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Cited by 4Cellular transport and secretionNeuroscience and Neuropharmacology ResearchExtracellular vesicles in disease

Synaptic Vesicle Recycling Through the Lens of Ultrafast Endocytosis

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Watanabe, Shigeki·2025·Annual Review of Neuroscience
DOI 10.1146/annurev-neuro-112723-040652PMC PMC12536329
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Abstract

The mechanisms underlying synaptic vesicle endocytosis remain controversial. In the 1970s, Heuser and Reese put forward a hypothesis that clathrin-mediated endocytosis is the predominant vesicle retrieval mechanism. In their seminal papers, another pathway was also described: uncoated large vesicles or cisternae emanating from the plasma membrane 1 s after a single stimulus. This pathway likely represents a recently described ultrafast endocytic pathway that recovers synaptic vesicles during physiological stimuli. Had we known of the existence of ultrafast endocytosis or paid more attention to the cisternae-based uptake pathway, would the experimental results over subsequent years have been interpreted differently? Here, I retrospectively review the literature on synaptic vesicle recycling through the lens of ultrafast endocytosis.

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  • Ultrafast endocytosis occurs within 50-100 milliseconds following stimulation, capturing approximately four vesicles at the very edge of the active zone, and is kinetically distinct from kiss-and-run and CME.

    “Ultrafast endocytosis occurs rapidly, within 50–100 milliseconds following stimulation, capturing approximately four vesicles at the very edge of the active zone [32]. This mechanism is specialized for rapidly restoring the surface area of the presynaptic membrane and is kinetically distinct from both kiss-and-run and clathrin-mediated endocytosis [33].”

    From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [33]

    The “Ultrafast endocytosis” section (page unavailable) places uptake lateral to the active zone and says it typically completes within 100 ms, though it can take over a second. The “Mechanisms of ultrafast endocytosis” section (page unavailable) reports uptake of membrane equivalent to 3–4 vesicles under a specific high-calcium condition, not capture of four intact vesicles as a general rule. The separate claim about kinetic distinction is attached to citation [33], not this source’s citation [32]. (LLM, conf=0.86)

