Sharing vesicles between central presynaptic terminals: Implications for synaptic function

Frontiers in Synaptic Neuroscience

Volumn , Issue JUN, 2010, Pages

  Staras, Kevin ^a   Branco, Tiago ^b,c  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Imaging; Neuron; Presynaptic terminal; Synaptic transmission; Synaptic vesicle

Indexed keywords

CADHERIN; CATENIN;

DENDRITE; ENDOCYTOSIS; HIPPOCAMPAL CA3 REGION; NERVE CELL PLASTICITY; NERVE FIBER; PRESYNAPTIC POTENTIAL; REVIEW; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

EID: 81255141537     PISSN: None     EISSN: 16633563     Source Type: Journal    
DOI: 10.3389/fnsyn.2010.00020     Document Type: Review

References (79)

1. Ahmari, S. E., Buchanan, J., and Smith, S. J. (2000). Assembly of presynaptic active zones from cytoplasmic transport packets. Nat. Neurosci. 3, 445-451.
2. Antonova, I., Arancio, O., Trillat, A. C., Wang, H. G., Zablow, L., Udo, H., Kandel, E. R., and Hawkins, R. D. (2001). Rapid increase in clusters of presynaptic proteins at onset of long-lasting potentiation. Science 294, 1547-1550.
3. Aravanis, A. M., Pyle, J. L., and Tsien, R. W. (2003). Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 423, 643-647.
4. Bamji, S. X., Rico, B., Kimes, N., and Reichardt, L. F. (2006). BDNF mobilizes synaptic vesicles and enhances synapse formation by disrupting cadherin-beta-catenin interactions. J. Cell Biol. 174, 289-299.
5. Bamji, S. X., Shimazu, K., Kimes, N., Huelsken, J., Birchmeier, W., Lu, B., and Reichardt, L. F. (2003). Role of beta-catenin in synaptic vesicle localization and presynaptic assembly. Neuron 40, 719-731.
6. Bats, C., Groc, L., and Choquet, D. (2007). The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 53, 719-734.
7. Betz, W. J., and Bewick, G. S. (1992). Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255, 200-203.
8. Branco, T., Marra, V., and Staras, K. (2010). Examining size-strength relationships at hippocampal synapses using an ultrastructural measurement of synaptic release probability. J. Struct. Biol. http://dx.doi.org/10.1016/j.jsb.2009.10.014.
9. Branco, T., and Staras, K. (2009). The probability of neurotransmitter release: variability and feedback control at single synapses. Nat. Rev. Neurosci. 10, 373-383.
10. Branco, T., Staras, K., Darcy, K. J., and Goda, Y. (2008). Local dendritic activity sets release probability at hippocampal synapses. Neuron 59, 475-485.
11. Brown, A. (2003). Axonal transport of membranous and nonmembranous cargoes: a unified perspective. J. Cell Biol. 160, 817-821.
12. Ceccarelli, B., Hurlbut, W. P., and Mauro, A. (1973). Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J. Cell Biol. 57, 499-524.
13. Chen, X., Barg, S., and Almers, W. (2008). Release of the styryl dyes from single synaptic vesicles in hippocampal neurons. J. Neurosci. 28, 1894-1903.
14. Colicos, M. A., Collins, B. E., Sailor, M. J., and Goda, Y. (2001). Remodeling of synaptic actin induced by photoconductive stimulation. Cell 107, 605-616.
15. Darcy, K. J., Staras, K., Collinson, L. M., and Goda, Y. (2006a). Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat. Neurosci. 9, 315-321.
16. Darcy, K. J., Staras, K., Collinson, L. M., and Goda, Y. (2006b). An ultrastructural readout of fluorescence recovery after photobleaching using correlative light and electron microscopy. Nat. Protoc. 1, 988-994.
