Metastasis suppressor tetraspanin CD82/KAI1 regulates ubiquitylation of epidermal growth factor receptor

Journal of Biological Chemistry

Volumn 288, Issue 36, 2013, Pages 26323-26334

  Odintsova, Elena ^a   Van Niel, Guillaume ^b   Conjeaud, Hélène ^c   Raposo, Graça ^b   Iwamoto, Ryo ^d   Mekada, Eisuke ^d   Berditchevski, Fedor ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DIDEROT   (France)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

SULFUR COMPOUNDS;

EPIDERMAL GROWTH FACTOR RECEPTORS; HEPARAN SULFATE PROTEOGLYCANS; HEPARIN BINDING; RECEPTOR TRAFFICKING; TETRASPANIN CD82; UBIQUITYLATION;

LIGANDS;

AMPHIREGULIN; CBL PROTEIN; CD82 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN KINASE C; SERINE; THREONINE; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL STIMULATION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME REGULATION; GENE DELETION; HUMAN; HUMAN CELL; LIGAND BINDING; METASTASIS INHIBITION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RECEPTOR UPREGULATION; REGULATORY MECHANISM; UBIQUITINATION;

EID: 84883733829     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.439380     Document Type: Article

References (45)

1. Berditchevski, F. (2001) Complexes of tetraspanins with integrins. More than meets the eye. J. Cell Sci. 114, 4143-4151
2. Hemler, M. (2003) Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu. Rev. Cell Dev. Biol. 19, 397-422
3. Charrin, S., le Naour, F., Silvie, O., Milhiet, P.-E., Boucheix, C., and Rubinstein, E. (2009) Lateral organisation of membrane proteins. tetraspanins spin their web. Biochem. J. 420, 133-154
4. Berditchevski, F., and Odintsova, E. (2007) Tetraspanins as regulators of protein trafficking. Traffic 8, 89-96
5. Odintsova, E., Sugiura, T., and Berditchevski, F. (2000) Attenuation of EGF receptor signaling by a metastasis suppressor, the tetraspanin CD82/ KAI-1. Curr. Biol. 10, 1009-1012
6. Odintsova, E., Butters, T. D., Monti, E., Sprong, H., van Meer, G., and Berditchevski, F. (2006) Gangliosides play an important role in the organization of CD82-enriched microdomains. Biochem. J. 400, 315-325
7. He, B., Liu, L., Cook, G. A., Grgurevich, S., Jennings, L. K., and Zhang, X. A. (2005) Tetraspanin CD82 attenuates cellular morphogenesis through down-regulating integrin alpha6-mediated cell adhesion. J. Biol. Chem. 280, 3346-3354
8. Sridhar, S. C., and Miranti, C. K. (2006) Tetraspanin KAI1/CD82 suppresses invasion by inhibiting integrin-dependent crosstalk with c-Met receptor and Src kinases. Oncogene 25, 2367-2378
9. Takahashi, M., Sugiura, T., Abe, M., Ishii, K., and Shirasuna, K. (2007) Regulation of c-Met signaling by the tetraspanin KAI-1/CD82 affects cancer cell migration. Int. J. Cancer 121, 1919-1929
10. Miranti, C. K. (2009) Controlling cell surface dynamics and signalling. How CD82 suppresses metastasis. Cell. Signal. 21, 196-211
11. Tsai, Y. C., and Weissman, A. M. (2011) Dissecting the diverse functions of the metastasis suppressor CD82/KAI1. FEBS Lett. 585, 3166-3173
12. Danglot, L., Chaineau, M., Dahan, M., Gendron, M. C., Boggetto, N., Perez, F., and Galli, T. (2010) Role of TI-VAMP and CD82 in EGFR cellsurface dynamics and signaling. J. Cell Sci. 123, 723-735
13. Escola, J. M., Kleijmeer, M. J., Stoorvogel, W., Griffith, J. M., Yoshie, O., and Geuze, H. J. (1998) Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J. Biol. Chem. 273, 20121-20127
