Involvement of Actin Polymerization in Vesicle Recruitment at the Calyx of Held Synapse

Sakaba, Takeshi; Neher, Erwin

doi:10.1523/jneurosci.23-03-00837.2003

Cited by 112 publications

(120 citation statements)

References 81 publications

(107 reference statements)

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“…Depolymerization of actin filaments suppresses the recovery of releasable SVs after depletion (12). Furthermore, we have reported that the posttetanic increase in the ratio of the FRP to SRP is abolished by inhibition of myosin ATPase (8).…”

Section: Recovery Of Rapidly Releasing Vesicles After a Predepleting mentioning

confidence: 87%

Actin-dependent rapid recruitment of reluctant synaptic vesicles into a fast-releasing vesicle pool

Lee

2012

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

105

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Glutamatergic synaptic terminals harbor reluctant synaptic vesicles (SVs) that contribute little to synchronous release during action potentials but are release competent when stimulated by sucrose or by direct intracellular application of calcium. It has been noted that the proximity of a release-competent SV to the calcium source is one of the primary factors that differentiate reluctant SVs from fastreleasing ones at the calyx of Held synapse. It has not been known whether reluctant SVs can be converted into fast-releasing ones. Here we show that reluctant SVs are recruited rapidly in an actindependent manner to become fast-releasing SVs once the pool of fast-releasing SVs is depleted by a short depolarization. Recovery of the pool of fast-releasing SVs was accompanied by a parallel reduction in the number of reluctant SVs. Quantitative analysis of the time course of depletion of fast-releasing SVs during high-frequency stimulation revealed that in the early phase of stimulation reluctant SVs are converted rapidly into fast-releasing ones, thereby counteracting short-term depression. During the late phase, however, after reluctant vesicles have been used up, another process of calmodulindependent recruitment of fast-releasing SVs is activated. These results document that reluctant SVs have a role in short-term plasticity and support the hypothesis of positional priming, which posits that reluctant vesicles are converted into fast-releasing ones via relocation closer to Ca 2+ -channels.readily releasable pool | synaptic vesicle dynamics S ynaptic strength is determined by quantal size, the number of release-competent synaptic vesicles (SVs), and their release probability (Pr). The estimate for the number of release-competent SVs, which also is referred to as the "readily releasable pool (RRP) size," depends heavily on the method used for its determination. The RRP size estimated by a cumulative plot of the excitatory postsynaptic currents (EPSC) amplitudes evoked by high-frequency afferent fiber stimulation (RRP cum ) is smaller than that estimated by the application of a hypertonic sucrose solution or presynaptic strong depolarization (1-3). This discrepancy reflects the presence of reluctant SVs, which are scarcely released by an action potential (AP) at glutamatergic synaptic terminals. Consistently, deconvolution analysis of EPSCs evoked by a long depolarizing pulse at the calyx of Held revealed that release-competent SVs can be separated into fast-and slowreleasing SV pools (FRP and SRP, respectively) (4). The FRP vesicles are responsible for phasic release during a high-frequency train of action potentials (APs), whereas the SRP vesicles contribute primarily to asynchronous release, when the intracellular concentration of calcium ions ([Ca 2+ ]) is increased globally during the late period of the train (2). Thus, SRP vesicles can be regarded largely as reluctant SVs at the calyx of Held.Despite the evidence for the presence of reluctant SVs at glutamatergic synapses, their role in short-term plasticity i...

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Section: Recovery Of Rapidly Releasing Vesicles After a Predepleting mentioning

confidence: 87%

Actin-dependent rapid recruitment of reluctant synaptic vesicles into a fast-releasing vesicle pool

Lee

2012

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

105

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“…Actin surrounds clusters of synaptic vesicles in presynaptic terminals and concentrates synapsin-1 at vesicle clusters (55). It also plays an important role in the dynamics of synaptic vesicle transfer to the readily releasable pool that is poised for rapid exocytosis, and both synapsin-1 and CaM are involved in those processes (55)(56)(57). Synapsin-1 is phosphorylated at Ser-603, which regulates trafficking of synaptic vesicles in vivo (54).…”

Section: Discussionmentioning

confidence: 99%

Ca2+-independent Activation of Ca2+/Calmodulin-dependent Protein Kinase II Bound to the C-terminal Domain of CaV2.1 Calcium Channels

Magupalli

Mochida

Jin

et al. 2013

Journal of Biological Chemistry

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“…Moreover, recovery of the fast-releasing vesicles was retarded, when recovery of the slowly releasing vesicles was slowed by disruption of actin polymerization or depletion of ATP in the presynaptic terminal (Sakaba and Neher, 2003). These observations led to the working hypothesis that the fast-releasing vesicles are derived from maturation from the slowly releasing synaptic vesicles (Wu and Borst, 1999;Sakaba and Neher, 2003). At the calyx of Held, the recruitment rate of the slowly releasing vesicles is 10 vesicles ms Ϫ1 , which persists even during a 500 ms step depolarization (our unpublished observation).…”

Section: Discussionmentioning

confidence: 99%

Roles of the Fast-Releasing and the Slowly Releasing Vesicles in Synaptic Transmission at the Calyx of Held

Sakaba¹

2006

J. Neurosci.

120

150

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In the calyx of Held, fast and slow components of neurotransmitter release can be distinguished during a step depolarization. The two components show different sensitivity to molecular/pharmacological manipulations. Here, their roles during a high-frequency train of action potential (AP)-like stimuli were examined by using both deconvolution of EPSCs and presynaptic capacitance measurements. During a 100 Hz train of AP-like stimuli, synchronous release showed a pronounced depression within the 20 stimuli. Asynchronous release persisted during the train, was variable in its amount, and was more prominent during a 300 Hz train. We have shown previously that slowly releasing vesicles were recruited faster than fast-releasing vesicles after depletion. By further slowing recovery of the fastreleasing vesicles by inhibiting calmodulin-dependent processes (Sakaba and Neher, 2001b), the slowly releasing vesicles were isolated during recovery from vesicle depletion. When a high-frequency train was applied, the isolated slowly releasing vesicles were released predominantly asynchronously. In contrast, synchronous release was mediated mainly by the fast-releasing vesicles. The results suggest that fast-releasing vesicles contribute mainly to synchronous release and that depletion of fast-releasing vesicles shape the synaptic depression of the synchronous phase of EPSCs, whereas slowly releasing vesicles are released mainly asynchronously during highfrequency stimulation. The latter is less subject to depression presumably because of a rapid vesicular recruitment process, which is a characteristic of this component.

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Involvement of Actin Polymerization in Vesicle Recruitment at the Calyx of Held Synapse

Cited by 112 publications

References 81 publications

Actin-dependent rapid recruitment of reluctant synaptic vesicles into a fast-releasing vesicle pool

Actin-dependent rapid recruitment of reluctant synaptic vesicles into a fast-releasing vesicle pool

Ca2+-independent Activation of Ca2+/Calmodulin-dependent Protein Kinase II Bound to the C-terminal Domain of CaV2.1 Calcium Channels

Roles of the Fast-Releasing and the Slowly Releasing Vesicles in Synaptic Transmission at the Calyx of Held

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