The RANK/RANKL/OPG system in tumorigenesis and metastasis of cancer stem cell: potential targets for anticancer therapy

References

• HofbauerLCHeufelderAERole of receptor activator of nuclear factor-κB ligand and osteoprotegerin in bone cell biologyJ Mol Med2001795–624325311485016
   PubMed Web of Science ®Google Scholar
• WongBRJosienRLeeSYVologodskaiaMSteinmanRMChoiYThe TRAF family of signal transducers mediates NF-κB activation by the TRANCE receptorJ Biol Chem19982734328355283599774460
   PubMed Web of Science ®Google Scholar
• BoyceBFXingLBiology of RANK, RANKL, and osteoprotegerinArthritis Res Ther2007911
   Google Scholar
• ChengMLFongLEffects of RANKL-targeted therapy in immunity and cancerFront Oncol2014332924432249
   PubMedGoogle Scholar
• FataJEKongYYLiJThe osteoclast differentiation factor osteoprotegerin-ligand is essential for mammary gland developmentCell20001031415011051546
   PubMed Web of Science ®Google Scholar
• HanadaRLeibbrandtAHanadaTCentral control of fever and female body temperature by RANKL/RANKNature2009462727250550919940926
   PubMed Web of Science ®Google Scholar
• HanadaRThe new function of RANKL/RANK system in the central nervous systemsNeurosci Res201171e22
   PubMedGoogle Scholar
• BucayNSarosiIDunstanCROsteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcificationGenes Dev1998129126012689573043
   PubMed Web of Science ®Google Scholar
• NdipAWilliamsAJudeEBThe RANKL/RANK/OPG signaling pathway mediates medial arterial calcification in diabetic Charcot neuroarthropathyDiabetes20116082187219621659498
   PubMed Web of Science ®Google Scholar
• OsakoMKNakagamiHShimamuraMCross-talk of receptor activator of nuclear factor-κB ligand signaling with renin–angiotensin system in vascular calcificationArterioscler Thromb Vasc Biol20133361287129623580147
   PubMed Web of Science ®Google Scholar
• ColemanREMetastatic bone disease: clinical features, pathophysiology and treatment strategiesCancer Treat Rev200127316517611417967
   PubMed Web of Science ®Google Scholar
• SchmiedelBJScheibleCANueblingTRANKL expression, function, and therapeutic targeting in multiple myeloma and chronic lymphocytic leukemiaCancer Res201373268369423139212
   PubMed Web of Science ®Google Scholar
• DeleaTEMcKiernanJBrandmanJImpact of skeletal complications on total medical care costs among patients with bone metastases of lung cancerJ Thorac Oncol20061657157617409919
   PubMed Web of Science ®Google Scholar
• LewisMAHendricksonAWMoynihanTJOncologic emergencies: pathophysiology, presentation, diagnosis, and treatmentCA Cancer J Clin201161528731421858793
   PubMed Web of Science ®Google Scholar
• IbrahimTRicciMScarpiEBongiovanniARicciRRivaNRANKL: a promising circulating marker for bone metastasis responseOncol Lett2016122970297527698885
   PubMed Web of Science ®Google Scholar
• HerzogCEOverview of sarcomas in the adolescent and young adult populationJ Pediatr Hematol Oncol200527421521815838394
   PubMed Web of Science ®Google Scholar
• GrimaudESoubigouLCouillaudSReceptor activator of nuclear factor κB ligand (RANKL)/osteoprotegerin (OPG) ratio is increased in severe osteolysisAm J Pathol200316352021203114578201
   PubMedGoogle Scholar
• LamoureuxFRichardPWittrantYTherapeutic relevance of osteoprotegerin gene therapy in osteosarcoma: blockade of the vicious cycle between tumor cell proliferation and bone resorptionCancer Res200767157308731817671200
   PubMed Web of Science ®Google Scholar
• ChenYDi GrappaMAMolyneuxSDRANKL blockade prevents and treats aggressive osteosarcomasSci Transl Med20157317317ra197
   PubMed Web of Science ®Google Scholar
• PearseRNSordilloEMYaccobySMultiple myeloma disrupts the TRANCE/osteoprotegerin cytokine axis to trigger bone destruction and promote tumor progressionProc Natl Acad Sci U S A20019820115811158611562486
   PubMedGoogle Scholar
• LewinJThomasDDenosumab: a new treatment option for giant cell tumor of boneDrugs Today (Barc)2013491169370024308016
   PubMedGoogle Scholar
