Cited by 238Cellular transport and secretionNeuroscience and Neuropharmacology ResearchExtracellular vesicles in disease

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Molecular Circuitry of Endocytosis at Nerve Terminals

Dittman, Jeremy, Ryan, Timothy A.·2009·Annual Review of Cell and Developmental Biology

DOI 10.1146/annurev.cellbio.042308.113302

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Abstract

Presynaptic terminals are specialized compartments of neurons responsible for converting electrical signals into secreted chemicals. This self-renewing process of chemical synaptic transmission is accomplished by the calcium-triggered fusion of neurotransmitter-containing vesicles with the plasma membrane and subsequent retrieval and recycling of vesicle components. Whereas the release of neurotransmitters has been studied for over 50 years, the process of synaptic vesicle endocytosis has remained much more elusive. The advent of imaging techniques suited to monitor membrane retrieval at presynaptic terminals and the discovery of the molecules that orchestrate endocytosis have revolutionized our understanding of this critical trafficking event.

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Background
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BackgroundMethod
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BackgroundSelf-citation
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“See supplemental figure 1 for red-green images 3568 | The Journal of Comparative Neurology JOHNSON ET AL. presynaptic Ca21 entry into the terminal critical for neurotransmitter release (Dittman & Ryan, 2009).”
Background
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Background
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Background
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“In contrast, an accessory protein of CME, such as dynamin, was neither enriched on CCVs nor stripped, indicating that it does not function as classical clathrin adaptor (Slepnev and De Camilli, 2000).”
MethodInfluential
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Background
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“Neurons have a specific trafficking system for synaptic vesicle (SV) dynamics (summarized in [1–3]).”
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“…but also endocytic pathways contribute to this process (Südhof, 2004; Schweizer and Ryan, 2006; LoGiudice and Matthews, 2007; Wu L.-G. et al., 2007; Dittman and Ryan, 2009; Yamashita, 2012; Rizzoli, 2014; Wu X.-S. et al., 2014; Kononenko and Haucke, 2015; Soykan et al., 2016; Watanabe and Boucrot,…”
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Binocular pattern deprivation interferes with the expression of proteins involved in primary visual cortex maturation in the cat
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“In principle, several mechanisms coupling endo- to exocytosis are conceivable: The membrane and proteins of the fused vesicles could diffuse laterally in the plasma membrane and represent a trigger for the endocytotic machinery (Dittman & Ryan, 2009).”
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Cortical Surface Area Correlates with STON2 Gene Ser307Pro Polymorphism in First-Episode Treatment-Naïve Patients with Schizophrenia
Xiang, B., Wu, J.-Y., Wang, Q., Li, M., Jiang, L.-J., Deng, W., Chen, Z., He, Z., Huang, C.-H., Han, Y., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064090 · Cited by 7
“Transport, fusion, and recycling of SV affected the normal synaptic function and were critical in maintaining the ability of the synapse to release a neurotransmitter based on sustained stimulation [30,31,32].”
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“Similarly, after the release event the molecules have to be recycled, regenerated, and resorted, which also consumes energy and time (Dittman and Ryan, 2009; LoGiudice and Matthews, 2007; Smith et al., 2008).”
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“Most cell types, including bipolar cells and the calyx of Held, exhibit at least two kinetic components to membrane retrieval (von Gersdorff & Matthews, 1994 b ; Neves & Lagnado, 1999 ; Wu et al., 2005 ; Dittman & Ryan, 2009 ).”
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The Calyx of Held Synapse
Borst, J. G., & Rusu, S. (2012) · Springer handbook of auditory research · doi:10.1007/978-1-4419-9517-9_5 · Cited by 14
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“Their results formed the basis of a model according to which synaptic vesicles collapse fully into the plasma membrane and are subsequently recycled through the formation of membrane ‘pits’, which become surrounded by a coat protein called clathrin and bud off as new vesicles.”
BackgroundResultInfluential
Lipids in the Processes of Exo- and Endocytosis of Synaptic Vesicles
Zefirov, A. L., & Petrov, A. M. (2011) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-011-9547-x · Cited by 5
“It has been suggested that the different stages of endocytosis involve not only clathrin, but a whole group of proteins: AP-2, AP-180, stonin, eps 15, epsin, endophilin, syndapin, dynamin, auxilin, Hsc70, synaptojanin, and others [3, 9].”
BackgroundInfluential
Differentiated SH-SY5Y cells exhibit neuronal features but lack synaptic maturity
Leuenberger, J., Ott, G., Nevian, T., Zuber, B., & Rostami, I. (2026) · Cell Death Discovery · doi:10.1038/s41420-026-03094-y · Cited by 4
“The medium was exchanged every three days until day 28.”
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Watanabe, S. (2025) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-112723-040652 · Cited by 4
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The AP-2 complex interacts with γ-TuRC and regulates the proliferative capacity of neural progenitors
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“AP-2 is the major clathrin adaptor protein for the CME (Robinson, 2004), which functions as a heterotetrameric complex comprised of α , β , μ , and σ subunits (Dittman & Ryan, 2009).”
Background
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“Muchhasbeen learnedabout the molecular composition, assembly, and function of synapses, the cellular junctions through which neurons communicate (1-3).”
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Genetic Analysis of Synaptogenesis
Lu, C. S., & Vactor, D. V. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397266-8.00104-6 · Cited by 3
A Surprisingly Singular Role for Endophilin in Synaptic Vesicle Recycling
Sullivan, J. (2011) · Neuron · doi:10.1016/j.neuron.2011.10.025 · Cited by 3
“Synaptojanin is then well positioned to degrade PI(4,5)P2 in the vesicle membrane, an essential step in the clathrin removal process (Dittman and Ryan, 2009).”
Background
Molecular and Morphological Correlates of Synaptic Vesicle Priming
Imig, C. (2014) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-4755 · Cited by 3
Live-cell imaging of endocytosed synaptophysin around individual hippocampal presynaptic active zones
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“However, the large size of quantum dots might have affected fusion pore openings and vesicle collapse (Dittman and Ryan, 2009).”
Background
Overview: Presynaptic Terminal Proteins Orchestrate Stepwise Synaptic Vesicle Phases
Mochida, S. (2014) · Springer eBooks · doi:10.1007/978-4-431-55166-9_1 · Cited by 2
“Modules often present in such factors include SH3 domains, BAR domains, ENTH/ANTH, and PH domains, whereas short amino acid motifs include proline-containing motifs (for SH3 domain binding), NPF motifs (for EH domain binding), clathrin boxes (for clathrin binding), and several motifs that recognize the appendage domai…”
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Nitric Oxide and Synaptic Transmission in the Cerebellum
Collado‐Alsina, A., Rampérez, A., Sánchez‐Prieto, J., & Torres, M. (2021) · Springer eBooks · doi:10.1007/978-3-030-23810-0_112 · Cited by 2
Optical analysis of synaptic vesicle protein molecules during exo- and endocytosis using pH-switchable fluorescent probes
Sinha, R. (2011) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-3156 · Cited by 2
A Single Vesicle Assay to Study the Electrochemical Gradient Regulation in Glutamatergic and GABAergic Synaptic Vesicles
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Autophagy and Protein Quality Control in Parkinson's DiseasePreprint
Martínez‐Vicente, M., & Vila, M. (2024) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a041619 · Cited by 2
Robust inhibitory glycinergic transmission and the effect of bafilomycin, folimycin and EIPA: lessons from the auditory brainstem
Pizzi, E., Hofmann, L. N., Singh, A., & Friauf, E. (2025) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2025.1625868 · Cited by 1
Key Events in Synaptic Vesicle Endocytosis
Ackermann, F., Joshua, A. M., & Brodi, L. (2012) · InTech eBooks · doi:10.5772/45785 · Cited by 1
“In many studies, however, the occurrence of bulk endocytosis in nerve terminals has been linked to non-physiological conditions, including excessive stimulation, or moderate stimulation combined with disruption of the clathrin machinery (15,24).”
Synaptische Übertragung
Heckmann, M., & Dudél, J. (2010) · Springer-Lehrbuch · doi:10.1007/978-3-642-01651-6_5 · Cited by 1
Presynaptic quantal size enhancement counteracts post‐tetanic release depression
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Molecular Chaperones in the Mammalian Brain: Regional Distribution, Cellular Compartmentalization and Synaptic Interactions
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“In nerve terminals where transmitter release is the most dynamic membrane trafficking event, AP-2 and AP-180 are particularly important adaptor proteins ( Dittman and Ryan 2009 ).”
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Soluble membrane trafficking proteins taking a break at silent synaptic vesicles
Brodin, L., Gregory, J. A., & Ackermann, F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113641108 · Cited by 1
“In response to action potentials, vesicles fuse with the plasma membrane to release neurotransmitter, which is followed by vesicle recycling via endocytosis (1).”
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Endocytic Machinery at the Neuronal Synapse
Milošević, I. (2014) · Springer eBooks · doi:10.1007/978-4-431-55166-9_10 · Cited by 1

