173
Views
65
CrossRef citations to date
0
Altmetric
Original Research

Combination of salinomycin and silver nanoparticles enhances apoptosis and autophagy in human ovarian cancer cells: an effective anticancer therapy

&
Pages 3655-3675 | Published online: 02 Aug 2016

References

  • WHO, IARC GLOBOCAN [homepage on the Internet]Cancer Incidence and Mortality Worldwide in 2008 Available from: http://globocan.iarc.fr/Accessed December 3, 2015
  • U.S. Cancer Statistics Working GroupUnited States Cancer Statistics: 1999–2012 Incidence and Mortality Web-Based ReportAtlanta, GADepartment of Health and Human Services, Centers for Disease Control and Prevention and National Cancer Institute2015
  • SmithLHMorrisCRYasmeenSParikh-PatelACressRDRomanoPSOvarian cancer: can we make the clinical diagnosis earlier?Cancer200510471398140716116591
  • KellandLThe resurgence of platinum-based cancer chemotherapyNat Rev Cancer20077857358417625587
  • GottesmanMMFojoTBatesSEMultidrug resistance in cancer: role of ATP-dependent transportersNat Rev Cancer200221485811902585
  • StegADBevisKSKatreAAStem cell pathways contribute to clinical chemoresistance in ovarian cancerClin Cancer Res201218386988122142828
  • Burgos-OjedaDRuedaBRBuckanovichRJOvarian cancer stem cell markers: prognostic and therapeutic implicationsCancer Lett201232211722334034
  • DeanMFojoTBatesSTumour stem cells and drug resistanceNat Rev Cancer20055427528415803154
  • LiFTiedeBMassagueJKangYBBeyond tumorigenesis: cancer stem cells in metastasisCell Res200717131417179981
  • SarkarBDoschJSimeoneDMCancer stem cells: a new theory regarding a timeless diseaseChem Rev200910973200320819522504
  • FfrenchBGaschCO’LearyJJGallagherMFDeveloping ovarian cancer stem cell models: laying the pipeline from discovery to clinical interventionMol Cancer20141326225495823
  • GuptaPBOnderTTJiangGZIdentification of selective inhibitors of cancer stem cells by high-throughput screeningCell2009138464565919682730
  • NaujokatCFuchsDOpelzGSalinomycin in cancer: a new mission for an old agentMol Med Rep20103455555921472278
  • DanforthHDRuffMDReidWMMillerRLAnticoccidial activity of salinomycin in battery raised broiler chickensPoult Sci1977563926932605065
  • MiyazakiYShibuyaMSugawaraHKawaguchiOHirsoeCSalinomycin, a new polyether antibioticJ Antibiotics197427118148214452657
  • YueWHamaiATonelliGInhibition of the autophagic flux by salinomycin in breast cancer stem-like/progenitor cells interferes with their maintenanceAutophagy20139571472923519090
  • MitaniMYamanishiTMiyazakiYSalinomycin: a new monovalent cation ionophoreBiochem Biophys Res Commun1975664123112361191289
  • FuchsDHeinoldAOpelzGDanielVNaujokatCSalinomycin induces apoptosis and overcomes apoptosis resistance in human cancer cellsBiochem Biophys Res Commun2009390374374919835841
  • LuDSChoiMYYuJCastroJEKippsTJCarsonDASalinomycin inhibits Wnt signaling and selectively induces apoptosis in chronic lymphocytic leukemia cellsProc Natl Acad Sci U S A201110832132531325721788521
  • KetolaKHilvoMHyotylainenTSalinomycin inhibits prostate cancer growth and migration via induction of oxidative stressBr J Cancer201210619910622215106
  • FuchsDDanielVSadeghiMOpelzGNaujokatCSalinomycin overcomes ABC transporter-mediated multidrug and apoptosis resistance in human leukemia stem cell-like KG-1a cellsBiochem Biophys Res Commun201039441098110420350531
  • RiccioniRDupuisMLBernabeiMThe cancer stem cell selective inhibitor salinomycin is a p-glycoprotein inhibitorBlood Cells Mol Dis2010451869220444629
