The phospho-dependent dynamin-syndapin interaction triggers activity-dependent bulk endocytosis of synaptic vesicles

Journal of Neuroscience

Volumn 29, Issue 24, 2009, Pages 7706-7717

  Clayton, Emma L ^a   Anggono, Victor ^b,c   Smillie, Karen J ^a   Chau, Ngoc ^b   Robinson, Phillip J ^b   Cousin, Michael A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF SYDNEY   (Australia)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN I; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; SYNDAPIN I; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SITE DIRECTED MUTAGENESIS; SYNAPSE VESICLE;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CALCINEURIN; CALCIUM; CARRIER PROTEINS; CELLS, CULTURED; CEREBELLUM; DEXTRANS; DYNAMIN I; ELECTRIC STIMULATION; ENDOCYTOSIS; GTP PHOSPHOHYDROLASES; HORSERADISH PEROXIDASE; HYDRAZONES; MICROSCOPY, IMMUNOELECTRON; MUTAGENESIS, SITE-DIRECTED; NEURAL INHIBITION; NEURONS; OLIGONUCLEOTIDES; PHOSPHORYLATION; POTASSIUM CHLORIDE; RATS; RATS, SPRAGUE-DAWLEY; SERINE; SYNAPTIC VESICLES; SYNAPTOPHYSIN; TIME FACTORS; TRANSFECTION;

EID: 67449143251     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1976-09.2009     Document Type: Article

References (39)

