Adenosine triphosphate and the late steps in calcium-dependent exocytosis at a ribbon synapse

Journal of General Physiology

Volumn 111, Issue 2, 1998, Pages 225-241

  Heidelberger, Ruth ^a,b  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Exocytosis; Membrane fusion; MgATP; Priming; Synaptic vesicle

Indexed keywords

ADENOSINE TRIPHOSPHATE;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; EXOCYTOSIS; GOLDFISH; MEMBRANE FUSION; NONHUMAN; RETINA NERVE CELL; SYNAPSE VESICLE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CYTOSOL; ELECTROPHYSIOLOGY; EXOCYTOSIS; EYE; GOLDFISH; KINETICS; MAGNESIUM; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; PHOTOLYSIS; PRESYNAPTIC TERMINALS; SYNAPSES;

EID: 0031939868     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.111.2.225     Document Type: Article

References (65)

1. Adler, E.M., G.J. Augustine, S.N. Duffy, and M.P. Charlton. 1991. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J. Neurosci. 11:1496-1507.
2. Alvarez de Toledo, G., and J.M. Fernandez. 1990. Patch-clamp measurements reveal multimodal distribution of granule sizes in rat mast cells. J. Cell Biol. 110:1033-1039.
3. Armstrong, D., and R. Eckert. 1987. Voltage-activated calcium channel that must be phosphorylated to respond to membrane depolarization. Proc. Natl. Acad. Sci. USA. 84:2518-2522.
4. Armstrong, D.L., M.F. Rossier, A.D. Shcherbatko, and R.E. White. 1991. Enzymatic gating of voltage-activated calcium channels. In Calcium Entry and Action at the Presynaptic Nerve Terminal. E.F. Stanley, M.C. Nowycky, and D.J. Triggle, editors. Ann. NY Acad. Sci. 635:26-35.
5. Augustine, G.J., M.E. Burns, W.M. DeBello, D.L. Pettit, and F.E. Schweizer. 1996. Exocytosis: proteins and perturbations. Annu. Rev. Pharmacol. Toxicol. 36:659-701.
6. 2+-activated exocytosis. J. Biol. Chem. 271:20223-20226.
7. Bean, A.J., R. Seifert, Y.A. Chen, R. Sacks, and R.H. Scheller. 1997. Hrs-2 is an ATPase implicated in calcium-regulated secretion. Nature. 385:826-829.
8. Bittner, M.A., and R.W. Holz. 1992a. Kinetic analysis of secretion from permeabilized adrenal chromaffin cells reveals distinct components. J. Biol. Chem. 267:16219-16225.
9. Bittner, M.A., and R.W. Holz. 1992b. A temperature-sensitive step in exocytosis. J. Biol. Chem. 267:16226-16229.
10. Bunt, A.H. 1971. Enzymatic digestion of synaptic ribbons in amphibian retinal photoreceptors. Brain Res. 25:571-577.
11. Chad, J.E., and R. Eckert. 1986. An enzymatic mechanism for calcium current inactivation in dialyzed helix neurons. J. Physiol. (Camb.). 378:31-51.
12. Chow, R.H., L. von Rüden, and E. Neher. 1992. Delay in vesicle fusion revealed in electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature. 356:60-63.
13. Dowling, J.E. 1987. Wiring of the retina. In The Retina. An Approachable Part of the Brain. The Belknap Press of Harvard University Press, Cambridge, MA. 42-80.
14. Ellis-Davies, G.C.R., and J.H. Kaplan. 1994. Nitrophenyl-EGTA, a photolabile chelator that selectively binds Ca2+ with high affinity and releases it rapidly upon photolysis. Proc. Natl. Acad. Sci. USA. 91:187-191.
15. Fields, R.D., and M.H. Ellisman. 1985. Synaptic morphology and differences in sensitivity. Science. 228:197-199.
16. Gillis, K.D. 1995. Techniques for membrane capacitance measurements. In Single Channel Recording. 2nd ed. B. Sakmann and E. Neher, editors. Plenum Publishing Corp., New York. 155-198.
17. Gillis, K.D., R. Moesnner, and E. Neher. 1996. Protein kinase C enhances exocytosis from chromaffin cells by increasing the size of the readily releasable pool of secretory granules. Neuron. 16: 1209-1220.
