Promoting endothelial function by S-nitrosoglutathione through the HIF-1α/VEGF pathway stimulates neurorepair and functional recovery following experimental stroke in rats

References

• GoASMozaffarianDRogerVLAmerican Heart Association Statistics Committee and Stroke Statistics SubcommitteeHeart disease and stroke statistics – 2014 update: a report from the American Heart AssociationCirculation20141293e28e29224352519
   PubMed Web of Science ®Google Scholar
• RosamondWFlegalKFurieKAmerican Heart Association Statistics Committee and Stroke Statistics SubcommitteeHeart disease and stroke statistics – 2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics SubcommitteeCirculation20081174e25e14618086926
   PubMed Web of Science ®Google Scholar
• MoskowitzMALoEHIadecolaCThe science of stroke: mechanisms in search of treatmentsNeuron201067218119820670828
   PubMed Web of Science ®Google Scholar
• MakiTHayakawaKPhamLDXingCLoEHAraiKBiphasic mechanisms of neurovascular unit injury and protection in CNS diseasesCNS Neurol Disord Drug Targets201312330231523469847
   PubMed Web of Science ®Google Scholar
• CramerSCRepairing the human brain after stroke. II. Restorative therapiesAnn Neurol200863554956018481291
   PubMed Web of Science ®Google Scholar
• CramerSCRepairing the human brain after stroke: I. Mechanisms of spontaneous recoveryAnn Neurol200863327228718383072
   PubMed Web of Science ®Google Scholar
• KhanMSekhonBGiriSS-Nitrosoglutathione reduces inflammation and protects brain against focal cerebral ischemia in a rat model of experimental strokeJ Cereb Blood Flow Metab200525217719215647746
   PubMed Web of Science ®Google Scholar
• LiuDHYuanFGHuSQEndogenous nitric oxide induces activation of apoptosis signal-regulating kinase 1 via S-nitrosylation in rat hippocampus during cerebral ischemia-reperfusionNeuroscience2013229364823137546
   PubMed Web of Science ®Google Scholar
• KhanMDhammuTSSakakimaHThe inhibitory effect of S-nitrosoglutathione on blood-brain barrier disruption and peroxynitrite formation in a rat model of experimental strokeJ Neurochem2012123Suppl 2869723050646
   PubMed Web of Science ®Google Scholar
• YinXHYanJZHouXYWuSLZhangGYNeuroprotection of S-nitrosoglutathione against ischemic injury by down-regulating Fas S-nitrosylation and downstream signalingNeuroscience201324829029823792322
   PubMed Web of Science ®Google Scholar
• KhanMJatanaMElangoCPaintliaASSinghAKSinghICerebrovascular protection by various nitric oxide donors in rats after experimental strokeNitric Oxide200615211412416524750
   PubMed Web of Science ®Google Scholar
• SakakimaHKhanMDhammuTSStimulation of functional recovery via the mechanisms of neurorepair by S-nitrosoglutathione and motor exercise in a rat model of transient cerebral ischemia and reperfusionRestor Neurol Neurosci201230538339622717646
   PubMed Web of Science ®Google Scholar
• ChouPCShunmugavelAEl SayedHPreclinical use of longitudinal MRI for screening the efficacy of S-nitrosoglutathione in treating spinal cord injuryJ Magn Reson Imaging20113361301131121590998
   PubMed Web of Science ®Google Scholar
• KhanMSakakimaHDhammuTSS-nitrosoglutathione reduces oxidative injury and promotes mechanisms of neurorepair following traumatic brain injury in ratsJ Neuroinflammation201187821733162
   PubMed Web of Science ®Google Scholar
• KhanMImYBShunmugavelAAdministration of S-nitrosoglutathione after traumatic brain injury protects the neuro-vascular unit and reduces secondary injury in a rat model of controlled cortical impactJ Neuroinflammation200963219889224
   PubMed Web of Science ®Google Scholar
• WonJSKimJAnnamalaiBShunmugavelASinghISinghAKProtective role of S-nitrosoglutathione (GSNO) against cognitive impairment in rat model of chronic cerebral hypoperfusionJ Alzheimers Dis201334362163523254638
   PubMed Web of Science ®Google Scholar
• KimuraHOguraTKurashimaYWeiszAEsumiHEffects of nitric oxide donors on vascular endothelial growth factor gene inductionBiochem Biophys Res Commun2002296497698212200144
   PubMed Web of Science ®Google Scholar
