The neuroprotective properties of the superoxide dismutase mimetic tempol correlate with its ability to reduce pathological glutamate release in a rodent model of stroke

Free Radical Biology and Medicine

Volumn 77, Issue , 2014, Pages 168-182

  Dohare, Preeti ^a   Hyzinski García, María C ^a   Vipani, Aarshi ^a   Bowens, Nicole H ^a   Nalwalk, Julia W ^a   Feustel, Paul J ^a   Keller, Richard W ^a   Jourd'Heuil, David ^a   Mongin, Alexander A ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

Antioxidants; Freeradicals; Glutamate release; Neuroprotection; Oxidativestress; Stroke; Superoxideanion

Indexed keywords

1,1 DIPHENYL 2 PICRYLHYDRAZYL; ANTIOXIDANT; DIHYDRORHODAMINE 123; GLUTAMIC ACID; HYDROGEN PEROXIDE; HYDROXYL RADICAL; NEUROPROTECTIVE AGENT; NORPHENAZONE; PEROXYNITRITE; SODIUM GLUCOSE COTRANSPORTER 1; SUPEROXIDE; SUPEROXIDE DISMUTASE; TEMPOL; ALANINE; AMINE OXIDE; PHENAZONE; PHENYLMETHYLPYRAZOLONE; SCAVENGER; SPIN LABELING; TAURINE;

AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN DAMAGE; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN SYNAPTOSOME; CEREBROVASCULAR ACCIDENT; COGNITION; CONTROLLED STUDY; DRUG POTENCY; GLIA CELL; IN VITRO STUDY; LASER DOPPLER FLOWMETRY; LATERAL BRAIN VENTRICLE; LIPID OXIDATION; LIPID PEROXIDATION; MALE; MICRODIALYSIS; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROLOGIC DISEASE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; RAT; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN; CELL CULTURE; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; INFARCTION, MIDDLE CEREBRAL ARTERY; METABOLISM; MOLECULAR MIMICRY; PATHOLOGY; SPIN LABELING; SPRAGUE DAWLEY RAT; SYNAPTOSOME;

ALANINE; ANIMALS; ANTIPYRINE; ASTROCYTES; BRAIN; CELLS, CULTURED; CYCLIC N-OXIDES; DRUG EVALUATION, PRECLINICAL; FREE RADICAL SCAVENGERS; GLUTAMIC ACID; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MOLECULAR MIMICRY; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; RATS, SPRAGUE-DAWLEY; SPIN LABELS; SUPEROXIDES; SYNAPTOSOMES; TAURINE;

EID: 84908270970     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.08.029     Document Type: Article

References (92)

