Error message

No crossref credentials set for sci

Vesicle Endocytosis Requires Dynamin-Dependent GTP Hydrolysis at a Fast CNS Synapse

Science, 7 January 2005
Vol. 307, Issue 5706, p. 124-127
DOI: 10.1126/science.1103631

Vesicle Endocytosis Requires Dynamin-Dependent GTP Hydrolysis at a Fast CNS Synapse

  1. Takayuki Yamashita,
  2. Toshihide Hige,
  3. Tomoyuki Takahashi*
  1. Department of Neurophysiology, University of Tokyo Graduate School of Medicine, Tokyo 113-0033, Japan.
  1. * To whom correspondence should be addressed. E-mail: ttakahas-tky{at}umin.ac.jp

Abstract

Molecular dependence of vesicular endocytosis was investigated with capacitance measurements at the calyx of Held terminal in brainstem slices. Intraterminal loading of botulinum toxin E revealed that the rapid capacitance transient implicated as “kiss-and-run” was unrelated to transmitter release. The release-related capacitance change decayed with an endocytotic time constant of 10 to 25 seconds, depending on the magnitude of exocytosis. Presynaptic loading of the nonhydrolyzable guanosine 5′-triphosphate (GTP) analog GTPgS or dynamin-1 proline-rich domain peptide abolished endocytosis. These compounds had no immediate effect on exocytosis, but caused a use-dependent rundown of exocytosis. Thus, the guanosine triphosphatase dynamin-1 is indispensable for vesicle endocytosis at this fast central nervous system (CNS) synapse.

  • Received for publication 3 August 2004.
  • Accepted for publication 10 November 2004.

Citation:

T. Yamashita, T. Hige, and T. Takahashi, Vesicle Endocytosis Requires Dynamin-Dependent GTP Hydrolysis at a Fast CNS Synapse. Science 307, 124-127 (2005).

Complexin Stabilizes Newly Primed Synaptic Vesicles and Prevents Their Premature Fusion at the Mouse Calyx of Held Synapse
S. Chang, K. Reim, M. Pedersen, E. Neher, N. Brose, and H. Taschenberger
J. Neurosci. 35, 8272-8290 (27 May 2015)

Ca2+ Dependence of Synaptic Vesicle Endocytosis
J. Leitz, and E. T. Kavalali
Neuroscientist 0, 1073858415588265v1-1073858415588265 (21 May 2015)

Brain-Derived Neurotrophic Factor Inhibits Calcium Channel Activation, Exocytosis, and Endocytosis at a Central Nerve Terminal
M. Baydyuk, X.-S. Wu, L. He, and L.-G. Wu
J. Neurosci. 35, 4676-4682 (18 March 2015)

Synaptic vesicle recycling: steps and principles
S. O. Rizzoli, X.-S. Wu, L. He, and L.-G. Wu
EMBO J. 33, 788-822 (16 April 2014)

The Yin and Yang of Calcium Effects on Synaptic Vesicle Endocytosis
X.-S. Wu, and L.-G. Wu
J. Neurosci. 34, 2652-2659 (12 February 2014)

Modes and Regulation of Endocytic Membrane Retrieval in Mouse Auditory Hair Cells
J. Neef, S. Jung, A. B. Wong, K. Reuter, T. Pangrsic, R. Chakrabarti, S. Kugler, C. Lenz, R. Nouvian, R. M. Boumil et al.
J. Neurosci. 34, 705-716 (15 January 2014)

Fast retrieval and autonomous regulation of single spontaneously recycling synaptic vesicles
J. Leitz, and E. T. Kavalali
elife 3, e03658-e03658 (1 January 2014)

Myosin Light Chain Kinase Accelerates Vesicle Endocytosis at the Calyx of Held Synapse
H.-Y. Yue, and J. Xu
J. Neurosci. 34, 295-304 (1 January 2014)

Fast neurotransmitter release regulated by the endocytic scaffold intersectin
T. Sakaba, N. L. Kononenko, J. Bacetic, A. Pechstein, J. Schmoranzer, L. Yao, H. Barth, O. Shupliakov, O. Kobler, K. Aktories et al.
Proc. Natl. Acad. Sci. USA 110, 8266-8271 (14 May 2013)

Amperometric Resolution of a Prespike Stammer and Evoked Phases of Fast Release from Retinal Bipolar Cells
C. P. Grabner, and D. Zenisek
J. Neurosci. 33, 8144-8158 (8 May 2013)

Rapid Synaptic Vesicle Endocytosis in Cone Photoreceptors of Salamander Retina
M. J. Van Hook, and W. B. Thoreson
J. Neurosci. 32, 18112-18123 (12 December 2012)

Synaptic Vesicle Endocytosis
Y. Saheki, and P. De Camilli
Cold Spring Harb. Perspect. Biol. 4, a005645-a005645 (1 September 2012)

A Membrane Pool Retrieved via Endocytosis Overshoot at Nerve Terminals: A Study of Its Retrieval Mechanism and Role
L. Xue, B. D. McNeil, X.-S. Wu, F. Luo, L. He, and L.-G. Wu
J. Neurosci. 32, 3398-3404 (7 March 2012)

