A pre-synaptic to-do list for coupling exocytosis to endocytosis

Current Opinion in Cell Biology

Volumn 18, Issue 4, 2006, Pages 416-421

  Ryan, Timothy A ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CLATHRIN; MEMBRANE PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; BLEACHING; CELL SELECTION; CELL SORTER; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; COATED VESICLE; ENDOCYTOSIS; EXOCYTOSIS; GENETIC SCREENING; MOLECULAR RECOGNITION; NERVE ENDING; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REVIEW; SEQUENCE ANALYSIS; STOICHIOMETRY; STRUCTURAL HOMOLOGY; SYNAPSE VESICLE; TEMPERATURE SENSITIVITY;

ANIMALS; CELL MEMBRANE; ENDOCYTOSIS; EXOCYTOSIS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PRESYNAPTIC TERMINALS; SYNAPTIC VESICLES;

EID: 33745755751     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2006.06.013     Document Type: Review

References (53)

1. Sudhof T.C. The synaptic vesicle cycle. Annu Rev Neurosci 27 (2004) 509-547
2. Sankaranarayanan S., and Ryan T.A. Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat Cell Biol 2 (2000) 197-204
3. Li Z., and Murthy V.N. Visualizing postendocytic traffic of synaptic vesicles at hippocampal synapses. Neuron 31 (2001) 593-605
4. Willig K.I., Rizzoli S.O., Westphal V., Jahn R., and Hell S.W. STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis. Nature 440 (2006) 935-939. The first application of an exciting super-resolution optical technique to analyze the density of Syt I in vesicles and on the plasma membrane.
5. Zhang J.Z., Davletov B.A., Sudhof T.C., and Anderson R.G. Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell 78 (1994) 751-760
6. Haucke V., and De Camilli P. AP-2 recruitment to synaptotagmin stimulated by tyrosine-based endocytic motifs. Science 285 (1999) 1268-1271
7. Gricliattit A., Hall L., Rosenblut R., and Suzuki D.T. Temperature-sensitive mutations in Drosophila melanogaster. XIV. A selection of immobile adults. Mol Gen Genet 120 (1973) 107-114
8. Fergestad T., and Broadie K. Interaction of stoned and synaptotagmin in synaptic vesicle endocytosis. J Neurosci 21 (2001) 1218-1227
9. Stimson D.T., Estes P.S., Rao S., Krishnan K.S., Kelly L.E., and Ramaswami M. Drosophila stoned proteins regulate the rate and fidelity of synaptic vesicle internalization. J Neurosci 21 (2001) 3034-3044
10. Phillips A.M., Smith M., Ramaswami M., and Kelly L.E. The products of the Drosophila stoned locus interact with synaptic vesicles via synaptotagmin. J Neurosci 20 (2000) 8254-8261
11. Fergestad T., Davis W.S., and Broadie K. The stoned proteins regulate synaptic vesicle recycling in the presynaptic terminal. J Neurosci 19 (1999) 5847-5860
12. Diril M.K., Wienisch M., Jung N., Klingauf J., and Haucke V. Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Dev Cell 10 (2006) 233-244. This paper provides the first evidence that sorting of the SV protein Syt I requires the coordinated effort of two different adaptors, AP-2 and stonin.
13. Brett T.J., and Traub L.M. Molecular structures of coat and coat-associated proteins: function follows form. Curr Opin Cell Biol (2006) this issue
14. Bonifacino J.S., and Traub L.M. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72 (2003) 395-447
15. Jarousse N., Wilson J.D., Arac D., Rizo J., and Kelly R.B. Endocytosis of synaptotagmin 1 is mediated by a novel, tryptophan-containing motif. Traffic 4 (2003) 468-478
16. Nicholson-Tomishima K., and Ryan T.A. Kinetic efficiency of endocytosis at mammalian CNS synapses requires synaptotagmin I. Proc Natl Acad Sci U S A 101 (2004) 16648-16652. This paper, as well as [17], provides direct evidence that a SV membrane protein directly controls the kinetics of endocytosis at nerve terminals.
17. Poskanzer K.E., Marek K.W., Sweeney S.T., and Davis G.W. Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 426 (2003) 559-563
