Open Access

Spatial and Temporal Heterogeneity in Clonal Evolution of Nonsmall-cell Lung Cancer: Implications for Therapy


Cite

Gerlinger M, Rowan AJ, Horswell S, Math M, Larkin J, Endesfelder D, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012 Mar 8;366(10):883–892. GerlingerM RowanAJ HorswellS MathM LarkinJ EndesfelderD Intratumor heterogeneity and branched evolution revealed by multiregion sequencing N Engl J Med 2012 Mar 8 366 10 883 892 Search in Google Scholar

Saunders NA, Simpson F, Thompson EW, Hill MM, Endo-Munoz L, Leggatt G, Minchin RF, Guminski A. Role of intratumoural heterogeneity in cancer drug resistance: molecular and clinical perspectives. EMBO Mol Med. 2012 Aug;4(8):675–84. SaundersNA SimpsonF ThompsonEW HillMM Endo-MunozL LeggattG MinchinRF GuminskiA Role of intratumoural heterogeneity in cancer drug resistance: molecular and clinical perspectives EMBO Mol Med 2012 Aug 4 8 675 84 Search in Google Scholar

Caswell DR, Swanton C. The role of tumour heterogeneity and clonal cooperativity in metastasis, immune evasion and clinical outcome. BMC Med. 2017 Jul 18;15(1):133. CaswellDR SwantonC The role of tumour heterogeneity and clonal cooperativity in metastasis, immune evasion and clinical outcome BMC Med 2017 Jul 18 15 1 133 Search in Google Scholar

Venkatesan S, Swanton C. Tumor Evolutionary Principles: How Intratumor Heterogeneity Influences Cancer Treatment and Outcome. Am Soc Clin Oncol Educ Book. 2016;35:e141–9. VenkatesanS SwantonC Tumor Evolutionary Principles: How Intratumor Heterogeneity Influences Cancer Treatment and Outcome Am Soc Clin Oncol Educ Book 2016 35 e141 9 Search in Google Scholar

Hiley CT, Swanton C. Spatial and temporal cancer evolution: causes and consequences of tumour diversity. Clin Med (Lond). 2014 Dec;14 Suppl 6:s33–7. HileyCT SwantonC Spatial and temporal cancer evolution: causes and consequences of tumour diversity Clin Med (Lond) 2014 Dec 14 Suppl 6 s33 7 Search in Google Scholar

Dagogo-Jack I, Shaw AT. Tumour heterogeneity and resistance to cancer therapies. Nat Rev Clin Oncol. 2018 Feb;15(2):81–94. Dagogo-JackI ShawAT Tumour heterogeneity and resistance to cancer therapies Nat Rev Clin Oncol 2018 Feb 15 2 81 94 Search in Google Scholar

McGranahan N, Swanton C. Biological and therapeutic impact of intratumor heterogeneity in cancer evolution. Cancer Cell. 2015 Jan 12;27(1):15–26. McGranahanN SwantonC Biological and therapeutic impact of intratumor heterogeneity in cancer evolution Cancer Cell 2015 Jan 12 27 1 15 26 Search in Google Scholar

McGranahan N, Swanton C. Clonal Heterogeneity and Tumor Evolution: Past, Present, and the Future. Cell. 2017 Feb 9;168(4):613–628. McGranahanN SwantonC Clonal Heterogeneity and Tumor Evolution: Past, Present, and the Future Cell 2017 Feb 9 168 4 613 628 Search in Google Scholar

Kuipers J, Jahn K, Beerenwinkel N. Advances in understanding tumour evolution through single-cell sequencing. Biochim Biophys Acta. 2017 Apr;1867(2):127–138. KuipersJ JahnK BeerenwinkelN Advances in understanding tumour evolution through single-cell sequencing Biochim Biophys Acta 2017 Apr 1867 2 127 138 Search in Google Scholar

Navin, N. E. (2014). Cancer genomics: one cell at a time. Genome Biology, 15(8), 452. NavinN. E. 2014 Cancer genomics: one cell at a time Genome Biology 15 8 452 Search in Google Scholar

Wang Y, Waters J, Leung ML, Unruh A, Roh W, Shi X, et al. Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature. 2014;512(7513):155–160. WangY WatersJ LeungML UnruhA RohW ShiX Clonal evolution in breast cancer revealed by single nucleus genome sequencing Nature 2014 512 7513 155 160 Search in Google Scholar