14. Vyas, J. M., Kim, Y.-M., Artavanis-Tsakonas, K., Love, J. C., Van der Veen, A. G., and Ploegh, H. L. (2007) Tubulation of class IIMHCcompartments is microtubule dependent and involves multiple endolysosomal membrane proteins in primary dendritic cells. J. Immunol. 178, 7199-7210
15. Xu, C., Zhang, Y. H., Thangavel, M., Richardson, M. M., Liu, L., Zhou, B., Zheng, Y., Ostrom, R. S., and Zhang, X. A. (2009) CD82 endocytosis and cholesterol-dependent reorganization of tetraspanin webs and lipid rafts. FASEB J. 23, 3237-3288
16. Sigismund, S., Confalonieri, S., Ciliberto, A., Polo, S., Scita, G., and Di Fiore, P. P. (2012) Endocytosis and signaling. Cell logistics shape the eukaryotic cell plan. Physiol. Rev. 92, 273-366
17. Sorkin, A., and Goh, L. K. (2009) Endocytosis and intracellular trafficking of ErbBs. Exp. Cell Res. 315, 683-696
18. Shearer, M., Bartkova, J., Bartek, J., Berdichevsky, F., Barnes, D., Millis, R., and Taylor-Papadimitriou, J. (1992) Studies of clonal cell lines developed from primary breast cancers indicate that the ability to undergo morphogenesis in vitro is lost early in malignancy. Int. J. Cancer 51, 602-612
19. Berditchevski, F., Odintsova, E., Sawada, S., and Gilbert, E. (2002) Expression of the palmitoylation-deficient CD151 weakens the association of 31 integrin with the tetraspanin-enriched microdomains and affects integrin-dependent signaling. J. Biol. Chem. 277, 36991-37000
20. Iwamoto, R., Mine, N., Kawaguchi, T., Minami, S., Saeki, K., and Mekada, E. (2010) HB-EGF function in cardiac valve development requires interaction with heparan sulfate proteoglycans. Development 137, 2205-2214
21. Takazaki, R., Shishido, Y., Iwamoto, R., and Mekada, E. (2004) Suppression of the biological activities of the epidermal growth factor (EGF)-like domain by the heparin-binding domain of heparin-binding EGF-like growth factor. J. Biol. Chem. 279, 47335-47343
22. Berditchevski, F., and Odintsova, E. (1999) Characterization of integrintetraspanin adhesion complexes. Role of tetraspanins in integrin signaling. J. Cell Biol. 146, 477-492
23. Bolte, S., and Cordelières, F. P. (2006) A guided tour into subcellular colocalisation analysis in light microscopy. J. Microsc. 224, 213-232
24. Kleijmeer, M. J., Raposo, G., and Geuze, H. J. (1996) Characterization of MHC class II compartments by immunoelectron microscopy. Methods 10, 191-207
25. Liou, W., Geuze, H. J., and Slot, J. W. (1996) Improving structural integrity of cryosections for immunogold labeling. Histochem. Cell Biol. 106, 41-58
26. Roepstorff, K., Grandal, M. V., Henriksen, L., Knudsen, S. L., Lerdrup, M., Grøvdal, L., Willumsen, B. M., and van Deurs, B. (2009) Differential effects of EGFR ligands on endocytic sorting of the receptor. Traffic 10, 1115-1127
27. Baldys, A., Göoz, M., Morinelli, T. A., Lee, M.-H., Raymond, J. R. Jr., Luttrell, L. M., and Raymond, J. R., Sr. (2009) Essential role of c-Cbl in amphiregulin-induced recycling and signaling of the endogenous epidermal growth factor receptor. Biochemistry 48, 1462-1473
28. Roepstorff, K., Grøvdal, L., Grandal, M., Lerdrup, M., and van Deurs, B. (2008) Endocytic downregulation of ErbB receptors. Mechanisms and relevance in cancer. Histochem. Cell Biol. 129, 563-578
29. Swaminathan, G., and Tsygankov, A. Y. (2006) The Cbl family proteins. Ring leaders in regulation of cell signalling. J. Cell. Physiol. 209, 21-43
