Combined treatment with metformin and gefitinib overcomes primary resistance to EGFR-TKIs with EGFR mutation via targeting IGF-1R signaling pathway

References

• InoueAKobayashiKMaemondoMUpdated overall survival results from a randomized phase III trial comparing gefitinib with carboplatin-paclitaxel for chemo-naive non-small cell lung cancer with sensitive EGFR gene mutations (NEJ002)Ann Oncol2013241545922967997
   PubMed Web of Science ®Google Scholar
• RosellRCarcerenyEGervaisRErlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trialLancet Oncol201213323924622285168
   PubMed Web of Science ®Google Scholar
• HanJYParkKKimSWFirst-SIGNAL: first-line single-agent iressa versus gemcitabine and cisplatin trial in never-smokers with adenocarcinoma of the lungJ Clin Oncol201230101122112822370314
   PubMed Web of Science ®Google Scholar
• MokTYangJJLamKCTreating patients with EGFR-sensitizing mutations: first line or second line – is there a difference?J Clin Oncol20133181081108823401448
   PubMed Web of Science ®Google Scholar
• JackmanDPaoWRielyGJClinical definition of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancerJ Clin Oncol201028235736019949011
   PubMed Web of Science ®Google Scholar
• LeeJKShinJYKimSPrimary resistance to epidermal growth factor receptor (EGFR) tyrosine kinase inhibitors (TKIs) in patients with non-small-cell lung cancer harboring TKI-sensitive EGFR mutations: an exploratory studyAnn Oncol20132482080208723559152
   PubMed Web of Science ®Google Scholar
• ParkKSRaffeldMMoonYWCRIPTO1 expression in EGFR-mutant NSCLC elicits intrinsic EGFR-inhibitor resistanceJ Clin Invest201412473003301524911146
   PubMed Web of Science ®Google Scholar
• MokTSWuYLThongprasertSGefitinib or carboplatin-paclitaxel in pulmonary adenocarcinomaN Engl J Med200936194795719692680
   PubMed Web of Science ®Google Scholar
• MaemondoMInoueAKobayashiKGefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFRN Engl J Med2010362252380238820573926
   PubMed Web of Science ®Google Scholar
• MitsudomiTMoritaSYatabeYGefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trialLancet Oncol201011212112820022809
   PubMed Web of Science ®Google Scholar
• ZhouCWuYLChenGErlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label, randomised, phase 3 studyLancet Oncol201112873574221783417
   PubMed Web of Science ®Google Scholar
• CaiHZhangYHanTKEverettRSThakkerDRCation-selective transporters are critical to the AMPK-mediated antiproliferative effects of metformin in human breast cancer cellsInt J Cancer201613892281229226669511
   PubMed Web of Science ®Google Scholar
• YangJWeiJWuYMetformin induces ER stress-dependent apoptosis through miR-708-5p/NNAT pathway in prostate cancerOncogenesis20154e15826075749
   PubMed Web of Science ®Google Scholar
• LiBLiXNiZDichloroacetate and metformin synergistically suppress the growth of ovarian cancer cellsOncotarget2016737594585947027449090
   PubMedGoogle Scholar
• QuinnBJKitagawaHMemmottRMGillsJJDennisPARepositioning metformin for cancer prevention and treatmentTrends Endocrinol Metab201324946948023773243
   PubMed Web of Science ®Google Scholar
• ChenHYaoWChuQSynergistic effects of metformin in combination with EGFR-TKI in the treatment of patients with advanced non-small cell lung cancer and type 2 diabetesCancer Lett201536919710226341687
   PubMed Web of Science ®Google Scholar
• LiLHanRXiaoHMetformin sensitizes EGFR-TKI-resistant human lung cancer cells in vitro and in vivo through inhibition of il-6 signaling and EMT reversalClin Cancer Res201420102714272624644001
   PubMed Web of Science ®Google Scholar
• SequistLVWaltmanBADias-SantagataDGenotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitorsSci Transl Med201137575ra26
   PubMed Web of Science ®Google Scholar
• ArcilaMEOxnardGRNafaKRebiopsy of lung cancer patients with acquired resistance to EGFR inhibitors and enhanced detection of the T790M mutation using a locked nucleic acid-based assayClin Cancer Res20111751169118021248300
   PubMed Web of Science ®Google Scholar
• YuHAArcilaMERekhtmanNAnalysis of tumor specimens at the time of acquired resistance to EGFR-TKI therapy in 155 patients with EGFR-mutant lung cancersClin Cancer Res20131982240224723470965
   PubMed Web of Science ®Google Scholar
