Proteasome inhibition blocks ligand-induced dynamic processing and internalization of epidermal growth factor receptor via altered receptor ubiquitination and phosphorylation

Cancer Research

Volumn 69, Issue 3, 2009, Pages 976-983

  Kesarwala, Aparna H ^a   Samrakandi, Mustapha M ^a   Piwnica Worms, David ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BORTEZOMIB; EPIDERMAL GROWTH FACTOR RECEPTOR; GREEN FLUORESCENT PROTEIN; LIGAND; LUCIFERASE; PROTEASOME; PROTEASOME INHIBITOR;

ARTICLE; BIOLUMINESCENCE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; INTERNALIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; UBIQUITINATION; WESTERN BLOTTING;

BORONIC ACIDS; EPIDERMAL GROWTH FACTOR; GENES, REPORTER; HELA CELLS; HUMANS; LUCIFERASES, FIREFLY; MICROSCOPY, FLUORESCENCE; PHOSPHORYLATION; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; PYRAZINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; TRANSFECTION; UBIQUITINATION;

EID: 59149102535     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-2938     Document Type: Article

References (39)

1. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001;2:127-37.
2. Joneson T, Bar-Sagi D. Ras effectors and their role in mitogenesis and oncogenesis. J Mol Med 1997;75:587-93.
3. Mosesson Y, Shtiegman K, Katz M, et al. Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J Biol Chem 2003;278:21323-6.
4. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 2006;21:737-48.
5. Hicke L, Riezman H. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 1996;84:277-87.
6. Miller K, Beardmore J, Kanety H, Schlessinger J, Hopkins CR. Localization of the epidermal growth factor (EGF) receptor within the endosome of EGF-stimulated epidermoid carcinoma (A431) cells. J Cell Biol 1986;102:500-9.
7. Futter CE, Pearse A, Hewlett LJ, Hopkins CR. Multi-vesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J Cell Biol 1996;132:1011-23.
8. Peschard P, Park M. Escape from Cbl-mediated downregulation: a recurrent theme for oncogenic deregulation of receptor tyrosine kinases. Cancer Cell 2003;3:519-23.
9. Wikstrand CJ, Reist CJ, Archer GE, Zalutsky MR, Bigner DD. The class III variant of the epidermal growth factor receptor (EGFRvIII): characterization and utilization as an immunotherapeutic target. J Neurovirol 1998;4:148-58.
10. Resnick MB, Routhier J, Konkin T, Sabo E, Pricolo VE. Epidermal growth factor receptor, c-MET, β-catenin, and p53 expression as prognostic indicators in stage II colon cancer: a tissue microarray study. Clin Cancer Res 2004;10:3069-75.
11. Abd El-Rehim DM, Pinder SE, Paish CE, et al. Expression and co-expression of the members of the epidermal growth factor receptor (EGFR) family in invasive breast carcinoma. Br J Cancer 2004;91:1532-42.
12. Veale D, Ashcroft T, Marsh C, Gibson GJ, Harris AL. Epidermal growth factor receptors in non-small cell lung cancer. Br J Cancer 1987;55:513-6.
13. Barker AJ, Gibson KH, Grundy W, et al. Studies leading to the identification of ZD1839 (IRESSA): an orally active, selective epidermal growth factor receptor tyrosine kinase inhibitor targeted to the treatment of cancer. Bioorg Med Chem Lett 2001;11:1911-4.
14. Wakeling AE, Guy SP, Woodburn JR, et al. ZD1839 (Iressa): an orally active inhibitor of epidermal growth factor signaling with potential for cancer therapy. Cancer Res 2002;62:5749-54.
15. Mendelsohn J, Baselga J. Status of epidermal growth factor receptor antagonists in the biology and treatment of cancer. J Clin Oncol 2003;21:2787-99.
