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Endocytic Machinery at the Neuronal Synapse

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Presynaptic Terminals

Abstract

Neurotransmission, a quantal process that conveys signals from one nerve cell to another, forms the basis of intercellular communication in nervous and sensory systems. Even at modest levels of neuronal activity, the hundreds of synaptic vesicles typically present at each synapse would be rapidly used up in the absence of equally robust mechanisms that form new synaptic vesicles. Thus, normal physiology of neuronal synapses is critically dependent on synaptic vesicle recycling. However, 40 years after Heuser and Reese showed that the synaptic vesicles are locally formed and recycled at the presynaptic terminal, the precise mechanism(s) of synaptic vesicle recycling remain(s) elusive. A major role in this process is thought to be played by clathrin-mediated endocytosis, a form of endocytosis that utilizes the clathrin coat, the GTPase dynamin, and a variety of accessory factors. The contribution of two other types of endocytosis, kiss-and-run and bulk endocytosis, to the regeneration of new synaptic vesicles is still an open question. This chapter summarizes current knowledge on endocytic modes and their machinery at the presynaptic terminals, with a strong emphasis on clathrin-mediated endocytosis as the predominant pathway of synaptic vesicle recycling. Given the essential nature of this topic, future progress in this field will not only advance our understanding of synaptic transmission but also have wide implications for neurophysiology, pharmacology, and medicine.

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References

  • Andersson F, Jakobsson J, Low P, Shupliakov O, Brodin L (2008) Perturbation of syndapin/PACSIN impairs synaptic vesicle recycling evoked by intense stimulation. J Neurosci 28:3925–3933

    CAS  PubMed  Google Scholar 

  • Antonescu CN, Danuser G, Schmid SL (2010) Phosphatidic acid plays a regulatory role in clathrin-mediated endocytosis. Mol Biol Cell 21:2944–2952

    CAS  PubMed Central  PubMed  Google Scholar 

  • Aravanis AM, Pyle JL, Tsien RW (2003) Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 423:643–647

    CAS  PubMed  Google Scholar 

  • Bakowska JC, Jenkins R, Pendleton J, Blackstone C (2005) The Troyer syndrome (SPG20) protein spartin interacts with Eps15. Biochem Biophys Res Commun 334:1042–1048

    CAS  PubMed  Google Scholar 

  • Bao H, Daniels RW, MacLeod GT, Charlton MP, Atwood HL, Zhang B (2005) AP180 maintains the distribution of synaptic and vesicle proteins in the nerve terminal and indirectly regulates the efficacy of Ca2+-triggered exocytosis. J Neurophysiol 94:1888–1903

    CAS  PubMed  Google Scholar 

  • Berridge MJ, Irvine RF (1984) Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312:315–321

    CAS  PubMed  Google Scholar 

  • Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166

    CAS  PubMed  Google Scholar 

  • Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72:395–447

    CAS  PubMed  Google Scholar 

  • Boulant S, Kural C, Zeeh JC, Ubelmann F, Kirchhausen T (2011) Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat Cell Biol 13:1124–1131

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brodsky FM (2012) Diversity of clathrin function: new tricks for an old protein. Annu Rev Cell Dev Biol 28:309–336

    CAS  PubMed  Google Scholar 

  • Campelo F, Malhotra V (2012) Membrane fission: the biogenesis of transport carriers. Annu Rev Biochem 81:407–427

    CAS  PubMed  Google Scholar 

  • Ceccarelli B, Hurlbut WP, Mauro A (1972) Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation. J Cell Biol 54:30–38

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ceccarelli B, Hurlbut WP, Mauro A (1973) Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol 57:499–524

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen H, De Camilli P (2005) The association of epsin with ubiquitinated cargo along the endocytic pathway is negatively regulated by its interaction with clathrin. Proc Natl Acad Sci U S A 102:2766–2771

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen H, Fre S, Slepnev VI, Capua MR, Takei K, Butler MH, Di Fiore PP, De Camilli P (1998) Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 394:793–797

    CAS  PubMed  Google Scholar 

  • Chen H, Slepnev VI, Di Fiore PP, De Camilli P (1999) The interaction of epsin and Eps15 with the clathrin adaptor AP-2 is inhibited by mitotic phosphorylation and enhanced by stimulation-dependent dephosphorylation in nerve terminals. J Biol Chem 274:3257–3260

    CAS  PubMed  Google Scholar 

  • Chen H, Ko G, Zatti A, Di Giacomo G, Liu L, Raiteri E, Perucco E, Collesi C, Min W, Zeiss C et al (2009) Embryonic arrest at midgestation and disruption of Notch signaling produced by the absence of both epsin 1 and epsin 2 in mice. Proc Natl Acad Sci U S A 106:13838–13843

    CAS  PubMed Central  PubMed  Google Scholar 

  • Choi S, Klingauf J, Tsien RW (2000) Postfusional regulation of cleft glutamate concentration during LTP at ‘silent synapses’. Nat Neurosci 3:330–336

    CAS  PubMed  Google Scholar 

  • Chung SH, Song WJ, Kim K, Bednarski JJ, Chen J, Prestwich GD, Holz RW (1998) The C2 domains of Rabphilin3A specifically bind phosphatidylinositol 4,5-bisphosphate containing vesicles in a Ca2+-dependent manner. In vitro characteristics and possible significance. J Biol Chem 273:10240–10248

    CAS  PubMed  Google Scholar 

  • Clayton EL, Evans GJ, Cousin MA (2008) Bulk synaptic vesicle endocytosis is rapidly triggered during strong stimulation. J Neurosci 28:6627–6632

