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Published in: European Journal of Applied Physiology 1/2012

01-01-2012 | Original Article

Effects of hyperbaric oxygenation on oxidative stress in acute transient focal cerebral ischemic rats

Authors: Ray-Yau Wang, Heng-Chih Chang, Chun-Hao Chen, Yi-Wei Tsai, Yea-Ru Yang

Published in: European Journal of Applied Physiology | Issue 1/2012

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Abstract

The aim of this study was to investigate the effects of hyperbaric oxygenation (HBO) after brain ischemia. Middle cerebral artery occlusion (MCAO) procedure was used to induce the brain ischemia. Rats were assigned to control or HBO group after brain ischemia. In order to examine the role of glutathione after HBO treatment, another group of brain ischemic rats were included to receive the glutathione synthesis inhibitor and HBO treatment. HBO was administered at a pressure of 3 atmospheres absolute for 1 h with 100% oxygen, starting at 3 h post brain ischemia in HBO groups. Animals in control group were placed in their home cage and exposed to normobaric room air. The infarct volume (IV), activation of astrocyte, and level of total glutathione and lipid peroxidation (LP) were assessed 24 h post-reperfusion. Significant reduction in IV was noted in HBO group when compared with control group. The activation of astrocyte was significantly increased in the right cerebral cortex and right striatum in the HBO group when compared with those of the control group. The glutathione level was higher with lower LP level in right cortex and right striatum after HBO as compared with those of the control. However, such effects of HBO treatment were markedly reduced by glutathione synthesis inhibitor administration. These results show that inhibiting glutathione synthesis dramatically reduces the effectiveness of HBO in acute transient focal cerebral ischemia.
Literature
go back to reference Chang HC, Yang YR, Wang SG, Wang RY (2009) Effects of treadmill training on motor performance and extracellular glutamate level in striatum in rats with or without transient middle cerebral artery occlusion. Behav Brain Res 205:450–455PubMedCrossRef Chang HC, Yang YR, Wang SG, Wang RY (2009) Effects of treadmill training on motor performance and extracellular glutamate level in striatum in rats with or without transient middle cerebral artery occlusion. Behav Brain Res 205:450–455PubMedCrossRef
go back to reference Chen ST, Hsu CY, Hogan EL, Maricq H, Balentine JD (1986) A model of focal ischemic stroke in the rat: reproducible extensive cortical infarction. Stroke 17:738–743PubMedCrossRef Chen ST, Hsu CY, Hogan EL, Maricq H, Balentine JD (1986) A model of focal ischemic stroke in the rat: reproducible extensive cortical infarction. Stroke 17:738–743PubMedCrossRef
go back to reference DeBow SB, Clark DL, MacLellan CL, Colbourne F (2003) Incomplete assessment of experimental cytoprotectants in rodent ischemia studies. Can J Neurol Sci 30:368–374PubMed DeBow SB, Clark DL, MacLellan CL, Colbourne F (2003) Incomplete assessment of experimental cytoprotectants in rodent ischemia studies. Can J Neurol Sci 30:368–374PubMed
go back to reference Desagher S, Glowinski J, Premont J (1996) Astrocytes protect neurons from hydrogen peroxide toxicity. J Neurosci 16:2553–2562PubMed Desagher S, Glowinski J, Premont J (1996) Astrocytes protect neurons from hydrogen peroxide toxicity. J Neurosci 16:2553–2562PubMed
go back to reference Dringen R, Pfeiffer B, Hamprecht B (1999) Synthesis of the antioxidant glutathione in neurons: supply by astrocytes of CysGly as precursor for neuronal glutathione. J Neurosci 19:562–569PubMed Dringen R, Pfeiffer B, Hamprecht B (1999) Synthesis of the antioxidant glutathione in neurons: supply by astrocytes of CysGly as precursor for neuronal glutathione. J Neurosci 19:562–569PubMed