16. Blackledge G, Averbuch S. Gefitinib ('Iressa', ZD1839) and new epidermal growth factor receptor inhibitors. Br J Cancer 2004;90:566-72.
17. Fukuoka M, Yano S, Giaccone G, et al. Multi-institutional randomized phase II trial of gefitinib for previously treated patients with advanced non-small-cell lung cancer. J Clin Oncol 2003;21:2237-46.
18. Lynch TJ, Bell DW, Sordella R, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004;350:2129-39.
19. Paez JG, Janne PA, Lee JC, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004;304:1497-500.
20. Pao W, Miller V, Zakowski M, et al. EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci U S A 2004;101:13306-11.
21. Arwert E, Hingtgen S, Figueiredo JL, et al. Visualizing the dynamics of EGFR activity and antiglioma therapies in vivo. Cancer Res 2007;67:7335-42.
22. Robinson CR, Sauer RT. Optimizing the stability of single-chain proteins by linker length and composition mutagenesis. Proc Natl Acad Sci U S A 1998;95:5929-34.
23. Kesarwala AH, Prior JL, Sun J, et al. Second-generation triple reporter for bioluminescence, micropositron emission tomography, and fluorescence imaging. Mol Imaging 2006;5:465-74.
24. Gross S, Piwnica-Worms D. Real-time imaging of ligand-induced IKK activation in intact cells and in living mice. Nat Methods 2005;2:607-14.
25. Moss BL, Gross S, Gammon ST, Vinjamoori A, Piwnica-Worms D. Identification of a ligand-induced transient refractory period in nuclear factor-κB signaling. J Biol Chem 2008;283:8687-98.
26. Neelam B, Richter A, Chamberlin SG, et al. Structure-function studies of ligand-induced epidermal growth factor receptor dimerization. Biochemistry 1998;37:4884-91.
27. Pruss RM, Herschman HR. Variants of 3T3 cells lacking mitogenic response to epidermal growth factor. Proc Natl Acad Sci U S A 1977;74:3918-21.
28. Osherov N, Levitzki A. Epidermal-growth-factor-dependent activation of the src-family kinases. Eur J Biochem 1994;225:1047-53.
29. Fernandez-Borja M, Wubbolts R, Calafat J, et al. Multivesicular body morphogenesis requires phosphatidyl-inositol 3-kinase activity. Curr Biol 1999;9:55-8.
30. Futter CE, Collinson LM, Backer JM, Hopkins CR. Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J Cell Biol 2001;155:1251-64.
31. Schmidt MH, Furnari FB, Cavenee WK, Bogler O. Epidermal growth factor receptor signaling intensity determines intracellular protein interactions, ubiquitination, and internalization. Proc Natl Acad Sci U S A 2003;100:6505-10.
32. Curto M, Cole B, Lallemand D, Liu C, McClatchey A. Contact-dependent inhibition of EGFR signaling by Nf2/ Merlin. J Cell Biol 2007;177:893-903.
33. Zimmer M. Green fluorescent protein (GFP): applications, structure, and related photophysical behavior. Chem Rev 2002;102:759-81.
34. Luker G, Pica C, Song J, Luker K, Piwnica-Worms D. Imaging 26S proteasome activity and inhibition in living mice. Nat Med 2003;9:969-73.
35. Milano A, Iaffaioli RV, Caponigro F. The proteasome: a worthwhile target for the treatment of solid tumours? Eur J Cancer 2007;43:1125-33.
36. Adams J. The proteasome: a suitable antineoplastic target. Nat Rev Cancer 2004;4:349-60.
37. Adams J, Palombella VJ, Sausville EA, et al. Proteasome inhibitors: a novel class of potent and effective antitumor agents. Cancer Res 1999;59:2615-22.
38. Richardson PG, Mitsiades C, Hideshima T, Anderson KC. Bortezomib: proteasome inhibition as an effective anticancer therapy. Annu Rev Med 2006;57:33-47.
39. Nencioni A, Grunebach F, Patrone F, Ballestrero A, Brossart P. Proteasome inhibitors: antitumor effects and beyond. Leukemia 2007;21:30-6.