Activity-dependent bulk synaptic vesicle endocytosis-A fast, high capacity membrane retrieval mechanism

Molecular Neurobiology

Volumn 39, Issue 3, 2009, Pages 185-189

  Cousin, M A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Activity; Bulk endocytosis; Calcium; Clathrin; Endocytosis; Nerve terminal; Synaptic vesicle

Indexed keywords

CALCINEURIN; CLATHRIN;

BRAIN REGION; CELL MEMBRANE; ENDOCYTOSIS; MOLECULAR MECHANICS; NERVE CELL; NERVE CONDUCTION; NERVE ENDING; NERVE POTENTIAL; NERVE STIMULATION; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; REVIEW; SYNAPSE VESICLE; SYNAPTIC MEMBRANE; ANIMAL; CYTOLOGY; METABOLISM;

ANIMALS; CELL MEMBRANE; ENDOCYTOSIS; NEURONS; SYNAPTIC VESICLES;

EID: 69449105753     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12035-009-8062-3     Document Type: Review

References (36)

1. SJ Royle L Lagnado 2003 Endocytosis at the synaptic terminal J Physiol 553 345 355 12963793 10.1113/jphysiol.2003.049221 1:CAS:528: DC%2BD2cXitlWntg%3D%3D (Pubitemid 37527539)
2. VN Murthy P De Camilli 2003 Cell biology of the presynaptic terminal Ann Rev Neurosci 26 701 728 14527272 10.1146/annurev.neuro.26.041002.131445 1:CAS:528:DC%2BD3sXntFSisbg%3D (Pubitemid 37064948)
3. B Granseth B Odermatt SJ Royle L Lagnado 2006 Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses Neuron 51 773 786 16982422 10.1016/j.neuron.2006.08.029 1:CAS:528:DC%2BD28XhtVGls7zN (Pubitemid 44374912)
4. J Balaji M Armbruster TA Ryan 2008 Calcium control of endocytic capacity at a CNS synapse J Neurosci 28 6742 6749 18579748 10.1523/JNEUROSCI.1082-08.2008 1:CAS:528:DC%2BD1cXotF2hurk%3D
5. B Ceccarelli WP Hurlbut A Mauro 1972 Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation J Cell Biol 54 30 38 4338962 10.1083/jcb.54.1.30 1:STN:280:DyaE383hvVGjtQ%3D%3D
6. B Ceccarelli WP Hurlbut A Mauro 1973 Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction J Cell Biol 57 499 524 4348791 10.1083/jcb.57.2.499 1:STN:280:DyaE3s7lsVWnsA%3D%3D
7. E Ales L Tabares JM Poyato V Valero M Lindau G Alvarez de Toledo 1999 High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism Nat Cell Biol 1 40 44 10559862 10.1038/9012 1:CAS:528: DyaK1MXksVKitr0%3D
8. CT Wang JC Lu J Bai PY Chang TF Martin ER Chapman MB Jackson 2003 Different domains of synaptotagmin control the choice between kiss-and-run and full fusion Nature 424 943 947 12931189 10.1038/nature01857 1:CAS:528: DC%2BD3sXmsV2isLo%3D (Pubitemid 37051685)
9. AF Oberhauser JM Fernandez 1996 A fusion pore phenotype in mast cells of the ruby-eye mouse Proc Natl Acad Sci USA 93 14349 14354 8962054 10.1073/pnas.93.25.14349 1:CAS:528:DyaK28XnsVKks74%3D (Pubitemid 26418969)
10. L He LG Wu 2007 The debate on the kiss-and-run fusion at synapses Trends Neurosci 30 447 455 17765328 10.1016/j.tins.2007.06.012 1:CAS:528: DC%2BD2sXhtVClsrrI (Pubitemid 47376946)
11. DA Richards C Guatimosim WJ Betz 2000 Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals Neuron 27 551 559 11055437 10.1016/S0896-6273(00)00065-9 1:CAS:528:DC%2BD3cXnt12ntL4%3D
12. GJ Evans MA Cousin 2007 Activity-dependent control of slow synaptic vesicle endocytosis by cyclin-dependent kinase 5 J Neurosci 27 401 411 17215401 10.1523/JNEUROSCI.3809-06.2007 1:CAS:528:DC%2BD2sXhtFSrs7o%3D (Pubitemid 46106014)
13. TM Miller JE Heuser 1984 Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction J Cell Biol 98 685 698 6607255 10.1083/jcb.98.2.685 1:STN:280:DyaL2c7htFOrtA%3D%3D
14. DA Richards C Guatimosim SO Rizzoli WJ Betz 2003 Synaptic vesicle pools at the frog neuromuscular junction Neuron 39 529 541 12895425 10.1016/S0896-6273(03)00405-7 1:CAS:528:DC%2BD3sXmsFOks7w%3D (Pubitemid 36937052)
15. H Teng RS Wilkinson 2000 Clathrin-mediated endocytosis near active zones in snake motor boutons J Neurosci 20 7986 7993 11050119 1:CAS:528: DC%2BD3cXnsl2mtrg%3D
16. AG Leenders G Scholten RP de Lange FH Lopes Da Silva WE Ghijsen 2002 Sequential changes in synaptic vesicle pools and endosome-like organelles during depolarization near the active zone of central nerve terminals Neurosci 109 195 206 10.1016/S0306-4522(01)00450-X 1:CAS:528:DC%2BD38XitVyqsQ%3D%3D (Pubitemid 34088157)
