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Review

Targeting cancer stem cells: emerging role of Nanog transcription factor

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Pages 1207-1220 | Published online: 04 Sep 2013

References

  • WichaMSLiuSDontuGCancer stem cells: an old idea – a paradigm shiftCancer Res200666418831890 discussion 1895–188616488983
  • VisvaderJELindemanGJCancer stem cells in solid tumours: accumulating evidence and unresolved questionsNat Rev Cancer200881075576818784658
  • JiangFQiuQKhannaAAldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancerMol Cancer Res20097333033819276181
  • LeeTKCastilhoACheungVCTangKHMaSNgIOCD24(+) liver tumor-initiating cells drive self-renewal and tumor initiation through STAT3-mediated NANOG regulationCell Stem Cell201191506321726833
  • IbrahimEEBabaei-JadidiRSaadeddinAEmbryonic NANOG activity defines colorectal cancer stem cells and modulates through AP1- and TCF-dependent mechanismsStem Cells201230102076208722851508
  • BaoSWuQMcLendonREGlioma stem cells promote radioresistance by preferential activation of the DNA damage responseNature2006444712075676017051156
  • BertoliniGRozLPeregoPHighly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatmentProc Natl Acad Sci U S A200910638162811628619805294
  • EramoALottiFSetteGIdentification and expansion of the tumorigenic lung cancer stem cell populationCell Death Differ200815350451418049477
  • PrinceMESivanandanRKaczorowskiAIdentification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinomaProc Natl Acad Sci U S A2007104397397817210912
  • BussolatiBBrunoSGrangeCFerrandoUCamussiGIdentification of a tumor-initiating stem cell population in human renal carcinomasFASEB J200822103696370518614581
  • SinghSKHawkinsCClarkeIDIdentification of human brain tumour initiating cellsNature2004432701539640115549107
  • BonnetDDickJEHuman acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cellNat Med1997377307379212098
  • Al-HajjMWichaMSBenito-HernandezAMorrisonSJClarkeMFProspective identification of tumorigenic breast cancer cellsProc Natl Acad Sci U S A200310073983398812629218
  • GalliRBindaEOrfanelliUIsolation and characterization of tumorigenic, stem-like neural precursors from human glioblastomaCancer Res200464197011702115466194
  • HemmatiHDNakanoILazareffJACancerous stem cells can arise from pediatric brain tumorsProc Natl Acad Sci U S A200310025151781518314645703
  • LapidotTSirardCVormoorJA cell initiating human acute myeloid leukaemia after transplantation into SCID miceNature199436764646456487509044
  • O’BrienCAPollettAGallingerSDickJEA human colon cancer cell capable of initiating tumour growth in immunodeficient miceNature2007445712310611017122772
  • Ricci-VitianiLLombardiDGPilozziEIdentification and expansion of human colon-cancer-initiating cellsNature2007445712311111517122771
  • SchattonTMurphyGFFrankNYIdentification of cells initiating human melanomasNature2008451717634534918202660
  • SinghSKClarkeIDTerasakiMIdentification of a cancer stem cell in human brain tumorsCancer Res200363185821582814522905
  • FillmoreCMKuperwasserCHuman breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapyBreast Cancer Res2008102R2518366788
  • WakamatsuYSakamotoNOoHZExpression of cancer stem cell markers ALDH1, CD44 and CD133 in primary tumor and lymph node metastasis of gastric cancerPathol Int201262211211922243781
  • TirinoVCamerlingoRFrancoRThe role of CD133 in the identification and characterisation of tumour-initiating cells in non-small-cell lung cancerEur J Cardiothorac Surg200936344645319464919
