Submaximal responses in calcium-triggered exocytosis are explained by differences in the calcium sensitivity of individual secretory vesicles

Journal of General Physiology

Volumn 112, Issue 5, 1998, Pages 559-567

  Blank, Paul S ^a   Cho, Myoung Soon ^a   Vogel, Steven S ^a,d   Kaplan, Doron ^a,c   Kang, Albert ^a   Malley, James ^b   Zimmerberg, Joshua ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c ISRAEL INSTITUTE FOR BIOLOGICAL RESEARCH   (Israel)

^d MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Cytoplasmic vesicles; Fertilization; Membrane fusion; Sea urchins; Secretion

Indexed keywords

CALCIUM;

ANIMAL TISSUE; ARTICLE; CHEMOSENSITIVITY; CONTROLLED STUDY; EGG; EXOCYTOSIS; MEMBRANE FUSION; MEMBRANE VESICLE; NONHUMAN; SEA URCHIN;

EID: 0031774259     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.112.5.559     Document Type: Article

References (34)

1. Augustine, G.J., and M.P. Charlton. 1986. Calcium dependence of presynaptic calcium current and post-synaptic response at the squid giant synapse. J. Physiol. (Camb.). 381:619-640.
2. Baker, P.F., and D.E. Knight. 1981. Calcium control of exocytosis and endocytosis in bovine adrenal medullary cells. Philos. Trans. R. Soc. Lond. B Biol. Sci. 296:83-103.
3. Baker, P.F., and M.J. Whitaker. 1978. Influence of ATP and calcium on the cortical reaction in sea urchin eggs. Nature. 276:513-515.
4. Berstein, G., T. Haga, and A. Ichiyama. 1989. Effect of lipid environment on the differential affinity of purified cerebral and atrial muscarinic acetylcholine receptors for pirenzepine. Mol. Pharmacol. 36:601-607.
5. Chernomordik, L., M.M. Kozlov, and J. Zimmerberg. 1995. Lipids in biological membrane fusion. J. Membr. Biol. 146:1-14.
6. Chess, A., L. Buck, M.M. Dowling, R. Axel, and J. Ngai. 1992. Molecular biology of smell: expression of the multigene family encoding putative odorant receptors. Cold Spring Harbor Symp. Quant. Biol. 57:505-516.
7. Dodge, F.A., and R. Rahamimoff. 1967. Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J. Physiol. (Camb.). 193:419-432.
8. Heinemann, C., L. von Ruden, R.H. Chow, and E. Neher. 1993. A two-step model of secretion control in neuroendocrine cells. Pflügers Arch. 424:105-112.
9. 2+. Biophys. J. 67:2546-2557.
10. Jackson, R.C., and J.H. Crabb. 1988. Cortical exocytosis in the sea urchin egg. Curr. Top. Membr. Transp. 32:45-85.
11. Kaplan, D., P. Bungay, J. Sullivan, and J. Zimmerberg. 1996. A rapid-flow perfusion chamber for high-resolution microscopy. J. Microsc. 181:286-297.
12. Kaplan, D., J. Zimmerberg, A. Puri, D. Sarkar, and R. Blumenthal. 1991. Single cell fusion events induced by influenza hemagglutinin: studies with rapid-flow, quantitative fluorescence microscopy. Exp. Cell Res. 195:137-144.
13. Knight, D.E., and M.C. Scrutton. 1986. Gaining access to the cytosol: the technique and some applications of electropermeabilization. Biochem. J. 234:497-506.
14. Knight, D.E., and P.F. Baker. 1982. Calcium-dependence of catecholamine release from bovine adrenal medullary cells after exposure to intense electric fields. J. Membr. Biol. 68:107-140.
15. Knight, D.E., and P.F. Baker. 1987. Exocytosis from the vesicle viewpoint: an overview. Ann. NY Acad. Sci. 493:504-523.
16. 2+-dependent manner. TINS (Trends Neurosci.). 18:177-183.
