Discovery and biological evaluation of novel dual EGFR/c-Met inhibitors

ACS Medicinal Chemistry Letters

Volumn 5, Issue 4, 2014, Pages 298-303

  Szokol, Bálint ^a   Gyulavári, Pál ^b   Kurkó, Ibolya ^a   Baska, Ferenc ^a,b   Szántai Kis, Csaba ^a   Greff, Zoltán ^a   Orfi, Zoltán ^b,c   Peták, István ^b,d   Pénzes, Kinga ^c   Torka, Robert ^c   Ullrich, Axel ^c   Orfi, László ^a,b   Vántus, Tibor ^b   Kéri, György ^a,b  

^a Vichem Chemie Research Ltd   (Hungary)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^d KPS Medical Biotechnology and Healthcare Services Ltd   (Hungary)

Author keywords

acquired resistance; c Met; EGFR; kinase inhibitor; NSCLC

Indexed keywords

AFATINIB; ANTINEOPLASTIC AGENT; BMS 777607; CRIZOTINIB; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ERLOTINIB; N [ 4 (QUINOLONE 4 YLOXY) PHENYL BIARYSULFONAMIDE DERIVATIVE; SULFONAMIDE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL DEATH; CELL MOTILITY; CELL VIABILITY; DRUG SYNTHESIS; ENZYMATIC ASSAY; ENZYME ACTIVITY; GENE AMPLIFICATION; GENE MUTATION; HYDROGEN BOND; HYDROGENATION; KINETICS; LUNG NON SMALL CELL CANCER; MICROWAVE IRRADIATION; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; WILD TYPE;

EID: 84898034287     PISSN: None     EISSN: 19485875     Source Type: Journal    
DOI: 10.1021/ml4003309     Document Type: Article

References (33)

