. 2018 Sep; 7(4):464-486.
doi: 10.21037/tlcr.2018.06.04.

Autochthonous murine models for the study of smoker and never-smoker associated lung cancers

Esra A Akbay 1 James Kim 2 
  • PMID: 30225211
  •     217 References
  •     6 citations


Lung cancer accounts for the greatest number of cancer deaths in the world. Tobacco smoke-associated cancers constitute the majority of lung cancer cases but never-smoker cancers comprise a significant and increasing fraction of cases. Recent genomic and transcriptomic sequencing efforts of lung cancers have revealed distinct sets of genetic aberrations of smoker and never-smoker lung cancers that implicate disparate biology and therapeutic strategies. Autochthonous mouse models have contributed greatly to our understanding of lung cancer biology and identified novel therapeutic targets and strategies in the era of targeted therapy. With the emergence of immuno-oncology, mouse models may continue to serve as valuable platforms for novel biological insights and therapeutic strategies. Here, we will review the variety of available autochthonous mouse models of lung cancer, their relation to human smoker and never-smoker lung cancers, and their application to immuno-oncology and immune checkpoint blockade that is revolutionizing lung cancer therapy.

Keywords: Lung cancer; mouse models; never-smoker; smoker.

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BMJ, 2004 Dec 23; 330(7485). PMID: 15613366    Free PMC article.
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Co-clinical trials demonstrate superiority of crizotinib to chemotherapy in ALK-rearranged non-small cell lung cancer and predict strategies to overcome resistance.
Zhao Chen, Esra Akbay, +14 authors, Kwok-Kin Wong.
Clin Cancer Res, 2013 Dec 12; 20(5). PMID: 24327273    Free PMC article.
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Biochemistry, biology, and carcinogenicity of tobacco-specific N-nitrosamines.
S S Hecht.
Chem Res Toxicol, 1998 Jun 24; 11(6). PMID: 9625726
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Cancer Cell, 2003 Sep 06; 4(2). PMID: 12957286
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Stephen G Spiro, Gerard A Silvestri.
Am J Respir Crit Care Med, 2005 Jun 18; 172(5). PMID: 15961694
Effective use of PI3K and MEK inhibitors to treat mutant Kras G12D and PIK3CA H1047R murine lung cancers.
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Nat Med, 2008 Nov 26; 14(12). PMID: 19029981    Free PMC article.
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Nathan P Young, Tyler Jacks.
Proc Natl Acad Sci U S A, 2010 May 19; 107(22). PMID: 20479239    Free PMC article.
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Mol Carcinog, 2015 Sep 09; 55(11). PMID: 26346412    Free PMC article.
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Adi F Gazdar, Paul A Bunn, John D Minna.
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From Mice to Men and Back: An Assessment of Preclinical Model Systems for the Study of Lung Cancers.
Adi F Gazdar, Fred R Hirsch, John D Minna.
J Thorac Oncol, 2016 Jan 03; 11(3). PMID: 26723239    Free PMC article.
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N Engl J Med, 2014 Sep 30; 371(21). PMID: 25264305    Free PMC article.
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Keiichi Ota, Koichi Azuma, +11 authors, Isamu Okamoto.
Clin Cancer Res, 2015 May 29; 21(17). PMID: 26019170
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EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy.
J Guillermo Paez, Pasi A Jänne, +14 authors, Matthew Meyerson.
Science, 2004 May 01; 304(5676). PMID: 15118125
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Checkpoint Inhibitors in Metastatic EGFR-Mutated Non-Small Cell Lung Cancer-A Meta-Analysis.
Chee Khoon Lee, Johnathan Man, +4 authors, James Chih-Hsin Yang.
J Thorac Oncol, 2016 Oct 22; 12(2). PMID: 27765535
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Pten inactivation accelerates oncogenic K-ras-initiated tumorigenesis in a mouse model of lung cancer.
Kentaro Iwanaga, Yanan Yang, +14 authors, Jonathan M Kurie.
Cancer Res, 2008 Feb 19; 68(4). PMID: 18281487    Free PMC article.
Mechanisms of acquired crizotinib resistance in ALK-rearranged lung Cancers.
