Live imaging of synaptic vesicle release and retrieval in dopaminergic neurons

Frontiers in Neural Circuits

Volumn 3, Issue JUN, 2009, Pages

  Mani, Meera ^a,b   Ryan, Timothy A ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Practices medicine and teaches at Weill Cornell Hospital   (United States)

Author keywords

Dopamine; Endocytosis; Exocytosis; Recycling; Synaptic vesicle

Indexed keywords

EID: 72149085931     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.04.003.2009     Document Type: Article

References (49)

1. Atluri, P. P., and Ryan, T. A. (2006). The kinetics of synaptic vesicle reacidification at hippocampal nerve terminals. J. Neurosci. 26, 2313-2320.
2. Balaji, J., Armbruster, M., and Ryan, T. A. (2008). Calcium control of endocytic capacity at a CNS synapse. J. Neurosci. 28, 6742-6749.
3. Baumert, M., Maycox, P. R., Navone, F., De Camilli, P., and Jahn, R. (1989). Synaptobrevin: an integral membrane protein of 18,000 daltons present in small synaptic vesicles of rat brain. EMBO J. 8, 379-384.
4. Betz, W. J., and Bewick, G. S. (1992). Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255, 200-203.
5. Bozza, T., McGann, J. P., Mombaerts, P., and Wachowiak, M. (2004). In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse. Neuron 42, 9-21.
6. 222dependence and time course of somatodendritic dopamine release: substantia nigra versus striatum. J. Neurosci. 21, 7841-7847.
7. Descarries, L., Berube-Carriere, N., Riad, M., Bo, G. D., Mendez, J. A., and Trudeau, L. E. (2008). Glutamate in dopamine neurons: synaptic versus diffuse transmission. Brain Res. Rev. 58, 290-302.
8. Di Paolo, G., Moskowitz, H. S., Gipson, K., Wenk, M. R., Voronov, S., Obayashi, M., Flavell, R., Fitzsimonds, R. M., Ryan, T. A., and De Camilli, P. (2004). Impaired PtdIns(4,5)P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking. Nature 431, 415-422.
9. Di Paolo, G., Sankaranarayanan, S., Wenk, M. R., Daniell, L., Perucco, E., Caldarone, B. J., Flavell, R., Picciotto, M. R., Ryan, T. A., Cremona, O., and De Camilli, P. (2002). Decreased synaptic vesicle recycling efficiency and cognitive deficits in amphiphysin 1 knockout mice. Neuron 33, 789-804.
10. Dittman, J. S., and Kaplan, J. M. (2006). Factors regulating the abundance and localization of synaptobrevin in the plasma membrane. Proc. Natl. Acad. Sci. USA 103, 11399-11404.
11. Ferguson, S. M., Brasnjo, G., Hayashi, M., Wolfel, M., Collesi, C., Giovedi, S., Raimondi, A., Gong, L. W., Ariel, P., Paradise, S., O'toole, E., Flavell, R., Cremona, O., Miesenbock, G., Ryan, T. A., and De Camilli, P. (2007). A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316, 570-574.
12. Fernández-Alfonso, T., and Ryan, T. A. (2004). The kinetics of synaptic vesicle pool depletion at CNS synaptic terminals. Neuron 41, 943-953.
13. Geffen, L. B., Jessell, T. M., Cuello, A. C., and Iversen, L. L. (1976). Release of dopamine from dendrites in rat substantia nigra. Nature 260, 258-260.
14. Grace, A. A., and Bunney, B. S. (1983). Intracellular and extracellular electrophysiology of nigral dopaminergic neurons-1. Identification and characterization. Neuroscience 10, 301-315.
15. Grace, A. A., and Bunney, B. S. (1984). The control of firing pattern in nigral dopamine neurons: single spike firing. J. Neurosci. 4, 2866-2876.
16. Grace A. A., and Onn, S. P. (1989). Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J. Neurosci. 9, 3463-3481.
17. Granseth, B., Odermatt, B., Royle, S. J., and Lagnado, L. (2006). Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51, 773-786.
18. Greengard, P. (2001). The neurobiology of slow synaptic transmission. Science 294, 1024-1030.
19. Jomphe, C., Bourque, M. J., Fortin, G. D., St-Gelais, F., Okano, H., Kobayashi, K., and Trudeau, L. E. (2005). Use of TH-EGFP transgenic mice as a source of identified dopaminergic neurons for physiological studies in postnatal cell culture. J. Neurosci. Methods 146, 1-12.
20. Khvotchev, M., and Kavalali, E. T. (2008). Pharmacology of neurotransmitter release: measuring exocytosis. Handb. Exp. Pharmacol. 184, 23-43.
21. Kim, W. T., Chang, S., Daniell, L., Cremona, O., Di Paolo, G., and De Camilli, P. (2002). Delayed reentry of recycling vesicles into the fusion-competent synaptic vesicle pool in synaptojanin 1 knockout mice. Proc. Natl. Acad. Sci. USA 99, 17143-17148.
22. Li, H., Waites, C. L., Staal, R. G., Dobryy, Y., Park, J., Sulzer, D. L., and Edwards, R. H. (2005). Sorting of vesicular monoamine transporter 2 to the regulated secretory pathway confers the somatodendritic exocytosis of monoamines. Neuron 48, 619-633.
23. Mani, M., Lee, S. Y., Lucast, L., Cremona, O., Di Paolo, G., De Camilli, P., and Ryan, T. A. (2007). The dual phosphatase activity of synaptojanin1 is required for both efficient synaptic vesicle endocytosis and reavailability at nerve terminals. Neuron 56, 1004-1018.