1. Andersson F, Jakobsson J, Löw P, Shupliakov O, Brodin L (2008) Perturbation of syndapin/PACSIN impairs synaptic vesicle recycling evoked by intense stimulation. J Neurosci 28:3925-3933.
2. Anggono V, Robinson PJ (2007) Syndapin I and endophilin I bind overlapping proline-rich regions of dynamin I: role in synaptic vesicle endocytosis. J Neurochem 102:931-943. (Pubitemid 47057288)
3. Anggono V, Smillie KJ, Graham ME, Valova VA, Cousin MA, Robinson PJ (2006) Syndapin I is the phosphorylation-regulated dynamin I partner in synaptic vesicle endocytosis. Nat Neurosci 9:752-760.
4. Balaji J, Armbruster M, Ryan TA (2008) Calcium control of endocytic capacity at a CNS synapse. J Neurosci 28:6742-6749.
5. Chan SA, Smith C (2001) Physiological stimuli evoke two forms of endocytosis in bovine chromaffin cells. J Physiol 537:871-885. (Pubitemid 34026614)
6. Clayton EL, Cousin MA (2008) Differential labelling of bulk endocytosis in nerve terminals by FM dyes. Neurochem Int 53:51-55.
7. Clayton EL, Evans GJ, Cousin MA (2008) Bulk synaptic vesicle endocytosis is rapidly triggered during strong stimulation. J Neurosci 28:6627-6632.
8. Cousin MA, Robinson PJ (2001) The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis. Trends Neurosci 24:659-665. (Pubitemid 33152773)
9. Cousin MA, Malladi CS, Tan TC, Raymond CR, Smillie KJ, Robinson PJ (2003) Synapsin I-associated phosphatidylinositol 3-kinase mediates synaptic vesicle delivery to the readily releasable pool. J Biol Chem 278:29065-29071. (Pubitemid 36935820)
10. Evans GJ, Cousin MA (2007) Activity-dependent control of slow synaptic vesicle endocytosis by cyclin-dependent kinase 5. J Neurosci 27:401-411. (Pubitemid 46106014)
11. Ferguson SM, Brasnjo G, Hayashi M, Wölfel M, Collesi C, Giovedi S, Raimondi A, Gong LW, Ariel P, Paradise S, O'toole E, Flavell R, Cremona O, Miesenböck G, Ryan TA, De Camilli P (2007) A selective activitydependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316:570-574. (Pubitemid 46683137)
12. Grabs D, Slepnev VI, Songyang Z, David C, Lynch M, Cantley LC, De Camilli P (1997) The SH3 domain of amphiphysin binds the proline-rich domain of dynamin at a single site that defines a new SH3 binding consensus sequence. J Biol Chem 272:13419-13425. (Pubitemid 27216776)
13. Graham ME, Anggono V, Bache N, Larsen MR, Craft GE, Robinson PJ (2007) The in vivo phosphorylation sites of rat brain dynamin I. J Biol Chem 282:14695-14707. (Pubitemid 47093363)
14. 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. (Pubitemid 44374912)
15. 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.
16. Henne WM, Kent HM, Ford MG, Hegde BG, Daumke O, Butler PJ, Mittal R, Langen R, Evans PR, McMahon HT (2007) Structure and analysis of FCHo2 F-BAR domain: a dimerizing and membrane recruitment module that effects membrane curvature. Structure 15:839-852. (Pubitemid 47042426)
17. 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. (Pubitemid 36258911)
18. Itoh T, Erdmann KS, Roux A, Habermann B, Werner H, De Camilli P (2005) Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell 9:791-804. (Pubitemid 41724107)
19. Jockusch WJ, Praefcke GJ, McMahon HT, Lagnado L (2005) Clathrindependent and clathrin-independent retrieval of synaptic vesicles in retinal bipolar cells. Neuron 46:869-878. (Pubitemid 40805348)
20. Klee CB, Crouch TH, Krinks MH (1979) Calcineurin: a calcium- and calmodulin-binding protein of the nervous system. Proc Natl Acad Sci U S A 76:6270-6273. (Pubitemid 10163382)
21. Kumashiro S, Lu YF, Tomizawa K, Matsushita M, Wei FY, Matsui H (2005) Regulation of synaptic vesicle recycling by calcineurin in different vesicle pools. Neurosci Res 51:435-443. (Pubitemid 40299331)
22. Lee SY, Voronov S, Letinic K, Nairn AC, Di Paolo G, De Camilli P (2005) Regulation of the interaction between PIPKI gamma and talin by prolinedirected protein kinases. J Cell Biol 168:789-799. (Pubitemid 40328162)
23. Lou X, Paradise S, Ferguson SM, De Camilli P (2008) Selective saturation of slow endocytosis at a giant glutamatergic central synapse lacking dynamin 1. Proc Natl Acad Sci U S A 105:17555-17560.
24. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T (2006) Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 10:839-850. (Pubitemid 43779110)
25. Marks B, Stowell MH, Vallis Y, Mills IG, Gibson A, Hopkins CR, McMahon HT (2001) GTPase activity of dynamin and resulting conformation change are essential for endocytosis. Nature 410:231-235. (Pubitemid 32216598)
26. 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. (Pubitemid 44852267)
27. Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303:495-499. (Pubitemid 38120842)
28. Qualmann B, Roos J, DiGregorio PJ, Kelly RB (1999) Syndapin I, a synaptic dynamin-binding protein that associates with the neural Wiskott-Aldrich syndrome protein. Mol Biol Cell 10:501-513. (Pubitemid 29156487)
29. 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. (Pubitemid 30951856)
30. 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. (Pubitemid 27335079)
31. Rizzo MA, Springer GH, Granada B, Piston DW (2004) An improved cyan fluorescent protein variant useful for FRET. Nat Biotechnol 22:445-449. (Pubitemid 38451376)
32. Rizzoli SO, Betz WJ (2005) Synaptic vesicle pools. Nat Rev Neurosci 6:57-69. (Pubitemid 40052139)
33. Royle SJ, Lagnado L (2003) Endocytosis at the synaptic terminal. J Physiol 553:345-355. (Pubitemid 37527539)
34. Shimada A, Niwa H, Tsujita K, Suetsugu S, Nitta K, Hanawa-Suetsugu K, Akasaka R, Nishino Y, Toyama M, Chen L, Liu ZJ, Wang BC, Yamamoto M, Terada T, Miyazawa A, Tanaka A, Sugano S, Shirouzu M, Nagayama K, Takenawa T, et al. (2007) Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129:761-772. (Pubitemid 46813111)
35. Shupliakov O, Löw P, Grabs D, Gad H, Chen H, David C, Takei K, De Camilli P, Brodin L (1997) Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276:259-263. (Pubitemid 27172685)
36. Tan TC, Valova VA, Malladi CS, Graham ME, Berven LA, Jupp OJ, Hansra G, McClure SJ, Sarcevic B, Boadle RA, Larsen MR, Cousin MA, Robinson PJ (2003) Cdk5 is essential for synaptic vesicle endocytosis. Nat Cell Biol 5:701-710. (Pubitemid 36986777)
37. Teng H, Lin MY, Wilkinson RS (2007) Macroendocytosis and endosome processing in snake motor boutons. J Physiol 582:243-262. (Pubitemid 46993573)
38. 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. (Pubitemid 350072088)
39. Wu W, Xu J, Wu XS, Wu LG (2005) Activity-dependent acceleration of endocytosis at a central synapse. J Neurosci 25:11676-11683. (Pubitemid 43098460)