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Sci Transl Med, 2012 Jan 27; 4(120). PMID: 22277784    Free PMC article.
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Establishment of a Conditional Transgenic Mouse Model Recapitulating EML4-ALK-Positive Human Non-Small Cell Lung Cancer.
Kyoung Ho Pyo, Sun Min Lim, +12 authors, Byoung Chul Cho.
J Thorac Oncol, 2016 Nov 12; 12(3). PMID: 27836576
Small cell lung cancer tumors and preclinical models display heterogeneity of neuroendocrine phenotypes.
Wei Zhang, Luc Girard, +8 authors, Adi F Gazdar.
Transl Lung Cancer Res, 2018 Mar 15; 7(1). PMID: 29535911    Free PMC article.
EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib.
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Proc Natl Acad Sci U S A, 2004 Aug 27; 101(36). PMID: 15329413    Free PMC article.
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Pembrolizumab versus Chemotherapy for PD-L1-Positive Non-Small-Cell Lung Cancer.
Martin Reck, Delvys Rodríguez-Abreu, +16 authors, KEYNOTE-024 Investigators.
N Engl J Med, 2016 Oct 11; 375(19). PMID: 27718847
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Risk of lung cancer from residential heating and cooking fuels in Montreal, Canada.
Agnihotram V Ramanakumar, Marie-Elise Parent, Jack Siemiatycki.
Am J Epidemiol, 2006 Dec 26; 165(6). PMID: 17189590
Never-smokers with lung cancer: epidemiologic evidence of a distinct disease entity.
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J Clin Oncol, 2006 May 20; 24(15). PMID: 16710022
Characterization of variant subclasses of cell lines derived from small cell lung cancer having distinctive biochemical, morphological, and growth properties.
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Cancer Res, 1985 Jun 01; 45(6). PMID: 2985258
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The ALK inhibitor ceritinib overcomes crizotinib resistance in non-small cell lung cancer.
Luc Friboulet, Nanxin Li, +21 authors, Jeffrey A Engelman.
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J W Tichelaar, W Lu, J A Whitsett.
J Biol Chem, 2000 Apr 15; 275(16). PMID: 10766812
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Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial.
Roy S Herbst, Paul Baas, +16 authors, Edward B Garon.
Lancet, 2015 Dec 30; 387(10027). PMID: 26712084
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Multiple cells-of-origin of mutant K-Ras-induced mouse lung adenocarcinoma.
Kate D Sutherland, Ji-Ying Song, +3 authors, Anton Berns.
Proc Natl Acad Sci U S A, 2014 Mar 04; 111(13). PMID: 24586047    Free PMC article.
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Thomas J Lynch, Daphne W Bell, +11 authors, Daniel A Haber.
N Engl J Med, 2004 May 01; 350(21). PMID: 15118073
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Nicola Normanno, Antonella De Luca, +7 authors, David S Salomon.
Gene, 2005 Dec 27; 366(1). PMID: 16377102
Highly Cited. Review.
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Chunxiao Xu, Christine M Fillmore, +21 authors, Kwok-Kin Wong.
Cancer Cell, 2014 May 06; 25(5). PMID: 24794706    Free PMC article.
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Marco Ciotti, Laura Giuliani, +5 authors, Cartesio Favalli.
Oncol Rep, 2006 Jun 21; 16(1). PMID: 16786144
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Nature, 2015 Jul 15; 524(7563). PMID: 26168399    Free PMC article.
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Carboplatin and pemetrexed with or without pembrolizumab for advanced, non-squamous non-small-cell lung cancer: a randomised, phase 2 cohort of the open-label KEYNOTE-021 study.
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Lancet Oncol, 2016 Oct 18; 17(11). PMID: 27745820    Free PMC article.
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A T Shaw, A M Varghese, +9 authors, G V Scagliotti.
Ann Oncol, 2012 Aug 14; 24(1). PMID: 22887466    Free PMC article.
Mapping the in vivo fitness landscape of lung adenocarcinoma tumor suppression in mice.
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Nat Genet, 2018 Apr 04; 50(4). PMID: 29610476    Free PMC article.
