WASH and Tsg101/ALIX-dependent diversion of stress-internalized EGFR from the canonical endocytic pathway

Nature Communications

Volumn 6, Issue , 2015, Pages

  Tomas, Alejandra ^a   Vaughan, Simon O ^a   Burgoyne, Thomas ^a   Sorkin, Alexander ^b   Hartley, John A ^c   Hochhauser, Daniel ^c   Futter, Clare E ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

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

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE P38; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UNCLASSIFIED DRUG; WASP AND SCAR HOMOLOGUE; ACTIN BINDING PROTEIN; DNA BINDING PROTEIN; ESCRT PROTEIN; TRANSCRIPTION FACTOR; WASH PROTEIN, HUMAN;

APOPTOSIS; CANCER; CELLS AND CELL COMPONENTS; DRUG; ENZYME ACTIVITY; LIGAND; POLYMERIZATION; PROTEIN; SUBPOPULATION; TUMOR;

ACTIN POLYMERIZATION; APOPTOSIS; ARTICLE; DRUG RESISTANCE; ENDOCYTOSIS; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; INTERNALIZATION; MULTIVESICULAR BODY; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; ULTRAVIOLET C RADIATION; METABOLISM; PROTEIN TRANSPORT;

DNA-BINDING PROTEINS; ENDOCYTOSIS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; HELA CELLS; HUMANS; MICROFILAMENT PROTEINS; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN TRANSPORT; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84935904669     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8324     Document Type: Article

References (43)

