Key physiological parameters dictate triggering of activity-dependent bulk endocytosis in hippocampal synapses

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Wenzel, Eva M ^a,c,d   Morton, Andrew ^b   Ebert, Katrin ^a   Welzel, Oliver ^a   Kornhuber, Johannes ^a   Cousin, Michael A ^b   Groemer, Teja W ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF OSLO   (Norway)

^d OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ACTIVITY DEPENDENT BULK ENDOCYTOSIS; ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTROSTIMULATION; EMBRYO; ENDOCYTOSIS; EXOCYTOSIS; FLUORESCENCE IMAGING; HIPPOCAMPUS; NERVE CELL STIMULATION; NERVE ENDING; NEUROTRANSMISSION; NONHUMAN; RAT; SYNAPSE; ANIMAL; CYTOLOGY; ENDOSOME; METABOLISM; PHYSIOLOGY; REPRODUCIBILITY; SYNAPTOSOME; ULTRASTRUCTURE; WISTAR RAT;

RATTUS;

ACTION POTENTIALS; ANIMALS; ELECTRIC STIMULATION; ENDOCYTOSIS; ENDOSOMES; HIPPOCAMPUS; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; REPRODUCIBILITY OF RESULTS; SYNAPSES;

EID: 84861839412     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038188     Document Type: Article

References (43)

