Antitumor effect of FGFR inhibitors on a novel cholangiocarcinoma patient derived xenograft mouse model endogenously expressing an FGFR2-CCDC6 fusion protein

Cancer Letters

Volumn 380, Issue 1, 2016, Pages 163-173

  Wang, Yu ^a,b   Ding, Xiwei ^b,c   Wang, Shaoqing ^b,d   Moser, Catherine D ^b   Shaleh, Hassan M ^b   Mohamed, Essa A ^b   Chaiteerakij, Roongruedee ^b   Allotey, Loretta K ^b   Chen, Gang ^b   Miyabe, Katsuyuki ^b   McNulty, Melissa S ^e   Ndzengue, Albert ^b   Barr Fritcher, Emily G ^f   Knudson, Ryan A ^f   Greipp, Patricia T ^f   Clark, Karl J ^e   Torbenson, Michael S ^f   Kipp, Benjamin R ^f   Zhou, Jie ^a   Barrett, Michael T ^g   Gustafson, Michael P ^f   Alberts, Steven R ^f   Borad, Mitesh J ^g   Roberts, Lewis R ^b   more..

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b MAYO CLINIC   (United States)

^c THE AFFILIATED DRUM TOWER HOSPITAL OF NANJING UNIVERSITY MEDICAL SCHOOL   (China)

^d QIQIHAR MEDICAL UNIVERSITY   (China)

^e MAYO GRADUATE SCHOOL   (United States)

^f Mayo Clinic   (United States)

^g MAYO CLINIC   (United States)

Author keywords

BGJ398; Dovitinib; FGFR2 fusion; Intrahepatic cholangiocarcinoma; Ponatinib

Indexed keywords

CCDC6 PROTEIN; CISPLATIN; DOVITINIB; FIBROBLAST GROWTH FACTOR RECEPTOR 2; GELATINASE A; GELATINASE B; GEMCITABINE; HYBRID PROTEIN; INFIGRATINIB; ONCOPROTEIN; PONATINIB; STROMELYSIN; UNCLASSIFIED DRUG; 3-(2,6-DICHLORO-3,5-DIMETHOXYPHENYL)-1-(6-(4-(4-ETHYLPIPERAZIN-1-YL)-PHENYLAMINO)PYRIMIDIN-4-YL)-1-METHYLUREA; 4-AMINO-5-FLUORO-3-(5-(4-METHYLPIPERAZIN-1-YL)-1H-BENZIMIDAZOL-2-YL)QUINOLIN-2(1H)-ONE; ANTINEOPLASTIC AGENT; BENZIMIDAZOLE DERIVATIVE; CARBANILAMIDE DERIVATIVE; CCDC6 PROTEIN, HUMAN; CYTOSKELETON PROTEIN; FGFR2 PROTEIN, HUMAN; IL2RG PROTEIN, MOUSE; IMIDAZOLE DERIVATIVE; INTERLEUKIN 2 RECEPTOR GAMMA; MMP2 PROTEIN, HUMAN; MMP3 PROTEIN, HUMAN; MMP9 PROTEIN, HUMAN; PYRIDAZINE DERIVATIVE; PYRIMIDINE DERIVATIVE; QUINOLONE DERIVATIVE;

ADVERSE OUTCOME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BILE DUCT CARCINOMA; CANCER COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG DOSE REDUCTION; DRUG EFFECT; DRUG POTENCY; DRUG POTENTIATION; ENZYME ANALYSIS; FEMALE; INTRACELLULAR SIGNALING; LUNG METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; BILE DUCT NEOPLASMS; CELL PROLIFERATION; CHOLANGIOCARCINOMA; COMPARATIVE STUDY; DEFICIENCY; DRUG EFFECTS; DRUG SCREENING; GENE FUSION; GENETICS; HUMAN; KNOCKOUT MOUSE; LUNG NEOPLASMS; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; SECONDARY; SIGNAL TRANSDUCTION; TIME FACTOR; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZIMIDAZOLES; BILE DUCT NEOPLASMS; CELL PROLIFERATION; CHOLANGIOCARCINOMA; CYTOSKELETAL PROTEINS; GENE FUSION; HUMANS; IMIDAZOLES; INTERLEUKIN RECEPTOR COMMON GAMMA SUBUNIT; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 3; MATRIX METALLOPROTEINASE 9; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; PHENYLUREA COMPOUNDS; PYRIDAZINES; PYRIMIDINES; QUINOLONES; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; SIGNAL TRANSDUCTION; TIME FACTORS; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84976531382     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2016.05.017     Document Type: Article

References (38)

