Synaptic vesicle endocytosis at a CNS nerve terminal: Faster kinetics at physiological temperatures and increased endocytotic capacity during maturation

Journal of Neurophysiology

Volumn 98, Issue 6, 2007, Pages 3349-3359

  Renden, Robert ^a   Von Gersdorff, Henrique ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; BRAIN STEM; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; ENDOCYTOSIS; EXCITATORY POSTSYNAPTIC POTENTIAL; EXOCYTOSIS; HEARING; MOUSE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; ROOM TEMPERATURE; SYNAPSE VESICLE; SYNAPTIC MEMBRANE; TEMPERATURE DEPENDENCE;

ACTION POTENTIALS; AGING; ALGORITHMS; ANIMALS; CENTRAL NERVOUS SYSTEM; ELECTRIC CAPACITANCE; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; ENDOCYTOSIS; EXCITATORY POSTSYNAPTIC POTENTIALS; EXOCYTOSIS; KINETICS; MICE; MICE, INBRED C57BL; PRESYNAPTIC TERMINALS; SYNAPTIC VESICLES; TEMPERATURE;

EID: 37549020622     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00898.2007     Document Type: Article

References (75)

1. Aravanis AM, Pyle JL, Tsien RW. Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 423: 643-647, 2003.
2. 2+, GTP, and dynamin but not clathrin. Proc Natl Acad Sci USA 92: 8328-8332, 1995.
3. Betz WJ, Angleson JK. The synaptic vesicle cycle. Annu Rev Physiol 60: 347-363, 1998.
4. Blatchley BJ, Cooper WA, Coleman JR. Development of auditory brainstem response to tone pip stimuli in the rat. Brain Res 429: 75-84, 1987.
5. Borst JG, Helmchen F, Sakmann B. Pre- and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat. J Physiol 489: 825-840, 1995.
6. Ceccarelli B, Hurlbut WP, Mauro A. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol 57: 499-524, 1973.
7. 2+ dynamics in presynaptic terminal and postsynaptic neuron of the rat auditory synapse. Brain Res 904: 341-344, 2001.
8. Cnops L, Hu TT, Vanden Broeck J, Burnat K, van den Bergh G, Arckens L. Age- and experience-dependent expression of dynamin I and synaptotagmin I in cat visual system. J Comp Neurol 504: 254-264, 2007.
9. de Lange RP, de Roos AD, Borst JG. Two modes of vesicle recycling in the rat calyx of Held. J Neurosci 23: 10164-10173, 2003.
10. Fedchyshyn MJ, Wang LY. Developmental transformation of the release modality at the calyx of Held synapse. J Neurosci 25: 4131-4140, 2005.
11. 2+-binding proteins calretinin and parvalbumin at the calyx of Held of rats and mice. Eur J Neurosci 20: 1473-1482, 2004.
12. Fergestad T, Broadie K. Interaction of stoned and synaptotagmin in synaptic vesicle endocytosis. J Neurosci 21: 1218-1227, 2001.
13. Ferguson SM, Brasnjo G, Hayashi M, Wolfel M, Collesi C, Giovedi S, Raimondi A, Gong LW, Ariel P, Paradise S, O'Toole E, Flavell R, Cremona O, Miesenbock G, Ryan TA, De Camilli P. A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316: 570-574, 2007.
14. Fernandez-Alfonso T, Ryan TA. The kinetics of synaptic vesicle pool depletion at CNS synaptic terminals. Neuron 41: 943-953, 2004.
15. Forsythe ID. Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro. J Physiol 479: 381-387, 1994.
16. 2+-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse. Neuron 21: 607-616, 1998.
17. Gandhi SP, Stevens CF. Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423: 607-613, 2003.
18. Gillis KD. Techniques for membrane capacitance measurements. In: Single-Channel Recording (2nd ed.), edited by Sakmann B, Neher E. New York: Plenum Press, 1995, p. 155-198.
19. Granseth B, Odermatt B, Royle SJ, Lagnado L. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51: 773-786, 2006.
20. Guinan JJ Jr, Li RY. Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat. Hear Res 49: 321-334, 1990.
21. Hallermann S, Pawlu C, Jonas P, Heckmann M. A large pool of releasable vesicles in a cortical glutamatergic synapse. Proc Natl Acad Sci USA 100: 8975-8980, 2003.