• HuSFuWLiTAntagonism of EGFR and Notch limits resistance to EGFR inhibitors and radiation by decreasing tumor-initiating cell frequencySci Transl Med20179380eaag033928275151
   PubMed Web of Science ®Google Scholar
• ZanellaERGalimiFSassiFIGF2 is an actionable target that identifies a distinct subpopulation of colorectal cancer patients with marginal response to anti-EGFR therapiesSci Transl Med20157272272ra12
   Web of Science ®Google Scholar
• CappuzzoFJannePASkokanMMET increased gene copy number and primary resistance to gefitinib therapy in non-small-cell lung cancer patientsAnn Oncol200920229830418836087
   PubMed Web of Science ®Google Scholar
• TanakaASueoka-AraganeNNakamuraTCo-existence of positive MET FISH status with EGFR mutations signifies poor prognosis in lung adenocarcinoma patientsLung Cancer2012751899421733594
   PubMed Web of Science ®Google Scholar
• NgKPHillmerAMChuahCTA common BIM deletion polymorphism mediates intrinsic resistance and inferior responses to tyrosine kinase inhibitors in cancerNat Med201218452152822426421
   PubMed Web of Science ®Google Scholar
• SosMLKokerMWeirBAPTEN loss contributes to erlotinib resistance in EGFR-mutant lung cancer by activation of Akt and EGFRCancer Res2009693256326119351834
   PubMed Web of Science ®Google Scholar
• InukaiMToyookaSItoSPresence of epidermal growth factor receptor gene T790M mutation as a minor clone in non-small cell lung cancerCancer Res200666167854785816912157
   PubMed Web of Science ®Google Scholar
• SuKYChenHYLiKCPretreatment epidermal growth factor receptor (EGFR) T790M mutation predicts shorter EGFR tyrosine kinase inhibitor response duration in patients with non-small-cell lung cancerJ Clin Oncol201230443344022215752
   PubMed Web of Science ®Google Scholar
• DongSQuXLiWThe long non-coding RNA, GAS5, enhances gefitinib-induced cell death in innate EGFR tyrosine kinase inhibitor-resistant lung adenocarcinoma cells with wide-type EGFR via down-regulation of the IGF-1R expressionJ Hematol Oncol201584325925741
   PubMed Web of Science ®Google Scholar
• MasagoKFujitaSTogashiYClinical significance of epidermal growth factor receptor mutations and insulin-like growth factor 1 and its binding protein 3 in advanced non-squamous non-small cell lung cancerOncol Rep201126479580321805046
   PubMed Web of Science ®Google Scholar
• KimGWSongJSChoiCMMultiple resistant factors in lung cancer with primary resistance to EGFR-TK inhibitors confer poor survivalLung Cancer201588213914625724261
   PubMed Web of Science ®Google Scholar
• IchiteNChouguleMBJacksonTFulzeleSVSafeSSinghMEnhancement of docetaxel anticancer activity by a novel diindolyl-methane compound in human non-small cell lung cancerClin Cancer Res200915254355219147759
   PubMed Web of Science ®Google Scholar
• MorgilloFWooJKKimESHongWKLeeHYHeterodimerization of insulin-like growth factor receptor/epidermal growth factor receptor and induction of survivin expression counteract the antitumor action of erlotinibCancer Res20066620101001011117047074
   PubMed Web of Science ®Google Scholar
• MorgilloFKimWYKimESCiardielloFHongWKLeeHYImplication of the insulin-like growth factor-IR pathway in the resistance of non-small cell lung cancer cells to treatment with gefitinibClin Cancer Res20071392795280317473213
   PubMed Web of Science ®Google Scholar
• GuixMFaberACWangSEAcquired resistance to EGFR tyrosine kinase inhibitors in cancer cells is mediated by loss of IGF-binding proteinsJ Clin Invest200811872609261918568074
   PubMed Web of Science ®Google Scholar
• CortotABRepellinCEShimamuraTResistance to irreversible EGF receptor tyrosine kinase inhibitors through a multistep mechanism involving the IGF1R pathwayCancer Res201373283484323172312
   PubMed Web of Science ®Google Scholar
• ChoiYJRhoJKJeonBSCombined inhibition of IGFR enhances the effects of gefitinib in H1650: a lung cancer cell line with EGFR mutation and primary resistance to EGFR-TK inhibitorsCancer Che-mother Pharmacol2010662381388
   Web of Science ®Google Scholar
• SheppardKKinrossKMSolomonBPearsonRBPhillipsWATargeting PI3 kinase/AKT/mTOR signaling in cancerCrit Rev Oncog2012171699522471665
   PubMedGoogle Scholar
• Vázquez de la TorreAJunyentFFolchJPI3k/akt inhibition induces apoptosis through p38 activation in neuronsPharmacol Res201370111612523376356
   PubMed Web of Science ®Google Scholar