Francis JM, Zhang CZ, Maire CL, Jung J, Manzo VE, Adalsteinsson VA, Homer H, Haidar S, Blumenstiel B, Pedamallu CS, Ligon AH, Love JC, Meyerson M, Ligon KL. EGFR variant heterogeneity in glioblastoma resolved through single-nucleus sequencing. Cancer Discov. 2014 Aug;4(8):956–71. FrancisJM ZhangCZ MaireCL JungJ ManzoVE AdalsteinssonVA HomerH HaidarS BlumenstielB PedamalluCS LigonAH LoveJC MeyersonM LigonKL EGFR variant heterogeneity in glioblastoma resolved through single-nucleus sequencing Cancer Discov 2014 Aug 4 8 956 71 Search in Google Scholar

Navin, N., Kendall, J., Troge, J., Andrews, P., Rodgers, L., McIndoo, J., … Wigler, M. (2011). Tumor Evolution Inferred by Single Cell Sequencing. Nature, 472(7341), 90–94. NavinN. KendallJ. TrogeJ. AndrewsP. RodgersL. McIndooJ. WiglerM. 2011 Tumor Evolution Inferred by Single Cell Sequencing Nature 472 7341 90 94 Search in Google Scholar

Jamal-Hanjani M, Wilson GA, McGranahan N, Birkbak NJ, Watkins TBK, Veeriah S, et al, TRACERx Consortium. Tracking the Evolution of Non-Small-Cell Lung Cancer. N Engl J Med. 2017 Jun 1;376(22):2109–2121 Jamal-HanjaniM WilsonGA McGranahanN BirkbakNJ WatkinsTBK VeeriahS TRACERx Consortium Tracking the Evolution of Non-Small-Cell Lung Cancer N Engl J Med 2017 Jun 1 376 22 2109 212 Search in Google Scholar

Shibata T. Current and future molecular profiling of cancer by next-generation sequencing. Jpn J Clin Oncol. 2015 Oct;45(10):895–9. ShibataT Current and future molecular profiling of cancer by next-generation sequencing Jpn J Clin Oncol 2015 Oct 45 10 895 9 Search in Google Scholar

Mar N, Vredenburgh JJ, Wasser JS. Targeting HER2 in the treatment of non-small cell lung cancer. Lung Cancer. 2015 Mar;87(3):220–5. MarN VredenburghJJ WasserJS Targeting HER2 in the treatment of non-small cell lung cancer Lung Cancer 2015 Mar 87 3 220 5 Search in Google Scholar

Cancer Genome Atlas Research Network. Comprehensive molecular profiling of lung adenocarcinoma. Nature 2014;511:543–50. Cancer Genome Atlas Research Network Comprehensive molecular profiling of lung adenocarcinoma Nature 2014 511 543 50 Search in Google Scholar

Gerlinger M, Swanton C. How Darwinian models inform therapeutic failure initiated by clonal heterogeneity in cancer medicine. Br J Cancer. 2010 Oct 12;103(8):1139–43. GerlingerM SwantonC How Darwinian models inform therapeutic failure initiated by clonal heterogeneity in cancer medicine Br J Cancer 2010 Oct 12 103 8 1139 43 Search in Google Scholar

Neelakantan, D. et al. (2015) Intratumoral heterogeneity: Clonal cooperation in epithelial-to-mesenchymal transition and metastasis. Cell Adh Migr, 9, 265–76. NeelakantanD. 2015 Intratumoral heterogeneity: Clonal cooperation in epithelial-to-mesenchymal transition and metastasis Cell Adh Migr 9 265 76 Search in Google Scholar

Saber A, Hiltermann TJN, Kok K, Terpstra MM, de Lange K, Timens W, Groen HJM, van den Berg A. Mutation patterns in small cell and non-small cell lung cancer patients suggest a different level of heterogeneity between primary and metastatic tumors. Carcinogenesis. 2017 Feb 1;38(2):144–151. SaberA HiltermannTJN KokK TerpstraMM de LangeK TimensW GroenHJM van den BergA Mutation patterns in small cell and non-small cell lung cancer patients suggest a different level of heterogeneity between primary and metastatic tumors Carcinogenesis 2017 Feb 1 38 2 144 151 Search in Google Scholar

