Single-dose Ag85B-ESAT6–loaded poly(lactic-co-glycolic acid) nanoparticles confer protective immunity against tuberculosis

References

• Global Tuberculosis Report 2017World Health Organization (WHO) Available from: https://www.who.int/tb/publications/global_report/gtbr2017_main_text.pdfAccessed June 21, 2018
   Google Scholar
• LucaSMihaescuTHistory of BCG Vaccine: Amaltea MedicalBucharestEditura Magister2013
   Google Scholar
• FinePEThe BCG story: lessons from the past and implications for the futureRev Infect Dis198911Supplement_2S353S3592652252
   PubMedGoogle Scholar
• FinePEVariation in protection by BCG: implications of and for heterologous immunityThe Lancet199534689861339134510.1016/S0140-6736(95)92348-9
   PubMed Web of Science ®Google Scholar
• OttenhoffTHKaufmannSHVaccines against tuberculosis: where are we and where do we need to go?PLoS Pathog201285e100260710.1371/journal.ppat.100260722589713
   PubMed Web of Science ®Google Scholar
• TamerisMDHatherillMLandryBSSafety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trialThe Lancet201338198711021102810.1016/S0140-6736(13)60177-4
   PubMed Web of Science ®Google Scholar
• Junqueira-KipnisAPNetoLMMKipnisARole of fused Mycobacterium tuberculosis immunogens and adjuvants in modern tuberculosis vaccinesFront Immunol2014518810.3389/fimmu.2014.0018824795730
   PubMed Web of Science ®Google Scholar
• FlynnJLChanJImmune evasion by Mycobacterium tuberculosis: living with the enemyCurr Opin Immunol200315445045512900278
   PubMed Web of Science ®Google Scholar
• GregoryAETitballRWilliamsonDVaccine delivery using nanopar-ticlesFront Cell Infect Microbiol201331310.3389/fcimb.2013.0007223532930
   PubMed Web of Science ®Google Scholar
• OyewumiMOKumarACuiZNano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune responsesExpert Rev Vaccines2010991095110710.1586/erv.10.8920822351
   PubMed Web of Science ®Google Scholar
• SilvaASoemaPSlütterBOssendorpFJiskootWPLGA particulate delivery systems for subunit vaccines: linking particle properties to immunogenicityHum Vaccin Immunother20161241056106910.1080/21645515.2015.111771426752261
   PubMed Web of Science ®Google Scholar
• AkagiTBabaMAkashiMBiodegradable nanoparticles as vaccine adjuvants and delivery systems: regulation of immune responses by nanoparticle-based vaccinePolymers in NanomedicineHeidelbergSpringer20113164
   Google Scholar
• MakadiaHKSiegelSJPoly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrierPolymers2011331377139710.3390/polym303137722577513
   PubMed Web of Science ®Google Scholar
• AndersonJMShiveMSBiodegradation and biocompatibility of PLA and PLGA microspheresAdv Drug Deliv Rev201264728210.1016/j.addr.2012.09.004
   Web of Science ®Google Scholar
• OhNParkJ-HEndocytosis and exocytosis of nanoparticles in mammalian cellsInt J Nanomedicine20149Suppl 15124872703
   PubMed Web of Science ®Google Scholar
• KanchanVPandaAKInteractions of antigen-loaded polylactide particles with macrophages and their correlation with the immune responseBiomaterials200728355344535710.1016/j.biomaterials.2007.08.01517825905
   PubMed Web of Science ®Google Scholar
• LawlorCO’ConnorGO’LearySTreatment of mycobacterium tuberculosis-infected macrophages with poly (lactic-co-glycolic acid) microparticles drives NFκB and autophagy dependent bacillary killingPLoS One2016112e014916710.1371/journal.pone.014916726894562
   PubMed Web of Science ®Google Scholar
• KasturiSPSkountzouIAlbrechtRAProgramming the magnitude and persistence of antibody responses with innate immunityNature2011470733554310.1038/nature0977121350488
   PubMed Web of Science ®Google Scholar
• ShiSHickeyAJPLGA microparticles in respirable sizes enhance an in vitro T cell response to recombinant Mycobacterium tuberculosis antigen TB10. 4-Ag85BPharm Res201027235036010.1007/s11095-009-0028-720024670
   PubMedGoogle Scholar
• KeijzerCSlütterBVan Der ZeeRJiskootWVan EdenWBroereFPLGA, PLGA-TMC and TMC-TPP nanoparticles differentially modulate the outcome of nasal vaccination by inducing tolerance or enhancing humoral immunityPLoS One2011611e2668410.1371/journal.pone.002668422073184
   PubMed Web of Science ®Google Scholar
• AllahyariMMohabatiRAmiriSSynergistic effect of rSAG1 and rGRA2 antigens formulated in PLGA microspheres in eliciting immune protection against Toxoplasama gondiiExp Parasitol201617023624610.1016/j.exppara.2016.09.00827663469
