The pan-HER family tyrosine kinase inhibitor afatinib overcomes HER3 ligand heregulin-mediated resistance to EGFR inhibitors in non-small cell lung cancer

Oncotarget

Volumn 6, Issue 32, 2015, Pages 33602-33611

  Yonesaka, Kimio ^a   Kudo, Keita ^a   Nishida, Satomi ^a   Takahama, Takayuki ^a   Iwasa, Tsutomu ^a   Yoshida, Takeshi ^a   Tanaka, Kaoru ^a   Takeda, Masayuki ^a   Kaneda, Hiroyasu ^a   Okamoto, Isamu ^b   Nishio, Kazuto ^a   Nakagawa, Kazuhiko ^a  

^a KINKI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

Afatinib; Erlotinib; Heregulin; Human epidermal growth factor receptor; Non small cell lung cancer

Indexed keywords

AFATINIB; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERLOTINIB; GEFITINIB; NEU DIFFERENTIATION FACTOR; PROTEIN KINASE B; VASCULOTROPIN RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 3; ERBB3 PROTEIN, HUMAN; LIGAND; NRG1 PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG SENSITIVITY; DRUG TREATMENT FAILURE; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; HUMAN; IC50; IN VITRO STUDY; MOUSE; NON SMALL CELL LUNG CANCER; NONHUMAN; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROTEIN BLOOD LEVEL; PROTEIN PHOSPHORYLATION; RANDOMIZED CONTROLLED TRIAL (TOPIC); SIGNAL TRANSDUCTION; TREATMENT RESPONSE; TUMOR GROWTH; ANIMAL; BAGG ALBINO MOUSE; CARCINOMA, NON-SMALL-CELL LUNG; DRUG RESISTANCE; DRUG SCREENING; ENZYMOLOGY; LUNG NEOPLASMS; METABOLISM; NUDE MOUSE; TUMOR CELL LINE;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; LIGANDS; LUNG NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEUREGULIN-1; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, ERBB-3; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84946023279     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5286     Document Type: Article

References (30)

