Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor

EMBO Journal

Volumn 21, Issue 18, 2002, Pages 4915-4926

  Mishra, Sanjay K ^a   Keyel, Peter A ^a   Hawryluk, Matthew J ^a   Agostinelli, Nicole R ^a   Watkins, Simon C ^a   Traub, Linton M ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Cargo selection; Clathrin; Disabled 2; Phosphoinositide; Receptor mediated endocytosis

Indexed keywords

ADAPTOR PROTEIN; BETA ARRESTIN; CELL PROTEIN; CLATHRIN; DISABLED 2 PROTEIN; EPSIN; LOW DENSITY LIPOPROTEIN RECEPTOR; PHOSPHOTYROSINE; TRANSCRIPTION FACTOR AP 2; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; INTERNALIZATION; MOLECULAR RECOGNITION; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEIN COMPLEX 2; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CLATHRIN; COS CELLS; ENDOCYTOSIS; FLUORESCENT DYES; GENES, REPORTER; GENES, TUMOR SUPPRESSOR; HELA CELLS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NEUROPEPTIDES; PEPTIDES; PHOSPHATIDYLINOSITOLS; PROTEIN BINDING; PROTEINS; RECEPTORS, LDL; RECOMBINANT FUSION PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 0037119952     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdf487     Document Type: Article

References (66)

