Mutations in the DDR2 kinase gene identify a novel therapeutic target in squamous cell lung cancer

Cancer Discovery

Volumn 1, Issue 1, 2011, Pages 78-89

  Hammerman, Peter S ^a   Sos, Martin L ^b   Ramos, Alex H ^c   Xu, Chunxiao ^a   Dutt, Amit ^c   Zhou, Wenjun ^a   Brace, Lear E ^a   Woods, Brittany A ^a   Lin, Wenchu ^a   Zhang, Jianming ^a   Deng, Xianming ^a   Lim, Sang Min ^a   Heynck, Stefanie ^b   Peifer, Martin ^b   Simard, Jeffrey R ^d   Lawrence, Michael S ^c   Onofrio, Robert C ^c   Salvesen, Helga B ^e,f   Seidel, Danila ^b   Zander, Thomas ^b,g   Heuckmann, Johannes M ^b   Soltermann, Alex ^h   Moch, Holger ^h   Koker, Mirjam ^b   Leenders, Frauke ^b   Gabler, Franziska ^b   Querings, Silvia ^b   Ansén, Sascha ^g   Brambilla, Elisabeth ⁱ   Brambilla, Christian ⁱ   Lorimier, Philippe ⁱ   Brustugun, Odd Terje ^j   Helland, Åslaug ^j   Petersen, Iver ^k   Clement, Joachim H ^k   Groen, Harry ^l   Timens, Wim ^l   Sietsma, Hannie ^l   Stoelben, Erich ^m   Wolf, Jürgen ^b,g   Beer, David G ⁿ   Tsao, Ming Sound ^o   Hanna, Megan ^a,c   Hatton, Charles ^a,c   Eck, Michael J ^a   Janne, Pasi A ^a   Johnson, Bruce E ^a   Winckler, Wendy ^c   Greulich, Heidi ^a,c   Bass, Adam J ^a   Cho, Jeonghee ^a   Rauh, Daniel ^d,p   Gray, Nathanael S ^a   Wong, Kwok Kin ^a   Haura, Eric B ^q   Thomas, Roman K ^b,d   Meyerson, Matthew ^a,c   more..

^a DANA FARBER CANCER INSTITUTE   (United States)

^b UNIVERSITY OF COLOGNE   (Germany)

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

^d CHEMICAL GENOMICS CENTRE OF THE MAX PLANCK SOCIETY   (Germany)

^e HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^f UNIVERSITY OF BERGEN   (Norway)

^g UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^h UNIVERSITY HOSPITAL ZURICH   (Switzerland)

ⁱ INSTITUT ALBERT BONNIOT   (France)

^j OSLO UNIVERSITY HOSPITAL   (Norway)

^k JENA UNIVERSITY HOSPITAL   (Germany)

^l UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^m KLINIKEN DER STADT KÖLN GGMBH   (Germany)

ⁿ UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^o PRINCESS MARGARET HOSPITAL   (Canada)

^p TU DORTMUND UNIVERSITY   (Germany)

^q H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DASATINIB; ERLOTINIB; GEFITINIB; GREEN FLUORESCENT PROTEIN; IMATINIB; INTERLEUKIN 3; PROTEIN TYROSINE KINASE INHIBITOR; SHORT HAIRPIN RNA;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CELL TRANSFORMATION; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DISCOIDIN DOMAIN RECEPTOR 2 TYROSINE KINASE GENE; DRUG WITHDRAWAL; GENE; GENE MUTATION; GENE SEQUENCE; GENE SILENCING; GENE VECTOR; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; LUNG ADENOCARCINOMA; LUNG DISEASE; LUNG SQUAMOUS CELL CARCINOMA; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; ONCOGENE SRC; PHOSPHORYLATION; PLEURA EFFUSION; POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIDE EFFECT; TUMOR VOLUME; VIRUS INFECTION; XENOGRAFT;

ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MICE; MICE, NUDE; MUTATION; NIH 3T3 CELLS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PYRIMIDINES; QUINAZOLINES; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, MITOGEN; SRC-FAMILY KINASES; THIAZOLES;

EID: 84866709500     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8274.CD-11-0005     Document Type: Article

References (48)