    CAS  PubMed Central  PubMed  Google Scholar 

  • Clayton EL, Anggono V, Smillie KJ, Chau N, Robinson PJ, Cousin MA (2009) The phospho-dependent dynamin-syndapin interaction triggers activity-dependent bulk endocytosis of synaptic vesicles. J Neurosci 29:7706–7717

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cocucci E, Aguet F, Boulant S, Kirchhausen T (2012) The first five seconds in the life of a clathrin-coated pit. Cell 150:495–507

    CAS  PubMed Central  PubMed  Google Scholar 

  • Collins BM, McCoy AJ, Kent HM, Evans PR, Owen DJ (2002) Molecular architecture and functional model of the endocytic AP2 complex. Cell 109:523–535

    CAS  PubMed  Google Scholar 

  • Conner SD, Schroter T, Schmid SL (2003) AAK1-mediated micro2 phosphorylation is stimulated by assembled clathrin. Traffic 4:885–890

    CAS  PubMed  Google Scholar 

  • Cremona O, De Camilli P (2001) Phosphoinositides in membrane traffic at the synapse. J Cell Sci 114:1041–1052

    CAS  PubMed  Google Scholar 

  • Cremona O, Di Paolo G, Wenk MR, Luthi A, Kim WT, Takei K, Daniell L, Nemoto Y, Shears SB, Flavell RA et al (1999) Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99:179–188

    CAS  PubMed  Google Scholar 

  • Daumke O, Roux A, Haucke V (2014) BAR domain scaffolds in dynamin-mediated membrane fission. Cell 156:882–892

    CAS  PubMed  Google Scholar 

  • De Camilli P, Jahn R (1990) Pathways to regulated exocytosis in neurons. Annu Rev Physiol 52:625–645

    PubMed  Google Scholar 

  • de Heuvel E, Bell AW, Ramjaun AR, Wong K, Sossin WS, McPherson PS (1997) Identification of the major synaptojanin-binding proteins in brain. J Biol Chem 272:8710–8716

    PubMed  Google Scholar 

  • De Matteis MA, Godi A (2004) PI-loting membrane traffic. Nat Cell Biol 6:487–492

    PubMed  Google Scholar 

  • Di Paolo G, De Camilli P (2003) Does clathrin pull the fission trigger? Proc Natl Acad Sci U S A 100:4981–4983

    PubMed Central  PubMed  Google Scholar 

  • Diril MK, Wienisch M, Jung N, Klingauf J, Haucke V (2006) Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Dev Cell 10:233–244

    CAS  PubMed  Google Scholar 

  • Dittman J, Ryan TA (2009) Molecular circuitry of endocytosis at nerve terminals. Annu Rev Cell Dev Biol 25:133–160

    CAS  PubMed  Google Scholar 

  • Dittmer JC, Dawson RM (1960) The isolation of a new complex lipid: triphosphoinostide from ox brain. Biochim Biophys Acta 40:379–380

    CAS  PubMed  Google Scholar 

  • Douglas WW (1968) Stimulus-secretion coupling: the concept and clues from chromaffin and other cells. Br J Pharmacol 34:451–474

    CAS  PubMed  Google Scholar 

  • Edeling MA, Smith C, Owen D (2006) Life of a clathrin coat: insights from clathrin and AP structures. Nat Rev Mol Cell Biol 7:32–44

    CAS  PubMed  Google Scholar 

  • Edvardson S, Cinnamon Y, Ta-Shma A, Shaag A, Yim YI, Zenvirt S, Jalas C, Lesage S, Brice A, Taraboulos A et al (2012) A deleterious mutation in DNAJC6 encoding the neuronal-specific clathrin-uncoating co-chaperone auxilin, is associated with juvenile parkinsonism. PLoS One 7:e36458

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T (2004) Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118:591–605

    CAS  PubMed  Google Scholar 

  • Ellis RB, Hawthorne JN (1961) The structures of beef-brain phosphoinositides. Biochim Biophys Acta 51:385–387

    CAS  PubMed  Google Scholar 

  • Fallon L, Belanger CM, Corera AT, Kontogiannea M, Regan-Klapisz E, Moreau F, Voortman J, Haber M, Rouleau G, Thorarinsdottir T et al (2006) A regulated interaction with the UIM protein Eps15 implicates parkin in EGF receptor trafficking and PI(3)K-Akt signalling. Nat Cell Biol 8:834–842

    CAS  PubMed  Google Scholar 

  • Faundez V, Horng JT, Kelly RB (1998) A function for the AP3 coat complex in synaptic vesicle formation from endosomes. Cell 93:423–432

    CAS  PubMed  Google Scholar 

  • Fergestad T, Davis WS, Broadie K (1999) The stoned proteins regulate synaptic vesicle recycling in the presynaptic terminal. J Neurosci 19:5847–5860

    CAS  PubMed  Google Scholar 

  • Ferguson SM, De Camilli P (2012) Dynamin, a membrane-remodelling GTPase. Nat Rev Mol Cell Biol 13:75–88

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ferguson SM, Brasnjo G, Hayashi M, Wolfel M, Collesi C, Giovedi S, Raimondi A, Gong LW, Ariel P, Paradise S et al (2007) A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316:570–574

    CAS  PubMed  Google Scholar 

  • Ferguson SM, Raimondi A, Paradise S, Shen H, Mesaki K, Ferguson A, Destaing O, Ko G, Takasaki J, Cremona O et al (2009) Coordinated actions of actin and BAR proteins upstream of dynamin at endocytic clathrin-coated pits. Dev Cell 17:811–822