   PubMed Web of Science ®Google Scholar
• MenYThomasinCMerkleHPGanderBCorradinGA single administration of tetanus toxoid in biodegradable microspheres elicits T cell and antibody responses similar or superior to those obtained with aluminum hydroxideVaccine19951376836897668038
   PubMed Web of Science ®Google Scholar
• ChudinaTLabyntsevAManoiloKKolyboDKomisarenkoSCellobiose-coated poly (lactideco-glycolide) particles loaded with diphtheria toxoid for per os immunizationCroat Med J2015562859325891867
   PubMed Web of Science ®Google Scholar
• LutsiakMKwonGSSamuelJBiodegradable nanoparticle delivery of a TH2-biased peptide for induction of TH1 immune responsesJ Pharm Pharmacol200658673974710.1211/jpp.58.6.000416734975
   PubMed Web of Science ®Google Scholar
• HuangS-SLiI-HPo-da HongM-KYDevelopment of Yersinia pestis F1 antigen-loaded microspheres vaccine against plagueInt J Nanomedicine2014981324550673
   PubMed Web of Science ®Google Scholar
• YoshidaAMatumotoMHshizumeHSelective delivery of rifampicin incorporated into poly (dl-lactic-co-glycolic) acid microspheres after phagocytotic uptake by alveolar macrophages, and the killing effect against intracellular Mycobacterium bovis Calmette–guérinMicrobes Infect2006892484249110.1016/j.micinf.2006.06.00416879999
   PubMedGoogle Scholar
• KhanNGowthamanUPahariSAgrewalaJNManipulation of costimulatory molecules by intracellular pathogens: veni, vidi, vici!!PLoS Pathog201286e100267610.1371/journal.ppat.100267622719245
   PubMedGoogle Scholar
• AndersenPAskgaardDLjungqvistLBentzonMWHeronIT-cell proliferative response to antigens secreted by Mycobacterium tuberculosisInfect Immun1991594155815631900811
   PubMed Web of Science ®Google Scholar
• HasløvKAndersenÅNagaiSGottschauASørensenTAndersenPGuinea pig cellular immune responses to proteins secreted by Myco-bacterium tuberculosisInfect Immun19956338048107868250
   PubMedGoogle Scholar
• BrandtLOettingerTHolmAAndersenABAndersenPKey epitopes on the ESAT-6 antigen recognized in mice during the recall of protective immunity to Mycobacterium tuberculosisJ Immunol19961578352735338871652
   PubMedGoogle Scholar
• CarpenterZKWilliamsonEDEylesJEMucosal delivery of microparticle encapsulated ESAT-6 induces robust cell-mediated responses in the lung milieuJ Control Release20051041677710.1016/j.jconrel.2005.01.01415866335
   PubMedGoogle Scholar
• DietrichJAndersenCRappuoliRDohertyTMJensenCGAndersenPMucosal administration of Ag85B-ESAT-6 protects against infection with Mycobacterium tuberculosis and boosts prior bacillus Calmette-Guerin immunityJ Immunol200617796353636017056566
   PubMedGoogle Scholar
• van DisselJTArendSMPrinsCAg85B–ESAT-6 adjuvanted with IC31 promotes strong and long-lived Mycobacterium tuberculosis specific T cell responses in naïve human volunteersVaccine201028203571358110.1016/j.vaccine.2010.02.09420226890
   PubMed Web of Science ®Google Scholar
• Van DisselJTSoonawalaDJoostenSAAg85B–ESAT-6 adjuvanted with IC31 promotes strong and long-lived Mycobacterium tuberculosis specific T cell responses in volunteers with previous BCG vaccination or tuberculosis infectionVaccine201129112100210910.1016/j.vaccine.2010.12.13521256189
   PubMed Web of Science ®Google Scholar
• HallLJClareSPickardDCharacterisation of a live Salmonella vaccine stably expressing the Mycobacterium tuberculosis Ag85B– ESAT6 fusion proteinVaccine200927496894690410.1016/j.vaccine.2009.09.00719755145
   PubMed Web of Science ®Google Scholar
• ManishMRahiAKaurMBhatnagarRSinghSA single-dose PLGA encapsulated protective antigen domain 4 nanoformulation protects mice against Bacillus anthracis spore challengePLoS One201384e6188510.1371/journal.pone.006188523637922
   PubMed Web of Science ®Google Scholar
• IgietsemeJUEkoFOHeQBlackCMAntibody regulation of T-cell immunity: implications for vaccine strategies against intracellular pathogensExpert Rev Vaccines200431233410.1586/14760584.3.1.2314761241
   PubMedGoogle Scholar
• EbensenTGuzmánCAImmune modulators with defined molecular targets: cornerstone to optimize rational vaccine designHum Vaccin200841132218376145
   PubMed Web of Science ®Google Scholar
• LeeSNguyenMTRecent advances of vaccine adjuvants for infectious diseasesImmune Netw2015152515710.4110/in.2015.15.2.5125922593