17. De Paola, V., Holtmaat, A., Knott, G., Song, S., Wilbrecht, L., Caroni, P., and Svoboda, K. (2006). Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron 49, 861-875.
18. De Robertis, E. D., and Bennett, H. S. (1954). A submicroscopic vesicular component of Schwann cells and nerve satellite cells. Exp. Cell Res. 6, 543-545.
19. De Robertis, E. D., and Bennett, H. S. (1955). Some features of the submicroscopic morphology of synapses in frog and earthworm. J. Biophys. Biochem. Cytol. 1, 47-58.
20. Fernandez-Alfonso, T., and Ryan, T. A. (2006). The efficiency of the synaptic vesicle cycle at central nervous system synapses. Trends Cell Biol. 16, 413-420.
21. Fernandez-Alfonso, T., and Ryan, T. A. (2008). A heterogeneous " resting" pool of synaptic vesicles that is dynamically interchanged across boutons in mammalian CNS synapses. Brain Cell Biol. 36, 87-100.
22. Fredj, N. B., and Burrone, J. (2009). A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat. Neurosci. 12, 751-758.
23. Gandhi, S. P., and Stevens, C. F. (2003). Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423, 607-613.
24. Garner, C. C., Waites, C. L., and Ziv, N. E. (2006). Synapse development: still looking for the forest, still lost in the trees. Cell Tissue Res. 326, 249-262.
25. Goda, Y., and Stevens, C. F. (1994). Two components of transmitter release at a central synapse. Proc. Natl. Acad. Sci. U.S.A. 91, 12942-12946.
26. 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.
27. Gray, N. W., Weimer, R. M., Bureau, I., and Svoboda, K. (2006). Rapid redistribution of synaptic PSD-95 in the neocortex in vivo. PLoS Biol. 4, e370. doi: 10.1371/journal.pbio.0040370.
28. Harata, N., Ryan, T. A., Smith, S. J., Buchanan, J., and Tsien, R. W. (2001). Visualizing recycling synaptic vesicles in hippocampal neurons by FM 1-43 photoconversion. Proc. Natl. Acad. Sci. U.S.A. 98, 12748-12753.
29. Heuser, J. E., and Reese, T. S. (1973). Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315-344.
30. Hopf, F. W., Waters, J., Mehta, S., and Smith, S. J. (2002). Stability and plasticity of developing synapses in hippocampal neuronal cultures. J. Neurosci. 22, 775-781.
31. Ishizuka, N., Weber, J., and Amaral, D. G. (1990). Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J. Comp. Neurol. 295, 580-623.
32. Jaskolski, F., and Henley, J. M. (2009). Synaptic receptor trafficking: the lateral point of view. Neuroscience 158, 19-24.
33. Jordan, R., Lemke, E. A., and Klingauf, J. (2005). Visualization of synaptic vesicle movement in intact synaptic boutons using fluorescence fluctuation spectroscopy. Biophys. J. 89, 2091-2102.
34. Kalla, S., Stern, M., Basu, J., Varoqueaux, F., Reim, K., Rosenmund, C., Ziv, N. E., and Brose, N. (2006). Molecular dynamics of a presynaptic active zone protein studied in Munc13-1-enhanced yellow fluorescent protein knock-in mutant mice. J. Neurosci. 26, 13054-13066.
35. Kraszewski, K., Daniell, L., Mundigl, O., and De Camilli, P. (1996). Mobility of synaptic vesicles in nerve endings monitored by recovery from photobleaching of synaptic vesicle-associated fluorescence. J. Neurosci. 16, 5905-5913.
36. Krueger, S. R., Kolar, A., and Fitzsimonds, R. M. (2003). The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons. Neuron 40, 945-957.
37. Lemke, E. A., and Klingauf, J. (2005). Single synaptic vesicle tracking in individual hippocampal boutons at rest and during synaptic activity. J. Neurosci. 25, 11034-11044.