1. Lynch, T. J.; Adjei, A. A.; Bunn, P. A., Jr.; Eisen, T. G.; Engelman, J.; Goss, G. D.; Haber, D. A.; Heymach, J. V.; Jänne, P. A.; Johnson, B. E.; Johnson, D. H.; Lilenbaum, R. C.; Meyerson, M.; Sandler, A. B.; Sequist, L. V.; Settleman, J.; Wong, K. K.; Hart, C. S. Summary statement: novel agents in the treatment of lung cancer: advances in epidermal growth factor receptor-targeted agents Clin. Cancer Res. 2006, 12, 4365-4371
2. Mendelsohn, J.; Baselga, J. The EGF receptor family as targets for cancer therapy Oncogene 2000, 19, 6550-6565
3. Paez, J. G.; Jänne, P. A.; Lee, J. C.; Tracy, S.; Greulich, H.; Gabriel, S.; Herman, P.; Kaye, F. J.; Lindeman, N.; Boggon, T. J.; Naoki, K.; Sasaki, H.; Fujii, Y.; Eck, M. J.; Sellers, W. R.; Johnson, B. E.; Meyerson, M. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy Science 2004, 304, 1497-1500
4. Sordella, R.; Bell, D. W.; Haber, D. A.; Settleman, J. Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways Science 2004, 305, 1163-1167
5. Lynch, T. J.; Bell, D. W.; Sordella, R.; Gurubhagavatula, S.; Okimoto, R. A.; Brannigan, B. W.; Harris, P. L.; Haserlat, S. M.; Supko, J. G.; Haluska, F. G.; Louis, D. N.; Christiani, D. C.; Settleman, J.; Haber, D. A. 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
6. Pao, W.; Miller, V. A.; Politi, K. A.; Riely, G. J.; Somwar, R.; Zakowski, M. F.; Kris, M. G.; Varmus, H. 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
7. Kobayashi, S.; Boggon, T. J.; Dayaram, T.; Jänne, P. A.; Kocher, O.; Meyerson, M.; Johnson, B. E.; Eck, M. J.; Tenen, D. G.; Halmos, B. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib N. Engl. J. Med. 2005, 352, 786-792
8. Kosaka, T.; Yatabe, Y.; Endoh, H.; Yoshida, K.; Hida, T.; Tsuboi, M.; Tada, H.; Kuwano, H.; Mitsudomi, T. Analysis of epidermal growth factor receptor gene mutation in patients with non-small cell lung cancer and acquired resistance to gefitinib Clin. Cancer Res. 2006, 12, 5764-5769
9. Balak, M. N.; Gong, Y.; Riely, G. J.; Somwar, R.; Li, A. R.; Zakowski, M. F.; Chiang, A.; Yang, G.; Ouerfelli, O.; Kris, M. G.; Ladanyi, M.; Miller, V. A.; Pao, W. Novel D761Y and common secondary T790M mutations in epidermal growth factor receptor-mutant lung adenocarcinomas with acquired resistance to kinase inhibitors Clin. Cancer Res. 2006, 12, 6494-6501
10. Looyenga, B. D.; Cherni, I.; Mackeigan, J. P.; Weiss, G. J. Tailoring tyrosine kinase inhibitors to fit the lung cancer genome Transl. Oncol. 2011, 4, 59-70
11. Stella, M. C.; Comoglio, P. M. HGF: a multifunctional growth factor controlling cell scattering Int. J. Biochem. Cell Biol. 1999, 31, 1357-1362
12. Engelman, J. A.; Zejnullahu, K.; Mitsudomi, T.; Song, Y.; Hyland, C.; Park, J. O.; Lindeman, N.; Gale, C. M.; Zhao, X.; Christensen, J.; Kosaka, T.; Holmes, A. J.; Rogers, A. M.; Cappuzzo, F.; Mok, T.; Lee, C.; Johnson, B. E.; Cantley, L. C.; Jänne, P. A. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling Science 2007, 316, 1039-43
13. Bean, J.; Brennan, C.; Shih, J. Y.; Riely, G.; Viale, A.; Wang, L.; Chitale, D.; Motoi, N.; Szoke, J.; Broderick, S.; Balak, M.; Chang, W. C.; Yu, C. J.; Gazdar, A.; Pass, H.; Rusch, V.; Gerald, W.; Huang, S. F.; Yang, P. C.; Miller, V.; Ladanyi, M.; Yang, C. H.; Pao, W. MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 20932-20937
14. Tang, Z.; Du, R.; Jiang, S.; Wu, C.; Barkauskas, D. S.; Richey, J.; Molter, J.; Lam, M.; Flask, C.; Gerson, S.; Dowlati, A.; Liu, L.; Lee, Z.; Halmos, B.; Wang, Y.; Kern, J. A.; Ma, P. C. Dual MET-EGFR combinatorial inhibition against T790M-EGFR-mediated erlotinib-resistant lung cancer Br. J. Cancer 2008, 99, 911-922
15. Chen, H. J.; Jiang, Y. L.; Lin, C. M.; Tsai, S. C.; Peng, S. F; Fushiya, S.; Hour, M. J.; Yang, J. S. Dual inhibition of EGFR and c-Met kinase activation by MJ-56 reduces metastasis of HT29 human colorectal cancer cells Int. J. Oncol. 2013, 43, 141-50
16. Liu, X.; Newton, R. C.; Scherle, A. P. Development of c-MET pathway inhibitors Expert Opin. Investig. Drugs 2011, 20, 1225-1241
17. Kao, H. F.; Lin, C. C.; Yang, J. C. EGFR inhibitors as the first-line systemic treatment for advanced non-small-cell lung cancer Future Oncol. 2013, 9, 991-1003
18. Mollard, A.; Warner, S. L.; Call, L. T.; Wade, M. L.; Bearss, J. J.; Verma, A.; Sharma, S.; Vankayalapati, H.; Bearss, D. J. Design, synthesis, and biological evaluation of a series of novel AXL kinase inhibitors ACS Med. Chem. Lett. 2011, 2 (12) 907-912
