Combination of graphene oxide–silver nanoparticle nanocomposites and cisplatin enhances apoptosis and autophagy in human cervical cancer cells

References

• International Agency for Research on CancerCervical cancer: estimated incidence, mortality and prevalence worldwide in 2012 Available from: http://globocan.iarc.fr/old/FactSheets/cancers/cervix-new.aspAccessed August 1, 2016
   Google Scholar
• American Cancer SocietyChemotherapy for cervical cancer2016 Available from: http://www.cancer.org/cancer/cervicalcancer/detailedguide/cervical-cancer-treating-chemotherapyAccessed August 1, 2016
   Google Scholar
• JemalABrayFCenterMMFerlayJWardEFormanDGlobal cancer statisticsCA Cancer J Clin2011612699021296855
   PubMed Web of Science ®Google Scholar
• FerlayJSoerjomataramIDikshitRCancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012Int J Cancer20151365E359E38625220842
   PubMed Web of Science ®Google Scholar
• AntonMHorkýMKuchtíckováSVojtĕsekBBláhaOImmunohistochemical detection of acetylation and phosphorylation of histone H3 in cervical smearsCeska Gynekol200469136
   PubMedGoogle Scholar
• Dueñas-GonzálezALizanoMCandelariaMCetinaLArceCCerveraEEpigenetics of cervical cancer: an overview and therapeutic perspectivesMol Cancer200543816248899
   PubMed Web of Science ®Google Scholar
• American Cancer SocietyWhat are the key statistics about cervical cancer?2016 Available from: http://www.cancer.org/cancer/cervicalcancer/detailedguide/cervical-cancer-key-statisticsAccessed January 6, 2017
   Google Scholar
• SoonthornthumTArias-PulidoHJosteNEpidermal growth factor receptor as a biomarker for cervical cancerAnn Oncol201122102166217821325449
   PubMedGoogle Scholar
• ZhangPXiMZhaoLClinical efficacy and failure pattern in patients with cervical esophageal cancer treated with definitive chemoradiotherapyRadiother Oncol2015116225726126233590
   PubMed Web of Science ®Google Scholar
• AsanoTHirohashiYTorigoeTBrother of the regulator of the imprinted site (BORIS) variant subfamily 6 is involved in cervical cancer stemness and can be a target of immunotherapyOncotarget2016710112231123726849232
   PubMedGoogle Scholar
• BlancoEHsiaoARuiz-EsparzaGULandryMGMeric-BernstamFFerrariMMolecular-targeted nanotherapies in cancer: enabling treatment specificityMol Oncol20115649250322071376
   PubMed Web of Science ®Google Scholar
• LiFZhaoCWangLMolecular-targeted agents combination therapy for cancer: developments and potentialsInt J Cancer201413461257126923649791
   PubMed Web of Science ®Google Scholar
• ZhangXFGurunathanSCombination of salinomycin and silver nanoparticles enhances apoptosis and autophagy in human ovarian cancer cells: an effective anticancer therapyInt J Nanomedicine2016113655367527536105
   PubMed Web of Science ®Google Scholar
• HarrisTJvon MaltzahnGBhatiaSNMultifunctional nanoparticles for cancer therapyAmijiMMNanotechnology for Cancer TherapyBoca Raton (FL)CRC Press20065975
   Google Scholar
• XiaoBMaLMerlinDNanoparticle-mediated co-delivery of chemotherapeutic agent and siRNA for combination cancer therapyExpert Opin Drug Deliv2017141657327337289
   PubMed Web of Science ®Google Scholar
• DuanXHeCKronSJLinWNanoparticle formulations of cisplatin for cancer therapyWiley Interdiscip Rev Nanomed Nanobiotechnol20168577679126848041
   PubMed Web of Science ®Google Scholar
• MelanieKHeikeZSibylleBSCharacterization of iron oxide nanoparticles adsorbed with cisplatin for biomedical applicationsPhys Med Biol200954175109512119661569
   PubMedGoogle Scholar
• ComengeJSoteloCRomeroFDetoxifying antitumoral drugs via nanoconjugation: the case of gold nanoparticles and cisplatinPloS One2012710e4756223082177
   PubMed Web of Science ®Google Scholar
