At low doses ethanol maintains blood–brain barrier (BBB) integrity after hypoxia and reoxygenation: a brain slice study

References

• Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood–brain barrier. Neurobiol Dis. 2010;37:13–25.
   PubMed Web of Science ®Google Scholar
• del Zoppo GJ, von Kummer R, Hamann GF. Ischaemic damage of brain microvessels: Inherent risks for thrombolytic treatment in stroke. J Neurol Neurosurg Psychiatry. 1998;65:1–9.
   PubMed Web of Science ®Google Scholar
• Simard JM, Kent TA, Chen M, Tarasov KV, Gerzanich V. Brain oedema in focal ischaemia: Molecular pathophysiology and theoretical implications. Lancet Neurol. 2007;6:258–68.
   PubMed Web of Science ®Google Scholar
• Gerriets T, Walberer M, Ritschel N, Tschernatsch M, Mueller C, Bachmann G, et al.. Edema formation in the hyperacute phase of ischemic stroke. Laboratory investigation. J Neurosurg. 2009;111:1036–42.
   PubMed Web of Science ®Google Scholar
• Latour LL, Kang DW, Ezzeddine MA, Chalela JA, Warach S. Early blood–brain barrier disruption in human focal brain ischemia. Ann Neurol. 2004;56:468–77.
   PubMed Web of Science ®Google Scholar
• Brouns R, Wauters A, De Surgeloose D, Marien P, De Deyn PP. Biochemical markers for blood–brain barrier dysfunction in acute ischemic stroke correlate with evolution and outcome. Eur Neurol. 2011;65:23–31.
   PubMed Web of Science ®Google Scholar
• Sandoval KE, Witt KA. Blood–brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis. 2008;32:200–19.
   PubMed Web of Science ®Google Scholar
• Zeng X, Asmaro K, Ren C, Gao M, Peng C, Ding JY, et al.. Acute ethanol treatment reduces blood–brain barrier dysfunction following ischemia/reperfusion injury. Brain Res. 2012;1437:127–33.
   PubMed Web of Science ®Google Scholar
• Wang F, Wang Y, Geng X, Asmaro K, Peng C, Sullivan JM, et al.. Neuroprotective effect of acute ethanol administration in a rat with transient cerebral ischemia. Stroke. 2012;43:205–10.
   PubMed Web of Science ®Google Scholar
• Adibhatla RM, Hatcher JF. Tissue plasminogen activator (tPA) and matrix metalloproteinases in the pathogenesis of stroke: therapeutic strategies. CNS Neurol Disord Drug Targets. 2008;7:243–53.
   PubMed Web of Science ®Google Scholar
• Asahi M, Wang X, Mori T, Sumii T, Jung JC, Moskowitz MA, et al.. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood–brain barrier and white matter components after cerebral ischemia. J Neurosci. 2001;21:7724–32.
   PubMed Web of Science ®Google Scholar
• Mori T, Wang X, Aoki T, Lo EH. Downregulation of matrix metalloproteinase-9 and attenuation of edema via inhibition of ERK mitogen activated protein kinase in traumatic brain injury. J Neurotrauma. 2002;19:1411–9.
   PubMed Web of Science ®Google Scholar
• Hjort N, Wu O, Ashkanian M, Sølling C, Mouridsen K, Christensen S, et al.. MRI detection of early blood–brain barrier disruption: parenchymal enhancement predicts focal hemorrhagic transformation after thrombolysis. Stroke. 2008;39:1025–8.
   PubMed Web of Science ®Google Scholar
• Rosell A, Cuadrado E, Ortega-Aznar A, Hernandez-Guillamon M, Lo EH, Montaner J. MMP-9-positive neutrophil infiltration is associated to blood–brain barrier breakdown and basal lamina type IV collagen degradation during hemorrhagic transformation after human ischemic stroke. Stroke. 2008;39:1121–6.
   PubMed Web of Science ®Google Scholar
• Dong X, Song YN, Liu WG, Guo XL. Mmp-9, a potential target for cerebral ischemic treatment. Curr Neuropharmacol. 2009;7:269–75.
   PubMed Web of Science ®Google Scholar
• Romanic AM, White RF, Arleth AJ, Ohlstein EH, Barone FC. Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke. 1998;29:1020–30.
   PubMed Web of Science ®Google Scholar
• Zador Z, Stiver S, Wang V, Manley GT. Role of aquaporin-4 in cerebral edema and stroke. Handb Exp Pharmacol. 2009:159–70.
   PubMedGoogle Scholar
• Higashida T, Peng C, Li J, Dornbos D, Teng K, Li X, et al.. Hypoxia-inducible factor-1α contributes to brain edema after stroke by regulating aquaporins and glycerol distribution in brain. Curr Neurovasc Res. 2011;8:44–51.
   PubMed Web of Science ®Google Scholar
• Manley GT, Fujimura M, Ma T, Noshita N, Filiz F, Bollen AW, et al.. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med. 2000;6:159–63.
   PubMed Web of Science ®Google Scholar
• Badaut J, Brunet JF, Regli L. Aquaporins in the brain: from aqueduct to ‘multi-duct’. Metab Brain Dis. 2007;22:251–63.
