Double patch clamp reveals that transient fusion (kiss-and-run) is a major mechanism of secretion in calf adrenal chromaffin cells: High calcium shifts the mechanism from kiss-and-run to complete fusion

Journal of Neuroscience

Volumn 26, Issue 11, 2006, Pages 3030-3036

  Elhamdani, Abdeladim ^a   Azizi, Fouad ^a   Artalejo, Cristina R ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chromaffin cell; Endocytosis; Exocytosis; Fusion pore; Kiss and run; Membrane capacitance

Indexed keywords

CALCIUM;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CATTLE; CELL FUSION; CELL SECRETION; CHROMAFFIN CELL; ENDOCYTOSIS; INCIDENCE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; TRANSIENT FUSION;

ACTION POTENTIALS; ADRENAL MEDULLA; ANIMALS; BARIUM; CALCIUM; CATTLE; CELL MEMBRANE; CHROMAFFIN CELLS; ELECTRIC CAPACITANCE; ELECTRIC STIMULATION; ENDOCYTOSIS; EXOCYTOSIS; INTRACELLULAR MEMBRANES; MEMBRANE FUSION; MODELS, BIOLOGICAL; PATCH-CLAMP TECHNIQUES; SECRETORY VESICLES; STRONTIUM;

EID: 33644993894     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5275-05.2006     Document Type: Article

References (43)