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fernandez-Alfonso T, Kwan R, Ryan TA (2006) Synaptic vesicles interchange their membrane proteins with a large surface reservoir during recycling. Neuron 51:179–186

    CAS  PubMed  Google Scholar 

  • Folch J (1946) Isolation of brain diphosphoinositide, a new phosphatide containing inositol meta diphosphate as a constituent. Fed Proc 5:134

    CAS  PubMed  Google Scholar 

  • Ford MG, Pearse BM, Higgins MK, Vallis Y, Owen DJ, Gibson A, Hopkins CR, Evans PR, McMahon HT (2001) Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291:1051–1055

    CAS  PubMed  Google Scholar 

  • Fotin A, Cheng Y, Grigorieff N, Walz T, Harrison SC, Kirchhausen T (2004) Structure of an auxilin-bound clathrin coat and its implications for the mechanism of uncoating. Nature 432:649–653

    CAS  PubMed  Google Scholar 

  • Frost A, Unger VM, De Camilli P (2009) The BAR domain superfamily: membrane-molding macromolecules. Cell 137:191–196

    CAS  PubMed  Google Scholar 

  • Gallop JL, Jao CC, Kent HM, Butler PJ, Evans PR, Langen R, McMahon HT (2006) Mechanism of endophilin N-BAR domain-mediated membrane curvature. Embo J 25:2898–2910

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gandhi SP, Stevens CF (2003) Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423:607–613

    CAS  PubMed  Google Scholar 

  • Glyvuk N, Tsytsyura Y, Geumann C, D‘Hooge R, Huve J, Kratzke M, Baltes J, Boening D, Klingauf J, Schu P (2010) AP-1/sigma1B-adaptin mediates endosomal synaptic vesicle recycling, learning and memory. Embo J 29:1318–1330

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gong LW, Di Paolo G, Diaz E, Cestra G, Diaz ME, Lindau M, De Camilli P, Toomre D (2005) Phosphatidylinositol phosphate kinase type I gamma regulates dynamics of large dense-core vesicle fusion. Proc Natl Acad Sci U S A 102:5204–5209

    CAS  PubMed Central  PubMed  Google Scholar 

  • Graham TR (2004) Flippases and vesicle-mediated protein transport. Trends Cell Biol 14:670–677

    CAS  PubMed  Google Scholar 

  • Gu M, Schuske K, Watanabe S, Liu Q, Baum P, Garriga G, Jorgensen EM (2008) Mu2 adaptin facilitates but is not essential for synaptic vesicle recycling in Caenorhabditis elegans. J Cell Biol 183:881–892

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gundelfinger ED, Kessels MM, Qualmann B (2003) Temporal and spatial coordination of exocytosis and endocytosis. Nat Rev Mol Cell Biol 4:127–139

    CAS  PubMed  Google Scholar 

  • Haffner C, Takei K, Chen H, Ringstad N, Hudson A, Butler MH, Salcini AE, Di Fiore PP, De Camilli P (1997) Synaptojanin 1: localization on coated endocytic intermediates in nerve terminals and interaction of its 170 kDa isoform with Eps15. FEBS Lett 419:175–180

    CAS  PubMed  Google Scholar 

  • Harata NC, Choi S, Pyle JL, Aravanis AM, Tsien RW (2006) Frequency-dependent kinetics and prevalence of kiss-and-run and reuse at hippocampal synapses studied with novel quenching methods. Neuron 49:243–256

    CAS  PubMed  Google Scholar 

  • Hayashi M, Raimondi A, O‘Toole E, Paradise S, Collesi C, Cremona O, Ferguson SM, De Camilli P (2008) Cell- and stimulus-dependent heterogeneity of synaptic vesicle endocytic recycling mechanisms revealed by studies of dynamin 1-null neurons. Proc Natl Acad Sci U S A 105:2175–2180

    CAS  PubMed Central  PubMed  Google Scholar 

  • He L, Wu LG (2007) The debate on the kiss-and-run fusion at synapses. Trends Neurosci 30:447–455

    CAS  PubMed  Google Scholar 

  • He L, Wu XS, Mohan R, Wu LG (2006) Two modes of fusion pore opening revealed by cell-attached recordings at a synapse. Nature 444:102–105

    CAS  PubMed  Google Scholar 

  • Heldwein EE, Macia E, Wang J, Yin HL, Kirchhausen T, Harrison SC (2004) Crystal structure of the clathrin adaptor protein 1 core. Proc Natl Acad Sci U S A 101:14108–14113

    CAS  PubMed Central  PubMed  Google Scholar 

  • Henne WM, Boucrot E, Meinecke M, Evergren E, Vallis Y, Mittal R, McMahon HT (2010) FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328:1281–1284

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heuser JE, Reese TS (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57:315–344

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ho HY, Rohatgi R, Lebensohn AM, Le M, Li J, Gygi SP, Kirschner MW (2004) Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell 118:203–216

    CAS  PubMed  Google Scholar 

  • Hokin MR, Hokin LE (1953) Enzyme secretion and the incorporation of P32 into phospholipides of pancreas slices. J Biol Chem 203:967–977

    CAS  PubMed  Google Scholar 

  • Holt M, Cooke A, Wu MM, Lagnado L (2003) Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells. J Neurosci 23:1329–1339

    CAS  PubMed  Google Scholar 

  • Hosoi N, Holt M, Sakaba T (2009) Calcium dependence of exo- and endocytotic coupling at a glutamatergic synapse. Neuron 63:216–229