  • SalvenPMustjokiSAlitaloRAlitaloKRafiiSVEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cellsBlood2003101116817212393704
  • YinAHMiragliaSZanjaniEDAC133, a novel marker for human hematopoietic stem and progenitor cellsBlood19979012500250129389720
  • SaigusaSTanakaKToiyamaYCorrelation of CD133, OCT4, and SOX2 in rectal cancer and their association with distant recurrence after chemoradiotherapyAnn Surg Oncol200916123488349819657699
  • DasBTsuchidaRMalkinDKorenGBaruchelSYegerHHypoxia enhances tumor stemness by increasing the invasive and tumorigenic side population fractionStem Cells20082671818183018467664
  • HoMMNgAVLamSHungJYSide population in human lung cancer cell lines and tumors is enriched with stem-like cancer cellsCancer Res200767104827483317510412
  • JiangYHeYLiHExpressions of putative cancer stem cell markers ABCB1, ABCG2, and CD133 are correlated with the degree of differentiation of gastric cancerGastric cancer201215444045022395309
  • FangDNguyenTKLeishearKA tumorigenic subpopulation with stem cell properties in melanomasCancer Res200565209328933716230395
  • ZhangJEspinozaLAKindersRJNANOG modulates stemness in human colorectal cancerOncogene Epub10222012
  • ZbindenMDuquetALorente-TrigosANgwabytSNBorgesIRuiz i AltabaANANOG regulates glioma stem cells and is essential in vivo acting in a cross-functional network with GLI1 and p53EMBO J201029152659267420581802
  • ShanJShenJLiuLNanog regulates self-renewal of cancer stem cells through the insulin-like growth factor pathway in human hepatocellular carcinomaHepatology20125631004101422473773
  • ChiouSHWangMLChouYTCoexpression of oct4 and nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem cell-like properties and epithelial-mesenchymal transdifferentiationCancer Res20107024104331044421159654
  • MitsuiKTokuzawaYItohHThe homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cellsCell2003113563164212787504
  • ChambersIColbyDRobertsonMFunctional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cellsCell2003113564365512787505
  • HyslopLStojkovicMArmstrongLDownregulation of NANOG induces differentiation of human embryonic stem cells to extraembryonic lineagesStem Cells20052381035104315983365
  • WangJRaoSChuJA protein interaction network for pluripotency of embryonic stem cellsNature2006444711736436817093407
  • KashyapVRezendeNCScotlandKBRegulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAsStem Cells Dev20091871093110819480567
  • WangJLevasseurDNOrkinSHRequirement of Nanog dimerization for stem cell self-renewal and pluripotencyProc Natl Acad Sci U S A2008105176326633118436640
  • PanGThomsonJANanog and transcriptional networks in embryonic stem cell pluripotencyCell Res2007171424917211451
  • BoothHAHollandPWEleven daughters of NANOGGenomics200484222923815233988
  • ZhangJWangXLiMNANOGP8 is a retrogene expressed in cancersFEBS J200627381723173016623708
  • FairbanksDJFairbanksADOgdenTHParkerGJMaughanPJNANOGP8: evolution of a human-specific retro-oncogeneG3 (Bethesda)20122111447145723173096
  • JeterCRBadeauxMChoyGFunctional evidence that the self-renewal gene NANOG regulates human tumor developmentStem Cells2009275993100519415763
  • OhJHDoHJYangHMIdentification of a putative transactivation domain in human NanogExp Mol Med200537325025416000880
  • DoHJLimHYKimJHSongHChungHMAn intact homeobox domain is required for complete nuclear localization of human NanogBiochem Biophys Res Commun2007353377077517196939
  • ParkSWDoHJHuhSHIdentification of a putative nuclear export signal motif in human NANOG homeobox domainBiochem Biophys Res Commun2012421348448922516749