   PubMed Web of Science ®Google Scholar
• Badaut J. Aquaglyceroporin 9 in brain pathologies. Neuroscience. 2010;168:1047–57.
   PubMed Web of Science ®Google Scholar
• Kett-White R, O'Connell MT, Hutchinson PJ, Al-Rawi PG, Gupta AK, Pickard JD, et al.. Extracellular amino acid changes in patients during reversible cerebral ischaemia. Acta Neurochir Suppl. 2005;95:83–8.
   PubMedGoogle Scholar
• Nurmi M, Kiianmaa K, Sinclair JD. Brain ethanol levels after voluntary ethanol drinking in AA and Wistar rats. Alcohol. 1999;19:113–8.
   PubMed Web of Science ®Google Scholar
• Peris J, Zharikova A, Li Z, Lingis M, MacNeill M, Wu MT, et al.. Brain ethanol levels in rats after voluntary ethanol consumption using a sweetened gelatin vehicle. Pharmacol Biochem Behav. 2006;85:562–8.
   PubMed Web of Science ®Google Scholar
• Quertemont E, Green HL, Grant KA. Brain ethanol concentrations and ethanol discrimination in rats: effects of dose and time. Psychopharmacology. 2003;168:262–70.
   PubMed Web of Science ®Google Scholar
• Kelly DF, Kozlowski DA, Haddad E, Echiverri A, Hovda DA, Lee SM. Ethanol reduces metabolic uncoupling following experimental head injury. J Neurotrauma. 2000;17:261–72.
   PubMed Web of Science ®Google Scholar
• Eckardt MJ, File SE, Gessa GL, Grant KA, Guerri C, Hoffman PL, et al.. Effects of moderate alcohol consumption on the central nervous system. Alcohol Clin Exp Res. 1998;22:998–1040.
   PubMed Web of Science ®Google Scholar
• Yuan Y, Peng C, Li K, Hussain M, Sikharam C, Guthikonda M, et al.. Ethanol reduces expression of apoptotic proteins after hypoxia/reoxygenation in a brain slice model. Neurol Res. 2012;34:373–8.
   PubMed Web of Science ®Google Scholar
• Fuller L, Dailey ME. Preparation of rodent hippocampal slice cultures. CSH Protoc. 2007;2007: pdb prot4848.
   PubMedGoogle Scholar
• Taylor CP, Weber ML, Gaughan CL, Lehning EJ, LoPachin RM. Oxygen/glucose deprivation in hippocampal slices: altered intraneuronal elemental composition predicts structural and functional damage. J Neurosci. 1999;19:619–29.
   PubMed Web of Science ®Google Scholar
• Badaut J, Ashwal S, Obenaus A. Aquaporins in cerebrovascular disease: A target for treatment of brain edema? Cerebrovasc Dis. 2011;31:521–31.
   PubMed Web of Science ®Google Scholar
• Ribeiro Mde C, Hirt L, Bogousslavsky J, Regli L, Badaut J. Time course of aquaporin expression after transient focal cerebral ischemia in mice. J Neurosci Res. 2006;83:1231–40.
   PubMed Web of Science ®Google Scholar
• Badaut J, Lasbennes F, Magistretti PJ, Regli L. Aquaporins in brain: Distribution, physiology, and pathophysiology. J Cereb Blood Flow Metab. 2002;22:367–78.
   PubMed Web of Science ®Google Scholar
• Go KG. The normal and pathological physiology of brain water. Adv Tech Stand Neurosurg. 1997;23:47–142.
   PubMedGoogle Scholar
• Kempski O. Cerebral edema. Semin Nephrol. 2001;21:303–7.
   PubMed Web of Science ®Google Scholar
• Amiry-Moghaddam M, Ottersen OP. The molecular basis of water transport in the brain. Nat Rev Neurosci. 2003;4:991–1001.
   PubMed Web of Science ®Google Scholar
• Manley GT, Binder DK, Papadopoulos MC, Verkman AS. New insights into water transport and edema in the central nervous system from phenotype analysis of aquaporin-4 null mice. Neuroscience. 2004;129:983–91.
   PubMed Web of Science ®Google Scholar
• Strbian D, Durukan A, Pitkonen M, Marinkovic I, Tatlisumak E, Pedrono E, et al.. The blood–brain barrier is continuously open for several weeks following transient focal cerebral ischemia. Neuroscience. 2008;153:175–81.
   PubMed Web of Science ®Google Scholar
• Henning EC, Latour LL, Warach S. Verification of enhancement of the CSF space, not parenchyma, in acute stroke patients with early blood–brain barrier disruption. J Cereb Blood Flow Metab. 2008;28:882–6.
   PubMed Web of Science ®Google Scholar
• Woessner JF. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 1991;5:2145–54.
   PubMed Web of Science ®Google Scholar
• Yurchenco PD, Schittny JC. Molecular architecture of basement membranes. FASEB J. 1990;4:1577–90.
   PubMed Web of Science ®Google Scholar
• Romanic AM, Madri JA. Extracellular matrix-degrading proteinases in the nervous system. Brain Pathol. 1994;4:145–56.