38. Li, Z., and Murthy, V. N. (2001). Visualizing postendocytic traffic of synaptic vesicles at hippocampal synapses. Neuron 31, 593-605.
39. Matteoli, M., Takei, K., Perin, M. S., Sudhof, T. C., and De Camilli, P. (1992). Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J. Cell Biol. 117, 849-861.
40. Mueller, V. J., Wienisch, M., Nehring, R. B., and Klingauf, J. (2004). Monitoring clathrin-mediated endocytosis during synaptic activity. J. Neurosci. 24, 2004-2012.
41. Murthy, V. N., Schikorski, T., Stevens, C. F., and Zhu, Y. (2001). Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32, 673-682.
42. Murthy, V. N., Sejnowski, T. J., and Stevens, C. F. (1997). Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18, 599-612.
43. Murthy, V. N., and Stevens, C. F. (1998). Synaptic vesicles retain their identity through the endocytic cycle. Nature 392, 497-501.
44. Nikonenko, I., Jourdain, P., and Muller, D. (2003). Presynaptic remodeling contributes to activity-dependent synaptogenesis. J. Neurosci. 23, 8498-8505.
45. Ninan, I., Liu, S., Rabinowitz, D., and Arancio, O. (2006). Early presynaptic changes during plasticity in cultured hippocampal neurons. EMBO J. 25, 4361-4371.
46. Okabe, S., Urushido, T., Konno, D., Okado, H., and Sobue, K. (2001). Rapid redistribution of the postsynaptic density protein PSD-Zip45 (Homer 1c) and its differential regulation by NMDA receptors and calcium channels. J. Neurosci. 21, 9561-9571.
47. Okamoto, K., Nagai, T., Miyawaki, A., and Hayashi, Y. (2004). Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat. Neurosci. 7, 1104-1112.
48. Palay, S. L. (1956). Synapses in the central nervous system. J. Biophys. Biochem. Cytol. 2, 193-202.
49. Petrini, E. M., Lu, J., Cognet, L., Lounis, B., Ehlers, M. D., and Choquet, D. (2009). Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 63, 92-105.
50. Rizzoli, S. O., and Betz, W. J. (2005). Synaptic vesicle pools. Nat. Rev. Neurosci. 6, 57-69.
51. Ryan, T. A. (2001). Presynaptic imaging techniques. Curr. Opin. Neurobiol. 11, 544-549.
52. Ryan, T. A., Reuter, H., Wendland, B., Schweizer, F. E., Tsien, R. W., and Smith, S. J. (1993). The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11, 713-724.
53. Ryan, T. A., Smith, S. J., and Reuter, H. (1996). The timing of synaptic vesicle endocytosis. Proc. Natl. Acad. Sci. U.S.A. 93, 5567-5571.
54. Sabo, S. L., Gomes, R. A., and McAllister, A. K. (2006). Formation of presynaptic terminals at predefined sites along axons. J. Neurosci. 26, 10813-10825.
55. Sara, Y., Virmani, T., Deak, F., Liu, X., and Kavalali, E. T. (2005). An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 45, 563-573.
56. Schweizer, F. E., and Ryan, T. A. (2006). The synaptic vesicle: cycle of exocytosis and endocytosis. Curr. Opin. Neurobiol. 16, 298-304.
57. Shakiryanova, D., Tully, A., and Levitan, E. S. (2006). Activity-dependent synaptic capture of transiting peptidergic vesicles. Nat. Neurosci. 9, 896-900.
58. Sharma, K., Fong, D. K., and Craig, A. M. (2006). Postsynaptic protein mobility in dendritic spines: long-term regulation by synaptic NMDA receptor activation. Mol. Cell. Neurosci. 31, 702-712.
59. Shepherd, G. M., and Harris, K. M. (1998). Three-dimensional structure and composition of CA3 → CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J. Neurosci. 18, 8300-8310.
60. Shtrahman, M., Yeung, C., Nauen, D. W., Bi, G. Q., and Wu, X. L. (2005). Probing vesicle dynamics in single hippocampal synapses. Biophys. J. 89, 3615-3627.
