Clathrin-Mediated Internalization Is Essential for Sustained EGFR Signaling but Dispensable for Degradation

Developmental Cell

Volumn 15, Issue 2, 2008, Pages 209-219

  Sigismund, Sara ^a   Argenzio, Elisabetta ^a   Tosoni, Daniela ^a   Cavallaro, Elena ^a   Polo, Simona ^a,b   Di Fiore, Pier Paolo ^a,b,c  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

Author keywords

CELLBIO; SIGNALING

Indexed keywords

CLATHRIN; EPIDERMAL GROWTH FACTOR RECEPTOR;

ARTICLE; CELL SURFACE; CONTROLLED STUDY; DNA SYNTHESIS; ENDOCYTOSIS; HUMAN; HUMAN CELL; INTERNALIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEIN COMPLEX 2; ANIMALS; CLATHRIN; DOWN-REGULATION; ENDOCYTOSIS; EPIDERMAL GROWTH FACTOR; FILIPIN; HELA CELLS; HUMANS; INTRACELLULAR SPACE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 48549088895     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2008.06.012     Document Type: Article

References (38)

1. Di Fiore P.P., Pierce J.H., Fleming T.P., Hazan R., Ullrich A., King C.R., Schlessinger J., and Aaronson S.A. Overexpression of the human EGF receptor confers an EGF-dependent transformed phenotype to NIH 3T3 cells. Cell 51 (1987) 1063-1070
2. Di Guglielmo G.M., Le Roy C., Goodfellow A.F., and Wrana J.L. Distinct endocytic pathways regulate TGF-β receptor signalling and turnover. Nat. Cell Biol. 5 (2003) 410-421
3. Emery G., and Knoblich J.A. Endosome dynamics during development. Curr. Opin. Cell Biol. 18 (2006) 407-415
4. Haglund K., Sigismund S., Polo S., Szymkiewicz I., Di Fiore P.P., and Dikic I. Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat. Cell Biol. 5 (2003) 461-466
5. Huang F., Khvorova A., Marshall W., and Sorkin A. Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. J. Biol. Chem. 279 (2004) 16657-16661
6. Jekely G., Sung H.H., Luque C.M., and Rorth P. Regulators of endocytosis maintain localized receptor tyrosine kinase signaling in guided migration. Dev. Cell 9 (2005) 197-207
7. Kaksonen M., Toret C.P., and Drubin D.G. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 7 (2006) 404-414
8. Kazazic M., Roepstorff K., Johannessen L.E., Pedersen N.M., van Deurs B., Stang E., and Madshus I.H. EGF-induced activation of the EGF receptor does not trigger mobilization of caveolae. Traffic 7 (2006) 1518-1527
9. Kornilova E., Sorkina T., Beguinot L., and Sorkin A. Lysosomal targeting of epidermal growth factor receptors via a kinase-dependent pathway is mediated by the receptor carboxyl-terminal residues 1022-1123. J. Biol. Chem. 271 (1996) 30340-30346
10. Lakadamyali M., Rust M.J., and Zhuang X. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124 (2006) 997-1009
11. Levkowitz G., Waterman H., Ettenberg S.A., Katz M., Tsygankov A.Y., Alroy I., Lavi S., Iwai K., Reiss Y., Ciechanover A., et al. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol. Cell 4 (1999) 1029-1040
12. Maldonado-Baez L., and Wendland B. Endocytic adaptors: recruiters, coordinators and regulators. Trends Cell Biol. 16 (2006) 505-513
13. Marco E., Wedlich-Soldner R., Li R., Altschuler S.J., and Wu L.F. Endocytosis optimizes the dynamic localization of membrane proteins that regulate cortical polarity. Cell 129 (2007) 411-422
14. Mayor S., and Pagano R.E. Pathways of clathrin-independent endocytosis. Nat. Rev. Mol. Cell Biol. 8 (2007) 603-612
15. Mills I.G. The interplay between clathrin-coated vesicles and cell signalling. Semin. Cell Dev. Biol. 18 (2007) 459-470
16. Mor A., and Philips M.R. Compartmentalized Ras/MAPK signaling. Annu. Rev. Immunol. 24 (2006) 771-800
17. Motley A., Bright N.A., Seaman M.N., and Robinson M.S. Clathrin-mediated endocytosis in AP-2-depleted cells. J. Cell Biol. 162 (2003) 909-918