    CAS  PubMed  Google Scholar 

  • Irvine RF (2005) Inositide evolution – towards turtle domination? J Physiol 566:295–300

    CAS  PubMed Central  PubMed  Google Scholar 

  • Itoh T, De Camilli P (2006) BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim Biophys Acta 1761:897–912

    CAS  PubMed  Google Scholar 

  • Jackson AP, Flett A, Smythe C, Hufton L, Wettey FR, Smythe E (2003) Clathrin promotes incorporation of cargo into coated pits by activation of the AP2 adaptor micro2 kinase. J Cell Biol 163:231–236

    CAS  PubMed Central  PubMed  Google Scholar 

  • Janssens PM (1988) The evolutionary origin of eukaryotic transmembrane signal transduction. Comp Biochem Physiol A Comp Physiol 90:209–223

    CAS  PubMed  Google Scholar 

  • Jiang J, Maes EG, Taylor AB, Wang L, Hinck AP, Lafer EM, Sousa R (2007) Structural basis of J cochaperone binding and regulation of Hsp70. Mol Cell 28:422–433

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jost M, Simpson F, Kavran JM, Lemmon MA, Schmid SL (1998) Phosphatidylinositol-4,5-bisphosphate is required for endocytic coated vesicle formation. Curr Biol 8:1399–1402

    CAS  PubMed  Google Scholar 

  • Jung N, Wienisch M, Gu M, Rand JB, Muller SL, Krause G, Jorgensen EM, Klingauf J, Haucke V (2007) Molecular basis of synaptic vesicle cargo recognition by the endocytic sorting adaptor stonin 2. J Cell Biol 179:1497–1510

    CAS  PubMed Central  PubMed  Google Scholar 

  • Keen JH, Willingham MC, Pastan IH (1979) Clathrin-coated vesicles: isolation, dissociation and factor-dependent reassociation of clathrin baskets. Cell 16:303–312

    CAS  PubMed  Google Scholar 

  • Kessels MM, Qualmann B (2004) The syndapin protein family: linking membrane trafficking with the cytoskeleton. J Cell Sci 117:3077–3086

    CAS  PubMed  Google Scholar 

  • Kim SH, Ryan TA (2009) A distributed set of interactions controls mu2 functionality in the role of AP-2 as a sorting adaptor in synaptic vesicle endocytosis. J Biol Chem 284:32803–32812

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kirchhausen T (1999) Adaptors for clathrin-mediated traffic. Annu Rev Cell Dev Biol 15:705–732

    CAS  PubMed  Google Scholar 

  • Kirchhausen T (2000) Clathrin. Annu Rev Biochem 69:699–727

    CAS  PubMed  Google Scholar 

  • Kirchhausen T (2009) Imaging endocytic clathrin structures in living cells. Trends Cell Biol 19:596–605

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kirchhausen T, Harrison SC (1981) Protein organization in clathrin trimers. Cell 23:755–761

    CAS  PubMed  Google Scholar 

  • Kittelmann M, Liewald JF, Hegermann J, Schultheis C, Brauner M, Steuer Costa W, Wabnig S, Eimer S, Gottschalk A (2013) In vivo synaptic recovery following optogenetic hyperstimulation. Proc Natl Acad Sci U S A 110:E3007–E3016

    CAS  PubMed Central  PubMed  Google Scholar 

  • Klingauf J, Kavalali ET, Tsien RW (1998) Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature 394:581–585

    CAS  PubMed  Google Scholar 

  • Klyachko VA, Jackson MB (2002) Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature 418:89–92

    CAS  PubMed  Google Scholar 

  • Koenig JH, Yamaoka K, Ikeda K (1998) Omega images at the active zone may be endocytotic rather than exocytotic: implications for the vesicle hypothesis of transmitter release. Proc Natl Acad Sci U S A 95:12677–12682

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kononenko NL, Diril MK, Puchkov D, Kintscher M, Koo SJ, Pfuhl G, Winter Y, Wienisch M, Klingauf J, Breustedt J et al (2013) Compromised fidelity of endocytic synaptic vesicle protein sorting in the absence of stonin 2. Proc Natl Acad Sci U S A 110:E526–E535

    CAS  PubMed Central  PubMed  Google Scholar 

  • Koroglu C, Baysal L, Cetinkaya M, Karasoy H, Tolun A (2013) DNAJC6 is responsible for juvenile parkinsonism with phenotypic variability. Parkinsonism Relat Disord 19:320–324

    PubMed  Google Scholar 

  • Krauss M, Kinuta M, Wenk MR, De Camilli P, Takei K, Haucke V (2003) ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type I gamma. J Cell Biol 162:113–124

    CAS  PubMed Central  PubMed  Google Scholar 

  • Larrabee MG, Klingman JD, Leicht WS (1963) Effects of temperature, calcium and activity on phospholipid metabolism in a synaptic ganglion. J Neurochem 10:549–570

    CAS  PubMed  Google Scholar 

  • Lee DW, Wu X, Eisenberg E, Greene LE (2006) Recruitment dynamics of GAK and auxilin to clathrin-coated pits during endocytosis. J Cell Sci 119:3502–3512

    CAS  PubMed  Google Scholar 

  • Lemmon MA (2003) Phosphoinositide recognition domains. Traffic 4:201–213

    CAS  PubMed  Google Scholar 

  • Lippincott J, Li R (2000) Involvement of PCH family proteins in cytokinesis and actin distribution. Microsc Res Tech 49:168–172

