Structural changes after transmitter release at the frog neuromuscular junction

doi:10.1083/jcb.88.3.564

This Article

	Full Text (PDF, 2562K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Heuser, J. E.
	Articles by Reese, T. S.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Heuser, J. E.
	Articles by Reese, T. S.


Social Bookmarking

	What's this?

ARTICLES

Structural changes after transmitter release at the frog neuromuscular junction

JE Heuser and TS Reese

The sequence of structural changes that occur during synaptic vesicle exocytosis was studied by quick-freezing muscles at different intervals after stimulating their nerves, in the presence of 4-aminopyridine to increase the number of transmitter quanta released by each stimulus. Vesicle openings began to appear at the active zones of the intramuscular nerves within 3-4 ms after a single stimulus. The concentration of these openings peaked at 5-6 ms, and then declined to zero 50-100 ms late. At the later times, vesicle openings tended to be larger. Left behind at the active zones, after the vesicle openings disappeared, were clusters of large intramembrane particles. The larger particles in these clusters were the same size as intramembrane particles in undischarged vesicles, and were slightly larger than the particles which form the rows delineating active zones. Because previous tracer work had shown that new vesicles do not pinch off from the plasma membrane at these early times, we concluded that the particle clusters originate from membranes of discharged vesicles which collapse into the plasmalemma after exocytosis. The rate of vesicle collapse appeared to be variable because different stages occurred simultaneously at most times after stimulation; this asynchrony was taken to indicate that the collapse of each exocytotic vesicle is slowed by previous nearby collapses. The ultimate fate of synaptic vesicle membrane after collapse appeared to be coalescence with the plasma membrane, as the clusters of particles gradually dispersed into surrounding areas during the first second after a stimulus. The membrane retrieval and recycling that reverse this exocytotic sequence have a slower onset, as has been described in previous reports.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Akbergenova, Y., Bykhovskaia, M. (2009). Stimulation-Induced Formation of the Reserve Pool of Vesicles in Drosophila Motor Boutons. J. Neurophysiol. 101: 2423-2433 [Abstract] [Full Text]
Chen, X., Winters, C. A., Reese, T. S. (2008). Life Inside a Thin Section: Tomography. J. Neurosci. 28: 9321-9327 [Full Text]
Siksou, L., Rostaing, P., Lechaire, J.-P., Boudier, T., Ohtsuka, T., Fejtova, A., Kao, H.-T., Greengard, P., Gundelfinger, E. D., Triller, A., Marty, S. (2007). Three-Dimensional Architecture of Presynaptic Terminal Cytomatrix. J. Neurosci. 27: 6868-6877 [Abstract] [Full Text]
Rosenberger, R. (2005). Bridging Philosophy of Technology and Neurobiological Research: Interpreting Images From the "Slam Freezer". Bulletin of Science Technology Society 25: 469-474 [Abstract]
Borycz, J. A., Borycz, J., Kubow, A., Kostyleva, R., Meinertzhagen, I. A. (2005). Histamine Compartments of the Drosophila Brain With an Estimate of the Quantum Content at the Photoreceptor Synapse. J. Neurophysiol. 93: 1611-1619 [Abstract] [Full Text]
Dalal, S., Rosser, M. F. N., Cyr, D. M., Hanson, P. I. (2004). Distinct Roles for the AAA ATPases NSF and p97 in the Secretory Pathway. Mol. Biol. Cell 15: 637-648 [Abstract] [Full Text]
Saviane, C., Mohajerani, M. H, Cherubini, E. (2003). An ID-like current that is downregulated by Ca2+ modulates information coding at CA3-CA3 synapses in the rat hippocampus. J. Physiol. 552: 513-524 [Abstract] [Full Text]
Xu, Y.-F., Autio, D., Rheuben, M. B., Atchison, W. D. (2002). Impairment of Synaptic Vesicle Exocytosis and Recycling During Neuromuscular Weakness Produced in Mice by 2,4-Dithiobiuret. J. Neurophysiol. 88: 3243-3258 [Abstract] [Full Text]
Silver, R. B., Kriebel, M. E., Keller, B., Pappas, G. D. (2001). Porocytosis: Quantal Synaptic Secretion of Neurotransmitter at the Neuromuscular Junction Through Arrayed Vesicles. Biol. Bull. 201: 263-264 [Full Text]
McIntosh, J. R. (2001). Electron Microscopy of Cells: A New Beginning for a New Century. JCB 153: f25-f32 [Full Text]
