Synaptic vesicle generation from central nerve terminal endosomes

Traffic

Volumn 16, Issue 3, 2015, Pages 229-240

  Kokotos, Alexandros C ^a   Cousin, Michael A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Clathrin; Dynamin; Endocytosis; Endosome; Presynapse; Vesicle

Indexed keywords

CLATHRIN;

ACTIVITY DEPENDENT BULK ENDOCYTOSIS; ARTICLE; BRAIN FUNCTION; CALCIUM TRANSPORT; CELL FUNCTION; CELL MEMBRANE; CENTRAL VERVE TERMINAL ENDOSOME; CLATHRIN MEDIATED ENDOCYTOSIS; ENDOCYTOSIS; ENDOSOME; EXTRACELLULAR CALCIUM; NERVE CONDUCTION; NERVE ENDING; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE VESICLE; ULTRAFAST ENDOCYTOSIS; ANIMAL; CENTRAL NERVOUS SYSTEM; PHYSIOLOGY;

ANIMALS; CELL MEMBRANE; CENTRAL NERVOUS SYSTEM; ENDOCYTOSIS; ENDOSOMES; NERVE ENDINGS; SYNAPTIC VESICLES;

EID: 84923183484     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12235     Document Type: Article

References (82)

1. Rizzoli SO, Betz WJ. Synaptic vesicle pools. Nat Rev Neurosci 2005;6:57-69.
2. Kim SH, Ryan TA. CDK5 serves as a major control point in neurotransmitter release. Neuron 2010;67:797-809.
3. Waites CL, Garner CC. Presynaptic function in health and disease. Trends Neurosci 2011;34:326-337.
4. Esposito G, Ana Clara F, Verstreken P. Synaptic vesicle trafficking and Parkinson's disease. Dev Neurobiol 2012;72:134-144.
5. Saheki Y, De Camilli P. Synaptic vesicle endocytosis. Cold Spring Harb Perspect Biol 2012;4:a005645.
6. Henne WM, Boucrot E, Meinecke M, Evergren E, Vallis Y, Mittal R, McMahon HT. FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 2010;328:1281-1284.
7. Hollopeter G, Lange JJ, Zhang Y, Vu TN, Gu M, Ailion M, Lambie EJ, Slaughter BD, Unruh JR, Florens L, Jorgensen EM. The membrane-associated proteins FCHo and SGIP are allosteric activators of the AP2 clathrin adaptor complex. eLife 2014;3:e03648.
8. Umasankar PK, Ma L, Thieman JR, Jha A, Doray B, Watkins SC, Traub LM. A clathrin coat assembly role for the muniscin protein central linker revealed by TALEN-mediated gene editing. eLife 2014;3:e04137.
9. Rao Y, Ruckert C, Saenger W, Haucke V. The early steps of endocytosis: from cargo selection to membrane deformation. Eur J Cell Biol 2012;91:226-233.
10. Doherty GJ, McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem 2009;78:857-902.
11. Ferguson SM, De Camilli P. Dynamin, a membrane-remodelling GTPase. Nat Rev Mol Cell Biol 2012;13:75-88.
12. Morlot S, Roux A. Mechanics of dynamin-mediated membrane fission. Annu Rev Biophys 2013;42:629-649.
13. Granseth B, Odermatt B, Royle SJ, Lagnado L. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 2006;51:773-786.
14. Zhu Y, Xu J, Heinemann SF. Two pathways of synaptic vesicle retrieval revealed by single-vesicle imaging. Neuron 2009;61:397-411.
15. Lopez-Murcia FJ, Royle SJ, Llobet A. Presynaptic clathrin levels are a limiting factor for synaptic transmission. J Neurosci 2014;34:8618-8629.
16. Wilhelm BG, Mandad S, Truckenbrodt S, Krohnert K, Schafer C, Rammner B, Koo SJ, Classen GA, Krauss M, Haucke V, Urlaub H, Rizzoli SO. Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins. Science 2014;344:1023-1028.
17. Cousin MA. Activity-dependent bulk synaptic vesicle endocytosis - a fast, high capacity membrane retrieval mechanism. Mol Neurobiol 2009;39:185-189.
18. Clayton EL, Cousin MA. The molecular physiology of activity-dependent bulk endocytosis of synaptic vesicles. J Neurochem 2009;111:901-914.
19. Cousin MA. Synaptic vesicle endocytosis and endosomal recycling in central nerve terminals: discrete trafficking routes? Neuroscientist 2014. Jul 15 [EPub ahead of print].
20. Watanabe S, Liu Q, Davis MW, Hollopeter G, Thomas N, Jorgensen NB, Jorgensen EM. Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions. eLife 2013;2:e00723.