• ZhangXFYanQShenWGurunathanSTrichostatin A enhances the apoptotic potential of palladium nanoparticles in human cervical cancer cellsInt J Mol Sci2016178E135427548148
   PubMedGoogle Scholar
• GeimAKNovoselovKSThe rise of grapheneNat Mater20076318319117330084
   PubMed Web of Science ®Google Scholar
• GurunathanSHanJWParkJHReduced graphene oxide-silver nanoparticle nanocomposite: a potential anticancer nanotherapyInt J Nanomedicine2015106257627626491296
   PubMed Web of Science ®Google Scholar
• GurunathanSHanJWEppakayalaVKimJHGreen synthesis of graphene and its cytotoxic effects in human breast cancer cellsInt J Nanomedicine201381015102723687445
   PubMed Web of Science ®Google Scholar
• GurunathanSHanJWKimESParkJHKimJHReduction of graphene oxide by resveratrol: a novel and simple biological method for the synthesis of an effective anticancer nanotherapeutic moleculeInt J Nanomedicine2015102951296925931821
   PubMed Web of Science ®Google Scholar
• GurunathanSHanJWEppakayalaVJeyarajMKimJHCytotoxicity of biologically synthesized silver nanoparticles in MDA-MB-231 human breast cancer cellsBiomed Res Int2013201353579623936814
   PubMed Web of Science ®Google Scholar
• GurunathanSJeongJKHanJWZhangXFParkJHKimJHMultidimensional effects of biologically synthesized silver nanoparticles in Helicobacter pylori, Helicobacter felis, and human lung (L132) and lung carcinoma A549 cellsNanoscale Res Lett20151011725977644
   PubMed Web of Science ®Google Scholar
• YuLZhangYZhangBLiuJEnhanced antibacterial activity of silver nanoparticles/halloysite nanotubes/graphene nanocomposites with sandwich-like structureSci Rep20144455124722502
   PubMed Web of Science ®Google Scholar
• YangYKHeCEHeWJReduction of silver nanoparticles onto graphene oxide nanosheets with N,N-dimethylformamide and SERS activities of GO/Ag compositesJ Nanopart Res2011131055715581
   Google Scholar
• ZhangZXuFGYangWSA facile one-pot method to high-quality Ag-graphene composite nanosheets for efficient surface-enhanced Raman scatteringChem Commun2011472264406442
   PubMedGoogle Scholar
• ChenXMSuBYWuGHPlatinum nanoflowers supported on graphene oxide nanosheets: their green synthesis, growth mechanism, and advanced electrocatalytic properties for methanol oxidationJ Mater Chem201222221128411289
   Web of Science ®Google Scholar
• GurunathanSKalishwaralalKVaidyanathanRBiosynthesis, purification and characterization of silver nanoparticles using Escherichia coliColloids Surf B Biointerfaces200974132833519716685
   PubMed Web of Science ®Google Scholar
• GurunathanSHanJWDayemAAEppakayalaVKimJHOxidative stress-mediated antibacterial activity of graphene oxide and reduced graphene oxide in Pseudomonas aeruginosaInt J Nanomedicine201275901591423226696
   PubMed Web of Science ®Google Scholar
• GurunathanSHanJParkJHKimJHAn in vitro evaluation of graphene oxide reduced by Ganoderma spp. in human breast cancer cells (MDA-MB-231)Int J Nanomedicine201491783179724741313
   PubMed Web of Science ®Google Scholar
• GurunathanSHanJWEppakayalaVKimJHBiocompatibility of microbially reduced graphene oxide in primary mouse embryonic fibroblast cellsColloids Surf B Biointerfaces2013105586623352948
   PubMed Web of Science ®Google Scholar
• DreyerDRJiaHPBielawskiCWGraphene oxide: a convenient carbocatalyst for facilitating oxidation and hydration reactionsAngew Chem Int Ed Engl201049386813681620602388
   PubMed Web of Science ®Google Scholar
• Al-MarriAHKhanMKhanMPulicaria glutinosa extract: a toolbox to synthesize highly reduced graphene oxide-silver nanocompositesInt J Mol Sci20151611131114225569090
   PubMedGoogle Scholar
• ThakurSKarakNGreen reduction of graphene oxide by aqueous phytoextractsCarbon N Y2012501453315339
   Web of Science ®Google Scholar