19. D'Angelo, N. D.; Bellon, S. F.; Booker, S. K.; Cheng, Y.; Coxon, A.; Dominguez, C.; Fellows, I.; Hoffman, D.; Hungate, R.; Kaplan-Lefko, P.; Lee, M. R.; Li, C.; Liu, L.; Rainbeau, E.; Reider, P. J.; Rex, K.; Siegmund, A.; Sun, Y.; Tasker, A. S.; Xi, N.; Xu, S.; Yang, Y.; Zhang, Y.; Burgess, T. L.; Dussault, I.; Kim, T. S. Design, synthesis, and biological evaluation of potent c-Met inhibitors J. Med. Chem. 2008, 51, 5766-79
20. Li, S.; Zhao, Y.; Wang, K.; Gao, Y.; Han, J.; Cui, B.; Gong, P. Discovery of novel 4-(2-fluorophenoxy)quinoline derivatives bearing 4-oxo-1,4- dihydrocinnoline-3-carboxamide moiety as c-Met kinase inhibitors Bioorg. Med. Chem. 2013, 21, 2843-2855
21. Furlan, A.; Colombo, F.; Kover, A.; Issaly, N.; Tintori, C.; Angeli, L.; Leroux, V.; Letard, S.; Amat, M.; Asses, Y.; Maigret, B.; Dubreuil, P.; Botta, M.; Dono, R.; Bosch, J.; Piccolo, O.; Passarella, D.; Maina, F. Identification of new aminoacid amides containing the imidazo[2,1-b]benzothiazol-2-ylphenyl moiety as inhibitors of tumorigenesis by oncogenic Met signaling Eur. J. Med. Chem. 2012, 47, 239-54
22. Cai, Z. W.; Wei, D.; Schroeder, G. M.; Cornelius, L. A.; Kim, K.; Chen, X. T.; Schmidt, R. J.; Williams, D. K.; Tokarski, J. S.; An, Y.; Sack, J. S.; Manne, V.; Kamath, A.; Zhang, Y.; Marathe, P.; Hunt, J. T.; Lombardo, L. J.; Fargnoli, J.; Borzilleri, R. M. Discovery of orally active pyrrolopyridine- and aminopyridine-based Met kinase inhibitors Bioorg. Med. Chem. Lett. 2008, 18, 3224-3229
23. Li, S.; Huang, Q.; Liu, Y.; Zhang, X.; Liu, S.; He, C.; Gong, P. Design, synthesis and antitumour activity of bisquinoline derivatives connected by 4-oxy-3-fluoroaniline moiety Eur. J. Med. Chem. 2013, 64, 62-73
24. Li, J.; Wu, N.; Tian, Y.; Zhang, J.; Wu, S. Aminopyridyl/pyrazinyl spiro[indoline-3,4′-piperidine]-2-ones as highly selective and efficacious c-Met/ALK inhibitors ACS Med. Chem. Lett. 2013, 4, 806-810
25. Qian, F.; Engst, S.; Yamaguchi, K.; Yu, P.; Won, K. A.; Mock, L.; Lou, T.; Tan, J.; Li, C.; Tam, D.; Lougheed, J.; Yakes, F. M.; Bentzien, F.; Xu, W.; Zaks, T.; Wooster, R.; Greshock, J.; Joly, A. H. 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. 2009, 69, 8009-8016
26. Schroeder, G. M.; An, Y.; Cai, Z. W.; Chen, X. T.; Clark, C.; Cornelius, L. A.; Dai, J.; Gullo-Brown, J.; Gupta, A.; Henley, B.; Hunt, J. T.; Jeyaseelan, R.; Kamath, A.; Kim, K.; Lippy, J.; Lombardo, L. J.; Manne, V.; Oppenheimer, S.; Sack, J. S.; Schmidt, R. J.; Shen, G.; Stefanski, K.; Tokarski, J. S.; Trainor, G. L.; Wautlet, B. S.; Wei, D.; Williams, D. K.; Zhang, Y.; Zhang, Y.; Fargnoli, J.; Borzilleri, R. M. Discovery of N -(4-(2-amino-3-chloropyridin-4- yloxy)-3-fluorophenyl)-4-ethoxy-1-(4-fluorophenyl)-2-oxo-1,2-dihydropyridine-3- carboxamide (BMS-777607), a selective and orally efficacious inhibitor of the Met kinase superfamily J. Med. Chem. 2009, 52, 1251-1254
27. Timofeevski, S. L.; McTigue, M. A.; Ryan, K.; Cui, J.; Zou, H. Y.; Zhu, J. X.; Chau, F.; Alton, G.; Karlicek, S.; Christensen, J. G.; Murray, B. W. Enzymatic characterization of c-Met receptor tyrosine kinase oncogenic mutants and kinetic studies with aminopyridine and triazolopyrazine inhibitors Biochemistry 2009, 48, 5339-5349
28. Moyer, J. D.; Barbacci, E. G.; Iwata, K. K; Arnold, L.; Boman, B.; Cunningham, A.; DiOrio, C.; Doty, J.; Morin, M. J.; Moyer, M. P.; Neveu, M.; Pollack, V. A.; Pustilnik, L. R.; Reynolds, M. M.; Sloan, D.; Theleman, A.; Miller, P. Induction of apoptosis and cell cycle arrest by CP-358,774, an inhibitor of epidermal growth factor receptor tyrosine kinase Cancer Res. 1997, 57, 4838-4848
29. Reid, A.; Vidal, L.; Shaw, H.; de Bono, J. Dual inhibition of ErbB1 (EGFR/HER1) and ErbB2 (HER2/neu) Eur. J. Cancer 2007, 43, 481-489
30. Krypuy, M.; Newnham, G. M.; Thomas, D. M.; Conron, M.; Dobrovic, A. High resolution melting analysis for the rapid and sensitive detection of mutations in clinical samples: KRAS codon 12 and 13 mutations in non-small cell lung cancer BMC Cancer 2006, 6, 295
31. Suda, K.; Tomizawa, K.; Mitsudomi, T. Biological and clinical significance of KRAS mutations in lung cancer: an oncogenic driver that contrasts with EGFR mutation Cancer Metastasis Rev. 2010, 29, 49-60
32. Patané, S.; Pietrancosta, N.; Hassani, H.; Leroux, V.; Maigret, B.; Kraus, J. L.; Dono, R.; Maina, F. A new Met inhibitory-scaffold identified by a focused forward chemical biological screen Biochem. Biophys. Res. Commun. 2008, 375, 184-189
33. Fram, S. T.; Wells, C. M.; Jones, G. E. HGF-induced DU145 cell scatter assay Methods Mol. Biol. 2011, 769, 31-40