Kalikaki A, Koutsopoulos A, Trypaki M, Souglakos J, Stathopoulos E, Georgoulias V, Mavroudis D, Voutsina A (2008) Comparison of EGFR and K-RAS gene status between primary tumours and corresponding metastases in NSCLC. Br J. Cancer 99(6):923–929. KalikakiA KoutsopoulosA TrypakiM SouglakosJ StathopoulosE GeorgouliasV MavroudisD VoutsinaA 2008 Comparison of EGFR and K-RAS gene status between primary tumours and corresponding metastases in NSCLC Br J. Cancer 99 6 923 929 Search in Google Scholar

de Bruin EC, McGranahan N, Mitter R, Salm M, Wedge DC, Yates L, et al. Spatial and temporal diversity in genomic instability processes defines lung cancer evolution. Science. 2014 Oct 10;346(6206):251–6. de BruinEC McGranahanN MitterR SalmM WedgeDC YatesL Spatial and temporal diversity in genomic instability processes defines lung cancer evolution Science 2014 Oct 10 346 6206 251 6 Search in Google Scholar

Izumchenko E, Chang X, Brait M, Fertig E, Kagohara LT, Bedi A, Marchionni L, Agrawal N, Ravi R, Jones S, Hoque MO, Westra WH, Sidransky D. Targeted sequencing reveals clonal genetic changes in the progression of early lung neoplasms and paired circulating DNA. Nat Commun. 2015 Sep 16;6:8258. IzumchenkoE ChangX BraitM FertigE KagoharaLT BediA MarchionniL AgrawalN RaviR JonesS HoqueMO WestraWH SidranskyD Targeted sequencing reveals clonal genetic changes in the progression of early lung neoplasms and paired circulating DNA Nat Commun 2015 Sep 16 6 8258 Search in Google Scholar

Sherwood J, Dearden S, Ratcliffe M, Walker J. Mutation status concordance between primary lesions and metastatic sites of advanced non-small-cell lung cancer and the impact of mutation testing methodologies: a literature review. J Exp Clin Cancer Res. 2015 Sep 4;34:92. SherwoodJ DeardenS RatcliffeM WalkerJ Mutation status concordance between primary lesions and metastatic sites of advanced non-small-cell lung cancer and the impact of mutation testing methodologies: a literature review J Exp Clin Cancer Res 2015 Sep 4 34 92 Search in Google Scholar

Nayak L, Lee EQ, Wen PY. Epidemiology of brain metastases. Curr Oncol Rep (2012) 14(1):48–54. NayakL LeeEQ WenPY Epidemiology of brain metastases Curr Oncol Rep 2012 14 1 48 54 Search in Google Scholar

Park S, Holmes-Tisch AJ, Cho EY, Shim YM, Kim J, Kim HS, et al. Discordance of molecular biomarkers associated with epidermal growth factor receptor pathway between primary tumors and lymph node metastasis in non-small cell lung cancer. J Thorac Oncol. 2009;4:809–15. ParkS Holmes-TischAJ ChoEY ShimYM KimJ KimHS Discordance of molecular biomarkers associated with epidermal growth factor receptor pathway between primary tumors and lymph node metastasis in non-small cell lung cancer J Thorac Oncol 2009 4 809 15 Search in Google Scholar

Brastianos PK, Carter SL, Santagata S, Cahill DP, Taylor-Weiner A, Jones RT, et al. Genomic Characterization of Brain Metastases Reveals Branched Evolution and Potential Therapeutic Targets. Cancer Discov. 2015 Nov;5(11):1164–1177. BrastianosPK CarterSL SantagataS CahillDP Taylor-WeinerA JonesRT Genomic Characterization of Brain Metastases Reveals Branched Evolution and Potential Therapeutic Targets Cancer Discov 2015 Nov 5 11 1164 1177 Search in Google Scholar

Izumchenko E, Chang X, Brait M, Fertig E, Kagohara LT, Bedi A, et al. Targeted sequencing reveals clonal genetic changes in the progression of early lung neoplasms and paired circulating DNA. Nat Commun. 2015 Sep 16;6:8258. IzumchenkoE ChangX BraitM FertigE KagoharaLT BediA Targeted sequencing reveals clonal genetic changes in the progression of early lung neoplasms and paired circulating DNA Nat Commun 2015 Sep 16 6 8258 Search in Google Scholar

Hata AN, Niederst MJ, Archibald HL, Gomez-Caraballo M, Siddiqui FM, Mulvey HE, et al. Tumor cells can follow distinct evolutionary paths to become resistant to epidermal growth factor receptor inhibition. Nat Med. 2016 Mar;22(3):262–9. HataAN NiederstMJ ArchibaldHL Gomez-CaraballoM SiddiquiFM MulveyHE Tumor cells can follow distinct evolutionary paths to become resistant to epidermal growth factor receptor inhibition Nat Med 2016 Mar 22 3 262 9 Search in Google Scholar