• FuCJZhaoGGZhangHJLiSEvaluation and characterization of reduced graphene oxide nanosheets as anode materials for lithium-ion batteriesInt J Electrochem Sci20138562696280
   Google Scholar
• GurunathanSHanJKimJHHumanin: A novel functional molecule for the green synthesis of grapheneColloids Surf B Biointerfaces201311137638323850746
   PubMed Web of Science ®Google Scholar
• NethravathiCRajamathiMChemically modified graphene sheets produced by the solvothermal reduction of colloidal dispersions of graphite oxideCarbon N Y2008461419941998
   Web of Science ®Google Scholar
• PhamTAKimJSKimJSJeongYTOne-step reduction of graphene oxide with L-glutathioneColloids Surf A Physicochem Eng Asp20113841–3543548
   Google Scholar
• DaveSHGongCCRobertsonAWWarnerJHGrossmanJCChemistry and structure of graphene oxide via direct imagingACS Nano20161087515752227397115
   PubMedGoogle Scholar
• HuCFLiuYLQinJLFabrication of reduced graphene oxide and sliver nanoparticle hybrids for Raman detection of absorbed folic acid: a potential cancer diagnostic probeACS Appl Mater Interfaces20135114760476823629451
   PubMedGoogle Scholar
• ShenJFShiMLiNFacile synthesis and application of Ag-chemically converted graphene nanocompositeNano Res201035339349
   Google Scholar
• BaoQZhangDQiPSynthesis and characterization of silver nanoparticle and graphene oxide nanosheet composites as a bactericidal agent for water disinfectionJ Colloid Interface Sci2011360246347021628064
   PubMed Web of Science ®Google Scholar
• DasMRSarmaRKSaikiaRKaleVSShelkeMVSenguptaPSynthesis of silver nanoparticles in an aqueous suspension of graphene oxide sheets and its antimicrobial activityColloids Surf B Biointerfaces2011831162221109409
   PubMed Web of Science ®Google Scholar
• YangBWLiuZMGuoZYIn situ green synthesis of silver-graphene oxide nanocomposites by using tryptophan as a reducing and stabilizing agent and their application in SERSAppl Surf Sci20143162227
   Web of Science ®Google Scholar
• ZhangDHLiuXHWangXGreen synthesis of graphene oxide sheets decorated by silver nanoprisms and their anti-bacterial propertiesJ Inorg Biochem201110591181118621708103
   PubMedGoogle Scholar
• AkhavanOGhaderiEAghayeeSFereydooniYTalebiAThe use of a glucose-reduced graphene oxide suspension for photothermal cancer therapyJ Mater Chem201222271377313781
   Web of Science ®Google Scholar
• de LunaLAde MoraesACConsonniSRComparative in vitro toxicity of a graphene oxide-silver nanocomposite and the pristine counterparts toward macrophagesJ Nanobiotechnology2016141226912341
   PubMed Web of Science ®Google Scholar
• MartelliLRagazziEDi MarioFBasatoMMartelliMCisplatin and oxaliplatin cytotoxic effects in sensitive and cisplatin-resistant human cervical tumor cells: time and mode of application dependencyAnticancer Res200929103931393719846931
   PubMed Web of Science ®Google Scholar
• MorenoDZalbaSNavarroIde IlarduyaCTGarridoMJPharmacodynamics of cisplatin-loaded PLGA nanoparticles administered to tumor-bearing miceEur J Pharm Biopharm201074226527419883755
   PubMed Web of Science ®Google Scholar
• BhirdeAAPatelSSousaAADistribution and clearance of PEG-single-walled carbon nanotube cancer drug delivery vehicles in miceNanomedicine (Lond)20105101535154621143032
   PubMed Web of Science ®Google Scholar
• LiXHChenXJOuWBKnockdown of creatine kinase B inhibits ovarian cancer progression by decreasing glycolysisInt J Biochem Cell Biol201345597998623416112
   PubMed Web of Science ®Google Scholar
• LiXXWangHLWangJEmodin enhances cisplatin-induced cytotoxicity in human bladder cancer cells through ROS elevation and MRP1 downregulationBMC Cancer20161657827485374
   PubMedGoogle Scholar
• NelAXiaTMadlerLLiNToxic potential of materials at the nanolevelScience2006311576162262716456071
