Synaptic vesicles in freeze-etched electric tissue of Torpedo

Nickel, E.; Potter, Lincoln T.

doi:10.1016/0006-8993(70)90352-5

Cited by 46 publications

(5 citation statements)

References 7 publications

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“…Vesicle fusions to the terminal membrane of electric organ have previously been demonstrated using freeze-etched samples of resting nerve terminals (27). The present results confirm this interpretation of the morphology in thin sectioned material and show that Ca can facilitate the fusion process.…”

Section: Possible Physiological Significance Of the Vesicular "Tight Junctions'supporting

confidence: 89%

Effects of Calcium-Containing Fixation Solutions on Cholinergic Synaptic Vesicles

Boyne

Bohan

Williams

1974

The Journal of Cell Biology

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Calcium (Ca)-containing fixation solutions applied to slices of electric organ of the electric ray, Narcine brasiliensis, have been shown to have three distinct ultrastructural effects on cholinergic synaptic vesicles of the nerve terminals.(a) An electron-dense particle (EDS) is observed within the vesicle; the particle is seen in unosmicated, unstained tissues and can be removed from thin sections by Ca-chelating agents. It is concluded that the EDS represents Ca bound by the vesicle. It is suggested that the bound ATP of the vesicle provides anionic Ca binding sites.(b) The vesicle membrane tends to 'crinkle' or collapse depending on the concentration of the other components of the fixative solution. The 'crinkling' or collapse are largely reversed by a wash step in the absence of Ca.(c) The presence of Ca results in the appearance of a population of vesicles which form characteristic fusions or 'tight' junctions with the terminal membrane. This appears to be morphological evidence for the proposal, which has been frequently put forward, that Ca facilitates such a fusion before discharge of vesicle-bound transmitter.With the discovery that the use of Ca-containing fixatives leads to the demonstration of a subpopulation of synaptic vesicles fused to the terminal membrane, we are led to propose that this is the ultrastructural location of the newly synthesized acetylcholine which has been shown by others to be preferentially released by stimulation.Recently, we (4) described fixation conditions which result in the appearance of a single, dense particle in many of the cholinergic vesicles of the neuroplaque junction of the electric ray, Narcine brasiliensis. Now we are presenting additional findings including the demonstration that calcium is necessary in the fixative solutions, if the particle is to be visualized.Oschman and Wall (29) have suggested that calcium-containing fixatives may facilitate the ultrastructural identification of calcium binding sites, which then appear as spots or plaques of high electron density. These electron-dense spots (EDS) were regarded as Ca binding sites in insect intestinal membranes because (a) they occurred only when Ca was included in the fixation solutions, and (b) they were visible in sections from aldehyde fixed, unosmicated tissues, indicating that the EDS have an intrinsic electron density. Hillman and Llinfis (15) and Oschman et al. (28) have recently analyzed Ca-dependent EDS in the membranes of the squid giant axon by energy dispersive X-ray "780

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Section: Possible Physiological Significance Of the Vesicular "Tight Junctions'supporting

confidence: 89%

Effects of Calcium-Containing Fixation Solutions on Cholinergic Synaptic Vesicles

Boyne

Bohan

Williams

1974

The Journal of Cell Biology

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“…Using conventional thin-section electron microscopy, Couteaux and Pécot-Dechavasine (1970) find fusing vesicles in close relation to active zones that are clearly different from fusing coated vesicles . In addition, Nickel and Potter (1970) have used freeze-etching, a technique that requires no chemical fixation, to examine the electric organ of Torpedo . Since the nerve terminals in this organ apparently contain few or no coated vesicles, the fusions they observe must predominantly involve synaptic vesicles .…”

Section: Discussionmentioning

confidence: 99%

“…If strong inference is the only recourse, there are two facts that should be considered . Synaptic vesicles do fuse with the presynaptic membrane in resting terminals, and both Couteaux and Pécot-Dechavassine (1970) and Nickel and Potter (1970) have demonstrated this . Much greater numbers of synaptic vesicles fuse with the presynaptic membrane in nerve terminals treated with BWSV.…”

