Dramatic antitumor effects of the dual MET/RON small-molecule inhibitor LY2801653 in non-small cell lung cancer

Cancer Research

Volumn 74, Issue 3, 2014, Pages 884-895

  Kawada, Ichiro ^a   Hasina, Rifat ^a   Arif, Qudsia ^a   Mueller, Jeffrey ^a   Smithberger, Erin ^a   Husain, Aliya N ^a   Vokes, Everett E ^a   Salgia, Ravi ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; HUMANS; INDAZOLES; LUNG NEOPLASMS; MICE; NIACINAMIDE; PEPTIDES; PROTO-ONCOGENE PROTEINS C-MET; RECEPTOR PROTEIN-TYROSINE KINASES; STAT3 TRANSCRIPTION FACTOR; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84893830885     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-3583     Document Type: Article

References (50)

1. 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.
2. 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.
3. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, et al. Identification of the transforming EML4-ALK fusion gene in nonsmall-cell lung cancer. Nature 2007;448:561-6.
4. Bergethon K, Shaw AT, Ou SH, Katayama R, Lovly CM, McDonald NT, et al. ROS1 rearrangements define a unique molecular class of lung cancers. J Clin Oncol 2012;30:863-70.
5. Sattler M, Reddy MM, Hasina R, Gangadhar T, Salgia R. The role of the c-Met pathway in lung cancer and the potential for targeted therapy. Ther Adv Med Oncol 2011;3:171-84.
6. Sadiq AA, Geynisman DM, Salgia R. Inhibition ofMETreceptor tyrosine kinase and its ligand hepatocyte growth factor. J Thorac Oncol 2011;6: S1810-1.
7. Sattler M, Salgia R. The MET axis as a therapeutic target. Update Cancer Ther 2009;3:109-18.
8. Krishnaswamy S, Kanteti R, Duke-Cohan JS, Loganathan S, Liu W, Ma PC, et al. Ethnic differences and functional analysis of MET mutations in lung cancer. Clin Cancer Res 2009;15:5714-23.
9. Okuda K, Sasaki H, Yukiue H, Yano M, Fujii Y. Met gene copy number predicts the prognosis for completely resected non-small cell lung cancer. Cancer Sci 2008;99:2280-5.
10. Cappuzzo F, Marchetti A, Skokan M, Rossi E, Gajapathy S, Felicioni L, et al. Increased MET gene copy number negatively affects survival of surgically resected non-small-cell lung cancer patients. J Clin Oncol 2009;27:1667-74.
11. GoH, Jeon YK, Park HJ, Sung SW, Seo JW, Chung DH. HighMETgene copy number leads to shorter survival in patients with non-small cell lung cancer. J Thorac Oncol 2010;5:305-13.
12. Kanteti R, Krishnaswamy S, Catenacci D, Tan YH, El-Hashani E, Cervantes G, et al. Differential expression of RON in small and nonsmall cell lung cancers. Genes Chromosomes Cancer 2012;51: 841-51.
13. Zhou YQ, He C, Chen YQ, Wang D, Wang MH. Altered expression of the RON receptor tyrosine kinase in primary human colorectal adenocarcinomas: generation of different splicing RON variants and their oncogenic potential. Oncogene 2003;22:186-97.
14. Zhou D, Pan G, Zheng C, Zheng J, Yian L, Teng X. Expression of the RON receptor tyrosine kinase and its association with gastric carcinoma versus normal gastric tissues. BMC Cancer 2008;8:353.
15. Follenzi A, Bakovic S, Gual P, Stella MC, Longati P, Comoglio PM. Cross-talk between the proto-oncogenes Met and Ron. Oncogene 2000;19:3041-9.
16. Catenacci DV, Cervantes G, Yala S, Nelson EA, El-Hashani E, Kanteti R, et al. RON (MST1R) is a novel prognostic marker and therapeutic target for gastroesophageal adenocarcinoma. Cancer Biol Ther 2011;12:9-46.
17. Wang MH, Padhye SS, Guin S, Ma Q, Zhou YQ. Potential therapeutics specific to c-MET/RON receptor tyrosine kinases for molecular targeting in cancer therapy. Acta Pharmacol Sin 2010;31:1181-8.
18. Sattler M, Pride YB, Ma P, Gramlich JL, Chu SC, Quinnan LA, et al. A novel small molecule met inhibitor induces apoptosis in cells transformed by the oncogenic TPR-MET tyrosine kinase. Cancer Res 2003;63:5462-9.
19. Maulik G, Kijima T, Ma PC, Ghosh SK, Lin J, Shapiro GI, et al. Modulation of the c-Met/hepatocyte growth factor pathway in small cell lung cancer. Clin Cancer Res 2002;8:620-7.
20. Ma PC, Kijima T, Maulik G, Fox EA, Sattler M, Griffin JD, et al. c-MET mutational analysis in small cell lung cancer: novel juxtamembrane domain mutations regulating cytoskeletal functions. Cancer Res 2003;63:6272-81.
21. Versele M, Talloen W, Rockx C, Geerts T, Janssen B, Lavrijssen T, et al. Response prediction to a multitargeted kinase inhibitor in cancer cell lines and xenograft tumors using high-content tyrosine peptide arrays with a kinetic readout. Mol Cancer Ther 2009;8:1846-55.
22. Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, Yao J, et al. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007;11:259-73.
23. Butovsky O, Siddiqui S, Gabriely G, Lanser AJ, Dake B, Murugaiyan G, et al. Modulating inflammatory monocytes with a unique microRNA gene signature ameliorates murine ALS. J Clin Invest 2012;122: 3063-87.
