A kinase-independent role for EGF receptor in autophagy initiation

Cell

Volumn 160, Issue 1-2, 2015, Pages 145-160

  Tan, Xiaojun ^a   Thapa, Narendra ^a   Sun, Yue ^a   Anderson, Richard A ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; EXOCYST; FIBROBLAST GROWTH FACTOR RECEPTOR 2; GEFITINIB; ONCOPROTEIN; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, HUMAN; EGFR PROTEIN, HUMAN; EXOC2 PROTEIN, HUMAN; LAPTM4B PROTEIN, HUMAN; MEMBRANE PROTEIN; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE; RUNDATAXIN PROTEIN, HUMAN; SIGNAL PEPTIDE; VESICULAR TRANSPORT PROTEIN;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; AUTOPHOSPHORYLATION; BIOTINYLATION; CELLULAR DISTRIBUTION; ENDOSOME; FEMALE; HEK293 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; STARVATION; UPREGULATION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; METABOLISM; TUMOR CELL LINE;

APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL LINE, TUMOR; ENDOSOMES; ERLOTINIB HYDROCHLORIDE; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; ONCOGENE PROTEINS; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; VESICULAR TRANSPORT PROTEINS;

EID: 84920945138     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.12.006     Document Type: Article

References (56)

1. J. Baselga, D. Rischin, M. Ranson, H. Calvert, E. Raymond, D.G. Kieback, S.B. Kaye, L. Gianni, A. Harris, and T. Bjork Phase I safety, pharmacokinetic, and pharmacodynamic trial of ZD1839, a selective oral epidermal growth factor receptor tyrosine kinase inhibitor, in patients with five selected solid tumor types J. Clin. Oncol. 20 2002 4292 4302
2. B.O. Bodemann, A. Orvedahl, T. Cheng, R.R. Ram, Y.H. Ou, E. Formstecher, M. Maiti, C.C. Hazelett, E.M. Wauson, and M. Balakireva RalB and the exocyst mediate the cellular starvation response by direct activation of autophagosome assembly Cell 144 2011 253 267
3. A. Brech, T. Ahlquist, R.A. Lothe, and H. Stenmark Autophagy in tumour suppression and promotion Mol. Oncol. 3 2009 366 375
4. H.S. Choi, E.H. Jeong, T.G. Lee, S.Y. Kim, H.R. Kim, and C.H. Kim Autophagy inhibition with monensin enhances cell cycle arrest and apoptosis induced by mTOR or epidermal growth factor receptor inhibitors in lung cancer cells Tuberc. Respir. Dis. (Seoul) 75 2013 9 17
5. K.J. Coker, J.V. Staros, and C.A. Guyer A kinase-negative epidermal growth factor receptor that retains the capacity to stimulate DNA synthesis Proc. Natl. Acad. Sci. USA 91 1994 6967 6971
6. W.H. Dragowska, S.A. Weppler, J.C. Wang, L.Y. Wong, A.I. Kapanen, J.S. Rawji, C. Warburton, M.A. Qadir, E. Donohue, and M. Roberge Induction of autophagy is an early response to gefitinib and a potential therapeutic target in breast cancer PLoS ONE 8 2013 e76503
7. E.R. Eden, I.J. White, A. Tsapara, and C.E. Futter Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction Nat. Cell Biol. 12 2010 267 272
8. S. Eimer, M.A. Belaud-Rotureau, K. Airiau, M. Jeanneteau, E. Laharanne, N. Véron, A. Vital, H. Loiseau, J.P. Merlio, and F. Belloc Autophagy inhibition cooperates with erlotinib to induce glioblastoma cell death Cancer Biol. Ther. 11 2011 1017 1027