22. He L, Wu XS, Mohan R, Wu LG. Two modes of fusion pore opening revealed by cell-attached recordings at a synapse. Nature 444: 102-105, 2006.
23. Heidelberger R, Zhou ZY, Matthews G. Multiple components of membrane retrieval in synaptic terminals revealed by changes in hydrostatic pressure. J Neurophysiol 88: 2509-2517, 2002.
24. Helmchen F, Borst JG, Sakmann B. Calcium dynamics associated with a single action potential in a CNS presynaptic terminal. Biophys J 72:1458-1471, 1997.
25. Hermann J, Pecka M, von Gersdorff H, Grothe B, Klug A. Synaptic transmission at the calyx of Held under in vivo like activity levels. J Neurophysiol 98: 807-820, 2007.
26. Holt M, Cooke A, Wu MM, Lagnado L. Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells. J Neurosci 23: 1329-1339, 2003.
27. Horrigan FT, Bookman RJ. Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron 13: 1119-1129, 1994.
28. Hull C, von Gersdorff H. Fast endocytosis is inhibited by GABA-mediated chloride influx at a presynaptic terminal. Neuron 44: 469-482, 2004.
29. 2+ dependence of exocytosis during development of mouse inner hair cells. J Physiol 563: 177-191, 2005.
30. Jung N, Haucke V. Clathrin-mediated endocytosis at synapses. Traffic 8: 1129-1136, 2007.
31. Kimura J, Miyamae S, Noma A. Identification of sodium-calcium exchange current in single ventricular cells of guinea-pig. J Physiol 384: 199-222, 1987.
32. Koh T-W, Korolchuk VI, Wairkar YP, Jiao W, Evergren E, Pan H, Zhou Y, Venken KJT, Shupliakov O, Robinson IM, O'Kane CJ, Bellen HJ. Eps15 and Dap160 control synaptic vesicle membrane retrieval and synapse development. J Cell Biol 178: 309-322, 2007.
33. Kushmerick C, Renden R, von Gersdorff H. Physiological temperatures reduce the rate of vesicle pool depletion and short-term depression via an acceleration of vesicle recruitment. J Neurosci 26: 1366-1377, 2006.
34. LoGiudice L, Matthews G. Endocytosis at ribbon synapses. Traffic 8: 1123-1128, 2007.
35. Micheva KD, Smith SJ. Strong effects of subphysiological temperature on the function and plasticity of mammalian presynaptic terminals. J Neurosci 25: 7481-7488, 2005.
36. Moser T, Beutner D. Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc Natl Acad Sci USA 97: 883-888, 2000.
37. Parsons TD, Lenzi D, Almers W, Roberts WM. Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell: capacitance measurements in saccular hair cells. Neuron 13: 875-883, 1994.
38. Postlethwaite M, Hennig MH, Steinert JR, Graham BP, Forsythe ID. Acceleration of AMPA receptor kinetics underlies temperature-dependent changes in synaptic strength at the rat calyx of Held. J Physiol 579: 69-84, 2007.
39. Price GD, Trussell LO. Estimate of the chloride concentration in a central glutamatergic terminal: a gramicidin perforated-patch study on the calyx of Held. J Neurosci 26: 11432-11436, 2006.
40. Rieke F, Schwartz EA. Asynchronous transmitter release: control of exocytosis and endocytosis at the salamander rod synapse. J Physiol 493: 1-8, 1996.
41. Rizzoli SO, Jahn R. Kiss-and-run, collapse and "readily retrievable" vesicles. Traffic 8: 1137-1144, 2007.
42. Roos J, Kelly RB. The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr Biol 9: 1411-1414, 1999.
43. Sakaba T. Roles of the fast-releasing and the slowly releasing vesicles in synaptic transmission at the calyx of held. J Neurosci 26: 5863-5871, 2006.
44. Sakaba T, Neher E. Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32: 1119-1131, 2001a.
45. Sakaba T, Neher E. Preferential potentiation of fast-releasing synaptic vesicles by cAMP at the calyx of Held. Proc Natl Acad Sci USA 98: 331-336, 2001b.
46. Sakaba T, Neher E. Involvement of actin polymerization in vesicle recruitment at the calyx of Held synapse. J Neurosci 23: 837-846, 2003.
47. Sätzler K, Sohl LF, Bollmann JH, Borst JG, Frotscher M, Sakmann B, Lubke JH. Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J Neurosci 22: 10567-10579, 2002.