24. Markov, D., Mosharov, E. V., Setlik, W., Gershon, M. D., and Sulzer, D. (2008). Secretory vesicle rebound hyperacidification and increased quantal size resulting from prolonged methamphetamine exposure. J. Neurochem. 107, 1709-1721.
25. Maroteaux, L., Campanelli, J. T., and Scheller, R. H. (1988). Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J. Neurosci. 8, 2804-2815.
26. Miesenböck, G., De Angelis, D. A., and Rothman, J. E. (1998). Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192-195.
27. Mitchell, S. J., and Ryan, T. A. (2004). Syntaxin-1A is excluded from recycling synaptic vesicles at nerve terminals. J. Neurosci. 24, 4884-4888.
28. Mosharov, E. V., Gong, L. W., Khanna, B., Sulzer, D., and Lindau, M. (2003). Intracellular patch electrochemistry: regulation of cytosolic catecholamines in chromaffin cells. J. Neurosci. 23, 5835-5845.
29. Nicholson-Tomishima, K. and Ryan, T. A. (2004). Kinetic efficiency of endocytosis at mammalian CNS synapses requires synaptotagmin I. Proc. Natl. Acad. Sci. USA 101, 16648-16652.
30. Nirenberg, M. J., Chan, J., Liu, Y., Edwards, R. H., and Pickel, V. M. (1996). Ultrastructural localization of the vesicular monoamine transporter-2 in midbrain dopaminergic neurons: potential sites for somatodendritic storage and release of dopamine. J. Neurosci. 16, 4135-4145.
31. Pollard, H. B., Shindo, H., Creutz, C. E., Pazoles, C. J., and Cohen, J. S. (1979). Internal pH and state of ATP in adrenergic chromaffin granules determined by 31P nuclear magnetic resonance spectroscopy. J. Biol. Chem. 254, 1170-1177.
32. Poskanzer, K. E., Marek, K. W., Sweeney, S. T., and Davis, G. W. (2003). Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 426, 559-563.
33. Pothos, E. N., Davila, V., and Sulzer, D. (1998). Presynaptic recording of quanta from midbrain dopamine neurons and modulation of the quantal size. J. Neurosci. 18, 4106-4118.
34. Pothos, E. N., Mosharov, E., Liu, K. P., Setlik, W., Haburcak, M., Baldini, G., Gershon, M. D., Tamir, H., and Sulzer, D. (2002). Stimulation-dependent regulation of the pH, volume and quantal size of bovine and rodent secretory vesicles. J. Physiol. 542, 453-476.
35. Rayport, S., Sulzer, D., Shi, W. X., Sawasdikosol, S., Monaco, J., Batson, D., and Rajendran, G. (1992). Identified postnatal mesolimbic dopamine neurons in culture: morphology and electrophysiology. J. Neurosci. 12, 4264-4280.
36. Rice, M. E., Cragg, S. J., and Greenfield, S. A. (1997). Characteristics of electrically evoked somatodendritic dopamine release in substantia nigra and ventral tegmental area in vitro. J. Neurophysiol. 77, 853-862.
37. Ryan, T. A., and Smith, S. J. (1995). Vesicle pool mobilization during action potential firing at hippocampal synapses. Neuron 14, 983-989.
38. Sankaranarayanan, S., De Angelis, D., Rothman, J. E., and Ryan, T. A. (2000). The use of pHluorins for optical measurements of presynaptic activity. Biophys. J. 79, 2199-2208.
39. Sankaranarayanan, S., and Ryan, T. A. (2000). Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat. Cell Biol. 2, 197-204.
40. Sankaranarayanan, S., and Ryan, T. A. (2001). Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat. Neurosci. 4, 129-136.
41. Singleton, A. B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum, R., Lincoln, S., Crawley, A., Hanson, M., Maraganore, D., Adler, C., Cookson, M. R., Muenter, M., Baptista, M., Miller, D., Blancato, J., Hardy, J., and Gwinn-Hardy, K. (2003). Alpha-synuclein locus triplication causes Parkinson's disease. Science 302, 841.
42. Sollner, T., Whiteheart, S. W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P., and Rothman, J. E. (1993). SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324.
43. Spillantini, M. G., Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R., and Goedert, M. (1997). Alpha-synuclein in Lewy bodies. Nature 388, 839-840.
44. St-Gélais, F., Legault, M., Bourque, M. J., Rompre, P. P., and Trudeau, L. E. (2004). Role of calcium in neurotensin-evoked enhancement in firing in mesencephalic dopamine neurons. J. Neurosci. 24, 2566-2574.
45. Sulzer, D., and Rayport, S. (1990). Amphetamine and other psychostimulants reduce pH gradients in midbrain dopaminergic neurons and chromaffin granules: a mechanism of action. Neuron 5, 797-808.
46. Sulzer, D., Sonders, M. S., Poulsen, N. W., and Galli, A. (2005). Mechanisms of neurotransmitter release by amphetamines: a review. Prog. Neurobiol. 75, 406-433.
47. Tabares, L., Ruiz, R., Linares-Clemente, P., Gaffield, M. A., de Toledo, G. A., Fernandez-Chacon, R., and Betz, W. J. (2007). Monitoring synaptic function at the neuromuscular junction of a mouse expressing synaptopHluorin. J. Neurosci. 27, 5422-5430.
48. Vernier, P., Moret, F., Callier, S., Snapyan, M., Wersinger, C., and Sidhu, A. (2004). The degeneration of dopamine neurons in Parkinson's disease: insights from embryology and evolution of the mesostriatocortical system. Ann. NY Acad. Sci. 1035:231-249.
49. Wise, R. A. (2004). Dopamine, learning and motivation. Nat. Rev. Neurosci. 5, 483-494.