    CAS  PubMed  Google Scholar 

  • Liu JP, Sim AT, Robinson PJ (1994) Calcineurin inhibition of dynamin I GTPase activity coupled to nerve terminal depolarization. Science 265:970–973

    CAS  PubMed  Google Scholar 

  • Loyet KM, Kowalchyk JA, Chaudhary A, Chen J, Prestwich GD, Martin TF (1998) Specific binding of phosphatidylinositol 4,5-bisphosphate to calcium-dependent activator protein for secretion (CAPS), a potential phosphoinositide effector protein for regulated exocytosis. J Biol Chem 273:8337–8343

    CAS  PubMed  Google Scholar 

  • Lundmark R, Carlsson SR (2003) Sorting nexin 9 participates in clathrin-mediated endocytosis through interactions with the core components. J Biol Chem 278:46772–46781

    CAS  PubMed  Google Scholar 

  • Lundmark R, Carlsson SR (2009) SNX9 – a prelude to vesicle release. J Cell Sci 122:5–11

    CAS  PubMed  Google Scholar 

  • Maritzen T, Podufall J, Haucke V (2010) Stonins–specialized adaptors for synaptic vesicle recycling and beyond? Traffic 11:8–15

    CAS  PubMed  Google Scholar 

  • Maritzen T, Koo SJ, Haucke V (2012) Turning CALM into excitement: AP180 and CALM in endocytosis and disease. Biol Cell 104:588–602

    CAS  PubMed  Google Scholar 

  • Martin TF (2001) PI(4,5)P(2) regulation of surface membrane traffic. Curr Opin Cell Biol 13:493–499

    CAS  PubMed  Google Scholar 

  • Massol RH, Boll W, Griffin AM, Kirchhausen T (2006) A burst of auxilin recruitment determines the onset of clathrin-coated vesicle uncoating. Proc Natl Acad Sci U S A 103:10265–10270

    CAS  PubMed Central  PubMed  Google Scholar 

  • McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12:517–533

    CAS  PubMed  Google Scholar 

  • McPherson PS, Garcia EP, Slepnev VI, David C, Zhang X, Grabs D, Sossin WS, Bauerfeind R, Nemoto Y, De Camilli P (1996) A presynaptic inositol-5-phosphatase. Nature 379:353–357

    CAS  PubMed  Google Scholar 

  • Merrifield CJ, Feldman ME, Wan L, Almers W (2002) Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4:691–698

    CAS  PubMed  Google Scholar 

  • Merrifield CJ, Perrais D, Zenisek D (2005) Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121:593–606

    CAS  PubMed  Google Scholar 

  • Mettlen M, Pucadyil T, Ramachandran R, Schmid SL (2009) Dissecting dynamin’s role in clathrin-mediated endocytosis. Biochem Soc Trans 37:1022–1026

    CAS  PubMed Central  PubMed  Google Scholar 

  • Miller TM, Heuser JE (1984) Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction. J Cell Biol 98:685–698

    CAS  PubMed  Google Scholar 

  • Milosevic I, Sorensen JB, Lang T, Krauss M, Nagy G, Haucke V, Jahn R, Neher E (2005) Plasmalemmal phosphatidylinositol-4,5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J Neurosci 25:2557–2565

    CAS  PubMed  Google Scholar 

  • Milosevic I, Giovedi S, Lou X, Raimondi A, Collesi C, Shen H, Paradise S, O‘Toole E, Ferguson S, Cremona O et al (2011) Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission. Neuron 72:587–601

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mooren OL, Galletta BJ, Cooper JA (2012) Roles for actin assembly in endocytosis. Annu Rev Biochem 81:661–686

    CAS  PubMed  Google Scholar 

  • Morlot S, Roux A (2013) Mechanics of dynamin-mediated membrane fission. Annu Rev Biophys 42:629–649

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mullen GP, Grundahl KM, Gu M, Watanabe S, Hobson RJ, Crowell JA, McManus JR, Mathews EA, Jorgensen EM, Rand JB (2012) UNC-41/stonin functions with AP2 to recycle synaptic vesicles in Caenorhabditis elegans. PLoS One 7:e40095

    CAS  PubMed Central  PubMed  Google Scholar 

  • Murthy VN, De Camilli P (2003) Cell biology of the presynaptic terminal. Annu Rev Neurosci 26:701–728

    CAS  PubMed  Google Scholar 

  • Murthy VN, Stevens CF (1998) Synaptic vesicles retain their identity through the endocytic cycle. Nature 392:497–501

    CAS  PubMed  Google Scholar 

  • Nakatsu F, Okada M, Mori F, Kumazawa N, Iwasa H, Zhu G, Kasagi Y, Kamiya H, Harada A, Nishimura K et al (2004) Defective function of GABA-containing synaptic vesicles in mice lacking the AP-3B clathrin adaptor. J Cell Biol 167:293–302

    CAS  PubMed Central  PubMed  Google Scholar 

  • Newell-Litwa K, Salazar G, Smith Y, Faundez V (2009) Roles of BLOC-1 and adaptor protein-3 complexes in cargo sorting to synaptic vesicles. Mol Biol Cell 20:1441–1453

    CAS  PubMed Central  PubMed  Google Scholar 

  • Okamoto M, Sudhof TC (1997) Mints, Munc18-interacting proteins in synaptic vesicle exocytosis. J Biol Chem 272:31459–31464

    CAS  PubMed  Google Scholar 

  • Owen DJ, Vallis Y, Noble ME, Hunter JB, Dafforn TR, Evans PR, McMahon HT (1999) A structural explanation for the binding of multiple ligands by the alpha-adaptin appendage domain. Cell 97:805–815