48. Scheuss V, Schneggenburger R, Neher E. Separation of presynaptic and postsynaptic contributions to depression by covariance analysis of successive EPSCs at the calyx of held synapse. J Neurosci 22: 728-739, 2002.
49. Schweizer FE, Ryan TA. The synaptic vesicle: cycle of exocytosis and endocytosis. Curr Opin Neurobiol 16: 298-304, 2006.
50. Smillie KJ, Evans GJ, Cousin MA. Developmental change in the calcium sensor for synaptic vesicle endocytosis in central nerve terminals. J Neurochem 94: 452-458, 2005.
51. Smith C, Neher E. Multiple forms of endocytosis in bovine adrenal chromaffin cells. J Cell Biol 139: 885-894, 1997.
52. Südhof TC. The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547, 2004.
53. Sun JY, Wu LG. Fast kinetics of exocytosis revealed by simultaneous measurements of presynaptic capacitance and postsynaptic currents at a central synapse. Neuron 30: 171-182, 2001.
54. Sun JY, Wu XS, Wu LG. Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature 417: 555-559, 2002.
55. Taschenberger H, Leao RM, Rowland KC, Spirou GA, von Gersdorff H. Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 36: 1127-1143, 2002.
56. Taschenberger H, von Gersdorff H. Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20: 9162-9173, 2000.
57. Teng H, Cole JC, Roberts RL, Wilkinson RS. Endocytic active zones: hot spots for endocytosis in vertebrate neuromuscular terminals. J Neurosci 19: 4855-4866, 1999.
58. Teng H, Wilkinson RS. Clathrin-mediated endocytosis near active zones in snake motor boutons. J Neurosci 20: 7986-7993, 2000.
59. 2+ in snake motor boutons. J Physiol 551: 103-114, 2003.
60. 2+. J Physiol 565: 743-750, 2005.
61. Trommershauser J, Schneggenburger R, Zippelius A, Neher E. Heterogeneous presynaptic release probabilities: functional relevance for short-term plasticity. Biophys J 84: 1563-1579, 2003.
62. von Gersdorff H, Borst JG. Short-term plasticity at the calyx of Held. Nat Rev Neurosci 3: 53-64, 2002.
63. von Gersdorff H, Matthews G. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367: 735-739, 1994.
64. von Gersdorff H, Schneggenburger R, Weis S, Neher E. Presynaptic depression at a calyx synapse: the small contribution of metabotropic glutamate receptors. J Neurosci 17: 8137-8146, 1997.
65. 2+ channels determines fast neurotransmitter release. Neuron 53: 563-575, 2007.
66. Wang LY, Kaczmarek LK. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394: 384-388, 1998.
67. Wolfel M, Lou X, Schneggenburger R. A mechanism intrinsic to the vesicle fusion machinery determines fast and slow transmitter release at a large CNS synapse. J Neurosci 27: 3198-3210, 2007.
68. 2+ sensitivity of vesicle pool depletion at a fast CNS synapse. J Neurosci 23: 7059-7068, 2003.
69. Wu LG. Kinetic regulation of vesicle endocytosis at synapses. Trends Neurosci 27: 548-554, 2004.
70. Wu SH, Kelly JB. Response of neurons in the lateral superior olive and medial nucleus of the trapezoid body to repetitive stimulation: intracellular and extracellular recordings from mouse brain slice. Hear Res 68: 189-201, 1993.
71. Wu W, Wu LG. Rapid bulk endocytosis and its kinetics of fission pore closure at a central synapse. Proc Natl Acad Sci USA 104: 10234-10239, 2007.
72. Wu W, Xu J, Wu XS, Wu LG. Activity-dependent acceleration of endocytosis at a central synapse. J Neurosci 25: 11676-11683, 2005.
73. Wu XS, Xue L, Mohan R, Paradiso K, Gillis KD, Wu LG. The origin of quantal size variation: vesicular glutamate concentration plays a significant role. J Neurosci 27: 3046-3056, 2007.
74. Yamashita T, Hige T, Takahashi T. Vesicle endocytosis requires dynamin-dependent GTP hydrolysis at a fast CNS synapse. Science 307: 124-127, 2005.
75. 2+ current and its efficacy in triggering transmitter release at the developing calyx of held synapse. J Neurosci 26: 5698-5708, 2006.