Sequential steps in clathrin-mediated synaptic vesicle endocytosis

Current Opinion in Neurobiology

Volumn 10, Issue 3, 2000, Pages 312-320

  Brodin, Lennart ^a   Löw, Peter ^a   Shupliakov, Oleg ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CLATHRIN; DYNAMIN; GUANOSINE TRIPHOSPHATASE; LYSOPHOSPHOLIPASE; PHOSPHATASE; SYNAPTOTAGMIN;

ANIMAL CELL; CELL MEMBRANE; ENDOCYTOSIS; HUMAN; HUMAN CELL; NERVE ENDING; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SYNAPSE; SYNAPSE VESICLE;

ANIMALS; CLATHRIN; ENDOCYTOSIS; NEURONS; SYNAPTIC VESICLES;

EID: 0342748583     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(00)00097-0     Document Type: Review

References (55)

1. Schmid S.L. Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu Rev Biochem. 66:1997;511-548.
2. Cremona O., De Camilli P. Synaptic vesicle endocytosis. Curr Opin Neurobiol. 7:1997;323-330.
3. Gonzalez-Gaitan M., Jackle H. Role of Drosophila alpha-adaptin in presynaptic vesicle recycling. Cell. 88:1997;767-776.
4. Shupliakov O., Löw P., Grabs D., Gad H., Chen H., David C., Takei K., De Camilli P., Brodin L. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science. 276:1997;259-263.
5. Zhang B., Koh Y.H., Beckstead R.B., Budnik V., Ganetzky B., Bellen H.J. Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron. 21:1998;1465-1475.
6. Nonet M.L., Holgado A.M., Brewer F., Serpe C.J., Norbeck B.A., Holleran J., Wei L.P., Hartwieg E., Jorgensen E.M., 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.
7. Morgan J.R., Zhao X., Womack M., Prasad K., Augustine G.J., Lafer E. A role for the clathrin assembly domain of AP180 in synaptic vesicle endocytosis. J Neurosci. 19:1999;10201-10212.
8. ••).
9. Fesce F., Meldolesi J. Peeping at the vesicle kiss. Nat Cell Biol. 1:1999;E3-E4.
10. Klingauf J., Kavalali E.T., Tsien R.W. Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature. 394:1998;581-585.
11. Marsh M., McMahon H.T. The structural era of endocytosis. Science. 285:1999;215-220.
12. Ungewickell E. Wrapping the package. Proc Natl Acad Sci USA. 96:1999;8809-8810.
13. Martin T.F. Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu Rev Cell Dev Biol. 14:1998;231-264.
14. Corvera S., D'Arrigo S., Stenmark H. Phosphoinositides in membrane traffic. Curr Opin Cell Biol. 11:1999;460-465.
15. Kelly R.B. Deconstructing membrane traffic. Trends Cell Biol 9:M29-M32. 1999.
16. Kirchhausen T., Bonifacino J.S., Riezman H. Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr Opin Cell Biol. 9:1997;488-495.
17. •).
18. ••)).
19. Gaidarov I., Keen J.H. Phosphoinositide-AP-2 interactions required for targeting to plasma membrane clathrin-coated pits. J Cell Biol. 146:1999;755-764.
20. Arneson L.S., Kunz J., Anderson R.A., Traub L.M. Coupled inositide phosphorylation and phospholipase D activation initiates clathrin-coat assembly on lysosomes. J Biol Chem. 274:1999;17794-17805.
21. Jost M., Simpson F., Kavran J.M., Lemmon M.A., Schmid S.L. Phosphatidylinositol (4,5) bisphosphate is required for endocytic coated vesicle formation. Curr Biol. 8:1998;1399-1402.
22. Schmid S.L., McNiven M.A., De Camilli P. Dynamin and its partners: a progress report. Curr Opin Cell Biol. 10:1998;504-512.
23. Roos J., Kelly R.B. Dap160, a neural-specific Eps15 homology and multiple SH3 domain-containing protein that interacts with Drosophila dynamin. J Biol Chem. 273:1998;9108-9119.
24. •)).
25. Sweitzer S.M., Hinshaw J.E. Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell. 93:1998;1021-1029.
26. Takei K., Haucke V., Slepnev V., Farsad K., Salazar M., Chen H., De Camilli P. Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell. 94:1998;131-141.
27. Stowell M.H.B., Marks B., Wigge P., McMahon H.T. Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nat Cell Biol. 1:1999;27-32.
28. Takei K., Slepnev V.I., Haucke V., De Camilli P. Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol. 1:1999;33-39. This study shows that amphiphysin 1 can bind lipid membranes, that it can transform spherical liposomes into narrow tubules, and that it can co-assemble with dynamin 1 and enhance the lipid-fragmenting activity of dynamin 1 in the presence of GTP. The results indicate a close functional relationship between amphiphysin and dynamin (see also (4,11)), and they suggest that both proteins may contribute to the generation of bilayer curvature during endocytic membrane budding.
29. Cremona O., Di Paolo G., Wenk M.K., Luthi A., Kim W., 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. Mice lacking synaptojanin 1 are shown to exhibit neurological deficits and die shortly after birth. The level of phosphatidylinositol-4,5-bisphosphate is increased in cultured neurons from knockout mice, and the generation of clathrin coats on protein-free liposomes (in the presence of ATP and GTPγS) is enhanced when normal cytosol is replaced with cytosol from knockout mice. The relative proportion of coated vesicles versus synaptic vesicles in nerve terminals of knockout mice is higher than in wild-type mice. A model is proposed in which synaptojanin facilitates the shedding of the clathrin coat after endocytosis.