go back to reference Dringen R, Gutterer JM, Hirrlinger J (2000) Glutathione metabolism in brain metabolic interaction between astrocytes and neurons in the defense against reactive oxygen species. Eur J Biochem 267:4912–4916PubMedCrossRef Dringen R, Gutterer JM, Hirrlinger J (2000) Glutathione metabolism in brain metabolic interaction between astrocytes and neurons in the defense against reactive oxygen species. Eur J Biochem 267:4912–4916PubMedCrossRef
go back to reference Drukarch B, Schepens E, Jongenelen CA, Stoof JC, Langeveld CH (1997) Astrocyte-mediated enhancement of neuronal survival is abolished by glutathione deficiency. Brain Res 770:123–130PubMedCrossRef Drukarch B, Schepens E, Jongenelen CA, Stoof JC, Langeveld CH (1997) Astrocyte-mediated enhancement of neuronal survival is abolished by glutathione deficiency. Brain Res 770:123–130PubMedCrossRef
go back to reference Facchinetti F, Dawson VL, Dawson TM (1998) Free radicals as mediators of neuronal injury. Cell Mol Neurobiol 18:667–682PubMedCrossRef Facchinetti F, Dawson VL, Dawson TM (1998) Free radicals as mediators of neuronal injury. Cell Mol Neurobiol 18:667–682PubMedCrossRef
go back to reference Gunther A, Kuppers-Tiedt L, Schneider PM, Kunert I, Berrouschot J, Schneider D, Rossner S (2005) Reduced infarct volume and differential effects on glial cell activation after hyperbaric oxygen treatment in rat permanent focal cerebral ischaemia. Eur J Neurosci 21:3189–3194PubMedCrossRef Gunther A, Kuppers-Tiedt L, Schneider PM, Kunert I, Berrouschot J, Schneider D, Rossner S (2005) Reduced infarct volume and differential effects on glial cell activation after hyperbaric oxygen treatment in rat permanent focal cerebral ischaemia. Eur J Neurosci 21:3189–3194PubMedCrossRef
go back to reference Halliwell BGJ (2007) Free radicals in biology and medicine. Oxford University Press, New York Halliwell BGJ (2007) Free radicals in biology and medicine. Oxford University Press, New York
go back to reference Heales SJ, Lam AA, Duncan AJ, Land JM (2004) Neurodegeneration or neuroprotection: the pivotal role of astrocytes. Neurochem Res 29:513–519PubMedCrossRef Heales SJ, Lam AA, Duncan AJ, Land JM (2004) Neurodegeneration or neuroprotection: the pivotal role of astrocytes. Neurochem Res 29:513–519PubMedCrossRef
go back to reference Huang ZX, Kang ZM, Gu GJ, Peng GN, Yun L, Tao HY, Xu WG, Sun XJ, Zhang JH (2007) Therapeutic effects of hyperbaric oxygen in a rat model of endothelin-1-induced focal cerebral ischemia. Brain Res 1153:204–213PubMedCrossRef Huang ZX, Kang ZM, Gu GJ, Peng GN, Yun L, Tao HY, Xu WG, Sun XJ, Zhang JH (2007) Therapeutic effects of hyperbaric oxygen in a rat model of endothelin-1-induced focal cerebral ischemia. Brain Res 1153:204–213PubMedCrossRef
go back to reference Liberto CM, Albrecht PJ, Herx LM, Yong VW, Levison SW (2004) Pro-regenerative properties of cytokine-activated astrocytes. J Neurochem 89:1092–1100PubMedCrossRef Liberto CM, Albrecht PJ, Herx LM, Yong VW, Levison SW (2004) Pro-regenerative properties of cytokine-activated astrocytes. J Neurochem 89:1092–1100PubMedCrossRef
go back to reference Lin TN, He YY, Wu G, Khan M, Hsu CY (1993) Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 24:117–121PubMedCrossRef Lin TN, He YY, Wu G, Khan M, Hsu CY (1993) Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 24:117–121PubMedCrossRef
go back to reference Lou M, Eschenfelder CC, Herdegen T, Brecht S, Deuschl G (2004) Therapeutic window for use of hyperbaric oxygenation in focal transient ischemia in rats. Stroke 35:578–583PubMedCrossRef Lou M, Eschenfelder CC, Herdegen T, Brecht S, Deuschl G (2004) Therapeutic window for use of hyperbaric oxygenation in focal transient ischemia in rats. Stroke 35:578–583PubMedCrossRef