18. Mukhopadhyay D., and Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315 (2007) 201-205
19. Neumann B., Held M., Liebel U., Erfle H., Rogers P., Pepperkok R., and Ellenberg J. High-throughput RNAi screening by time-lapse imaging of live human cells. Nat. Methods 3 (2006) 385-390
20. Newmyer S.L., and Schmid S.L. Dominant-interfering Hsc70 mutants disrupt multiple stages of the clathrin-coated vesicle cycle in vivo. J. Cell Biol. 152 (2001) 607-620
21. Orth J.D., Krueger E.W., Weller S.G., and McNiven M.A. A novel endocytic mechanism of epidermal growth factor receptor sequestration and internalization. Cancer Res. 66 (2006) 3603-3610
22. Parton R.G., and Simons K. The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8 (2007) 185-194
23. Penengo L., Mapelli M., Murachelli A.G., Confalonieri S., Magri L., Musacchio A., Di Fiore P.P., Polo S., and Schneider T.R. Crystal structure of the ubiquitin binding domains of rabex-5 reveals two modes of interaction with ubiquitin. Cell 124 (2006) 1183-1195
24. Pruss R.M., and Herschman H.R. Variants of 3T3 cells lacking mitogenic response to epidermal growth factor. Proc. Natl. Acad. Sci. USA 74 (1977) 3918-3921
25. Puthenveedu M.A., and von Zastrow M. Cargo regulates clathrin-coated pit dynamics. Cell 127 (2006) 113-124
26. Raiborg C., Bache K.G., Gillooly D.J., Madshus I.H., Stang E., and Stenmark H. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat. Cell Biol. 4 (2002) 394-398
27. Sigismund S., Woelk T., Puri C., Maspero E., Tacchetti C., Transidico P., Di Fiore P.P., and Polo S. Clathrin-independent endocytosis of ubiquitinated cargos. Proc. Natl. Acad. Sci. USA 102 (2005) 2760-2765
28. Soldati T., and Schliwa M. Powering membrane traffic in endocytosis and recycling. Nat. Rev. Mol. Cell Biol. 7 (2006) 897-908
29. Sorkin A. Cargo recognition during clathrin-mediated endocytosis: a team effort. Curr. Opin. Cell Biol. 16 (2004) 392-399
30. Sorkin A., Krolenko S., Kudrjavtceva N., Lazebnik J., Teslenko L., Soderquist A.M., and Nikolsky N. Recycling of epidermal growth factor-receptor complexes in A431 cells: identification of dual pathways. J. Cell Biol. 112 (1991) 55-63
31. Sorkin A., Waters C., Overholser K.A., and Carpenter G. Multiple autophosphorylation site mutations of the epidermal growth factor receptor. Analysis of kinase activity and endocytosis. J. Biol. Chem. 266 (1991) 8355-8362
32. Stoscheck C.M., and Carpenter G. Down regulation of epidermal growth factor receptors: direct demonstration of receptor degradation in human fibroblasts. J. Cell Biol. 98 (1984) 1048-1053
33. Tosoni D., Puri C., Confalonieri S., Salcini A.E., De Camilli P., Tacchetti C., and Di Fiore P.P. TTP specifically regulates the internalization of the transferrin receptor. Cell 123 (2005) 875-888
34. van Dam E.M., and Stoorvogel W. Dynamin-dependent transferrin receptor recycling by endosome-derived clathrin-coated vesicles. Mol. Biol. Cell 13 (2002) 169-182
35. Vieira A.V., Lamaze C., and Schmid S.L. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 274 (1996) 2086-2089
36. von Zastrow M., and Sorkin A. Signaling on the endocytic pathway. Curr. Opin. Cell Biol. 19 (2007) 436-445
37. Wang X., Bo J., Bridges T., Dugan K.D., Pan T.C., Chodosh L.A., and Montell D.J. Analysis of cell migration using whole-genome expression profiling of migratory cells in the Drosophila ovary. Dev. Cell 10 (2006) 483-495
38. Wiley H.S., and Cunningham D.D. The endocytotic rate constant. A cellular parameter for quantitating receptor-mediated endocytosis. J. Biol. Chem. 257 (1982) 4222-4229