  • ParkIHZhaoRWestJAReprogramming of human somatic cells to pluripotency with defined factorsNature2008451717514114618157115
  • TheunissenTWCostaYRadzisheuskayaAReprogramming capacity of Nanog is functionally conserved in vertebrates and resides in a unique homeodomainDevelopment2011138224853486522028025
  • KurodaTTadaMKubotaHOctamer and Sox elements are required for transcriptional cis regulation of Nanog gene expressionMol Cell Biol20052562475248515743839
  • DoHJLeeWYLimHYTwo potent transactivation domains in the C-terminal region of human NANOG mediate transcriptional activation in human embryonic carcinoma cellsJ Cell Biochem200910661079108919229867
  • WilliamsRLHiltonDJPeaseSMyeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cellsNature198833662006846873143916
  • NiwaHMiyazakiJSmithAGQuantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cellsNat Genet200024437237610742100
  • AmsterdamARaananCSchreiberLFreyhanOSchechtmanLGivolDLocalization of the stem cell markers LGR5 and Nanog in the normal and the cancerous human ovary and their inter-relationshipActa Histochem2013115433033823092806
  • EzehUITurekPJReijoRAClarkATHuman embryonic stem cell genes OCT4, NANOG, STELLAR, and GDF3 are expressed in both seminoma and breast carcinomaCancer2005104102255226516228988
  • HartAHHartleyLParkerKThe pluripotency homeobox gene NANOG is expressed in human germ cell tumorsCancer2005104102092209816206293
  • Hoei-HansenCEAlmstrupKNielsenJEStem cell pluripotency factor NANOG is expressed in human fetal gonocytes, testicular carcinoma in situ and germ cell tumoursHistopathology2005471485615982323
  • LinTDingYQLiJMOverexpression of Nanog protein is associated with poor prognosis in gastric adenocarcinomaMed Oncol201229287888521336986
  • GuoYLiuSWangPExpression profile of embryonic stem cell-associated genes Oct4, Sox2 and Nanog in human gliomasHistopathology201159476377522014056
  • PanYJiaoJZhouCChengQHuYChenHNanog is highly expressed in ovarian serous cystadenocarcinoma and correlated with clinical stage and pathological gradePathobiology201077628328821266826
  • WenJParkJYParkKHOct4 and Nanog expression is associated with early stages of pancreatic carcinogenesisPancreas201039562262620173672
  • ChiouSHYuCCHuangCYPositive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinomaClin Cancer Res200814134085409518593985
  • GillisAJStoopHBiermannKExpression and interdependencies of pluripotency factors LIN28, OCT3/4, NANOG and SOX2 in human testicular germ cells and tumours of the testisInt J Androl2011344 Pt 2e160e17421631526
  • ZhouXZhouYPHuangGRExpression of the stem cell marker, Nanog, in human endometrial adenocarcinomaInt J Gynecol Pathol201130326227021464727
  • NagataTShimadaYSekineSPrognostic significance of NANOG and KLF4 for breast cancerBreast cancer2012
  • LeeMNamEJKimSWKimSKimJHKimYTPrognostic impact of the cancer stem cell-related marker NANOG in ovarian serous carcinomaInt J Gynecol Cancer20122291489149623095773
  • MengHMZhengPWangXYOverexpression of nanog predicts tumor progression and poor prognosis in colorectal cancerCancer Biol Ther201094
  • NiuCSLiDXLiuYHFuXMTangSFLiJExpression of NANOG in human gliomas and its relationship with undifferentiated glioma cellsOncol Rep201126359360121573506
  • JeterCRLiuBLiuXNANOG promotes cancer stem cell characteristics and prostate cancer resistance to androgen deprivationOncogene201130363833384521499299
  • PoAFerrettiEMieleEHedgehog controls neural stem cells through p53-independent regulation of NanogEMBO J201029152646265820581804
  • VillasanteAPiazzollaDLiHGomez-LopezGDjabaliMSerranoMEpigenetic regulation of Nanog expression by Ezh2 in pluripotent stem cellsCell Cycle20111091488149821490431