• LimaBLamGKXieLEndogenous S-nitrosothiols protect against myocardial injuryProc Natl Acad Sci U S A2009106156297630219325130
   PubMed Web of Science ®Google Scholar
• KeQCostaMHypoxia-inducible factor-1 (HIF-1)Mol Pharmacol20067051469148016887934
   PubMed Web of Science ®Google Scholar
• IyerNVKotchLEAganiFCellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alphaGenes Dev19981221491629436976
   PubMed Web of Science ®Google Scholar
• KasivisvanathanVShalhoubJLimCSShepherdACThaparADaviesAHHypoxia-inducible factor-1 in arterial disease: a putative therapeutic targetCurr Vasc Pharmacol20119333334920807188
   PubMed Web of Science ®Google Scholar
• HartenSKAshcroftMMaxwellPHProlyl hydroxylase domain inhibitors: a route to HIF activation and neuroprotectionAntioxid Redox Signal201012445948019737089
   PubMed Web of Science ®Google Scholar
• PalmerLAGastonBJohnsRANormoxic stabilization of hypoxia-inducible factor-1 expression and activity: redox-dependent effect of nitrogen oxidesMol Pharmacol20005861197120311093754
   PubMed Web of Science ®Google Scholar
• WellmanTLJenkinsJPenarPLTranmerBZahrRLounsburyKMNitric oxide and reactive oxygen species exert opposing effects on the stability of hypoxia-inducible factor-1alpha (HIF-1alpha) in explants of human pial arteriesFASEB J200418237938114657004
   PubMedGoogle Scholar
• CarverDJGastonBDerondeKPalmerLAAkt-mediated activation of HIF-1 in pulmonary vascular endothelial cells by S-nitrosoglutathioneAm J Respir Cell Mol Biol200737325526317541013
   PubMed Web of Science ®Google Scholar
• MetzenEZhouJJelkmannWFandreyJBruneBNitric oxide impairs normoxic degradation of HIF-1alpha by inhibition of prolyl hydroxylasesMol Biol Cell20031483470348112925778
   PubMed Web of Science ®Google Scholar
• SinghSPWishnokJSKeshiveMDeenWMTannenbaumSRThe chemistry of the S-nitrosoglutathione/glutathione systemProc Natl Acad Sci U S A1996932514428144338962068
   PubMed Web of Science ®Google Scholar
• HessDTStamlerJSRegulation by S-nitrosylation of protein post-translational modificationJ Biol Chem201228774411441822147701
   PubMed Web of Science ®Google Scholar
• StamlerJSJarakiOOsborneJNitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albuminProc Natl Acad Sci U S A19928916767476771502182
   PubMed Web of Science ®Google Scholar
• KlugeIGutteck-AmslerUZollingerMDoKQS-nitrosoglutathione in rat cerebellum: identification and quantification by liquid chromatography-mass spectrometryJ Neurochem1997696259926079375694
   PubMed Web of Science ®Google Scholar
• BryanNSRassafTMaloneyRECellular targets and mechanisms of nitros(yl)ation: an insight into their nature and kinetics in vivoProc Natl Acad Sci U S A2004101124308431315014175
   PubMed Web of Science ®Google Scholar
• TsikasDSandmannJHolzbergDPantazisPRaidaMFrölichJCDetermination of S-nitrosoglutathione in human and rat plasma by high-performance liquid chromatography with fluorescence and ultraviolet absorbance detection after precolumn derivatization with o-phthalaldehydeAnal Biochem19992731324010452796
   PubMed Web of Science ®Google Scholar
• MatsumotoAGowAJMembrane transfer of S-nitrosothiolsNitric Oxide201125210210721377531
   PubMed Web of Science ®Google Scholar
• RadomskiMWReesDDDutraAMoncadaSS-nitroso-glutathione inhibits platelet activation in vitro and in vivoBr J Pharmacol199210737457491335336
   PubMed Web of Science ®Google Scholar
• SavidgeTCNewmanPPothoulakisCEnteric glia regulate intestinal barrier function and inflammation via release of S-nitroso-glutathioneGastroenterology200713241344135817408650
   PubMed Web of Science ®Google Scholar
• RassafTPollLWBrouzosPPositive effects of nitric oxide on left ventricular function in humansEur Heart J200627141699170516782717
   PubMed Web of Science ®Google Scholar
• KonorevEATarpeyMMJosephJBakerJEKalyanaramanBS-nitrosoglutathione improves functional recovery in the isolated rat heart after cardioplegic ischemic arrest-evidence for a cardioprotective effect of nitric oxideJ Pharmacol Exp Ther199527412002067616400
   PubMed Web of Science ®Google Scholar