1. Ajioka, R.S. and Kaplan, J. (1987) Characterization of endocytic compartments using the horseradish peroxidase-diaminobenzidine density shift technique. J. Cell Biol., 104, 77-85.
2. Arneson, L.S., Kunz, J., Anderson, R.A. and Traub, L.M. (1999) Coupled inositide phosphorylation and phospholipase D activation initiates clathrin-coat assembly on lysosomes. J. Biol. Chem., 274, 17794-17805.
3. Bonifacino, J.S. and Dell'Angelica, E.C. (1999) Molecular bases for the recognition of tyrosine-based sorting signals. J. Cell Biol., 145, 923-926.
4. Brett, T.J., Traub, L.M. and Fremont, D.H. (2002) Accessory protein recruitment motifs in clathrin-mediated endocytosis. Structure, 10, 797-809.
5. Buss, F., Arden, S.D., Lindsay, M., Luzio, J.P. and Kendrick-Jones, J. (2001) Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis. EMBO J., 20, 3676-3684.
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. Chen, W.J., Goldstein, J.L. and Brown, M.S. (1990) NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem., 265, 3116-3123.
8. Cooper, J.A. and Howell, B.W. (1999) Lipoprotein receptors: signaling functions in the brain? Cell, 97, 671-674.
9. Cupers, P., Jadhav, A.P. and Kirchhausen, T. (1998) Assembly of clathrin coats disrupts the association between Eps15 and AP-2 adaptors. J. Biol. Chem., 273, 1847-1850.
10. deBeer, T., Hoofnagle, A.N., Enmon, J.L., Bowers, R.C., Yamabhai, M., Kay, B.K. and Overduin, M. (2000) Molecular mechanism of NPF recognition by EH domains. Nat. Struct. Biol., 7, 1018-1022.
11. Dell'Angelica, E.C. (2001) Clathrin-binding proteins: got a motif? Join the network! Trends Cell Biol., 11, 315-318.
12. Dho, S.E., French, M.B., Woods, S.A. and McGlade, C.J. (1999) Characterization of four mammalian numb protein isoforms. Identification of cytoplasmic and membrane-associated variants of the phosphotyrosine binding domain. J. Biol. Chem., 274, 33097-33104.
13. Drake, M.T. and Traub, L.M. (2001) Interaction of two structurallydistinct sequence types with the clathrin terminal domain β-propeller. J. Biol. Chem., 276, 28700-28709.
14. Drake, M.T., Downs, M.A. and Traub, L.M. (2000) Epsin binds to clathrin by associating directly with the clathrin-terminal domain: evidence for cooperative binding through two discrete sites. J. Biol. Chem., 275, 6479-6489.
15. 2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science, 291, 1051-1055.
16. Gaidarov, I. and Keen, J.H. (1999) Phosphoinositide-AP-2 interactions required for targeting to plasma membrane clathrin-coated pits. J. Cell Biol., 146, 755-764.
17. Garcia, C.K. et al. (2001) Autosomal recessive hypercholesterolemia caused by mutations in a putative LDL receptor adaptor protein. Science, 292, 1394-1398.
18. Gillooly, D.J., Morrow, I.C., Lindsay, M., Gould, R., Bryant, N.J., Gaullier, J.M., Parton, R.G. and Stenmark, H. (2000) Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J., 19, 4577-4588.
19. Goldstein, J.L. and Brown, M.S. (2001) Molecular. medicine. The cholesterol quartet. Science, 292, 1310-1312.
20. 2-adrenergic receptor. Nature, 383, 447-450.
21. Gotthardt, M., Trommsdorff, M., Nevitt, M.F., Shelton, J., Richardson, J.A., Stockinger, W., Nimpf, J. and Herz, J. (2000) Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction. J. Biol. Chem., 275, 25616-25624.
22. Herz, J. (2001) The LDL receptor gene family: (un)expected signal transducers in the brain. Neuron, 29, 571-581.
23. Hocevar, B.A., Smine, A., Xu, X.X. and Howe, P.H. (2001) The adaptor molecule Disabled-2 links the transforming growth factor β receptors to the Smad pathway. EMBO J., 20, 2789-2801.
24. Homayouni, R., Rice, D.S., Sheldon, M. and Curran, T. (1999) Disabled-1 binds to the cytoplasmic domain of amyloid precursor-like protein 1. J. Neurosci., 19, 7507-7515.
25. Howell, B.W., Lanier, L.M., Frank, R., Gertler, F.B. and Cooper, J.A. (1999) The disabled 1 phosphotyrosine-binding domain binds to the internalization signals of transmembrane glycoproteins and to phospholipids. Mol. Cell. Biol., 19, 5179-5188.
