Developmental shift to a mechanism of synaptic vesicle endocytosis requiring nanodomain Ca2+

Yamashita, Takayuki; Eguchi, Kohgaku; Saitoh, Naoto; Gersdorff, Henrique von; Takahashi, Tomoyuki

doi:10.1038/nn.2576

Cited by 91 publications

(130 citation statements)

References 48 publications

(98 reference statements)

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“…Our data are difficult to reconcile with the assumption of a nanodomain control of exocytosis (Neher, 1998;Augustine et al, 2003;Brandt et al, 2005;Goutman and Glowatzki, 2007;Yamashita et al, 2010), at least in its extreme form. According to this assumption, the vesicle with its Ca 2ϩ sensors is in such close proximity to a Ca 2ϩ channel that it senses the gating of essentially this single channel only, and Ca 2ϩ influx through this single channel suffices to trigger the vesicle's fusion.…”

contrasting

confidence: 73%

An Improved Model for the Rate–Level Functions of Auditory-Nerve Fibers

Heil

Neubauer

Irvine³

2011

J. Neurosci.

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Acoustic information is conveyed to the brain by the spike patterns in auditory-nerve fibers (ANFs). In mammals, each ANF is excited via a single ribbon synapse in a single inner hair cell (IHC), and the spike patterns therefore also provide valuable information about those intriguing synapses. Here we reexamine and model a key property of ANFs, the dependence of their spike rates on the sound pressure level of acoustic stimuli (rate-level functions). We build upon the seminal model of Sachs and Abbas (1974), which provides good fits to experimental data but has limited utility for defining physiological mechanisms. We present an improved, physiologically plausible model according to which the spike rate follows a Hill equation and spontaneous activity and its experimentally observed tight correlation with ANF sensitivity are emergent properties. We apply it to 156 cat ANF rate-level functions using frequencies where the mechanics are linear and find that a single Hill coefficient of 3 can account for the population of functions. We also demonstrate a tight correspondence between ANF rate-level functions and the Ca 2ϩ dependence of exocytosis from IHCs, and derive estimates of the effective intracellular Ca 2ϩ concentrations at the individual active zones of IHCs. We argue that the Hill coefficient might reflect the intrinsic, biochemical Ca 2ϩ cooperativity of the Ca 2ϩ sensor involved in exocytosis from the IHC. The model also links ANF properties with properties of psychophysical absolute thresholds.

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contrasting

confidence: 73%

An Improved Model for the Rate–Level Functions of Auditory-Nerve Fibers

Heil

Neubauer

Irvine³

2011

J. Neurosci.

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“…In contrast to the above conclusion, prolonging the stimulation train, which increases calcium influx, prolongs endocytosis at many preparations, such as goldfish ribbon-type synapses (von Gersdorff and Matthews, 1994), frog neuromuscular junctions (Wu and Betz, 1996), hippocampal synapses (Sankaranarayanan and Ryan, 2000;Balaji et al, 2008;Sun et al, 2010), calyces (Sun et al, 2002;Wu et al, 2005;Yamashita et al, 2005;Renden and von Gersdorff, 2007), and chromaffin cells (Artalejo et al, 1995;Elhamdani et al, 2006). A pioneering study two decades ago shows that increasing the intracellular calcium concentration at goldfish ribbon-type synapses inhibits endocytosis, suggesting that calcium inhibits endocytosis (von Gersdorff and Matthews, 1994).…”

Section: Introductionmentioning

confidence: 93%

“…Recent studies at calyces and hippocampal synapses show that calcium may speed up slow, rapid, and bulk endocytosis by tens of folds, suggesting that calcium triggers endocytosis (Hosoi et al, 2009;Wu et al, 2009;Sun et al, 2010). Consequently, how calcium triggers endocytosis has been actively studied (Sun et al, 2010;Yamashita et al, 2010;J. Yao et al, 2011;Yao and Sakaba, 2012;L.H.…”

Section: Introductionmentioning

confidence: 99%

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The Yin and Yang of Calcium Effects on Synaptic Vesicle Endocytosis