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Mol Neurobiol, 2004 Jul 13; 30(1). PMID: 15247487
Synergy of radiotherapy and PD-1 blockade in Kras-mutant lung cancer.
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JCI Insight, 2016 Oct 05; 1(9). PMID: 27699275    Free PMC article.
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J Thorac Oncol, 2010 May 27; 5(7). PMID: 20502360
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The pivotal role of IKKα in the development of spontaneous lung squamous cell carcinomas.
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Mechanistic insight into ALK receptor tyrosine kinase in human cancer biology.
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Nat Rev Cancer, 2013 Sep 26; 13(10). PMID: 24060861
Highly Cited. Review.
Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial.
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Lung Cancer, 2001 Feb 13; 31(2-3). PMID: 11165392
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Carcinogenesis, 2003 May 29; 24(5). PMID: 12771031
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Front Biosci (Elite Ed), 2013 Jun 12; 5(3). PMID: 23747909
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Nature, 2013 Aug 16; 500(7463). PMID: 23945592    Free PMC article.
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Nature, 2014 Aug 01; 511(7511). PMID: 25079552    Free PMC article.
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Acquired C797S Mutation upon Treatment with a T790M-Specific Third-Generation EGFR Inhibitor (HM61713) in Non-Small Cell Lung Cancer.
Haa-Na Song, Ki Sun Jung, +11 authors, Myung-Ju Ahn.
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Sara Raimondi, Paolo Boffetta, +28 authors, Emanuela Taioli.
Mutat Res, 2005 Jul 13; 592(1-2). PMID: 16009381
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Hanke L Matlung, Katka Szilagyi, Neil A Barclay, Timo K van den Berg.
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Highly Cited. Review.
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P Vineis, L Airoldi, +24 authors, E Riboli.
BMJ, 2005 Feb 01; 330(7486). PMID: 15681570    Free PMC article.
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David P Carbone, Martin Reck, +27 authors, CheckMate 026 Investigators.
N Engl J Med, 2017 Jun 22; 376(25). PMID: 28636851    Free PMC article.
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The neuroblastoma-associated F1174L ALK mutation causes resistance to an ALK kinase inhibitor in ALK-translocated cancers.
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Cancer Res, 2010 Oct 30; 70(24). PMID: 21030459    Free PMC article.
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Maki Inoue, Hideaki Toki, +9 authors, Tetsuo Noda.
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A new mouse model to explore the initiation, progression, and therapy of BRAFV600E-induced lung tumors.
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Genes Dev, 2007 Feb 15; 21(4). PMID: 17299132    Free PMC article.
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Clonal History and Genetic Predictors of Transformation Into Small-Cell Carcinomas From Lung Adenocarcinomas.
June-Koo Lee, Junehawk Lee, +20 authors, Young Seok Ju.
J Clin Oncol, 2017 May 13; 35(26). PMID: 28498782
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Sox2 cooperates with Lkb1 loss in a mouse model of squamous cell lung cancer.
Anandaroop Mukhopadhyay, Kristofer C Berrett, +5 authors, Trudy G Oliver.
Cell Rep, 2014 Jun 24; 8(1). PMID: 24953650    Free PMC article.
Identifying and targeting ROS1 gene fusions in non-small cell lung cancer.
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Clin Cancer Res, 2012 Aug 25; 18(17). PMID: 22919003    Free PMC article.
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Nivolumab versus Docetaxel in Advanced Squamous-Cell Non-Small-Cell Lung Cancer.
Julie Brahmer, Karen L Reckamp, +22 authors, David R Spigel.
N Engl J Med, 2015 Jun 02; 373(2). PMID: 26028407    Free PMC article.
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Ludmil B Alexandrov, Young Seok Ju, +11 authors, Michael R Stratton.
Science, 2016 Nov 05; 354(6312). PMID: 27811275    Free PMC article.
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Oncogenic RAS Signaling Promotes Tumor Immunoresistance by Stabilizing PD-L1 mRNA.
Matthew A Coelho, Sophie de Carné Trécesson, +11 authors, Julian Downward.
Immunity, 2017 Dec 17; 47(6). PMID: 29246442    Free PMC article.