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confidence: 90%

Changes in the Fine Structure of the Neuromuscular Junction of the Frog Caused by Black Widow Spider Venom

Clark

Hurlbut

Mauro

1972

The Journal of Cell Biology

199

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Application of black widow spider venom to the neuromuscular junction of the frog causes an increase in the frequency of miniature end-plate potentials (min.e.p.p.) and a reduction in the number of synaptic vesicles in the nerve terminal. Shortly after the increase in min.e.p.p. frequency, the presynaptic membrane of the nerve terminal has either infolded or "lifted." Examination of these infoldings or lifts reveals synaptic vesicles in various stages of fusion with the presynaptic membrane. After the supply of synaptic vesicles has been exhausted, the presynaptic membrane returns to its original position directly opposite the end-plate membrane. The terminal contains all of its usual components with the exception of the synaptic vesicles. The only other alteration of the structures making up the neuromuscular junction occurs in the axon leading to the terminal. Instead of completely filling out its Schwann sheath, the axon has pulled away and its axoplasm appears to be denser than the control. The relation of these events to the vesicle hypothesis is discussed.

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“…I. HUBBARD AND S. F. JONES sumably contained in vesicles, with nerve terminal membranes (Del Castillo & Katz, 1956a). Concurrently however with increasing evidence that vesicles do contain and release acetylcholine (ACh) (De Robertis, 1964;Elmqvist & Quastel, 1965;Whittaker, 1965;Sheridan, Whittaker & Israel, 1966;Israel, Gautron & Lesbats, 1968;Jones & Kwanbunbumpen, 1970a, b; Nickel & Potter, 1970;Potter, 1970;Heuser, Katz & Miledi, 1971) has been the accumulation of evidence that vesicles are not randomly arranged in nerve terminals but are congregated adjacent to specific anatomical featuresat neuromuscular junctions, particularly the dense staining areas of the nerve terminal membrane and the subsynaptic folds of the muscle membrane (Birks, Huxley & Katz, 1960;Hubbard & Kwanbunbumpen, 1968).…”

Section: Introductionmentioning

confidence: 99%

Spontaneous quantal transmitter release: a statistical analysis and some implications

Hubbard¹,

Jones²

1973

The Journal of Physiology

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1. Miniature end-plate potentials (m.e.p.p.s) were intra- and extracellularly recorded from neuromuscular junctions in rat phrenic nerve-diaphragm preparations in vitro.2. Statistical analysis of the intervals between m.e.p.p.s showed that when the mean number of events in time t was plotted as a function of the variance of the events in time t there was a significant deviation from the straight line relationship expected for a Poisson process. Computer simulation showed that this deviation is explicable if release was generated by the random phasing of the activity of a number of releasing sites.3. There was no indication that release of one quantum influences the probability of release of remaining quanta (drag, clustering). It is suggested that m.e.p.p.s whose amplitude is larger than the mode result from the release of the contents of vesicles whose volume is also supramodal.4. The effects of depolarization of nerve terminals upon the variance-mean curve suggest an increase in the activity of sites rather than an increase in their number.5. Statistical analysis indicated at least 200 +/- 100 (mean +/- 1 S.E.) releasing sites. This number is of the same order as the number of sites of vesicle aggregation and presynaptic membrane density seen in electron micrographs of nerve terminals of this preparation.

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Synaptic vesicles in freeze-etched electric tissue of Torpedo

Cited by 46 publications

References 7 publications

Effects of Calcium-Containing Fixation Solutions on Cholinergic Synaptic Vesicles

Effects of Calcium-Containing Fixation Solutions on Cholinergic Synaptic Vesicles

Changes in the Fine Structure of the Neuromuscular Junction of the Frog Caused by Black Widow Spider Venom

Spontaneous quantal transmitter release: a statistical analysis and some implications

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