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References 85 · Cited by 4

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  1. Albillos A, Dernick G, Horstmann H, Almers W, Toledo G.A. de, and Lindau M, 1997. The exocytotic event in chromaffin cells revealed by patch amperometry. Nature, 389 (6650), 509– 512. 9333242
  2. Alés E, Tabares L, Poyato JM, Valero V, Lindau M, and Toledo G.A. de, 1999. High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nature Cell Biology, 1 (1), 40– 44. 10559862
  3. Alvarez de Toledo G, Fernández-Chacón R, and Fernández JM, 1993. Release of secretory products during transient vesicle fusion. Nature, 363 (6429), 554– 558. 8505984
  4. Anggono V, Smillie KJ, Graham ME, Valova VA, Cousin MA, and Robinson PJ, 2006. Syndapin I is the phosphorylation-regulated dynamin I partner in synaptic vesicle endocytosis. Nature neuroscience, 9 (6), 752– 760. 16648848 PMC2082060
  5. Antonny B, Burd C, De Camilli P, Chen E, Daumke O, Faelber K, Ford M, Frolov VA, Frost A, Hinshaw JE, Kirchhausen T, Kozlov MM, Lenz M, Low HH, McMahon H, Merrifield C, Pollard TD, Robinson PJ, Roux A, and Schmid S, 2016. Membrane fission by dynamin: what we know and what we need to know. The EMBO Journal, 35 (21), 2270– 2284. 27670760 PMC5090216
  6. Armbruster M, Messa M, Ferguson SM, De Camilli P, and Ryan TA, 2013. Dynamin phosphorylation controls optimization of endocytosis for brief action potential bursts. eLife, 2, e00845. 23908769 PMC3728620
  7. Ashrafi G, Wu Z, Farrell RJ, and Ryan TA, 2017. GLUT4 Mobilization Supports Energetic Demands of Active Synapses. Neuron, 93 (3), 606– 615.e3. 28111082 PMC5330257
  8. Balaji J, Armbruster M, and Ryan TA, 2008. Calcium control of endocytic capacity at a CNS synapse. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 28 (26), 6742– 6749. 18579748 PMC2671224
  9. del Castillo J and Katz B, 1956. Biophysical aspects of neuro-muscular transmission. Progress in Biophysics and Biophysical Chemistry, 6, 121– 170. 13420190
  10. Ceccarelli B, Hurlbut WP, and Mauro A, 1972. Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation. The Journal of Cell Biology, 54 (1), 30– 38. 4338962 PMC2108853
  11. Ceccarelli B, Hurlbut WP, and Mauro A, 1973. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. The Journal of Cell Biology, 57 (2), 499– 524. 4348791 PMC2108980
  12. Chanaday NL, Cousin MA, Milosevic I, Watanabe S, and Morgan JR, 2019. The Synaptic Vesicle Cycle Revisited: New Insights into the Modes and Mechanisms. Journal of Neuroscience, 39 (42), 8209– 8216. 31619489 PMC6794917
  13. Chanaday NL and Kavalali ET, 2018. Optical detection of three modes of endocytosis at hippocampal synapses. eLife, 7, e36097. 29683423 PMC5959719
  14. Chiang H-C, Shin W, Zhao W-D, Hamid E, Sheng J, Baydyuk M, Wen PJ, Jin A, Momboisse F, and Wu L-G, 2014. Post-fusion structural changes and their roles in exocytosis and endocytosis of dense-core vesicles. Nature Communications, 5, 3356. PMC4267856 24561832
  15. Cousin MA, 2009. Activity-dependent bulk synaptic vesicle endocytosis--a fast, high capacity membrane retrieval mechanism. Molecular Neurobiology, 39 (3), 185– 189. 19266323 PMC2871594
  16. Cousin MA, 2017. Integration of Synaptic Vesicle Cargo Retrieval with Endocytosis at Central Nerve Terminals. Frontiers in Cellular Neuroscience, 11. PMC5541026 28824381
  17. Delvendahl I, Vyleta NP, von Gersdorff H, and Hallermann S, 2016. Fast, Temperature-Sensitive and Clathrin-Independent Endocytosis at Central Synapses. Neuron, 90 (3), 492– 498. 27146271 PMC5125781
  18. Diril MK, Wienisch M, Jung N, Klingauf J, and Haucke V, 2006. Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Developmental cell, 10 (2), 233– 244. 16459302
  19. Eichel K, Jullié D, Barsi-Rhyne B, Latorraca NR, Masureel M, Sibarita J-B, Dror RO, and von Zastrow M, 2018. Catalytic activation of β-arrestin by GPCRs. Nature, 557 (7705), 381– 386. 29720660 PMC6058965
