SH3-domain-containing proteins function at distinct steps in clathrin-coated vesicle formation

Nature Cell Biology

Volumn 1, Issue 2, 1999, Pages 119-124

  Simpson, Fiona ^a   Hussain, Natasha K ^b   Qualmann, Britta ^c   Kelly, Regis B ^c   Brian K, Kay ^d   McPherson, Peter S ^b   Schmid, Sandra L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMPHIPHYSIN; CARRIER PROTEIN; CLATHRIN; DYNAMIN; GLUTATHIONE TRANSFERASE; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATE; HYBRID PROTEIN; INTERSECTIN 1; NERVE PROTEIN; PACSIN1 PROTEIN, HUMAN; PACSIN1 PROTEIN, RAT; SH3GL2 PROTEIN, HUMAN; SH3GL2 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ADIPOCYTE; ANIMAL; ARTICLE; CELL CULTURE; CELL STRAIN 3T3; CHEMISTRY; COATED VESICLE; CYTOLOGY; ENDOCYTOSIS; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY; SRC HOMOLOGY DOMAIN; ULTRASTRUCTURE;

3T3 CELLS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ADENOSINE TRIPHOSPHATE; ADIPOCYTES; ANIMALS; CARRIER PROTEINS; CLATHRIN; COATED VESICLES; DYNAMINS; ENDOCYTOSIS; GLUTATHIONE TRANSFERASE; GTP PHOSPHOHYDROLASES; GUANOSINE TRIPHOSPHATE; HUMANS; MICE; NERVE TISSUE PROTEINS; RECOMBINANT FUSION PROTEINS; SRC HOMOLOGY DOMAINS; TUMOR CELLS, CULTURED;

EID: 0033147449     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/10091     Document Type: Article

References (50)

