135
Views
20
CrossRef citations to date
0
Altmetric
Review

Anti-VEGF therapy in the management of retinopathy of prematurity: what we learn from representative animal models of oxygen-induced retinopathy

Pages 81-90 | Published online: 20 May 2016

References

  • AshtonNEditorial: retrolental fibroplasia now retinopathy of prematurityBr J Ophthalmol198468689
  • HartnettMEPennJSMechanisms and management of retinopathy of prematurityN Engl J Med20123672515252623268666
  • AielloLPAveryRLArriggPGVascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disordersNew Engl J Med1994331148014877526212
  • DavidovicSPNikolicSVCuricNJChanges of serum VEGF concentration after intravitreal injection of avastin in treatment of diabetic retinopathyEur J Ophthalmol20122279279822344470
  • WuWCLienRLiaoPJSerum levels of vascular endothelial growth factor and related factors after intravitreous bevacizumab injection for retinopathy of prematurityJAMA Ophthalmol201513339139725569026
  • AchenMGStackerSAThe vascular endothelial growth factor family; proteins which guide the development of the vasculatureInt J Exp Pathol19987925526510193309
  • GerberHPHillanKJRyanAMVEGF is required for growth and survival in neonatal miceDevelopment19991261149115910021335
  • FerraraNGerberHPLecouterJThe biology of VEGF and its receptorsNat Med2003966967612778165
  • Mintz-HittnerHAKennedyKAChuangAZEfficacy of intravitreal bevacizumab for stage 3+ retinopathy of prematurityN Engl J Med201136460361521323540
  • GeloneckMMChuangAZClarkWLRefractive outcomes following bevacizumab monotherapy compared with conventional laser treatment: a randomized clinical trialJAMA Ophthalmol20141321327133325103848
  • KongLFryMAl-SamarraieMGilbertCSteinkullerPGAn update on progress and the changing epidemiology of causes of childhood blindness worldwideJ AAPOS20121650150723237744
  • HuJREactivation of retinopathy of prematurity after bevacizumab injectionArch Opthalmol201213010001006
  • SmithLEHWesolowskiEMcLellanAOxygen-induced retinopathy in the mouseInvest Ophthalmol Vis Sci1994351011117507904
  • PennJSHenryMMTolmanBLExposure to alternating hypoxia and hyperoxia causes severe proliferative retinopathy in the newborn ratPediatr Res1994367247317898981
  • FlowerRWBlakeDARetrolental fibroplasia: evidence for a role of the prostaglandin cascade in the pathogenesis of oxygen-induced retinopathy in the newborn beaglePediatr Res198115129313027027156
  • AshtonNGarnerAKnightGIntermittent oxygen in retrolental fibroplasiaAm J Ophthalmol1971711531605542121
  • NakaoSArimaMIshikawaKIntravitreal anti-VEGF therapy blocks inflammatory cell infiltration and re-entry into the circulation in retinal angiogenesisInvest Ophthalmol Vis Sci2012534323432822661475
  • TokunagaCCMittonKPDaileyWEffects of anti-VEGF treatment on the recovery of the developing retina following oxygen-induced retinopathyInvest Ophthalmol Vis Sci2014551884189224550366
  • McCloskeyMWangHJiangYSmithGWStrangeJHartnettMEAnti-VEGF antibody leads to later atypical intravitreous neovascularization and activation of angiogenic pathways in a rat model of retinopathy of prematurityInvest Ophthalmol Vis Sci2013542020202623449716
  • KerteszNWuJChenTHPSucovHMWuHThe role of erythropoietin in regulating angiogenesisDev Biol200427610111015531367
  • WangHByfieldGJiangYSmithGWMcCloskeyMHartnettMEVEGF-mediated STAT3 activation inhibits retinal vascularization by downregulating erythropoietin expressionAm J Pathol20121801243125322230249
  • RobinsonCJStringerSEThe splice variants of vascular endothelial growth factor (VEGF) and their receptorsJ Cell Sci200111485386511181169