• ChenQSieversREVargaMPharmacological inhibition of S-nitrosoglutathione reductase improves endothelial vasodilatory function in rats in vivoJ Appl Physiol (1985)2013114675276023349456
   PubMed Web of Science ®Google Scholar
• MatsudaFSakakimaHYoshidaYThe effects of early exercise on brain damage and recovery after focal cerebral infarction in ratsActa Physiol (Oxf)2011201227528720726846
   PubMed Web of Science ®Google Scholar
• SwansonRAMortonMTTsao-WuGSavalosRADavidsonCSharpFRA semiautomated method for measuring brain infarct volumeJ Cereb Blood Flow Metab19901022902931689322
   PubMed Web of Science ®Google Scholar
• MahmoodAGoussevALuDLong-lasting benefits after treatment of traumatic brain injury (TBI) in rats with combination therapy of marrow stromal cells (MSCs) and simvastatinJ Neurotrauma200825121441144719072586
   PubMed Web of Science ®Google Scholar
• LiYChenJChenXGHuman marrow stromal cell therapy for stroke in rat: neurotrophins and functional recoveryNeurology200259451452312196642
   PubMed Web of Science ®Google Scholar
• BorlonganCVSanbergPRElevated body swing test: a new behavioral parameter for rats with 6-hydroxydopamine-induced hemiparkinsonismJ Neurosci1995157 Pt 2537253787623159
   PubMed Web of Science ®Google Scholar
• MonvilleCTorresEMDunnettSBComparison of incremental and accelerating protocols of the rotarod test for the assessment of motor deficits in the 6-OHDA modelJ Neurosci Methods2006158221922316837051
   PubMed Web of Science ®Google Scholar
• ZhuYBuQLiuXHuWWangYNeuroprotective effect of TAT-14-3-3ε fusion protein against cerebral ischemia/reperfusion injury in ratsPLoS One201493e9333424671253
   PubMed Web of Science ®Google Scholar
• MontesanoRPepperMSMöhle-SteinleinURisauWWagnerEFOrciLIncreased proteolytic activity is responsible for the aberrant morphogenetic behavior of endothelial cells expressing the middle T oncogeneCell19906234354452379237
   PubMed Web of Science ®Google Scholar
• PrasadRGiriSNathNSinghISinghAKGSNO attenuates EAE disease by S-nitrosylation-mediated modulation of endothelial-monocyte interactionsGlia2007551657717019693
   PubMed Web of Science ®Google Scholar
• BovePFHristovaMWesleyUVOlsonNLounsburyKMvan der VlietAInflammatory levels of nitric oxide inhibit airway epithelial cell migration by inhibition of the kinase ERK1/2 and activation of hypoxia-inducible factor-1 alphaJ Biol Chem200828326179191792818424783
   PubMed Web of Science ®Google Scholar
• HePPhilbrickMJAnXWuJMessmer-BlustAFLiJEndothe-lial differentiation gene-1, a new downstream gene is involved in RTEF-1 induced angiogenesis in endothelial cellsPLoS One201492e8814324520353
   PubMed Web of Science ®Google Scholar
• JatanaMGiriSAnsariMAInhibition of NF-kappaB activation by 5-lipoxygenase inhibitors protects brain against injury in a rat model of focal cerebral ischemiaJ Neuroinflammation200631216689995
   PubMed Web of Science ®Google Scholar
• ValableSMontanerJBellailAVEGF-induced BBB permeability is associated with an MMP-9 activity increase in cerebral isch-emia: both effects decreased by Ang-1J Cereb Blood Flow Metab200525111491150415902195
   PubMed Web of Science ®Google Scholar
• MooberrySLMechanism of action of 2-methoxyestradiol: new developmentsDrug Resist Updat20036635536114744499
   PubMed Web of Science ®Google Scholar
• LokJGuptaPGuoSCell-cell signaling in the neurovascular unitNeurochem Res200732122032204517457674
   PubMed Web of Science ®Google Scholar
• WeiLErinjeriJPRovainenCMWoolseyTACollateral growth and angiogenesis around cortical strokeStroke20013292179218411546914
   PubMed Web of Science ®Google Scholar
• ChenJZhangZGLiYStatins induce angiogenesis, neurogenesis, and synaptogenesis after strokeAnn Neurol200353674375112783420
   PubMed Web of Science ®Google Scholar
• ChenJCuiXZacharekANiaspan increases angiogenesis and improves functional recovery after strokeAnn Neurol2007621495817557352
   PubMed Web of Science ®Google Scholar
• KawasakiKSmithRSJrHsiehCMSunJChaoJLiaoJKActivation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates nitric oxide-induced endothelial cell migration and angiogenesisMol Cell Biol200323165726573712897144
