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Shock/Sepsis/Trauma/Critical care| Volume 184, ISSUE 2, e27-e35, October 2013

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Protective effects of hydrogen sulfide in a rat model of traumatic brain injury via activation of mitochondrial adenosine triphosphate–sensitive potassium channels and reduction of oxidative stress

  • Author Footnotes
    1 Xiaofan Jiang and Yi Huang contributed equally to this work.
    Xiaofan Jiang
    Footnotes
    1 Xiaofan Jiang and Yi Huang contributed equally to this work.
    Affiliations
    Department of Neurosurgery, Xijing Institute of Clinical Neuroscience, Xiing Hospital, Fourth Military Medical University, Xi’an, Shaanxi Province, People’s Republic of China
    Search for articles by this author
  • Author Footnotes
    1 Xiaofan Jiang and Yi Huang contributed equally to this work.
    Yi Huang
    Footnotes
    1 Xiaofan Jiang and Yi Huang contributed equally to this work.
    Affiliations
    Department of Anesthesiology, Xiing Hospital, Fourth Military Medical University, Xi’an, Shaanxi Province, People’s Republic of China
    Search for articles by this author
  • Wei Lin
    Affiliations
    Department of Neurosurgery, Xijing Institute of Clinical Neuroscience, Xiing Hospital, Fourth Military Medical University, Xi’an, Shaanxi Province, People’s Republic of China
    Search for articles by this author
  • Dakuan Gao
    Affiliations
    Department of Neurosurgery, Xijing Institute of Clinical Neuroscience, Xiing Hospital, Fourth Military Medical University, Xi’an, Shaanxi Province, People’s Republic of China
    Search for articles by this author
  • Zhou Fei
    Correspondence
    Corresponding author. Department of Neurosurgery, Xijing Institute of Clinical Neuroscience, Xiing Hospital, Fourth Military Medical University, Xi’an 710032, Shaanxi Province, P. R. China. Tel.: +86 29 84775323; fax: +86 29 84775567.
    Affiliations
    Department of Neurosurgery, Xijing Institute of Clinical Neuroscience, Xiing Hospital, Fourth Military Medical University, Xi’an, Shaanxi Province, People’s Republic of China
    Search for articles by this author
  • Author Footnotes
    1 Xiaofan Jiang and Yi Huang contributed equally to this work.
Published:April 10, 2013DOI:https://doi.org/10.1016/j.jss.2013.03.067
Protective effects of hydrogen sulfide in a rat model of traumatic brain injury via activation of mitochondrial adenosine triphosphate–sensitive potassium channels and reduction of oxidative stress
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      Abstract

      Background

      Hydrogen sulfide (H2S) is considered an important neuromodulator in the central nervous system. We designed the present study to investigate the effects of exogenous H2S in a rat model of traumatic brain injury (TBI) and the mechanism(s) that underlie this effect.

      Methods

      We induced a TBI model by controlled cortical impact injury. We intraperitoneally administered sodium hydrosulfide (NaHS) (an H2S donor) (3 mg/kg) or vehicle alone at 5 min after a TBI operation. We then measured the H2S level, brain edema, blood-brain barrier integrity, neurologic dysfunction, and lesion volume in all animals. Moreover, we assessed the role of mitochondrial adenosine triphosphate–sensitive potassium (mitoKATP)channels by intraperitoneal injection of the selective blocker 5-hydroxydecanoate before NaHS administration. In addition, we detected the levels of oxidative products and the activities of antioxidant enzymes in brain tissue.

      Results

      Administration of NaHS significantly increased the H2S level of brain tissue in TBI-challenged rats. The TBI-challenged animals exhibited significant brain injuries, characterized by an increase of blood-brain barrier permeability, brain edema, and lesion volume, as well as neurologic dysfunction, which were significantly ameliorated by NaHS treatment. However, the protective effects of H2S in TBI could be abolished by the mitoKATPchannel blocker 5-hydroxydecanoate. Moreover, we found that NaHS treatment increased endogenous antioxidant enzymatic activities and decreased oxidative product levels in brain tissue of TBI-challenged rats.