  • KimJHYooHIKangHSRoJYoonSSalinomycin sensitizes antimitotic drugs-treated cancer cells by increasing apoptosis via the prevention of G2 arrestBiochem Biophys Res Commun201241819810322244892
  • ZhiQMChenXHJiJSalinomycin can effectively kill ALDH (high) stem-like cells on gastric cancerBiomed Pharmacother201165750951521996439
  • WangYEffects of salinomycin on cancer stem cell in human lung adenocarcinoma A549 CellsMed Chem20117210611121222617
  • OakPSKoppFThakurCCombinatorial treatment of mammospheres with trastuzumab and salinomycin efficiently targets HER2-positive cancer cells and cancer stem cellsInt J Cancer2012131122808281922511343
  • KimJHChaeMKimWKSalinomycin sensitizes cancer cells to the effects of doxorubicin and etoposide treatment by increasing DNA damage and reducing p21 proteinBr J Pharmacol2011162377378420973777
  • Al DhaheriYAttoubSArafatKSalinomycin induces apoptosis and senescence in breast cancer: upregulation of p21, downregulation of survivin and histone H3 and H4 hyperacetylationBiochim Biophys Acta2013183043121313523352703
  • ArafatKIratniRTakahashiTInhibitory effects of salinomycin on cell survival, colony growth, migration, and invasion of human non-small cell lung cancer A549 and LNM35: involvement of NAG-1PLoS One201386e6693123805285
  • VerdoodtBVogtMSchmitzILiffersSTTannapfelAMirmohammadsadeghASalinomycin induces autophagy in colon and breast cancer cells with concomitant generation of reactive oxygen speciesPLoS One201279e4413223028492
  • YoonMJKangYJKimIYMonensin, a polyether ionophore antibiotic, overcomes TRAIL resistance in glioma cells via endoplasmic reticulum stress, DR5 upregulation and c-FLIP downregulationCarcinogenesis20133481918192823615398
  • ChenXSchluesenerHJNanosilver: a nanoproduct in medical applicationToxicol Lett2008176111218022772
  • ReidyBHaaseALuchADawsonKALynchIMechanisms of silver nanoparticle release, transformation and toxicity: a critical review of current knowledge and recommendations for future studies and applicationsMaterials20136622952350
  • GurunathanSLeeKJKalishwaralalKSheikpranbabuSVaidyanathanREomSHAntiangiogenic properties of silver nanoparticlesBiomaterials200930316341635019698986
  • SriramMIKanthSBMKalishwaralalKGurunathanSAntitumor activity of silver nanoparticles in Dalton’s lymphoma ascites tumor modelInt J Nanomedicine2010575376221042421
  • GurunathanSHanJWEppakayalaVJeyarajMKimJHCytotoxicity of biologically synthesized silver nanoparticles in MDA-MB-231 human breast cancer cellsBiomed Res Int2013201353579623936814
  • ParkMVNeighAMVermeulenJPThe effect of particle size on the cytotoxicity, inflammation, developmental toxicity and genotoxicity of silver nanoparticlesBiomaterials201132369810981721944826
  • HsinYHChenaCFHuangSShihTSLaiPSChuehPJThe apoptotic effect of nanosilver is mediated by a ROS- and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cellsToxicol Lett2008179313013918547751
  • AshaRaniPVMunGLKHandeMPValiyaveettilSCytotoxicity and genotoxicity of silver nanoparticles in human cellsACS Nano20093227929019236062
  • Franco-MolinaMAMendoza-GamboaESierra-RiveraCAAntitumor activity of colloidal silver on MCF-7 human breast cancer cellsJ Exp Clin Cancer Res20102914821080962
  • SanpuiPChattopadhyayAGhoshSSInduction of apoptosis in cancer cells at low silver nanoparticle concentrations using chitosan nanocarrierACS Appl Mater Interfaces20113221822821280584