1. T. Brott, and J. Bogousslavsky Treatment of acute ischemic stroke N. Engl. J. Med. 343 2000 710 722
2. R. Lozano, M. Naghavi, K. Foreman, S. Lim, K. Shibuya, V. Aboyans, J. Abraham, T. Adair, R. Aggarwal, S.Y. Ahn, M. Alvarado, H.R. Anderson, L.M. Anderson, K.G. Andrews, C. Atkinson, L.M. Baddour, S. Barker-Collo, D.H. Bartels, M.L. Bell, and E.J. Benjamin Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010 Lancet 380 2012 2095 2128
3. A. Towfighi, and J.L. Saver Stroke declines from third to fourth leading cause of death in the United States: historical perspective and challenges ahead Stroke 42 2011 2351 2355
4. M.C. Fang, D.M. Cutler, and A.B. Rosen Trends in thrombolytic use for ischemic stroke in the United States J. Hosp. Med. 5 2010 406 409
5. M.D. Ginsberg Neuroprotection for ischemic stroke: past, present and future Neuropharmacology 55 2008 363 389
6. P. Lipton Ischemic cell death in brain neurons Physiol. Rev. 79 1999 1431 1568
7. A.A. Mongin Disruption of ionic and cell volume homeostasis in cerebral ischemia: the perfect storm Pathophysiology 14 2007 183 193
8. D.W. Choi Glutamate neurotoxicity and diseases of the nervous system Neuron 1 1988 623 634
9. S.M. Rothman, and J.W. Olney Excitotoxicity and the NMDA receptor Trends Neurosci. 10 1987 299 302
10. U. Dirnagl, C. Iadecola, and M.A. Moskowitz Pathobiology of ischaemic stroke: an integrated view Trends Neurosci. 22 1999 391 397
11. Y. Wang, V.L. Dawson, and T.M. Dawson Poly(ADP-ribose) signals to mitochondrial AIF: a key event in parthanatos Exp. Neurol. 218 2009 193 202
12. P.H. Chan Reactive oxygen radicals in signaling and damage in the ischemic brain J. Cereb. Blood Flow Metab. 21 2001 2 14
13. I. Margaill, M. Plotkine, and D. Lerouet Antioxidant strategies in the treatment of stroke Free Radic. Biol. Med. 39 2005 429 443
14. P. Pacher, J.S. Beckman, and L. Liaudet Nitric oxide and peroxynitrite in health and disease Physiol. Rev. 87 2007 315 424
15. A. Denicola, B.A. Freeman, M. Trujillo, and R. Radi Peroxynitrite reaction with carbon dioxide/bicarbonate: kinetics and influence on peroxynitrite-mediated oxidations Arch. Biochem. Biophys. 333 1996 49 58
16. D. Jourd'heuil, F.L. Jourd'heuil, P.S. Kutchukian, R.A. Musah, D.A. Wink, and M.B. Grisham Reaction of superoxide and nitric oxide with peroxynitrite: implications for peroxynitrite-mediated oxidation reactions in vivo J. Biol. Chem. 276 2001 28799 28805
17. A.F. Samdani, T.M. Dawson, and V.L. Dawson Nitric oxide synthase in models of focal ischemia Stroke 28 1997 1283 1288
18. X. Cao, and J. Phillis W. alpha-Phenyl-tert-butyl-nitrone reduces cortical infarct and edema in rats subjected to focal ischemia Brain Res. 644 1994 267 272
19. Z. Huang, P.L. Huang, N. Panahian, T. Dalkara, M.C. Fishman, and M.A. Moskowitz Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase Science 265 1994 1883 1885
20. G. Yang, P.H. Chan, J. Chen, E. Carlson, S.F. Chen, P. Weinstein, C.J. Epstein, and H. Kamii Human copper-zinc superoxide dismutase transgenic mice are highly resistant to reperfusion injury after focal cerebral ischemia Stroke 25 1994 165 170
21. K. Murakami, T. Kondo, M. Kawase, Y. Li, S. Sato, S.F. Chen, and P.H. Chan Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency J. Neurosci. 18 1998 205 213
22. S. Kuroda, R. Tsuchidate, M.L. Smith, K.R. Maples, and B.K. Siesjo Neuroprotective effects of a novel nitrone, NXY-059, after transient focal cerebral ischemia in the rat J. Cereb. Blood Flow Metab. 19 1999 778 787
23. G.B. Mackensen, M. Patel, H. Sheng, C.L. Calvi, I. Batinic-Haberle, B.J. Day, L.P. Liang, I. Fridovich, J.D. Crapo, R.D. Pearlstein, and D.S. Warner Neuroprotection from delayed postischemic administration of a metalloporphyrin catalytic antioxidant J. Neurosci. 21 2001 4582 4592
24. The Edaravone Study Group Effect of a novel free radical scavenger, edaravone (MCI-186), on acute brain infarction: randomized, placebo-controlled, double-blind study at multicenters Cerebrovasc. Dis. 15 2003 222 229