18. Glick, B.S., and J.E. Rothman. 1987. Possible role for fatty acylcoenzyme A in intracellular protein transport. Nature. 326:309-312.
19. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:3440-3450.
20. 2+-activated secretion. Nature. 374:173-177.
21. Hay, J.C., and T.F.J. Martin. 1992. Resolution of regulated secretion into sequential MgATP-dependent and calcium-dependent stages mediated by distinct cytosolic proteins. J. Cell Biol. 119:139-151.
22. Heidelberger, R., C. Heinemann, E. Neher, and G. Matthews. 1994. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature. 371:513-515.
23. Heidelberger, R., and G. Matthews. 1992. Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. J. Physiol. 477:235-256.
24. Heidelberger, R., and G. Matthews. 1997. A requirement for MgATP in endocytosis and pool-refilling, but not in late steps of exocytosis. Biophys. J. 72:228a. (Abstr.)
25. 2+. Biophys. J. 67:2546-2557.
26. Holz, R.W., M.A. Bittner, S.C. Peppers, R.A. Senter, and D.A. Eberhard. 1989. MgATP-independent and MgATP-dependent exocytosis. J. Biol. Chem. 264:5412-5419.
27. Ishida, A.T., W.K. Stell, and D.A. Lightfoot. 1980. Rod and cone inputs to bipolar cells in goldfish retina. J. Comp. Neurol. 191:315-335.
28. Kaneko, A., and M. Tachibana. 1985. A voltage-clamp analysis of membrane currents in solitary bipolar cells dissociated from Carassius auratus. J. Physiol. (Camb.). 385:131-152.
29. Kaplan, J.H., and G.C.R. Ellis-Davies. 1988. Photolabile chelators for the rapid photorelease of divalent cations. Proc. Natl. Acad. Sci. USA. 85:6571-6575.
30. Koenig, J.H., T. Kosaka, and K. Ikeda. 1989. The relationship between the number of synaptic vesicles and the amount of transmitter released. J. Neurosci. 9:1937-1942.
31. Kumakura, K., K. Sasaki, T. Sakurai, M. Ohara-Imaizumi, H. Misonou, S. Nakamura, Y. Matsuda, and Y. Nonomura. 1994. Essential role of myosin light chain kinase in the mechanism for ATP-dependent priming of exocytosis in adrenal chromaffin cells. J. Neurosci. 14:7695-7703.
32. Lindau, M., and E. Neher. 1988. Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflügers Arch. 411:137-146.
33. Llinas, R., M. Sugimori, and R.B. Silver. 1992. Microdomains of high calcium concentration in a presynaptic terminal. Science. 256:677-679.
34. Marc, R.E., W.-L.S. Liu, M. Kalloniatis, S.F. Raiguel, and E. Van Haesendonck. 1990. Patterns of glutamate immunoreactivity in the goldfish retina. J. Neurosci. 10:4006-4034.
35. 2+-activated steps of dense core granule exocytosis. Cold Spring Harbor Symp. Quant. Biol. 60:197-204.
36. Mayer, A., W. Wickner, and A. Haas. 1996. Sec18p (NSF)-driven release of Sec17p (α-SNAP) can precede docking and fusion of yeast vacuoles. Cell. 85:83-94.
37. 2+ Complex. Biochemistry. 31:8856-8861.
38. Mennerick, S., and G. Matthews. 1996. Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron. 17:1241-1249.
39. Messler, P., H. Harz, and R. Uhl. 1996. Instrumentation for multiwavelengths excitation imaging. J. Neurosci. Methods. 69:137-147.
40. Neher, E., and R.S. Zucker. 1993. Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron. 10: 21-30.
41. Nichols, B.J., C. Ungermann, H.R.B. Pelham, W.T. Wickner, and A. Haas. 1997. Homotypic vacuolar fusion mediated by t-and v-SNAREs. Nature. 387:199-202.
42. 2+ compounds mimic the physiological stimulus for secretion? J. Physiol. Paris. 89:71-75.
