Abstract
NERVE terminals are unique among cellular secretory systems in that they can sustain vesicular release at a high rate. Although little is known about the mechanisms that account for the distinctive features of neurotransmitter release, it can be assumed that neuron-specific proteins are involved. One such protein family, the synapsins, are believed to regulate neurotransmitter release through phosphorylation-dependent interactions with synaptic vesicles and cytoskeletal elements1. Here we show that clusters of vesicles at synaptic release sites are composed of two pools, a distal pool containing synapsin and a proximal pool devoid of synapsin and located adjacent to the presynaptic membrane. Pre-synaptic injection of synapsin antibodies resulted in the loss of the distal pool, without any apparent effect on the proximal pool. Depletion of this distal pool was associated with a marked depression of neurotransmitter release evoked by high-frequency (18-20 Hz) but not by low-frequency (0.2 Hz) stimulation. Thus the availability of the synapsin-associated pool of vesicles seems to be required to sustain release of neurotransmitter in response to high-frequency bursts of impulses.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Greengard, P., Valtorta, F., Czernik, A. J. & Benfenati, F. Science 259, 780–785 (1993).
Brodin, L., Shupliakov, O. & Grillner, S. in Molecular and Cellular Mechanisms of Neurotransmitter Release (eds Stjärne, L. et al.) 205–221 (Raven, New York, 1994).
Shupliakov, O., Pieribone, V. A., Gad, H. & Brodin, L. Eur. J. Neurosci. 7, 1111–1116 (1995).
Shupliakov, O., Brodin, L., Cullheim, S., Ottersen, O. P. & Storm-Mathisen, J. J. Neurosci. 12, 3789–3803 (1992).
Wickelgren, W. O., Leonard, J. P., Grimes, M. J. & Clark, R. D. J. Neurosci. 5, 1188–1201 (1985).
Matthew, W. D., Tsavaler, L. & Reichart, L. F. J. Cell Biol. 91, 257–269 (1981).
Brose, N., Petrenko, A. G., Südhof, T. C. & Jahn, R. Science 256, 1021–1025 (1992).
DeBello, W. M., Betz, H. & Augustine, G. J. Cell 74, 947–950 (1993).
Buchanan, J., Moore, L., Hill, R. H., Wallén, P. & Grillner, S. S. Biol. Cybernet. 67, 123–131 (1992).
Bennett, M. K. & Scheller, R. H. Proc. natn. Acad. Sci. U.S.A. 90, 2559–2563 (1993).
Kelly, R. B. Cell 72 (suppl.), 43–53 (1993).
Söllner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H. & Rothman, J. E. Cell 75, 409–418 (1993).
Ferro-Novick, S. & Jahn, R. Nature 370, 191–193 (1994).
Benfenati, F. et al. J. Cell Biol. 123, 1845–1855 (1993).
Rosahl, T. W. et al. Cell 75, 661–670 (1993).
De Camilli, P., Cameron, R. & Greengard, P. J. Cell Biol. 96, 1337–1354 (1983).
Mandell, J. W., Czernik, A. J., De Camilli, P., Greengard, P. & Townes-Anderson, E. J. Neurosci. 12, 1736–1749 (1992).
Katz, B. The Release of Neural Transmitter Substances (Thomas, Springfield, Illinois, 1969).
Atwood, H. L. & Wojtowicz, J. M. in International Review of Neurobiology Vol. 28 (eds Smythies, J. R. & Bradley, R. J.) 275–362 (Academic, New York, 1986).
Peters, A., Palay, S. L. & Webster, H. F. The Fine Structure of the Nervous System. Neurons and their Supporting Cells (Oxford University Press, Oxford, UK, 1991).
Südhof, T. C. et al. Science 245, 1474–1480 (1989).
Rubenstein, J. L., Greengard, P. & Czernik, A. J. Synapse 13, 161–172 (1993).
Brodin, L., Shupliakov, O., Hellgren, J., Pieribore, V. A. & Hill, R. J. J. Neurophysiol. 72, 592–604 (1994).
Rovainen, C. M. Physiol. Rev. 59, 1007–1077 (1979).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Pieribone, V., Shupliakov, O., Brodin, L. et al. Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375, 493–497 (1995). https://doi.org/10.1038/375493a0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/375493a0
- Springer Nature Limited
This article is cited by
-
Damaged mitochondria coincide with presynaptic vesicle loss and abnormalities in alzheimer’s disease brain
Acta Neuropathologica Communications (2023)
-
Synapsin condensation controls synaptic vesicle sequestering and dynamics
Nature Communications (2023)
-
Synaptic vesicle proteins and ATG9A self-organize in distinct vesicle phases within synapsin condensates
Nature Communications (2023)
-
An interaction between synapsin and C9orf72 regulates excitatory synapses and is impaired in ALS/FTD
Acta Neuropathologica (2022)
-
Cannabinoid receptor activation acutely increases synaptic vesicle numbers by activating synapsins in human synapses
Molecular Psychiatry (2021)