go back to reference Lou M, Chen Y, Ding M, Eschenfelder CC, Deuschl G (2006) Involvement of the mitochondrial ATP-sensitive potassium channel in the neuroprotective effect of hyperbaric oxygenation after cerebral ischemia. Brain Res Bull 69:109–116PubMedCrossRef Lou M, Chen Y, Ding M, Eschenfelder CC, Deuschl G (2006) Involvement of the mitochondrial ATP-sensitive potassium channel in the neuroprotective effect of hyperbaric oxygenation after cerebral ischemia. Brain Res Bull 69:109–116PubMedCrossRef
go back to reference Makar TK, Nedergaard M, Preuss A, Gelbard AS, Perumal AS, Cooper AJ (1994) Vitamin E, ascorbate, glutathione, glutathione disulfide, and enzymes of glutathione metabolism in cultures of chick astrocytes and neurons: evidence that astrocytes play an important role in antioxidative processes in the brain. J Neurochem 62:45–53PubMedCrossRef Makar TK, Nedergaard M, Preuss A, Gelbard AS, Perumal AS, Cooper AJ (1994) Vitamin E, ascorbate, glutathione, glutathione disulfide, and enzymes of glutathione metabolism in cultures of chick astrocytes and neurons: evidence that astrocytes play an important role in antioxidative processes in the brain. J Neurochem 62:45–53PubMedCrossRef
go back to reference Mergenthaler P, Dirnagl U, Meisel A (2004) Pathophysiology of stroke: lessons from animal models. Metab Brain Dis 19:151–167PubMedCrossRef Mergenthaler P, Dirnagl U, Meisel A (2004) Pathophysiology of stroke: lessons from animal models. Metab Brain Dis 19:151–167PubMedCrossRef
go back to reference Mesples B, Plaisant F, Fontaine RH, Gressens P (2005) Pathophysiology of neonatal brain lesions: lessons from animal models of excitotoxicity. Acta Paediatr 94:185–190PubMedCrossRef Mesples B, Plaisant F, Fontaine RH, Gressens P (2005) Pathophysiology of neonatal brain lesions: lessons from animal models of excitotoxicity. Acta Paediatr 94:185–190PubMedCrossRef
go back to reference Mink RB, Dutka AJ (1995) Hyperbaric oxygen after global cerebral ischemia in rabbits does not promote brain lipid peroxidation. Crit Care Med 23:1398–1404PubMedCrossRef Mink RB, Dutka AJ (1995) Hyperbaric oxygen after global cerebral ischemia in rabbits does not promote brain lipid peroxidation. Crit Care Med 23:1398–1404PubMedCrossRef
go back to reference Noda Y, McGeer PL, McGeer EG (1983) Lipid peroxide distribution in brain and the effect of hyperbaric oxygen. J Neurochem 40:1329–1332PubMedCrossRef Noda Y, McGeer PL, McGeer EG (1983) Lipid peroxide distribution in brain and the effect of hyperbaric oxygen. J Neurochem 40:1329–1332PubMedCrossRef
go back to reference Ostrowski RP, Colohan AR, Zhang JH (2006) Neuroprotective effect of hyperbaric oxygen in a rat model of subarachnoid hemorrhage. Acta Neurochir Suppl 96:188–193PubMedCrossRef Ostrowski RP, Colohan AR, Zhang JH (2006) Neuroprotective effect of hyperbaric oxygen in a rat model of subarachnoid hemorrhage. Acta Neurochir Suppl 96:188–193PubMedCrossRef
go back to reference Ozden TA, Uzun H, Bohloli M, Toklu AS, Paksoy M, Simsek G, Durak H, Issever H, Ipek T (2004) The effects of hyperbaric oxygen treatment on oxidant and antioxidants levels during liver regeneration in rats. Tohoku J Exp Med 203:253–265PubMedCrossRef Ozden TA, Uzun H, Bohloli M, Toklu AS, Paksoy M, Simsek G, Durak H, Issever H, Ipek T (2004) The effects of hyperbaric oxygen treatment on oxidant and antioxidants levels during liver regeneration in rats. Tohoku J Exp Med 203:253–265PubMedCrossRef
go back to reference Rahman I, Kode A, Biswas SK (2006) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1:3159–3165PubMedCrossRef Rahman I, Kode A, Biswas SK (2006) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1:3159–3165PubMedCrossRef
go back to reference Raps SP, Lai JC, Hertz L, Cooper AJ (1989) Glutathione is present in high concentrations in cultured astrocytes but not in cultured neurons. Brain Res 493:398–401PubMedCrossRef Raps SP, Lai JC, Hertz L, Cooper AJ (1989) Glutathione is present in high concentrations in cultured astrocytes but not in cultured neurons. Brain Res 493:398–401PubMedCrossRef