25. K. Toyoda, K. Fujii, M. Kamouchi, H. Nakane, S. Arihiro, Y. Okada, S. Ibayashi, and M. Iida Free radical scavenger, edaravone, in stroke with internal carotid artery occlusion J. Neurol. Sci. 221 2004 11 17
26. Y.D. Cheng, L. Al Khoury, and J.A. Zivin Neuroprotection for ischemic stroke: two decades of success and failure NeuroRx 1 2004 36 45
27. M.D. Ginsberg Life after Cerovive: a personal perspective on ischemic neuroprotection in the post-NXY-059 era Stroke 38 2007 1967 1972
28. H.C. Diener, K.R. Lees, P. Lyden, J. Grotta, A. Davalos, S.M. Davis, A. Shuaib, T. Ashwood, W. Wasiewski, V. Alderfer, H.G. Hardemark, and L. Rodichok NXY-059 for the treatment of acute stroke: pooled analysis of the SAINT I and II trials Stroke 39 2008 1751 1758
29. H. Pearson The bitterest pill Nature 444 2006 532 533
30. M.D. Hill Stroke: the dashed hopes of neuroprotection Lancet Neurol. 6 2007 2 3
31. S.I. Savitz A critical appraisal of the NXY-059 neuroprotection studies for acute stroke: a need for more rigorous testing of neuroprotective agents in animal models of stroke Exp. Neurol. 205 2007 20 25
32. R.E. Haskew, A.A. Mongin, and H.K. Kimelberg Peroxynitrite enhances astrocytic volume-sensitive excitatory amino acid release via a src tyrosine kinase-dependent mechanism J. Neurochem. 82 2002 903 912
33. 2+/calmodulin-dependent protein kinase II J. Biol. Chem. 280 2005 3548 3554
34. T.J. Harrigan, I.F. Abdullaev, D. Jourd'heuil, and A.A. Mongin Activation of microglia with zymosan promotes excitatory amino acid release via volume-regulated anion channels: the role of NADPH oxidases J. Neurochem. 106 2008 2449 2462
35. R.E. Haskew-Layton, A. Rudkouskaya, Y. Jin, P.J. Feustel, H.K. Kimelberg, and A.A. Mongin Two distinct modes of hypoosmotic medium-induced release of excitatory amino acids and taurine in the rat brain in vivo PLoS One 3 2008 e3543
36. E.Z. Longa, P.R. Weinstein, S. Carlson, and R. Cummins Reversible middle cerebral artery occlusion without craniectomy in rats Stroke 20 1989 84 91
37. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 2009 Elsevier/Academic Press San Diego
38. J.B. Bederson, L.H. Pitts, S.M. Germano, M.C. Nishimura, R.L. Davis, and H.M. Bartkowski Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats Stroke 17 1986 1304 1308
39. W.S. Rasband ImageJ 1997 U.S. National Institutes of Health Bethesda
40. R.A. Swanson, M.T. Morton, G. Tsao-Wu, R.A. Savalos, C. Davidson, and F.R. Sharp A semiautomated method for measuring brain infarct volume J. Cereb. Blood Flow Metab. 10 1990 290 293
41. J.H. Garcia, S. Wagner, K.F. Liu, and X.J. Hu Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats: statistical validation Stroke 26 1995 627 634
42. T. Schallert, M. Upchurch, N. Lobaugh, S.B. Farrar, W.W. Spirduso, P. Gilliam, D. Vaughn, and R.E. Wilcox Tactile extinction: distinguishing between sensorimotor and motor asymmetries in rats with unilateral nigrostriatal damage Pharmacol. Biochem. Behav. 16 1982 455 462
43. M. Balkaya, J.M. Krober, A. Rex, and M. Endres Assessing post-stroke behavior in mouse models of focal ischemia J. Cereb. Blood Flow Metab. 33 2013 330 338
44. Y. Ando, and M. Steiner Sulfhydryl and disulfide groups of platelet membranes. I. Determination of sulfhydryl groups Biochim. Biophys. Acta 311 1973 26 37
45. M.C. Hyzinski-Garcia, M.Y. Vincent, R.E. Haskew-Layton, P. Dohare, R.W. Keller Jr., and A.A. Mongin Hypoosmotic swelling modifies glutamate-glutamine cycle in the cerebral cortex and in astrocyte cultures J. Neurochem. 118 2011 140 152
46. N.H. Bowens, P. Dohare, Y.H. Kuo, and A.A. Mongin DCPIB, the proposed selective blocker of volume-regulated anion channels, inhibits several glutamate transport pathways in glial cells Mol. Pharmacol. 83 2013 22 32
47. G. Gegelashvili, N.C. Danbolt, and A. Schousboe Neuronal soluble factors differentially regulate the expression of the GLT1 and GLAST glutamate transporters in cultured astroglia J. Neurochem. 69 1997 2612 2615
48. K. Nakajima, Y. Tohyama, S. Kohsaka, and T. Kurihara Ability of rat microglia to uptake extracellular glutamate Neurosci. Lett. 307 2001 171 174