• SantiniDPerroneGRoatoIExpression pattern of receptor activator of NFκB (RANK) in a series of primary solid tumors and related bone metastasesJ Cell Physiol2011226378078420857484
   PubMed Web of Science ®Google Scholar
• DougallWCMolecular pathways: osteoclast-dependent and osteoclast-independent roles of the RANKL/RANK/OPG pathway in tumorigenesis and metastasisClin Cancer Res201218232633522031096
   PubMed Web of Science ®Google Scholar
• Gonzalez-SuarezEJacobAPJonesJRANK ligand mediates progestin-induced mammary epithelial proliferation and carcinogenesisNature2010468732010310720881963
   PubMed Web of Science ®Google Scholar
• AlbanyCHahnNMNovel bone-targeting agents in prostate cancerProstate Cancer Prostatic Dis201417211211824662963
   PubMedGoogle Scholar
• KieselLKohlARole of the RANK/RANKL pathway in breast cancerMaturitas201686101626921922
   PubMed Web of Science ®Google Scholar
• TsubakiMTakedaTYoshizumiMUedaEItohTImanoMRANK–RANKL interactions are involved in cell adhesion-mediated drug resistance in multiple myeloma cell linesTumour Biol20163779099911026762414
   PubMedGoogle Scholar
• NolanEVaillantFBranstetterDRANK ligand as a potential target for breast cancer prevention in BRCA1-mutation carriersNat Med201622893393927322743
   PubMed Web of Science ®Google Scholar
• AzimHAPeccatoriFABrohéeSRANK-ligand (RANKL) expression in young breast cancer patients and during pregnancyBreast Cancer Res20151712425849336
   PubMed Web of Science ®Google Scholar
• SiglVOwusu-BoaiteyKJoshiPARANKL/RANK control Brca1 mutation-driven mammary tumorsCell Res201626776177427241552
   PubMed Web of Science ®Google Scholar
• ZhangLTengYFanYThe E3 ubiquitin ligase Cbl-b improves the prognosis of RANK positive breast cancer patients by inhibiting RANKL-induced cell migration and metastasisOncotarget2015626229182293326087197
   PubMedGoogle Scholar
• SchramekDLeibbrandtASiglVOsteoclast differentiation factor RANKL controls development of progestin-driven mammary cancerNature201046873209810220881962
   PubMed Web of Science ®Google Scholar
• EmeryJGMcDonnellPBurkeMBOsteoprotegerin is a receptor for the cytotoxic ligand TRAILJ Biol Chem19982732314363143679603945
   PubMed Web of Science ®Google Scholar
• HolenICrossSSNeville-WebbeHLOsteoprotegerin (OPG) expression by breast cancer cells in vitro and breast tumours in vivo – a role in tumour cell survival?Breast Cancer Res Treat200592320721516155791
   PubMed Web of Science ®Google Scholar
• OwenSYeLSandersAJMasonMDJiangWGExpression profile of receptor activator of nuclear-κB (RANK), RANK ligand (RANKL) and osteoprotegerin (OPG) in breast cancerAnticancer Res201333119920623267146
   PubMed Web of Science ®Google Scholar
• WeichhausMChungSTConnellyLOsteoprotegerin in breast cancer: beyond bone remodelingMol Cancer201514111726054853
   PubMedGoogle Scholar
• TanWZhangWStrasnerATumour-infiltrating regulatory T cells stimulate mammary cancer metastasis through RANKL-RANK signallingNature2011470733554855321326202
   PubMed Web of Science ®Google Scholar
• PalafoxMFerrerIPellegriniPRANK induces epithelial–mesenchymal transition and stemness in human mammary epithelial cells and promotes tumorigenesis and metastasisCancer Res201272112879288822496457
   PubMed Web of Science ®Google Scholar
• TsubakiMKomaiMFujimotoSIActivation of NF-κB by the RANKL/RANK system up-regulates snail and twist expressions and induces epithelial-to-mesenchymal transition in mammary tumor cell linesJ Exp Clin Cancer Res2013326224011086
   PubMed Web of Science ®Google Scholar
• BlakeMLTometskoMMillerRJonesJCDougallWCRANK expression on breast cancer cells promotes skeletal metastasisClin Exp Metastasis201431223324524272640
   PubMed Web of Science ®Google Scholar
• PfitznerBMBranstetterDLoiblSRANK expression as a prognostic and predictive marker in breast cancerBreast Cancer Res Treat2014145230731524737168
   PubMedGoogle Scholar
• FortnerRTSarinkDSchockHOsteoprotegerin and breast cancer risk by hormone receptor subtype: a nested case-control study in the EPIC cohortBMC Med2017152628173834
   PubMedGoogle Scholar