    CAS  PubMed  Google Scholar 

  • Owen DJ, Vallis Y, Pearse BM, McMahon HT, Evans PR (2000) The structure and function of the beta 2-adaptin appendage domain. Embo J 19:4216–4227

    CAS  PubMed Central  PubMed  Google Scholar 

  • Owen DJ, Collins BM, Evans PR (2004) Adaptors for clathrin coats: structure and function. Annu Rev Cell Dev Biol 20:153–191

    CAS  PubMed  Google Scholar 

  • Paillart C, Li J, Matthews G, Sterling P (2003) Endocytosis and vesicle recycling at a ribbon synapse. J Neurosci 23:4092–4099

    CAS  PubMed  Google Scholar 

  • Pearse BM (1975) Coated vesicles from pig brain: purification and biochemical characterization. J Mol Biol 97:93–98

    CAS  PubMed  Google Scholar 

  • Pearse BM (1976) Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles. Proc Natl Acad Sci U S A 73:1255–1259

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pechstein A, Shupliakov O, Haucke V (2010) Intersectin 1: a versatile actor in the synaptic vesicle cycle. Biochem Soc Trans 38:181–186

    CAS  PubMed  Google Scholar 

  • Perera RM, Zoncu R, Lucast L, De Camilli P, Toomre D (2006) Two synaptojanin 1 isoforms are recruited to clathrin-coated pits at different stages. Proc Natl Acad Sci U S A 103:19332–19337

    CAS  PubMed Central  PubMed  Google Scholar 

  • Phillips AM, Ramaswami M, Kelly LE (2010) Stoned. Traffic 11:16–24

    CAS  PubMed  Google Scholar 

  • Polo S, Sigismund S, Faretta M, Guidi M, Capua MR, Bossi G, Chen H, De Camilli P, Di Fiore PP (2002) A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416:451–455

    CAS  PubMed  Google Scholar 

  • Posor Y, Eichhorn-Gruenig M, Puchkov D, Schoneberg J, Ullrich A, Lampe A, Muller R, Zarbakhsh S, Gulluni F, Hirsch E et al (2013) Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate. Nature 499:233–237

    CAS  PubMed  Google Scholar 

  • Pyle JL, Kavalali ET, Piedras-Renteria ES, Tsien RW (2000) Rapid reuse of readily releasable pool vesicles at hippocampal synapses. Neuron 28:221–231

    CAS  PubMed  Google Scholar 

  • Quan A, Robinson PJ (2013) Syndapin–a membrane remodelling and endocytic F-BAR protein. FEBS J 280:5198–5212

    CAS  PubMed  Google Scholar 

  • Raimondi A, Ferguson SM, Lou X, Armbruster M, Paradise S, Giovedi S, Messa M, Kono N, Takasaki J, Cappello V et al (2011) Overlapping role of dynamin isoforms in synaptic vesicle endocytosis. Neuron 70:1100–1114

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ralser M, Nonhoff U, Albrecht M, Lengauer T, Wanker EE, Lehrach H, Krobitsch S (2005) Ataxin-2 and huntingtin interact with endophilin-A complexes to function in plastin-associated pathways. Hum Mol Genet 14:2893–2909

    CAS  PubMed  Google Scholar 

  • Rana RS, Hokin LE (1990) Role of phosphoinositides in transmembrane signaling. Physiol Rev 70:115–164

    CAS  PubMed  Google Scholar 

  • Ringstad N, Nemoto Y, De Camilli P (1997) The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc Natl Acad Sci U S A 94:8569–8574

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rizzoli SO, Jahn R (2007) Kiss-and-run, collapse and ‘readily retrievable’ vesicles. Traffic 8:1137–1144

    CAS  PubMed  Google Scholar 

  • Roth TF, Porter KR (1964) Yolk protein uptake in the Oocyte of the mosquito Aedes aegypti L. J Cell Biol 20:313–332

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rothman JE, Schmid SL (1986) Enzymatic recycling of clathrin from coated vesicles. Cell 46(1):5–9

    Google Scholar 

  • Ryan TA, Reuter H, Smith SJ (1997) Optical detection of a quantal presynaptic membrane turnover. Nature 388:478–482

    CAS  PubMed  Google Scholar 

  • Saarikangas J, Zhao H, Lappalainen P (2010) Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Physiol Rev 90:259–289

    CAS  PubMed  Google Scholar 

  • Saffarian S, Cocucci E, Kirchhausen T (2009) Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol 7:e1000191

    PubMed Central  PubMed  Google Scholar 

  • Saheki Y, De Camilli P (2012) Synaptic vesicle endocytosis. Cold Spring Harb Perspect Biol 4:a005645

    PubMed Central  PubMed  Google Scholar 

  • Sato K, Ernstrom GG, Watanabe S, Weimer RM, Chen CH, Sato M, Siddiqui A, Jorgensen EM, Grant BD (2009) Differential requirements for clathrin in receptor-mediated endocytosis and maintenance of synaptic vesicle pools. Proc Natl Acad Sci U S A 106:1139–1144

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schafer DA (2002) Coupling actin dynamics and membrane dynamics during endocytosis. Curr Opin Cell Biol 14:76–81

    CAS  PubMed  Google Scholar 

  • Schiavo G, Gu QM, Prestwich GD, Sollner TH, Rothman JE (1996) Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin. Proc Natl Acad Sci U S A 93:13327–13332