17. Llinas, R., I.Z. Steinberg, and K. Walton. 1976. Presynaptic calcium currents and their relationship to synaptic transmission: voltage clamp study in squid giant synapse and theoretical model for the calcium gate. Proc. Natl. Acad. Sci. USA. 73:2918-2922.
18. Llinas, R., I.Z. Steinberg, and K. Walton. 1981. Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys. J. 33:323-352.
19. McLaughlin, S., and M. Whitaker. 1988. Cations that alter surface potentials of lipid bilayers increase the calcium requirement for exocytosis in sea urchin eggs. J. Physiol. (Camb.). 396:189-204.
20. Moy, G.W., G.S. Kopf, C. Gache, and V.D. Vacquier. 1983. Calcium-mediated release of glucanase activity from cortical granules of sea urchin eggs. Dev. Biol. 100:267-274.
21. Ninomiya, Y., T. Kishimoto, T. Yamazawa, H. Ikeda, Y. Miyashita, and H. Kasai. 1997. Kinetic diversity in the fusion of exocytotic vesicles. EMBO (Eur. Mol. Biol. Organ.). 16:929-934.
22. Sarafian, T., D. Aunis, and M. Bader. 1987. Loss of proteins from digitonin-permeabilized adrenal chromaffin cells essential for exocytosis. J. Biol. Chem. 34:16671-16676.
23. Sasaki, H., and D. Epel. 1983. Cortical vesicle exocytosis in isolated cortices of sea urchin eggs: description of a turbidimetric assay and its utilization in studying effects of different media on discharge. Dev. Biol. 98:327-337.
24. Shen, S.S. 1995. Mechanisms of calcium regulation in sea urchin eggs and their activities during fertilization. In Current Topics in Developmental Biology. Vol. 30. R.A. Pedersen and G.P. Schatten, editors. Academic Press, Inc., New York. 63-101.
25. Simon, S.M., and R.R. Llinas. 1985. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys. J. 48:485-498.
26. Tsien, R.Y., and T.J. Rink. 1980. Neutral carrier ion-selective micro-electrodes for measurement of intracellular free calcium. Biochim. Biophys. Acta. 599:623-638.
27. Vacquier, V. 1975. The isolation of intact cortical granules from sea urchin eggs: calcium ions trigger granule discharge. Dev. Biol. 43: 62-74.
28. Vogel, S.S., K. Delaney, and J. Zimmerberg. 1991. The sea urchin cortical reaction. A model system for studying the final steps of calcium-triggered vesicle fusion. Ann. NY Acad. Sci. 635:35-44.
29. Vogel, S.S., E.A. Leikina, and L.V. Chernomordik. 1993. Lysophosphatidylcholine reversibly arrests exocytosis and viral fusion at a stage between triggering and membrane merger. J. Biol. Chem. 268:25764-25768.
30. Vogel, S.S., P.S. Blank, and J. Zimmerberg. 1996. Poisson-distributed active fusion complexes underlie die control of the rate and extent of exocytosis by calcium. J. Cell Biol. 134:329-338.
31. Zimmerberg, J., C. Sardet, and D. Epel. 1985. Exocytosis of sea urchin egg cortical vesicles in vitro is retarded by hyperosmotic sucrose: kinetics of fusion monitored by quantitative light-scattering microscopy. J. Cell Biol. 101:2398-2410.
32. Zimmerberg, J., J. Sullivan, and P.M. Bungay. 1992. Rapid exchange imaging chamber for stop-flow microscopy. US Patent 5,170,286.
33. Zimmerberg, J., S.S. Vogel, and L.V. Chernomordik. 1993. Mechanisms of membrane fusion. Annu. Rev. Biophys. Biomol. Struct. 224: 33-66.
34. Zucker, R.S., and A.L. Fogelson. 1986. Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels. Proc. Natl. Acad. Sci. USA. 83: 3032-3036.