Dopamine neurons release transmitter via a flickering fusion pore

Nature Neuroscience

Volumn 7, Issue 4, 2004, Pages 341-346

  Staal, Roland G W ^a   Mosharov, Eugene V ^a,b   Sulzer, David ^a,b  

^a Howard Hughes Medical Institute   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON FIBER; DOPAMINE; NEUROTRANSMITTER; PHORBOL ESTER; STAUROSPORINE;

AMPEROMETRY; ANIMAL CELL; ARTICLE; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; EXOCYTOSIS; MEMBRANE FUSION; MESENCEPHALON; NERVE CELL CULTURE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE;

ANIMALS; DOPAMINE; ELECTROPHYSIOLOGY; EXOCYTOSIS; MESENCEPHALON; MODELS, NEUROLOGICAL; NEURONS; PROTEIN TRANSPORT; RATS; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 1842612454     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1205     Document Type: Article

References (48)

1. Valtorta, F., Meldolesi, J. & Fesce, R. Synaptic vesicles: is kissing a matter of competence? Trends Cell Biol. 11, 324-328 (2001).
2. Heuser, J.E. & Reese, T.S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315-344 (1973).
3. Ceccarelli, B., Hurlbut, W.P. & Mauro, A. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J. Cell Biol. 57, 499-524 (1973).
4. Sun, J.Y., Wu, X.S. & Wu, L.G. Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature 417, 555-559 (2002).
5. Klyachko, V.A. & Jackson, M.B. Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature 418, 89-92 (2002).
6. Henkel, A.W. & Betz, W.J. Staurosporine blocks evoked release of FM1-43 but not acetylcholine from frog motor nerve terminals. J. Neurosci. 15, 8246-8258 (1995).
7. Gandhi, S.P. & Stevens, C.F. Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423, 607-613 (2003).
8. Aravanis, A.M., Pyle, J.L. & Tsien, R.W. Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 423, 643-647 (2003).
9. Stiles, J.R., Van Helden, D., Bartol, T.M. Jr., Salpeter, E.E. & Salpeter, M.M. Miniature endplate current rise times less than 100 microseconds from improved dual recordings can be modeled with passive acetylcholine diffusion from a synaptic vesicle. Proc. Natl. Acad. Sci. USA 93, 5747-5752 (1996).
10. Pothos, E.N., Davila, V. & Sulzer, D. Presynaptic recording of quanta from midbrain dopamine neurons and modulation of the quantal size. J. Neurosci. 18, 4106-4118 (1998).
11. Pothos, E.N. et al. Synaptic vesicle transporter expression regulates vesicle phenotype and quantal size. J. Neurosci. 20, 7297-7306 (2000).
12. Bittner, M.A. Alpha-latrotoxin and its receptors CIRL (latrophilin) and neurexin 1 alpha mediate effects on secretion through multiple mechanisms. Biochimie 82, 447-452 (2000).
13. Bruns, D. & Jahn, R. Real-time measurement of transmitter release from single synaptic vesicles. Nature 377, 62-65 (1995).
14. Hochstetler, S.E., Puopolo, M., Gustincich, S., Raviola, E. & Wightman, R.M. Real-time amperometric measurements of zeptomole quantities of dopamine released from neurons. Anal. Chem. 72, 489-496 (2000).
15. Hartmann, J., Scepek, S. & Lindau, M. Regulation of granule size in human and horse eosinophils by number of fusion events among unit granules. J. Physiol. (Lond.) 483, 201-209 (1995).
16. Lollike, K., Borregaard, N. & Lindau, M. The exocytotic fusion pore of small granules has a conductance similar to an ion channel. J. Cell Biol. 129, 99-104 (1995).
17. Albillos, A. et al. The exocytic event in chromaffin cells revealed by patch amperometry. Nature 389, 509-512 (1997).
18. Betz, A. et al. Munc13-1 is a presynaptic phorbol ester receptor that enhances neurotransmitter release. Neuron 21, 123-136 (1998).
19. Rhee, J.S. et al. Beta phorbol ester- and diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108, 121-133 (2002).
20. Zhu, H., Hille, B. & Xu, T. Sensitization of regulated exocytosis by protein kinase C. Proc. Natl. Acad. Sci. USA 99, 17055-17059 (2002).
21. 2+-sensitive pool of vesicles is regulated by protein kinase C in adrenal chromaffin cells. Proc. Natl. Acad. Sci. USA 99, 17060-17065 (2002).
22. Wang, P., Wang, C.T., Bai, J., Jackson, M.B. & Chapman, E.R. Mutations in the effector binding loops in the C2A and C2B domains of synaptotagmin I disrupt exocytosis in a nonadditive manner. J. Biol. Chem. 278, 47030-47037 (2003).
23. Graham, M.E., Fisher, R.J. & Burgoyne, R.D. Measurement of exocytosis by amperometry in adrenal chromaffin cells: effects of clostridial neurotoxins and activation of protein kinase C on fusion pore kinetics. Biochimie 82, 469-479 (2000).