9. J.A. Ewald, J.C. Wilkinson, C.A. Guyer, and J.V. Staros Ligand- and kinase activity-independent cell survival mediated by the epidermal growth factor receptor expressed in 32D cells Exp. Cell Res. 282 2003 121 131
10. C.M. Fader, and M.I. Colombo Autophagy and multivesicular bodies: two closely related partners Cell Death Differ. 16 2009 70 78
11. Y. Feng, D. He, Z. Yao, and D.J. Klionsky The machinery of macroautophagy Cell Res. 24 2014 24 41
12. S. Foerster, T. Kacprowski, V.M. Dhople, E. Hammer, S. Herzog, H. Saafan, S. Bien-Möller, M. Albrecht, U. Völker, and C.A. Ritter Characterization of the EGFR interactome reveals associated protein complex networks and intracellular receptor dynamics Proteomics 13 2013 3131 3144
13. J.R. Friedman, J.R. Dibenedetto, M. West, A.A. Rowland, and G.K. Voeltz Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature Mol. Biol. Cell 24 2013 1030 1040
14. C. Fung, X. Chen, J.R. Grandis, and U. Duvvuri EGFR tyrosine kinase inhibition induces autophagy in cancer cells Cancer Biol. Ther. 13 2012 1417 1424
15. S.B. Goldberg, J.G. Supko, J.W. Neal, A. Muzikansky, S. Digumarthy, P. Fidias, J.S. Temel, R.S. Heist, A.T. Shaw, and P.O. McCarthy A phase I study of erlotinib and hydroxychloroquine in advanced non-small-cell lung cancer J. Thorac. Oncol. 7 2012 1602 1608
16. Y. Gorzalczany, Y. Gilad, D. Amihai, I. Hammel, R. Sagi-Eisenberg, and O. Merimsky Combining an EGFR directed tyrosine kinase inhibitor with autophagy-inducing drugs: a beneficial strategy to combat non-small cell lung cancer Cancer Lett. 310 2011 207 215
17. M. Hamasaki, N. Furuta, A. Matsuda, A. Nezu, A. Yamamoto, N. Fujita, H. Oomori, T. Noda, T. Haraguchi, and Y. Hiraoka Autophagosomes form at ER-mitochondria contact sites Nature 495 2013 389 393
18. W. Han, H. Pan, Y. Chen, J. Sun, Y. Wang, J. Li, W. Ge, L. Feng, X. Lin, and X. Wang EGFR tyrosine kinase inhibitors activate autophagy as a cytoprotective response in human lung cancer cells PLoS ONE 6 2011 e18691
19. C. He, and B. Levine The Beclin 1 interactome Curr. Opin. Cell Biol. 22 2010 140 149
20. S.C. Helle, G. Kanfer, K. Kolar, A. Lang, A.H. Michel, and B. Kornmann Organization and function of membrane contact sites Biochim. Biophys. Acta 1833 2013 2526 2541
21. B. Jutten, and K.M. Rouschop EGFR signaling and autophagy dependence for growth, survival, and therapy resistance Cell Cycle 13 2014 42 51
22. B. Jutten, T.G. Keulers, M.B. Schaaf, K. Savelkouls, J. Theys, P.N. Span, M.A. Vooijs, J. Bussink, and K.M. Rouschop EGFR overexpressing cells and tumors are dependent on autophagy for growth and survival Radiother. Oncol. 108 2013 479 483
23. Y. Kabeya, N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, and T. Yoshimori LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing EMBO J. 19 2000 5720 5728
24. G. Kasper, A. Vogel, I. Klaman, J. Gröne, I. Petersen, B. Weber, E. Castaños-Vélez, E. Staub, and D. Mennerich The human LAPTM4b transcript is upregulated in various types of solid tumours and seems to play a dual functional role during tumour progression Cancer Lett. 224 2005 93 103