2014

J. Neurosci.

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A large number of studies suggest that calcium triggers and accelerates vesicle endocytosis at many synapses and non-neuronal secretory cells. However, many studies show that prolonging the duration of the stimulation train, which induces more calcium influx, slows down endocytosis; and several studies suggest that instead of triggering endocytosis, calcium actually inhibits endocytosis. Here we addressed this apparent conflict at a large nerve terminal, the calyx of Held in rat brainstem, in which recent studies suggest that transient calcium increase up to tens of micromolar concentration at the micro/nano domain triggers endocytosis. By dialyzing 0 -1 M calcium into the calyx via a whole-cell pipette, we found that slow endocytosis was inhibited by calcium dialysis in a concentration-dependent manner. Thus, prolonged, small, and global calcium increase inhibits endocytosis, whereas transient and large calcium increase at the micro/nano domain triggers endocytosis and facilitates endocytosis. This yin and yang effect of calcium may reconcile apparent conflicts regarding whether calcium accelerates or inhibits endocytosis. Whether endocytosis is fast or slow depends on the net outcome between the yin and yang effect of calcium.

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“…whether this channel is identical to the recently identified Drosophila melanogaster synaptic vesicle protein known as flower is not yet proven 76 . Differential sensitivity to Ca 2+ buffers suggests that local microdomain Ca 2+ created by multiple channels also underlies slow endocytosis at the calyx of Held 34,95 .…”

Section: Calcium Regulationmentioning

confidence: 99%

Protein scaffolds in the coupling of synaptic exocytosis and endocytosis

2011

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Communication between nerve cells largely occurs at chemical synapses -specialized sites of cell-cell contact where electrical signals trigger the exocytic release of neurotransmitter, which in turn activates postsynaptic receptor channels. The efficacy with which such chemical signals are transmitted is crucial for the functioning of the nervous system. Modulation of neurotransmission enables nerve cells to respond to a vast range of stimulus patterns. Synaptic activity can also be tremendously diverse; from the fast synapses of the hippocampus, to slow neuropeptide-containing synapses. Indeed, some signalling pathways are active in the absence of stimulation, such as those involved in the processing of sensory information, which transmit tonically at high rates of up to 100 Hz or more 1,2 .Intriguing questions arise from these facts, including how high rates of neurotransmission can be maintained over long periods of time, and what limits the ability of a given synapse to release neurotransmitter during sustained periods of activity. Recent data indicate that in many synapses, exocytosis of neurotransmitter is coupled to endocytosis, and that synapses have evolved a specialized apparatus of scaffolding proteins to comply with these demands. Such scaffolds aid the temporal and spatial coupling of exocytosis and endocytosis, and are crucial for maintaining rapid neurotransmission during sustained activity 3 .Exocytosis of neurotransmitter is triggered by stimulusinduced calcium influx into the nerve terminal 4,5 and the subsequent fusion of synaptic vesicles with the presynaptic plasma membrane at specialized regions called active zones (BOX 1). Exocytosed synaptic vesicle membrane proteins and lipids in turn are recycled at the endocytic or periactive zone (BOX 1) that surrounds the release site, to restore functional synaptic vesicle pools for reuse and to ensure long-term functionality of the synapse 6-8 (FIG. 1). Depending on the type of synapse and the stimulation frequency, several modes of endocytosis with different time constants -for example, fast and slow endocytosisseem to operate 7,9,10 . Clathrin-mediated endocytosis arguably represents the main pathway of synaptic vesicle endocytosis 6,8,11 , although other modes -for example, fast kiss-and-run exocytosis and endocytosis -could operate in parallel.Although the machineries for exocytic membrane fusion 12,13 and for endocytic retrieval of synaptic vesicle membranes have been studied separately in some detail 6,14 , comparatively little is known about the coupling between exocytosis and endocytosis. Here we synthesize recent data from physiological, morphological and biochemical studies in several model systems into hypothetical models for scaffold-based mechanisms underlying exocytic-endocytic coupling.The synaptic vesicle cycle Synaptic vesicle pools. Some defining features of chemical synapses are the presence of one or several clusters of synaptic vesicles in the presynaptic nerve terminal, and ultrastructural specializations at the pre-and postsy...

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Developmental shift to a mechanism of synaptic vesicle endocytosis requiring nanodomain Ca2+

Cited by 91 publications

References 48 publications

An Improved Model for the Rate–Level Functions of Auditory-Nerve Fibers

An Improved Model for the Rate–Level Functions of Auditory-Nerve Fibers

The Yin and Yang of Calcium Effects on Synaptic Vesicle Endocytosis

Protein scaffolds in the coupling of synaptic exocytosis and endocytosis

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