  • XuFDaiCZhangRZhaoYPengSJiaCNanog: a potential biomarker for liver metastasis of colorectal cancerDig Dis Sci20125792340234622562535
  • HeAQiWHuangYCD133 expression predicts lung metastasis and poor prognosis in osteosarcoma patients: A clinical and experimental studyExp Ther Med20124343544123181114
  • LeungELFiscusRRTungJWNon-small cell lung cancer cells expressing CD44 are enriched for stem cell-like propertiesPLoS One2010511e1406221124918
  • HanJZhangFYuMRNA interference-mediated silencing of NANOG reduces cell proliferation and induces G0/G1 cell cycle arrest in breast cancer cellsCancer Lett20123211808822381696
  • ChoiSCChoiJHParkCYAhnCMHongSJLimDSNanog regulates molecules involved in stemness and cell cycle-signaling pathway for maintenance of pluripotency of P19 embryonal carcinoma stem cellsJ Cell Physiol2012227113678369222378194
  • SiuMKWongESKongDSStem cell transcription factor NANOG controls cell migration and invasion via dysregulation of E-cadherin and FoxJ1 and contributes to adverse clinical outcome in ovarian cancersOncogene201332303500350922945654
  • NohKHKimBWSongKHNanog signaling in cancer promotes stem-like phenotype and immune evasionJ Clin Invest2012122114077409323093782
  • NohKHLeeYHJeonJHCancer vaccination drives Nanog-dependent evolution of tumor cells toward an immune-resistant and stem-like phenotypeCancer Res20127271717172722337995
  • GuTTLiuSYZhengPSCytoplasmic NANOG-positive stromal cells promote human cervical cancer progressionAm J Pathol2012181265266122683467
  • KalmarTLimCHaywardPRegulated fluctuations in nanog expression mediate cell fate decisions in embryonic stem cellsPLoS Biol200977e100014919582141
  • MacArthurBDSevillaALenzMNanog-dependent feedback loops regulate murine embryonic stem cell heterogeneityNat Cell Biol201214111139114723103910
  • GolubovskayaVMFAK and Nanog cross talk with p53 in cancer stem cellsAnticancer Agents Med Chem201313457658022934707
  • LinTChaoCSaitoSp53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expressionNat Cell Biol20057216517115619621
  • MoonJHKwonSJunEKNanog-induced dedifferentiation of p53-deficient mouse astrocytes into brain cancer stem-like cellsBiochem Biophys Res Commun2011412117518121810410
  • HongHTakahashiKIchisakaTSuppression of induced pluripotent stem cell generation by the p53-p21 pathwayNature200946072591132113519668191
  • YuJVodyanikMASmuga-OttoKInduced pluripotent stem cell lines derived from human somatic cellsScience200731858581917192018029452
  • ClementVSanchezPde TriboletNRadovanovicIRuiz i AltabaAHEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicityCurr Biol200717216517217196391
  • BourillotPYAksoyISchreiberVNovel STAT3 target genes exert distinct roles in the inhibition of mesoderm and endoderm differentiation in cooperation with NanogStem Cells20092781760177119544440
  • TorresJWattFMNanog maintains pluripotency of mouse embryonic stem cells by inhibiting NFkappaB and cooperating with Stat3Nat Cell Biol200810219420118223644
  • BourguignonLYEarleCWongGSpevakCCKruegerKStem cell marker (Nanog) and Stat-3 signaling promote MicroRNA-21 expression and chemoresistance in hyaluronan/CD44-activated head and neck squamous cell carcinoma cellsOncogene201231214916021685938
  • SuzukiARayaAKawakamiYNanog binds to Smad1 and blocks bone morphogenetic protein-induced differentiation of embryonic stem cellsProc Natl Acad Sci U S A200610327102941029916801560
  • TangYLuoYJiangZJak/Stat3 signaling promotes somatic cell reprogramming by epigenetic regulationStem Cells201230122645265622968989