49. M.S. Blois Antioxidant determinations by the use of a stable free radical Nature 181 1958 1199 1200
50. J. Storch, and E. Ferber Detergent-amplified chemiluminescence of lucigenin for determination of superoxide anion production by NADPH oxidase and xanthine oxidase Anal. Biochem. 169 1988 262 267
51. F. Hajos An improved method for the preparation of synaptosomal fractions in high purity Brain Res. 93 1975 485 489
52. A. Rudkouskaya, V. Sim, A.A. Shah, P.J. Feustel, D. Jourd'heuil, and A.A. Mongin Long-lasting inhibition of presynaptic metabolism and neurotransmitter release by protein S-nitrosylation Free Radic. Biol. Med. 49 2010 757 769
53. H. Ohkawa, N. Ohishi, and K. Yagi Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction Anal. Biochem. 95 1979 351 358
54. J.P. Crow Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxynitrite in vitro: implications for intracellular measurement of reactive nitrogen and oxygen species Nitric Oxide 1 1997 145 157
55. B. Kalyanaraman, V. Darley-Usmar, K.J. Davies, P.A. Dennery, H.J. Forman, M.B. Grisham, G.E. Mann, K. Moore, L.J. Roberts, and H. Ischiropoulos Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations Free Radic. Biol. Med. 52 2012 1 6
56. U. Banderali, and G. Roy Anion channels for amino-acids in Mdck cells Am. J. Physiol. 263 1992 C1200 C1207
57. K. Kirk, and K. Strange Functional properties and physiological roles of organic solute channels Annu. Rev. Physiol. 60 1998 719 739
58. H.B. van der Worp, E.S. Sena, G.A. Donnan, D.W. Howells, and M.R. Macleod Hypothermia in animal models of acute ischaemic stroke: a systematic review and meta-analysis Brain 130 2007 3063 3074
59. H.K. Kimelberg, and A.A. Mongin Swelling-activated release of excitatory amino acids in the brain: relevance for pathophysiology Contrib. Nephrol. 123 1998 240 257
60. H.K. Kimelberg Astrocytic swelling in cerebral ischemia as a possible cause of injury and target for therapy Glia 50 2005 389 397
61. Y. Seki, P.J. Feustel, R.W. Keller Jr., B.I. Tranmer, and H.K. Kimelberg Inhibition of ischemia-induced glutamate release in rat striatum by dihydrokinate and an anion channel blocker Stroke 30 1999 433 440
62. H.K. Kimelberg, S.K. Goderie, S. Higman, S. Pang, and R.A. Waniewski Swelling-induced release of glutamate, aspartate, and taurine from astrocyte cultures J. Neurosci. 10 1990 1583 1591
63. Z.C. Ye, M.S. Wyeth, S. Baltan-Tekkok, and B.R. Ransom Functional hemichannels in astrocytes: a novel mechanism of glutamate release J. Neurosci. 23 2003 3588 3596
64. B. Fogal, J. Li, D. Lobner, L.D. McCullough, and S.J. Hewett System x(c)- activity and astrocytes are necessary for interleukin-1 beta-mediated hypoxic neuronal injury J. Neurosci. 27 2007 10094 10105
65. P.J. Feustel, Y. Jin, and H.K. Kimelberg Volume-regulated anion channels are the predominant contributors to release of excitatory amino acids in the ischemic cortical penumbra Stroke 35 2004 1164 1168
66. - currents in rat cultured astrocytes J. Physiol. 572 2006 677 689
67. S. Bannai, H. Sato, T. Ishii, and Y. Sugita Induction of cystine transport activity in human fibroblasts by oxygen J. Biol. Chem. 264 1989 18480 18484
68. S.A. Patel, B.A. Warren, J.F. Rhoderick, and R.J. Bridges Differentiation of substrate and non-substrate inhibitors of transport system xc(-): an obligate exchanger of l-glutamate and l-cystine Neuropharmacology 46 2004 273 284
69. •- or as SOD mimics? J. Biol. Chem. 271 1996 26026 26031
70. A.A. Mongin, and H.K. Kimelberg Astrocytic swelling in neuropathology H. Kettenmann, B.R. Ransom, Neuroglia 2005 Oxford Univ. Press Oxford/New York 550 562
71. B.R. Shivakumar, S.V. Kolluri, and V. Ravindranath Glutathione and protein thiol homeostasis in brain during reperfusion after cerebral ischemia J. Pharmacol. Exp. Ther. 274 1995 1167 1173
72. H. Benveniste, J. Drejer, A. Schousboe, and N.H. Diemer Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis J. Neurochem. 43 1984 1369 1374