18. Poskanzer K.E., Fetter R.D., and Davis G.W. Discrete residues in the c(2)b domain of synaptotagmin I independently specify endocytic rate and synaptic vesicle size. Neuron 50 (2006) 49-62. The authors provide a detailed dissection of the regions in Syt I that control endocytosis and are able to distinguish separate control of endocytic vesicle size and retrieval speed.
19. Wenk M.R., Pellegrini L., Klenchin V.A., Di Paolo G., Chang S., Daniell L., Arioka M., Martin T.F., and De Camilli P. PIP kinase Iγ is the major PI(4,5)P(2) synthesizing enzyme at the synapse. Neuron 32 (2001) 79-88
20. 2 on demand during synaptic activity. Animals that lack the critical PI(4)P kinase cannot maintain the balance of exocytosis and endocytosis at nerve terminals during synaptic activity.
21. De Camilli P., Chen H., Hyman J., Panepucci E., Bateman A., and Brunger A.T. The ENTH domain. FEBS Lett 513 (2002) 11-18
22. Ford M.G., Mills I.G., Peter B.J., Vallis Y., Praefcke G.J., Evans P.R., and McMahon H.T. Curvature of clathrin-coated pits driven by epsin. Nature 419 (2002) 361-366
23. Hinrichsen L., Meyerholz A., Groos S., and Ungewickell E.J. Bending a membrane: How clathrin affects budding. Proc Nat Acad Sci USA 103 (2006) 8715-8720. Using electron microscopic analysis of cells depleted of clathrin through the use of siRNA, the authors show that clathrin is essential for generating curved membranes at sites where AP-2 is clustered.
24. Zhang B., Koh Y.H., Beckstead R.B., Budnik V., Ganetzky B., and Bellen H.J. Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 21 (1998) 1465-1475
25. Morgan J.R., Zhao X., Womack M., Prasad K., Augustine G.J., and Lafer E.M. A role for the clathrin assembly domain of AP180 in synaptic vesicle endocytosis. J Neurosci 19 (1999) 10201-10212
26. Nonet M.L., Holgado A.M., Brewer F., Serpe C.J., Norbeck B.A., Holleran J., Wei L., Hartwieg E., Jorgensen E.M., and Alfonso A. UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol Biol Cell 10 (1999) 2343-2360
27. Lichte B., Veh R.W., Meyer H.E., and Kilimann M.W. Amphiphysin, a novel protein associated with synaptic vesicles. EMBO J 11 (1992) 2521-2530
28. Evergren E., Marcucci M., Tomilin N., Low P., Slepnev V., Andersson F., Gad H., Brodin L., De Camilli P., and Shupliakov O. Amphiphysin is a component of clathrin coats formed during synaptic vesicle recycling at the lamprey giant synapse. Traffic 5 (2004) 514-528
29. Takei K., Slepnev V.I., Haucke V., and De Camilli P. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1 (1999) 33-39
30. Peter B.J., Kent H.M., Mills I.G., Vallis Y., Butler P.J., Evans P.R., and McMahon H.T. BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303 (2004) 495-499. The authors solve the structure of the Drosophila amphiphysin BAR domain, revealing its curved structure, which provides a potential basis for its role in generating or sensing membrane curvature.
31. Yoshida Y., Kinuta M., Abe T., Liang S., Araki K., Cremona O., Di Paolo G., Moriyama Y., Yasuda T., De Camilli P., et al. The stimulatory action of amphiphysin on dynamin function is dependent on lipid bilayer curvature. EMBO J 23 (2004) 3483-3491
32. Di Paolo G., Sankaranarayanan S., Wenk M.R., Daniell L., Perucco E., Caldarone B.J., Flavell R., Picciotto M.R., Ryan T.A., Cremona O., et al. Decreased synaptic vesicle recycling efficiency and cognitive deficits in amphiphysin 1 knockout mice. Neuron 33 (2002) 789-804
33. Gallop J.L., Butler P.J., and McMahon H.T. Endophilin and CtBP/BARS are not acyl transferases in endocytosis or Golgi fission. Nature 438 (2005) 675-678
34. Farsad K., Ringstad N., Takei K., Floyd S.R., Rose K., and De Camilli P. Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J Cell Biol 155 (2001) 193-200
35. Dickman D.K., Horne J.A., Meinertzhagen I.A., and Schwarz T.L. A slowed classical pathway rather than kiss-and-run mediates endocytosis at synapses lacking synaptojanin and endophilin. Cell 123 (2005) 521-533. This paper, along with [36,37], demonstrates a clear requirement for endophilin in synaptic vesicle endocytosis.