   PubMed Web of Science ®Google Scholar
• AggerEMNovel adjuvant formulations for delivery of anti-tuberculosis vaccine candidatesAdv Drug Deliv Rev2016102738210.1016/j.addr.2015.11.01226596558
   PubMed Web of Science ®Google Scholar
• ZhuBDockrellHMOttenhoffTHEvansTGZhangYTuberculosis vaccines: opportunities and challengesRespirology201823435936810.1111/resp.1324529341430
   PubMed Web of Science ®Google Scholar
• AllahyariMMohitEPeptide/protein vaccine delivery system based on PLGA particlesHum Vaccin Immunother201612380682810.1080/21645515.2015.110280426513024
   PubMed Web of Science ®Google Scholar
• JoshiVBGearySMSalemAKBiodegradable particles as vaccine delivery systems: size mattersAaps J2013151859410.1208/s12248-012-9418-623054976
   PubMed Web of Science ®Google Scholar
• KirbyDJRosenkrandsIAggerEMAndersenPCoombesAGPerrieYPLGA microspheres for the delivery of a novel subunit TB vaccineJ Drug Target200816428229310.1080/1061186080190046218446607
   PubMed Web of Science ®Google Scholar
• DhimanNKhullerGProtective efficacy of mycobacterial 71-kDa cell wall associated protein using poly (DL-lactide-co-glycolide) microparticles as carrier vehiclesFEMS Immunol Med Microbiol199821119289657317
   PubMedGoogle Scholar
• ConwayMAMadrigal-EstebasLMcCleanSBraydenDJMillsKHProtection against Bordetella pertussis infection following parenteral or oral immunization with antigens entrapped in biodegradable particles: effect of formulation and route of immunization on induction of TH1 and TH2 cellsVaccine20011915–161940195011228364
   PubMed Web of Science ®Google Scholar
• DeSRobinsonDHParticle size and temperature effect on the physical stability of PLGA nanospheres and microspheres containing BodipyAAPS PharmSciTech200454182410.1208/pt050453
   Web of Science ®Google Scholar
• QiCChenYJingQ-ZWangX-GPreparation and characterization of catalase-loaded solid lipid nanoparticles protecting enzyme against proteolysisInt J Mol Sci20111274282429310.3390/ijms1207428221845078
   PubMed Web of Science ®Google Scholar
• HamborgMKramerRSchantéCEThe physical stability of the recombinant tuberculosis fusion antigens h1 and h56J Pharm Sci2013102103567357810.1002/jps.2366923873630
   PubMed Web of Science ®Google Scholar
• WangYLiPKongLChitosan-modified PLGA nanoparticles with versatile surface for improved drug deliveryAAPS PharmSciTech201314258559210.1208/s12249-013-9943-323463262
   PubMed Web of Science ®Google Scholar
• FogedCBrodinBFrokjaerSSundbladAParticle size and surface charge affect particle uptake by human dendritic cells in an in vitro modelInt J Pharm2005298231532210.1016/j.ijpharm.2005.03.03515961266
   PubMed Web of Science ®Google Scholar
• ChampionJAWalkerAMitragotriSRole of particle size in phagocytosis of polymeric microspheresPharm Res20082581815182110.1007/s11095-008-9562-y18373181
   PubMed Web of Science ®Google Scholar
• LiXSloatBRYanasarnNCuiZRelationship between the size of nanoparticles and their adjuvant activity: data from a study with an improved experimental designEur J Pharm Biopharm201178110711610.1016/j.ejpb.2010.12.01721182941
   PubMed Web of Science ®Google Scholar
• OlsenAWvan PinxterenLAOkkelsLMRasmussenPBAndersenPProtection of mice with a tuberculosis subunit vaccine based on a fusion protein of antigen 85b and esat-6Infect Immun20016952773277810.1128/IAI.69.5.2773-2778.200111292688
   PubMedGoogle Scholar
• EllnerJJHirschCSWhalenCCCorrelates of protective immunity to Mycobacterium tuberculosis in humansClin Infect Dis200030Supplement_3S279S28210.1086/31387410875800
   PubMedGoogle Scholar
• XuYLiuWShenHYanJQuDWangHRecombinant Mycobacterium bovis BCG expressing the chimeric protein of antigen 85B and ESAT-6 enhances the TH1 cell-mediated responseClin Vacc Immunol20091681121112610.1128/CVI.00112-09
   PubMedGoogle Scholar
• NicoleteRDos SantosDFFaccioliLHThe uptake of PLGA micro or nanoparticles by macrophages provokes distinct in vitro inflammatory responseInt Immunopharmacol201111101557156310.1016/j.intimp.2011.05.01421621649
   PubMed Web of Science ®Google Scholar
• ShiCWangXZhangHXuZLiYYuanLImmune responses and protective efficacy induced by 85B antigen and early secreted antigenic target-6 kDa antigen fusion protein secreted by recombinant bacille Calmette–GuérinActa Biochim Biophys Sin (Shanghai)200739429029617417685
   PubMedGoogle Scholar