24. Mordant P, Loriot Y, Lahon B, Castier Y, Leseche G, Soria JC, et al. Bioluminescent orthotopic mouse models of human localized nonsmall cell lung cancer: feasibility and identification of circulating tumour cells. PloS ONE 2011;6:e26073.
25. Bertino P, Piccardi F, Porta C, Favoni R, Cilli M, Mutti L, et al. Imatinib mesylate enhances therapeutic effects of gemcitabine in human malignant mesothelioma xenografts. Clin Cancer Res 2008;14:541-8.
26. Jagadeeswaran R, Surawska H, Krishnaswamy S, Janamanchi V, Mackinnon AC, Seiwert TY, et al. Paxillin is a target for somatic mutations in lung cancer: implications for cell growth and invasion. Cancer Res 2008;68:132-42.
27. TanYH, Krishnaswamy S, Nandi S, Kanteti R, Vora S, Onel K, et al. CBL is frequently altered in lung cancers: its relationship to mutations in MET and EGFR tyrosine kinases. PloS ONE 2010;5:e8972.
28. Lo FY, Tan YH, Cheng HC, Salgia R, Wang YC. An E3 ubiquitin ligase: c-Cbl: a new therapeutic target of lung cancer. Cancer 2011;117: 5344-50.
29. Maulik G, Madhiwala P, Brooks S, Ma PC, Kijima T, Tibaldi EV, et al. Activated c-Met signals through PI3K with dramatic effects on cytoskeletal functions in small cell lung cancer. J Cell Mol Med 2002;6: 539-53.
30. Yan SB, Peek VL, Ajamie R, Buchanan SG, Graff JR, Heidler SA, et al. LY2801653 is an orally bioavailable multi-kinase inhibitor with potent activity against MET, MST1R, and other oncoproteins, and displays anti-tumor activities in mouse xenograft models. Invest New Drugs 2013;31:833-44.
31. Ma PC, Tretiakova MS, MacKinnon AC, Ramnath N, Johnson C, Dietrich S, et al. Expression and mutational analysis of MET in human solid cancers. Genes Chromosomes Cancer 2008;47:1025-37.
32. Tretiakova M, Salama AK, Karrison T, Ferguson MK, Husain AN, Vokes EE, et al. MET and phosphorylated MET as potential biomarkers in lung cancer. J Environ Pathol Toxicol Oncol 2011;30:341-54.
33. Eckerich C, Schulte A, Martens T, Zapf S, Westphal M, Lamszus K. RON receptor tyrosine kinase in human gliomas: expression, function, and identification of a novel soluble splice variant. J Neurochem 2009;109:969-80.
34. Ma Q, Zhang K, Yao HP, Zhou YQ, Padhye S, Wang MH. Inhibition of MSP-RON signaling pathway in cancer cells by a novel soluble form of RON comprising the entire sema sequence. Int J Oncol 2010;36: 1551-61.
35. Akervall J, Guo X, Qian CN, Schoumans J, Leeser B, Kort E, et al. Genetic and expression profiles of squamous cell carcinoma of the head and neck correlate with cisplatin sensitivity and resistance in cell lines and patients. Clin Cancer Res 2004;10:8204-13.
36. 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.
37. 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.
38. Suda K, Murakami I, Katayama T, Tomizawa K, Osada H, Sekido Y, et al. Reciprocal and complementary role of MET amplification and EGFR T790M mutation in acquired resistance to kinase inhibitors in lung cancer. Clin Cancer Res 2010;16:5489-98.
39. Catenacci DV, Henderson L, Xiao SY, Patel P, Yauch RL, Hegde P, et al. Durable complete response of metastatic gastric cancer with anti-Met therapy followed by resistance at recurrence. Cancer Discov 2011;1:573-9.
40. Puri N, Salgia R. Synergism of EGFR and c-Met pathways, crosstalk and inhibition, in non-small cell lung cancer. J Carcinog 2008;7:9.
41. Bagai R, Ma PC. Combined treatment with MET inhibitors and other therapies in lung cancer. Transl Lung Cancer Res 2012;1:214-8.
42. Padda S, Neal JW, Wakelee HA. MET inhibitors in combination with other therapies in non-small cell lung cancer. Transl Lung Cancer Res 2012;1:238-53.
43. Menis J, Giaj Levra M, Novello S. MET inhibition in lung cancer. Transl Lung Cancer Res 2013;2:23-39.
44. Scagliotti GV, Novello S, Schiller JH, Hirsh V, Sequist LV, Soria JC, et al. Rationale and design of MARQUEE: a phase III, randomized, doubleblind study of tivantinib plus erlotinib versus placebo plus erlotinib in previously treated patients with locally advanced or metastatic, nonsquamous, non-small-cell lung cancer. Clin Lung Cancer 2012;13: 391-5.
45. ArQule II. Woburn, MA: ArQule, Inc.; [cited 2012 Oct 2]. Available from: http://investors.arqule.com/releasedetail.cfm?ReleaseID=710618.
46. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, et al. Stat3 as an oncogene. Cell 1999;98:295-303.
47. Bowman T, Garcia R, Turkson J, Jove R. STATs in oncogenesis. Oncogene 2000;19:2474-88.
48. Gherardi E, Birchmeier W, Birchmeier C, Vande Woude G. Targeting MET in cancer: rationale and progress. Nat Rev Cancer 2012;12: 89-103.
49. Whiteside TL. The tumor microenvironment and its role in promoting tumor growth. Oncogene 2008;27:5904-12.
50. Teicher BA. Tumor models for efficacy determination. Mol Cancer Ther 2006;5:2435-43.