Kinase domain activation of FGFR2 yields high-grade lung adenocarcinoma sensitive to a pan-FGFR inhibitor in a mouse model of NSCLC

Cancer Research

Volumn 74, Issue 17, 2014, Pages 4676-4684

  Tchaicha, Jeremy H ^a,b,c   Akbay, Esra A ^a,b,c   Altabef, Abigail ^a,c   Mikse, Oliver R ^a,b,c   Kikuchi, Eiki ^a,b,c   Rhee, Kevin ^a,c   Liao, Rachel G ^a,d   Bronson, Roderick T ^b   Sholl, Lynette M ^e   Meyerson, Matthew ^a,b,d   Hammerman, Peter S ^a,b,d   Wong, Kwok Kin ^a,b,c,f  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Ludwig Institute for Cancer   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f Belfer Institute for Innovative Cancer Science   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; FGFR2 PROTEIN, HUMAN; FIBROBLAST GROWTH FACTOR RECEPTOR 2; PROTEIN KINASE INHIBITOR; PROTEIN P53;

ADENOCARCINOMA; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; C57BL MOUSE; CARCINOMA, NON-SMALL-CELL LUNG; DISEASE MODEL; DRUG EFFECTS; FEMALE; GENETICS; HUMAN; LUNG NEOPLASMS; MALE; METABOLISM; MOUSE; MUTATION; TRANSGENIC ANIMAL;

ADENOCARCINOMA; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; LUNG NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MUTATION; PROTEIN KINASE INHIBITORS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84907056979     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-3218     Document Type: Article

References (38)

