The EH and SH3 domain Ese proteins regulate endocytosis by linking to dynamin and Eps15

EMBO Journal

Volumn 18, Issue 5, 1999, Pages 1159-1171

  Sengar, Ameet S ^a,b   Wang, Wei ^a   Bishay, Joseph ^a   Cohen, Samuel ^a   Egan, Sean E ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

EH domains; Endocytosis; Eps15; Ese; SH3 domains

Indexed keywords

ADAPTOR PROTEIN; CLATHRIN; DYNAMIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENDOCYTOSIS; GENETIC CONSERVATION; MAMMAL; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; YEAST;

MAMMALIA;

EID: 0033106167     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.5.1159     Document Type: Article

References (54)

1. Benedetti, H., Raths, S., Crausaz, F. and Riezman, H. (1994) The END3 gene encodes a protein that is required for the internalization step of endocytosis and for actin cytoskeleton organization in yeast. Mol. Biol. Cell, 5, 1023-1037.
2. Benmerah, A., Gagnon, J., Begue, B., Megarbane, B., Dautry-Varsat, A. and Cerf-Bensussan, N. (1995) The tyrosine kinase substrate EPS15 is constitutively associated with the plasma membrane adaptor AP2. J. Cell Biol., 131, 1831-1838.
3. Benmerah, A., Begue, B., Dautry-Vasat, A. and Cerf-Bensussan, N. (1996) The Ear of α-adaptin interacts with the COOH-terminal domain of the EPS15 protein. J. Biol. Chem., 271, 12111-12116.
4. Benmerah, A., Lamaze, C., Begue, B., Schmid, S.L., Dautry-Varsat, A. and Cerf-Bensussan, N. (1998) AP-2/Eps15 interaction is required for receptor-mediated endocytosis. J. Cell Biol., 140, 1055-1062.
5. Carbone, R., Fre, S., Iannolo, G., Belleudi, F.P.M., Pelicci, P.G., Torrisi, M.R. and Di Fiore, P.P. (1997) Eps15 and eps15R are essential components of the endocytic pathway. Cancer Res., 57, 5498-5504.
6. Chen, H., Fre, S., Slepnev, V.I., Capua, M.R., Takei, K., Butler, M.H., Di Fiore, P.P. and De Camilli, P. (1998) Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature, 394, 793-797.
7. Coda, L., Salcini, A.E., Confalonieri, S., Pelicci, G., Sorkina, T., Sorkin, A., Pelicci, P.G. and Di Fiore, P.P. (1998) Eps15R is a tyrosine kinase substrate with characteristics of a docking protein possibly involved in coated pits-mediated internalization. J. Biol. Chem., 273, 3003-3012.
8. Cupers, P., ter Haar, E., Boll, W. and Kirchhausen, T. (1997) Parallel dimers and anti-parallel tetramers formed by epidermal growth factor receptor pathway substrate clone 15 (Eps15). J. Biol. Chem., 272, 33430-33434.
9. De Camilli, P., Emr, S.D., McPherson, P.S. and Novick, P. (1996) Phosphoinositides as regulators in membrane traffic. Science, 271, 1533-1539.
10. 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 the brain. J. Biol. Chem., 272, 8710-8716.
11. Di Fiore, P.P., Pelicci, P.G. and Sorkin, A. (1997) EH: a novel protein-protein interaction domain potentially involved in intracellular sorting. Trends Biochem. Sci., 22, 411-413.
12. Fazioli, F., Minichiello, L., Matoskova, B., Wong, W.T. and Di Fiore, P.P. (1993) Eps15, a novel tyrosine kinase substrate, exhibits transforming activity. Mol. Cell. Biol., 13, 5814-5828.
13. Gout, I. et al. (1993) The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell, 75, 25-36.
14. Guipponi, M., Scott, H.S., Chen, H., Schebesta, A., Rossier, C. and Antonarakis, S.E. (1998) Two isoforms of a human intersectin (ITSN) protein are produced by brain-specific alternative splicing of a stop codon. Genomics, 53, 369-376.