      Conclusions

      Exogenous H2S administered at an appropriate dose can exert a protective effect against TBI via activation of mitoKATP channels and reduction of oxidative stress.

      Keywords

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      References

        • Elliott M.B.
        • Jallo J.J.
        • Barbe M.F.
        • et al.
        Hypertonic saline attenuates tissue loss and astrocyte hypertrophy in a model of traumatic brain injury.
        Brain Res. 2009; 1305: 183
        View in Article
        • Langlois J.A.
        • Rutland-Brown W.
        • Wald M.M.
        The epidemiology and impact of traumatic brain injury: a brief overview.
        J Head Trauma Rehabil. 2006; 21: 375
        View in Article
        • Davis A.E.
        Cognitive impairments following traumatic brain injury: etiologies and interventions.
        Crit Care Nurs Clin North Am. 2000; 12: 447
        View in Article
        • Narayan R.K.
        • Michel M.E.
        • Ansell B.
        • et al.
        Clinical trials in head injury.
        J Neurotrauma. 2002; 19: 503
        View in Article
        • McAllister T.W.
        Psychopharmacological issues in the treatment of TBI and PTSD.
        Clin Neuropsychol. 2009; 23: 1338
        View in Article
        • Marklund N.
        • Clausen F.
        • Lewander T.
        • et al.
        Monitoring of reactive oxygen species production after traumatic brain injury in rats with microdialysis and the 4-hydroxybenzoic acid trapping method.
        J Neurotrauma. 2001; 18: 1217
        View in Article
        • Marklund N.
        • Lewander T.
        • Clausen F.
        • et al.
        Effects of the nitrone radical scavengers PBN and S-PBN on in vivo trapping of reactive oxygen species after traumatic brain injury in rats.
        J Cereb Blood Flow Metab. 2001; 21: 1259
        View in Article
        • Homsi S.
        • Federico F.
        • Croci N.
        • et al.
        Minocycline effects on cerebral edema: relations with inflammatory and oxidative stress markers following traumatic brain injury in mice.
        Brain Res. 2009; 1291: 122
        View in Article
        • Kimura H.
        • Shibuya N.
        • Kimura Y.
        Hydrogen sulfide is a signaling molecule and a cytoprotectant.
        Antioxid Redox Signal. 2012; 17: 45
        View in Article
        • Yang G.
        Hydrogen sulfide in cell survival: a double-edged sword.
        Expert Rev Clin Pharmacol. 2011; 4: 33
        View in Article
        • Hu L.F.
        • Lu M.
        • Hon Wong P.T.
        • et al.
        Hydrogen sulfide: neurophysiology and neuropathology.
        Antioxid Redox Signal. 2011; 15: 405
        View in Article
        • Tan B.H.
        • Wong P.T.
        • Bian J.S.
        Hydrogen sulfide: a novel signaling molecule in the central nervous system.
        Neurochem Int. 2010; 56: 3
        View in Article
        • Chai W.
        • Wang Y.
        • Lin J.Y.
        • et al.
        Exogenous hydrogen sulfide protects against traumatic hemorrhagic shock via attenuation of oxidative stress.
        J Surg Res. 2012; 176: 210
        View in Article
        • Kimura Y.
        • Kimura H.
        Hydrogen sulfide protects neurons from oxidative stress.
        FASEB J. 2004; 18: 1165
        View in Article
        • Kimura Y.
        • Dargusch R.
        • Schubert D.
        • et al.
        Hydrogen sulfide protects HT22 neuronal cells from oxidative stress.
        Antioxid Redox Signal. 2006; 8: 661
        View in Article
        • Yonezawa D.
        • Sekiguchi F.
        • Miyamoto M.
        • et al.
        A protective role of hydrogen sulfide against oxidative stress in rat gastric mucosal epithelium.
        Toxicology. 2007; 241: 11
        View in Article
        • Ganster F.
        • Burban M.
        • de la Bourdonnaye M.
        • et al.
