ERBB3-independent activation of the PI3K pathway in EGFR-mutant lung adenocarcinomas

Cancer Research

Volumn 75, Issue 6, 2015, Pages 1035-1045

  Song, Xiaoling ^a   Fan, Pang Dian ^b   Bantikassegn, Amlak ^a   Guha, Udayan ^b,d   Threadgill, David W ^c   Varmus, Harold ^b,e   Politi, Katerina ^a,b  

^a YALE CANCER CENTER   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; GAB1 PROTEIN; GAB2 PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SCATTER FACTOR RECEPTOR; TAMOXIFEN; TETRACYCLINE; UNCLASSIFIED DRUG; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN; QUINAZOLINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CHEMOSENSITIVITY; CONTROLLED STUDY; DISEASE MODEL; ENZYME ACTIVATION; ERBB3 GENE; GENE DELETION; GENE MUTATION; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; LUNG CANCER CELL LINE; LUNG CARCINOGENESIS; MOUSE; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; TREATMENT RESPONSE; TUMOR REGRESSION; ADENOCARCINOMA; ANIMAL; GENETICS; LUNG NEOPLASMS; MUTATION; PHYSIOLOGY; TUMOR CELL LINE;

ADENOCARCINOMA; ANIMALS; CELL LINE, TUMOR; ERLOTINIB HYDROCHLORIDE; HUMANS; LUNG NEOPLASMS; MICE; MUTATION; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3; SIGNAL TRANSDUCTION;

EID: 84933076147     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-1625     Document Type: Article

References (33)