Piotrowska Z, Niederst MJ, Karlovich CA, Wakelee HA, Neal JW, Mino-Kenudson M, et al. Heterogeneity Underlies the Emergence of EGFRT790 Wild-Type Clones Following Treatment of T790M-Positive Cancers with a Third-Generation EGFR Inhibitor. Cancer Discov. 2015 Jul;5(7):713–22. PiotrowskaZ NiederstMJ KarlovichCA WakeleeHA NealJW Mino-KenudsonM Heterogeneity Underlies the Emergence of EGFRT790 Wild-Type Clones Following Treatment of T790M-Positive Cancers with a Third-Generation EGFR Inhibitor Cancer Discov 2015 Jul 5 7 713 22 Search in Google Scholar

Sequist, L. V., Waltman, B. A., Dias-Santagata, D., Digumarthy, S., Turke, A. B., Fidias, P., Engelman, J. A. (2011). Genotypic and Histological Evolution of Lung Cancers Acquiring Resistance to EGFR Inhibitors. Science Translational Medicine, 3(75), 75ra26. SequistL. V. WaltmanB. A. Dias-SantagataD. DigumarthyS. TurkeA. B. FidiasP. EngelmanJ. A. 2011 Genotypic and Histological Evolution of Lung Cancers Acquiring Resistance to EGFR Inhibitors Science Translational Medicine 3 75 75ra26 Search in Google Scholar

Song A, Kim TM, Kim DW, Kim S, Keam B, Lee SH, Heo DS. Molecular Changes Associated with Acquired Resistance to Crizotinib in ROS1-Rearranged Non-Small Cell Lung Cancer. Clin Cancer Res. 2015 May 15;21(10):2379–87. SongA KimTM KimDW KimS KeamB LeeSH HeoDS Molecular Changes Associated with Acquired Resistance to Crizotinib in ROS1-Rearranged Non-Small Cell Lung Cancer Clin Cancer Res 2015 May 15 21 10 2379 87 Search in Google Scholar

Drilon A, Somwar R, Wagner JP, Vellore NA, Eide CA, Zabriskie MS, et al. A Novel Crizotinib-Resistant Solvent-Front Mutation Responsive to Cabozantinib Therapy in a Patient with ROS1-Rearranged Lung Cancer. Clin Cancer Res. 2016 May 15;22(10):2351–8. DrilonA SomwarR WagnerJP VelloreNA EideCA ZabriskieMS A Novel Crizotinib-Resistant Solvent-Front Mutation Responsive to Cabozantinib Therapy in a Patient with ROS1-Rearranged Lung Cancer Clin Cancer Res 2016 May 15 22 10 2351 8 Search in Google Scholar

Awad MM, Katayama R, McTigue M, Liu W, Deng YL, Brooun A, et al. Acquired resistance to crizotinib from a mutation in CD74-ROS1. N Engl J Med. 2013 Jun 20;368(25):2395–401. AwadMM KatayamaR McTigueM LiuW DengYL BroounA Acquired resistance to crizotinib from a mutation in CD74-ROS1 N Engl J Med 2013 Jun 20 368 25 2395 401 Search in Google Scholar

Gerlinger M, Norton L, Swanton C. Acquired resistance to crizotinib from a mutation in CD74-ROS1. N Engl J Med. 2013 Sep 19;369(12):1172–3. GerlingerM NortonL SwantonC Acquired resistance to crizotinib from a mutation in CD74-ROS1 N Engl J Med 2013 Sep 19 369 12 1172 3 Search in Google Scholar

Abbosh C, Birkbak NJ, Wilson GA, Jamal-Hanjani M, Constantin T, Salari R, et al. Phylogenetic ctDNA analysis depicts early-stage lung cancer evolution. Nature. 2017 Apr 26;545(7655):446–451. AbboshC BirkbakNJ WilsonGA Jamal-HanjaniM ConstantinT SalariR Phylogenetic ctDNA analysis depicts early-stage lung cancer evolution Nature 2017 Apr 26 545 7655 446 451 Search in Google Scholar

Hayes DF, Paoletti C. Circulating tumour cells: insights into tumour heterogeneity. J Intern Med. 2013 Aug;274(2):137–43. HayesDF PaolettiC Circulating tumour cells: insights into tumour heterogeneity J Intern Med 2013 Aug 274 2 137 43 Search in Google Scholar