17. +-stimulation contain a plethora of presynaptic membrane proteins Neurosci 94 985 996 10.1016/S0306-4522(99)00351-6 1:CAS:528:DyaK1MXmsVWiu70%3D (Pubitemid 29474988)
18. G Di Paolo HS Moskowitz K Gipson MR Wenk S Voronov M Obayashi R Flavell RM Fitzsimonds TA Ryan P De Camilli 2004 Impaired PtdIns(4, 5) P2 synthesis in nerve terminals produces defects in synaptic vesicle trafficking Nature 431 415 422 15386003 10.1038/nature02896 (Pubitemid 39329574)
19. M Hayashi A Raimondi E O'Toole S Paradise C Collesi O Cremona SM Ferguson P De Camilli 2008 Cell- and stimulus-dependent heterogeneity of synaptic vesicle endocytic recycling mechanisms revealed by studies of dynamin 1-null neurons Proc Natl Acad Sci USA 105 2175 2180 18250322 10.1073/pnas.0712171105 1:CAS:528:DC%2BD1cXitl2lsL0%3D
20. M Holt A Cooke MM Wu L Lagnado 2003 Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells J Neurosci 23 1329 1339 12598621 1:CAS:528:DC%2BD3sXit1antLg%3D
21. RP de Lange AD de Roos JG Borst 2003 Two modes of vesicle recycling in the rat calyx of Held J Neurosci 23 10164 10173 14602833
22. C Paillart J Li G Matthews P Sterling 2003 Endocytosis and vesicle recycling at a ribbon synapse J Neurosci 23 4092 4099 12764096 1:CAS:528:DC%2BD3sXktFKgur0%3D
23. W Wu LG Wu 2007 Rapid bulk endocytosis and its kinetics of fission pore closure at a central synapse Proc Natl Acad Sci USA 104 10234 10239 17551019 10.1073/pnas.0611512104 1:CAS:528:DC%2BD2sXmvVCms7o%3D (Pubitemid 47175292)
24. EL Clayton GJ Evans MA Cousin 2008 Bulk synaptic vesicle endocytosis is rapidly triggered during strong stimulation J Neurosci 28 6627 6632 18579735 10.1523/JNEUROSCI.1445-08.2008 1:CAS:528:DC%2BD1cXotF2htbo%3D
25. H Teng MY Lin RS Wilkinson 2007 Macroendocytosis and endosome processing in snake motor boutons J Physiol 582 243 262 17478535 10.1113/jphysiol.2007. 130989 1:CAS:528:DC%2BD2sXotFals7w%3D (Pubitemid 46993573)
26. S Sankaranarayanan TA Ryan 2000 Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system Nat Cell Biol 2 197 204 10783237 10.1038/35008615 1:CAS:528:DC%2BD3cXivVSlsbg%3D (Pubitemid 30795776)
27. CB Klee TH Crouch MH Krinks 1979 Calcineurin: a calcium- and calmodulin-binding protein of the nervous system Proc Natl Acad Sci USA 76 6270 3 293720 10.1073/pnas.76.12.6270 1:CAS:528:DyaL3cXntFeruw%3D%3D (Pubitemid 10163382)
28. SA Chan C Smith 2001 Physiological stimuli evoke two forms of endocytosis in bovine chromaffin cells J Physiol 537 871 885 11744761 10.1113/jphysiol. 2001.012838 1:CAS:528:DC%2BD38XntVGluw%3D%3D (Pubitemid 34026614)
29. S Kumashiro YF Lu K Tomizawa M Matsushita FY Wei H Matsui 2005 Regulation of synaptic vesicle recycling by calcineurin in different vesicle pools Neurosci Res 51 435 443 15740806 10.1016/j.neures.2004.12.018 1:CAS:528:DC%2BD2MXhvVersrw%3D (Pubitemid 40299331)
30. EL Clayton MA Cousin 2008 Differential labelling of bulk endocytosis in nerve terminals by FM dyes Neurochem Int 53 51 55 18586059 10.1016/j.neuint. 2008.06.002 1:CAS:528:DC%2BD1cXpslSls74%3D
31. MA Cousin PJ Robinson 2001 The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis Trends Neurosci 24 659 665 11672811 10.1016/S0166-2236(00)01930-5 1:CAS:528:DC%2BD3MXnslels7o%3D (Pubitemid 33152773)
32. JH Koenig K Ikeda 1989 Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval J Neurosci 9 3844 3860 2573698 1:CAS:528:DyaK3cXhs1KrtA%3D%3D
33. K Takei O Mundigl L Daniell P De Camilli 1996 The synaptic vesicle cycle: A single vesicle budding step involving clathrin and dynamin J Cell Biol 133 1237 1250 8682861 10.1083/jcb.133.6.1237 1:CAS:528:DyaK28XjslKjsbk%3D (Pubitemid 26192326)
34. 2+-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse Neuron 21 607 616 9768846 10.1016/S0896- 6273(00)80570-X 1:CAS:528:DyaK1cXms1eht7g%3D (Pubitemid 28475511)
35. J Kasprowicz S Kuenen K Miskiewicz RL Habets L Smitz P Verstreken 2008 Inactivation of clathrin heavy chain inhibits synaptic recycling but allows bulk membrane uptake J Cell Biol 182 1007 1016 18762582 10.1083/jcb.200804162 1:CAS:528:DC%2BD1cXhtFejtL3K
36. H Heerssen RD Fetter GW Davis 2008 Clathrin dependence of synaptic-vesicle formation at the Drosophila neuromuscular junction Curr Biol 18 401 409 18356056 10.1016/j.cub.2008.02.055 1:CAS:528:DC%2BD1cXjs1GqsL4%3D