1. Jones, S. & Rappoport, J. Z. Interdependent epidermal growth factor receptor signalling and trafficking. Int. J. Biochem. Cell Biol. 51, 23-28 (2014).
2. Sorkin, A. & Goh, L. K. Endocytosis and intracellular trafficking of ErbBs. Exp. Cell Res. 315, 683-696 (2009).
3. Murphy, J. E., Padilla, B. E., Hasdemir, B., Cottrell, G. S. & Bunnett, N. W. Endosomes: a legitimate platform for the signaling train. Proc. Natl Acad. Sci. USA 106, 17615-17622 (2009).
4. Scaltriti, M. & Baselga, J. The epidermal growth factor receptor pathway: a model for targeted therapy. Clin. Cancer Res. 12, 5268-5272 (2006).
5. Chong, C. R. & Janne, P. A. The quest to overcome resistance to EGFR-targeted therapies in cancer. Nature Med. 19, 1389-1400 (2013).
6. Zwang, Y. & Yarden, Y. p38 MAP kinase mediates stress-induced internalization of EGFR: implications for cancer chemotherapy. EMBO J. 25, 4195-4206 (2006).
7. Khan, E. M. et al. Epidermal growth factor receptor exposed to oxidative stress undergoes Src-and caveolin-1-dependent perinuclear trafficking. J. Biol. Chem. 281, 14486-14493 (2006).
8. Tomas, A., Futter, C. E. & Eden, E. R. EGF receptor trafficking: consequences for signaling and cancer. Trends Cell Biol. 24, 26-34 (2014).
9. Oksvold, M. P., Huitfeldt, H. S., Ostvold, A. C. & Skarpen, E. UV induces tyrosine kinase-independent internalisation and endosome arrest of the EGF receptor. J. Cell Sci. 115, 793-803 (2002).
10. Stenmark, H. et al. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13, 1287-1296 (1994).
11. White, I. J., Bailey, L. M., Aghakhani, M. R., Moss, S. E. & Futter, C. E. EGF stimulates annexin 1-dependent inward vesiculation in a multivesicular endosome subpopulation. EMBO J. 25, 1-12 (2006).
12. Marks, M. S. & Seabra, M. C. The melanosome: membrane dynamics in black and white. Nat. Rev. Mol. Cell Biol. 2, 738-748 (2001).
13. Leonhardt, R. M., Vigneron, N., Hee, J. S., Graham, M. & Cresswell, P. Critical residues in the PMEL/Pmel17 N-terminus direct the hierarchical assembly of melanosomal fibrils. Mol. Biol. Cell 24, 964-981 (2013).
14. Berson, J. F., Harper, D. C., Tenza, D., Raposo, G. & Marks, M. S. Pmel17 initiates premelanosome morphogenesis within multivesicular bodies. Mol. Biol. Cell 12, 3451-3464 (2001).
15. van, N. G. et al. The tetraspanin CD63 regulates ESCRT-independent and-dependent endosomal sorting during melanogenesis. Dev. Cell 21, 708-721 (2011).
16. Burgoyne, T. et al. Expression of OA1 limits the fusion of a subset of MVBs with lysosomes-a mechanism potentially involved in the initial biogenesis of melanosomes. J. Cell Sci. 126, 5143-5152 (2013).
17. Gautreau, A., Oguievetskaia, K. & Ungermann, C. Function and regulation of the endosomal fusion and fission machineries. Cold Spring Harb. Perspect. Biol 6 (2014).
18. Seaman, M. N., Gautreau, A. & Billadeau, D. D. Retromer-mediated endosomal protein sorting: all WASHed up! Trends Cell Biol. 23, 522-528 (2013).
19. McGough, I. J. et al. Retromer binding to FAM21 and the WASH complex is perturbed by the Parkinson disease-linked VPS35(D620N) mutation. Curr. Biol. 24, 1670-1676 (2014).
20. Freeman, C., Seaman, M. N. & Reid, E. The hereditary spastic paraplegia protein strumpellin: characterisation in neurons and of the effect of disease mutations on WASH complex assembly and function. Biochim. Biophys. Acta 1832, 160-173 (2013).
21. Setty, S. R. et al. BLOC-1 is required for cargo-specific sorting from vacuolar early endosomes toward lysosome-related organelles. Mol. Biol. Cell 18, 768-780 (2007).
22. Ryder, P. V. et al. The WASH complex, an endosomal Arp2/3 activator, interacts with the Hermansky-Pudlak syndrome complex BLOC-1 and its cargo phosphatidylinositol-4-kinase type IIalpha. Mol. Biol. Cell 24, 2269-2284 (2013).
23. Gomez, T. S., Gorman, J. A., de Narvajas, A. A., Koenig, A. O. & Billadeau, D. D. Trafficking defects in WASH-knockout fibroblasts originate from collapsed endosomal and lysosomal networks. Mol. Biol. Cell 23, 3215-3228 (2012).
24. Raiborg, C. & Stenmark, H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458, 445-452 (2009).
25. Jahngen-Hodge, J. et al. Regulation of ubiquitin-conjugating enzymes by glutathione following oxidative stress. J. Biol. Chem. 272, 28218-28226 (1997).
26. Eden, E. R., Huang, F., Sorkin, A. & Futter, C. E. The role of EGF receptor ubiquitination in regulating its intracellular traffic. Traffic 13, 329-337 (2012).
27. Mageswaran, S. K., Dixon, M. G., Curtiss, M., Keener, J. P. & Babst, M. Binding to any ESCRT can mediate ubiquitin-independent cargo sorting. Traffic 15, 212-229 (2014).
28. Amorim, N. A. et al. Interaction of HIV-1 Nef with the host protein alix promotes lysosomal targeting of CD4 receptor. J. Biol. Chem. 289, 27744-27756 (2014).
29. Dores, M. R. et al. AP-3 regulates PAR1 ubiquitin-independent MVB/lysosomal sorting via an ALIX-mediated pathway. Mol. Biol. Cell 23, 3612-3623 (2012).
30. Bissig, C. & Gruenberg, J. ALIX and the multivesicular endosome: ALIX in Wonderland. Trends Cell Biol. 24, 19-25 (2014).
31. Winograd-Katz, S. E. & Levitzki, A. Cisplatin induces PKB/Akt activation and p38(MAPK) phosphorylation of the EGF receptor. Oncogene 25, 7381-7390 (2006).
32. Sigismund, S. et al. Threshold-controlled ubiquitination of the EGFR directs receptor fate. EMBO J. 32, 2140-2157 (2013).
33. Grandal, M. V. et al. Differential roles of Grb2 and AP-2 in p38MAPK-and EGF-Induced EGFR Internalization. Traffic 13, 576-585 (2012).
34. Goh, L. K., Huang, F., Kim, W., Gygi, S. & Sorkin, A. Multiple mechanisms collectively regulate clathrin-mediated endocytosis of the epidermal growth factor receptor. J. Cell Biol. 189, 871-883 (2010).
35. Le Blanc, I. et al. Endosome-to-cytosol transport of viral nucleocapsids. Nat. Cell Biol. 7, 653-664 (2005).
36. Tice, D. A., Biscardi, J. S., Nickles, A. L. & Parsons, S. J. Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc. Natl Acad. Sci.USA 96, 1415-1420 (1999).
37. Carter, R. E. & Sorkin, A. Endocytosis of functional epidermal growth factor receptor-green fluorescent protein chimera. J. Biol. Chem. 273, 35000-35007 (1998).
38. Nichols, S. E., Harper, D. C., Berson, J. F. & Marks, M. S. A novel splice variant of Pmel17 expressed by human melanocytes and melanoma cells lacking some of the internal repeats. J. Invest Dermatol. 121, 821-830 (2003).
39. Razi, M. & Futter, C. E. Distinct roles for Tsg101 and Hrs in multivesicular body formation and inward vesiculation. Mol. Biol. Cell 17, 3469-3483 (2006).
40. Matsuo, H. et al. Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science 303, 531-534 (2004).
41. Edgar, J. R., Eden, E. R. & Futter, C. E. Hrs-and CD63-dependent competing mechanisms make different sized endosomal intraluminal vesicles. Traffic 15, 197-211 (2014).
42. Tomas, A., Futter, C. & Moss, S. E. Annexin 11 is required for midbody formation and completion of the terminal phase of cytokinesis. J. Cell Biol. 165, 813-822 (2004).
43. Futter, C. E. et al. In polarized MDCK cells basolateral vesicles arise from clathrin-gamma-adaptin-coated domains on endosomal tubules. J. Cell Biol. 141, 611-623 (1998).