        Effects of hydrogen sulfide on hemodynamics, inflammatory response and oxidative stress during resuscitated hemorrhagic shock in rats.
        Crit Care. 2010; 14: R165
        View in Article
        • Benetti L.R.
        • Campos D.
        • Gurgueira S.A.
        • et al.
        Hydrogen sulfide inhibits oxidative stress in lungs from allergic mice in vivo.
        Eur J Pharmacol. 2013; 698: 463
        View in Article
        • Liu Y.Y.
        • Nagpure B.V.
        • Wong P.T.
        • et al.
        Hydrogen sulfide protects SH-SY5Y neuronal cells against D-galactose induced cell injury by suppression of advanced glycation end products formation and oxidative stress.
        Neurochem Int. 2013; 62: 603
        View in Article
        • Yin J.
        • Tu C.
        • Zhao J.
        • et al.
        Exogenous hydrogen sulfide protects against global cerebral ischemia/reperfusion injury via its anti-oxidative, anti-inflammatory and anti-apoptotic effects in rats.
        Brain Res. 2013; 1491: 188
        View in Article
        • Shen X.
        • Pattillo C.B.
        • Pardue S.
        • et al.
        Measurement of plasma hydrogen sulfide in vivo and in vitro.
        Free Radic Biol Med. 2011; 50: 1021
        View in Article
        • Xiong Y.
        • Mahmood A.
        • Lu D.
        • et al.
        Role of gender in outcome after traumatic brain injury and therapeutic effect of erythropoietin in mice.
        Brain Res. 2007; 1185: 301
        View in Article
        • Longhi L.
        • Saatman K.E.
        • Raghupathi R.
        • et al.
        A review and rationale for the use of genetically engineered animals in the study of traumatic brain injury.
        J Cereb Blood Flow Metab. 2001; 21: 1241
        View in Article
        • Hall E.D.
        • Bryant Y.D.
        • Cho W.
        • et al.
        Evolution of post-traumatic neurodegeneration after controlled cortical impact traumatic brain injury in mice and rats as assessed by the de Olmos silver and fluorojade staining methods.
        J Neurotrauma. 2008; 25: 235
        View in Article
        • Yu S.
        • Kaneko Y.
        • Bae E.
        • et al.
        Severity of controlled cortical impact traumatic brain injury in rats and mice dictates degree of behavioral deficits.
        Brain Res. 2009; 1287: 157
        View in Article
        • Ji X.
        • Tian Y.
        • Xie K.
        • et al.
        Protective effects of hydrogen-rich saline in a rat model of traumatic brain injury via reducing oxidative stress.
        J Surg Res. 2012; 178: e9
        View in Article
        • Barzo P.
        • Marmarou A.
        • Fatouros P.
        • et al.
        Magnetic resonance imaging-monitored acute blood-brain barrier changes in experimental traumatic brain injury.
        J Neurosurg. 1996; 85: 1113
        View in Article
        • Beaumont A.
        • Marmarou A.
        • Hayasaki K.
        • et al.
        The permissive nature of blood brain barrier (BBB) opening in edema formation following traumatic brain injury.
        Acta Neurochir Suppl. 2000; 76: 125
        View in Article
        • Dogan A.
        • Rao A.M.
        • Baskaya M.K.
        • et al.
        Effects of ifenprodil, a polyamine site NMDA receptor antagonist, on reperfusion injury after transient focal cerebral ischemia.
        J Neurosurg. 1997; 87: 921
        View in Article
        • Feeney D.M.
        • Westerberg V.S.
        Norepinephrine and brain damage: alpha noradrenergic pharmacology alters functional recovery after cortical trauma.
        Can J Psychol. 1990; 44: 233
        View in Article
        • Zhang Y.
        • Xiong Y.
        • Mahmood A.
        • et al.
        Therapeutic effects of erythropoietin on histological and functional outcomes following traumatic brain injury in rats are independent of hematocrit.
