Parallel RNA interference screens identify EGFR activation as an escape mechanism in FGFR3-mutant cancer

Cancer Discovery

Volumn 3, Issue 9, 2013, Pages 1058-1071

  Herrera Abreu, Maria Teresa ^a   Pearson, Alex ^a   Campbell, James ^a   Shnyder, Steve D ^c   Knowles, Margaret A ^d   Ashworth, Alan ^a   Turner, Nicholas C ^a,b  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b ROYAL MARSDEN HOSPITAL   (United Kingdom)

^c UNIVERSITY OF BRADFORD   (United Kingdom)

^d ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1 TERT BUTYL 3 [6 (3, 5 DIMETHOXYPHENYL) 2 (4 DIETHYLAMINOBUTYLAMINO) PYRIDO [2, 3 D] PYRIMIDIN 7 YL] UREA; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 3; GEFITINIB; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLADDER CANCER; CELL VIABILITY; CLONOGENIC ASSAY; CONTROLLED STUDY; FOLLOW UP; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; MOUSE; NEOPLASM; NONHUMAN; POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; RECEPTOR SENSITIVITY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR VOLUME; TUMOR XENOGRAFT; WESTERN BLOTTING;

ANIMALS; CELL LINE, TUMOR; HETEROGRAFTS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; NEOPLASM TRANSPLANTATION; NEOPLASMS; PROTEIN KINASE INHIBITORS; PYRIMIDINES; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 3; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; THIAZOLES;

EID: 84885229945     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-12-0569     Document Type: Article

References (45)

