Burgoyne R. D. Control of exocytosis in adrenal chromaffin cells. Biochim Biophys Acta. 1991 Jul 22;1071(2):174–202. doi: 10.1016/0304-4157(91)90024-q. [DOI] [PubMed] [Google Scholar]
  7. Burgoyne R. D., Morgan A. Evidence for a role of calpactin in calcium-dependent exocytosis. Biochem Soc Trans. 1990 Dec;18(6):1101–1104. doi: 10.1042/bst0181101. [DOI] [PubMed] [Google Scholar]
  8. Burgoyne R. D., Morgan A., O'Sullivan A. J. A major role for protein kinase C in calcium-activated exocytosis in permeabilised adrenal chromaffin cells. FEBS Lett. 1988 Sep 26;238(1):151–155. doi: 10.1016/0014-5793(88)80246-1. [DOI] [PubMed] [Google Scholar]
  9. Burgoyne R. D., Morgan A., O'Sullivan A. J. The control of cytoskeletal actin and exocytosis in intact and permeabilized adrenal chromaffin cells: role of calcium and protein kinase C. Cell Signal. 1989;1(4):323–334. doi: 10.1016/0898-6568(89)90051-x. [DOI] [PubMed] [Google Scholar]
  10. Cheek T. R., Barry V. A., Berridge M. J., Missiaen L. Bovine adrenal chromaffin cells contain an inositol 1,4,5-trisphosphate-insensitive but caffeine-sensitive Ca2+ store that can be regulated by intraluminal free Ca2+. Biochem J. 1991 May 1;275(Pt 3):697–701. doi: 10.1042/bj2750697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cheek T. R., Burgoyne R. D. Cyclic AMP inhibits both nicotine-induced actin disassembly and catecholamine secretion from bovine adrenal chromaffin cells. J Biol Chem. 1987 Aug 25;262(24):11663–11666. [PubMed] [Google Scholar]
  12. Cheek T. R., Burgoyne R. D. Nicotine-evoked disassembly of cortical actin filaments in adrenal chromaffin cells. FEBS Lett. 1986 Oct 20;207(1):110–114. doi: 10.1016/0014-5793(86)80022-9. [DOI] [PubMed] [Google Scholar]
  13. Cheek T. R., Jackson T. R., O'Sullivan A. J., Moreton R. B., Berridge M. J., Burgoyne R. D. Simultaneous measurements of cytosolic calcium and secretion in single bovine adrenal chromaffin cells by fluorescent imaging of fura-2 in cocultured cells. J Cell Biol. 1989 Sep;109(3):1219–1227. doi: 10.1083/jcb.109.3.1219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cheek T. R., O'Sullivan A. J., Moreton R. B., Berridge M. J., Burgoyne R. D. Spatial localization of the stimulus-induced rise in cytosolic Ca2+ in bovine adrenal chromaffin cells. Distinct nicotinic and muscarinic patterns. FEBS Lett. 1989 Apr 24;247(2):429–434. doi: 10.1016/0014-5793(89)81385-7. [DOI] [PubMed] [Google Scholar]
  15. Cheek T. R., O'Sullivan A. J., Moreton R. B., Berridge M. J., Burgoyne R. D. The caffeine-sensitive Ca2+ store in bovine adrenal chromaffin cells; an examination of its role in triggering secretion and Ca2+ homeostasis. FEBS Lett. 1990 Jun 18;266(1-2):91–95. doi: 10.1016/0014-5793(90)81514-o. [DOI] [PubMed] [Google Scholar]
  16. Creutz C. E., Pazoles C. J., Pollard H. B. Identification and purification of an adrenal medullary protein (synexin) that causes calcium-dependent aggregation of isolated chromaffin granules. J Biol Chem. 1978 Apr 25;253(8):2858–2866. [PubMed] [Google Scholar]
  17. Drust D. S., Creutz C. E. Aggregation of chromaffin granules by calpactin at micromolar levels of calcium. Nature. 1988 Jan 7;331(6151):88–91. doi: 10.1038/331088a0. [DOI] [PubMed] [Google Scholar]
  18. Dunn L. A., Holz R. W. Catecholamine secretion from digitonin-treated adrenal medullary chromaffin cells. J Biol Chem. 1983 Apr 25;258(8):4989–4993. [PubMed] [Google Scholar]
  19. Holz R. W., Senyshyn J., Bittner M. A. Mechanisms involved in calcium-dependent exocytosis. Ann N Y Acad Sci. 1991;635:382–392. doi: 10.1111/j.1749-6632.1991.tb36506.x. [DOI] [PubMed] [Google Scholar]
