Quantitative investigations of amperometric spike feet suggest different controlling factors of the fusion pore in exocytosis at chromaffin cells

Biophysical Chemistry

Volumn 143, Issue 3, 2009, Pages 124-131

  Amatore, Christian ^a   Arbault, Stéphane ^a   Bonifas, Imelda ^a   Guille, Manon ^a  

^a Centre National de la Recherche Scientifique   (France)

Author keywords

Amperometry; Carbon fiber microelectrode; Chromaffin cell; Exocytosis; Foot; Pre spike feature

Indexed keywords

BARIUM ION; CARBON FIBER; CATECHOLAMINE; NEUROTRANSMITTER; POTASSIUM ION;

AMPEROMETRY; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL STIMULATION; CHROMAFFIN CELL; CONTROLLED STUDY; CORRELATION ANALYSIS; EXOCYTOSIS; MICROELECTRODE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROBABILITY; QUANTITATIVE ANALYSIS; REPRODUCIBILITY; SECRETORY VESICLE; SPIKE WAVE;

ANIMALS; BARIUM; CATECHOLAMINES; CATTLE; CELL FUSION; CELL MEMBRANE; CELLS, CULTURED; CHROMAFFIN CELLS; ELECTRODES; EXOCYTOSIS; KINETICS; NEUROTRANSMITTER AGENTS; POTASSIUM; SECRETORY VESICLES;

BOVINAE;

EID: 67349168757     PISSN: 03014622     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bpc.2009.04.007     Document Type: Article

References (53)