        Brain Res. 2009; 1294: 153
        View in Article
        • Liu D.D.
        • Kao S.J.
        • Chen H.I.
        N-acetylcysteine attenuates acute lung injury induced by fat embolism.
        Crit Care Med. 2008; 36: 565
        View in Article
        • Elrod J.W.
        • Calvert J.W.
        • Morrison J.
        • et al.
        Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function.
        Proc Natl Acad Sci U S A. 2007; 104: 15560
        View in Article
        • Francis R.C.
        • Vaporidi K.
        • Bloch K.D.
        • et al.
        Protective and detrimental effects of sodium sulfide and hydrogen sulfide in murine ventilator-induced lung injury.
        Anesthesiology. 2011; 115: 1012
        View in Article
        • Lenzlinger P.M.
        • Hans V.H.
        • Joller-Jemelka H.I.
        • et al.
        Markers for cell-mediated immune response are elevated in cerebrospinal fluid and serum after severe traumatic brain injury in humans.
        J Neurotrauma. 2001; 18: 479
        View in Article
        • Lewen A.
        • Matz P.
        • Chan P.H.
        Free radical pathways in CNS injury.
        J Neurotrauma. 2000; 17: 871
        View in Article
        • Tyurin V.A.
        • Tyurina Y.Y.
        • Borisenko G.G.
        • et al.
        Oxidative stress following traumatic brain injury in rats: quantitation of biomarkers and detection of free radical intermediates.
        J Neurochem. 2000; 75: 2178
        View in Article
        • Kumar A.
        • Panigrahi I.
        • Basu S.
        • et al.
        Urinary malondialdehyde levels in newborns following delivery room resuscitation.
        Neonatology. 2008; 94: 96
        View in Article
        • Sakamoto M.
        • Takaki E.
        • Yamashita K.
        • et al.
        Nonenzymatic derived lipid peroxide, 8-iso-PGF2 alpha, participates in the pathogenesis of delayed cerebral vasospasm in a canine SAH model.
        Neurol Res. 2002; 24: 301
        View in Article
        • Satpute R.M.
        • Kashyap R.S.
        • Deopujari J.Y.
        • et al.
        Protection of PC12 cells from chemical ischemia induced oxidative stress by Fagonia arabica.
        Food Chem Toxicol. 2009; 47: 2689
        View in Article
        • Busija D.W.
        • Lacza Z.
        • Rajapakse N.
        • et al.
        Targeting mitochondrial ATP-sensitive potassium channels—a novel approach to neuroprotection.
        Brain Res Brain Res Rev. 2004; 46: 282
        View in Article
        • Johansen D.
        • Ytrehus K.
        • Baxter G.F.
        Exogenous hydrogen sulfide (H2S) protects against regional myocardial ischemia-reperfusion injury—Evidence for a role of KATP channels.
        Basic Res Cardiol. 2006; 101: 53
        View in Article
        • Peers C.
        • Bauer C.C.
        • Boyle J.P.
        • et al.
        Modulation of ion channels by hydrogen sulfide.
        Antioxid Redox Signal. 2012; 17: 95
        View in Article
        • Tang G.
        • Wu L.
        • Liang W.
        • et al.
        Direct stimulation of K(ATP) channels by exogenous and endogenous hydrogen sulfide in vascular smooth muscle cells.
        Mol Pharmacol. 2005; 68: 1757
        View in Article
        • Zhang M.
        • Shan H.
        • Wang T.
        • et al.
        Dynamic change of hydrogen sulfide after traumatic brain injury and its effect in mice.
        Neurochem Res. 2013; 38: 714
        View in Article

      Article info

      Publication history

      Published online: April 10, 2013
      Accepted: March 20, 2013
      Received in revised form: March 19, 2013
      Received: January 6, 2013

      Identification

      DOI: https://doi.org/10.1016/j.jss.2013.03.067

      Copyright

      © 2013 Elsevier Inc. Published by Elsevier Inc. All rights reserved.

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