ATP-Dependent calcium uptake by cholinergic synaptic vesicles isolated fromtorpedo electric organ

Israël, Maurice; Manaranche, R.; Marsal, Jordi; Meunier, François-Marie; Morel, Nicolas; Frachon, Paule; Lesbats, B.

doi:10.1007/bf01940565

Cited by 100 publications

(49 citation statements)

References 41 publications

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“…Further, recent modeling efforts have emphasized the important role played by intraterminal calcium buffering in kinetics of transmitter release (28)(29)(30)(31)(32)(33). These results are interesting in light of our own because of the several lines of evidence indicating that synaptic vesicles can act as strong buffers of cytosolic calcium (17,(34)(35)(36)(37)(38)(39). Given the packed vesicle morphology of layer Ib synapses and calcium uptake by presynaptic vesicles, we would expect a substantially increased calcium buffering capacity in these synapses.…”

Section: Discussionmentioning

confidence: 85%

Facilitating and nonfacilitating synapses on pyramidal cells: a correlation between physiology and morphology.

Bower¹,

Haberly

1986

Proc. Natl. Acad. Sci. U.S.A.

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Pyramidal cells in piriform cortex receive excitatory inputs from two different sources that are segregated onto adjacent segments of their apical dendrites. The present studies show that excitatory postsynaptic potentials (EPSPs) evoked by primary olfactory tract afferents that terminate on distal apical segments display paired shock facilitation whereas ESPSs evoked by intrinsic association fibers that terminate on proximal apical segments do not. An ultrastructural comparison of the presynaptic elements of these two fiber systems has revealed that the facilitating olfactory tract afferent synapses have a much lower packing density of synaptic vesicles than do the nonfacilitating association fiber synapses. Further, a search of the literature has revealed that where both morphological and physiological data are available for the same synapses, this same correlation appears to apply. We propose a hypothesis to account for this correlation based on synaptic vesicles to buffer internal calcium and the biochemical characteristics of preterminal calcium-dependent mechanisms affecting the number of vesicles available for release.At many synapses, the second of an identical pair of appropriately timed presynaptic activations evokes a larger excitatory postsynaptic potential (EPSP) than the first (1-4). This synaptic property, termed paired shock facilitation, has been demonstrated in numerous peripheral and central nervous system synapses. However, there are also synapses that do not facilitate. The factors underlying this difference in the physiological characteristics of different synapses are as yet unknown, but presumably a fundamental mechanism regulating neurotransmitter release is involved. We report here the existence of a system that appears to be well suited for study of the mechanism of paired shock facilitation. Using in vitro brain slices of olfactory (piriform) cortex, we have found that the apical dendrites of single pyramidal cells are contacted by facilitating and nonfacilitating synapses with each type spatially segregated from the other and arising from different fiber systems. Specifically, EPSPs evoked by primary olfactory tract afferents that terminate on distal apical dendritic segments display paired shock facilitation, whereas EPSPs evoked by intrinsic association fibers that terminate on proximal apical segments do not (see Fig. 1). Previous ultrastructural studies comparing the presynaptic elements of these two fiber systems showed that the facilitating olfactory tract afferent synapses have a much lower packing density of synaptic vesicles than do the nonfacilitating association fiber synapses. Further, a search of the literature has revealed that where both morphological and physiological data are available, this same correlation appears to apply for other excitatory synapses. We therefore propose a hypothesis that may account for this correlation based on the ability of synaptic vesicles to buffer internal calcium and therefore affect the ability of subsequent vesicles to be mobi...

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Section: Discussionmentioning

confidence: 85%

Facilitating and nonfacilitating synapses on pyramidal cells: a correlation between physiology and morphology.

Bower¹,

Haberly

1986

Proc. Natl. Acad. Sci. U.S.A.

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“…In brief, cholinergic synaptic vesicles were obtained from the electric organ of Torpedo by sucrose gradient centrifugation (17). Ionic concentration of synaptic vesicle fractions was lowered by controlled dialysis in an isosmotic medium.…”

Section: Methodsmentioning

confidence: 99%

Control of neurotransmitter release by an internal gel matrix in synaptic vesicles

Reigada

Díez‐Pérez

Gorostiza

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

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Neurotransmitters are stored in synaptic vesicles, where they have been assumed to be in free solution. Here we report that in Torpedo synaptic vesicles, only 5% of the total acetylcholine (ACh) or ATP content is free, and that the rest is adsorbed to an intravesicular proteoglycan matrix. This matrix, which controls ACh and ATP release by an ion-exchange mechanism, behaves like a smart gel. That is, it releases neurotransmitter and changes its volume when challenged with small ionic concentration change. Immunodetection analysis revealed that the synaptic vesicle proteoglycan SV2 is the core of the intravesicular matrix and is responsible for immobilization and release of ACh and ATP. We suggest that in the early steps of vesicle fusion, this internal matrix regulates the availability of free diffusible ACh and ATP, and thus serves to modulate the quantity of transmitter released.

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“…They may function as internal Ca 2+ stores to supply localized regions for initiation of neurotransmitter exocytosis [21], or as Ca 2+ loaded bags useful for its exocytotic extrusion [20]. Indeed, it has been reported that synaptic vesicles are able to take up Ca 2+ by an ATP-dependent process [11,16], but the mechanisms of Ca 2+ accumulation are not still clarified. Although several types of ATPase systems have been observed [3,10,16,22,23], their activities were not well distinguished with respect to their specific biochemical characteristics.…”

mentioning

confidence: 99%

Ca2+-H+ antiport activity in synaptic vesicles isolated from sheep brain cortex

Gonçalves

Meireles

Gravato

et al. 1998

Neuroscience Letters

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Synaptic vesicles isolated from sheep brain cortex exhibit an ATP-dependent Ca 2+ accumulation that is inhibited by the protonophore uncoupler carbonyl cyanide m-chorophenylhydrazone (CCCP) and completely released by the Ca 2+ ionophore ionomycin. This transport activity was sensitive to the V-type ATPase inhibitor, bafilomycin, but not to the P-type ATPase inhibitor, vanadate. We also observed that the proton gradient, established across the synaptic vesicle membranes in the presence of ATP, is partially dissipated by the addition of Ca 2+ (100-860 mM) in correlation to an increase of ATP hydrolysis by the H + -pumping ATPase. In contrast, the activity of the H

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ATP-Dependent calcium uptake by cholinergic synaptic vesicles isolated fromtorpedo electric organ

Cited by 100 publications

References 41 publications

Facilitating and nonfacilitating synapses on pyramidal cells: a correlation between physiology and morphology.

Facilitating and nonfacilitating synapses on pyramidal cells: a correlation between physiology and morphology.

Control of neurotransmitter release by an internal gel matrix in synaptic vesicles

Ca2+-H+ antiport activity in synaptic vesicles isolated from sheep brain cortex

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