  • HawkinsKMohametLRitsonSMerryCLWardCME-cadherin and, in its absence, N-cadherin promotes Nanog expression in mouse embryonic stem cells via STAT3 phosphorylationStem Cells20123091842185122696497
  • TayYZhangJThomsonAMLimBRigoutsosIMicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiationNature200845572161124112818806776
  • TayYMTamWLAngYSMicroRNA-134 modulates the differentiation of mouse embryonic stem cells, where it causes post-transcriptional attenuation of Nanog and LRH1Stem Cells2008261172917916804
  • NiuCSYangYChengCDMiR-134 regulates the proliferation and invasion of glioblastoma cells by reducing Nanog expressionInt J Oncol20134251533154023467648
  • PennaEOrsoFCiminoDmicroRNA-214 contributes to melanoma tumour progression through suppression of TFAP2CEMBO J201130101990200721468029
  • YangHKongWHeLMicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTENCancer Res200868242543318199536
  • XuCXXuMTanLMicroRNA miR-214 regulates ovarian cancer cell stemness by targeting p53/NanogJ Biol Chem201228742349703497822927443
  • FarehMTurchiLVirolleVThe miR 302-367 cluster drastically affects self-renewal and infiltration properties of glioma-initiating cells through CXCR4 repression and consequent disruption of the SHH-GLI-NANOG networkCell Death Differ201219223224421720384
  • PiestunDKochupurakkalBSJacob-HirschJNanog transforms NIH3T3 cells and targets cell-type restricted genesBiochem Biophys Res Commun2006343127928516540082
  • LinYLHanZBXiongFYMalignant transformation of 293 cells induced by ectopic expression of human NanogMol Cell Biochem20113511–210911621246261
  • ParkSWLimHYDoHJRegulation of human growth and differentiation factor 3 gene expression by NANOG in human embryonic carcinoma NCCIT cellsFEBS Lett2012586193529353522963770
  • YinXLiYWZhangBHCoexpression of stemness factors Oct4 and Nanog predict liver resectionAnn Surg Oncol20121992877288722461131
  • YangLZhangXZhangMIncreased nanog expression promotes tumor development and Cisplatin resistance in human esophageal cancer cellsCell Physiol Biochem201230494395223221432
  • TsaiLLYuCCChangYCYuCHChouMYMarkedly increased Oct4 and Nanog expression correlates with cisplatin resistance in oral squamous cell carcinomaJ Oral Pathol Med201140862162821342274
  • BourguignonLYPeyrollierKXiaWGiladEHyaluronan-CD44 interaction activates stem cell marker Nanog, Stat-3-mediated MDR1 gene expression, and ankyrin-regulated multidrug efflux in breast and ovarian tumor cellsJ Biol Chem200828325176351765118441325
  • XuYA new role for p53 in maintaining genetic stability in embryonic stem cellsCell Cycle20054336336415701975
  • van den BergDLZhangWYatesAEstrogen-related receptor beta interacts with Oct4 to positively regulate Nanog gene expressionMol Cell Biol200828195986599518662995
  • FestucciaNOsornoRHalbritterFEsrrb is a direct Nanog target gene that can substitute for Nanog function in pluripotent cellsCell Stem Cell201211447749023040477
  • AbholdELKiangARahimyEEGFR kinase promotes acquisition of stem cell-like properties: a potential therapeutic target in head and neck squamous cell carcinoma stem cellsPLoS One201272e3245922384257
  • YangJLiaoDChenCTumor-associated macrophages regulate murine breast cancer stem cells through a novel paracrine EGFR/Stat3/Sox-2 signaling pathwayStem Cells201331224825823169551
  • YiDKuoSZZhengHActivation of PDGFR and EGFR promotes the acquisition of a stem cell-like phenotype in schwannomasOtol Neurot201233916401647
  • MaLZhangGMiaoXBCancer stem-like cell properties are regulated by EGFR/AKT/beta-catenin signaling and preferentially inhibited by gefitinib in nasopharyngeal carcinomaFEBS J201328092027204123461856