Santarpia M, Liguori A, Karachaliou N, Gonzalez-Cao M, Daffinà MG, D’Aveni A, Marabello G, Altavilla G, Rosell R. Osimertinib in the treatment of non-small-cell lung cancer: design, development and place in therapy. Lung Cancer (Auckl). 2017 Aug 18;8:109–125. SantarpiaM LiguoriA KarachaliouN Gonzalez-CaoM DaffinàMG D’AveniA MarabelloG AltavillaG RosellR Osimertinib in the treatment of non-small-cell lung cancer: design, development and place in therapy Lung Cancer (Auckl) 2017 Aug 18 8 109 125 Search in Google Scholar

Santarpia M, Liguori A, Karachaliou N, Gonzalez-Cao M, Daffinà MG, D’Aveni A, et al. Osimertinib in the treatment of non-small-cell lung cancer: design, development and place in therapy. Lung Cancer (Auckl). 2017 Aug 18;8:109–125. SantarpiaM LiguoriA KarachaliouN Gonzalez-CaoM DaffinàMG D’AveniA Osimertinib in the treatment of non-small-cell lung cancer: design, development and place in therapy Lung Cancer (Auckl) 2017 Aug 18 8 109 125 Search in Google Scholar

Navin, N. E. (2015). The first five years of single-cell cancer genomics and beyond. Genome Research, 25(10), 1499–1507. NavinN. E. 2015 The first five years of single-cell cancer genomics and beyond Genome Research 25 10 1499 1507 Search in Google Scholar

Craigie M, Squires J, Miles K. Can CT measures of tumour heterogeneity stratify risk for nodal metastasis in patients with non-small cell lung cancer? Clin Radiol. 2017 Oct;72(10):899.e1–899.e7 CraigieM SquiresJ MilesK Can CT measures of tumour heterogeneity stratify risk for nodal metastasis in patients with non-small cell lung cancer? Clin Radiol 2017 Oct 72 10 899.e1 899.e7 Search in Google Scholar

Nair VS, Gevaert O, Davidzon G, Napel S, Graves EE, Hoang CD, et al. Prognostic PET 18F-FDG uptake imaging features are associated with major oncogenomic alterations in patients with resected non-small cell lung cancer. Cancer research. 2012; 72(15):3725±34. NairVS GevaertO DavidzonG NapelS GravesEE HoangCD Prognostic PET 18F-FDG uptake imaging features are associated with major oncogenomic alterations in patients with resected non-small cell lung cancer Cancer research 2012 72 15 3725 34 Search in Google Scholar

Park S, Ha S, Lee SH, Paeng JC, Keam B, Kim TM, et al. Intratumoral heterogeneity characterized by pretreatment PET in non-small cell lung cancer patients predicts progression-free survival on EGFR tyrosine kinase inhibitor. PLoS One. 2018 Jan 31;13(1):e0189766. ParkS HaS LeeSH PaengJC KeamB KimTM Intratumoral heterogeneity characterized by pretreatment PET in non-small cell lung cancer patients predicts progression-free survival on EGFR tyrosine kinase inhibitor PLoS One 2018 Jan 31 13 1 e0189766 Search in Google Scholar

Dong ZY, Zhai HR, Hou QY, Su J, Liu SY, Yan HH, et al. Mixed Responses to Systemic Therapy Revealed Potential Genetic Heterogeneity and Poor Survival in Patients with Non-Small Cell Lung Cancer. Oncologist. 2017 Jan;22(1):61–69. DongZY ZhaiHR HouQY SuJ LiuSY YanHH Mixed Responses to Systemic Therapy Revealed Potential Genetic Heterogeneity and Poor Survival in Patients with Non-Small Cell Lung Cancer Oncologist 2017 Jan 22 1 61 69 Search in Google Scholar

Tricker EM, Xu C, Uddin S, Capelletti M, Ercan D, Ogino A, Pratilas CA, Rosen N, Gray NS, Wong KK, Jänne PA. Combined EGFR/MEK Inhibition Prevents the Emergence of Resistance in EGFR-Mutant Lung Cancer. Cancer Discov. 2015 Sep;5(9):960–971. TrickerEM XuC UddinS CapellettiM ErcanD OginoA PratilasCA RosenN GrayNS WongKK JännePA Combined EGFR/MEK Inhibition Prevents the Emergence of Resistance in EGFR-Mutant Lung Cancer Cancer Discov 2015 Sep 5 9 960 971 Search in Google Scholar