15. Haffner, C., Takei, K., Chen, H., Ringstad, N., Hudson, A., Butler, M.H., Salcini, A.E., Di Fiore, P.P. and De Camilli, P. (1997) Synaptojanin I: localization on coated endocytic intermediates in nerve terminals and interaction of its 170 kDa isoform with Eps15. FEBS Lett., 419, 175-180.
16. Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science, 279, 509-514.
17. Iannolo, G., Salcini, A.E., Gaidarov, I., Goodman, O.B.J., Baulida, J., Carpenter, G., Pelicci, P.G., Di Fiore, P.P. and Keen, J.H. (1997) Mapping of the molecular determinants involved in the interaction between Eps15 and AP2. Cancer Res., 57, 240-245.
18. McNiven, M.A. (1998) Dynamin: a molecular motor with pinchase action. Cell, 94, 151-154.
19. McPherson, P.S. et al. (1996) A presynaptic inositol-5-phosphatase. Nature, 379, 353-357.
20. McPherson, P.S., de Heuvel, E., Phillie, J., Wang, W., Sengar, A. and Egan, S. (1998) EH domain-dependent interactions between Eps15 and clathrin-coated vesicle protein p95. Biochem. Biophys. Res. Commun., 244, 701-705.
21. Munn, A.L., Stevenson, B.J., Geli, M.I. and Riezman, H. (1995) end5, end6 and end7: mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol. Biol. Cell, 6, 1721-1742.
22. Nalefski, E.A. and Falke, J.J. (1996) The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci., 5, 2375-2390.
23. Raths, S., Rohrer, J., Crausaz, F. and Riezman, H. (1993) end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae. J. Cell Biol., 120, 55-65.
24. Ren, R., Mayer, B.J., Cicchetti, P. and Baltimore, D. (1993) Identification of a ten-amino acid proline-rich SH3 binding site. Science, 259, 1157-1161.
25. Riezman, H., Woodman, P.G., van Meer, G. and Marsh, M. (1997) Molecular mechanisms of endocytosis. Cell, 91, 731-738.
26. 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.
27. Robinson, M.S. (1997) Coats and budding vesicles. Trends Cell Biol., 7, 99-102.
28. Roos, J. and Kelly, R.B. (1998) Dap 160, a neural-specific Eps15 homology and multiple SH3 domain-containing protein that interacts with Drosophila dynamin. J. Biol. Chem., 273, 19108-19119.
29. Salcini, A.E., Confalonieri, S., Doria, M., Santolini, E., Tassi, E., Minencova, O., Cesareni, G., Pelicci, P.G. and Di Fiore, P.P. (1997) Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module. Genes Dev., 11, 2239-2249.
30. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Schmid, S.L. (1997) Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem., 66, 511-548.
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. Schumacher, C., Knudsen, B.S., Ohuchi, T., Di Fiore, P.P., Glassman, R.H. and Hanafusa, H. (1995) The SH3 domain of Crk binds specifically to a conserved proline-rich motif in Eps15 and Eps15R. J. Biol. Chem., 270, 15341-15347.
34. Shupliakov, O., Low, 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.
35. Sparks, A.B., Hoffman, N.G., McConnel, S.J., Fowlkes, D.M. and Kay, B.K. (1996) Cloning of ligand targets: sytematic isolation of SH3 domain-containing proteins. Nature Biotechnol., 14, 741-744.
36. Stenmark, H., Bucci, C. and Zerial, M. (1995) Expression of Rab GTPases using recombinant vaccinia virus. Methods Enzymol., 257, 155-164.
37. Stukenberg, P.T., Lustig, K.D., McGarry, T.J., King, R.W., Kuang, J. and Kirschner, M.W. (1997) Systematic identification of mitotic phosphoproteins. Curr. Biol., 7, 338-348.