Fergestad, T., Broadie, K. (2001). Interaction of Stoned and Synaptotagmin in Synaptic Vesicle Endocytosis. J. Neurosci. 21: 1218-1227 [Abstract] [Full Text]
Angleson, J. K., Betz, W. J. (2001). Intraterminal Ca2+ and Spontaneous Transmitter Release at the Frog Neuromuscular Junction. J. Neurophysiol. 85: 287-294 [Abstract] [Full Text]
Fukuda, M., Moreira, J. E., Liu, V., Sugimori, M., Mikoshiba, K., Llinás, R. R. (2000). Role of the conserved WHXL motif in the C terminus of synaptotagmin in synaptic vesicle docking. Proc. Natl. Acad. Sci. USA 10.1073/pnas.260491197v1 [Abstract] [Full Text]
Smith, R. M., Baibakov, B., Ikebuchi, Y., White, B. H., Lambert, N. A., Kaczmarek, L. K., Vogel, S. S. (2000). Exocytotic Insertion of Calcium Channels Constrains Compensatory Endocytosis to Sites of Exocytosis. JCB 148: 755-768 [Abstract] [Full Text]
DiGregorio, D. A., Peskoff, A., Vergara, J. L. (1999). Measurement of Action Potential-Induced Presynaptic Calcium Domains at a Cultured Neuromuscular Junction. J. Neurosci. 19: 7846-7859 [Abstract] [Full Text]
Meir, A., Ginsburg, S., Butkevich, A., Kachalsky, S. G., Kaiserman, I., Ahdut, R., Demirgoren, S., Rahamimoff, R. (1999). Ion Channels in Presynaptic Nerve Terminals and Control of Transmitter Release. Physiol. Rev. 79: 1019-1088 [Abstract] [Full Text]
Teng, H., Cole, J. C., Roberts, R. L., Wilkinson, R. S. (1999). Endocytic Active Zones: Hot Spots for Endocytosis in Vertebrate Neuromuscular Terminals. J. Neurosci. 19: 4855-4866 [Abstract] [Full Text]
Vogel, S. S., Smith, R. M., Baibakov, B., Ikebuchi, Y., Lambert, N. A. (1999). Calcium influx is required for endocytotic membrane retrieval. Proc. Natl. Acad. Sci. USA 96: 5019-5024 [Abstract] [Full Text]
Koenig, J. H., Yamaoka, K., Ikeda, K. (1998). Omega images at the active zone may be endocytotic rather than exocytotic: Implications for the vesicle hypothesis of transmitter release. Proc. Natl. Acad. Sci. USA 95: 12677-12682 [Abstract] [Full Text]
Rettig, J., Heinemann, C., Ashery, U., Sheng, Z.-H., Yokoyama, C. T., Catterall, W. A., Neher, E. (1997). Alteration of Ca2+ Dependence of Neurotransmitter Release by Disruption of Ca2+ Channel/Syntaxin Interaction. J. Neurosci. 17: 6647-6656 [Abstract] [Full Text]
Burns, A. L., Benson, D., Howard, M. J., Margiotta, J. F. (1997). Chick Ciliary Ganglion Neurons Contain Transcripts Coding for Acetylcholine Receptor-Associated Protein at Synapses (Rapsyn). J. Neurosci. 17: 5016-5026 [Abstract] [Full Text]
von Gersdorff, H., Matthews, G. (1997). Depletion and Replenishment of Vesicle Pools at a Ribbon-Type Synaptic Terminal. J. Neurosci. 17: 1919-1927 [Abstract] [Full Text]
Chen, B.-M., Grinnell, A. D. (1997). Kinetics, Ca2+ Dependence, and Biophysical Properties of Integrin-Mediated Mechanical Modulation of Transmitter Release from Frog Motor Nerve Terminals. J. Neurosci. 17: 904-916 [Abstract] [Full Text]
Schneider, S.�W., Sritharan, K.�C., Geibel, J.�P., Oberleithner, H., Jena, B.�P. (1997). Surface dynamics in living acinar cells imaged by atomic force microscopy: Identification of plasma membrane structures involved in�exocytosis. Proc. Natl. Acad. Sci. USA 94: 316-321 [Abstract] [Full Text]
Estes, P. S., Roos, J., van der Bliek, A., Kelly, R. B., Krishnan, K. S., Ramaswami, M. (1996). Traffic of Dynamin within Individual Drosophila Synaptic Boutons Relative to Compartment-Specific Markers. J. Neurosci. 16: 5443-5456 [Abstract] [Full Text]
Hudspeth, A.J., Issa, N.P. (1996). Confocal-microscopic Visualization of Membrane Addition during Synaptic Exocytosis at Presynaptic Active Zones of Hair Cells. Cold Spring Harb Symp Quant Biol 61: 303-307 [Abstract]
Parsons, T.D., Coorssen, J.R., Hortmann, H., Lee, A.K., Tse, F.W., Almers, W. (1995). The Last Seconds in the Life of a Secretory Vesicle. Cold Spring Harb Symp Quant Biol 60: 389-396 [Abstract]
White, J. (1992). Membrane fusion. Science 258: 917-924 [Abstract]
Bailey, C., Chen, M (1983). Morphological basis of long-term habituation and sensitization in Aplysia. Science 220: 91-93 [Abstract]
Fukuda, M., Moreira, J. E., Liu, V., Sugimori, M., Mikoshiba, K., Llinas, R. R. (2000). Role of the conserved WHXL motif in the C terminus of synaptotagmin in synaptic vesicle docking. Proc. Natl. Acad. Sci. USA 97: 14715-14719 [Abstract] [Full Text]