  • WangHSmithGWYangZShort hairpin RNA-mediated knockdown of VEGFA in Muller cells reduces intravitreal neovascularization in a rat model of retinopathy of prematurityAm J Pathol201318396497423972394
  • BuddSJHartnettMEIncreased angiogenic factors associated with peripheral avascular retina and intravitreous neovascularization: a model of retinopathy of prematurityArch Ophthalmol201012858959520457980
  • BatesDOCuiTGDoughtyJMVEGF165b, an inhibitory splice variant of vascular endothelial growth factor, is down-regulated in renal cell carcinomaCancer Res2002624123413112124351
  • GuFLiXKongJVEGF111b, a new member of VEGFxxxb isoforms and induced by mitomycin C, inhibits angiogenesisBiochem Biophys Res Commun2013441182424125722
  • Beazley-LongNHuaJJehleTVEGF-A165b is an endogenous neuroprotective splice isoform of vascular endothelial growth factor A in vivo and in vitroAm J Pathol201318391892923838428
  • PerrinRMKonopatskayaOQiuYHarperSBatesDOChurchillAJDiabetic retinopathy is associated with a switch in splicing from anti- to pro-angiogenic isoforms of vascular endothelial growth factorDiabetologia2005482422242716193288
  • HuaJSpeeCKaseSRecombinant human VEGF165b inhibits experimental choroidal neovascularizationInvest Ophthalmol Vis Sci2010514282428820237252
  • WoolardJWangWYBevanHSVEGF165b, an inhibitory vascular endothelial growth factor splice variant: mechanism of action, in vivo effect on angiogenesis and endogenous protein expressionCancer Res2004647822783515520188
  • RennelESHamdollah-ZadehMAWheatleyERRecombinant human VEGF165b protein is an effective anti-cancer agent in miceEur J Cancer2008441883189418657413
  • BabaTMcLeodDSEdwardsMMVEGF 165 b in the developing vasculatures of the fetal human eyeDev Dyn201224159560722275161
  • MagnussenALRennelESHuaJVEGF-A165b is cytoprotective and antiangiogenic in the retinaInvest Ophthalmol Vis Sci2010514273428120237249
  • GammonsMVDickADHarperSJBatesDOSRPK1 inhibition modulates VEGF splicing to reduce pathological neovascularization in a rat model of retinopathy of prematurityInvest Ophthalmol Vis Sci2013545797580623761094
  • NowakDGAminEMRennelESRegulation of vascular endothelial growth factor (VEGF) splicing from pro-angiogenic to anti-angiogenic isoforms: a novel therapeutic strategy for angiogenesisJ Biol Chem20102855532554019906640
  • FerraraNRole of vascular endothelial growth factor in regulation of physiological angiogenesisAm J Physiol Cell Physiol2001280C1358C136611350730
  • FerraraNDavis-SmythTThe biology of vascular endothelial growth factorEndocr Rev1997184259034784
  • FoxtonRHFinkelsteinAVijaySVEGF-A is necessary and sufficient for retinal neuroprotection in models of experimental glaucomaAm J Pathol20131821379139023416159
  • WangHYangZJiangYQuantitative analyses of retinal vascular area and density after different methods to reduce VEGF in a rat model of retinopathy of prematurityInvest Ophthalmol Vis Sci20145573774424425858
  • HartnettMEMartiniukDByfieldGGeisenPZengGBautchVLNeutralizing VEGF decreases tortuosity and alters endothelial cell division orientation in arterioles and veins in a rat model of ROP: relevance to plus diseaseInvest Ophthalmol Vis Sci2008493107311418378573
  • ZengGTaylorSMMcColmJROrientation of endothelial cell division is regulated by VEGF signaling during blood vessel formationBlood20071091345135217068148
  • PrenticeHMBiswalMRDoreyCKBlanksJCHypoxia-regulated retinal glial cell-specific promoter for potential gene therapy in diseaseInvest Ophthalmol Vis Sci2011528562857021960554