21. Watanabe S, Rost BR, Camacho-Perez M, Davis MW, Sohl-Kielczynski B, Rosenmund C, Jorgensen EM. Ultrafast endocytosis at mouse hippocampal synapses. Nature 2013;504:242-247.
22. Bonanomi D, Fornasiero EF, Valdez G, Halegoua S, Benfenati F, Menegon A, Valtorta F. Identification of a developmentally regulated pathway of membrane retrieval in neuronal growth cones. J Cell Sci 2008;121(Pt 22):3757-3769.
23. Grant BD, Donaldson JG. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 2009;10:597-608.
24. Fredj NB, Burrone J. A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat Neurosci 2009;12:751-758.
25. Richards DA, Guatimosim C, Betz WJ. Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals. Neuron 2000;27:551-559.
26. Cheung G, Jupp OJ, Cousin MA. Activity-dependent bulk endocytosis and clathrin-dependent endocytosis replenish specific synaptic vesicle pools in central nerve terminals. J Neurosci 2010;30:8151-8161.
27. Shupliakov O. The synaptic vesicle cluster: a source of endocytic proteins during neurotransmitter release. Neuroscience 2009;158:204-210.
28. Denker A, Krohnert K, Buckers J, Neher E, Rizzoli SO. The reserve pool of synaptic vesicles acts as a buffer for proteins involved in synaptic vesicle recycling. Proc Natl Acad Sci USA 2011;108:17183-17188.
29. Krabben L, Fassio A, Bhatia VK, Pechstein A, Onofri F, Fadda M, Messa M, Rao Y, Shupliakov O, Stamou D, Benfenati F, Haucke V. Synapsin I senses membrane curvature by an amphipathic lipid packing sensor motif. J Neurosci 2011;31:18149-18154.
30. Granseth B, Lagnado L. The role of endocytosis in regulating the strength of hippocampal synapses. J Physiol 2008;586(Pt 24):5969-5982.
31. Hua Y, Sinha R, Thiel CS, Schmidt R, Huve J, Martens H, Hell SW, Egner A, Klingauf J. A readily retrievable pool of synaptic vesicles. Nat Neurosci 2011;14:833-839.
32. Watanabe S, Trimbuch T, Camacho-Perez M, Rost BR, Brokowski B, Sohl-Kielczynski B, Felies A, Davis MW, Rosenmund C, Jorgensen EM. Clathrin regenerates synaptic vesicles from endosomes. Nature 2014. Oct 8 [EPub ahead of print].
33. de Lange RP, de Roos AD, Borst JG. Two modes of vesicle recycling in the rat calyx of Held. J Neurosci 2003;23:10164-10173.
34. Wu Y, O'Toole ET, Girard M, Ritter B, Messa M, Liu X, McPherson PS, Ferguson SM, De Camilli P. A dynamin 1-, dynamin 3- and clathrin-independent pathway of synaptic vesicle recycling mediated by bulk endocytosis. eLife 2014;3:e01621.
35. Vargas KJ, Makani S, Davis T, Westphal CH, Castillo PE, Chandra SS. Synucleins regulate the kinetics of synaptic vesicle endocytosis. J Neurosci 2014;34:9364-9376.
36. Cheung G, Cousin MA. Adaptor protein complexes 1 and 3 are essential for generation of synaptic vesicles from activity-dependent bulk endosomes. J Neurosci 2012;32:6014-6023.
37. Cheung G, Cousin MA. Synaptic vesicle generation from activity-dependent bulk endosomes requires calcium and calcineurin. J Neurosci 2013;33:3370-3379.
38. Glyvuk N, Tsytsyura Y, Geumann C, D'Hooge R, Huve J, Kratzke M, Baltes J, Boening D, Klingauf J, Schu P. AP-1/sigma1B-adaptin mediates endosomal synaptic vesicle recycling, learning and memory. EMBO J 2010;29:1318-1330.
39. Kononenko NL, Puchkov D, Classen GA, Walter AM, Pechstein A, Sawade L, Kaempf N, Trimbuch T, Lorenz D, Rosenmund C, Maritzen T, Haucke V. Clathrin/AP-2 mediate synaptic vesicle reformation from endosome-like vacuoles but are not essential for membrane retrieval at central synapses. Neuron 2014;82:981-988.
40. Robinson MS. Adaptable adaptors for coated vesicles. Trends Cell Biol 2004;14:167-174.
41. Newell-Litwa K, Chintala S, Jenkins S, Pare JF, McGaha L, Smith Y, Faundez V. Hermansky-Pudlak protein complexes, AP-3 and BLOC-1, differentially regulate presynaptic composition in the striatum and hippocampus. J Neurosci 2010;30:820-831.