• CuyàsECorominas-FajaBMartínMMBRCA1 haplo insufficiency cell-autonomously activates RANKL expression and generates denosumab-responsive breast cancer-initiating cellsOncotarget2017821350193503228388533
   PubMedGoogle Scholar
• WidschwendterMBurnellMFraserLOsteoprotegerin (OPG), the endogenous inhibitor of receptor activator of NF-κB ligand (RANKL), is dysregulated in BRCA mutation carriersBioMedicine201521013311339
   Google Scholar
• ReyesMEFujiiTBranstetterDPoor prognosis of patients with triple-negative breast cancer can be stratified by RANK and RANKL dual expressionBreast Cancer Res Treat20171641576728417335
   PubMedGoogle Scholar
• ChenGSircarKAprikianAPottiAGoltzmanDRabbaniSAExpression of RANKL/RANK/OPG in primary and metastatic human prostate cancer as markers of disease stage and functional regulationCancer2006107228929816752412
   PubMed Web of Science ®Google Scholar
• HolenICroucherPIHamdyFCEatonCLOsteoprotegerin (OPG) is a survival factor for human prostate cancer cellsCancer Res20026261619162311912131
   PubMedGoogle Scholar
• LuoJLTanWRiconoJMNuclear cytokine-activated IKKα controls prostate cancer metastasis by repressing MaspinNature2007446713669069417377533
   PubMedGoogle Scholar
• Odero-MarahVAWangRChuGReceptor activator of NF-κB ligand (RANKL) expression is associated with epithelial to mesenchymal transition in human prostate cancer cellsCell Res200818885887018645583
   PubMed Web of Science ®Google Scholar
• MillerRERoudierMJonesJArmstrongACanonJDougallWCRANK ligand inhibition plus docetaxel improves survival and reduces tumor burden in a murine model of prostate cancer bone metastasisMol Cancer Ther2008772160216918606716
   PubMed Web of Science ®Google Scholar
• SiampanopoulouMEl Mantani OrdoulidisSMoustakasGThe role of serum osteoprotegerin in metastatic prostate cancer – a case control studyHippokratia201620213313828416910
   PubMedGoogle Scholar
• TakayamaKInoueTNaritaSInhibition of the RANK/RANKL signaling with osteoprotegerin prevents castration-induced acceleration of bone metastasis in castration-insensitive prostate cancerCancer Lett201739710311028373003
   PubMed Web of Science ®Google Scholar
• ChenLMKuoCHLaiTYRANKL increases migration of human lung cancer cells through intercellular adhesion molecule-1 up-regulationJ Cell Biochem2011112393394121328467
   PubMedGoogle Scholar
• Curioni-FontecedroAHusmannLSoldiniDStahelRAPrimary non-small cell lung cancer response upon treatment with denosumabLung Cancer201382350650824075124
   PubMedGoogle Scholar
• MillerREJonesJCTometskoMBlakeMLDougallWCRANKL inhibition blocks osteolytic lesions and reduces skeletal tumor burden in models of non-small-cell lung cancer bone metastasesJ Thorac Oncol20149334535424496001
   PubMedGoogle Scholar
• MikamiSKatsubeKIOyaMIncreased RANKL expression is related to tumour migration and metastasis of renal cell carcinomasJ Pathol2009218453053919455604
   PubMed Web of Science ®Google Scholar
• SasakiAIshikawaKHaraguchiNReceptor activator of nuclear factor-κB ligand (RANKL) expression in hepatocellular carcinoma with bone metastasisAnn Surg Oncol20071431191119917195907
   PubMed Web of Science ®Google Scholar
• JonesDHNakashimaTSanchezOHRegulation of cancer cell migration and bone metastasis by RANKLNature2006440708469269616572175
   PubMed Web of Science ®Google Scholar
• KhanISMouchessMLZhuMLEnhancement of an anti-tumor immune response by transient blockade of central T cell toleranceJ Exp Med2014211576176824752296
   PubMedGoogle Scholar
• HeymannMFRietALe GoffBBattagliaSPaineauJHeymannDOPG, RANK and RANK ligand expression in thyroid lesionsRegul Pept20081481–3465318367263
   PubMedGoogle Scholar
• ItoRNakayamaHYoshidaKExpression of osteoprotegerin correlates with aggressiveness and poor prognosis of gastric carcinomaVirchows Arch2003443214615112838418
   PubMedGoogle Scholar
• MizutaniYMatsubaraHYamamotoKPrognostic significance of serum osteoprotegerin levels in patients with bladder carcinomaCancer200410181794180215386310
   PubMedGoogle Scholar