1. Alés E, Tabares L, Poyato JM, Valero V, Lindau M, Alvarez de Toledo G (1999) High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat Cell Biol 1:40-44.
2. Alvarez de Toledo G, Fernandez-Chacon R, Fernandez JM (1993) Release of secretory products during transient vesicle fusion. Nature 363:554-558.
3. Aravanis AM, Payle JL, Harata NC, Tsien RW (2003) Imaging single synaptic vesicles undergoing repeated fusion events: kissing, running, and kissing again. Neuropharmacology 45:797-813.
4. 2+, GTP and dynamin but not clathrin. Proc Natl Acad Sci USA 92:8328-8332.
5. Artalejo CR, Elhamdani A, Palfrey HC (1996) Calmodulin is the divalent cation receptor for rapid endocytosis, but not exocytosis, in adrenal chromaffin cells. Neuron 16:195-205.
6. Artalejo CR, Elhamdani A, Palfrey HC (1998) Secretion: dense-core vesicles can kiss-and-run too! Curr Biol 8:R62-R65.
7. Artalejo CR, Elhamdani A, Palfrey HC (2002) Sustained stimulation shifts the mechanism of endocytosis from dynamin-1-dependent rapid endocytosis to clathrin- and dynamin-2-mediated slow endocytosis in chromaffin cells. Proc Natl Acad Sci USA 99:6358-6363.
8. Ceccarelli B, Hurlbut WP, Mauro A (1973) Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol 57:499-524.
9. Choi S, Klingauf J, Tsien RW (2000) Postfusional regulation of cleft glutamate concentration during LTP at "silent synapses." Nat Neurosci 3:330-336.
10. Debus K, Lindau M (2000) Resolution of patch capacitance recordings and fusion pore conductances in small vesicles. Biophys J 78:2983-2997.
11. De Camilli P, Slepnev VI, Shupliakov O, Brodin L (2000) Synaptic vesicle endocytosis. In: Synapses (Cowan WM, Südhof TC, Stevens CF, eds), pp 217-274. Baltimore: Johns Hopkins UP.
12. Del Castillo J, Katz B (1954) Quantal components of the end-plate potential. J Physiol (Lond) 124:560-573.
13. Dernick G, Alvarez de Toledo G, Lindau M (2003) Exocytosis of single chromaffin granules in cell-free inside-out membrane patches. Nat Cell Biol 5:358-362.
14. Dickman DK, Horne JA, Meinertzhagen IA, Schwarz TL (2005) A slowed classical pathway rather than kiss-and-run mediates endocytosis at synapses lacking synaptojanin and endophilin. Cell 123:521-533.
15. Duncan RR, Greaves J, Wiegand UK, Matskevich L, Bodammer G, Apps DK, Shipston MJ, Chow RH (2003) Functional and spatial segregation of secretory vesicle pools according to vesicle age. Nature 422:176-180.
16. Elhamdani A, Zhou Z, Artalejo CR (1998) Timing of dense-core vesicle exocytosis depends on the facilitation L-type Ca channel in adrenal chromaffin cells. J Neurosci 18:6230-6240.
17. Elhamdani A, Martin TFJ, Kowalchyk JA, Artalejo CR (1999) CAPS (Ca-dependent activator protein for secretion) is critical for the fusion of dense-core vesicles with the membrane in calf adrenal chromaffin cells. J Neurosci 19:7375-7383.
18. Elhamdani A, Palfrey HC, Artalejo CR (2001) Quantal size is dependent on stimulation frequency and calcium entry in calf chromaffin cells. Neuron 31:819-830.
19. Fernandez JM, Neher E, Gomperts BD (1984) Capacitance measurements reveal stepwise fusion events in degranulating mast cells. Nature 312:453-455.
20. Fulop T, Radabaugh S, Smith C (2005) Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. J Neurosci 25:7324-7332.
21. Gandhi SP, Stevens CF (2003) Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423:607-613.
22. Graham ME, O'Callaghan DW, McMahon HT, Burgoyne RD (2002) Dynamin-dependent and dynamin-independent processes contribute to the regulation of single vesicle release kinetics and quantal size. Proc Natl Acad Sci USA 99:7124-7129.
23. 2+-triggered exocytosis. Science 304:289-292.
24. Henkel AW, Meiri H, Horstmann H, Lindau M, Almers W (2000) Rhythmic opening and closing of vesicles during constitutive exo- and endocytosis in chromaffin cells. EMBO J 19:84-93.
25. Heuser JE, Reese TS (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 133:315-344.
26. Holroyd P, Lang T, Wenzel D, De Camilli P, Jahn R (2002) Imaging direct, dynamin-dependent recapture of fusing secretory granules on plasma membrane lawns from PC12 cells. Proc Natl Acad Sci USA 24:16806-16811.
27. Klyachko VA, Jackson MB (2002) Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature 418:89-92.
28. Krupa B, Liu G (2004) Does the fusion pore contribute to synaptic plasticity? Trends Neurosci 27:62-66.
29. Kuromi H, Kidokoro Y (1999) The optically determined size of exo/endo cycling vesicle pool correlates with the quantal content at the neuromuscular junction of Drosophila larvae. J Neurosci 19:1557-1565.
30. Kuromi H, Yoshihara M, Kidokoro Y (1997) An inhibitory role of calcineurin in endocytosis of synaptic vesicles at larvae. Neurosci Res 27:101-113.
31. Li Z, Burrone J, Tyler WJ, Hartman KN, Albeanu DF, Murthy VN (2005) Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin. Proc Natl Acad Sci USA 102:6131-6136.
32. Murthy VN, De Camilli P (2003) Cell biology of the presynaptic terminal. Annu Rev Neurosci 26:701-728.
33. Neher E, Marty A (1982) Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc Natl Acad Sci USA 79:6712-6716.
34. Ornberg RL, Furuya S, Goping G, Kuijpers GA (1995) Granule swelling in stimulated bovine adrenal chromaffin cells: regulation by internal granule pH. Cell Tissue Res 279:85-92.
35. Palfrey HC, Artalejo CR (1998) Vesicle recycling revisited: rapid endocytosis may be the first step. Neuroscience 83:969-989.
36. Pawlu C, DiAntonio A, Heckmann M (2004) Postfusional control of quantal current shape. Neuron 42:607-618.
37. Renger JJ, Egles C, Liu G (2001) A developmental switch in neurotransmitter flux enhances synaptic efficacy by affecting AMPA receptor activation. Neuron 29:469-484.
38. Richards DA, Bai J, Chapman ER (2005) Two modes of exocytosis at hippocampal synapses revealed by rate of FM1-43 efflux from individual vesicles. J Cell Biol 168:929-939.
39. Staal RG, Mosharov EV, Sulzer D (2004) Dopamine neurons release transmitter via a flickering fusion pore. Nat Neurosci 7:341-346.
40. Stevens CF, Williams JH (2000) "Kiss and run" exocytosis at hippocampal synapses. Proc Natl Acad Sci USA 97:12828-12833.
41. Südhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509-547.
42. Taraska JW, Perrais D, Ohara-Imaizumi M, Nagamatsu S, Almers W (2003) Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells. Proc Natl Acad Sci USA 100 :2070-2075.
43. Zakharenko SS, Zablow L, Siegelbaum SA (2002) Altered presynaptic vesicle release and cycling during mGluR-dependent LTD. Neuron 35:1099-1110.