  • BiswalMRPrenticeHMDoreyCKBlanksJCA hypoxia-responsive glial cell-specific gene therapy vector for targeting retinal neovascularizationInvest Ophthalmol Vis Sci2014558044805325377223
  • AielloLPPierceEAFoleyEDSuppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteinsProc Natl Acad Sci U S A19959210457104617479819
  • HartnettMEPathophysiology and mechanisms of severe retinopathy of prematurityOphthalmology201512220021025444347
  • AhnGOSeitaJHongBJTranscriptional activation of hypoxia-inducible factor-1 (HIF-1) in myeloid cells promotes angiogenesis through VEGF and S100A8Proc Natl Acad Sci U S A20141112698270324497508
  • LindenTKatschinskiDMEckhardtKScheidAPagelHWengerRHThe antimycotic ciclopirox olamine induces HIF-1α stability, VEGF expression, and angiogenesisFASEB J20031776176312594177
  • SearsJEHoppeGEbrahemQAnand-ApteBProlyl hydroxylase inhibition during hyperoxia prevents oxygen-induced retinopathyProc Natl Acad Sci2008105198981990319057008
  • LiuHZhangWXuZCaldwellRWCaldwellRBBrooksSEHyperoxia causes regression of vitreous neovascularization by downregulating VEGF/VEGFR2 pathwayInvest Ophthalmol Vis Sci20135491893123307955
  • SaitoYUppalAByfieldGBuddSHartnettMEActivated NAD(P)H oxidase from supplemental oxygen induces neovascularization independent of VEGF in retinopathy of prematurity modelInvest Ophthalmol Vis Sci2008491591159818385079
  • TrichonasGLeeTJHoppeGAuJSearsJEProlyl hydroxylase inhibition during hyperoxia prevents oxygen-induced retinopathy in the rat 50/10 modelInvest Ophthalmol Vis Sci2013544919492623761085
  • HaaseVHRegulation of erythropoiesis by hypoxia-inducible factorsBlood Rev201327415323291219
  • ChenJConnorKMAdermanCMSmithLEErythropoietin deficiency decreases vascular stability in miceJ Clin Invest200811852653318219389
  • ChenJConnorKMAdermanCMWillettKLAspegrenOPSmithLEHSuppression of retinal neovascularization by erythropoietin siRNA in a mouse model of proliferative retinopathyInvest Ophthalmol Vis Sci2009501329133518952918
  • MowatFMGonzalezFLuhmannUFEndogenous erythropoietin protects neuroretinal function in ischemic retinopathyAm J Pathol20121801726173922342523
  • MannelloFTontiGAMErythropoietin and Its receptor in breast cancer: putting together the pieces of the puzzleOncologist20081376176818596367
  • NakanoMSatohKFukumotoYImportant role of erythropoietin receptor to promote VEGF expression and angiogenesis in peripheral ischemia in miceCirc Res200710066266917293480
  • YangZWangHJiangYHartnettMEVEGFA activates erythropoietin receptor and enhances VEGFR2-mediated pathological angiogenesisAm J Pathol20141841230123924630601
  • BlokhinaOVirolainenEFagerstedtKVAntioxidants, oxidative damage and oxygen deprivation stress: a reviewAnn Bot200291179194
  • ThannickalVJFanburgBLReactive oxygen species in cell signalingAm J Physiol Lung Cell Mol Physiol2000279L1005L102811076791
  • WangHZhangSXHartnettMESignaling pathways triggered by oxidative stress that mediate features of severe retinopathy of prematurityJAMA Ophthalmol2013131808523307212
  • Al ShabraweyMBartoliMEl RemessyABInhibition of NAD(P)H Oxidase activity blocks vascular endothelial growth factor overexpression and neovascularization during ischemic retinopathyAm J Pathol200516759960716049343
  • TanSMStefanovicNTanGWilkinson-BerkaJLde HaanJBLack of the antioxidant glutathione peroxidase-1 (GPx1) exacerbates retinopathy of prematurity in miceInvest Ophthalmol Vis Sci20135455556223287791
  • FuZJLiSYKociokNWongDChungSKLoACAldose reductase deficiency reduced vascular changes in neonatal mouse retina in oxygen-induced retinopathyInvest Ophthalmol Vis Sci2012535698571222836764