30. Guo S., Stolz L.E., Lemrow S.M., York J.D. SAC1-like domains of yeast SAC1, INP52, and INP53 and of human synaptojanin encode polyphosphoinositide phosphatases. J Biol Chem. 274:1999;12990-12995.
31. ••).
32. Witke W., Podtelejnikov A.V., Di Nardo A., Sutherland J.D., Gurniak C.B., Dotti C., Mann M. In mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly. EMBO J. 17:1998;967-976.
33. Roos J., Kelly R.B. The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr Biol. 9:1999;1411-1414.
34. Gustafsson J., Shupliakov O., Takei K., Löw P., De Camilli P., Brodin L. GTPγS induces an actin matrix associated with coated endocytic intermediates in presynaptic regions. Soc Neurosci Abstr. 327:1998;19.
35. Sone M., Hoshino M., Suzuki E., Kuroda S., Kaibuchi K., Nakagoshi H., Saigo K., Nabeshima Y., Hama C. Still life, a protein in synaptic terminals of Drosophila homologous to GDP-GTP exchangers. Science. 275:1997;543-547.
36. Gaidarov I., Santini F., Warren R.A., Keen J.H. Spatial control of coated pit dynamics in living cells. Nat Cell Biol. 1:1999;1-7. A fusion protein consisting of green fluorescent protein and clathrin light chain is used to study dynamic aspects of endocytosis in COS-1 cells and other mammalian cell lines. The mobility of invaginating clathrin-coated pits is shown to be limited, but increases after disruption of the actin cytoskeleton. Coated pits are found to form repeatedly at defined sites, while other regions are excluded.
37. Gad H., Löw P., Zotova E., Brodin L., Shupliakov O. Dissociation between Ca2+-evoked synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central vertebrate synapse. Neuron. 21:1998;607-616.
38. Brodin L., Bakeeva L., Shupliakov O. Presynaptic mitochondria and the temporal pattern of neurotransmitter release. Phil Trans R Soc Lond B Biol Sci. 354:1999;365-372.
39. Rodal S.K., Skretting G., Garred O., Vilhardt F., van Deurs B., Sandvig K. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell. 10:1999;961-974.
40. Subtil A., Gaidarov I., Kobylarz K., Lampson M.A., Keen J.H., McGraw T.E. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc Natl Acad Sci USA. 96:1999;6775-6780.
41. Simpson F., Hussain N.K., Qualmann B., Kelly R.B., Kay B.K., McPherson P., Schmid S.L. SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation. Nat Cell Biol. 1:1999;119-124.
42. Merrifield C.J., Moss S.E., Ballestrem C., Imhof B.A., Giese G., Wunderlich I., Almers W. Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nat Cell Biol. 1:1999;72-74. A fusion protein consisting of green fluorescent protein and actin is used to study the dynamics of actin filaments during endocytosis in mast cells. Actin 'tails' formed during endocytosis are shown to follow the endocytic vesicle as it moves into the cell.
43. Machesky L.M., Insall R.H. Signalling to actin dynamics. J Cell Biol. 146:1999;267-272.
44. •)).
45. Sever S., Muhlberg A.B., Schmid S.L. Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature. 398:1999;481-486. The GTPase effector domain (GED) of dynamin is shown to function as a GTPase-activating protein (GAP) which coordinates dynamin self-assembly with increased GTPase activity. Mutations causing a defect in assembly-stimulated GTPase activity are shown to stimulate, rather than inhibit, endocytosis. This finding is not compatible with previous models of dynamin function which suggested that endocytic membrane fission is driven by dynamin's GTPase activity. A model is proposed in which dynamin-GTP is in an active conformation which recruits the fission machinery that is required for vesicle formation.
46. ••)).
47. Huttner W.B. Protein and lipid sorting in the secretory and endocytic pathways - receptors and mechanisms. Semin Cell Dev Biol. 9:1998;491-492.
48. Murthy V.N., Stevens C.F. Synaptic vesicles retain their identity through the endocytic cycle. Nature. 392:1998;497-501.
49. •)).
50. Ramjaun A., Phillie J., de Heuvel E., McPherson P.S. The N terminus of amphiphysin II mediates dimerization and plasma membrane targeting. J Biol Chem. 274:1999;19785-19791.
51. Okamoto M., Schoch Südhof T. EHSH1/Intersectin, a protein that contains EH and SH3 domains and binds to dynamin and SNAP-25. J Biol Chem. 26:1999;18446-18454.
52. Slepnev V.I., Ochoa G.C., Butler M.H., Grabs D., Camilli P.D. Role of phosphorylation in regulation of the assembly of endocytic coat complexes. Science. 281:1998;821-824.
53. Sankaranarayanan S., Ryan T.A. Real-time measurement of vesicle SNARE recycling in synapses of the central nervous system. Nat Cell Biol. 2:2000;197-204. A pH-sensitive GFP linked to synaptobrevin (also known as vesicle-associated membrane protein, or VAMP) was used to monitor vesicle recycling in cultured hippocampal neurons. The measured time courses are consistent with a single, presumably clathrin-mediated, endocytic pathway.
54. Plohmann M., Lange R., Vopper G., Cremer H., Heinlein V.A., Scheff S., Baldwin S.A., Leitges M., Cramer M., Paulsson M., Barthels D. PACSIN, a brain protein that is upregulated upon differentiation into neuronal cells. Eur J Biochem. 256:1998;210-211.
55. Takei K., McPherson P.S., Schmid S.L., De Camilli P. Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature. 374:1995;186-190.