1. Lennes IT, Lynch TJ. Quality indicators in cancer care: development and implementation for improved health outcomes in non-small-cell lung cancer. Clin Lung Cancer 2009;10:341-6.
2. West H, Harpole D, Travis W. Histologic considerations for individualized systemic therapy approaches for the management of nonsmall cell lung cancer. Chest 2009;136:1112-8.
3. Pao W, Miller VA, Politi KA, Riely GJ, Somwar R, Zakowski MF, et al. 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.
4. 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.
5. 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.
6. Shigematsu H, Lin L, Takahashi T, Nomura M, Suzuki M, Wistuba II, et al. Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancers. J Natl Cancer Inst 2005;97:339-46.
7. Sasaki T, Rodig SJ, Chirieac LR, Janne PA. The biology and treatment of EML4-ALK non-small cell lung cancer. Eur J Cancer 2010;46:1773-80.
8. Hammerman PS, Janne PA, Johnson BE. Resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin Cancer Res 2009;15:7502-9.
9. Mok TS, Wu YL, Thongprasert S, Yang CH, Chu DT, Saijo N, et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009;361:947-57.
10. Shaw AT, Yeap BY, Mino-Kenudson M, Digumarthy SR, Costa DB, Heist RS, et al. Clinical features and outcome of patients with non-small-cell lung cancer who harbor EML4-ALK. J Clin Oncol 2009;27:4247-53.
11. Weiss J, Sos ML, Seidel D, Peifer M, Zander T, Heuckmann JM, et al. Frequent and focal FGFR1 amplification associates with therapeutically tractable FGFR1 dependency in squamous cell lung cancer. Sci Transl Med 2010;2:62ra93.
12. Vogel W, Gish GD, Alves F, Pawson T. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1997;1:13-23.
13. Vogel W. Discoidin domain receptors: structural relations and functional implications. FASEB J 1999;13 Suppl:S77-82.
14. Shrivastava A, Radziejewski C, Campbell E, Kovac L, McGlynn M, Ryan TE, et al. An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol Cell 1997;1:25-34.
15. Leitinger B. Molecular analysis of collagen binding by the human discoidin domain receptors, DDR1 and DDR2. Identification of collagen binding sites in DDR2. J Biol Chem 2003;278:16761-9.
16. Ikeda K, Wang LH, Torres R, Zhao H, Olaso E, Eng FJ, et al. Discoidin domain receptor 2 interacts with Src and Shc following its activation by type I collagen. J Biol Chem 2002;277:19206-12.
17. Olaso E, Labrador JP, Wang L, Ikeda K, Eng FJ, Klein R, et al. Discoidin domain receptor 2 regulates fibroblast proliferation and migration through the extracellular matrix in association with transcriptional activation of matrix metalloproteinase-2. J Biol Chem 2002;277:3606-13.
18. Labrador JP, Azcoitia V, Tuckermann J, Lin C, Olaso E, Manes S, et al. The collagen receptor DDR2 regulates proliferation and its elimination leads to dwarfism. EMBO Rep 2001;2:446-52.
19. Ford CE, Lau SK, Zhu CQ, Andersson T, Tsao MS, Vogel WF. Expression and mutation analysis of the discoidin domain receptors1 and 2 in non-small cell lung carcinoma. Br J Cancer 2007;96:808-14.
20. 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.
21. Day E, Waters B, Spiegel K, Alnadaf T, Manley PW, Buchdunger E, et al. Inhibition of collagen-induced discoidin domain receptor1 and 2 activation by imatinib, nilotinib and dasatinib. Eur J Pharmacol 2008;599:44-53.
22. Raponi M, Zhang Y, Yu J, Chen G, Lee G, Taylor JM, et al. Gene expression signatures for predicting prognosis of squamous cell and adenocarcinomas of the lung. Cancer Res 2006;66:7466-72.
23. Bass AJ, Watanabe H, Mermel CH, Yu S, Perner S, Verhaak RG, et al. SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas. Nat Genet 2009;41:1238-42.
24. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010;463:899-905.
25. Stegmeier F, Warmuth M, Sellers WR, Dorsch M. Targeted cancer therapies in the twenty-first century: lessons from imatinib. Clin Pharmacol Ther 2010;87:543-52.
26. Manley PW, Drueckes P, Fendrich G, Furet P, Liebetanz J, Martiny-Baron G, et al. Extended kinase profile and properties of the protein kinase inhibitor nilotinib. Biochim Biophys Acta 2010;1804:445-53.