1. [1] von Hahn, T., Ciesek, S., Wegener, G., Plentz, R.R., Weismuller, T.J., Wedemeyer, H., et al. Epidemiological trends in incidence and mortality of hepatobiliary cancers in Germany. Scand. J. Gastroenterol 46 (2011), 1092–1098.
2. [2] Yang, J.D., Kim, B., Sanderson, S.O., Sauver, J.S., Yawn, B.P., Larson, J.J., et al. Biliary tract cancers in Olmsted County, Minnesota, 1976–2008. Am. J. Gastroenterol 107 (2012), 1256–1262.
3. [3] Bertuccio, P., Bosetti, C., Levi, F., Decarli, A., Negri, E., La Vecchia, C., A comparison of trends in mortality from primary liver cancer and intrahepatic cholangiocarcinoma in Europe. Ann. Oncol 24 (2013), 1667–1674.
4. [4] Njei, B., Changing pattern of epidemiology in intrahepatic cholangiocarcinoma. Hepatology 60 (2014), 1107–1108.
5. [5] Pinter, M., Hucke, F., Zielonke, N., Waldhor, T., Trauner, M., Peck-Radosavljevic, M., et al. Incidence and mortality trends for biliary tract cancers in Austria. Liver Int 34 (2014), 1102–1108.
6. [6] Rizvi, S., Gores, G.J., Pathogenesis, diagnosis, and management of cholangiocarcinoma. Gastroenterology 145 (2013), 1215–1229.
7. [7] Razumilava, N., Gores, G.J., Cholangiocarcinoma. Lancet 383 (2014), 2168–2179.
8. [8] Valle, J., Wasan, H., Palmer, D.H., Cunningham, D., Anthoney, A., Maraveyas, A., et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N. Engl. J. Med 362 (2010), 1273–1281.
9. [9] Sandhu, D.S., Baichoo, E., Roberts, L.R., Fibroblast growth factor signaling in liver carcinogenesis. Hepatology 59 (2014), 1166–1173.
10. [10] Parker, B.C., Engels, M., Annala, M., Zhang, W., Emergence of FGFR family gene fusions as therapeutic targets in a wide spectrum of solid tumours. J. Pathol 232 (2014), 4–15.
11. [11] Borad, M.J., Gores, G.J., Roberts, L.R., Fibroblast growth factor receptor 2 fusions as a target for treating cholangiocarcinoma. Curr. Opin. Gastroenterol 31 (2015), 264–268.
12. [12] Wu, Y.M., Su, F., Kalyana-Sundaram, S., Khazanov, N., Ateeq, B., Cao, X., et al. Identification of targetable FGFR gene fusions in diverse cancers. Cancer Discov 3 (2013), 636–647.
13. [13] Arai, Y., Totoki, Y., Hosoda, F., Shirota, T., Hama, N., Nakamura, H., et al. Fibroblast growth factor receptor 2 tyrosine kinase fusions define a unique molecular subtype of cholangiocarcinoma. Hepatology 59 (2014), 1427–1434.
14. [14] Borad, M.J., Champion, M.D., Egan, J.B., Liang, W.S., Fonseca, R., Bryce, A.H., et al. Integrated genomic characterization reveals novel, therapeutically relevant drug targets in FGFR and EGFR pathways in sporadic intrahepatic cholangiocarcinoma. PLoS Genet, 10, 2014, e1004135.
15. [15] Graham, R.P., Barr Fritcher, E.G., Pestova, E., Schulz, J., Sitailo, L.A., Vasmatzis, G., et al. Fibroblast growth factor receptor 2 translocations in intrahepatic cholangiocarcinoma. Hum. Pathol 45 (2014), 1630–1638.
16. [16] Ross, J.S., Wang, K., Gay, L., Al-Rohil, R., Rand, J.V., Jones, D.M., et al. New routes to targeted therapy of intrahepatic cholangiocarcinomas revealed by next-generation sequencing. Oncologist 19 (2014), 235–242.
17. [17] Sia, D., Losic, B., Moeini, A., Cabellos, L., Hao, K., Revill, K., et al. Massive parallel sequencing uncovers actionable FGFR2-PPHLN1 fusion and ARAF mutations in intrahepatic cholangiocarcinoma. Nat. Commun, 6, 2015, 6087.
18. [18] Ang, C., Role of the fibroblast growth factor receptor axis in cholangiocarcinoma. J. Gastroenterol. Hepatol 30 (2015), 1116–1122.
19. [19] O'Hare, T., Shakespeare, W.C., Zhu, X., Eide, C.A., Rivera, V.M., Wang, F., et al. AP24534, a pan-BCR-ABL inhibitor for chronic myeloid leukemia, potently inhibits the T315I mutant and overcomes mutation-based resistance. Cancer Cell 16 (2009), 401–412.
20. [20] Gozgit, J.M., Wong, M.J., Moran, L., Wardwell, S., Mohemmad, Q.K., Narasimhan, N.I., et al. Ponatinib (AP24534), a multitargeted pan-FGFR inhibitor with activity in multiple FGFR-amplified or mutated cancer models. Mol. Cancer Ther 11 (2012), 690–699.
21. [21] Sivanand, S., Pena-Llopis, S., Zhao, H., Kucejova, B., Spence, P., Pavia-Jimenez, A., et al. A validated tumorgraft model reveals activity of dovitinib against renal cell carcinoma. Sci. Transl. Med, 4, 2012, 137ra175.