1. Granseth B, Odermatt B, Royle SJ, Lagnado L, (2006) Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51: 773-786.
2. Newton AJ, Kirchhausen T, Murthy VN, (2006) Inhibition of dynamin completely blocks compensatory synaptic vesicle endocytosis. Proc Natl Acad Sci U S A 103: 17955-17960.
3. Alvarez de Toledo G, Fernández-Chacón R, Fernández JM, (1993) Release of secretory products during transient vesicle fusion. Nature 363: 554-558.
4. Fernández JM, Neher E, Gomperts BD, (1984) Capacitance measurements reveal stepwise fusion events in degranulating mast cells. Nature 312: 453-455.
5. Neher E, Marty A, (1982) Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc Natl Acad Sci U S A 79: 6712-6716.
6. Albillos A, Dernick G, Horstmann H, Almers W, Alvarez de Toledo G, et al. (1997) The exocytotic event in chromaffin cells revealed by patch amperometry. Nature 389: 509-512.
7. Henkel AW, Kang G, Kornhuber J, (2001) A common molecular machinery for exocytosis and the 'kiss-and-run' mechanism in chromaffin cells is controlled by phosphorylation. J Cell Sci 114: 4613-4620.
8. Dittman J, Ryan TA, (2009) Molecular circuitry of endocytosis at nerve terminals. Annu Rev Cell Dev Biol 25: 133-160.
9. Clayton EL, Evans GJ, Cousin MA, (2008) Bulk synaptic vesicle endocytosis is rapidly triggered during strong stimulation. J Neurosci 28: 6627-6632.
10. Sankaranarayanan S, Ryan TA, (2001) Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat Neurosci 4: 129-136.
11. Rizzoli SO, Betz WJ, (2005) Synaptic vesicle pools. Nat Rev Neurosci 6: 57-69.
12. Royle SJ, Lagnado L, (2003) Endocytosis at the synaptic terminal. J Physiol 553: 345-355.
13. Wu LG, Ryan TA, Lagnado L, (2007) Modes of vesicle retrieval at ribbon synapses, calyx-type synapses, and small central synapses. J Neurosci 27: 11793-11802.
14. Cheung G, Jupp OJ, Cousin MA, (2010) Activity-dependent bulk endocytosis and clathrin-dependent endocytosis replenish specific synaptic vesicle pools in central nerve terminals. J Neurosci 30: 8151-8161.
15. Richards DA, Guatimosim C, Betz WJ, (2000) Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals. Neuron 27: 551-559.
16. 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.
17. 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.
18. 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.
19. Koenig JH, Ikeda K, (1996) Synaptic vesicles have two distinct recycling pathways. J Cell Biol 135: 797-808.
20. Paillart C, Li J, Matthews G, Sterling P, (2003) Endocytosis and vesicle recycling at a ribbon synapse. J Neurosci 23: 4092-4099.
21. Teng H, Lin MY, Wilkinson RS, (2007) Macroendocytosis and endosome processing in snake motor boutons. J Physiol 582: 243-262.
22. Wu W, Xu J, Wu XS, Wu LG, (2005) Activity-dependent acceleration of endocytosis at a central synapse. J Neurosci 25: 11676-11683.
23. Clayton EL, Cousin MA, (2009) The molecular physiology of activity-dependent bulk endocytosis of synaptic vesicles. J Neurochem 111: 901-914.
24. Welzel O, Tischbirek CH, Jung J, Kohler EM, Svetlitchny A, et al. (2010) Synapse clusters are preferentially formed by synapses with large recycling pool sizes. PLoS One 5: e13514.
25. Sankaranarayanan S, Ryan TA, (2000) Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat Cell Biol 2: 197-204.
26. Dorostkar MM, Dreosti E, Odermatt B, Lagnado L, (2010) Computational processing of optical measurements of neuronal and synaptic activity in networks. J Neurosci Methods 188: 141-150.
27. Stroebel A, Welzel O, Kornhuber J, Groemer TW, (2010) Background determination-based detection of scattered peaks. Microsc Res Tech 73: 1115-1122.
28. Groemer TW, Klingauf J, (2007) Synaptic vesicles recycling spontaneously and during activity belong to the same vesicle pool. Nat Neurosci 10: 145-147.
29. Welzel O, Henkel AW, Stroebel AM, Jung J, Tischbirek CH, et al. (2011) Systematic heterogeneity of fractional vesicle pool sizes and release rates of hippocampal synapses. Biophys J 100: 593-601.
30. Dunnett CW, (1964) New Tables For Multiple Comparisons With A Control. Biometrics 20: 482-491.
31. Clayton EL, Cousin MA, (2009) Quantitative monitoring of activity-dependent bulk endocytosis of synaptic vesicle membrane by fluorescent dextran imaging. J Neurosci Methods 185: 76-81.
32. Clayton EL, Cousin MA, (2008) Differential labelling of bulk endocytosis in nerve terminals by FM dyes. Neurochem Int 53: 51-55.
33. Clayton EL, Anggono V, Smillie KJ, Chau N, Robinson PJ, et al. (2009) The phospho-dependent dynamin-syndapin interaction triggers activity-dependent bulk endocytosis of synaptic vesicles. J Neurosci 29: 7706-7717.
34. Clayton EL, Sue N, Smillie KJ, O'Leary T, Bache N, et al. (2010) Dynamin I phosphorylation by GSK3 controls activity-dependent bulk endocytosis of synaptic vesicles. Nat Neurosci 13: 845-851.
35. Kim SH, Choi HJ, Lee KW, Hong NH, Sung BH, et al. (2006) Interaction of SPIN90 with syndapin is implicated in clathrin-mediated endocytic pathway in fibroblasts. Genes Cells 11: 1197-1211.
36. Lencer WI, Weyer P, Verkman AS, Ausiello DA, Brown D, (1990) FITC-dextran as a probe for endosome function and localization in kidney. Am J Physiol 258: C309-317.
37. Meunier FA, Nguyen TH, Colasante C, Luo F, Sullivan RK, et al. (2010) Sustained synaptic-vesicle recycling by bulk endocytosis contributes to the maintenance of high-rate neurotransmitter release stimulated by glycerotoxin. J Cell Sci 123: 1131-1140.
38. Bartos M, Vida I, Jonas P, (2007) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8: 45-56.
39. Martens H, Weston MC, Boulland JL, Gronborg M, Grosche J, et al. (2008) Unique luminal localization of VGAT-C terminus allows for selective labeling of active cortical GABAergic synapses. J Neurosci 28: 13125-13131.
40. Hua Y, Sinha R, Thiel CS, Schmidt R, Huve J, et al. (2011) A readily retrievable pool of synaptic vesicles. Nat Neurosci 14: 833-839.
41. Mutch SA, Kensel-Hammes P, Gadd JC, Fujimoto BS, Allen RW, et al. (2011) Protein quantification at the single vesicle level reveals that a subset of synaptic vesicle proteins are trafficked with high precision. J Neurosci 31: 1461-1470.
42. Sara Y, Mozhayeva MG, Liu X, Kavalali ET, (2002) Fast vesicle recycling supports neurotransmission during sustained stimulation at hippocampal synapses. J Neurosci 22: 1608-1617.
43. D'Angelo E, De Zeeuw CI, (2009) Timing and plasticity in the cerebellum: focus on the granular layer. Trends Neurosci 32: 30-40.