  20. Fatt P and Katz B, 1951. An analysis of the end-plate potential recorded with an intracellular electrode. The Journal of Physiology, 115 (3), 320– 370. 14898516 PMC1392060
  21. Fatt P and Katz B, 1952. Spontaneous subthreshold activity at motor nerve endings. The Journal of Physiology, 117 (1), 109– 128. 14946732 PMC1392564
  22. Ferguson SM, Brasnjo G, Hayashi M, Wölfel M, Collesi C, Giovedi S, Raimondi A, Gong L-W, Ariel P, Paradise S, O’Toole E, Flavell R, Cremona O, Miesenböck G, Ryan TA, and De Camilli P, 2007. A Selective Activity-Dependent Requirement for Dynamin 1 in Synaptic Vesicle Endocytosis. Science, 316 (5824), 570– 574. 17463283
  23. Fesce R, Grohovaz F, Valtorta F, and Meldolesi J, 1994. Neurotransmitter release: fusion or ‘kiss-and-run’? Trends in Cell Biology, 4 (1), 1– 4. 14731821
  24. Gan Q and Watanabe S, 2018. Synaptic Vesicle Endocytosis in Different Model Systems. Frontiers in Cellular Neuroscience, 12, 171. 30002619 PMC6031744
  25. Ge L, Shin W, Arpino G, Wei L, Chan CY, Bleck CKE, Zhao W, and Wu L-G, 2022. Sequential compound fusion and kiss-and-run mediate exo- and endocytosis in excitable cells. Science Advances, 8 (24), eabm6049. 35714180 PMC9205584
  26. von Gersdorff H and Matthews G, 1994. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature, 367 (6465), 735– 739. 7906397
  27. Gimber N, Tadeus G, Maritzen T, Schmoranzer J, and Haucke V, 2015. Diffusional spread and confinement of newly exocytosed synaptic vesicle proteins. Nature Communications, 6, 8392. PMC4598626 26399746
  28. Granseth B, Odermatt B, Royle SJ, and Lagnado L, 2006. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron, 51 (6), 773– 786. 16982422
  29. Gu M, Liu Q, Watanabe S, Sun L, Hollopeter G, Grant BD, and Jorgensen EM, 2013. AP2 hemicomplexes contribute independently to synaptic vesicle endocytosis. eLife, 2, e00190. 23482940 PMC3591783
  30. Haberstock-Debic H, Kim K-A, Yu YJ, and von Zastrow M, 2005. Morphine promotes rapid, arrestin-dependent endocytosis of mu-opioid receptors in striatal neurons. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 25 (34), 7847– 7857. 16120787 PMC6725258
  31. Harata NC, Aravanis AM, and Tsien RW, 2006. Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion. Journal of Neurochemistry, 97 (6), 1546– 1570. 16805768
  32. Harris TW, Hartwieg E, Horvitz HR, and Jorgensen EM, 2000. Mutations in Synaptojanin Disrupt Synaptic Vesicle Recycling. The Journal of Cell Biology, 150 (3), 589– 600. 10931870 PMC2175188
  33. Hayashi M, Raimondi A, O’Toole E, Paradise S, Collesi C, Cremona O, Ferguson SM, and De Camilli P, 2008. Cell- and stimulus-dependent heterogeneity of synaptic vesicle endocytic recycling mechanisms revealed by studies of dynamin 1-null neurons. Proceedings of the National Academy of Sciences of the United States of America, 105 (6), 2175– 2180. 18250322 PMC2538894
  34. He L and Wu L-G, 2007. The debate on the kiss-and-run fusion at synapses. Trends in Neurosciences, 30 (9), 447– 455. 17765328
  35. He L, Wu X-S, Mohan R, and Wu L-G, 2006. Two modes of fusion pore opening revealed by cell-attached recordings at a synapse. Nature, 444 (7115), 102– 105. 17065984
  36. Heuser J and Reese T, 1979. Synaptic-Vesicle Exocytosis Captured by Quick-Freezing. In: Fourth Intensive Study Program in the Neuroscience. Cambridge: M.I.T. press, 573– 600.
  37. Heuser JE and Reese TS, 1973. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. The Journal of Cell Biology, 57 (2), 315– 344. 4348786 PMC2108984
  38. Heuser JE and Reese TS, 1981. Structural changes after transmitter release at the frog neuromuscular junction. The Journal of Cell Biology, 88 (3), 564– 580. 6260814 PMC2112753
  39. Heuser JE, Reese TS, Dennis MJ, Jan Y, Jan L, and Evans L, 1979. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. The Journal of Cell Biology, 81 (2), 275– 300. 38256 PMC2110310
