Activation of the AXL kinase causes resistance to EGFR-targeted therapy in lung cancer

Nature Genetics

Volumn 44, Issue 8, 2012, Pages 852-860

  Zhang, Zhenfeng ^a,b   Lee, Jae Cheol ^c   Lin, Luping ^d   Olivas, Victor ^d   Au, Valerie ^b   Laframboise, Thomas ^a   Abdel Rahman, Mohamed ^a   Wang, Xiaoqi ^b   Levine, Alan D ^a   Rho, Jin Kyung ^e   Choi, Yun Jung ^e   Choi, Chang Min ^c,e   Kim, Sang We ^c   Jang, Se Jin ^e   Park, Young Soo ^e   Kim, Woo Sung ^e   Lee, Dae Ho ^c   Lee, Jung Shin ^c   Miller, Vincent A ^f   Arcila, Maria ^f   Ladanyi, Marc ^f   Moonsamy, Philicia ^f   Sawyers, Charles ^f   Boggon, Titus J ^g   Ma, Patrick C ^h   Costa, Carlota ^i,j   Taron, Miquel ^i,j   Rosell, Rafael ^i,j   Halmos, Balazs ^b   Bivona, Trever G ^d,f   more..

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NewYork Presbyterian Hospital   (United States)

^c University of Ulsan College of Medicine   (South Korea)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e University of Ulsan   (South Korea)

^f MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^g YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h CASE WESTERN RESERVE UNIVERSITY   (United States)

ⁱ HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^j INSTITUT UNIVERSITARI DEXEUS   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AFATINIB; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GEFITINIB; GROWTH ARREST SPECIFIC PROTEIN 6; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN; PROTEIN AXL; PROTEIN KINASE B; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; VIMENTIN;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER RESISTANCE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; IN VIVO STUDY; LUNG NON SMALL CELL CANCER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR XENOGRAFT; UPREGULATION;

ADULT; AGED; ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LUNG NEOPLASMS; MALE; MIDDLE AGED; MUTATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MET; QUINAZOLINES; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84864402225     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.2330     Document Type: Article

References (29)

1. Paez, J.G. et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 304, 1497-1500 (2004).
2. Pao, W. 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. USA 101, 13306-13311 (2004).
3. Lynch, T.J. et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 350, 2129-2139 (2004).
4. Sordella, R., Bell, D.W., Haber, D.A. & Settleman, J. Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 305, 1163-1167 (2004).
5. Jänne, P.A., Gray, N. & Settleman, J. Factors underlying sensitivity of cancers to small-molecule kinase inhibitors. Nat. Rev. Drug Discov. 8, 709-723 (2009).
6. Gazdar, A.F. Personalized medicine and inhibition of EGFR signaling in lung cancer. N. Engl. J. Med. 361, 1018-1020 (2009).
7. Kobayashi, S. et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 352, 786-792 (2005).
8. Pao, W. et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med. 2, e73 (2005).
9. Engelman, J.A. et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316, 1039-1043 (2007).
10. Turke, A.B. et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 17, 77-88 (2010).
11. Bivona, T.G. et al. FAS and NF-κB signalling modulate dependence of lung cancers on mutant EGFR. Nature 471, 523-526 (2011).
12. Arcila, M.E. et al. Rebiopsy of lung cancer patients with acquired resistance to EGFR inhibitors and enhanced detection of the T790M mutation using a locked nucleic acid-based assay. Clin. Cancer Res. 17, 1169-1180 (2011).
13. Bean, J. et al. MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib. Proc. Natl. Acad. Sci. USA 104, 20932-20937 (2007).
14. Sequist, L.V. et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci. Transl. Med. 3, 75ra26 (2011).
15. Linger, R.M., Keating, A.K., Earp, H.S. & Graham, D.K. Taking aim at Mer and Axl receptor tyrosine kinases as novel therapeutic targets in solid tumors. Expert Opin. Ther. Targets 14, 1073-1090 (2010).
16. Keating, A.K. et al. Inhibition of Mer and Axl receptor tyrosine kinases in astrocytoma cells leads to increased apoptosis and improved chemosensitivity. Mol. Cancer Ther. 9, 1298-1307 (2010).
17. Vuoriluoto, K. et al. Vimentin regulates EMT induction by Slug and oncogenic H-Ras and migration by governing Axl expression in breast cancer. Oncogene 30, 1436-1448 (2011).
18. Suda, K. et al. Epithelial to mesenchymal transition in an epidermal growth factor receptor-mutant lung cancer cell line with acquired resistance to erlotinib. J. Thorac. Oncol. 6, 1152-1161 (2011).
19. Ye, X. et al. An anti-Axl monoclonal antibody attenuates xenograft tumor growth and enhances the effect of multiple anticancer therapies. Oncogene 29, 5254-5264 (2010).
20. Qian, F. et al. Inhibition of tumor cell growth, invasion, and metastasis by EXEL-2880 (XL880, GSK1363089), a novel inhibitor of HGF and VEGF receptor tyrosine kinases. Cancer Res. 69, 8009-8016 (2009).
21. Yun, C.H. et al. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc. Natl. Acad. Sci. USA 105, 2070-2075 (2008).
22. Polyak, K. & Weinberg, R.A. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat. Rev. Cancer 9, 265-273 (2009).
23. Jackman, D. et al. Clinical definition of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancer. J. Clin. Oncol. 28, 357-360 (2010).
24. Burchert, A., Attar, E.C., McCloskey, P., Fridell, Y.W. & Liu, E.T. Determinants for transformation induced by the Axl receptor tyrosine kinase. Oncogene 16, 3177-3187 (1998).
25. Tai, K.Y., Shieh, Y.S., Lee, C.S., Shiah, S.G. & Wu, C.W. AXL promotes cell invasion by inducing MMP-9 activity through activation of NF-κB and Brg-1. Oncogene 27, 4044-4055 (2008).
26. Azumi, N. & Battifora, H. The distribution of vimentin and keratin in epithelial and nonepithelial neoplasms. A comprehensive immunohistochemical study on formalin-and alcohol-fixed tumors. Am. J. Clin. Pathol. 88, 286-296 (1987).
27. Chitale, D. et al. An integrated genomic analysis of lung cancer reveals loss of DUSP4 in EGFR-mutant tumors. Oncogene 28, 2773-2783 (2009).
28. Rosell, R., Wei, J. & Taron, M. Circulating microRNA signatures of tumor-derived exosomes for early diagnosis of non-small-cell lung cancer. Clin. Lung Cancer 10, 8-9 (2009).
29. Brevet, M., Arcila, M. & Ladanyi, M. Assessment of EGFR mutation status in lung adenocarcinoma by immunohistochemistry using antibodies specific to the two major forms of mutant EGFR. J. Mol. Diagn. 12, 169-176 (2010).