22. [22] Guagnano, V., Furet, P., Spanka, C., Bordas, V., Le Douget, M., Stamm, C., et al. Discovery of 3-(2,6-dichloro-3,5-dimethoxy-phenyl)-1-{6-[4-(4-ethyl-piperazin-1-yl)-phenylamin o]-pyrimidin-4-yl}-1-methyl-urea (NVP-BGJ398), a potent and selective inhibitor of the fibroblast growth factor receptor family of receptor tyrosine kinase. J. Med. Chem 54 (2011), 7066–7083.
23. [23] Guagnano, V., Kauffmann, A., Wohrle, S., Stamm, C., Ito, M., Barys, L., et al. FGFR genetic alterations predict for sensitivity to NVP-BGJ398, a selective pan-FGFR inhibitor. Cancer Discov 2 (2012), 1118–1133.
24. [24] Huang, D., Ding, Y., Luo, W.M., Bender, S., Qian, C.N., Kort, E., et al. Inhibition of MAPK kinase signaling pathways suppressed renal cell carcinoma growth and angiogenesis in vivo. Cancer Res 68 (2008), 81–88.
25. [25] Yang, X., Liang, L., Zhang, X.F., Jia, H.L., Qin, Y., Zhu, X.C., et al. MicroRNA-26a suppresses tumor growth and metastasis of human hepatocellular carcinoma by targeting interleukin-6-Stat3 pathway. Hepatology 58 (2013), 158–170.
26. [26] Angevin, E., Lopez-Martin, J.A., Lin, C.C., Gschwend, J.E., Harzstark, A., Castellano, D., et al. Phase I study of dovitinib (TKI258), an oral FGFR, VEGFR, and PDGFR inhibitor, in advanced or metastatic renal cell carcinoma. Clin. Cancer Res 19 (2013), 1257–1268.
27. [27] Stetler-Stevenson, W.G., The tumor microenvironment: regulation by MMP-independent effects of tissue inhibitor of metalloproteinases-2. Cancer Metastasis Rev 27 (2008), 57–66.
28. [28] Elewa, M.A., Al-Gayyar, M.M., Schaalan, M.F., Abd El Galil, K.H., Ebrahim, M.A., El-Shishtawy, M.M., Hepatoprotective and anti-tumor effects of targeting MMP-9 in hepatocellular carcinoma and its relation to vascular invasion markers. Clin. Exp. Metastasis 32 (2015), 479–493.
29. [29] Ardi, V.C., Van den Steen, P.E., Opdenakker, G., Schweighofer, B., Deryugina, E.I., Quigley, J.P., Neutrophil MMP-9 proenzyme, unencumbered by TIMP-1, undergoes efficient activation in vivo and catalytically induces angiogenesis via a basic fibroblast growth factor (FGF-2)/FGFR-2 pathway. J. Biol. Chem 284 (2009), 25854–25866.
30. [30] Pintucci, G., Yu, P.J., Sharony, R., Baumann, F.G., Saponara, F., Frasca, A., et al. Induction of stromelysin-1 (MMP-3) by fibroblast growth factor-2 (FGF-2) in FGF-2-/- microvascular endothelial cells requires prolonged activation of extracellular signal-regulated kinases-1 and -2 (ERK-1/2). J. Cell. Biochem 90 (2003), 1015–1025.
31. [31] Williams, S.V., Hurst, C.D., Knowles, M.A., Oncogenic FGFR3 gene fusions in bladder cancer. Hum. Mol. Genet 22 (2013), 795–803.
32. [32] Singh, D., Chan, J.M., Zoppoli, P., Niola, F., Sullivan, R., Castano, A., et al. Transforming fusions of FGFR and TACC genes in human glioblastoma. Science 337 (2012), 1231–1235.
33. [33] Chase, A., Bryant, C., Score, J., Cross, N.C., Ponatinib as targeted therapy for FGFR1 fusions associated with the 8p11 myeloproliferative syndrome. Haematologica 98 (2013), 103–106.
34. [34] Ren, M., Qin, H., Ren, R., Cowell, J.K., Ponatinib suppresses the development of myeloid and lymphoid malignancies associated with FGFR1 abnormalities. Leukemia 27 (2013), 32–40.
35. [35] Wynes, M.W., Hinz, T.K., Gao, D., Martini, M., Marek, L.A., Ware, K.E., et al. FGFR1 mRNA and protein expression, not gene copy number, predict FGFR TKI sensitivity across all lung cancer histologies. Clin. Cancer Res 20 (2014), 3299–3309.
36. [36] Damaraju, V.L., Kuzma, M., Mowles, D., Cass, C.E., Sawyer, M.B., Interactions of multitargeted kinase inhibitors and nucleoside drugs: Achilles heel of combination therapy?. Mol. Cancer Ther 14 (2015), 236–245.
37. [37] Onesti, C.E., Romiti, A., Roberto, M., Falcone, R., Marchetti, P., Recent advances for the treatment of pancreatic and biliary tract cancer after first-line treatment failure. Expert Rev. Anticancer Ther 15 (2015), 1183–1198.
38. [38] Trudel, S., Li, Z.H., Wei, E., Wiesmann, M., Chang, H., Chen, C., et al. CHIR-258, a novel, multitargeted tyrosine kinase inhibitor for the potential treatment of t(4;14) multiple myeloma. Blood 105 (2005), 2941–2948.