  20. Ichimura T., Isobe T., Okuyama T., Takahashi N., Araki K., Kuwano R., Takahashi Y. Molecular cloning of cDNA coding for brain-specific 14-3-3 protein, a protein kinase-dependent activator of tyrosine and tryptophan hydroxylases. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7084–7088. doi: 10.1073/pnas.85.19.7084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kim K. T., Westhead E. W. Cellular responses to Ca2+ from extracellular and intracellular sources are different as shown by simultaneous measurements of cytosolic Ca2+ and secretion from bovine chromaffin cells. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9881–9885. doi: 10.1073/pnas.86.24.9881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Knight D. E., Sugden D., Baker P. F. Evidence implicating protein kinase C in exocytosis from electropermeabilized bovine chromaffin cells. J Membr Biol. 1988 Aug;104(1):21–34. doi: 10.1007/BF01871899. [DOI] [PubMed] [Google Scholar]
  24. Knight D. E., von Grafenstein H., Athayde C. M. Calcium-dependent and calcium-independent exocytosis. Trends Neurosci. 1989 Nov;12(11):451–458. doi: 10.1016/0166-2236(89)90095-7. [DOI] [PubMed] [Google Scholar]
  25. Koffer A., Tatham P. E., Gomperts B. D. Changes in the state of actin during the exocytotic reaction of permeabilized rat mast cells. J Cell Biol. 1990 Sep;111(3):919–927. doi: 10.1083/jcb.111.3.919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Morgan A., Burgoyne R. D. Exo1 and Exo2 proteins stimulate calcium-dependent exocytosis in permeabilized adrenal chromaffin cells. Nature. 1992 Feb 27;355(6363):833–836. doi: 10.1038/355833a0. [DOI] [PubMed] [Google Scholar]
  27. Morgan A., Burgoyne R. D. Interaction between protein kinase C and Exo1 (14-3-3 protein) and its relevance to exocytosis in permeabilized adrenal chromaffin cells. Biochem J. 1992 Sep 15;286(Pt 3):807–811. doi: 10.1042/bj2860807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Morgan A., Burgoyne R. D. Relationship between arachidonic acid release and Ca2(+)-dependent exocytosis in digitonin-permeabilized bovine adrenal chromaffin cells. Biochem J. 1990 Nov 1;271(3):571–574. doi: 10.1042/bj2710571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nakata T., Sobue K., Hirokawa N. Conformational change and localization of calpactin I complex involved in exocytosis as revealed by quick-freeze, deep-etch electron microscopy and immunocytochemistry. J Cell Biol. 1990 Jan;110(1):13–25. doi: 10.1083/jcb.110.1.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. O'Sullivan A. J., Burgoyne R. D. A comparison of bradykinin, angiotensin II and muscarinic stimulation of cultured bovine adrenal chromaffin cells. Biosci Rep. 1989 Apr;9(2):243–252. doi: 10.1007/BF01116001. [DOI] [PubMed] [Google Scholar]
  31. O'Sullivan A. J., Cheek T. R., Moreton R. B., Berridge M. J., Burgoyne R. D. Localization and heterogeneity of agonist-induced changes in cytosolic calcium concentration in single bovine adrenal chromaffin cells from video imaging of fura-2. EMBO J. 1989 Feb;8(2):401–411. doi: 10.1002/j.1460-2075.1989.tb03391.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Patzak A., Böck G., Fischer-Colbrie R., Schauenstein K., Schmidt W., Lingg G., Winkler H. Exocytotic exposure and retrieval of membrane antigens of chromaffin granules: quantitative evaluation of immunofluorescence on the surface of chromaffin cells. J Cell Biol. 1984 May;98(5):1817–1824. doi: 10.1083/jcb.98.5.1817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pender N., Burgoyne R. D. Histamine stimulates exocytosis in a sub-population of bovine adrenal chromaffin cells. Neurosci Lett. 1992 Sep 14;144(1-2):207–210. doi: 10.1016/0304-3940(92)90751-r. [DOI] [PubMed] [Google Scholar]
  34. Perrin D., Möller K., Hanke K., Söling H. D. cAMP and Ca(2+)-mediated secretion in parotid acinar cells is associated with reversible changes in the organization of the cytoskeleton. J Cell Biol. 1992 Jan;116(1):127–134. doi: 10.1083/jcb.116.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Phillips J. H., Burridge K., Wilson S. P., Kirshner N. Visualization of the exocytosis/endocytosis secretory cycle in cultured adrenal chromaffin cells. J Cell Biol. 1983 Dec;97(6):1906–1917. doi: 10.1083/jcb.97.6.1906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Pollard H. B., Burns A. L., Rojas E. A molecular basis for synexin-driven, calcium-dependent membrane fusion. J Exp Biol. 1988 Sep;139:267–286. doi: 10.1242/jeb.139.1.267. [DOI] [PubMed] [Google Scholar]