30. Pedraza-Alva, G., Sawasdikosol, S., Liu, Y. C., Mérida, L. B., Cruz-Muñoz, M. E., Oceguera-Yañez, F., Burakoff, S. J., and Rosenstein, Y. (2001) Regulation of Cbl molecular interactions by the co-receptor molecule CD43 in human T cells. J. Biol. Chem. 276, 729-737
31. Melander, F., Andersson, T., and Dib, K. (2004) Engagement of 2 integrins recruits 14-3-3 proteins to c-Cbl in human neutrofils. Biochem. Biophys. Res. Commun. 317, 1000-1005
32. Zhang, X. A., Bontrager, A. L., and Hemler, M. E. (2001) Transmembrane- 4 superfamily proteins associate with activated protein kinase C (PKC) and link PKC to specific 1 integrins. J. Biol. Chem. 276, 25005-25013
33. Bao, J., Alroy, I., Waterman, H., Schejter, E. D., Brodie, C., Gruenberg, J., and Yarden, Y. (2000) Threonine phosphorylation diverts internalised epidermal growth factor receptors from a degradative pathway to the recycling endosome. J. Biol. Chem. 275, 26178-26186
34. Cotton, C. U., Hobert, M. E., Ryan, S., and Carlin, C. R. (2013) Basolateral EGF receptor sorting regulated by functionally distinct mechanisms in renal epithelial cells. Traffic 14, 337-354
35. Stern, K. A., Place, T. L., and Lill, N. L. (2008) EGF and amphiregulin differentially regulate Cbl recruitment to endosomes and EGF receptor fate. Biochem. J 410, 585-594
36. Forsten-Williams, K., Chu, C. L., Fannon, M., Buczek-Thomas, J. A., and Nugent, M. A. (2008) Control of growth factor networks by heparan sulfate proteoglycans. Ann. Biomed. Eng. 36, 2134-2148
37. Gitay-Goren, H., Soker, S., Vlodavsky, I., and Neufeld, G. (1992) The binding of vascular endothelial growth factor to its receptors is dependent on cell-surface-associated heparin-like molecules. J. Biol. Chem. 267, 6093-6098
38. Higashiyama, S., Abraham, J. A., and Klagsbrun, M. (1993) Heparin-binding EGF-like growth factor stimulation of smooth muscle cell migration. Dependence on interactions with cell surface heparan sulfate. J. Cell Biol. 122, 933-940
39. Mahtouk, K., Cremer, F. W., Rème, T., Jourdan, M., Baudard, M., Moreaux, J., Requirand, G.,Fiol, G., De Vos, J., Moos, M., Quittet, P., Goldschmidt, H., Rossi, J. F., Hose, D., and Klein, B. (2006) Heparan sulfate proteoglycans are essential for the myeloma cell growth activity of EGFfamily ligands in multiple myeloma. Oncogene 25, 7180-7191
40. Couchman, J. R. (2010) Transmembrane signalling. Proteoglycans. Annu. Rev. Cell Dev. Biol. 26, 89-114
41. Keum, E., Kim, Y., Kim, J., Kwon, S., Lim, Y., Han, I., and Oh, E.-S. (2004) Syndecan-4 regulates localization, activity and stability of protein kinase C. Biochem. J. 378, 1007-1014
42. Fan, T.-C., Chang, H.-T., Chen, I-W., Wang, H.-Y., and Chang, M. D.-T. (2007) A heparan sulfate-facilitated and raft-dependent macropinocytosis of eosinophil cationic protein. Traffic 8, 1778-1795
43. Tkachenko, E., Lutgens, E., Stan, R.-V., and Simons, M. (2004) Fibroblast growth factor 2 endocytosis in endothelial cells proceed via syndecan-4- dpendent macropinocytic pathway. J. Cell Sci. 117, 3189-3199
44. Lambaerts, K., Wilcox-Adelman, S. A., and Zimmermann, P. (2009) The signalling mechanisms of syndecan heparan sulfate proteoglycans. Curr. Opin. Cell Biol. 21, 662-669
45. Clague, M. J., Liu, H., and Urbé, S. (2012) Governance of endocytic trafficking and signaling by reversible ubiquitylation. Dev. Cell 23, 457-467