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schuske KR, Richmond JE, Matthies DS, Davis WS, Runz S, Rube DA, van der Bliek AM, Jorgensen EM (2003) Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40:749–762

    CAS  PubMed  Google Scholar 

  • Sen A, Madhivanan K, Mukherjee D, Aguilar RC (2012) The epsin protein family: coordinators of endocytosis and signaling. Biomol Conc 3:117–126

    CAS  Google Scholar 

  • Shin N, Lee S, Ahn N, Kim SA, Ahn SG, YongPark Z, Chang S (2007) Sorting nexin 9 interacts with dynamin 1 and N-WASP and coordinates synaptic vesicle endocytosis. J Biol Chem 282:28939–28950

    CAS  PubMed  Google Scholar 

  • Slepnev VI, De Camilli P (2000) Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nat Rev Neurosci 1:161–172

    CAS  PubMed  Google Scholar 

  • Smythe E (2002) Regulating the clathrin-coated vesicle cycle by AP2 subunit phosphorylation. Trends Cell Biol 12:352–354

    CAS  PubMed  Google Scholar 

  • Soulet F, Yarar D, Leonard M, Schmid SL (2005) SNX9 regulates dynamin assembly and is required for efficient clathrin-mediated endocytosis. Mol Biol Cell 16:2058–2067

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stamnes M (2002) Regulating the actin cytoskeleton during vesicular transport. Curr Opin Cell Biol 14:428–433

    CAS  PubMed  Google Scholar 

  • Stimson DT, Estes PS, Rao S, Krishnan KS, Kelly LE, Ramaswami M (2001) Drosophila stoned proteins regulate the rate and fidelity of synaptic vesicle internalization. J Neurosci 21:3034–3044

    CAS  PubMed  Google Scholar 

  • Sudhof TC (2013) Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 80:675–690

    CAS  PubMed  Google Scholar 

  • Suh BC, Hille B (2005) Regulation of ion channels by phosphatidylinositol 4,5-bisphosphate. Curr Opin Neurobiol 15:370–378

    CAS  PubMed  Google Scholar 

  • Takei K, Mundigl O, Daniell L, De Camilli P (1996) The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J Cell Biol 133:1237–1250

    CAS  PubMed  Google Scholar 

  • Takei K, Haucke V, Slepnev V, Farsad K, Salazar M, Chen H, De Camilli P (1998) Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell 94:131–141

    CAS  PubMed  Google Scholar 

  • Takei K, Slepnev VI, Haucke V, De Camilli P (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1:33–39

    CAS  PubMed  Google Scholar 

  • Tan MS, Yu JT, Tan L (2013) Bridging integrator 1 (BIN1): form, function, and Alzheimer’s disease. Trends Mol Med 19:594–603

    CAS  PubMed  Google Scholar 

  • Tavaria M, Gabriele T, Anderson RL, Mirault ME, Baker E, Sutherland G, Kola I (1995) Localization of the gene encoding the human heat shock cognate protein, HSP73, to chromosome 11. Genomics 29:266–268

    CAS  PubMed  Google Scholar 

  • Taylor MJ, Perrais D, Merrifield CJ (2011) A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol 9:e1000604

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tebar F, Sorkina T, Sorkin A, Ericsson M, Kirchhausen T (1996) Eps15 is a component of clathrin-coated pits and vesicles and is located at the rim of coated pits. J Biol Chem 271:28727–28730

    CAS  PubMed  Google Scholar 

  • Teng H, Lin MY, Wilkinson RS (2007) Macroendocytosis and endosome processing in snake motor boutons. J Physiol 582:243–262

    CAS  PubMed Central  PubMed  Google Scholar 

  • ter Haar E, Harrison SC, Kirchhausen T (2000) Peptide-in-groove interactions link target proteins to the beta-propeller of clathrin. Proc Natl Acad Sci U S A 97:1096–1100

    PubMed Central  PubMed  Google Scholar 

  • Tomlinson RV, Ballou CE (1961) Complete characterization of the myo-inositol polyphosphates from beef brain phosphoinositide. J Biol Chem 236:1902–1906

    CAS  PubMed  Google Scholar 

  • Torri-Tarelli F, Haimann C, Ceccarelli B (1987) Coated vesicles and pits during enhanced quantal release of acetylcholine at the neuromuscular junction. J Neurocytol 16:205–214

    CAS  PubMed  Google Scholar 

  • Traub LM (2003) Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J Cell Biol 163:203–208

    CAS  PubMed Central  PubMed  Google Scholar 

  • Traub LM, Downs MA, Westrich JL, Fremont DH (1999) Crystal structure of the alpha appendage of AP-2 reveals a recruitment platform for clathrin-coat assembly. Proc Natl Acad Sci U S A 96:8907–8912

    CAS  PubMed Central  PubMed  Google Scholar 

  • Trempe JF, Chen CX, Grenier K, Camacho EM, Kozlov G, McPherson PS, Gehring K, Fon EA (2009) SH3 domains from a subset of BAR proteins define a Ubl-binding domain and implicate parkin in synaptic ubiquitination. Mol Cell 36:1034–1047

    CAS  PubMed  Google Scholar 

  • Tsyba L, Nikolaienko O, Dergai O, Dergai M, Novokhatska O, Skrypkina I, Rynditch A (2011) Intersectin multidomain adaptor proteins: regulation of functional diversity. Gene 473:67–75

    CAS  PubMed  Google Scholar 

  • Umasankar PK, Sanker S, Thieman JR, Chakraborty S, Wendland B, Tsang M, Traub LM (2012) Distinct and separable activities of the endocytic clathrin-coat components Fcho1/2 and AP-2 in developmental patterning. Nat Cell Biol 14:488–501