73. H. Hagberg, A. Lehmann, M. Sandberg, B. Nystrom, I. Jacobson, and A. Hamberger Ischemia-induced shift of inhibitory and excitatory amino acids from intra- to extracellular compartments J. Cereb. Blood Flow Metab. 5 1985 413 419
74. J.W. Phillis, D. Song, and M.H. O'Regan Inhibition by anion channel blockers of ischemia-evoked release of excitotoxic and other amino acids from rat cerebral cortex Brain Res. 758 1997 9 16
75. J.W. Phillis, D. Song, and M.H. O'Regan Tamoxifen, a chloride channel blocker, reduces glutamate and aspartate release from the ischemic cerebral cortex Brain Res. 780 1998 352 355
76. Y. Zhang, H. Zhang, P.J. Feustel, and H.K. Kimelberg DCPIB, a specific inhibitor of volume regulated anion channels (VRACs), reduces infarct size in MCAo and the release of glutamate in the ischemic cortical penumbra Exp. Neurol. 210 2008 514 520
77. H.K. Kimelberg, P.J. Feustel, Y. Jin, J. Paquette, A. Boulos, R.W. Keller Jr., and B.I. Tranmer Acute treatment with tamoxifen reduces ischemic damage following middle cerebral artery occlusion Neuroreport 11 2000 2675 2679
78. H.K. Kimelberg, Y. Jin, C. Charniga, and P.J. Feustel Neuroprotective activity of tamoxifen in permanent focal ischemia J. Neurosurg. 99 2003 138 142
79. N.C. Danbolt Glutamate uptake Prog. Neurobiol. 65 2001 1 105
80. E.H. Lo, T. Dalkara, and M.A. Moskowitz Mechanisms, challenges and opportunities in stroke Nat. Rev. Neurosci. 4 2003 399 415
81. D. Trotti, D. Rossi, O. Gjesdal, L.M. Levy, G. Racagni, N.C. Danbolt, and A. Volterra Peroxynitrite inhibits glutamate transporter subtypes J. Biol. Chem. 271 1996 5976 5979
82. A. Ahmad, M.M. Khan, H. Javed, S.S. Raza, T. Ishrat, M.B. Khan, M.M. Safhi, and F. Islam Edaravone ameliorates oxidative stress associated cholinergic dysfunction and limits apoptotic response following focal cerebral ischemia in rat Mol. Cell. Biochem. 367 2012 215 225
83. R. Radi, J.S. Beckman, K.M. Bush, and B.A. Freeman Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide Arch. Biochem. Biophys. 288 1991 481 487
84. C.S. Wilcox, and A. Pearlman Chemistry and antihypertensive effects of tempol and other nitroxides Pharmacol. Rev. 60 2008 418 469
85. J. De Cristobal, M.A. Moro, A. Davalos, J. Castillo, J.C. Leza, J. Camarero, M.I. Colado, P. Lorenzo, and I. Lizasoain Neuroprotective effect of aspirin by inhibition of glutamate release after permanent focal cerebral ischaemia in rats J. Neurochem. 79 2001 456 459
86. C. Berger, A. Stauder, F. Xia, C. Sommer, and S. Schwab Neuroprotection and glutamate attenuation by acetylsalicylic acid in temporary but not in permanent cerebral ischemia Exp. Neurol. 210 2008 543 548
87. R. Rak, D.L. Chao, R.M. Pluta, J.B. Mitchell, E.H. Oldfield, and J.C. Watson Neuroprotection by the stable nitroxide Tempol during reperfusion in a rat model of transient focal ischemia J. Neurosurg. 92 2000 646 651
88. R.R. Leker, A. Teichner, G. Lavie, E. Shohami, I. Lamensdorf, and H. Ovadia The nitroxide antioxidant tempol is cerebroprotective against focal cerebral ischemia in spontaneously hypertensive rats Exp. Neurol. 176 2002 355 363
89. H. Sheng, J.J. Enghild, R. Bowler, M. Patel, I. Batinic-Haberle, C.L. Calvi, B.J. Day, R.D. Pearlstein, J.D. Crapo, and D.S. Warner Effects of metalloporphyrin catalytic antioxidants in experimental brain ischemia Free Radic. Biol. Med. 33 2002 947 961
90. H. Shichinohe, S. Kuroda, H. Yasuda, T. Ishikawa, M. Iwai, M. Horiuchi, and Y. Iwasaki Neuroprotective effects of the free radical scavenger Edaravone (MCI-186) in mice permanent focal brain ischemia Brain Res. 1029 2004 200 206
91. N. Zhang, M. Komine-Kobayashi, R. Tanaka, M. Liu, Y. Mizuno, and T. Urabe Edaravone reduces early accumulation of oxidative products and sequential inflammatory responses after transient focal ischemia in mice brain Stroke 36 2005 2220 2225
92. B. Xiao, F.F. Bi, Y.Q. Hu, F.F. Tian, Z.G. Wu, H.M. Mujlli, L. Ding, and X.F. Zhou Edaravone neuroprotection effected by suppressing the gene expression of the Fas signal pathway following transient focal ischemia in rats Neurotox. Res. 12 2007 155 162