61. Sorra, K. E., and Harris, K. M. (1993). Occurrence and three-dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in hippocampal area CA1. J. Neurosci. 13, 3736-3748.
62. Star, E. N., Newton, A. J., and Murthy, V. N. (2005). Real-time imaging of Rab3a and Rab5a reveals differential roles in presynaptic function. J. Physiol. (Lond.) 569, 103-117.
63. Staras, K. (2007). Share and share alike: trading of presynaptic elements between central synapses. Trends Neurosci. 30, 292-298.
64. Staras, K., Branco, T., Burden, J. J., Pozo, K., Darcy, K. J., Marra, V., Ratnayaka, A., and Goda, Y. (2010). A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons. Neuron 66, 37-44.
65. Stettler, D. D., Yamahachi, H., Li, W., Denk, W., and Gilbert, C. D. (2006). Axons and synaptic boutons are highly dynamic in adult visual cortex. Neuron 49, 877-887.
66. Sudhof, T. C. (2004). The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547.
67. 2+-sensor model for neurotransmitter release in a central synapse. Nature 450, 676-682.
68. Tanaka, H., Shan, W., Phillips, G. R., Arndt, K., Bozdagi, O., Shapiro, L., Huntley, G. W., Benson, D. L., and Colman, D. R. (2000). Molecular modification of N-cadherin in response to synaptic activity. Neuron 25, 93-107.
69. Takei, K., Mundigl, O., Daniell, L., and De Camilli, P. (1996). The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J. Cell Biol. 133, 1237-1250.
70. Thiagarajan, T. C., Lindskog, M., and Tsien, R. W. (2005). Adaptation to synaptic inactivity in hippocampal neurons. Neuron 47, 725-737.
71. Tsuriel, S., Fisher, A., Wittenmayer, N., Dresbach, T., Garner, C. C., and Ziv, N. E. (2009). Exchange and redistribution dynamics of the cytoskeleton of the active zone molecule bassoon. J. Neurosci. 29, 351-358.
72. Tsuriel, S., Geva, R., Zamorano, P., Dresbach, T., Boeckers, T., Gundelfinger, E. D., Garner, C. C., and Ziv, N. E. (2006). Local sharing as a predominant determinant of synaptic matrix molecular dynamics. PLoS Biol. 4, e271. doi: 10.1371/journal.pbio.0040271.
73. Tyler, W. J., Zhang, X. L., Hartman, K., Winterer, J., Muller, W., Stanton, P. K., and Pozzo-Miller, L. (2006). BDNF increases release probability and the size of a rapidly recycling vesicle pool within rat hippocampal excitatory synapses. J. Physiol. (Lond.) 574, 787-803.
74. Voglmaier, S. M., and Edwards, R. H. (2007). Do different endocytic pathways make different synaptic vesicles? Curr. Opin. Neurobiol. 17, 374-380.
75. Westphal, V., Rizzoli, S. O., Lauterbach, M. A., Kamin, D., Jahn, R., and Hell, S. W. (2008). Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 320, 246-249.
76. Westrum, L. E., and Blackstad, T. W. (1962). An electron microscopic study of the stratum radiatum of the rat hippocampus (regio superior, CA 1) with particular emphasis on synaptology. J. Comp. Neurol. 119, 281-309.
77. Wong, M. Y., Shakiryanova, D., and Levitan, E. S. (2009). Presynaptic ryanodine receptor-CamKII signaling is required for activity-dependent capture of transiting vesicles. J. Mol. Neurosci. 37, 146-150.
78. Zakharenko, S. S., Patterson, S. L., Dragatsis, I., Zeitlin, S. O., Siegelbaum, S. A., Kandel, E. R., and Morozov, A. (2003). Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron 39, 975-990.
79. Zhang, Q., Li, Y., and Tsien, R. W. (2009). The dynamic control of kiss-and-run and vesicular reuse probed with single nanoparticles. Science 323, 1448-1453.