42. Voglmaier SM, Kam K, Yang H, Fortin DL, Hua Z, Nicoll RA, Edwards RH. Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 2006;51:71-84.
43. Kim SH, Ryan TA. Synaptic vesicle recycling at CNS snapses without AP-2. J Neurosci 2009;29:3865-3874.
44. Kratzke M, Candiello E, Schmidt B, Jahn O, Schu P. AP-1/sigma1B-dependent SV protein recycling is regulated in early endosomes and is coupled to AP-2 endocytosis. Mol Neurobiol 2014. Aug 17 [EPub ahead of print].
45. Hoopmann P, Punge A, Barysch SV, Westphal V, Buckers J, Opazo F, Bethani I, Lauterbach MA, Hell SW, Rizzoli SO. Endosomal sorting of readily releasable synaptic vesicles. Proc Natl Acad Sci USA 2010;107:19055-19060.
46. Uytterhoeven V, Kuenen S, Kasprowicz J, Miskiewicz K, Verstreken P. Loss of skywalker reveals synaptic endosomes as sorting stations for synaptic vesicle proteins. Cell 2011;145:117-132.
47. Zlatic SA, Grossniklaus EJ, Ryder PV, Salazar G, Mattheyses AL, Peden AA, Faundez V. Chemical-genetic disruption of clathrin function spares adaptor complex 3-dependent endosome vesicle biogenesis. Mol Biol Cell 2013;24:2378-2388.
48. Kasprowicz J, Kuenen S, Miskiewicz K, Habets RL, Smitz L, Verstreken P. Inactivation of clathrin heavy chain inhibits synaptic recycling but allows bulk membrane uptake. J Cell Biol 2008;182:1007-1016.
49. Heerssen H, Fetter RD, Davis GW. Clathrin dependence of synaptic-vesicle formation at the Drosophila neuromuscular junction. Curr Biol 2008;18:401-409.
50. Takei K, Mundigl O, Daniell L, De Camilli P. The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J Cell Biol 1996;133:1237-1250.
51. Krauss M, Kinuta M, Wenk MR, De Camilli P, Takei K, Haucke V. ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Igamma. J Cell Biol 2003;162:113-124.
52. von Kleist L, Stahlschmidt W, Bulut H, Gromova K, Puchkov D, Robertson MJ, MacGregor KA, Tomilin N, Pechstein A, Chau N, Chircop M, Sakoff J, von Kries JP, Saenger W, Krausslich HG, et al. Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell 2011;146:471-484.
53. Gerasimenko JV, Tepikin AV, Petersen OH, Gerasimenko OV. Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr Biol 1998;8:1335-1338.
54. Lundqvist-Gustafsson H, Gustafsson M, Dahlgren C. Dynamic ca(2+)changes in neutrophil phagosomes A source for intracellular ca(2+)during phagolysosome formation? Cell Calcium 2000;27:353-362.
55. Saito M, Hanson PI, Schlesinger P. Luminal chloride-dependent activation of endosome calcium channels: patch clamp study of enlarged endosomes. J Biol Chem 2007;282:27327-27333.
56. Martina JA, Lelouvier B, Puertollano R. The calcium channel mucolipin-3 is a novel regulator of trafficking along the endosomal pathway. Traffic 2009;10:1143-1156.
57. Lelouvier B, Puertollano R. Mucolipin-3 regulates luminal calcium, acidification, and membrane fusion in the endosomal pathway. J Biol Chem 2011;286:9826-9832.
58. Lee SY, Wenk MR, Kim Y, Nairn AC, De Camilli P. Regulation of synaptojanin 1 by cyclin-dependent kinase 5 at synapses. Proc Natl Acad Sci USA 2004;101:546-551.
59. Lee SY, Voronov S, Letinic K, Nairn AC, Di Paolo G, De Camilli P. Regulation of the interaction between PIPKI gamma and talin by proline-directed protein kinases. J Cell Biol 2005;168:789-799.
60. Haucke V, Di Paolo G. Lipids and lipid modifications in the regulation of membrane traffic. Curr Opin Cell Biol 2007;19:426-435.
61. Chang-Ileto B, Frere SG, Chan RB, Voronov SV, Roux A, Di Paolo G. Synaptojanin 1-mediated PI(4, 5)P2 hydrolysis is modulated by membrane curvature and facilitates membrane fission. Dev Cell 2011;20:206-218.
62. Milosevic I, Giovedi S, Lou X, Raimondi A, Collesi C, Shen H, Paradise S, O'Toole E, Ferguson S, Cremona O, De Camilli P. Recruitment of endophilin to clathrin-coated pit necks is required for efficient vesicle uncoating after fission. Neuron 2011;72:587-601.