24. 2+ and protein kinase C via distinct mechanisms. EMBO J. 17, 4340-4345 (1998).
25. Gillis, K.D., Mossner, R. & Neher, E. Protein kinase C enhances exocytosis from chromaffin cells by increasing the size of the readily releasable pool of secretory granules. Neuron 16, 1209-1220 (1996).
26. Wightman, R.M. et al. Temporally resolved catecholamine spikes correspond to single vesicle release from individual chromaffin cells. Proc. Natl. Acad. Sci. USA 88, 10754-10758 (1991).
27. Chen, G., Gavin, P.F., Luo, G. & Ewing, A.G. Observation and quantitation of exocytosis from the cell body of a fully developed neuron in Planorbis corneus. J. Neurosci. 15, 7747-7755 (1995).
28. Jaffe, E.H., Marty, A., Schulte, A. & Chow, R.H. Extrasynaptic vesicular transmitter release from the somata of substantia nigra neurons in rat midbrain slices. J. Neurosci. 18, 3548-3553 (1998).
29. Girod, R., Correges, P., Jacquet, J. & Dunant, Y. Space and time characteristics of transmitter release at the nerve-electroplaque junction of Torpedo. J. Physiol. 471, 129-157 (1993).
30. Hafez, I., Stolpe, A. & Lindau, M. Compound exocytosis and cumulative fusion in eosinophils. J. Biol. Chem. 278, 44921-44928 (2003).
31. Alvarez de Toledo, G., Fernandez-Chacon, R. & Fernandez, J.M. Release of secretory products during transient vesicle fusion. Nature 363, 554-558 (1993).
32. Zhou, Z., Misler, S. & Chow, R.H. Rapid fluctuations in transmitter release from single vesicles in bovine adrenal chromaffin cells. Biophys. J. 70, 1543-1552 (1996).
33. Cremona, O. & De Camilli, P. Synaptic vesicle endocytosis. Curr. Opin. Neurobiol. 7, 323 (1997).
34. Pickel, V.M., Nirenberg, M.J. & Milner, T.A. Ultrastructural view of central catecholaminergic transmission: immunocytochemical localization of synthesizing enzymes, transporters and receptors. J. Neurocytol. 25, 843-856 (1996).
35. Garris, P.A., Ciolkowski, E.L., Pastore, P. & Wightman, R.M. Efflux of dopamine from the synaptic cleft in the nucleus accumbens of the rat brain. J. Neurosci. 14, 6084-6093 (1994).
36. Schmitz, Y., Benoit-Marand, M., Gonon, F. & Sulzer, D. Presynaptic plasticity of dopaminergic neurotransmission. J. Neurochem. 87, 273-289 (2003).
37. Gonon, F. et al. Geometry and kinetics of dopaminergic transmission in the rat striatum and in mice lacking the dopamine transporter. Prog. Brain Res. 125, 291-302 (2000).
38. Sulzer, D. & Pothos, E.N. Presynaptic mechanisms that regulate quantal size. Rev. Neurosci. 11, 159-212 (2000).
39. Cragg, S.J., Nicholson, C., Kume-Kick, J., Tao, L. & Rice, M.E. Dopamine-mediated volume transmission in midbrain is regulated by distinct extracellular geometry and uptake. J. Neurophysiol. 85, 1761-1771 (2001).
40. Pothos, E.N., Przedborski, S., Davila, V., Schmitz, Y. & Sulzer, D. D2-Like dopamine autoreceptor activation reduces quantal size in PC12 cells. J. Neurosci. 18, 5575-5585 (1998).
41. Colquhoun, D. & Sigworth, F.J. Fitting and statistical analysis of single-channel records. in Single-Channel Recording (eds. Sakmann, B. & Neher, E.) 483-587 (Plenum, New York, 1995).
42. Colliver, T., Hess, E., Pothos, E.N., Sulzer, D. & Ewing, A.G. Quantitative and statistical analysis of the shape of amperometric spikes recorded from two populations of cells. J. Neurochem. 74, 1086-1097 (1999).
43. Berg, H.C. Random Walks in Biology 152 (Princeton Univ. Press, Princeton, 1983).
44. Nicholson, C. Diffusion of ions and macromolecules in brain tissue. in Monitoring Molecules in Neuroscience Vol. 8 (eds. Rollema, H., Abercrombie, E., Sulzer, D. & Zackheim, J.) 71-73 (Rutgers Press, Newark, New Jersey, 1999).
45. Jeremic, A., Kelly, M., Choo, S.J., Stromer, M.H. & Jena, B.P. Reconstituted fusion pore. Biophys. J. 85, 2035-2043 (2003).
46. Rice, M.E. et al. Direct monitoring of dopamine and 5-HT release in substantia nigra and ventral tegmental area in vitro. Exp. Brain Res. 100, 395-406 (1994).
47. Schmitz, Y., Lee, C.J., Schmauss, C., Gonon, F. & Sulzer, D. Amphetamine distorts synaptic dopamine overflow: effects on D2 autoreceptors, transporters, and synaptic vesicle stores. J. Neurosci. 21, 5916-5924 (2001).
48. Levant, B. The D3 dopamine receptor: neurobiology and potential clinical relevance. Pharmacol. Rev. 49, 231-252 (1997).