Glutathione monoethyl ester improves functional recovery, enhances neuron survival, and stabilizes spinal cord blood flow after spinal cord injury in rats

Neuroscience

Volumn 130, Issue 3, 2005, Pages 639-649

  Guizar Sahagun G ^a   Ibarra, A ^a   Espitia, A ^a   Martinez A ^a   Madrazo, I ^a   Franco Bourland, R E ^a,b  

^a INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

^b Department of Biochemistry   (Mexico)

Author keywords

antioxidant; ischemia; microcirculation; neuroprotective; oxidative stress; secondary damage

Indexed keywords

GLUTATHIONE ETHYL ESTER; METHYLPREDNISOLONE SODIUM SUCCINATE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD FLOW; CELL COUNT; CELL MEMBRANE PERMEABILITY; CELL SURVIVAL; CONTROLLED STUDY; EVALUATION; EXPERIMENTAL ANIMAL; ISOTOPE LABELING; LASER DOPPLER FLOWMETRY; MICROVASCULARIZATION; MOTOR PERFORMANCE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; RED NUCLEUS; SPINAL CORD INJURY;

ANIMALS; BODY WEIGHT; CELL SURVIVAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE; MICROCIRCULATION; MOVEMENT; NEURONS; RATS; RED NUCLEUS; REGIONAL BLOOD FLOW; SPINAL CORD; SPINAL CORD INJURIES;

EID: 10044242356     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.09.056     Document Type: Article

References (92)