26. Inoue, A., Sato, O., Homma, K. and Ikebe, M. (2002) DOC-2/DAB2 is the binding partner of myosin VI. Biochem. Biophys. Res. Commun., 292, 300-307.
27. Itoh, T., Koshiba, S., Kigawa, T., Kikuchi, A., Yokoyama, S. and Takenawa, T. (2001) Role of the ENTH domain in phosphatidylinositol-4, 5-bisphosphate binding and endocytosis. Science, 291, 1047-1051.
28. Kalthoff, C., Alves, J., Urbanke, C., Knorr, R. and Ungewickell, E.J. (2002) Unusual structural organization of the endocytic proteins AP180 and epsin 1. J. Biol. Chem., 277, 8209-8216.
29. Laporte, S.A., Oakley, R.H., Zhang, J., Holt, J.A., Ferguson, S.S., Caron, M.G. and Barak, L.S. (1999) The β2-adrenergic receptor/β-arrestin complex recruits the clathrin adaptor AP-2 during endocytosis. Proc. Natl Acad. Sci. USA, 96, 3712-3717.
30. Laporte, S.A., Oakley, R.H., Holt, J.A., Barak, L.S. and Caron, M.G. (2000) The interaction of β-arrestin with the AP-2 adaptor is required for the clustering of β2-adrenergic receptor into clathrin-coated pits. J. Biol. Chem., 275, 23120-23126.
31. Lee, P.S., Wang, Y., Dominguez, M.G., Yeung, Y.G., Murphy, M.A., Bowtell, D.D. and Stanley, E.R. (1999) The Cb1 protooncoprotein stimulates CSF-1 receptor multiubiquitination and endocytosis and attenuates macrophage proliferation. EMBO J., 18, 3616-3628.
32. Leheste, J.R. et al. (1999) Megalin knockout mice as an animal model of low molecular weight proteinuria. Am. J. Pathol., 155, 1361-1370.
33. Li, Y., Lu, W., Marzolo, M.P. and Bu, G. (2001) Differential functions of members of the low density lipoprotein receptor family suggested by their distinct endocytosis rates. J. Biol. Chem., 276, 18000-18006.
34. Margolis, B. (1996) The PI/PTB domain: a new protein interaction domain involved in growth factor receptor signaling. J. Lab. Clin. Med., 128, 235-241.
35. Martina, J.A., Bonangelino, C.J., Aguilar, R.C. and Bonifacino, J.S. (2001) Stonin 2: an adaptor-like protein that interacts with components of the endocytic machinery. J. Cell Biol., 153, 1111-1120.
36. Miller, W.E. and Lefkowitz, R.J. (2001) Expanding roles for β-arrestins as scaffolds and adapters in GPCR signaling and trafficking. Curr. Opin. Cell Biol., 13, 139-145.
37. Mishra, S.K., Agostinelli, N.R., Brett, T.J., Mizukami, I., Ross, T.S. and Traub, L.M. (2001) Clathrin- and AP-2-binding sites in HIP1 uncover a general assembly role for endocytic accessory proteins. J. Biol. Chem., 276, 46230-46236.
38. Morris, S.M. and Cooper, J.A. (2001) Disabled-2 colocalizes with the LDLR in clathrin-coated pits and interacts with AP-2. Traffic, 2, 111-123.
39. Morris, S.M., Arden, S.D., Roberts, R.C., Kendrick-Jones, J., Cooper, J.A., Luzio, J.P. and Buss, F. (2002a) Myosin VI binds to and localises with Dab2, potentially linking receptor-mediated endocytosis and the actin cytoskeleton. Traffic, 3, 331-341.
40. Morris, S.M., Tallquist, M.D., Rock, C.O. and Cooper, J.A. (2002b) Dual roles for the Dab2 adaptor protein in embryonic development and kidney transport. EMBO J., 21, 1555-1564.
41. Nesterov, A., Carter, R.E., Sorkina, T., Gill, G.N. and Sorkin, A. (1999) Inhibition of the receptor-binding function of clathrin adaptor protein AP-2 by dominant-negative mutant μ2 subunit and its effects on endocytosis. EMBO J., 18, 2489-2499.
42. Nonet, M.L. et al. (1999) UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol. Biol. Cell, 10, 2343-2360.
43. Norman, D., Sun, X.M., Bourbon, M., Knight, B.L., Naoumova, R.P. and Soutar, A.K. (1999) Characterization of a novel cellular defect in patients with phenotypic homozygous familial hypercholesterolemia. J. Clin. Invest., 104, 619-628.
44. Ohno, H., J., S., Fournier, M.-C., Bosshart, H., Rhee, I., Miyatake, S., Saito, T., Galluser, A., Kirchhausen, T. and Bonifacino, J.S. (1995) Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science, 269, 1872-1875.
45. Oleinikov, A.V., Zhao, J. and Makker, S.P. (2000) Cytosolic adaptor protein Dab2 is an intracellular ligand of endocytic receptor gp600/megalin. Biochem. J., 347 Pt 3, 613-621.
46. Owen, D.J. and Evans, P.R. (1998) A structural explanation for the recognition of tyrosine-based endocytotic signals. Science, 282, 1327-1332.