1. Riese DJII, Stern DF. Specificity within the EGF family/ErbB receptor family signaling network. Bioessays 1998;20:41-8.
2. Guy PM, Platko JV, Cantley LC, Cerione RA, Carraway KL III. Insect cell-expressed p180erbB3 possesses an impaired tyrosine kinase activity. Proc Natl Acad Sci U S A 1994;91:8132-6.
3. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, 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.
4. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004;304:1497-500.
5. Pao W, Miller V, Zakowski M, Doherty J, Politi K, Sarkaria I, 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.
6. Yang CH. EGFR tyrosine kinase inhibitors for the treatment of NSCLC in East Asia: present and future. Lung Cancer 2008;60:S23-30.
7. Greulich H, Chen TH, Feng W, Janne PA, Alvarez JV, Zappaterra M, et al. Oncogenic transformation by inhibitor-sensitive and -resistant EGFR mutants. PLoS Med 2005;2:e313.
8. Ji H, Li D, Chen L, Shimamura T, Kobayashi S, McNamara K, et al. The impact of human EGFR kinase domain mutations on lung tumorigenesis and in vivo sensitivity to EGFR-targeted therapies. Cancer Cell 2006;9:485-95.
9. Politi K, Zakowski MF, Fan PD, Schonfeld EA, Pao W, Varmus HE. Lung adenocarcinomas induced in mice by mutant EGF receptors found in human lung cancers respond to a tyrosine kinase inhibitor or to downregulation of the receptors. Genes Dev 2006;20:1496-510.
10. Uramoto H, Mitsudomi T. Which biomarker predicts benefit from EGFR-TKI treatment for patients with lung cancer? Br J Cancer 2007;96:857-63.
11. Pao W, Miller VA, Politi KA, Riely GJ, Somwar R, Zakowski MF, et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2005;2:e73.
12. Sordella R, Bell DW, Haber DA, Settleman J. Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 2004;305:1163-7.
13. Rodrigues GA, Falasca M, Zhang Z, Ong SH, Schlessinger J. A novel positive feedback loop mediated by the docking protein Gab1 and phosphatidylinositol 3-kinase in epidermal growth factor receptor signaling. Mol Cell Biol 2000;20:1448-59.
14. Soltoff SP, Carraway KL III, Prigent SA, Gullick WG, Cantley LC. ErbB3 is involved in activation of phosphatidylinositol 3-kinase by epidermal growth factor. Mol Cell Biol 1994;14:3550-8.
15. Engelman JA, Janne PA, Mermel C, Pearlberg J, Mukohara T, Fleet C, et al. ErbB-3 mediates phosphoinositide 3-kinase activity in gefitinib-sensitive non-small cell lung cancer cell lines. Proc Natl Acad Sci U S A 2005;102:3788-93.
16. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007;316:1039-43.
17. Schoeberl B, Faber AC, Li D, Liang MC, Crosby K, Onsum M, et al. An ErbB3 antibody, MM-121, is active in cancers with ligand-dependent activation. Cancer Res 2010;70:2485-94.
18. Lee D, Yu M, Lee E, Kim H, Yang Y, Kim K, et al. Tumor-specific apoptosis caused by deletion of the ERBB3 pseudo-kinase in mouse intestinal epithelium. J Clin Invest 2009;119:2702-13.
19. Taniguchi H, He M, Wu P, Kim S, Paik R, Sugino K, et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 2011;71:995-1013.
20. Perl AK, Wert SE, Nagy A, Lobe CG, Whitsett JA. Early restriction of peripheral and proximal cell lineages during formation of the lung. Proc Natl Acad Sci U S A 2002;99:10482-7.
21. Chmielecki J, Foo J, Oxnard GR, Hutchinson K, Ohashi K, Somwar R, et al. Optimization of dosing for EGFR-mutant non-small cell lung cancer with evolutionary cancer modeling. Sci Transl Med 2011;3:90ra59.
22. Songyang Z, Shoelson SE, Chaudhuri M, Gish G, Pawson T, Haser WG, et al. SH2 domains recognize specific phosphopeptide sequences. Cell 1993;72:767-78.
23. Cuevas BD, Lu Y, Mao M, Zhang J, LaPushin R, Siminovitch K, et al. Tyrosine phosphorylation of p85 relieves its inhibitory activity on phosphatidylinositol 3-kinase. J Biol Chem 2001;276:27455-61.
24. Rordorf-Nikolic T, Van Horn DJ, Chen D, White MF, Backer JM. Regulation of phosphatidylinositol 3′-kinase by tyrosyl phosphoproteins. Full activation requires occupancy of both SH2 domains in the 85-kDa regulatory subunit. J Biol Chem 1995;270:3662-6.
25. Okutani T, Okabayashi Y, Kido Y, Sugimoto Y, Sakaguchi K, Matuoka K, et al. Grb2/Ash binds directly to tyrosines 1068 and 1086 and indirectly to tyrosine 1148 of activated human epidermal growth factor receptors in intact cells. J Biol Chem 1994;269:31310-4.
26. Mattoon DR, Lamothe B, Lax I, Schlessinger J. The docking protein Gab1 is the primary mediator of EGF-stimulated activation of the PI-3K/Akt cell survival pathway. BMC Biol 2004;2:24.
27. Kong M, Mounier C, Wu J, Posner BI. Epidermal growth factor-induced phosphatidylinositol 3-kinase activation and DNA synthesis. Identification of Grb2-associated binder 2 as the major mediator in rat hepatocytes. J Biol Chem 2000;275:36035-42.
28. Fujioka T, Kim JH, Adachi H, Saito K, Tsujimoto M, Yokoyama S, et al. Further evidence for the involvement of insulin receptor substrates in epidermal growth factor-induced activation of phosphatidylinositol 3-kinase. Eur J Biochem 2001;268:4158-68.
29. Maeda Y, Tsuchiya T, Hao H, Tompkins DH, Xu Y, Mucenski ML, et al. Kras (G12D) and Nkx2-1 haploinsufficiency induce mucinous adenocarcinoma of the lung. J Clin Invest 2012;122:4388-400.
30. Rudin CM, Liu W, Desai A, Karrison T, Jiang X, Janisch L, et al. Pharmacogenomic and pharmacokinetic determinants of erlotinib toxicity. J Clin Oncol 2008;26:1119-27.
31. Lahlou H, Muller T, Sanguin-Gendreau V, Birchmeier C, Muller WJ. Uncoupling of PI3K from ErbB3 impairs mammary gland development but does not impact on ErbB2-induced mammary tumorigenesis. Cancer Res 2012;72:3080-90.
32. Sithanandam G, Smith GT, Fields JR, Fornwald LW, Anderson LM. Alternate paths from epidermal growth factor receptor to Akt in malignant versus nontransformed lung epithelial cells: ErbB3 versus Gab1. Am J Respir Cell Mol Biol 2005;33:490-9.
33. Turke AB, Zejnullahu K, Wu YL, Song Y, Dias-Santagata D, Lifshits E, et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010;17:77-88.