36. Verstreken P., Kjaerulff O., Lloyd T.E., Atkinson R., Zhou Y., Meinertzhagen I.A., and Bellen H.J. Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109 (2002) 101-112
37. Gad H., Ringstad N., Low P., Kjaerulff O., Gustafsson J., Wenk M., Di Paolo G., Nemoto Y., Crun J., Ellisman M.H., et al. Fission and uncoating of synaptic clathrin-coated vesicles are perturbed by disruption of interactions with the SH3 domain of endophilin. Neuron 27 (2000) 301-312
38. Schuske K.R., Richmond J.E., Matthies D.S., Davis W.S., Runz S., Rube D.A., van der Bliek A.M., and Jorgensen E.M. Endophilin is required for synaptic vesicle endocytosis by localizing synaptojanin. Neuron 40 (2003) 749-762
39. Verstreken P., Koh T.W., Schulze K.L., Zhai R.G., Hiesinger P.R., Zhou Y., Mehta S.Q., Cao Y., Roos J., and Bellen H.J. Synaptojanin is recruited by endophilin to promote synaptic vesicle uncoating. Neuron 40 (2003) 733-748
40. Koenig J.H., and Ikeda K. Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J Neurosci 9 (1989) 3844-3860
41. Takei K., McPherson P.S., Schmid S.L., and De Camilli P. Tubular membrane invaginations coated by dynamin rings are induced by GTP-γ S in nerve terminals. Nature 374 (1995) 186-190
42. Danino D., Moon K.H., and Hinshaw J.E. Rapid constriction of lipid bilayers by the mechanochemical enzyme dynamin. J Struct Biol 147 (2004) 259-267. This study uses cryo-electron microscopy to show that upon GTP hydrolysis the helical assembly of dynamin constricts around the lipid membrane it surrounds.
43. Chen Y.J., Zhang P., Egelman E.H., and Hinshaw J.E. The stalk region of dynamin drives the constriction of dynamin tubes. Nat Struct Mol Biol 11 (2004) 574-575. Cryo-electron microscopy was used to solve the structure of dynamin in both the constricted and non-contricted states to ∼20 Å resolution.
44. Cousin M.A., and Robinson P.J. The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis. Trends Neurosci 24 (2001) 659-665
45. Anggono V., Smillie K.J., Graham M.E., Valova V.A., Cousin M.A., and Robinson P.J. Syndapin I is the phosphorylation-regulated dynamin I partner in synaptic vesicle endocytosis. Nat Neurosci 9 (2006) 752-760. This paper identifies syndapin as a specific binding partner of dynamin that is controlled by the cycle of phosphorylation and dephosphorylation of dynamin that occurs during synaptic activity.
46. Kessels M.M., and Qualmann B. The syndapin protein family: linking membrane trafficking with the cytoskeleton. J Cell Sci 117 (2004) 3077-3086
47. Itoh T., Erdmann K.S., Roux A., Habermann B., Werner H., and De Camilli P. Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev Cell 9 (2005) 791-804
48. Shupliakov O., Bloom O., Gustafsson J.S., Kjaerulff O., Low P., Tomilin N., Pieribone V.A., Greengard P., and Brodin L. Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proc Natl Acad Sci U S A 99 (2002) 14476-14481
49. Sankaranarayanan S., Atluri P., and Ryan T.A. Actin serves a molecular scaffolding not a propulsive role in presynaptic function. Nat Neurosci 6 (2003) 127-135
50. Cremona O., Di Paolo G., Wenk M.R., Luthi A., Kim W.T., Takei K., Daniell L., Nemoto Y., Shears S.B., Flavell R.A., et al. Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99 (1999) 179-188
51. Atluri P.P., and Ryan T.A. The kinetics of synaptic vesicle reacidification at hippocampal nerve terminals. J Neurosci 26 (2006) 2313-2320
52. Cousin M.A., and Nicholls D.G. Synaptic vesicle recycling in cultured cerebellar granule cells: role of vesicular acidification and refilling. J Neurochem 69 (1997) 1927-1935
53. Zhou Q., Petersen C.C., and Nicoll R.A. Effects of reduced vesicular filling on synaptic transmission in rat hippocampal neurones. J Physiol 525 (2000) 195-206