25. D.J. Klionsky, F.C. Abdalla, H. Abeliovich, R.T. Abraham, A. Acevedo-Arozena, K. Adeli, L. Agholme, M. Agnello, P. Agostinis, and J.A. Aguirre-Ghiso Guidelines for the use and interpretation of assays for monitoring autophagy Autophagy 8 2012 445 544
26. C.A. Lamb, T. Yoshimori, and S.A. Tooze The autophagosome: origins unknown, biogenesis complex Nat. Rev. Mol. Cell Biol. 14 2013 759 774
27. X. Li, and Z. Fan The epidermal growth factor receptor antibody cetuximab induces autophagy in cancer cells by downregulating HIF-1alpha and Bcl-2 and activating the beclin 1/hVps34 complex Cancer Res. 70 2010 5942 5952
28. L. Li, X.H. Wei, Y.P. Pan, H.C. Li, H. Yang, Q.H. He, Y. Pang, Y. Shan, F.X. Xiong, G.Z. Shao, and R.L. Zhou LAPTM4B: a novel cancer-associated gene motivates multidrug resistance through efflux and activating PI3K/AKT signaling Oncogene 29 2010 5785 5795
29. X. Li, Y. Lu, T. Pan, and Z. Fan Roles of autophagy in cetuximab-mediated cancer therapy against EGFR Autophagy 6 2010 1066 1077
30. Y. Li, L. Zou, Q. Li, B. Haibe-Kains, R. Tian, Y. Li, C. Desmedt, C. Sotiriou, Z. Szallasi, and J.D. Iglehart Amplification of LAPTM4B and YWHAZ contributes to chemotherapy resistance and recurrence of breast cancer Nat. Med. 16 2010 214 218
31. L. Li, Y. Shan, H. Yang, S. Zhang, M. Lin, P. Zhu, X.Y. Chen, J. Yi, M.A. McNutt, G.Z. Shao, and R.L. Zhou Upregulation of LAPTM4B-35 promotes malignant transformation and tumorigenesis in L02 human liver cell line Anat. Rec. (Hoboken) 294 2011 1135 1142
32. Y. Li, Q. Zhang, R. Tian, Q. Wang, J.J. Zhao, J.D. Iglehart, Z.C. Wang, and A.L. Richardson Lysosomal transmembrane protein LAPTM4B promotes autophagy and tolerance to metabolic stress in cancer cells Cancer Res. 71 2011 7481 7489
33. Y.Y. Li, S.K. Lam, J.C. Mak, C.Y. Zheng, and J.C. Ho Erlotinib-induced autophagy in epidermal growth factor receptor mutated non-small cell lung cancer Lung Cancer 81 2013 354 361
34. X.R. Liu, R.L. Zhou, Q.Y. Zhang, Y. Zhang, Y.Y. Jin, M. Lin, J.A. Rui, and D.X. Ye Structure analysis and expressions of a novel tetratransmembrane protein, lysosoma-associated protein transmembrane 4 beta associated with hepatocellular carcinoma World J. Gastroenterol. 10 2004 1555 1559
35. K. Matsunaga, T. Saitoh, K. Tabata, H. Omori, T. Satoh, N. Kurotori, I. Maejima, K. Shirahama-Noda, T. Ichimura, and T. Isobe Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages Nat. Cell Biol. 11 2009 385 396
36. J. Mendelsohn, and J. Baselga Epidermal growth factor receptor targeting in cancer Semin. Oncol. 33 2006 369 385
37. J.G. Paez, P.A. Jänne, J.C. Lee, S. Tracy, H. Greulich, S. Gabriel, P. Herman, F.J. Kaye, N. Lindeman, and T.J. Boggon EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy Science 304 2004 1497 1500
38. Y. Sakuma, S. Matsukuma, Y. Nakamura, M. Yoshihara, S. Koizume, H. Sekiguchi, H. Saito, H. Nakayama, Y. Kameda, and T. Yokose Enhanced autophagy is required for survival in EGFR-independent EGFR-mutant lung adenocarcinoma cells Lab. Invest. 93 2013 1137 1146
39. J. Schlessinger Cell signaling by receptor tyrosine kinases Cell 103 2000 211 225
40. G.Z. Shao, R.L. Zhou, Q.Y. Zhang, Y. Zhang, J.J. Liu, J.A. Rui, X. Wei, and D.X. Ye Molecular cloning and characterization of LAPTM4B, a novel gene upregulated in hepatocellular carcinoma Oncogene 22 2003 5060 5069