  40. Hua Y, Sinha R, Thiel CS, Schmidt R, Hüve J, Martens H, Hell SW, Egner A, and Klingauf J, 2011. A readily retrievable pool of synaptic vesicles. Nature neuroscience, 14 (7), 833– 839. 21666673
  41. Imoto Y, Raychaudhuri S, Ma Y, Fenske P, Sandoval E, Itoh K, Blumrich E-M, Matsubayashi HT, Mamer L, Zarebidaki F, Söhl-Kielczynski B, Trimbuch T, Nayak S, Iwasa JH, Liu J, Wu B, Ha T, Inoue T, Jorgensen EM, Cousin MA, Rosenmund C, and Watanabe S, 2022. Dynamin is primed at endocytic sites for ultrafast endocytosis. Neuron, S0896-6273(22) 00548– 7. PMC9464723 35809574
  42. Imoto Y, Xue J, Luo L, Raychaudhuri S, Itoh K, Ma Y, Craft GE, Kwan AH, Ogunmowo TH, Ho A, Mackay JP, Ha T, Watanabe S, and Robinson PJ, 2024. Dynamin 1xA interacts with Endophilin A1 via its spliced long C-terminus for ultrafast endocytosis. The EMBO Journal, 43 (16), 3327– 3357. 38907032 PMC11329700
  43. Jakobsson J, Gad H, Andersson F, Löw P, Shupliakov O, and Brodin L, 2008. Role of epsin 1 in synaptic vesicle endocytosis. Proceedings of the National Academy of Sciences of the United States of America, 105 (17), 6445– 6450. 18430801 PMC2359800
  44. Jospin M, Watanabe S, Joshi D, Young S, Hamming K, Thacker C, Snutch TP, Jorgensen EM, and Schuske K, 2007. UNC-80 and the NCA ion channels contribute to endocytosis defects in synaptojanin mutants. Current Biology: CB, 17 (18), 1595– 1600. 17825559
  45. Jullié D, Stoeber M, Sibarita J-B, Zieger HL, Bartol TM, Arttamangkul S, Sejnowski TJ, Hosy E, and von Zastrow M, 2020. A Discrete Presynaptic Vesicle Cycle for Neuromodulator Receptors. Neuron, 105 (4), 663– 677.e8. 31837915 PMC7035187
  46. Katz B., 1969. The Release of Neural Transmitter Substances. Liverpool: Liverpool University Press.
  47. Kavalali ET and Jorgensen EM, 2014. Visualizing presynaptic function. Nature Neuroscience, 17 (1), 10– 16. 24369372
  48. Kim SH and Ryan TA, 2009. Synaptic vesicle recycling at CNS synapses without AP-2. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 29 (12), 3865– 3874. 19321783 PMC2713063
  49. Kittelmann M, Liewald JF, Hegermann J, Schultheis C, Brauner M, Costa WS, Wabnig S, Eimer S, and Gottschalk A, 2013. In vivo synaptic recovery following optogenetic hyperstimulation. Proceedings of the National Academy of Sciences, 110 (32), E3007– E3016. PMC3740886 23878262
  50. Koenig JH and Ikeda K, 1989. Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 9 (11), 3844– 3860. 2573698 PMC6569944
  51. Koenig JH and Ikeda K, 1996. Synaptic vesicles have two distinct recycling pathways. The Journal of Cell Biology, 135 (3), 797– 808. 8909551 PMC2121054
  52. Koh T-W, Verstreken P, and Bellen HJ, 2004. Dap160/intersectin acts as a stabilizing scaffold required for synaptic development and vesicle endocytosis. Neuron, 43 (2), 193– 205. 15260956
  53. Kononenko NL and Haucke V, 2015. Molecular mechanisms of presynaptic membrane retrieval and synaptic vesicle reformation. Neuron, 85 (3), 484– 496. 25654254
  54. Kononenko NL, Puchkov D, Classen GA, Walter AM, Pechstein A, Sawade L, Kaempf N, Trimbuch T, Lorenz D, Rosenmund C, Maritzen T, and Haucke V, 2014. Clathrin/AP-2 mediate synaptic vesicle reformation from endosome-like vacuoles but are not essential for membrane retrieval at central synapses. Neuron, 82 (5), 981– 988. 24908483
  55. Kusick GF, Chin M, Raychaudhuri S, Lippmann K, Adula KP, Hujber EJ, Vu T, Davis MW, Jorgensen EM, and Watanabe S, 2020. Synaptic vesicles transiently dock to refill release sites. Nature Neuroscience, 23 (11), 1329– 1338. 32989294 PMC8054220
  56. Logan T, Bendor J, Toupin C, Thorn K, and Edwards RH, 2017. α-Synuclein promotes dilation of the exocytotic fusion pore. Nature Neuroscience, 20 (5), 681– 689. 28288128 PMC5404982
  57. Marie B, Sweeney ST, Poskanzer KE, Roos J, Kelly RB, and Davis GW, 2004. Dap160/intersectin scaffolds the periactive zone to achieve high-fidelity endocytosis and normal synaptic growth. Neuron, 43 (2), 207– 219. 15260957