43. Oberhauser, A.F., I.M. Robinson, and J.M. Fernandez. 1996. Simultaneous capacitance and amperometric measurements of exocytosis: a comparison. Biophys. J. 71:1131-1139.
44. Orci, L., V.M. Malhotra, M. Amherdt, T. Serafini, and J.E. Rothman. 1989. Dissection of a single round of vesicular transport: sequential intermediates for intercisternal movement in the golgi stack. Cell. 56:357-368.
45. Otto, H., P.I. Hanson, and R. Jahn. 1997. Assembly and disassembly of a ternary complex of synaptobrevin, syntaxin, and SNAP-25 in the membrane of synaptic vesicles. Proc. Natl. Acad. Sci. USA. 94: 6197-6120.
46. Parsons, T.D., J.R. Coorssen, H. Horstmann, and W. Almers. 1995. Docked granules, the exocytotic burst, and the need for ATP hydrolysis in endocrine cells. Neuron. 15:1085-1096.
47. Parsons, T.D., G.C.R. Ellis-Davis, and W. Almers. 1996. Millisecond studies of calcium-dependent exocytosis in pituitary melanotrophes: comparison of the photolabile calcium chelators nitrophenyl-EGTA and DM-nitrophen. Cell Calc. 19:185-192.
48. Raviola, E., and N.B. Gilula. 1975. Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. J. Cell Biol. 65:192-222.
49. Roberts, W.M., R.A. Jacobs, and A.J. Hudspeth. 1990. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J. Neurosci. 10:3664-3684.
50. Rothman, J.E. 1994. Mechanisms of intracellular protein transport. Nature. 372:55-63.
51. Rothman, J.E., and L. Orci. 1992. Molecular dissection of the secretory pathway. Nature. 355:409-415.
52. Smith, R.M., and A.E. Martell. 1989. Critical Stability Constants. Vol. 6, 2nd supplement. Plenum Publishing Corp., New York. pp. 288.
53. Söllner, T., M.K. Bennett, S.W. Whiteheart, R.H. Scheller, and J.E. Rothman. 1993b. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell. 75:409-418.
54. Söllner, T., S.W. Whiteheart, M. Brunner, H. Erdjument-Bromage, S. Geromanos, P. Tempst, and J.E. Rothman. 1993a. SNAP receptors implicated in vesicle targeting and fusion. Nature. 362:318-324.
55. Steyer, J.A., H. Horstmann, and W. Almers. 1997. Transport, docking and exocytosis of single secretory granules in live chrornaffin cells. Nature. 388:474-478.
56. Südhof, T.C. 1995. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature. 375:645-653.
57. Tachibana, M., and T. Okada. 1991. Release of endogenous excitatory amino acids from ON-type bipolar cells isolated from goldfish retina. J. Neurosci. 11:2199-2208.
58. Tachibana, M., T. Okada, T. Arimura, K. Kobayashi, and M. Piccolino. 1993. Dihydropyridine-sensitive calcium current mediates neurotransmitter release from bipolar cells of the goldfish retina. J. Neurosci. 13:2898-2909.
59. 2+ receptor controls the final steps in peptide secretion from pituitary melanotrophs. Neuron. 11:93-104.
60. Trube, G. 1979. Anion dependence of the contractions of skinned cardiac cells. Pflügers Arch. 379:121-123.
61. von Gersdorff, H., and G. Matthews. 1994. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature. 367:735-739.
62. von Gersdorff, H., and G. Matthews. 1996. Calcium-dependent inactivation of calcium current in synaptic terminals of retinal bipolar neurons. J. Neurosci. 15:115-122.
63. von Gersdorff, H., and G. Matthews. 1997. Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal. J. Neurosci. 17:1919-1927.
64. von Gersdorff, H., E. Vardi, G. Matthews, and P. Sterling. 1996. Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron. 16:1221-1227.
65. Walch-Solimena, C., J. Blasi, L., Edelmann, E.R. Chapman, G.F. von Mollard, and R. Jahn. 1995. The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling. J. Cell Biol. 128:637-645.