1. Hynes NE, Lane HA. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer. 2005; 5:341-354.
2. Yonesaka K, Zejnullahu K, Lindeman N, Homes AJ, Jackman DM, Zhao F, Rogers AM, Johnson BE, Jänne PA. Autocrine production of amphiregulin predicts sensitivity to both gefitinib and cetuximab in EGFR wild-type cancers. Clin Cancer Res. 2008; 14:6963-6973.
3. Paez JG, Jänne PA, Lee JC, Tracy S, Greulich H, Gabriel S, Herman P, Kaye FJ, Lindeman N, Boggon TJ, Naoki K, Sasaki H, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science. 2004; 304:1497-1500.
4. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, Harris PL, Haserlat SM, Supko JG, Haluska FG, Louis DN, Christiani DC, 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; 350:2129-2139.
5. Sequist LV, Waltman BA, Dias-Santagata D, Digumarthy S, Turke AB, Fidias P, Bergethon K, Shaw AT, Gettinger S, Cosper AK, Akhavanfard S, Heist RS, et al. Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Sci Transl Med. 2011; 3:75ra26.
6. Kobayashi S, Boggon T, Dayaram T, Jänne PA, Kocher O, Meyerson M, Johnson BE, Eck MJ, Tenen DG, Halmos B. EGFR mutation and resistance of non-small cell lung cancer to gefitinib. N Engl J Med. 2005; 352:786-792.
7. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, Lindeman N, Gale CM, Zhao X, Christensen J, Kosaka T, Holmes AJ, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science. 2007; 316:1039-1043.
8. Takezawa K, Pirazzoli V, Arcila ME, Nebhan CA, Song X, de Stanchina E, Ohashi K, Janjigian YY, Spitzler PJ, Melnick MA, Riely GJ, Kris MG, et al. HER2 amplification: a potential mechanism of acquired resistance to EGFR inhibition in EGFRmutant lung cancers that lack the second-site EGFRT790M mutation. Cancer Discov. 2012; 2:922-933.
9. Yano S, Wang W, Li Q, Matsumoto K, Sakurama H, Nakamura T, Ogino H, Kakiuchi S, Hanibuchi M, Nishioka Y, Uehara H, Mitsudomi T, et al. Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations. Cancer Res. 2008; 68:9479-9487.
10. Li D, Ambrogio L, Shimamura T, Kubo S, Takahashi M, Chirieac LR, Padera RF, Shapiro GI, Baum A, Himmelsbach F, Rettig WJ, Meyerson M, et al. BIBW2992, an irreversible EGFR/HER2 inhibitor highly effective in preclinical lung cancer models. Oncogene. 2008; 27:4702-4711.
11. Sequist LV, Yang JCH, Yamamoto N, O'Byrne K, Hirsh V, Mok T, Geater SL, Orlov S, Tsai CM, Boyer M, Su WC, Bennouna J, et al. Phase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutations. J Clin Oncol. 2013; 31:3327-3334.
12. Wu YL, Zhou C, Hu CP, Feng J, Lu S, Huang Y, Li W, Hou M, Shi JH, Lee KY, Xu CR, Massey D, et al. Afatinib versus cisplatin plus gemcitabine for first-line treatment of Asian patients with advanced non-small-cell lung cancer harbouring EGFR mutations (LUX-Lung 6): an open-label, randomised phase 3 trial. Lancet Oncol. 2014; 15:213-222.
13. Yang JC, Wu YL, Schuler M, Sebastian M, Popat S, Yamamoto N, Zhou C, Hu CP, O'Byrne K, Feng J, Lu S, Huang Y, et al. Afatinib versus cisplatin-based chemotherapy for EGFR mutation-positive lung adenocarcinoma (LUX-Lung 3 and LUX-Lung 6): analysis of overall survival data from two randomised, phase 3 trials. Lancet Oncol. 2015; 16:141-151.
14. Engelman JA, Zejnullahu K, Gale CM, Lifshits E, Gonzales AJ, Shimamura T, Zhao F, Vincent PW, Naumov GN, Bradner JE, Althaus IW, Gandhi L, et al. PF00299804, an irreversible pan-ERBB inhibitor, is effective in lung cancer models with EGFR and ERBB2 mutations that are resistant to gefitinib. Cancer Res. 2007; 67:11924-11932.
15. Ercan D, Zejnullahu K, Yonesaka K, Xiao Y, Capelletti M, Rogers A, Lifshits E, Brown A, Lee C, Christensen JG, Kwiatkowski DJ, Engelman JA, et al. Amplification of EGFR T790M causes resistance to an irreversible EGFR inhibitor. Oncogene. 2010; 29:2346-2356.
16. Katakami N, Atagi S, Goto K, Hida T, Horai T, Inoue A, Ichinose Y, Koboyashi K, Takeda K, Kiura K, Nishio K, Seki Y, et al. LUX-Lung 4: A Phase II trial of afatinib in patients with advanced non-small-cell lung cancer who progressed during prior treatment with erlotinib, gefitinib, or both. J Clin Oncol. 2013; 31:3335-3341.