   PubMed Web of Science ®Google Scholar
• ZhangRLZhangZGChoppMTargeting nitric oxide in the subacute restorative treatment of ischemic strokeExpert Opin Investig Drugs2013227843851
   PubMed Web of Science ®Google Scholar
• TengHZhangZGWangLCoupling of angiogenesis and neu-rogenesis in cultured endothelial cells and neural progenitor cells after strokeJ Cereb Blood Flow Metab200828476477117971789
   PubMed Web of Science ®Google Scholar
• LeeCZXueZZhuYYangGYYoungWLMatrix metalloproteinase-9 inhibition attenuates vascular endothelial growth factor-induced intracerebral hemorrhageStroke20073892563256817673717
   PubMed Web of Science ®Google Scholar
• BauerATBürgersHFRabieTMartiHHMatrix metalloproteinase-9 mediates hypoxia-induced vascular leakage in the brain via tight junction rearrangementJ Cereb Blood Flow Metab201030483784819997118
   PubMed Web of Science ®Google Scholar
• LeeCZXueZHaoQYangGYYoungWLNitric oxide in vascular endothelial growth factor-induced focal angiogenesis and matrix metalloproteinase-9 activity in the mouse brainStroke20094082879288119498186
   PubMed Web of Science ®Google Scholar
• AggarwalAKheraASinghISandhirRS-nitrosoglutathione prevents blood–brain barrier disruption associated with increased matrix metalloproteinase-9 activity in experimental diabetesJ Neurochem Epub201494
   Web of Science ®Google Scholar
• KeXJZhangJJChanges in HIF-1α, VEGF, NGF and BDNF levels in cerebrospinal fluid and their relationship with cognitive impairment in patients with cerebral infarctionJ Huazhong Univ Sci Technolog Med Sci201333343343723771673
   PubMedGoogle Scholar
• ZhangZYanJTaheriSLiuKJShiHHypoxia-inducible factor 1 contributes to N-acetylcysteine’s protection in strokeFree Radic Biol Med20146882124296245
   PubMed Web of Science ®Google Scholar
• WangZTsaiLKMunasingheJChronic valproate treatment enhances postischemic angiogenesis and promotes functional recovery in a rat model of ischemic strokeStroke20124392430243622811460
   PubMed Web of Science ®Google Scholar
• ZhouDMatchettGAJadhavVDachNZhangJHThe effect of 2-methoxyestradiol, a HIF-1 alpha inhibitor, in global cerebral ischemia in ratsNeurol Res200830326827117716391
   PubMed Web of Science ®Google Scholar
• YasinskaIMSumbayevVVS-nitrosation of Cys-800 of HIF-1alpha protein activates its interaction with p300 and stimulates its transcriptional activityFEBS Lett20035491–310510912914934
   PubMed Web of Science ®Google Scholar
• SchonhoffCMMatsuokaMTummalaHS-nitrosothiol depletion in amyotrophic lateral sclerosisProc Natl Acad Sci U S A200610372404240916461917
   PubMed Web of Science ®Google Scholar
• JuTCChenSDLiuCCYangDIProtective effects of S-nitrosoglutathione against amyloid beta-peptide neurotoxicityFree Radic Biol Med200538793894915749390
   PubMed Web of Science ®Google Scholar
• RauhalaPMohanakumarKPSzirakiILinAMChiuehCCS-nitrosothiols and nitric oxide, but not sodium nitroprusside, protect nigrostriatal dopamine neurons against iron-induced oxidative stress in vivoSynapse199623158608723136
   PubMed Web of Science ®Google Scholar
• TerpolilliNAMoskowitzMAPlesnilaNNitric oxide: considerations for the treatment of ischemic strokeJ Cereb Blood Flow Metab20123271332134622333622
   PubMed Web of Science ®Google Scholar
• RashidPAWhitehurstALawsonNBathPMPlasma nitric oxide (nitrate/nitrite) levels in acute stroke and their relationship with severity and outcomeJ Stroke Cerebrovasc Dis2003122828717903909
   PubMedGoogle Scholar
• HeissCLauerTDejamAPlasma nitroso compounds are decreased in patients with endothelial dysfunctionJ Am Coll Cardiol200647357357916458138
   PubMed Web of Science ®Google Scholar
• RobertsBWMitchellJKilgannonJHChanskyMETrzeciakSNitric oxide donor agents for the treatment of ischemia/reperfusion injury in human subjects: a systematic reviewShock201339322923923358103
   PubMed Web of Science ®Google Scholar
• PlutaRMOldfieldEHBakhtianKDSafety and feasibility of long-term intravenous sodium nitrite infusion in healthy volunteersPLoS One201161e1450421249218
   PubMed Web of Science ®Google Scholar