1. Sudhof T.C. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27 (2004) 509-547
2. Wang Y., and Tang B.L. SNAREs in neurons - beyond synaptic vesicle exocytosis (Review). Mol. Memb. Biol. 23 (2006) 377-384
3. Lieberman J. The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nat. Rev. Immunol. 3 (2003) 361-370
4. Hong W.J. Cytotoxic T lymphocyte exocytosis: bring on the SNAREs. Trends Cell Biol. 15 (2005) 644-650
5. Burgoyne R.D., and Morgan A. Secretory granule exocytosis. Physiol. Rev. 83 (2003) 581-632
6. An S., and Zenisek D. Regulation of exocytosis in neurons and neuroendocrine cells. Curr. Opin. Neurobiol. 14 (2004) 522-530
7. Lindau M., and de Toledo G.A. The fusion pore. Biochim. Biophys. Acta, Mol. Cell Res. 1641 (2003) 167-173
8. Fernandez-Peruchena C., Navas S., Montes M.A., and de Toledo G.A. Fusion pore regulation of transmitter release. Brains Res. Rev. 49 (2005) 406-415
9. de Toledo G.A., Fernandez-Chacon R., and Fernandez J.M. Release of secretory products during transient vesicle fusion. Nature 363 (1993) 554-558
10. Albillos A., Dernick G., Horstmann H., Almers W., de Toledo G.A., and Lindau M. The exocytotic event in chromaffin cells revealed by patch amperometry. Nature 389 (1997) 509-512
11. Zenisek D., Steyer J.A., and Almers W. Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406 (2000) 849-854
12. Takahashi N., Kishimoto T., Nemoto T., Kadowaki T., and Kasai H. Fusion pore dynamics and insulin granule exocytosis in the pancreatic islet. Science 297 (2002) 1349-1352
13. Kasai H., Kishimoto T., Nemoto T., Hatakeyama H., Liu T.T., and Takahashi N. Two-photon excitation imaging of exocytosis and endocytosis and determination of their spatial organization. Adv. Drug Deliv. Rev. 58 (2006) 850-877
14. Schroeder T.J., Jankowski J.A., Kawagoe K.T., Wightman R.M., Lefrou C., and Amatore C. Analysis of diffusional broadening of vesicular packets of catecholamines released from biological cells during exocytosis. Anal. Chem. 64 (1992) 3077-3083
15. Wightman R.M., Jankowski J.A., Kennedy R.T., Kawagoe K.T., Schroeder T.J., Leszczyszyn D.J., Near J.A., Diliberto E.J., and Viveros O.H. Temporally resolved catecholamine spikes correspond to single vesicle release from individual chromaffin cells. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 10754-10758
16. Dernick G., Gong L.W., Tabares L., de Toledo G.A., and Lindau M. Patch amperometry: high-resolution measurements of single-vesicle fusion and release. Nat. Methods 2 (2005) 699-708
17. Wightman R.M., Schroeder T.J., Finnegan J.M., Ciolkowski E.L., and Pihel K. Time-course of release of catecholamines from individual vesicles during exocytosis at adrenal-medullary cells. Biophys. J. 68 (1995) 383-390
18. Chow R.H., Vonruden L., and Neher E. Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature 356 (1992) 60-63
19. Zhou Z., Misler S., and Chow R.H. Rapid fluctuations in transmitter release from single vesicles in bovine adrenal chromaffin cells. Biophys. J. 70 (1996) 1543-1552
20. Sombers L.A., Hanchar H.J., Colliver T.L., Wittenberg N., Cans A., Arbault S., Amatore C., and Ewing A.G. The effects of vesicular volume on secretion through the fusion pore in exocytotic release from PC12 cells. J. Neurosci. 24 (2004) 303-309
21. Mosharov E.V., and Sulzer D. Analysis of exocytotic events recorded by amperometry. Nat. Methods 2 (2005) 651-658
22. Amatore C., Arbault S., Bonifas I., Bouret Y., Erard M., Ewing A.G., and Sombers L.A. Correlation between vesicle quantal size and fusion pore release in chromaffin cell exocytosis. Biophys. J. 88 (2005) 4411-4420
23. Grabner C.P., Price S.D., Lysakowski A., and Fox A.P. Mouse chromaffin cells have two populations of dense core vesicles. J. Neurophysiol. 94 (2005) 2093-2104
24. Amatore C., Bouret Y., and Midrier L. Time-resolved dynamics of the vesicle membrane during individual exocytotic secretion events, as extracted from amperometric monitoring of adrenaline exocytosis from chromaffin cells. Chem. Eur. J. 5 (1999) 2151-2162
25. Sulzer D., and Pothos E.N. Regulation of quantal size by presynaptic mechanisms. Rev. Neurosci. 11 (2000) 159-212
26. Gong L.W., Hafez I., de Toledo G.A., and Lindau M. Secretory vesicles membrane area is regulated in tandem with quantal size in chromaffin cells. J. Neurosci. 23 (2003) 7917-7921
27. Colliver T.L., Pyott S.J., Achalabun M., and Ewing A.G. VMAT-mediated changes in quantal size and vesicular volume. J. Neurosci. 20 (2000) 5276-5282