Chaib I, Karachaliou N, Pilotto S, Codony Servat J, Cai X, Li X, et al. Co-activation of STAT3 and YES-Associated Protein 1 (YAP1) Pathway in EGFR-Mutant NSCLC. J Natl Cancer Inst. 2017 Sep 1;109(9). ChaibI KarachaliouN PilottoS Codony ServatJ CaiX LiX Co-activation of STAT3 and YES-Associated Protein 1 (YAP1) Pathway in EGFR-Mutant NSCLC J Natl Cancer Inst 2017 Sep 1 109 9 Search in Google Scholar

Niederst MJ, Hu H, Mulvey HE, Lockerman EL, Garcia AR, Piotrowska Z, Sequist LV, Engelman JA. The Allelic Context of the C797S Mutation Acquired upon Treatment with Third-Generation EGFR Inhibitors Impacts Sensitivity to Subsequent Treatment Strategies. Clin Cancer Res. 2015 Sep 1;21(17):3924–33. NiederstMJ HuH MulveyHE LockermanEL GarciaAR PiotrowskaZ SequistLV EngelmanJA The Allelic Context of the C797S Mutation Acquired upon Treatment with Third-Generation EGFR Inhibitors Impacts Sensitivity to Subsequent Treatment Strategies Clin Cancer Res 2015 Sep 1 21 17 3924 33 Search in Google Scholar

Govindan R, Ding L, Griffith M, Subramanian J, Dees ND, Kanchi KL, et al. Genomic landscape of non-small cell lung cancer in smokers and never-smokers. Cell. 2012 Sep14;150(6):1121–34. GovindanR DingL GriffithM SubramanianJ DeesND KanchiKL Genomic landscape of non-small cell lung cancer in smokers and never-smokers Cell 2012 Sep 14 150 6 1121 34 Search in Google Scholar

Casadevall D, Clavé S, Taus Á, Hardy-Werbin M, Rocha P, Lorenzo M, Menéndez S, Salido M, Albanell J, Pijuan L, Arriola E. Heterogeneity of Tumor and Immune Cell PD-L1 Expression and Lymphocyte Counts in Surgical NSCLC Samples. Clin Lung Cancer. 2017 Nov;18(6):682–691.e5. CasadevallD ClavéS TausÁ Hardy-WerbinM RochaP LorenzoM MenéndezS SalidoM AlbanellJ PijuanL ArriolaE Heterogeneity of Tumor and Immune Cell PD-L1 Expression and Lymphocyte Counts in Surgical NSCLC Samples Clin Lung Cancer 2017 Nov 18 6 682 691.e5 Search in Google Scholar

Bassanelli M, Sioletic S, Martini M, Giacinti S, Viterbo A, Staddon A, Liberati F, Ceribelli A. Heterogeneity of PD-L1 Expression and Relationship with Biology of NSCLC. Anticancer Res. 2018 Jul;38(7):3789–3796. BassanelliM SioleticS MartiniM GiacintiS ViterboA StaddonA LiberatiF CeribelliA Heterogeneity of PD-L1 Expression and Relationship with Biology of NSCLC Anticancer Res 2018 Jul 38 7 3789 3796 Search in Google Scholar

Lee WC, Diao L, Wang J, Zhang J, Roarty EB, Varghese S, Chow CW, Fujimoto J, Behrens C, Cascone T, Peng W, Kalhor N, Moran CA, Weissferdt A, Johnson FM, William WN Jr, Swisher SG, Lee JJ, Hong WK, Heymach JV, Wistuba II, Futreal PA, Zhang J. Multiregion gene expression profiling reveals heterogeneity in molecular subtypes and immunotherapy response signatures in lung cancer. Mod Pathol. 2018 Jun;31(6):947–955. LeeWC DiaoL WangJ ZhangJ RoartyEB VargheseS ChowCW FujimotoJ BehrensC CasconeT PengW KalhorN MoranCA WeissferdtA JohnsonFM WilliamWNJr SwisherSG LeeJJ HongWK HeymachJV WistubaII FutrealPA ZhangJ Multiregion gene expression profiling reveals heterogeneity in molecular subtypes and immunotherapy response signatures in lung cancer Mod Pathol 2018 Jun 31 6 947 955 Search in Google Scholar

eISSN:
1792-362X
Language:
English
Publication timeframe:
4 times per year
Journal Subjects:
Medicine, Clinical Medicine, Internal Medicine, Haematology, Oncology