1. Schmid, S. L., McNiven, M. A. & De Camilli, P. Dynamin and its partners: a progress report. Curr. Opin. Cell Biol. 10, 504-512 (1998).
2. Sever, S., Muhlberg, A. B. & Schmid, S. L. Impairment of dynamin's GAP domain stimulates receptor-mediated endocytosis. Nature 398, 481-486 (1999).
3. David, C., McPherson, P. S., Mundigl, O. & de Camilli, P. 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 (1996).
4. Leprince, C. et al. A new member of the amphiphysin family connecting endocytosis and signal transduction pathways. J. Biol. Chem. 272, 15101-15105 (1997).
5. Ramjaun, A. R., Micheva, K. D., Bouchelet, I. & McPherson, P. S. Identification and characterization of a nerve terminal-enriched amphiphysin isoform. J. Biol. Chem. 272, 16700-16706 (1997).
6. de Heuvel, E. et al. Identification of the major synaptojanin-binding proteins in brain. J. Biol. Chem. 272, 8710-8716 (1997).
7. Ringstad, N., Nemoto, Y. & De Camilli, P. 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 (1997).
8. 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, 19108-19119 (1998).
9. Yamabhai, M. et al. Intersectin, a novel adaptor protein with two eps15 homology and five src homology 3 domains. J. Biol. Chem. 273, 31401-31407 (1998).
10. Senger, A. S., Wang, W., Bishay, J., Cohen, S. & Egan, S. E. The EH and SH3 domain Ese proteins regulate endocytosis by linking to dynamin and Eps15. EMBO J. 18, 1159-1171 (1999).
11. Qualmann, B., Roos, J., DiGregorio, P. J. & Kelly, R. B. Syndapin I, a synaptic dynamin-binding protein that associates with the neural Wiskott-Aldrich syndrome protein. Mol. Biol. Cell 10, 501-513 (1999).
12. Gout, I. et al. The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell 75, 25-36 (1993).
13. McPherson, P. S. et al. A presynaptic inositol 5 phosphatase. Nature 379, 353-357 (1996).
14. McPherson, P. S. et al. Interaction of Grb2 via its Src homology 3 domains with synaptic proteins including synapsin I. Proc. Natl Acad. Sci. USA 91, 6486-6490 (1994).
15. Wigge, P. & McMahon, H. T. The amphiphysin family of proteins and their role in endocytosis at the synapse. Trends Neurosci. 21, 339-344 (1998).
16. Shupliakov, O. et al. Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276, 259-263 (1997).
17. Wigge, P., Vallis, Y. & McMahon, H. T. Inhibition of receptor-mediated endocytosis by the amphiphysin SH3 domain. Curr. Biol. 7, 554-560 (1997).
18. Di Fiore, P. P., Pelicci, P. G. & Sorkin, A. EH: a novel protein-protein interaction domain potentially involved in intracellular sorting. Trends Biochem. Sci. 22, 411-413 (1997).
19. Hussain, N. K. et al. Splice variants of intersectin are components of the endocytic machinery in neurons and non-neuronal cells. J. Biol. Chem. 274, 15671-15677 (1999).
20. Mahaffey, D. T., Moore, M. S., Brodsky, F. M. & Anderson, R. G. W. Coat proteins isolated from clathrin coated vesicles can assemble into coated pits. J. Cell Biol. 108, 1615-1624 (1989).
21. Lin, H. C., Moore, M. S., Sanan, D. A. & Anderson, R. G. W. Reconstitution of clathrin-coated pit budding from plasma membranes. J. Cell Biol. 114, 881-891 (1991).
22. Gilbert, A., Paccaud, J. P. & Carpentier, J. L. Direct measurement of clathrin-coated vesicle formation using a cell-free assay. J. Cell Sci. 110, 3105-3115 (1997).
23. Schmid, S. L. & Smythe, E. Stage-specific assays for coated pit formation and coated vesicle budding in vitro. J. Cell Biol. 114, 869-880 (1991).
24. Smythe, E., Carter, L. L. & Schmid, S. L. Cytosol- and clathrin-dependent stimulation of endocytosis in vitro by purified adaptors. J. Cell Biol. 119, 1163-1171 (1992).
25. Schmid, S. L. Clathrin-coated vesicle formation and protein sorting: An integrated process. Annu. Rev. Biochem. 66, 511-548 (1997).
26. Orci, L. et al. Budding from Golgi membranes requires the coatomer complex of non-clathrin coat proteins. Nature 362, 648-652 (1993).
27. Barlowe, C. et al. COPII: A membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895-907 (1994).
28. Damke, H., Baba, T., Warnock, D. E. & Schmid, S. L. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J. Cell Biol. 127, 915-934 (1994).
29. Oh, P., McIntosh, D. P. & Schnitzer, J. E. Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J. Cell Biol. 141, 101-114 (1998).
30. Ostermann, J. et al. Stepwise assembly of functionally active transport vesicles. Cell 75, 1015-1025 (1993).
31. Rowe, T. et al. COPII vesicles derived from mammalian endoplasmic reticulum (ER) microsomes recruit COP1. J. Cell Biol. 135, 895-911 (1996).
32. 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, 1399-1402 (1998).
33. Achiriloaie, M., Barylko, B. & Albenesi, J. P. Essential role of the dynamin pleckstrin homology domain in receptor-mediated endocytosis. Mol. Cell Biol. 19, 1410-1415 (1999).
34. Lee, A., Frank, D. W., Marks, M. S. & Lemmon, M. A. Dominant-negative inhibition of receptor-mediated endocytosis by a dynamin-1 mutant with a defective pleckstrin homology domain. Curr. Biol. 9, 261-264 (1999).
35. Vallis, Y., Wigge, P., Marks, B., Evans, P. R. & McMahon, H. T. Importance of the pleckstrin homology domain of dynamin in clathrin-mediated endocytosis. Curr. Biol. 9, 257-260 (1999).
36. Carter, L. L., Redelmeier, T. E., Woolenweber, L. A. & Schmid, S. L. Multiple GTP-binding proteins participate in clathrin-coated vesicle-mediated endocytosis. J. Cell Biol. 120, 37-45 (1993).
37. Micheva, K. D., Kay, B. K. & McPherson, P. S. Synaptojanin forms two separate complexes in the nerve terminal. Interactions with endophilin and amphiphysin. J. Biol. Chem. 272, 27239-27245 (1997).
38. Wang, Z. & Moran, M. F. Requirement for the adapter protein GRB2 in EGF receptor endocytosis. Science 272, 1935-1939 (1996).
39. Sparks, A. B. et al. Distinct ligand preferences of Src homology 3 domains from Src, Yes, Abl, Cortactin, p53bp2, PLCg, Crk, and Grb2. Proc. Natl Acad. Sci. USA 93, 1540-1544 (1996).
40. Robinson, P. J. et al. Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals. Nature 365, 163-166 (1993).
41. Lamaze, C., Baba, T., Redelmeier, T. E. & Schmid, S. L. Recruitment of epidermal growth factor receptor and transferrin receptors into coated pits in vitro: differing biochemical requirements. Mol. Biol. Cell 3, 1181-1194 (1993).
42. Schmid, S. L. & Carter, L. L. ATP is required for receptor-mediated endocytosis in intact cells. J. Cell Biol. 111, 2307-2318 (1990).
43. Heuser, J. E. & Reese, T. S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315-344 (1973).
44. Estes, P. S. et al. Traffic of dynamin within individual Drosophila synaptic boutons relative to compartment specific markers. J. Neurosci. 16, 5443-5456 (1996).
45. Gaidarov, I., Santini, F., Warren, R. A. & Keen, J. H. Spatial control of coated pit dynamics in living cells. Nature Cell Biol. 1, 1-7 (1999).
46. Micheva, K. D., Ramjaun, A. R., Kay, B. K. & McPherson, P. S. SH3 domain-dependent interactions of endophilin with amphiphysin. FEBS Lett. 414, 308-312 (1997).
47. Warnock, D. E., Terlecky, L. J. & Schmid, S. L. Dynamin GTPase is stimulated by crosslinking through the C-terminal proline-rich domain. EMBO J. 14, 1322-1328 (1995).
48. Harlow, E. & Lane, D. Antibodies: A Laboratory Manual (Cold Spring Harbor Publications, Cold Spring Harbor, 1988).
49. Warnock, D. E., Baba, T. & Schmid, S. L. Ubiquitously expressed dynamin-II has a higher intrinsic GTPase activity and a greater propensity for self-assembly than neuronal dynamin-I. Mol. Biol. Cell 8, 2553-2562 (1997).
50. Muhlberg, A. B., Warnock, D. E. & Schmid, S. L. Domain structure and intramolecular regulation of dynamin GTPase. EMBO J. 16, 6676-6683 (1997).