63. Cousin MA, Robinson PJ. The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis. Trends Neurosci 2001;24:659-665.
64. Anggono V, Smillie KJ, Graham ME, Valova VA, Cousin MA, Robinson PJ. Syndapin I is the phosphorylation-regulated dynamin I partner in synaptic vesicle endocytosis. Nat Neurosci 2006;9:752-760.
65. Clayton EL, Anggono V, Smillie KJ, Chau N, Robinson PJ, Cousin MA. The phospho-dependent dynamin-syndapin interaction triggers activity-dependent bulk endocytosis of synaptic vesicles. J Neurosci 2009;29:7706-7717.
66. Park RJ, Shen H, Liu L, Liu X, Ferguson SM, De Camilli P. Dynamin triple knockout cells reveal off target effects of commonly used dynamin inhibitors. J Cell Sci 2013;126(Pt 22):5305-5312.
67. Kittelmann M, Liewald JF, Hegermann J, Schultheis C, Brauner M, Steuer Costa W, Wabnig S, Eimer S, Gottschalk A. In vivo synaptic recovery following optogenetic hyperstimulation. Proc Natl Acad Sci USA 2013;110:E3007-E3016.
68. Naslavsky N, Caplan S. EHD proteins: key conductors of endocytic transport. Trends Cell Biol 2011;21:122-131.
69. Daumke O, Lundmark R, Vallis Y, Martens S, Butler PJ, McMahon HT. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 2007;449:923-927.
70. Jovic M, Kieken F, Naslavsky N, Sorgen PL, Caplan S. Eps15 homology domain 1-associated tubules contain phosphatidylinositol-4-phosphate and phosphatidylinositol-(4, 5)-bisphosphate and are required for efficient recycling. Mol Biol Cell 2009;20:2731-2743.
71. Pant S, Sharma M, Patel K, Caplan S, Carr CM, Grant BD. AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling. Nat Cell Biol 2009;11:1399-1410.
72. Braun A, Pinyol R, Dahlhaus R, Koch D, Fonarev P, Grant BD, Kessels MM, Qualmann B. EHD proteins associate with syndapin I and II and such interactions play a crucial role in endosomal recycling. Mol Biol Cell 2005;16:3642-3658.
73. Jakobsson J, Ackermann F, Andersson F, Larhammar D, Low P, Brodin L. Regulation of synaptic vesicle budding and dynamin function by an EHD ATPase. J Neurosci 2011;31:13972-13980.
74. Vijayakrishnan N, Woodruff EA 3rd, Broadie K. Rolling blackout is required for bulk endocytosis in non-neuronal cells and neuronal synapses. J Cell Sci 2009;122(Pt 1):114-125.
75. Kasprowicz J, Kuenen S, Swerts J, Miskiewicz K, Verstreken P. Dynamin photoinactivation blocks Clathrin and alpha-adaptin recruitment and induces bulk membrane retrieval. J Cell Biol 2014;204:1141-1156.
76. Evans GJ, Cousin MA. Activity-dependent control of slow synaptic vesicle endocytosis by cyclin-dependent kinase 5. J Neurosci 2007;27:401-411.
77. Clayton EL, Sue N, Smillie KJ, O'Leary T, Bache N, Cheung G, Cole AR, Wyllie DJ, Sutherland C, Robinson PJ, Cousin MA. Dynamin I phosphorylation by GSK3 controls activity-dependent bulk endocytosis of synaptic vesicles. Nat Neurosci 2010;13:845-851.
78. Newell-Litwa K, Seong E, Burmeister M, Faundez V. Neuronal and non-neuronal functions of the AP-3 sorting machinery. J Cell Sci 2007;120(Pt 4):531-541.
79. Hua Z, Leal-Ortiz S, Foss SM, Waites CL, Garner CC, Voglmaier SM, Edwards RH. v-SNARE composition distinguishes synaptic vesicle pools. Neuron 2011;71:474-487.
80. Ramirez DM, Khvotchev M, Trauterman B, Kavalali ET. Vti1a identifies a vesicle pool that preferentially recycles at rest and maintains spontaneous neurotransmission. Neuron 2012;73:121-134.
81. Raingo J, Khvotchev M, Liu P, Darios F, Li YC, Ramirez DM, Adachi M, Lemieux P, Toth K, Davletov B, Kavalali ET. VAMP4 directs synaptic vesicles to a pool that selectively maintains asynchronous neurotransmission. Nat Neurosci 2012;15:738-745.
82. Scheuber A, Rudge R, Danglot L, Raposo G, Binz T, Poncer JC, Galli T. Loss of AP-3 function affects spontaneous and evoked release at hippocampal mossy fiber synapses. Proc Natl Acad Sci USA 2006;103:16562-16567.