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Drug resistance via feedback activation of Stat3 in oncogene-addicted cancer cells.
Ho-June Lee, Guanglei Zhuang, +3 authors, Jeff Settleman.
Cancer Cell, 2014 Jul 30; 26(2). PMID: 25065853
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The Prognostic Role of KRAS Mutation in Patients with Advanced NSCLC Treated with Second- or Third-line Chemotherapy.
Martin Svaton, Ondrej Fiala, +4 authors, Ondrej Topolcan.
Anticancer Res, 2016 Mar 16; 36(3). PMID: 26977001
Pembrolizumab for the treatment of non-small-cell lung cancer.
Edward B Garon, Naiyer A Rizvi, +25 authors, KEYNOTE-001 Investigators.
N Engl J Med, 2015 Apr 22; 372(21). PMID: 25891174
Highly Cited.
Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors.
Lecia V Sequist, Belinda A Waltman, +19 authors, Jeffrey A Engelman.
Sci Transl Med, 2011 Mar 25; 3(75). PMID: 21430269    Free PMC article.
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Lung adenocarcinomas induced in mice by mutant EGF receptors found in human lung cancers respond to a tyrosine kinase inhibitor or to down-regulation of the receptors.
Katerina Politi, Maureen F Zakowski, +3 authors, Harold E Varmus.
Genes Dev, 2006 May 18; 20(11). PMID: 16705038    Free PMC article.
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PTEN is a potent suppressor of small cell lung cancer.
Min Cui, Arnaud Augert, +5 authors, David MacPherson.
Mol Cancer Res, 2014 Feb 01; 12(5). PMID: 24482365    Free PMC article.
The structure of a human p110alpha/p85alpha complex elucidates the effects of oncogenic PI3Kalpha mutations.
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Science, 2007 Dec 15; 318(5857). PMID: 18079394
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Exon 5 polymorphisms in the O6-alkylguanine DNA alkyltransferase gene and lung cancer risk in non-smokers exposed to second-hand smoke.
Catherine Cohet, Stephane Borel, +7 authors, Paolo Boffetta.
Cancer Epidemiol Biomarkers Prev, 2004 Feb 20; 13(2). PMID: 14973087
Preclinical rationale for use of the clinically available multitargeted tyrosine kinase inhibitor crizotinib in ROS1-translocated lung cancer.
Hiroyuki Yasuda, Lorena L de Figueiredo-Pontes, Susumu Kobayashi, Daniel B Costa.
J Thorac Oncol, 2012 May 24; 7(7). PMID: 22617245    Free PMC article.
Genetic and clonal dissection of murine small cell lung carcinoma progression by genome sequencing.
David G McFadden, Thales Papagiannakopoulos, +18 authors, Tyler Jacks.
Cell, 2014 Mar 19; 156(6). PMID: 24630729    Free PMC article.
Highly Cited.
Rapid modelling of cooperating genetic events in cancer through somatic genome editing.
Francisco J Sánchez-Rivera, Thales Papagiannakopoulos, +8 authors, Tyler Jacks.
Nature, 2014 Oct 23; 516(7531). PMID: 25337879    Free PMC article.
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SOX2 is an amplified lineage-survival oncogene in lung and esophageal squamous cell carcinomas.
Adam J Bass, Hideo Watanabe, +45 authors, Matthew Meyerson.
Nat Genet, 2009 Oct 06; 41(11). PMID: 19801978    Free PMC article.
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K-Ras(G12C) inhibitors allosterically control GTP affinity and effector interactions.
Jonathan M Ostrem, Ulf Peters, +2 authors, Kevan M Shokat.
Nature, 2013 Nov 22; 503(7477). PMID: 24256730    Free PMC article.
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Nivolumab plus ipilimumab as first-line treatment for advanced non-small-cell lung cancer (CheckMate 012): results of an open-label, phase 1, multicohort study.
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Lancet Oncol, 2016 Dec 10; 18(1). PMID: 27932067    Free PMC article.
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Preclinical Murine Models for Lung Cancer: Clinical Trial Applications.
Amelia Kellar, Cay Egan, Don Morris.
