Endophilin/sh3p4 is required for the transition from early to late stages in clathrin-mediated synaptic vesicle endocytosis

Neuron

Volumn 24, Issue 1, 1999, Pages 143-154

  Ringstad, Niels ^a   Gad, Helge ^b   Löw, Peter ^b   Di Paolo, Gilbert ^a   Brodin, Lennart ^b   Shupliakov, Oleg ^b   De Camilli, Pietro ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; CLATHRIN; DYNAMIN; GUANOSINE TRIPHOSPHATASE; PHOSPHATASE;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; ENDOCYTOSIS; IMMUNOELECTRON MICROSCOPY; IMMUNOGOLD STAINING; LAMPREY; MEMBRANE STRUCTURE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SPINAL CORD; SYNAPSE VESICLE;

EID: 0033199465     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80828-4     Document Type: Article

References (44)

1. Baba, T., Ueda, H., Terada, N., Fujii, Y., and Ohno, S. (1999). Immunocytochemical study of endocytotic structures accumulated in HeLa cells transformed with a temperature-sensitive mutant of dynamin. J. Histochem. Cytochem. 47, 637-648.
2. Ball, C.L., Hunt, S.P., and Robinson, M.S. (1995). Expression and localization of alpha-adaptin isoforms. J. Cell Sci. 108, 2865-2875.
3. Brodin, L., Shupliakov, O., Hellgren, J., Pieribone, V., and Hill, R. (1994). The reticulospinal glutamate synapse in lamprey: plasticity and presynaptic variability. J. Neurophysiol. 72, 592-604.
4. Chen, M.S., Obar, R.A., Schroeder, C.C., Austin, T.W., Poodry, CA., Wadsworth, S.C., and Vallee, R.B. (1991). Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature 351, 583-586.
5. Cremona, O., and De Camilli, P. (1997). Synaptic vesicle exocytosis. Curr. Opin. Neurobiol. 7, 323-330.
6. Damke, H., Baba, T., Warnock, D.E., and Schmid, S.L. (1994). Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934.
7. David, C., McPherson, P.S., Mundigl, O., and De Camilli, P. (1996). A role of amphiphysin in synaptic vesicle endocytosis suggested by its binding to dynamin in nerve terminals. Proc. Natl. Acad. Sci. USA 93, 331-335.
8. De Camilli, P., Harris, S.M., Jr., Huttner, W.B., and Greengard, P. (1983). Synapsin I (Protein I), a nerve terminal-specific phosphoprotein. II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose-embedded synaptosomes. J. Cell Biol. 96, 1355-1373.
9. de Heuvel, E., Bell, A.W., Ramjaun, A.R., Wong, K., Sossin, W.S., and McPherson, P.S. (1997). Identification of the major synaptojanin-binding proteins in brain. J. Biol. Chem. 272, 8710-8716.
10. Faundez, V., Horng, J.T., and Kelly, R.B. (1998). A function for the AP3 coat complex in synaptic vesicle formation from endosomes. Cell 93, 423-432.
11. 2+-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse. Neuron 21, 607-616.
12. Gonzélez-Gaitén, M., and Jäckle, H. (1997). Role of Drosophila α-adaptin in presynaptic vesicle recycling. Cell 88, 767-776.
13. Grabs, D., Slepnev, V.I., Songyang, Z., David, C., Lynch, M., Cantley, L.C., and 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.
14. Guo, S., Stolz, L.E., Lemrow, S.M., and York, J.D. (1999). SAC1-like domains of yeast SAC1, INP52, and INP53 and of human synaptojanin encode polyphosphoinositide phosphatases. J. Biol. Chem. 274, 12990-12995.
15. Herskovits, J.S., Burgess, C.C., Obar, R.A., and Vallee, R.B. (1993). Effects of mutant rat dynamin on endocytosis. J. Cell Biol. 122, 565-578.
16. Heuser, J.E. (1980). Three-dimensional visualization of coated vesicle formation in fibroblasts. J. Cell Biol. 84, 560-583.
17. Heuser, J.E. (1989). Effects of cytoplasmic acidification on clathrin lattice morphology. J. Cell Biol. 108, 401-411.
18. Heuser, J.E., and Reese, T.S. (1973). Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315-344.
19. Kirchhausen, T., and Harrison, S.C. (1981). Protein organization in clathrin trimers. Cell 23, 755-761.
20. Koenig, J.H., and Ikeda, K. (1989). Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 9, 3844-3860.
21. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
22. Maycox, P.R., Link, E., Reetz, A., Morris, S.A., and Jahn, R. (1992). Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J. Cell Biol. 118, 1379-1388.
23. McPherson, P.S., Garcia, E.P., Slepnev, V.I., David, C., Zhang, X., Grabs, D., Sossin, W.S., Bauerfeind, R., Nemoto, Y., and De Camilli, P. (1996). A presynaptic inositol-5-phosphatase. Nature 379, 353-357.
24. Micheva, K.D., Kay, B.K., and McPherson, P.S. (1997). Synaptojanin forms two separate complexes in the nerve terminal. Interactions with endophilin and amphiphysin. J. Biol. Chem. 272, 27239-27245.
25. Moore, M.S., Mahaffey, D.T., Brodsky, F.M., and Anderson, R.G. (1987). Assembly of clathrin-coated pits onto purified plasma membranes. Science 236, 558-563.
26. Pfeffer, S.R., and Kelly, R.B. (1985). The subpopulation of brain coated vesicles that carries synaptic vesicle proteins contains two unique polypeptides. Cell 40, 949-957.
27. Pieribone, V.A., Shupliakov, O., Brodin, L., Hilfiker-Rothenfluh, S., Czernik, A.J., and Greengard, P. (1995). Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375, 493-497.
28. Qualmann, B., Roos, J., DiGregorio, P.J., and Kelly, R.B. (1999). Syndapin I, a synaptic dynamin-binding protein that associates with the neural Wiskott-Aldrich syndrome protein. Mol. Biol. Cell 10, 501-513.
29. Raucher, D., and Sheetz, M.P. (1999). Membrane expansion increases endocytosis rate during mitosis. J. Cell Biol. 144, 497-506.
30. Ringstad, N., Nemoto, Y., and 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. USA 94, 8569-8574.
31. Rodal, S.K., Skretting, G., Garred, O., Vilhardt, F., van Deurs, B., and Sandvig, K. (1999). Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell 4, 961-974.
32. Schmid, S.L., McNiven, M.A., and De Camilli, P. (1998). Dynamin and its partners: a progress report. Curr. Opin. Cell Biol. 10, 504-512.
33. Schmidt, A., and Huttner, W.B. (1998). Biogenesis of synaptic-like microvesicles in perforated PC12 cells. Methods Enzymol. 16, 160-169.
34. Shupliakov, O., Pieribone, V., Gad, H., and Brodin, L. (1995). Synaptic vesicle depletion in reticulospinal axons is reduced by 5-HT: direct evidence for presynaptic modulation of glutamatergic transmission. Eur. J. Neurosci. 7, 1111-1116.
35. Shupliakov, O., Löw, P., Grabs, D., Gad, H., Chen, H., David, C., Takei, K., De Camilli, P., and Brodin, L. (1997). Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276, 259-263.
36. Smith, C.J., Grigorieff, N., and Pearse, B.M. (1998). Clathrin coats at 21 Å resolution: a cellular assembly designed to recycle multiple membrane receptors. EMBO J. 17, 4943-4953.
37. Takei, K., McPherson, P.S., Schmid, S.L., and De Camilli, P. (1995). Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature 374, 186-190.
38. Takei, K., Mundigl, O., Daniell, L., and De Camilli, P. (1996). The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin. J. Cell Biol. 133, 1237-1250.
39. Takei, K., Slepnev, V., Haucke, V., and De Camilli, P. (1999). Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1, 33-39.
40. ter Haar, E., Musacchio, A., Harrison, S.C., and Kirchhausen, T. (1998). Atomic structure of clathrin: a beta propeller terminal domain joins an alpha zigzag linker. Cell 95, 563-573.
41. Towbin, H., Staehelin, T., and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354.
42. van der Bliek, A.M., and Meyerowitz, E.M. (1991). Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351, 411-414.
43. Witke, W., Podtelejnikov, A.V., Di Nardo, A., Sutherland, J.D., Gurniak, C.B., Dotti, C., and Mann, M. (1998). In mouse brain profilin I and profilin II associate with regulators of the endocytic pathway and actin assembly. EMBO J. 17, 967-976.
44. Zhang, B., Koh, Y.H., Beckstead, R.B., Budnik, V., Ganetzky, B., and Bellen, H.J. (1998). Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 21, 1465-1475.