  58. Miller TM and Heuser JE, 1984. Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction. The Journal of Cell Biology, 98 (2), 685– 698. 6607255 PMC2113115
  59. Milosevic I., 2018. Revisiting the Role of Clathrin-Mediated Endoytosis in Synaptic Vesicle Recycling. Frontiers in Cellular Neuroscience, 12. PMC5807904 29467622
  60. Milosevic I, Giovedi S, Lou X, Raimondi A, Collesi C, Shen H, Paradise S, O’Toole E, Ferguson S, Cremona O, and De Camilli P, 2011. Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission. Neuron, 72 (4), 587– 601. 22099461 PMC3258500
  61. Mochida S., 2022. Mechanisms of Synaptic Vesicle Exo- and Endocytosis. Biomedicines, 10 (7), 1593. 35884898 PMC9313035
  62. Myeong J, Stunault MI, Klyachko VA, and Ashrafi G, 2024. Metabolic regulation of single synaptic vesicle exo- and endocytosis in hippocampal synapses. Cell Reports, 43 (5), 114218. 38758651 PMC11221188
  63. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, and Bamberg E, 2003. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proceedings of the National Academy of Sciences of the United States of America, 100 (24), 13940– 13945. 14615590 PMC283525
  64. Nonet ML, Holgado AM, Brewer F, Serpe CJ, Norbeck BA, Holleran J, Wei L, Hartwieg E, Jorgensen EM, and Alfonso A, 1999. UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Molecular biology of the cell, 10 (7), 2343– 2360. 10397769 PMC25452
  65. Olivas TJ, Wu Y, Yu S, Luan L, Choi P, Guinn ED, Nag S, De Camilli PV, Gupta K, and Melia TJ, 2023. ATG9 vesicles comprise the seed membrane of mammalian autophagosomes. The Journal of Cell Biology, 222 (7), e202208088. 37115958 PMC10148236
  66. Pearse BM, 1976. Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles. Proceedings of the National Academy of Sciences of the United States of America, 73 (4), 1255– 1259. 1063406 PMC430241
  67. Raimondi A, Ferguson SM, Lou X, Armbruster M, Paradise S, Giovedi S, Messa M, Kono N, Takasaki J, Cappello V, O’Toole E, Ryan TA, and De Camilli P, 2011. Overlapping role of dynamin isoforms in synaptic vesicle endocytosis. Neuron, 70 (6), 1100– 1114. 21689597 PMC3190241
  68. Richards DA, 2010. Regulation of exocytic mode in hippocampal neurons by intra-bouton calcium concentration. The Journal of physiology, 588 (Pt 24), 4927– 4936. 20962005 PMC3036188
  69. Richards DA, Guatimosim C, and Betz WJ, 2000. Two Endocytic Recycling Routes Selectively Fill Two Vesicle Pools in Frog Motor Nerve Terminals. Neuron, 27 (3), 551– 559. 11055437
  70. Rizzoli SO and Jahn R, 2007. Kiss-and-run, collapse and ‘readily retrievable’ vesicles. Traffic (Copenhagen, Denmark), 8 (9), 1137– 1144. 17645434
  71. Robertson JD, 1956. THE ULTRASTRUCTURE OF A REPTILIAN MYONEURAL JUNCTION. The Journal of Biophysical and Biochemical Cytology, 2 (4), 381– 394. 13357502 PMC2229705
  72. Roth TF and Porter KR, 1964. YOLK PROTEIN UPTAKE IN THE OOCYTE OF THE MOSQUITO AEDES AEGYPTI. L. The Journal of Cell Biology, 20 (2), 313– 332. 14126875 PMC2106398
  73. Saheki Y and De Camilli P, 2012. Synaptic vesicle endocytosis. Cold Spring Harbor Perspectives in Biology, 4 (9), a005645. 22763746 PMC3428771
  74. Schmidt A, Wolde M, Thiele C, Fest W, Kratzin H, Podtelejnikov AV, Witke W, Huttner WB, and Söling HD, 1999. Endophilin I mediates synaptic vesicle formation by transfer of arachidonate to lysophosphatidic acid. Nature, 401 (6749), 133– 141. 10490020
  75. Shupliakov O, Löw P, Grabs D, Gad H, Chen H, David C, Takei K, De Camilli P, and Brodin L, 1997. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science (New York, N.Y.), 276 (5310), 259– 263. 9092476
  76. Soykan T, Kaempf N, Sakaba T, Vollweiter D, Goerdeler F, Puchkov D, Kononenko NL, and Haucke V, 2017. Synaptic Vesicle Endocytosis Occurs on Multiple Timescales and Is Mediated by Formin-Dependent Actin Assembly. Neuron, 93 (4), 854– 866.e4. 28231467
  77. Stephens T, Wu Z, and Liu J, 2017. Mechanics of post-fusion exocytotic vesicle. Physical Biology, 14 (3), 035004. 28535147 PMC13329946