go back to reference Reitan JA, Kien ND, Thorup S, Corkill G (1990) Hyperbaric oxygen increases survival following carotid ligation in gerbils. Stroke 21:119–123PubMedCrossRef Reitan JA, Kien ND, Thorup S, Corkill G (1990) Hyperbaric oxygen increases survival following carotid ligation in gerbils. Stroke 21:119–123PubMedCrossRef
go back to reference Sagara JI, Miura K, Bannai S (1993) Maintenance of neuronal glutathione by glial cells. J Neurochem 61:1672–1676PubMedCrossRef Sagara JI, Miura K, Bannai S (1993) Maintenance of neuronal glutathione by glial cells. J Neurochem 61:1672–1676PubMedCrossRef
go back to reference Sun L, Marti HH, Veltkamp R (2008) Hyperbaric oxygen reduces tissue hypoxia and hypoxia-inducible factor-1 alpha expression in focal cerebral ischemia. Stroke 39:1000–1006PubMedCrossRef Sun L, Marti HH, Veltkamp R (2008) Hyperbaric oxygen reduces tissue hypoxia and hypoxia-inducible factor-1 alpha expression in focal cerebral ischemia. Stroke 39:1000–1006PubMedCrossRef
go back to reference Swanson RA, Ying W, Kauppinen TM (2004) Astrocyte influences on ischemic neuronal death. Curr Mol Med 4:193–205PubMedCrossRef Swanson RA, Ying W, Kauppinen TM (2004) Astrocyte influences on ischemic neuronal death. Curr Mol Med 4:193–205PubMedCrossRef
go back to reference Takahashi M, Iwatsuki N, Ono K, Tajima T, Akama M, Koga Y (1992) Hyperbaric oxygen therapy accelerates neurologic recovery after 15-minute complete global cerebral ischemia in dogs. Crit Care Med 20:1588–1594PubMedCrossRef Takahashi M, Iwatsuki N, Ono K, Tajima T, Akama M, Koga Y (1992) Hyperbaric oxygen therapy accelerates neurologic recovery after 15-minute complete global cerebral ischemia in dogs. Crit Care Med 20:1588–1594PubMedCrossRef
go back to reference Trendelenburg G, Dirnagl U (2005) Neuroprotective role of astrocytes in cerebral ischemia: focus on ischemic preconditioning. Glia 50:307–320PubMedCrossRef Trendelenburg G, Dirnagl U (2005) Neuroprotective role of astrocytes in cerebral ischemia: focus on ischemic preconditioning. Glia 50:307–320PubMedCrossRef
go back to reference Wada K, Miyazawa T, Nomura N, Tsuzuki N, Nawashiro H, Shima K (2001) Preferential conditions for and possible mechanisms of induction of ischemic tolerance by repeated hyperbaric oxygenation in gerbil hippocampus. Neurosurgery 49:160–166 discussion 166-167PubMed Wada K, Miyazawa T, Nomura N, Tsuzuki N, Nawashiro H, Shima K (2001) Preferential conditions for and possible mechanisms of induction of ischemic tolerance by repeated hyperbaric oxygenation in gerbil hippocampus. Neurosurgery 49:160–166 discussion 166-167PubMed
go back to reference Wang RY, Wang PS, Yang YR (2003) Effect of age in rats following middle cerebral artery occlusion. Gerontology 49:27–32PubMedCrossRef Wang RY, Wang PS, Yang YR (2003) Effect of age in rats following middle cerebral artery occlusion. Gerontology 49:27–32PubMedCrossRef
go back to reference Yang YR, Wang RY, Wang PS (2003a) Early and late treadmill training after focal brain ischemia in rats. Neurosci Lett 339:91–94PubMedCrossRef Yang YR, Wang RY, Wang PS (2003a) Early and late treadmill training after focal brain ischemia in rats. Neurosci Lett 339:91–94PubMedCrossRef
go back to reference Yang YR, Wang RY, Wang PS, Yu SM (2003b) Treadmill training effects on neurological outcome after middle cerebral artery occlusion in rats. Can J Neurol Sci 30:252–258PubMed Yang YR, Wang RY, Wang PS, Yu SM (2003b) Treadmill training effects on neurological outcome after middle cerebral artery occlusion in rats. Can J Neurol Sci 30:252–258PubMed
Metadata
Title
Effects of hyperbaric oxygenation on oxidative stress in acute transient focal cerebral ischemic rats
Authors
Ray-Yau Wang
Heng-Chih Chang
Chun-Hao Chen
Yi-Wei Tsai
Yea-Ru Yang
Publication date
01-01-2012
Publisher
Springer-Verlag
Published in
European Journal of Applied Physiology / Issue 1/2012
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-011-1976-2

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