Biomed Res Int, 2015 Jun 13; 2015. PMID: 26064932    Free PMC article.
A combined analysis of North American case-control studies of residential radon and lung cancer.
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J Toxicol Environ Health A, 2006 Apr 13; 69(7). PMID: 16608828
A genetic mouse model for metastatic lung cancer with gender differences in survival.
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Oncogene, 2007 May 09; 26(48). PMID: 17486075
Helical domain and kinase domain mutations in p110alpha of phosphatidylinositol 3-kinase induce gain of function by different mechanisms.
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Proc Natl Acad Sci U S A, 2008 Feb 13; 105(7). PMID: 18268322    Free PMC article.
Highly Cited.
Molecular Determinants of Response to Anti-Programmed Cell Death (PD)-1 and Anti-Programmed Death-Ligand 1 (PD-L1) Blockade in Patients With Non-Small-Cell Lung Cancer Profiled With Targeted Next-Generation Sequencing.
Hira Rizvi, Francisco Sanchez-Vega, +29 authors, Matthew D Hellmann.
J Clin Oncol, 2018 Jan 18; 36(7). PMID: 29337640    Free PMC article.
Highly Cited.
EGFR Mutations and Resistance to Irreversible Pyrimidine-Based EGFR Inhibitors.
Dalia Ercan, Hwan Geun Choi, +5 authors, Pasi A Jänne.
Clin Cancer Res, 2015 May 08; 21(17). PMID: 25948633    Free PMC article.
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Genomic landscape of non-small cell lung cancer in smokers and never-smokers.
Ramaswamy Govindan, Li Ding, +18 authors, Richard K Wilson.
Cell, 2012 Sep 18; 150(6). PMID: 22980976    Free PMC article.
Highly Cited.
Co-occurring genomic alterations define major subsets of KRAS-mutant lung adenocarcinoma with distinct biology, immune profiles, and therapeutic vulnerabilities.
Ferdinandos Skoulidis, Lauren A Byers, +34 authors, John V Heymach.
Cancer Discov, 2015 Jun 13; 5(8). PMID: 26069186    Free PMC article.
Highly Cited.
The Allelic Context of the C797S Mutation Acquired upon Treatment with Third-Generation EGFR Inhibitors Impacts Sensitivity to Subsequent Treatment Strategies.
Matthew J Niederst, Haichuan Hu, +5 authors, Jeffrey A Engelman.
Clin Cancer Res, 2015 May 13; 21(17). PMID: 25964297    Free PMC article.
Highly Cited.
The discovery of the benzhydroxamate MEK inhibitors CI-1040 and PD 0325901.
Stephen D Barrett, Alexander J Bridges, +17 authors, Haile Tecle.
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A quantitative and multiplexed approach to uncover the fitness landscape of tumor suppression in vivo.
Zoë N Rogers, Christopher D McFarland, +4 authors, Monte M Winslow.
Nat Methods, 2017 May 23; 14(7). PMID: 28530655    Free PMC article.
The role of RAS oncogene in survival of patients with lung cancer: a systematic review of the literature with meta-analysis.
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Highly Cited. Systematic Review.
Mutational landscape of EGFR-, MYC-, and Kras-driven genetically engineered mouse models of lung adenocarcinoma.
David G McFadden, Katerina Politi, +14 authors, Harold Varmus.
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Air pollution and lung cancer risks in China--a meta-analysis.
Yu Zhao, Shuxiao Wang, +2 authors, Jiming Hao.
Sci Total Environ, 2006 Jan 13; 366(2-3). PMID: 16406110
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Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer.
Manabu Soda, Young Lim Choi, +15 authors, Hiroyuki Mano.
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Highly Cited.
Is previous respiratory disease a risk factor for lung cancer?
Rachel Denholm, Joachim Schüz, +32 authors, Ann C Olsson.
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Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma.
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Di Ma, Xuezhi Hao, +2 authors, Junling Li.
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Comprehensive genomic characterization of squamous cell lung cancers.
Cancer Genome Atlas Research Network.
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Mouse model for ROS1-rearranged lung cancer.
Yasuhito Arai, Yasushi Totoki, +10 authors, Tatsuhiro Shibata.
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