  • GurunathanSParkJHHanJWKimJHComparative assessment of the apoptotic potential of silver nanoparticles synthesized by Bacillus tequilensis and Calocybe indica in MDA-MB-231 human breast cancer cells: targeting p53 for anticancer therapyInt J Nanomedicine2015104203422226170659
  • GurunathanSRapid biological synthesis of silver nanoparticles and their enhanced antibacterial effects against Escherichia fergusonii and Streptococcus mutansArab J Chem2014
  • SatapathySRMohapatraPPreetRSilver-based nanoparticles induce apoptosis in human colon cancer cells mediated through p53Nanomedicine (Lond)2013881307132223514434
  • JangamreddyJRJainMVHallbeckALRobergKLotfiKLosMJGlucose starvation-mediated inhibition of salinomycin induced autophagy amplifies cancer cell specific cell deathOncotarget2015612101341014525912307
  • GurunathanSKalishwaralalKVaidyanathanRBiosynthesis, purification and characterization of silver nanoparticles using Escherichia coliColloids Surf B Biointerfaces200974132833519716685
  • WhiteRJReynoldsIJMitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposureJ Neurosci19961618568856978795624
  • SareenDvan GinkelPRTakachJCMitochondria as the primary target of resveratrol-induced apoptosis in human retinoblastoma cellsInvest Ophthalmol Vis Sci20064793708371616936077
  • HanJWGurunathanSJeongJKOxidative stress mediated cytotoxicity of biologically synthesized silver nanoparticles in human lung epithelial adenocarcinoma cell lineNanoscale Res Lett20149145925242904
  • GurunathanSJeongJKHanJWZhangXFParkJHKimJHMultidimensional effects of biologically synthesized silver nanoparticles in Helicobacter pylori, Helicobacter felis, and human lung (L132) and lung carcinoma A549 cellsNanoscale Res Lett2015103525852332
  • SastryCSSrinivasYRaoPVAssay of cisapride in pharmaceutical formulations by extraction spectrophotometryTalanta199744451752618966770
  • SathiyaCKAkilandeswariSFabrication and characterization of silver nanoparticles using Delonix elata leaf brothSpectrochim Acta A Mol Biomol Spectrosc201412833734124681317
  • ShankarSSRaiAAhmadASastryMRapid synthesis of Au, Ag, and bimetallic Au core-Ag shell nanoparticles using neem (Azadirachta indica) leaf brothJ Colloid Interface Sci2004275249650215178278
  • MukherjeeSChowdhuryDKotcherlakotaRPotential theranostics application of bio-synthesized silver nanoparticles (4-in-1 system)Theranostics20144331633524505239
  • GurunathanSHanJWKwonDNKimJHEnhanced antibacterial and anti-biofilm activities of silver nanoparticles against Gram-negative and Gram-positive bacteriaNanoscale Res Lett20149137325136281
  • ZhangXFGurunathanSKimJHEffects of silver nanoparticles on neonatal testis development in miceInt J Nanomedicine2015106243625626491295
  • ZhangXFChoiYJHanJWDifferential nanoreprotoxicity of silver nanoparticles in male somatic cells and spermatogonial stem cellsInt J Nanomedicine2015101335135725733828
  • ZhangGNLiangYZhouLJCombination of salinomycin and gemcitabine eliminates pancreatic cancer cellsCancer Lett2011313213714422030254
  • ZhangBWangXYCaiFFChenWJLoeschUZhongXYAntitumor properties of salinomycin on cisplatin-resistant human ovarian cancer cells in vitro and in vivo: involvement of p38 MAPK activationOncol Rep20132941371137823338561
  • KimKYKimSHYuSNSalinomycin enhances doxorubicin-induced cytotoxicity in multidrug resistant MCF-7/MDR human breast cancer cells via decreased efflux of doxorubicinMol Med Rep20151221898190425892525
  • ZhouSWangFFWongETSalinomycin: a novel anticancer agent with known anti-coccidial activitiesCurr Med Chem201320334095410123931281