   PubMed Web of Science ®Google Scholar
• PorterNACaldwellSEMillsKAMechanisms of free radical oxidation of unsaturated lipidsLipids19953042772907609594
   PubMed Web of Science ®Google Scholar
• ZhouJLiPXueXFSalinomycin induces apoptosis in cisplatin-resistant colorectal cancer cells by accumulation of reactive oxygen speciesToxicol Lett2013222213914523916687
   PubMedGoogle Scholar
• MaharjanSOkuMTsudaMHosekiJSakaiYMitochondrial impairment triggers cytosolic oxidative stress and cell death following proteasome inhibitionSci Rep20144589625077633
   PubMed Web of Science ®Google Scholar
• WangGQGastmanBRWieckowskiEApoptosis-resistant mitochondria in T cells selected for resistance to Fas signalingJ Biol Chem200127653610361911063743
   PubMedGoogle Scholar
• ZamzamiNMarchettiPCastedoMSequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell deathJ Exp Med199518223673777629499
   PubMed Web of Science ®Google Scholar
• ZamzamiNSusinSAMarchettiPMitochondrial control of nuclear apoptosisJ Exp Med19961834153315448666911
   PubMed Web of Science ®Google Scholar
• Melendez-ZajglaJCruzEMaldonadoVEspinozaAMMitochondrial changes during the apoptotic process of HeLa cells exposed to cisplatinBiochem Mol Biol Int199947576577110365247
   PubMedGoogle Scholar
• MuldoonLLWalker-RosenfeldSLHaleCPurcellSEBennettLCNeuweltEARescue from enhanced alkylator-induced cell death with low molecular weight sulfur-containing chemoprotectantsJ Pharmacol Exp Ther2001296379780511181909
   PubMedGoogle Scholar
• HamersFPBrakkeeJHCavallettiEReduced glutathione protects against cisplatin-induced neurotoxicity in ratsCancer Res19935335445498425186
   PubMedGoogle Scholar
• TraversoNRicciarelliRNittiMRole of glutathione in cancer progression and chemoresistanceOxid Med Cell Longev2013201397291323766865
   PubMed Web of Science ®Google Scholar
• LevineAJp53, The cellular gatekeeper for growth and divisionCell19978833233319039259
   PubMed Web of Science ®Google Scholar
• LoweSWRuleyHEJacksTHousmanDEp53-Dependent apoptosis modulates the cytotoxicity of anticancer agentsCell19937469579678402885
   PubMed Web of Science ®Google Scholar
• AlloucheMBettaiebAVindisCRousseAGrignonCLaurentGInfluence of Bcl-2 overexpression on the ceramide pathway in daunorubicin-induced apoptosis of leukemic cellsOncogene19971415183718459150390
   PubMedGoogle Scholar
• SuenDFNorrisKLYouleRJMitochondrial dynamics and apoptosisGenes Dev200822121577159018559474
   PubMed Web of Science ®Google Scholar
• Hernandez-FloresGOrtiz-LazarenoPCLerma-DiazJMPentoxifylline sensitizes human cervical tumor cells to cisplatin-induced apoptosis by suppressing NF-kappa B and decreased cell senescenceBMC Cancer20111148322074157
   PubMed Web of Science ®Google Scholar
• PorterAGJanickeRUEmerging roles of caspase-3 in apoptosisCell Death Differ1999629910410200555
   PubMed Web of Science ®Google Scholar
• EliopoulosAGKerrDJHerodJThe control of apoptosis and drug resistance in ovarian cancer: influence of p53 and Bcl-2Oncogene1995117121712287478541
   PubMedGoogle Scholar
• LoweSWBodisSMcClatcheyAp53 Status and the efficacy of cancer therapy in vivoScience199426651868078107973635
   PubMed Web of Science ®Google Scholar
• MrozRMSchinsRPFLiHNanoparticle-driven DNA damage mimics irradiation-related carcinogenesis pathwaysEur Respir J200831224125118057054
   PubMed Web of Science ®Google Scholar
• ParienteRParienteJARodriguezABEspinoJMelatonin sensitizes human cervical cancer HeLa cells to cisplatin-induced cytotoxicity and apoptosis: effects on oxidative stress and DNA fragmentationJ Pineal Res2016601556426462739
   PubMed Web of Science ®Google Scholar