17. Miller VA, Hirsh V, Cadranel J, Chen YM, Park K, Kim SW, Zhou C, Su WC, Wang M, Sun Y, Heo DS, Crino L, et al. Afatinib versus placebo for patients with advanced, metastatic non-small-cell lung cancer after failure of erlotinib, gefitinib, or both, and one or two lines of chemotherapy (LUX-Lung 1): a phase 2b/3 randomised trial. Lancet Oncol. 2012; 13:528-538.
18. Jänne PA, Yang JC, Kim DW, Planchard D, Ohe Y, Ramalingam SS, Ahn MJ, Kim SW, Su WC, Horn L, Haggstrom D, Felip E, et al. AZD9291 in EGFR inhibitorresistant non-small-cell lung cancer. N Engl J Med. 2015; 372:1689-1699.
19. Sequist LV, Soria JC, Goldman JW, Wakelee HA, Gadgeel SM, Varga A, Papadimitrakopoulou V, Solomon BJ, Oxnard GR, Dziadziuszko R, Aisner DL, Doebele RC, et al. Rociletinib in EGFR-mutated non-small-cell lung cancer. N Engl J Med. 2015; 372:1700-1709.
20. Zhou BB, Peyton M, He B, Liu C, Girard L, Caudler E, Lo Y, Baribaud F, Mikami I, Reguart N, Yang G, Li Y, et al. Targeting ADAM-mediated ligand cleavage to inhibit HER3 and EGFR pathways in non-small cell lung cancer. Cancer Cell. 2006; 10:39-50.
21. Aguilar Z, Akita RW, Finn RS, Ramos BL, Pegram MD, Kabbinavar FF, Pietras RJ, Pisacane P, Sliwkowski MX, Slamon DJ. Biologic effects of heregulin/neu differentiation factor on normal and malignant human breast and ovarian epithelial cells. Oncogene. 1999; 18:6050-6062.
22. Yonesaka K, Hirotani K, Kawakami H, Takeda M, Kaneda H, Sakai K, Okamoto I, Nishio K, Jänne PA, Nakagawa K. Anti-HER3 monoclonal antibody patritumab sensitizes refractory non-small cell lung cancer to the epidermal growth factor receptor inhibitor erlotinib. Oncogene. 2015; May 11; doi: 10.1038/onc.2015.142.
23. Yonesaka K, Zejnullahu K, Okamoto I, Satoh T, Cappuzzo F, Souglakos J, Ercan D, Rogers A, Roncalli M, Takeda M, Fujisaka Y, Philips J, et al. Activation of ERBB2 signaling causes resistance to the EGFR-directed therapeutic antibody cetuximab. Sci Transl Med. 2011; 3:99ra86.
24. Schoeberl B, Faber AC, Li D, Liang MC, Crosby K, Onsum M, Burenkova O, Pace E, Walton Z, Nie L, Fulgham A, Song Y, et al. An ErbB3 antibody, MM-121, is active in cancers with ligand-dependent activation. Cancer Res. 2010; 70:2485-2494.
25. Mendella J, Freemana DJ, Fenga W, Hettmannb T, Schneiderb M, Blumb S, Ruhe J, Bange J, Nakamaru K, Chen S, Tsuchihashi Z, von Pawel J, et al. Clinical translation and validation of a predictive biomarker for patritumab, an anti-human epidermal growth factor receptor 3 (HER3) monoclonal antibody, in patients with advanced non-small cell lung cancer. EBioMedicine. 2015; 2:264-271.
26. Sequist LV, Lopez-Chavez A, Doebele RC, Gray JE, Harb WA, Modiano MR, Jackman DM, Baggstrom MQ, Atmaca A, Felip E, Provencio M, Cobo M, et al. A randomized phase 2 trial of MM-121, a fully human monoclonal antibody targeting ErbB3, in combination with erlotinib in EGFR wildtype NSCLC patients. J Clin Oncol. 2014; 32:5s.
27. Wind S, Schmid M, Erhardt J, Goeldner RG, Stopfer P. Pharmacokinetics of afatinib, a selective irreversible ErbB family blocker, in patients with advanced solid tumours. Clin Pharmacokinet. 2013; 52:1101-1109.
28. Zhang Q, Park E, Kani K, Landgraf R. Functional isolation of activated and unilaterally phosphorylated heterodimers of ERBB2 and ERBB3 as scaffolds in ligand-dependent signaling. Proc Natl Acad Sci USA. 2012; 109:13237-13242.
29. Jura N, Shan Y, Cao X, Shaw DE, Kuriyan J. Structural analysis of the catalytically inactive kinase domain of the human EGF receptor 3. Proc Natl Acad Sci USA. 2009; 106:21608-21613.
30. Soria JC, Felip E, Cobo M, Lu S, Syrigos K, Lee KH, Göker E, Georgoulias V, Li W, Isla D, Guclu SZ, Morabito A, et al. Afatinib versus erlotinib as second-line treatment of patients with advanced squamous cell carcinoma of the lung (LUX-Lung 8): an open-label randomised controlled phase 3 trial. Lancet Oncol. 2015; 16:897-907.