  78. Teng H, Cole JC, Roberts RL, and Wilkinson RS, 1999. Endocytic active zones: hot spots for endocytosis in vertebrate neuromuscular terminals. The Journal of neuroscience: the official journal of the Society for Neuroscience, 19 (12), 4855– 4866. 10366620 PMC6782649
  79. Torri-Tarelli F, Grohovaz F, Fesce R, and Ceccarelli B, 1985. Temporal coincidence between synaptic vesicle fusion and quantal secretion of acetylcholine. The Journal of Cell Biology, 101 (4), 1386– 1399. 2995407 PMC2113930
  80. Verstreken P, Kjaerulff O, Lloyd TE, Atkinson R, Zhou Y, Meinertzhagen IA, and Bellen HJ, 2002. Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell, 109 (1), 101– 112. 11955450
  81. Verstreken P, Koh T-W, Schulze KL, Zhai RG, Hiesinger PR, Zhou Y, Mehta SQ, Cao Y, Roos J, and Bellen HJ, 2003. Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron, 40 (4), 733– 748. 14622578
  82. Watanabe S and Boucrot E, 2017. Fast and ultrafast endocytosis. Current Opinion in Cell Biology, 47, 64– 71. 28391090
  83. Watanabe S, Davis MW, and Jorgensen EM, 2014. Flash-and-Freeze Electron Microscopy: Coupling Optogenetics with High-Pressure Freezing. In: Nägerl UV and Triller A, eds. Nanoscale Imaging of Synapses. Springer New York, 43– 57.
  84. Watanabe S, Liu Q, Davis MW, Hollopeter G, Thomas N, Jorgensen NB, and Jorgensen EM, 2013. Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions. eLife, 2, e00723. 24015355 PMC3762212
  85. Watanabe S, Mamer LE, Raychaudhuri S, Luvsanjav D, Eisen J, Trimbuch T, Söhl-Kielczynski B, Fenske P, Milosevic I, Rosenmund C, and Jorgensen EM, 2018. Synaptojanin and Endophilin Mediate Neck Formation during Ultrafast Endocytosis. Neuron, 98 (6), 1184– 1197.e6. 29953872 PMC6086574
  86. Watanabe S, Rost BR, Camacho-Pérez M, Davis MW, Söhl-Kielczynski B, Rosenmund C, and Jorgensen EM, 2013. Ultrafast endocytosis at mouse hippocampal synapses. Nature, 504 (7479), 242– 247. 24305055 PMC3957339
  87. Yang S, Park D, Manning L, Hill SE, Cao M, Xuan Z, Gonzalez I, Dong Y, Clark B, Shao L, Okeke I, Almoril-Porras A, Bai J, De Camilli P, and Colón-Ramos DA, 2022. Presynaptic autophagy is coupled to the synaptic vesicle cycle via ATG-9. Neuron, 110 (5), 824– 840.e10. 35065714 PMC9017068
  88. Zhang Q, Cao Y-Q, and Tsien RW, 2007. Quantum dots provide an optical signal specific to full collapse fusion of synaptic vesicles. Proceedings of the National Academy of Sciences of the United States of America, 104 (45), 17843– 17848. 17968015 PMC2077028
  89. Zhang Q, Li Y, and Tsien RW, 2009. The dynamic control of kiss-and-run and vesicular reuse probed with single nanoparticles. Science (New York, N.Y.), 323 (5920), 1448– 1453. 19213879 PMC2696197
  90. Zhu Y, Xu J, and Heinemann SF, 2009. Two Pathways of Synaptic Vesicle Retrieval Revealed by Single-Vesicle Imaging. Neuron, 61 (3), 397– 411. 19217377 PMC2707496

Authors
Watanabe, S.
Affiliations
Johns Hopkins University (US)
Corresponding author
Watanabe, Shigeki
ORCID
Watanabe, Shigeki
Venue
Annual Review of Neuroscience
Publisher
Annual Reviews
Published
2025-07-16
Volume
48
Issue
1
Pages
297-310
ISSN
  • 0147-006X (ISSN-L)
  • 1545-4126
DOI
10.1146/annurev-neuro-112723-040652
PMC
PMC12536329
OpenAlex
W4412483717
Cited by
4
References
85
Citations by year
2026: 3 · 2025: 1
FWCI
0.48
Type
journal article
Language
en
Open access
Licence
Locations
  • Annual Review of Neuroscience (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
Funders
  • National Institutes of Health (1dp2ns111133-01)
  • National Institute of Neurological Disorders and Stroke (DP2 NS111133, R01NS105810, R35NS132153)
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 recycling, clathrin-mediated endocytosis, synaptic vesicle retrieval, neurotransmitter release
MeSH terms
Animals, Endocytosis, Humans, Synaptic Transmission, Synaptic Vesicles

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