  • WangFDaiWQWangYGThe synergistic in vitro and in vivo antitumor effect of combination therapy with salinomycin and 5-fluorouracil against hepatocellular carcinomaPLoS One201495e9741424816638
  • CalzolariASaulleEDe AngelisMLSalinomycin potentiates the cytotoxic effects of TRAIL on glioblastoma cell linesPLoS One201494e9443824740347
  • KimJHKimTYKimHSHongSYoonSLower salinomycin concentration increases apoptotic detachment in high-density cancer cellsInt J Mol Sci20121310131691318223202945
  • LiekeTRamackersWBergmannSKlempnauerJWinklerMKloseJImpact of salinomycin on human cholangiocarcinoma: induction of apoptosis and impairment of tumor cell proliferation in vitroBMC Cancer20121246623057720
  • QinLSJiaPFZhangZQZhangSMROS-p53-cyclophilin-D signaling mediates salinomycin-induced glioma cell necrosisJ Exp Clin Cancer Res2015345726024660
  • KimSChoiJEChoiJOxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cellsToxicol In Vitro20092361076108419508889
  • Suzuki-KarasakiYSuzuki-KarasakiMUchidaMOchiaiTDepolarization controls TRAIL-sensitization and tumor-selective killing of cancer cells: crosstalk with ROSFront Oncol2014412824910845
  • LegrandCBourJMJacobCLactate dehydrogenase (LDH) activity of the number of dead cells in the medium of cultured eukaryotic cells as markerJ Biotechnol19922532312431368802
  • BurdJFUsategui-GomezMA colorimetric assay for serum lactate dehydrogenaseClin Chim Acta19734632232274725386
  • ZhouJLiPXueXFSalinomycin induces apoptosis in cisplatin-resistant colorectal cancer cells by accumulation of reactive oxygen speciesToxicol Lett2013222213914523916687
  • Martinez-ReyesICuezvaJMThe H+-ATP synthase: a gate to ROS-mediated cell death or cell survivalBiochim Biophys Acta2014183771099111224685430
  • TraversoNRicciarelliRNittiMRole of glutathione in cancer progression and chemoresistanceOxid Med Cell Longev2013201397291323766865
  • KimKYYuSNLeeSYSalinomycin-induced apoptosis of human prostate cancer cells due to accumulated reactive oxygen species and mitochondrial membrane depolarizationBiochem Biophys Res Commun20114131808621871443
  • NelAXiaTMadlerLLiNToxic potential of materials at the nanolevelScience2006311576162262716456071
  • GurunathanSHanJWDayemAAEppakayalaVKimJHOxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosaInt J Nanomedicine201275901591423226696
  • PorterNACaldwellSEMillsKAMechanisms of free radical oxidation of unsaturated lipidsLipids19953042772907609594
  • LiuDPeiZFNaeemMS5-aminolevulinic acid activates antioxidative defence system and seedling growth in Brassica napus L. under Water-deficit stressJ Agron Crop Sci20111974284295
  • AndonFTFadeelBProgrammed cell death: molecular mechanisms and implications for safety assessment of nanomaterialsAcc Chem Res201346373374222720979
  • MaharjanSOkuMTsudaMHosekiJSakaiYMitochondrial impairment triggers cytosolic oxidative stress and cell death following proteasome inhibitionSci Rep20144589625077633
  • WangXDThe expanding role of mitochondria in apoptosisGene Dev200115222922293311711427
  • WenCYHuangLLChenJXGambogic acid inhibits growth, induces apoptosis, and overcomes drug resistance in human colorectal cancer cellsInt J Oncol20154751663167126397804
  • ManciniMAndersonBOCaldwellESedghinasabMPatyPBHockenberyDMMitochondrial proliferation and paradoxical membrane depolarization during terminal differentiation and apoptosis in a human colon carcinoma cell lineJ Cell Biol199713824494699230085
  • JangamreddyJRGhavamiSGrabarekJSalinomycin induces activation of autophagy, mitophagy and affects mitochondrial polarity: differences between primary and cancer cellsBiochim Biophys Acta2013183392057206923639289