• CuiXPengHJinJRANK overexpression as a novel esophageal cancer marker: validated immunohistochemical analysis of two different ethnicitiesInt J Clin Exp Pathol2015822249225825973136
   PubMedGoogle Scholar
• SchmiedelBJGrosse-HovestLSalihHRA “vicious cycle” of NK-cell immune evasion in acute myeloid leukemia mediated by RANKL?Oncoimmunology201325e2385023762785
   PubMedGoogle Scholar
• SuTLiJMengMBone marrow stromal cells induced activation of nuclear factor κB signaling protects non-Hodgkin’s B lymphoma cells from apoptosisTumour Biol2016378107451075226873486
   PubMedGoogle Scholar
• SchmohlJUNueblingTWildJKroellTKanzLSalihHRExpression of RANK-L and in part of PD-1 on blasts in patients with acute myeloid leukemia correlates with prognosisEur J Haematol201697651752727096305
   PubMedGoogle Scholar
• KostenuikPJNguyenHQMcCabeJDenosumab, a fully human monoclonal antibody to RANKL, inhibits bone resorption and increases BMD in knock-in mice that express chimeric (murine/human) RANKLJ Bone Miner Res200924218219519016581
   PubMed Web of Science ®Google Scholar
• PeddiPLopez-OlivoMAPrattGFSuarez-AlmazorMEDenosumab in patients with cancer and skeletal metastases: a systematic review and meta-analysisCancer Treat Rev20133919710422898302
   PubMed Web of Science ®Google Scholar
• PalmeriniEChawlaNSFerrariSDenosumab in advanced/unresectable giant-cell tumour of bone (GCTB): for how long?Eur J Cancer20177611812428324746
   PubMed Web of Science ®Google Scholar
• van der HeijdenLDijkstraPDSBlayJYGelderblomHGiant cell tumour of bone in the denosumab eraEur J Cancer201777758328365529
   PubMed Web of Science ®Google Scholar
• NolanEVaillantFBranstetterDRANK ligand as a potential target for breast cancer prevention in BRCA1-mutation carriersNat Med201622893393927322743
   PubMed Web of Science ®Google Scholar
• HeathDJVanderkerkenKChengXAn osteoprotegerin-like peptidomimetic inhibits osteoclastic bone resorption and osteolytic bone disease in myelomaCancer Res200767120220817210700
   PubMedGoogle Scholar
• KimHChoiHKShinJHSelective inhibition of RANK blocks osteoclast maturation and function and prevents bone loss in miceJ Clin Invest2009119481382519258703
   PubMedGoogle Scholar
• TéletchéaSStresingVHervouetSNovel RANK antagonists for the treatment of bone-resorptive disease: theoretical predictions and experimental validationJ Bone Miner Res20142961466147724390798
   PubMedGoogle Scholar
• ZhaoYJinMMaJInhibition effect of enteropeptidase on RANKL–RANK signalling by cleavage of RANKFEBS Lett2013587182958296423954298
   PubMed Web of Science ®Google Scholar
• NaiduVGBabuKRThwinMMSatishRLKumarPVGopalakrishnakonePRANKL targeted peptides inhibit osteoclastogenesis and attenuate adjuvant induced arthritis by inhibiting NF-κB activation and down regulating inflammatory cytokinesChem Biol Interact2013203246747923333834
   PubMed Web of Science ®Google Scholar
• MaRXuJDongBKautherMDJägerMWedemeyerCInhibition of osteoclastogenesis by RNA interference targeting RANKBMC Musculoskelet Disord20121315422913338
   PubMedGoogle Scholar
• BrennanTCRybchynMSGreenWAtwaSConigraveADMasonRSOsteoblasts play key roles in the mechanisms of action of strontium ranelateBr J Pharmacol200915771291130019563530
   PubMed Web of Science ®Google Scholar
• XiuYXuHZhaoCChloroquine reduces osteoclastogenesis in murine osteoporosis by preventing TRAF3 degradationJ Clin Invest2014124129731024316970
   PubMed Web of Science ®Google Scholar
• MaXLiuYZhangYYuXWangWZhaoDJolkinolide B inhibits RANKL-induced osteoclastogenesis by suppressing the activation NF-κB and MAPK signaling pathwaysBiochem Biophys Res Commun2014445228228824491533
   PubMed Web of Science ®Google Scholar
• HaHShimKSKimTWater extract of Acer tegmentosum reduces bone destruction by inhibiting osteoclast differentiation and functionMolecules20141943940395424694651
   PubMedGoogle Scholar
• IhnHJKimJABaeYCShinHIBaekMCParkEKAfatinib ameliorates osteoclast differentiation and function through downregulation of RANK signaling pathwaysBMB Rep201750315015528256196
   PubMedGoogle Scholar