A Selective Activity-Dependent Requirement for Dynamin 1 in Synaptic Vesicle Endocytosis

Ferguson, Shawn M.; Brasnjo, Gabor; Hayashi, Mitsuko; Wölfel, Markus; Collesi, Chiara; Giovedì, Silvia; Raimondi, Andrea; Gong, Lin; Ariel, Pablo; Paradise, Summer; O’Toole, Eileen; Flavell, Richard A.; Cremona, Ottavio; Miesenböck, Gero; Ryan, Timothy A.; Camilli, Pietro De

doi:10.1126/science.1140621

Cited by 459 publications

(667 citation statements)

References 36 publications

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“…2) and dynamin-catalyzed fission 58,67 . In agreement with this, dynamin 1 knockout mice exhibit a striking, activity-dependent accumulation of tubular coated endocytic intermediates 48 . Data from dynamin temperature-sensitive mutant flies (shibire ts ) suggest a possible role for dynamin that may go beyond its established role in endocytic membrane fission (see below).…”

Section: Box 1 | Presynaptic Organization -Exocytic and Endocytic Zonesmentioning

confidence: 54%

“…Molecular analysis using genetic, biochemical and optical imaging approaches have provided strong evidence for an important, if not essential, role of clathrin-and dynamin-mediated endocytosis in synaptic vesicle reformation 11,48 . Acute chemical, sustained genetic or RnAi-mediated perturbation of clathrin 11 or dynamin function in a variety of organisms and model systems 7,48-51 causes strong defects in synaptic vesicle recycling.…”

Section: Box 1 | Presynaptic Organization -Exocytic and Endocytic Zonesmentioning

confidence: 99%

“…Although a precise mechanism has not yet emerged, several tentative connections between dynamin and Ca 2+ -dependent exocyticendocytic coupling have been uncovered. Dynamin 1 knockout mice display severe defects in synaptic vesicle endocytosis during stimulus-driven Ca 2+ influx 48 .…”

Section: Super-resolution Light Microscopic Techniquesmentioning

confidence: 99%

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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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Section: Box 1 | Presynaptic Organization -Exocytic and Endocytic Zonesmentioning

confidence: 54%

Section: Box 1 | Presynaptic Organization -Exocytic and Endocytic Zonesmentioning

confidence: 99%

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Protein scaffolds in the coupling of synaptic exocytosis and endocytosis

2011

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“…Block of dynamin I function has no effect on the final endosomal scission step under elevated stimulation conditions where a dynamin II and clathrin mediated process predominates in adrenal chromaffin cells [4,22]. This seems not to extend to neuronal preparations where dynamin I seems to be directly associated with clathrin-mediated internalization of small, clear vesicle membrane [46][47][48] where it is activated under elevated stimulus conditions [26,[49][50][51]. This point is of note for several reasons.…”

Section: Discussionmentioning

confidence: 97%

“…Chronic disruption of dynamin I may result in overall poor cell health. Genetic knock out of dynamin I results in compromised animal health and viability [26]. In order to guard against non-specific effects of chronic dynamin I disruption, we chose an alternate disruption approach.…”

Section: Membrane Trafficking Exhibits Differential Activity-dependenmentioning

confidence: 99%

Dynamin I plays dual roles in the activity-dependent shift in exocytic mode in mouse adrenal chromaffin cells

Fulop

Doreian

Smith

2008

Archives of Biochemistry and Biophysics

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Under low stimulation, adrenal chromaffin cells release freely-soluble catecholamines through a restricted granule fusion pore while retaining the large neuropeptide-containing proteinacious granule core. Elevated activity causes dilation of the pore and release of all granule contents. Thus, physiological differential transmitter release is achieved through regulation of fusion pore dilation. We examined the mechanism for pore dilation utilizing a combined approach of peptide transfection, electrophysiology, electrochemistry and quantitative imaging techniques. We report that disruption of dynamin I function alters both fusion modes. Under low stimulation, interference with dynamin I does not affect granule fusion but blocks its re-internalization. In full collapse mode, disruption of dynamin I limits fusion pore dilation, but does not block membrane re-internalization. These data suggest that dynamin I is involved in both modes of exocytosis by regulating contraction or dilation of the fusion pore and thus contributes to activity-dependent differential transmitter release from the adrenal medulla.

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Balancing presynaptic release and endocytic membrane retrieval at hair cell ribbon synapses

Pangršič

Vogl

2018

FEBS Letters

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The timely and reliable processing of auditory and vestibular information within the inner ear requires highly sophisticated sensory transduction pathways. On a cellular level, these demands are met by hair cells, which respond to sound waves – or alterations in body positioning – by releasing glutamate‐filled synaptic vesicles (SVs) from their presynaptic active zones with unprecedented speed and exquisite temporal fidelity, thereby initiating the auditory and vestibular pathways. In order to achieve this, hair cells have developed anatomical and molecular specializations, such as the characteristic and name‐giving ‘synaptic ribbons’ – presynaptically anchored dense bodies that tether SVs prior to release – as well as other unique or unconventional synaptic proteins. The tightly orchestrated interplay between these molecular components enables not only ultrafast exocytosis, but similarly rapid and efficient compensatory endocytosis. So far, the knowledge of how endocytosis operates at hair cell ribbon synapses is limited. In this Review, we summarize recent advances in our understanding of the SV cycle and molecular anatomy of hair cell ribbon synapses, with a focus on cochlear inner hair cells.

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A Selective Activity-Dependent Requirement for Dynamin 1 in Synaptic Vesicle Endocytosis

Cited by 459 publications

References 36 publications

Protein scaffolds in the coupling of synaptic exocytosis and endocytosis

Protein scaffolds in the coupling of synaptic exocytosis and endocytosis

Dynamin I plays dual roles in the activity-dependent shift in exocytic mode in mouse adrenal chromaffin cells

Balancing presynaptic release and endocytic membrane retrieval at hair cell ribbon synapses

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