  • Braydich-StolleLHussainSSchlagerJJHofmannMCIn vitro cytotoxicity of nanoparticles in mammalian germline stem cellsToxicol Sci200588241241916014736
  • HussainSMHessKLGearhartJMGeissKTSchlagerJJIn vitro toxicity of nanoparticles in BRL 3A rat liver cellsToxicol In Vitro200519797598316125895
  • VogelsteinBLaneDLevineAJSurfing the p53 networkNature2000408681030731011099028
  • XiaMKnezevicDVassilevLTp21 does not protect cancer cells from apoptosis induced by nongenotoxic p53 activationOncogene201130334635520871630
  • GartelALTynerALTranscriptional regulation of the p21 (WAF1/CIP1) geneExp Cell Res199924622802899925742
  • AbbasTDuttaAp21 in cancer: intricate networks and multiple activitiesNat Rev Cancer20099640041419440234
  • McIlwainDRBergerTMakTWCaspase functions in cell death and diseaseCold Spring Harb Perspect Biol201354a00865623545416
  • NicholsonDWThornberryNACaspases: killer proteasesTrends Biochem Sci19972282993069270303
  • CrynsVYuanJYProteases to die forGene Dev19981211155115709620844
  • PorterAGJanickeRUEmerging roles of caspase-3 in apoptosisCell Death Differ1999629910410200555
  • LeeHGLeeJMShinSJSalinomycin inhibited cell proliferation and induced apoptosis in human uterine leiomyoma cellsObstet Gynecol Sci201457650150625469339
  • GurunathanSHanJWParkJHReduced graphene oxide-silver nanoparticle nanocomposite: a potential anticancer nanotherapyInt J Nanomedicine2015106257627626491296
  • AllenDLLindermanJKRoyRRApoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweightingAm J Physiol19972732 pt 1C579C5879277355
  • KitazumiITsukaharaMRegulation of DNA fragmentation: the role of caspases and phosphorylationFEBS J2011278342744121182594
  • ThompsonCBApoptosis in the pathogenesis and treatment of diseaseScience19952675203145614627878464
  • JacobsonMDWeilMRaffMCProgrammed cell death in animal developmentCell19978833473549039261
  • TaatjesDJSobelBEBuddRCMorphological and cytochemical determination of cell death by apoptosisHistochem Cell Biol20081291334318000678
  • LiJYuanJCaspases in apoptosis and beyondOncogene200827486194620618931687
  • Alvarez-GonzalezRSpringHMullerMBurkleASelective loss of poly(ADP-ribose) and the 85-kDa fragment of poly(ADP-ribose) polymerase in nucleoli during alkylation-induced apoptosis of HeLa cellsJ Biol Chem199927445321223212610542247
  • MrozRMSchinsRPLiHNanoparticle-driven DNA damage mimics irradiation-related carcinogenesis pathwaysEur Respir J200831224125118057054
  • Al DhaheriYEidAAbuQamarSMitotic arrest and apoptosis in breast cancer cells induced by Origanum majorana extract: upregulation of TNF-alpha and downregulation of survivin and mutant p53PLoS One201382e5664923451065
  • KimJSSungJHJiJHIn vivo genotoxicity of silver nanoparticles after 90-day silver nanoparticle inhalation exposureSaf Health Work201121343822953185
  • FoldbjergRDangDAAutrupHCytotoxicity and genotoxicity of silver nanoparticles in the human lung cancer cell line, A549Arch Toxicol201185774375020428844
  • AwasthiKKAwasthiAKumarNRoyPAwasthiKJohnPJSilver nanoparticle induced cytotoxicity, oxidative stress, and DNA damage in CHO cellsJ Nanopart Res20131591898
  • KimHRShinDYParkYJParkCWOhSMChungKHSilver nanoparticles induce p53-mediated apoptosis in human bronchial epithelial (BEAS-2B) cellsJ Toxicol Sci201439340141224849675
  • StromhaugPEKlionskyDJApproaching the molecular mechanism of autophagyTraffic20012852453111489210
  • WangCWKlionskyDJThe molecular mechanism of autophagyMol Med200393–4657612865942