38. Sweitzer, S.M. and Hinshaw, J.E. (1998) Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell, 93, 1021-1029.
39. Takei, K., Haucke, V., Slepnev, V., Farsad, K., Salazar, M., Chen, H. and De Camilli, P. (1998) Generation of coated intermediates of clathrin-mediated endocytosis on protein-free liposomes. Cell, 94, 131-141.
40. Tang, H.-Y. and Cai, M. (1996) The EH-domain-containing protein Pan1 is required for normal organization of the actin cytoskeleton in Saccharomyces cerevisiae. Mol. Cell. Biol., 16, 4897-4914.
41. Tang, H.Y., Munn, A. and Cai, M. (1997) EH domain proteins Pan1p and End3p are components of a complex that plays a dual role in organization of the cortical actin cytoskeleton and endocytosis in Saccharomyces cerevisiae. Mol. Cell. Biol., 17, 4294-4304.
42. Tebar, F., Sorkina, T., Sorkin, A., Ericsson, M. and Kirchausen, T. (1996) Eps15 is a component of clathrin-coated pits and vesicles and is located at the rim of coated pits. J. Biol. Chem., 271, 28727-28730.
43. Tebar, F., Confalonieri, S., Carter, R.E., Di Fiore, P.P. and Sorkin, A. (1997) Eps15 is constitutively oligomerized due to homophilic interaction of its coiled-coil domain. J. Biol. Chem., 272, 15413-15418.
44. Urrutia, R., Henley, J.R., Cook, T. and McNiven, M.A. (1997) The dynamins: redundant or distinct functions for an expanding family of related GTPases? Proc. Natl Acad. Sci. USA, 94, 377-384.
45. Wang, Z. and Moran, M.F. (1996) Requirement for the adapter protein Grb2 in EGF receptor endocytosis. Science, 272, 1935-1939.
46. Warnock, D.E. and Schmid, S.L. (1996) Dynamin GTPase, a force-generating molecular switch. BioEssays, 18, 885-893.
47. Wendland, B. and Emr, S.D. (1998) Pan1p, yeast eps15, functions as a multivalent adaptor that coordinates protein-protein interactions essential for endocytosis. J. Cell Biol., 141, 71-84.
48. Wendland, B., McCaffery, J.M., Xiao, Q. and Emr, S.D. (1996) A novel fluorescence-activated cell sorter-based screen for yeast endocytosis mutants identifies a yeast homologue of mammalian eps15. J. Cell Biol., 135, 1485-1500.
49. Wendland, B., Emr, S.D. and Riezman, H. (1998) Protein traffic in the yeast endocytic and vacuolar protein sorting pathways. Curr. Opin. Cell Biol., 10, 513-522.
50. Wesp, A., Hicke, L., Palecek, J., Lombardi, R., Aust, T., Munn, A.L. and Riezman, H. (1997) End4p/Sla2p interacts with actin-associated proteins for endocytosis in Saccharomyces cerevisiae. Mol. Biol. Cell, 8, 2291-2306.
51. Wigge, P., Kohler, K., Vallis, Y., Doyle, C.A., Owen, D., Hunt, S.P. and McMahon, H.T. (1997a) Amphiphysin heterodimers: potential role in clathrin-mediated endocytosis. Mol. Biol. Cell, 8, 2003-2015.
52. Wigge, P., Vallis, Y. and McMahon, H.T. (1997b) Inhibition of receptor-mediated endocytosis by the amphiphysin SH3 domain. Curr. Biol., 7, 554-560.
53. Wong, W.T., Schumacher, C., Salcini, A.E., Romano, A., Castagnino, P., Pelicci, P.G. and Di Fiore, P.P. (1995) A protein-binding domain, EH, identified in the receptor tyrosine kinase substrate EPS15 and conserved in evolution. Proc. Natl Acad. Sci. USA, 92, 9530-9534.
54. Yamabhai, M., Hoffman, N.G., Hardison, N.L., McPherson, P.S., Castagnoli, L., Cesareni, G. and Kay, B.K. (1998) Intersectin, a novel adaptor protein with two eps15 homology and five src homology 3 domains. J. Biol. Chem., 273, 31401-31407.