1. Wao H, Mhaskar R, Kumar A, Miladinovic B, Djulbegovic B. Survival of patients with non-small cell lung cancer without treatment: a systematic review and meta-analysis. Syst Rev 2013;2:10.
2. Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med 2008;359:1367-80.
3. Elbauomy Elsheikh S, Green AR, Lambros MB, Turner NC, Grainge MJ, Powe D, et al. FGFR1 amplification in breast carcinomas: a chromo-genic in situ hybridisation analysis. Breast Cancer Res 2007;9:R23.
4. Dutt A, Ramos AH, Hammerman PS, Mermel C, Cho J, Sharifnia T, et al. Inhibitor-sensitive FGFR1 amplification in human non-small cell lung cancer. PLoS One 2011;6:e20351.
5. Tran TN, Selinger CI, Kohonen-Corish MR, McCaughan BC, Kennedy CW, O'Toole SA, et al. Fibroblast growth factor receptor 1 (FGFR1) copy number is an independent prognostic factor in non-small cell lung cancer. Lung Cancer 2013;81:462-7.
6. Schultheis AM, Bos M, Schmitz K, Wilsberg L, Binot E, Wolf J, et al. Fibroblast growth factor receptor 1 (FGFR1) amplification is a potential therapeutic targetin small-cell lung cancer. Mod Pathol 2014;27:214-21.
7. Dutt A, Salvesen HB, Chen TH, Ramos AH, Onofrio RC, Hatton C, et al. Drug-sensitive FGFR2 mutations in endometrial carcinoma. Proc Natl Acad Sci U S A 2008;105:8713-7.
8. Imielinski M, Berger AH, Hammerman PS, Hernandez B, Pugh TJ, Hodis E, et al. Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell 2012;150:1107-20.
9. Cancer Genome Atlas Research N. Comprehensive genomic characterization of squamous cell lung cancers. Nature 2012;489: 519-25.
10. Davies H, Hunter C, Smith R, Stephens P, Greenman C, Bignell G, et al. Somatic mutations of the protein kinase gene family in human lung cancer. Cancer Res 2005;65:7591-5.
11. Jang JH, Shin KH, Park JG. Mutations in fibroblast growth factor receptor 2 and fibroblast growth factor receptor 3 genes associated with human gastric and colorectal cancers. Cancer Res 2001;61: 3541-3.
12. Gust KM, McConkey DJ, Awrey S, Hegarty PK, Qing J, Bondaruk J, et al. Fibroblast growth factor receptor 3 is a rational therapeutic target in bladder cancer. Mol Cancer Ther 2013;12:1245-54.
13. Rosty C, Aubriot MH, Cappellen D, Bourdin J, Cartier I, Thiery JP, et al. Clinical and biological characteristics of cervical neoplasias with FGFR3 mutation. Mol Cancer 2005;4:15.
14. Williams SV, Hurst CD, Knowles MA. Oncogenic FGFR3 gene fusions in bladder cancer. Hum Mol Genet 2013;22:795-803.
15. Kalff A, Spencer A. The t(4;14) translocation and FGFR3 overexpres-sion in multiple myeloma: prognostic implications and current clinical strategies. Blood Cancer J 2012;2:e89.
16. Wu YM, Su F, Kalyana-Sundaram S, Khazanov N, Ateeq B, Cao X, et al. Identification of targetable FGFR gene fusions in diverse cancers. Cancer Discov 2013;3:636-47.
17. Clark JC, Tichelaar JW, Wert SE, Itoh N, Perl AK, Stahlman MT, et al. FGF-10 disrupts lung morphogenesis and causes pulmonary adenomas in vivo. Am J Physiol Lung Cell Mol Physiol 2001;280:L705-15.
18. Tichelaar JW, Lu W, Whitsett JA. Conditional expression of fibroblast growth factor-7 in the developing and mature lung. J Biol Chem 2000;275:11858-64.
19. Zhao B, Chua SS, Burcin MM, Reynolds SD, Stripp BR, Edwards RA, et al. Phenotypic consequences of lung-specific inducible expression of FGF-3. Proc Natl Acad Sci U S A 2001;98:5898-903.
20. Yin Y, Betsuyaku T, Garbow JR, Miao J, Govindan R, Ornitz DM. Rapid induction of lung adenocarcinoma by fibroblast growth factor 9 signaling through FGF receptor 3. Cancer Res 2013;73:5730-41.
21. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, Ornitz DM. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 2006;281:15694-700.
22. Liao RG, Jung J, Tchaicha J, Wilkerson MD, Sivachenko A, Beau-champ EM, et al. Inhibitor-sensitive FGFR2 and FGFR3 mutations in lung squamous cell carcinoma. Cancer Res 2013;73:5195-205.
23. Chen Z, Sasaki T, Tan X, Carretero J, Shimamura T, Li D, et al. Inhibition of ALK, PI3K/MEK, and HSP90 in murinelungadenocarcinomainduced by EML4-ALK fusion oncogene. Cancer Res 2010;70:9827-36.
24. Beard C, Hochedlinger K, Plath K, Wutz A, Jaenisch R. Efficient method to generate single-copy transgenic mice by site-specific integration in embryonic stem cells. Genesis 2006;44:23-8
25. 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 2011; 54:7066-83.
26. Chen Z, Cheng K, Walton Z, Wang Y, Ebi H, Shimamura T, et al. A murine lung cancer co-clinical trial identifies genetic modifiers of therapeutic response. Nature 2012;483:613-7.
27. Kim Y, Hammerman PS, Kim J, Yoon JA, Lee Y, Sun JM, et al. Integrative and comparative genomic analysis of lung squamous cell carcinomas in East Asian patients. J Clin Oncol 2014;32:121-8.
28. Turner N, Grose R. Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 2010;10:116-29.
29. Wakelee H, Belani CP. Optimizing first-line treatment options for patients with advanced NSCLC. Oncologist 2005;10 Suppl 3:1-10.
30. Ji H, Li D, Chen L, Shimamura T, Kobayashi S, McNamara K, et al. The impact of human EGFR kinase domain mutations on lung tumorigen-esis and in vivo sensitivity to EGFR-targeted therapies. Cancer Cell 2006;9:485-95.
31. Dailey L, Ambrosetti D, Mansukhani A, Basilico C. Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev 2005;16:233-47.
32. Jackson EL, Olive KP, Tuveson DA, Bronson R, Crowley D, Brown M, et al. The differential effects of mutant p53 alleles on advanced murine lung cancer. Cancer Res 2005;65:10280-8.
33. Murakami M, Nguyen LT, Zhuang ZW, Moodie KL, Carmeliet P, Stan RV, et al. The FGF system has a key role in regulating vascular integrity. J Clin Invest 2008;118:3355-66.
34. Gotoh N. Control of stemness by fibroblast growth factor signaling in stem cells and cancer stem cells. Curr Stem Cell Res Ther 2009;4:9-15.
35. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006;6: 392-401.
36. Meuwissen R, Berns A. Mouse models for human lung cancer. Genes Dev 2005;19:643-64.
37. Dakir EH, Feigenbaum L, Linnoila RI. Constitutive expression of human keratin 14 gene in mouse lung induces premalignant lesions and squamous differentiation. Carcinogenesis 2008;29:2377-84.
38. Xiao Z, Jiang Q, Willette-Brown J, Xi S, Zhu F, Burkett S, et al. The pivotal role of IKKalpha in the development of spontaneous lung squamous cell carcinomas. Cancer Cell 2013;23:527-40.