47. Penheiter, S.G., Mitchell, H., Garamszegi, N., Edens, M., Dore, J.J., Jr and Leof, E.B. (2002) Internalization-dependent and -independent requirements for transforming growth factor β receptor signaling via the Smad pathway. Mol. Cell. Biol., 22, 4750-4759.
48. Polo, S., Sigismund, S., Faretta, M., Guidi, M., Capua, M.R., Bossi, G., Chen, H., De Camilli, P. and Di Fiore, P.P. (2002) A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature, 416, 451-455.
49. Ramjaun, A.R. and McPherson, P.S. (1998) Multiple amphiphysin II splice variants display differential clathrin binding: identification of two distinct clathrin-binding sites. J. Neurochem., 70, 2369-2376.
50. Ravichandran, K.S., Zhou, M.M., Pratt, J.C., Harlan, J.E., Walk, S.F., Fesik, S.W. and Burakoff, S.J. (1997) Evidence for a requirement for both phospholipid and phosphotyrosine binding via the Shc phosphotyrosine-binding domain in vivo. Mol. Cell. Biol., 17, 5540-5549.
51. Santini, F., Gaidarov, I. and Keen, J.H. (2002) G protein-coupled receptor/arrestin3 modulation of the endocytic machinery. J. Cell Biol., 156, 665-676.
52. Santolini, E., Salcini, A.E., Kay, B.K., Yamabhai, M. and Di Fiore, P.P. (1999) The EH network. Exp. Cell Res., 253, 186-209.
53. Santolini, E., Puri, C., Salcini, A.E., Gagliani, M.C., Pelicci, P.G., Tacchetti, C. and Di Fiore, P.P. (2000) Numb is an endocytic protein. J. Cell Biol., 151, 1345-1352.
54. Scott, M.G., Benmerah, A., Muntaner, O. and Marullo, S. (2002) Recruitment of activated G protein-coupled receptors to pre-existing clathrin-coated pits in living cells. J. Biol. Chem., 277, 3552-3559.
55. Sheng, Z., Sun, W., Smith, E., Cohen, C. and Xu, X.X. (2000) Restoration of positioning control following Disabled-2 expression in ovarian and breast tumor cells. Oncogene, 19, 4847-4854.
56. Slepnev, V.I., Ochoa, G.C., Butler, M.H. and De Camilli, P. (2000) Tandem arrangement of the clathrin and AP-2 binding domains in amphiphysin 1 and disruption of clathrin coat function mediated by amphiphysin fragments comprising these sites. J. Biol. Chem., 275, 17583-17589.
57. Su, H.P., Nakada-Tsukui, K., Tosello-Trampont, A.C., Li, Y., Bu, G., Henson, P.M. and Ravichandran, K.S. (2002) Interaction of CED-6/GULP, an adapter protein involved in engulfment of apoptotic cells, with CED-1 and CD91/LRP. J. Biol. Chem., 277, 11772-11779.
58. Takeuchi, H., Matsuda, M., Yamamoto, T., Kanematsu, T., Kikkawa, U., Yagisawa, H., Watanabe, Y. and Hirata, M. (1998) PTB domain of insulin receptor substrate-1 binds inositol compounds. Biochem. J., 334, 211-218.
59. Trommsdorff, M., Borg, J.P., Margolis, B. and Herz, J. (1998) Interaction of cytosolic adaptor proteins with neuronal apolipoprotein E receptors and the amyloid precursor protein. J. Biol. Chem., 273, 33556-33560.
60. Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., Hammer, R.E., Richardson, J.A. and Herz, J. (1999) Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell, 97, 689-701.
61. Velier, J., Kim, M., Schwarz, C., Kim, T.W., Sapp, E., Chase, K., Aronin, N. and DiFiglia, M. (1998) Wild-type and mutant huntingtins function in vesicle trafficking in the secretory and endocytic pathways. Exp. Neurol., 152, 34-40.
62. Wanker, E.E., Rovira, C., Scherzinger, E., Hasenbank, R., Walter, S., Tait, D., Colicelli, J. and Lehrach, H. (1997) HIP-I: a huntingtin interacting protein isolated by the yeast two-hybrid system. Hum. Mol. Genet., 6, 487-495.
63. Warren, R.A., Green, F.A., Stenberg, P.E. and Enns, C.A. (1998) Distinct saturable pathways for the endocytosis of different tyrosine motifs. J. Biol. Chem., 273, 17056-17063.
64. Xu, X.X., Yang, W., Jackowski, S. and Rock, C.O. (1995) Cloning of a novel phosphoprotein regulated by colony-stimulating factor 1 shares a domain with the Drosophila disabled gene product. J. Biol. Chem., 270, 14184-14191.
65. 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.
66. Zhu, Y., Drake, M.T. and Kornfeld, S. (1999) ADP-ribosylation factor 1 dependent clathrin-coat assembly on synthetic liposomes. Proc. Natl Acad. Sci. USA, 96, 5013-5018.