  • ParkSWChoCSJunHOAnti-angiogenic effect of luteolin on retinal neovascularization via blockade of reactive oxygen species productionInvest Ophthalmol Vis Sci2012537718772623099493
  • TanSMDeliyantiDFiggettWATaliaDMde HaanJBWilkinson-BerkaJLEbselen by modulating oxidative stress improves hypoxia-induced macroglial Muller cell and vascular injury in the retinaExp Eye Res20151361825912997
  • BeharryKDCaiCLSharmaPHydrogen peroxide accumulation in the choroid during intermittent hypoxia increases risk of severe oxygen-induced retinopathy in neonatal ratsInvest Ophthalmol Vis Sci2013547644765724168990
  • WangHYangZJiangYHartnettMEEndothelial NADPH oxidase 4 mediates vascular endothelial growth factor receptor 2-induced intravitreal neovascularization in a rat model of retinopathy of prematurityMol Vis20142023124124623966
  • DatlaSRPeshavariyaHDustingGJMahadevKGoldsteinBJJiangFImportant role of Nox4 type nADPH oxidase in angiogenic responses in human microvascular endothelial cells in vitroArterioscler Thromb Vasc Biol2007272319232417717289
  • StevensonLMatesanzNColhounLReduced nitro-oxidative stress and neural cell death suggests a protective role for microglial cells in TNFalpha−/− mice in ischemic retinopathyInvest Ophthalmol Vis Sci2010513291329920107169
  • SaitoYGeisenPUppalAHartnettMEInhibition of NAD(P)H oxidase reduces apoptosis and avascular retina in an animal model of retinopathy of prematurityMol Vis20071384085317615545
  • RistoriCFilippiLDal MonteMRole of the adrenergic system in a mouse model of oxygen-induced retinopathy: antiangiogenic effects of beta-adrenoreceptor blockadeInvest Ophthalmol Vis Sci20115215517020739470
  • SmithCPSharmaSSteinleJJAge-related changes in sympathetic neurotransmission in rat retina and choroidExp Eye Res200784758117074321
  • MartiniDMonteMDRistoriCAntiangiogenic effects of beta2 -adrenergic receptor blockade in a mouse model of oxygen-induced retinopathyJ Neurochem20111191317132921988318
  • Dal MonteMMartiniDLatinaVPavanBFilippiLBagnoliPBeta-adrenoreceptor agonism influences retinal responses to hypoxia in a model of retinopathy of prematurityInvest Ophthalmol Vis Sci2012532181219222410551
  • GiancottiFGRuoslahtiEIntegrin signalingScience19992851028103310446041
  • ByzovaTVGoldmanCKPamporiNA Mechanism for modulation of cellular responses to VEGF: activation of the integrinsMolecular Cell2000685186011090623
  • NingACuiJMaberleyDMaPMatsubaraJExpression of integrins in human proliferative diabetic retinopathy membranesCan J Ophthalmol20084368368819020635
  • Wilkinson-BerkaJLJonesDTaylorGSB-267268, a nonpeptidic antagonist of alpha(v)beta3 and alpha(v)beta5 integrins, reduces angiogenesis and VEGF expression in a mouse model of retinopathy of prematurityInvestigative Ophthalmol Vis Sci20064716001605
  • YoshidaTGongJXuZWeiYDuhEJInhibition of pathological retinal angiogenesis by the integrin alphavbeta3 antagonist tetraiodothyroacetic acid (tetrac)Exp Eye Res201294414822123068
  • AdamsRHEichmannAAxon guidance molecules in vascular patterningCold Spring Harb Perspect Biol20102a00187520452960
  • LobovIBRenardRAPapadopoulosNDelta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sproutingProc Natl Acad Sci U S A20071043219322417296940
  • JonesCANishiyaNLondonNRSlit2-Robo4 signalling promotes vascular stability by blocking Arf6 activityNat Cell Biol2009111325133119855388
  • JonesCALondonNRChenHRobo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyper-permeabilityNat Med20081444845318345009
  • RamaNDubracAMathivetTSlit2 signaling through Robo1 and Robo2 is required for retinal neovascularizationNat Med20152148349125894826