27. Li J, Rix U, Fang B, Bai Y, Edwards A, Colinge J, et al. A chemical and phosphoproteomic characterization of dasatinib action in lung cancer. Nat Chem Biol 2010;6:291-9.
28. 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.
29. Haura EB, Tanvetyanon T, Chiappori A, Williams C, Simon G, Antonia S, et al. Phase I/II study of the Src inhibitor dasatinib in combination with erlotinib in advanced non-small-cell lung cancer. J Clin Oncol 2010;28:1387-94.
30. Tonon G, Wong KK, Maulik G, Brennan C, Feng B, Zhang Y, et al. High-resolution genomic profiles of human lung cancer. Proc Natl Acad Sci U S A 2005;102:9625-30.
31. Ramos AH, Dutt A, Mermel C, Perner S, Cho J, Lafargue CJ, et al. Amplification of chromosomal segment 4q12 in non-small cell lung cancer. Cancer Biol Ther 2009;8:2042-50.
32. Sos ML, Michel K, Zander T, Weiss J, Frommolt P, Peifer M, et al. Predicting drug susceptibility of non-small cell lung cancers based on genetic lesions. J Clin Invest 2009;119:1727-40.
33. Du J, Bernasconi P, Clauser KR, Mani DR, Finn SP, Beroukhim R, et al. Bead-based profiling of tyrosine kinase phosphorylation identifies SRC as a potential target for glioblastoma therapy. Nat Biotechnol 2009;27:77-83.
34. Quintas-Cardama A, Kantarjian H, Cortes J. Imatinib and beyond-exploring the full potential of targeted therapy for CML. Nat Rev Clin Oncol 2009;6:535-43.
35. Kim LC, Rix U, Haura EB. Dasatinib in solid tumors. Expert Opin Investig Drugs 2010;19:415-25.
36. O'Hare T, Shakespeare WC, Zhu X, Eide CA, Rivera VM, Wang F, et al. AP24534, a pan-BCR-ABL inhibitor for chronic myeloid leukemia, potently inhibits the T315I mutant and overcomes mutationbased resistance. Cancer Cell 2009;16:401-12.
37. Song L, Morris M, Bagui T, Lee FY, Jove R, Haura EB. Dasatinib (BMS-354825) selectively induces apoptosis in lung cancer cells dependent on epidermal growth factor receptor signaling for survival. Cancer Res 2006;66:5542-8.
38. Nosaka T, Kawashima T, Misawa K, Ikuta K, Mui AL, Kitamura T. STAT5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells. EMBO J 1999;18:4754-65.
39. Hennequin LF, Ballard P, Boyle FT, Delouvrie B, Ellston RP, Halsall CT, et al. Novel 4-anilinoquinazolines with C-6 carbon-linked side chains: synthesis and structure-activity relationship of a series of potent, orally active, EGF receptor tyrosine kinase inhibitors. Bioorg Med Chem Lett 2006;16:2672-6.
40. Johnson FM, Bekele BN, Feng L, Wistuba I, Tang XM, Tran HT, et al. Phase II study of dasatinib in patients with advanced non-small-cell lung cancer. J Clin Oncol 2010;28:4609-15.
41. McDermott U, Iafrate AJ, Gray NS, Shioda T, Classon M, Maheswaran S, et al. Genomic alterations of anaplastic lymphoma kinase may sensitize tumors to anaplastic lymphoma kinase inhibitors. Cancer Res 2008;68:3389-95.
42. Kan Z, Jaiswal BS, Stinson J, Janakiraman V, Bhatt D, Stern HM, et al. Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 2010;466:869-73.
43. Statpages. org [homepage on the Internet]. [updated 2011 February 17; cited 2011 January 12]. Available from: http://statpages.org/ proppowr.html
44. Bargal R, Cormier-Daire V, Ben-Neriah Z, Le Merrer M, Sosna J, Melki J, et al. Mutations in DDR2 gene cause SMED with short limbs and abnormal calcifications. Am J Hum Genet 2009; 84:80-4.
45. Ali BR, Xu H, Akawi NA, John A, Karuvantevida NS, Langer R, et al. Trafficking defects and loss of ligand binding are the underlying causes of all reported DDR2 missense mutations found in SMED-SL patients. Hum Mol Genet 2010;19:2239-50.
46. Moffat J, Grueneberg DA, Yang X, Kim SY, Kloepfer AM, Hinkle G, et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 2006;124:1283-98.
47. Luo B, Cheung HW, Subramanian A, Sharifnia T, Okamoto M, Yang X, et al. Highly parallel identification of essential genes in cancer cells. Proc Natl Acad Sci U S A 2008;105:20380-5.
48. Broad Institute. org [homepage on the Internet]. 2010 [cited 2011 January 12]. Available from: http://www.broadinstitute.org/rnai/ public /resources/protocols