Reduced release probability prevents vesicle depletion and transmission failure at dynamin mutant synapses
X. Lou, F. Fan, M. Messa, A. Raimondi, Y. Wu, L. L. Looger, S. M. Ferguson, and P. De Camilli
Proc. Natl. Acad. Sci. USA 109, E515-E523 (21 February 2012)

Activity-dependent modulation of endocytosis by calmodulin at a large central synapse
L. Yao, and T. Sakaba
Proc. Natl. Acad. Sci. USA 109, 291-296 (3 January 2012)

Involvement of Ca2+ Channel Synprint Site in Synaptic Vesicle Endocytosis
H. Watanabe, T. Yamashita, N. Saitoh, S. Kiyonaka, A. Iwamatsu, K. P. Campbell, Y. Mori, and T. Takahashi
J. Neurosci. 30, 655-660 (13 January 2010)

Synaptic Vesicle Recycling at CNS Synapses without AP-2
S. H. Kim, and T. A. Ryan
J. Neurosci. 29, 3865-3874 (25 March 2009)

Selective saturation of slow endocytosis at a giant glutamatergic central synapse lacking dynamin 1
X. Lou, S. Paradise, S. M. Ferguson, and P. De Camilli
Proc. Natl. Acad. Sci. USA 105, 17555-17560 (11 November 2008)

Calcium Control of Endocytic Capacity at a CNS Synapse
J. Balaji, M. Armbruster, and T. A. Ryan
J. Neurosci. 28, 6742-6749 (25 June 2008)

Quantitative Analysis of Calcium-Dependent Vesicle Recruitment and Its Functional Role at the Calyx of Held Synapse
N. Hosoi, T. Sakaba, and E. Neher
J. Neurosci. 27, 14286-14298 (26 December 2007)

Single-vesicle imaging reveals that synaptic vesicle exocytosis and endocytosis are coupled by a single stochastic mode
J. Balaji, and T. A. Ryan
Proc. Natl. Acad. Sci. USA 104, 20576-20581 (18 December 2007)

Synaptic Vesicle Endocytosis at a CNS Nerve Terminal: Faster Kinetics at Physiological Temperatures and Increased Endocytotic Capacity During Maturation
R. Renden, and H. von Gersdorff
J. Neurophysiol. 98, 3349-3359 (1 December 2007)

Modes of Vesicle Retrieval at Ribbon Synapses, Calyx-Type Synapses, and Small Central Synapses
L.-G. Wu, T. A. Ryan, and L. Lagnado
J. Neurosci. 27, 11793-11802 (31 October 2007)

A Selective Activity-Dependent Requirement for Dynamin 1 in Synaptic Vesicle Endocytosis
S. M. Ferguson, G. Brasnjo, M. Hayashi, M. Wolfel, C. Collesi, S. Giovedi, A. Raimondi, L.-W. Gong, P. Ariel, S. Paradise et al.
Science 316, 570-574 (27 April 2007)

A Mechanism Intrinsic to the Vesicle Fusion Machinery Determines Fast and Slow Transmitter Release at a Large CNS Synapse
M. Wolfel, X. Lou, and R. Schneggenburger
J. Neurosci. 27, 3198-3210 (21 March 2007)

Fast Synaptic Vesicle Reuse Slows the Rate of Synaptic Depression in the CA1 Region of Hippocampus
M. Ertunc, Y. Sara, C. Chung, D. Atasoy, T. Virmani, and E. T. Kavalali
J. Neurosci. 27, 341-354 (10 January 2007)

Inhibition of dynamin completely blocks compensatory synaptic vesicle endocytosis
A. J. Newton, T. Kirchhausen, and V. N. Murthy
Proc. Natl. Acad. Sci. USA 103, 17955-17960 (21 November 2006)

Roles of the fast-releasing and the slowly releasing vesicles in synaptic transmission at the calyx of held.
T. Sakaba, T. Kirchhausen, and V. N. Murthy
J. Neurosci. 26, 5863-5871 (31 May 2006)

The kinetics of synaptic vesicle reacidification at hippocampal nerve terminals.
P. P. Atluri, and T. A. Ryan
J. Neurosci. 26, 2313-2320 (22 February 2006)

Synapsins regulate use-dependent synaptic plasticity in the calyx of Held by a Ca2+/calmodulin-dependent pathway
J. Sun, P. Bronk, X. Liu, W. Han, and T. C. Sudhof
Proc. Natl. Acad. Sci. USA 103, 2880-2885 (21 February 2006)

Physiological Temperatures Reduce the Rate of Vesicle Pool Depletion and Short-Term Depression via an Acceleration of Vesicle Recruitment
C. Kushmerick, R. Renden, and H. von Gersdorff
J. Neurosci. 26, 1366-1377 (1 February 2006)

Glutamate Transporter Studies Reveal the Pruning of Metabotropic Glutamate Receptors and Absence of AMPA Receptor Desensitization at Mature Calyx of Held Synapses
R. Renden, H. Taschenberger, N. Puente, D. A. Rusakov, R. Duvoisin, L.-Y. Wang, K. P. Lehre, and H. von Gersdorff
J. Neurosci. 25, 8482-8497 (14 September 2005)

Highlights from the Literature
H. Taschenberger, N. Puente, D. A. Rusakov, R. Duvoisin, L.-Y. Wang, K. P. Lehre, and H. von Gersdorff
Physiology 20, 81-85 (1 April 2005)

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882