  • BottiJDjavaheri-MergnyMPilatteYCodognoPAutophagy signaling and the cogwheels of cancerAutophagy200622677316874041
  • SuzukiKKirisakoTKamadaYMizushimaNNodaTOhsumiYThe pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formationEMBO J200120215971598111689437
  • KlionskyDJCreggJMDunnWAA unified nomenclature for yeast autophagy-related genesDev Cell20035453954514536056
  • MizushimaNYamamotoAMatsuiMYoshimoriTOhsumiYIn vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome markerMol Biol Cell20041531101111114699058
  • ReggioriFKlionskyDJAutophagosomes: biogenesis from scratch?Curr Opin Cell Biol200517441542215978794
  • LiangXHJacksonSSeamanMInduction of autophagy and inhibition of tumorigenesis by beclin 1Nature1999402676267267610604474
  • GozuacikDKimchiAAutophagy as a cell death and tumor suppressor mechanismOncogene200423162891290615077152
  • MathewRWhiteEWhy sick cells produce tumors – the protective role of autophagyAutophagy20073550250517611387
  • DegenhardtKMathewRBeaudoinBAutophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesisCancer Cell2006101516416843265
  • ChenNDebnathJAutophagy and tumorigenesisFEBS Lett201058471427143520035753
  • RadoshevichLMurrowLChenNATG12 conjugation to ATG3 regulates mitochondrial homeostasis and cell deathCell2010142459060020723759
  • RubinszteinDCCodognoPLevineBAutophagy modulation as a potential therapeutic target for diverse diseasesNat Rev Drug Discov201211970973022935804
  • YooBHZagryazhskayaALiYLUpregulation of ATG3 contributes to autophagy induced by the detachment of intestinal epithelial cells from the extracellular matrix, but promotes autophagy-independent apoptosis of the attached cellsAutophagy20151181230124626061804
  • KlionskyDJAutophagy: from phenomenology to molecular understanding in less than a decadeNat Rev Mol Cell Biol200781193193717712358
  • NishidaKKyoiSYamaguchiOSadoshimaJOtsuKThe role of autophagy in the heartCell Death Differ2009161313819008922
  • YousefiSPerozzoRSchmidICalpain-mediated cleavage of Atg5 switches autophagy to apoptosisNat Cell Biol20068101124113216998475
  • PyoJOJangMHKwonYKEssential roles of Atg5 and FADD in autophagic cell death – dissection of autophagic cell death into vacuole formation and cell deathJ Biol Chem200528021207222072915778222
  • EspertLDenizotMGrimaldiMAutophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4J Clin Invest200611682161217216886061
  • NemotoTTanidaITanida-MiyakeEThe mouse APG10 homologue, an E2-like enzyme for Apg12p conjugation, facilitates MAP-LC3 modificationJ Biol Chem200327841395173952612890687
  • ZoisCEKoukourakisMIRadiation-induced autophagy in normal and cancer cells towards novel cytoprotection and radio-sensitization policies?Autophagy20095444245019164950
  • MizushimaNKumaAKobayashiYMouse Apg16L, a novel WD-repeat protein, targets to the autophagic isolation membrane with the Apg12-Apg5 conjugateJ Cell Sci2003116pt 91679168812665549
  • XieZPKlionskyDJAutophagosome formation: core machinery and adaptationsNat Cell Biol20079101102110917909521
  • KloseJStankovMVKleineMInhibition of autophagic flux by salinomycin results in anti-cancer effect in hepatocellular carcinoma cellsPLoS One201495e9597024816744
  • WirawanEBergheTVLippensSAgostinisPVandenabeelePAutophagy: for better or for worseCell Res2012221436121912435
  • ChaabaneWUserSDEl-GazzahMAutophagy, apoptosis, mitoptosis and necrosis: interdependence between those pathways and effects on cancerArch Immunol Ther Exp (Warsz)2013611435823229678