  • HyderAEhnertSHinzHNusslerAKFandrichFUngefrorenHEGF and HB-EGF enhance the proliferation of programmable cells of monocytic origin (PCMO) through activation of MEK/ERK signaling and improve differentiation of PCMO-derived hepatocyte-like cellsCell Commun Signal20121012322873932
  • WatanabeSUmeharaHMurayamaKOkabeMKimuraTNakanoTActivation of Akt signaling is sufficient to maintain pluripotency in mouse and primate embryonic stem cellsOncogene200625192697270716407845
  • StormMPBoneHKBeckCGRegulation of Nanog expression by phosphoinositide 3-kinase-dependent signaling in murine embryonic stem cellsJ Biol Chem200728296265627317204467
  • XuCXieDYuSCbeta-Catenin/POU5F1/SOX2 transcription factor complex mediates IGF-I receptor signaling and predicts poor prognosis in lung adenocarcinomaCancer Res201373103181318923539445
  • LindgrenAGNatsuharaKTianELoss of Pten causes tumor initiation following differentiation of murine pluripotent stem cells due to failed repression of NanogPLoS One201161e1647821304588
  • HoBOlsonGFigelSGelmanICanceWGGolubovskayaVMNanog increases focal adhesion kinase (FAK) promoter activity and expression and directly binds to FAK protein to be phosphorylatedJ Biol Chem201228722186561867322493428
  • WangMLPanCMChiouSHOncostatin m modulates the mesenchymal-epithelial transition of lung adenocarcinoma cells by a mesenchymal stem cell-mediated paracrine effectCancer Res201272226051606423139208
  • ZhuYSunZHanQHuman mesenchymal stem cells inhibit cancer cell proliferation by secreting DKK-1Leukemia200923592593319148141
  • OrimoAGuptaPBSgroiDCStromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretionCell2005121333534815882617
  • SunZHanQZhuYNANOG has a role in mesenchymal stem cells’ immunomodulatory effectStem Cells Dev20112091521152821235326
  • DuYShiLWangTLiuZWangZNanog siRNA plus Cisplatin may enhance the sensitivity of chemotherapy in esophageal cancerJ Cancer Res Clin Oncol2012138101759176722714588
  • ShaoWPaulAAbbasiSA novel polyethyleneimine-coated adeno-associated virus-like particle formulation for efficient siRNA delivery in breast cancer therapy: preparation and in vitro analysisInt J Nanomedicine201271575158622619514
  • ChiouGYCherngJYHsuHSCationic polyurethanes-short branch PEI-mediated delivery of Mir145 inhibited epithelial-mesenchymal transdifferentiation and cancer stem-like properties and in lung adenocarcinomaJ Control Release2012159224025022285547
  • PengCHCherngJYChiouGYDelivery of Oct4 and SirT1 with cationic polyurethanes-short branch PEI to aged retinal pigment epitheliumBiomaterials201132349077908821890195
  • LoWLChienYChiouGYNuclear localization signal-enhanced RNA interference of EZH2 and Oct4 in the eradication of head and neck squamous cell carcinoma-derived cancer stem cellsBiomaterials201233143693370922361100
  • MachidaKTsukamotoHMkrtchyanHToll-like receptor 4 mediates synergism between alcohol and HCV in hepatic oncogenesis involving stem cell marker NanogProc Natl Acad Sci U S A200910651548155319171902
  • HeddlestonJMLiZMcLendonREHjelmelandABRichJNThe hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotypeCell Cycle20098203274328419770585
  • KimJSKimBSKimJParkCSChungIYThe phosphoinositide-3-kinase/Akt pathway mediates the transient increase in Nanog expression during differentiation of F9 cellsArch Pharm Res20103371117112520661723
  • TsaiCCSuPFHuangYFYewTLHungSCOct4 and Nanog directly regulate Dnmt1 to maintain self-renewal and undifferentiated state in mesenchymal stem cellsMol Cell201247216918222795133