1. Cappellen D, De Oliveira C, Ricol D, de Medina S, Bourdin J, Saster-Garau X, et al. Frequent activating mutations of FGFR3 in human bladder and cervix carcinomas. Nat Genet 1999; 23: 18-20
2. Pollock PM, Gartside MG, Dejeza LC, Powell MA, Mallon MA, Davies H, et al. Frequent activating FGFR2 mutations in endometrial carcinomas parallel germline mutations associated with craniosynostosis and skeletal dysplasia syndromes. Oncogene 2007; 26: 7158-62
3. 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
4. Courjal F, Cuny M, Simony-Lafontaine J, Louason G, Speiser P, Zeillinger R, et al. Mapping of DNA amplifications at 15 chromosomal localizations in 1875 breast tumors: definition of phenotypic groups Cancer Res 1997; 57: 4360-7
5. Weiss J, Sos ML, Seidel D, Peifer M, Zander T, Heuckmann JM, et al. Frequent and focal FGFR1 amplifi cation associates with therapeutically tractable FGFR1 dependency in squamous cell lung cancer. Sci Transl Med 2010; 2: 62ra93
6. Kunii K, Davis L, Gorenstein J, Hatch H, Yashiro M, Di Bacco A, et al. FGFR2-amplifi ed gastric cancer cell lines require FGFR2 and Erbb3 signaling for growth and survival. Cancer Res 2008; 68: 2340-8
7. Heiskanen M, Kononen J, Barlund M, Torhorst J, Sauter G, Kallioniemi A, et al. CGH, cDNA and tissue microarray analyses implicate FGFR2 amplifi cation in a small subset of breast tumors. Anal Cell Pathol 2001; 22: 229-34
8. Singh D, Chan JM, Zoppoli P, Niola F, Sullivan R, Castano A, et al. Transforming fusions of FGFR and TACC genes in human glioblastoma. Science 2012; 337: 1231-5
9. 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
10. Turner N, Grose R. Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 2010; 10: 116-29
11. Turner N, Lambros MB, Horlings HM, Pearson A, Sharpe R, Natrajan R, et al. Integrative molecular profi ling of triple negative breast cancers identifi es amplicon drivers and potential therapeutic targets. Oncogene 2010; 29: 2013-23
12. Tannheimer SL, Rehemtulla A, Ethier SP. Characterization of fi broblast growth factor receptor 2 overexpression in the human breast cancer cell line SUM-52PE. Breast Cancer Res 2000; 2: 311-20
13. Lamont FR, Tomlinson DC, Cooper PA, Shnyder SD, Chester JD, Knowles MA. Small molecule FGF receptor inhibitors block FGFRdependent urothelial carcinoma growth in vitro and in vivo. Br J Cancer 2011; 104: 75-82
14. Andre F, Bachelot TD, Campone M, Dalenc F, Perez-Garcia JM, Hurvitz SA, et al. Targeting FGFR with dovitinib (TKI258): Preclinical and clinical data in breast cancer. Clin Cancer Res 2013; 19: 3693-702
15. Soria JC, Dienstmann R, de Braud F, Cereda R, Bahleda R, Hollebecque A, et al. First-in-man study of E-3810, a novel VEGFR and FGFR inhibitor, in patients with advanced solid tumors. Ann Oncol 2012; 23: L2.5
16. Berns K, Horlings HM, Hennessy BT, Madiredjo M, Hijmans EM, Beelen K, et al. A functional genetic approach identifi es the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 2007; 12: 395-402
17. Prahallad A, Sun C, Huang S, Di Nicolantonio F, Salazar R, Zecchin D, et al. Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature 2012; 483: 100-3
18. Turner NC, Lord CJ, Iorns E, Brough R, Swift S, Elliott R, et al. A synthetic lethal siRNA screen identifying genes mediating sensitivity to a PARP inhibitor. EMBO J 2008; 27: 1368-77
19. Avraham R, Yarden Y. Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat Rev Mol Cell Biol 2011; 12: 104-17
20. Wang Z, Wang M, Lazo JS, Carr BI. Identifi cation of epidermal growth factor receptor as a target of Cdc25A protein phosphatase. J Biol Chem 2002; 277: 19470-5
21. Wang R, He G, Nelman-Gonzalez M, Ashorn CL, Gallick GE, Stukenberg PT, et al. Regulation of Cdc25C by ERK-MAP kinases during the G2 /M transition. Cell 2007; 128: 1119-32
22. Naski MC, Wang Q, Xu J, Ornitz DM. Graded activation of fi broblast growth factor receptor 3 by mutations causing achondroplasia and thanatophoric dysplasia. Nat Genet 1996; 13: 233-7
23. Rousseau F, el Ghouzzi V, Delezoide A L, Legeai-Mallet L, Le Merrer M, Munnich A, et al. Missense FGFR3 mutations create cysteine residues in thanatophoric dwarfi sm type I (TD1). Hum Mol Genet 1996; 5: 509-12.
24. di Martino E, L'Hote CG, Kennedy W, Tomlinson DC, Knowles MA Mutant fi broblast growth factor receptor 3 induces intracellular signaling and cellular transformation in a cell type- and mutation-specifi cmanner. Oncogene 2009; 28: 4306-16
25. Chandarlapaty S, Sawai A, Scaltriti M, Rodrik-Outmezguine V, Grbovic-Huezo O, Serra V, et al. AKT inhibition relieves feedback suppression of receptor tyrosine kinase expression and activity. Cancer Cell 2011; 19: 58-71
26. Serra V, Scaltriti M, Prudkin L, Eichhorn PJ, Ibrahim YH, Chandarlapaty S, et al. PI3K inhibition results in enhanced HER signaling and acquired ERK dependency in HER2-overexpressing breast cancer. Oncogene 2011; 30: 2547-57
27. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, et al. A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 2008; 26: 127-32
28. Oneyama C, Ikeda J, Okuzaki D, Suzuki K, Kanou T, Shintani Y, et al. MicroRNA-mediated downregulation of mTOR/FGFR3 controls tumor growth induced by Src-related oncogenic pathways. Oncogene 2011; 30: 3489-501
29. Parker BC, Annala MJ, Cogdell DE, Granberg KJ, Sun Y, Ji P, et al. The tumorigenic FGFR3-TACC3 gene fusion escapes miR-99a regulation in glioblastoma. J Clin Invest 2013; 123: 855-65
30. Catto JW, Miah S, Owen HC, Bryant H, Myers K, Dudziec E, et al. Distinct microRNA alterations characterize high- and low-grade bladder cancer. Cancer Res 2009; 69: 8472-81
31. Ishizawar R, Parsons SJ. c-Src and cooperating partners in human cancer. Cancer Cell 2004; 6: 209-14
32. B romann PA, Korkaya H, Courtneidge SA. The interplay between Srcfamily kinases and receptor tyrosine kinases. Oncogene 2004; 23: 7957-68.
33. Wilson TR, Fridlyand J, Yan Y, Penuel E, Burton L, Chan E, et al. Widespread pote ntial for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012; 487: 505-9
34. Corcoran RB, Ebi H, Turke AB, Coffee EM, Nishino M, Cogdill AP, et al. EGFR-mediated re-activation of MAPK signaling contributes to insensitivity of BRAF mutant colorectal cancers to RAF inhibition with vemurafenib. Cancer Discov 2012; 2: 227-35
35. Garofalo M, Romano G, Di Leva G, Nuovo G, Jeon YJ, Ngankeu A, et al. EGFR and MET receptor tyrosine kinase-altered microRNA expression induces tumorigenesis and gefi tinib resistance in lung cancers. Nat Med 2011; 18: 74-82
36. Straussman R, Morikawa T, Shee K, Barzily-Rokni M, Qian ZR, Du J, et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012; 487: 500-4
37. Wang W, Eddy R, Condeelis J. The cofilin pathway in breast cancer invasion and metastasis. Nat Rev Cancer 2007; 7: 429-40
38. Williams SV, Hurst CD, Knowles MA. Oncogenic FGFR3 gene fusions in bladder cancer. Hum Mol Genet 2013; 22: 795-803
39. Harbinski F, Craig VJ, Sanghavi S, Jeffery D, Liu L, Sheppard KA, et al. Rescue screens with secreted proteins reveal compensatory potential of receptor tyrosine kinases in driving cancer growth. Cancer Discov 2012; 2: 948-59
40. Qing J, Du X, Chen Y, Chan P, Li H, Wu P, et al. Antibody-based targeting of FGFR3 in bladder carcinoma and t(4;14)-positive multiple myeloma in mice. J Clin Invest 2009; 119: 1216-29
41. Trudel S, Stewart AK, Rom E, Wei E, Li ZH, Kotzer S, et al. The inhibitory anti-FGFR3 antibody, PRO-001, is cytotoxic to t(4;14) multiple myeloma cells. Blood 2006; 107: 4039-46
42. Brough R, Frankum JR, Sims D, Mackay A, Mendes-Pereira AM, Bajrami I, et al. Functional viability profiles of breast cancer. Cancer Discov 2011; 1: 260-73
43. Turner N, Pearson A, Sharpe R, Lambros M, Geyer F, Lopez-Garcia MA, et al. FGFR1 amplification drives endocrine therapy resistance and is a therapeutic target in breast cancer. Cancer Res 2010; 70: 2085-94.
44. Sanchez-Carbayo M, Socci N D, Lozano J, Saint F, Cordon-Cardo C. Defining molecular profi les of poor outcome in patients with invasive bladder cancer using oligonucleotide microarrays. J Clin Oncol 2006; 24: 778-89.
45. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, et al. ONCOMINE: a cancer microarray database and integrated datamining platform. Neoplasia 2004; 6: 1-6