    CAS  PubMed Central  PubMed  Google Scholar 

  • Umeda A, Meyerholz A, Ungewickell E (2000) Identification of the universal cofactor (auxilin 2) in clathrin coat dissociation. Eur J Cell Biol 79:336–342

    CAS  PubMed  Google Scholar 

  • Ungewickell E, Ungewickell H, Holstein SE, Lindner R, Prasad K, Barouch W, Martin B, Greene LE, Eisenberg E (1995) Role of auxilin in uncoating clathrin-coated vesicles. Nature 378:632–635

    CAS  PubMed  Google Scholar 

  • Van Jaarsveld PP, Nandi PK, Lippoldt RE, Saroff H, Edelhoch H (1981) Polymerization of clathrin protomers into basket structures. Biochemistry 20:4129–4135

    PubMed  Google Scholar 

  • Verstreken P, Koh TW, Schulze KL, Zhai RG, Hiesinger PR, Zhou Y, Mehta SQ, Cao Y, Roos J, Bellen HJ (2003) Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40:733–748

    CAS  PubMed  Google Scholar 

  • Vinatier J, Herzog E, Plamont MA, Wojcik SM, Schmidt A, Brose N, Daviet L, El Mestikawy S, Giros B (2006) Interaction between the vesicular glutamate transporter type 1 and endophilin A1, a protein essential for endocytosis. J Neurochem 97:1111–1125

    CAS  PubMed  Google Scholar 

  • Voglmaier SM, Kam K, Yang H, Fortin DL, Hua Z, Nicoll RA, Edwards RH (2006) Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 51:71–84

    CAS  PubMed  Google Scholar 

  • von Kleist L, Stahlschmidt W, Bulut H, Gromova K, Puchkov D, Robertson MJ, MacGregor KA, Tomilin N, Pechstein A, Chau N et al (2011) Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 146:471–484

    Google Scholar 

  • Wang Q, Navarro MV, Peng G, Molinelli E, Goh SL, Judson BL, Rajashankar KR, Sondermann H (2009) Molecular mechanism of membrane constriction and tubulation mediated by the F-BAR protein Pacsin/Syndapin. Proc Natl Acad Sci U S A 106:12700–12705

    CAS  PubMed Central  PubMed  Google Scholar 

  • Watanabe S, Liu Q, Davis MW, Hollopeter G, Thomas N, Jorgensen NB, Jorgensen EM (2013) Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions. eLife 2:e00723

    PubMed Central  PubMed  Google Scholar 

  • Wenk MR, De Camilli P (2004) Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals. Proc Natl Acad Sci U S A 101:8262–8269

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wienisch M, Klingauf J (2006) Vesicular proteins exocytosed and subsequently retrieved by compensatory endocytosis are nonidentical. Nat Neurosci 9:1019–1027

    CAS  PubMed  Google Scholar 

  • Willig KI, Rizzoli SO, Westphal V, Jahn R, Hell SW (2006) STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis. Nature 440:935–939

    CAS  PubMed  Google Scholar 

  • Woodward MP, Roth TF (1978) Coated vesicles: characterization, selective dissociation, and reassembly. Proc Natl Acad Sci U S A 75:4394–4398

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wu W, Wu LG (2007) Rapid bulk endocytosis and its kinetics of fission pore closure at a central synapse. Proc Natl Acad Sci U S A 104:10234–10239

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wu LG, Hamid E, Shin W, Chiang HC (2014) Exocytosis and endocytosis: modes, functions, and coupling mechanisms. Annu Rev Physiol 76:301–331

    CAS  PubMed  Google Scholar 

  • Xiao J, Kim LS, Graham TR (2006) Dissection of Swa2p/auxilin domain requirements for cochaperoning Hsp70 clathrin-uncoating activity in vivo. Mol Biol Cell 17:3281–3290

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xing Y, Böcking T, Wolf M, Grigorieff N, Kirchhausen T, Harrison SC (2010) Structure of clathrin coat with bound Hsc70 and auxilin: mechanism of Hsc70-facilitated disassembly. EMBO J 29:655–665

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yim YI, Sun T, Wu LG, Raimondi A, De Camilli P, Eisenberg E, Greene LE (2010) Endocytosis and clathrin-uncoating defects at synapses of auxilin knockout mice. Proc Natl Acad Sci U S A 107:4412–4417

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang Q, Cao YQ, Tsien RW (2007) Quantum dots provide an optical signal specific to full collapse fusion of synaptic vesicles. Proc Natl Acad Sci U S A 104:17843–17848

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang Q, Li Y, Tsien RW (2009) The dynamic control of kiss-and-run and vesicular reuse probed with single nanoparticles. Science 323:1448–1453

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

I would like to apologize to the authors of many important papers whose work I may have inadvertently failed to cite here due to space constraints. I thank Dr Ante Milosevic for his kind help with the figures and Dr Nuno Raimundo for discussion. My work is supported by the Emmy Noether Young Investigator Award from German Research Foundation (DFG).

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  1. European Neuroscience Institute (ENI), Grisebachstr. 5, 37077, Göttingen, Germany

    Ira Milosevic

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  1. Department of Physiology, Tokyo Medical University, Tokyo, Japan

    Sumiko Mochida

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Milosevic, I. (2015). Endocytic Machinery at the Neuronal Synapse. In: Mochida, S. (eds) Presynaptic Terminals. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55166-9_10

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