   PubMed Web of Science ®Google Scholar
• McColl BW, Rose N, Robson FH, Rothwell NJ, Lawrence CB. Increased brain microvascular MMP-9 and incidence of haemorrhagic transformation in obese mice after experimental stroke. J Cereb Blood Flow Metab. 2010;30:267–72.
   PubMed Web of Science ®Google Scholar
• McColl BW, Rothwell NJ, Allan SM. Systemic inflammation alters the kinetics of cerebrovascular tight junction disruption after experimental stroke in mice. J Neurosci. 2008;28:9451–62.
   PubMed Web of Science ®Google Scholar
• Huang J, Upadhyay UM, Tamargo RJ. Inflammation in stroke and focal cerebral ischemia. Surg Neurol. 2006;66:232–45.
   PubMed Web of Science ®Google Scholar
• Liguz-Lecznar M, Ziemka-Nalecz M, Aleksy M, Kossut M, Skangiel-Kramska J, Nowicka D. Comparison of matrix metalloproteinase activation after focal cortical ischemia in young adult and aged mice. J Neurosci Res. 2012;90:203–12.
   PubMed Web of Science ®Google Scholar
• Tien HC, Tremblay LN, Rizoli SB, Gelberg J, Chughtai T, Tikuisis P, et al.. Association between alcohol and mortality in patients with severe traumatic head injury. Arch Surg. 2006;141:1185–91; discussion 1192.
   PubMedGoogle Scholar
• Zehendner CM, Librizzi L, de Curtis M, Kuhlmann CR, Luhmann HJ. Caspase-3 contributes to ZO-1 and CI-5 tight-junction disruption in rapid anoxic neurovascular unit damage. PLoS One. 2011;6:e16760.
   PubMed Web of Science ®Google Scholar
• Milner R, Hung S, Wang X, Spatz M, del Zoppo GJ. The rapid decrease in astrocyte-associated dystroglycan expression by focal cerebral ischemia is protease-dependent. J Cereb Blood Flow Metab. 2008;28:812–23.
   PubMed Web of Science ®Google Scholar
• Bertuglia S, Giusti A. Microvascular oxygenation and oxidative stress during postischemic reperfusion. PO2, ROS, and NO during reperfusion. Adv Exp Med Biol. 2005;566:23–9.
   PubMed Web of Science ®Google Scholar
• Schaller B, Graf R. Cerebral ischemia and reperfusion: the pathophysiologic concept as a basis for clinical therapy. J Cereb Blood Flow Metab. 2004;24:351–71.
   PubMed Web of Science ®Google Scholar
• Gidday JM, Gasche YG, Copin JC, Shah AR, Perez RS, Shapiro SD, et al.. Leukocyte-derived matrix metalloproteinase-9 mediates blood–brain barrier breakdown and is proinflammatory after transient focal cerebral ischemia. Am J Physiol Heart Circ Physiol. 2005;289:H558–68.
   PubMed Web of Science ®Google Scholar
• Rosenberg GA, Cunningham LA, Wallace J, Alexander S, Estrada EY, Grossetete M, et al.. Immunohistochemistry of matrix metalloproteinases in reperfusion injury to rat brain: activation of MMP-9 linked to stromelysin-1 and microglia in cell cultures. Brain Res. 2001;893:104–12.
   PubMed Web of Science ®Google Scholar
• Rosenberg GA, Estrada EY, Dencoff JE. Matrix metalloproteinases and TIMPs are associated with blood–brain barrier opening after reperfusion in rat brain. Stroke. 1998;29:2189–95.
   PubMed Web of Science ®Google Scholar
• Zhao YJ, Yang GY, Ben-Joseph O, Ross BD, Chenevert TL, Domino EF. Acute ethanol effects on focal cerebral ischemia in fasted rats. Alcohol Clin Exp Res. 1998;22:717–22.
   PubMed Web of Science ®Google Scholar
• Floreani NA, Rump TJ, Abdul Muneer PM, Alikunju S, Morsey BM, Brodie MR, et al.. Alcohol-induced interactive phosphorylation of Src and toll-like receptor regulates the secretion of inflammatory mediators by human astrocytes. J Neuroimmune Pharmacol. 2010;5:533–45.
   PubMed Web of Science ®Google Scholar
• Alikunju S, Abdul Muneer PM, Zhang Y, Szlachetka AM, Haorah J. The inflammatory footprints of alcohol-induced oxidative damage in neurovascular components. Brain Behav Immun. 2011;25 Suppl.1:S129–36.
   PubMed Web of Science ®Google Scholar
• Montaner J, Alvarez-Sabin J, Molina CA, Anglés A, Abilleira S, Arenillas J, et al.. Matrix metalloproteinase expression is related to hemorrhagic transformation after cardioembolic stroke. Stroke. 2001;32:2762–7.
   PubMed Web of Science ®Google Scholar
• Rosell A, Ortega-Aznar A, Alvarez-Sabin J, Fernández-Cadenas I, Ribó M, Molina CA, et al.. Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke. 2006;37:1399–406.
   PubMed Web of Science ®Google Scholar