• WongVKLiTLawBYSaikosaponin-D, a novel SERCA inhibitor, induces autophagic cell death in apoptosis-defective cellsCell Death Dis20134e72023846222
   PubMed Web of Science ®Google Scholar
• HuLLSunSLWangTPOncolytic Newcastle disease virus triggers cell death of lung cancer spheroids and is enhanced by pharmacological inhibition of autophagyAm J Cancer Res20155123612362326885450
   PubMed Web of Science ®Google Scholar
• HanahanDWeinbergRAHallmarks of cancer: the next generationCell2011144564667421376230
   PubMed Web of Science ®Google Scholar
• BaoLJJaramilloMCZhangZBNrf2 induces cisplatin resistance through activation of autophagy in ovarian carcinomaInt J Clin Exp Pathol2014741502151324817946
   PubMed Web of Science ®Google Scholar
• MaskeyDYousefiSSchmidIATG5 is induced by DNA-damaging agents and promotes mitotic catastrophe independent of autophagyNat Commun20134213023945651
   PubMed Web of Science ®Google Scholar
• MehrpourMEsclatineABeauICodognoPAutophagy in health and disease. 1. Regulation and significance of autophagy: an overviewAm J Physiol Cell Physiol20102984C776C78520089931
   PubMed Web of Science ®Google Scholar
• LinWMLiZGBlockage of cisplatin-induced autophagy sensitizes cervical cancer cells to cisplatinGenet Mol Res2015144169051691226681037
   PubMedGoogle Scholar
• HuangYPGuerrero-PrestonRRatovitskiEAPhospho-ΔNp63α-dependent regulation of autophagic signaling through transcription and micro-RNA modulationCell Cycle20121161247125922356768
   PubMed Web of Science ®Google Scholar
• HanJWGurunathanSJeongJKOxidative stress mediated cytotoxicity of biologically synthesized silver nanoparticles in human lung epithelial adenocarcinoma cell lineNanoscale Res Lett2014945925242904
   PubMed Web of Science ®Google Scholar
• DegenhardtKMathewRBeaudoinBAutophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesisCancer Cell2006101516416843265
   PubMed Web of Science ®Google Scholar
• GozuacikDKimchiAAutophagy as a cell death and tumor suppressor mechanismOncogene200423162891290615077152
   PubMed Web of Science ®Google Scholar
• LiangXHJacksonSSeamanMInduction of autophagy and inhibition of tumorigenesis by beclin 1Nature1999402676267267610604474
   PubMed Web of Science ®Google Scholar
• MathewRWhiteEWhy sick cells produce tumors: the protective role of autophagyAutophagy20073550250517611387
   PubMed Web of Science ®Google Scholar
• ChenYQMcMillan-WardEKongJMIsraelsSJGibsonSBMitochondrial electron-transport-chain inhibitors of complexes I and II induce autophagic cell death mediated by reactive oxygen speciesJ Cell Sci2007120234155416618032788
   PubMedGoogle Scholar
• DuanWJJinXYLiQSTashiroSOnoderaSIkejimaTSilibinin induced autophagic and apoptotic cell death in HT1080 cells through a reactive oxygen species pathwayJ Pharmacol Sci20101131485620431246
   PubMed Web of Science ®Google Scholar
• HuFWeiFWangYLWuBBFangYXiongBEGCG synergizes the therapeutic effect of cisplatin and oxaliplatin through autophagic pathway in human colorectal cancer cellsJ Pharmacol Sci20151281273426003085
   PubMedGoogle Scholar
• FruehaufJPMeyskensFLReactive oxygen species: a breath of life or death?Clin Cancer Res200713378979417289868
   PubMed Web of Science ®Google Scholar
• LiaoLLiuJDreadenECConvergent synthetic platform for single-nanoparticle combination cancer therapy: ratiometric loading and controlled release of cisplatin, doxorubicin, and camptothecinJ Am Chem Soc2014136165896589924724706
   PubMed Web of Science ®Google Scholar
• PathakRKDharSA nanoparticle cocktail: temporal release of predefined drug combinationsJ Am Chem Soc2015137268324832726086212
   PubMed Web of Science ®Google Scholar
• PathakRKDharSCombined chemo-anti-inflammatory prodrugs and nanoparticlesSynlett2016271116071612
   Google Scholar