Authors: Dittman, J., & Ryan, T. A.
Affiliations: Weill Cornell Medicine (US)
ORCID: Dittman, Jeremy
Ryan, Timothy A.
Venue: Annual Review of Cell and Developmental Biology
Publisher: Annual Reviews
Published: 2009-11-01
Volume: 25
Issue: 1
Pages: 133-160
ISSN: 1081-0706 (ISSN-L)
1530-8995
DOI: 10.1146/annurev.cellbio.042308.113302
OpenAlex: W2167118899
Cited by: 238
References: 157
Citations by year: 2026: 4 · 2025: 5 · 2024: 5 · 2023: 7 · 2022: 7 · 2021: 8 · 2020: 20 · 2019: 9 · 2018: 6 · 2017: 9 · 2016: 8 · 2015: 22 · 2014: 27 · 2013: 28 · 2012: 28
FWCI: 1.85
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Cell and Developmental Biology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Neurological Disorders and Stroke (R01NS036942)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
Keywords: synaptic vesicle endocytosis, presynaptic terminals, neurotransmitter release, membrane retrieval, vesicle recycling, calcium-triggered exocytosis, synaptic vesicle trafficking, endocytic machinery
MeSH terms: Animals, Cell Membrane, Endocytosis, Synapses, Synaptic Vesicles, Presynaptic Terminals

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Molecular Circuitry of Endocytosis at Nerve Terminals

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