41. A. Sobhakumari, B.M. Schickling, L. Love-Homan, A. Raeburn, E.V. Fletcher, A.J. Case, F.E. Domann, F.J.J. Miller Jr., and A.L. Simons NOX4 mediates cytoprotective autophagy induced by the EGFR inhibitor erlotinib in head and neck cancer cells Toxicol. Appl. Pharmacol. 272 2013 736 745
42. A. Sorkin, and L.K. Goh Endocytosis and intracellular trafficking of ErbBs Exp. Cell Res. 314 2008 3093 3106
43. D. Soulieres, N.N. Senzer, E.E. Vokes, M. Hidalgo, S.S. Agarwala, and L.L. Siu Multicenter phase II study of erlotinib, an oral epidermal growth factor receptor tyrosine kinase inhibitor, in patients with recurrent or metastatic squamous cell cancer of the head and neck J. Clin. Oncol. 22 2004 77 85
44. Q. Sun, W. Fan, and Q. Zhong Regulation of Beclin 1 in autophagy Autophagy 5 2009 713 716
45. S. Vergarajauregui, J.A. Martina, and R. Puertollano LAPTMs regulate lysosomal function and interact with mucolipin 1: new clues for understanding mucolipidosis type IV J. Cell Sci. 124 2011 459 468
46. Y. Wei, Z. Zou, N. Becker, M. Anderson, R. Sumpter, G. Xiao, L. Kinch, P. Koduru, C.S. Christudass, and R.W. Veltri EGFR-mediated Beclin 1 phosphorylation in autophagy suppression, tumor progression, and tumor chemoresistance Cell 154 2013 1269 1284
47. Z. Weihua, R. Tsan, W.C. Huang, Q. Wu, C.H. Chiu, I.J. Fidler, and M.C. Hung Survival of cancer cells is maintained by EGFR independent of its kinase activity Cancer Cell 13 2008 385 393
48. E. White Deconvoluting the context-dependent role for autophagy in cancer Nat. Rev. Cancer 12 2012 401 410
49. H.S. Wiley Trafficking of the ErbB receptors and its influence on signaling Exp. Cell Res. 284 2003 78 88
50. H. Yang, F. Xiong, X. Wei, Y. Yang, M.A. McNutt, and R. Zhou Overexpression of LAPTM4B-35 promotes growth and metastasis of hepatocellular carcinoma in vitro and in vivo Cancer Lett. 294 2010 236 244
51. Y. Zhong, Q. Wang, X. Li, Y. Yan, J. Backer, B. Chait, N. Heintz, and Z. Yue Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex Nat. Cell Biol. 11 2009 468 476
52. Y. Zou, Y.H. Ling, J. Sironi, E.L. Schwartz, R. Perez-Soler, and B. Piperdi The autophagy inhibitor chloroquine overcomes the innate resistance of wild-type EGFR non-small-cell lung cancer cells to erlotinib J. Thorac. Oncol. 8 2013 693 702
53. Y. Churin, L. Al-Ghoul, O. Kepp, T.F. Meyer, W. Birchmeier, and M. Naumann Helicobacter pylori CagA protein targets the c-Met receptor and enhances the motogenic response J. Cell Biol. 161 2003 249 255
54. S. Moskalenko, D.O. Henry, C. Rosse, G. Mirey, J.H. Camonis, and M.A. White The exocyst is a Ral effector complex Nat. Cell Biol. 4 2002 66 72
55. S. Moskalenko, C. Tong, C. Rosse, G. Mirey, E. Formstecher, L. Daviet, J. Camonis, and M.A. White Ral GTPases regulate exocyst assembly through dual subunit interactions J. Biol. Chem. 278 2003 51743 51748
56. N. Thapa, Y. Sun, M. Schramp, S. Choi, K. Ling, and R.A. Anderson Phosphoinositide signaling regulates the exocyst complex and polarized integrin trafficking in directionally migrating cells Dev. Cell 22 2012 116 130