28. Schroeder T.J., Borges R., Finnegan J.M., Pihel K., Amatore C., and Wightman R.M. Temporally resolved, independent stages of individual exocytotic secretion events. Biophys. J. 70 (1996) 1061-1068
29. Amatore C., Arbault S., Bonifas I., Bouret Y., Erard M., and Guille M. Dynamics of full fusion during vesicular exocytotic events: release of adrenaline by chromaffin cells. Chem. Phys. Chem. 4 (2003) 147-154
30. Amatore C., Arbault S., Bouret Y., Guille M., Lemaître F., and Verchier Y. Invariance of exocytotic events detected by amperometry as a function of the carbon fiber microelectrode diameter. Anal. Chem. 8 (2009) 3087-3093
31. Burgoyne R.D., and Barclay J.W. Splitting the quantum: regulation of quantal release during vesicle fusion. Trends Neurosci. 25 (2002) 176-178
32. Jahn R., and Scheller R.H. SNAREs - engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7 (2006) 631-643
33. Zimmerberg J., and Gawrisch K. The physical chemistry of biological membranes. Nat. Chem. Biol. 2 (2006) 564-567
34. Martens S., and McMahon H.T. Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 9 (2008) 543-556
35. Neher E. Cell physiology - secretion without full fusion. Nature 363 (1993) 497-498
36. Ales E., Tabares L., Poyato J.M., Valero V., Lindau M., and de Toledo G.A. High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat. Cell Biol. 1 (1999) 40-44
37. Amatore C., Arbault S., Guille M., and Lemaitre F. Electrochemical monitoring of single cell secretion: vesicular exocytosis and oxidative stress. Chem. Rev. 108 (2008) 2585-2621
38. Amatore C., Arbault S., Guille M., and Lemaître F. The nature and efficiency of neurotransmitter exocytosis also depend on physicochemical parameters. Chem. Phys. Chem. 8 (2007) 1597-1605
39. Pihel K., Hsieh S., Jorgenson J.W., and Wightman R.M. Electrochemical detection of histamine and 5-hydroxytryptamine at isolated mast-cells. Anal. Chem. 67 (1995) 4514-4521
40. Arbault S., Pantano P., Jankowski J.A., Vuillaume M., and Amatore C. Monitoring an oxidative stress mechanism at a single human fibroblast. Anal. Chem. 67 (1995) 3382-3390
41. Finnegan J.M., Pihel K., Cahill P.S., Huang L., Zerby S.E., Ewing A.G., Kennedy R.T., and Wightman R.M. Vesicular quantal size measured by amperometry at chromaffin, mast, pheochromocytoma, and pancreatic beta-cells. J. Neurochem. 66 (1996) 1914-1923
42. Ciolkowski E.L., Maness K.M., Cahill P.S., Wightman R.M., Evans D.H., Fosset B., and Amatore C. Disproportionation during electrooxidation of catecholamines at carbon-fiber microelectrodes. Anal. Chem. 66 (1994) 3611-3617
43. Wang C.T., Grishanin R., Earles C.A., Chang P.Y., Martin T.F.J., Chapman E.R., and Jackson M.B. Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 294 (2001) 1111-1115
44. Jackson M.B., and Chapman E.R. Fusion pores and fusion machines in Ca2+-triggered exocytosis. Annu. Rev. Biophys. Biomol. Struct. 35 (2006) 135-160
45. Detoledo G.A., and Fernandez J.M. Compound versus multigranular exocytosis in peritoneal mast-cells. J. Gen. Physiol. 95 (1990) 397-409
46. Hafez I., Stolpe A., and Lindau M. Compound exocytosis and cumulative fusion in eosinophils. J. Biol. Chem. 278 (2003) 44921-44928
47. Pickett J.A., and Edwardson J.M. Compound exocytosis: mechanisms and functional significance. Traffic 7 (2006) 109-116
48. Rizzoli S.O., and Jahn R. Kiss-and-run, collapse and 'Readily Retrievable' vesicles. Traffic 8 (2007) 1137-1144
49. Jankowski J.A., Finnegan J.M., and Wightman R.M. Extracellular ionic composition alters kinetics of vesicular release of catecholamines and quantal size during exocytosis at adrenal-medullary cells. J. Neurochem. 63 (1994) 1739-1747
50. Amatore C., Arbault S., Bouret Y., Guille M., Lemaitre F., and Verchier Y. Regulation of exocytosis in chromaffin cells by trans-insertion of lysophosphatidylcholine and arachidonic acid into the outer leaflet of the cell membrane. Chembiochem 7 (2006) 1998-2003
51. Amatore C., Bouret Y., Travis E.R., and Wightman R.M. Interplay between membrane dynamics, diffusion and swelling pressure governs individual vesicular exocytotic events during release of adrenaline by chromaffin cells. Biochimie 82 (2000) 481-496
52. Amatore C., Arbault S., Bonifas I., Guille M., Lemaître F., and Verchier Y. Relationship between amperometric pre-spike feet and secretion granule composition in chromaffin cells: an overview. Biophys. Chem. 129 (2007) 181-189
53. Livett B.G. Adrenal-medullary chromaffin cells-in vitro. Physiol. Rev. 64 (1984) 1103-1161