  37. Putney J. W., Jr A model for receptor-regulated calcium entry. Cell Calcium. 1986 Feb;7(1):1–12. doi: 10.1016/0143-4160(86)90026-6. [DOI] [PubMed] [Google Scholar]
  38. Robinson I. M., Burgoyne R. D. A distinct 2,5-di-(tert-butyl)-1,4-benzohydroquinone-sensitive calcium store in bovine adrenal chromaffin cells. FEBS Lett. 1991 Sep 9;289(2):151–154. doi: 10.1016/0014-5793(91)81057-f. [DOI] [PubMed] [Google Scholar]
  39. Robinson I. M., Burgoyne R. D. Characterisation of distinct inositol 1,4,5-trisphosphate-sensitive and caffeine-sensitive calcium stores in digitonin-permeabilised adrenal chromaffin cells. J Neurochem. 1991 May;56(5):1587–1593. doi: 10.1111/j.1471-4159.1991.tb02055.x. [DOI] [PubMed] [Google Scholar]
  40. Robinson I. M., Cheek T. R., Burgoyne R. D. Ca2+ influx induced by the Ca(2+)-ATPase inhibitors 2,5-di-(t-butyl)-1,4-benzohydroquinone and thapsigargin in bovine adrenal chromaffin cells. Biochem J. 1992 Dec 1;288(Pt 2):457–463. doi: 10.1042/bj2880457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sarafian T., Aunis D., Bader M. F. Loss of proteins from digitonin-permeabilized adrenal chromaffin cells essential for exocytosis. J Biol Chem. 1987 Dec 5;262(34):16671–16676. [PubMed] [Google Scholar]
  42. Simon S. M., Llinás R. R. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys J. 1985 Sep;48(3):485–498. doi: 10.1016/S0006-3495(85)83804-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Smith S. J., Augustine G. J. Calcium ions, active zones and synaptic transmitter release. Trends Neurosci. 1988 Oct;11(10):458–464. doi: 10.1016/0166-2236(88)90199-3. [DOI] [PubMed] [Google Scholar]
  44. Stauderman K. A., McKinney R. A., Murawsky M. M. The role of caffeine-sensitive Ca2+ stores in agonist- and inositol 1,4,5-trisphosphate-induced Ca2+ release from bovine adrenal chromaffin cells. Biochem J. 1991 Sep 15;278(Pt 3):643–650. doi: 10.1042/bj2780643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Stauderman K. A., Murawsky M. M., Pruss R. M. Agonist-dependent patterns of cytosolic Ca2+ changes in single bovine adrenal chromaffin cells: relationship to catecholamine release. Cell Regul. 1990 Aug;1(9):683–691. doi: 10.1091/mbc.1.9.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Stauderman K. A., Murawsky M. M. The inositol 1,4,5-trisphosphate-forming agonist histamine activates a ryanodine-sensitive Ca2+ release mechanism in bovine adrenal chromaffin cells. J Biol Chem. 1991 Oct 15;266(29):19150–19153. [PubMed] [Google Scholar]
  47. Terbush D. R., Holz R. W. Activation of protein kinase C is not required for exocytosis from bovine adrenal chromaffin cells. The effects of protein kinase C(19-31), Ca/CaM kinase II(291-317), and staurosporine. J Biol Chem. 1990 Dec 5;265(34):21179–21184. [PubMed] [Google Scholar]
  48. Toker A., Ellis C. A., Sellers L. A., Aitken A. Protein kinase C inhibitor proteins. Purification from sheep brain and sequence similarity to lipocortins and 14-3-3 protein. Eur J Biochem. 1990 Jul 31;191(2):421–429. doi: 10.1111/j.1432-1033.1990.tb19138.x. [DOI] [PubMed] [Google Scholar]
  49. Vitale M. L., Rodríguez Del Castillo A., Tchakarov L., Trifaró J. M. Cortical filamentous actin disassembly and scinderin redistribution during chromaffin cell stimulation precede exocytosis, a phenomenon not exhibited by gelsolin. J Cell Biol. 1991 Jun;113(5):1057–1067. doi: 10.1083/jcb.113.5.1057. [DOI] [PMC free article] [PubMed] [Google Scholar]

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