• LimSMKimHRChoEKTargeted sequencing identifies genetic alterations that confer primary resistance to EGFR tyrosine kinase inhibitor (Korean Lung Cancer Consortium)Oncotarget2016724363113632027121209
   PubMedGoogle Scholar
• GallagherEJLeRoithDThe proliferating role of insulin and insulin-like growth factors in cancerTrends Endocrinol Metab2010211061061820663687
   PubMed Web of Science ®Google Scholar
• van der VeekenJOliveiraSSchiffelersRMStormGvan Bergen En HenegouwenPMRooversRCCrosstalk between epidermal growth factor receptor- and insulin-like growth factor-1 receptor signaling: implications for cancer therapyCurr Cancer Drug Targets20099674876019754359
   PubMed Web of Science ®Google Scholar
• PrenekLBoldizsárFKugyelkaRThe regulation of the mitochondrial apoptotic pathway by glucocorticoid receptor in collaboration with Bcl-2 family proteins in developing T cellsApoptosis201722223925327888447
   PubMed Web of Science ®Google Scholar
• IshiiYNhiayiMKTseEKnockout serum replacement promotes cell survival by preventing BIM from inducing mitochondrial cytochrome C releasePLoS One20151010e014058526473951
   PubMed Web of Science ®Google Scholar
• RosichLSaborit-VillarroyaILópez-GuerraMThe phospha-tidylinositol-3-kinase inhibitor NVP-BKM120 overcomes resistance signals derived from microenvironment by regulating the Akt/FoxO3a/Bim axis in chronic lymphocytic leukemia cellsHaematologica201398111739174723850807
   PubMed Web of Science ®Google Scholar
• ArouiSDardevetLNajlaouiFPTEN-regulated AKT/FoxO3a/Bim signaling contributes to human cell glioblastoma apoptosis by platinum-maurocalcin conjugateInt J Biochem Cell Biol201677pt A152227210502
   PubMed Web of Science ®Google Scholar
• LuoZZangMGuoWAMPK as a metabolic tumor suppressor: control of metabolism and cell growthFuture Oncol20106345747020222801
   PubMed Web of Science ®Google Scholar
• XuJNZengCZhouYMetformin inhibits StAR expression in human endometriotic stromal cells via AMPK mediated disruption of CREB-CRTC2 complex formationJ Clin Endocrinol Metab20149982795280324823468
   PubMed Web of Science ®Google Scholar
• Vazquez-MartinAOliveras-FerrarosCDel BarcoSIf mammalian target of metformin indirectly is mammalian target of rapamycin, then the insulin-like growth factor-1 receptor axis will audit the efficacy of metformin in cancer clinical trialsJ Clin Oncol20092733e207e20919858375
   PubMed Web of Science ®Google Scholar
• Martin-CastilloBVazquez-MartinAOliveras-FerrarosCMenendezJAMetformin and cancer: doses, mechanisms and the dandelion and hormetic phenomenaCell Cycle2010961057106420305377
   PubMed Web of Science ®Google Scholar
• Abo-ElmattyDMAhmedEATawfikMKHelmySAMetformin enhancing the antitumor efficacy of carboplatin against Ehrlich solid carcinoma grown in diabetic mice: effect on IGF-1 and tumoral expression of IGF-1 receptorsInt Immunopharmacol201744728628088698
   PubMed Web of Science ®Google Scholar
• TandonMChenZOthmanAHPratapJRole of Runx2 in IGF-1Rβ/Akt-and AMPK/Erk-dependent growth, survival and sensitivity towards metfor-min in breast cancer bone metastasisOncogene201635364730474026804175
   PubMed Web of Science ®Google Scholar
• KarneviESaidKAnderssonRRosendahlAHMetformin-mediated growth inhibition involves suppression of the IGF-I receptor signalling pathway in human pancreatic cancer cellsBMC Cancer20131323523663483
   PubMed Web of Science ®Google Scholar
• LiLWangYPengTMetformin restores crizotinib sensitivity in crizotinib-resistant human lung cancer cells through inhibition of IGF1-R signaling pathwayOncotarget2016723344423445227144340
   PubMedGoogle Scholar
• SalaniBMaffioliSHamoudaneMCaveolin-1 is essential for metformin inhibitory effect on IGF1 action in non-small-cell lung cancer cellsFASEB J201226278879822038047
   PubMed Web of Science ®Google Scholar
• XiaoZSperlBUllrichAKnyazevPMetformin and salinomycin as the best combination for the eradication of NSCLC monolayer cells and their alveospheres (cancer stem cells) irrespective of EGFR, KRAS, EML4/ALK and LKB1 statusOncotarget2014524128771289025375092
   PubMedGoogle Scholar
• MorgilloFSassoFCDella CorteCMSynergistic effects of metformin treatment in combination with gefitinib, a selective EGFR tyrosine kinase inhibitor, in LKB1 wild-type NSCLC cell linesClin Cancer Res201319133508351923695170
   PubMed Web of Science ®Google Scholar