1. M. Aksenova, D.A. Butterfield, S.X. Zhang, M. Underwood, J.W. Geddes Increased protein oxidation and decreased creatine kinase BB expression and activity after spinal cord contusion injury J Neurotrauma 19 2002 491 502
2. D.K. Anderson, E.D. Hall Pathophysiology of spinal cord trauma Ann Emerg Med 22 1993 987 992
3. M.E. Anderson, F. Powrie, R.N. Puri, A. Meister Glutathione monoethyl ester: preparation, uptake by tissues, and conversion to glutathione Arch Biochem Biophys 239 1985 538 548
4. M.E. Anderson, M. Underwood, R.J. Bridges, A. Meister Glutathione metabolism at the blood-cerebrospinal fluid barrier FASEB J 3 1989 2527 2531
5. M.E. Anderson Glutathione: an overview of biosynthesis and modulation Chem Biol Interact 111-112 1998 1 14
6. M.F. Anderson, M. Nilsson, P.S. Eriksson, N.R. Sims Glutathione monoethyl ester provides neuroprotection in a rat model of stroke Neurosci Lett 354 2004 163 165
7. M.F. Anderson, M. Nilsson, N.R. Sims Glutathione monoethylester prevents mitochondrial glutathione depletion during focal cerebral ischemia Neurochem Int 44 2004 153 159
8. D.L. Anthes, E. Theriault, C.H. Tator Ultrastructural evidence for arteriolar vasospasm after spinal cord trauma Neurosurgery 39 1996 804 814
9. M. Antri, D. Orsal, J.Y. Barthe Locomotor recovery in the chronic spinal rat: effects of long-term treatment with a 5-HT2 agonist Eur J Neurosci 16 2002 467 476
10. E. Arosio, S. De Marchi, M. Zannoni, M. Prior, A. Lechi Effect of glutathione infusion on leg arterial circulation, cutaneous microcirculation, and pain-free walking distance in patients with peripheral obstructive arterial disease: a randomized, double-blind, placebo-controlled trial Mayo Clin Proc 77 2002 754 759
11. R.D. Azbill, X. Mu, A.J. Bruce-Keller, M.P. Mattson, J.E. Springer Impaired mitochondrial function, oxidative stress and altered antioxidant enzyme activities following traumatic spinal cord injury Brain Res 765 1997 283 290
12. D.M. Basso, M.S. Beattie, J.C. Bresnahan Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection Exp Neurol 139 1996 244 256
13. D.L. Behrmann, J.C. Bresnahan, M.S. Beattie Modeling of acute spinal cord injury in the rat: neuroprotection and enhanced recovery with methylprednisolone, U-74006F and YM-14673 Exp Neurol 126 1994 61 75
14. M.B. Bracken Methylprednisolone and acute spinal cord injury: an update of the randomized evidence Spine 26 2001 S47 S54
15. J.M. Braughler, E.D. Hall, E.D. Means, T.R. Waters, D.K. Anderson Evaluation of an intensive methylprednisolone sodium succinate dosing regimen in experimental spinal cord injury J Neurosurg 67 1987 102 105
16. G.D. Carlson, Y. Minato, A. Okada, C.D. Gorden, K.E. Warden, J.M. Barbeau, C.L. Biro, E. Bahnuik, H.H. Bohlman, J.C. Lamanna Early time-dependent decompression for spinal cord injury: vascular mechanisms of recovery J Neurotrauma 14 1997 951 962
17. P.Y. Cheung, R. Schulz Glutathione causes coronary vasodilation via a nitric oxide- and soluble guanylate cyclase-dependent mechanism Am J Physiol 273 1997 H1231 H1238
18. F. Dabbeni-Sala, M. Floreani, D. Franceschini, S.D. Skaper, P. Giusti Kainic acid induces selective mitochondrial oxidative phosphorylation enzyme dysfunction in cerebellar granule neurons: protective effects of melatonin and GSH ethyl ester FASEB J 15 2001 1786 1788
19. R.J. Dumont, D.O. Okonkwo, S. Verma, R.J. Hurlbert, P.T. Boulos, D.B. Ellegala, A.S. Dumont Acute spinal cord injury, part I: pathophysiologic mechanisms Clin Neuropharmacol 24 2001 254 264
20. M.G. Fehlings, C.H. Tator The relationships among the severity of spinal cord injury, residual neurological function, axon counts, and counts of retrogradely labeled neurons after experimental spinal cord injury Exp Neurol 132 1995 220 228
21. K. Fouad, V. Pedersen, M.E. Schwab, C. Brosamle Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses Curr Biol 11 2001 1766 1770
22. M. Gaviria, A. Privat, P. d'Arbigny, J. Kamenka, H. Haton, F. Ohanna Neuroprotective effects of a novel NMDA antagonist, gacyclidine, after experimental contusive spinal cord injury in adult rats Brain Res 874 2000 200 209
23. y Gimenez, M. Ribotta, M. Gaviria, V. Menet, A. Privat Strategies for regeneration and repair in spinal cord traumatic injury Prog Brain Res 137 2002 191 212
24. B. Goldstein, J.W. Little, R.M. Harris Axonal sprouting following incomplete spinal cord injury: an experimental model J Spinal Cord Med 20 1997 200 206
25. R.J. Gryglewski, R.M. Palmer, S. Moncada Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor Nature 320 1986 454 456
26. A. Guha, C.H. Tator, C.R. Smith, I. Piper Improvement in post-traumatic spinal cord blood flow with a combination of a calcium channel blocker and a vasopressor J Trauma 29 1989 1440 1447
27. A.G. Hall Review: the role of glutathione in the regulation of apoptosis Eur J Clin Invest 29 1999 238 245
28. E.D. Hall, D.L. Wolf, J.M. Braughler Effects of a single large dose of methylprednisolone sodium succinate on experimental posttraumatic spinal cord ischemia: dose-response and time-action analysis J Neurosurg 61 1984 124 130
29. P.W. Hitchon, L.J. Mouw, T.N. Rogge, J.C. Torner, A.K. Miller Response of spinal cord blood flow to the nitric oxide inhibitor nitroarginine Neurosurgery 39 1996 795 803
30. A. Holtz, B. Nystrom, B. Gerdin Effect of methylprednisolone on motor function and spinal cord blood flow after spinal cord compression in rats Acta Neurol Scand 82 1990 68 73
31. J.C. Houk, J. Keifer, A.G. Barto Distributed motor commands in the limb premotor network Trends Neurosci 16 1993 27 33
32. C.E. Hulsebosch Recent advances in pathophysiology and treatment of spinal cord injury Adv Physiol Educ 26 2002 238 255
33. R.J. Hurlbert The role of steroids in acute spinal cord injury: an evidence-based analysis Spine 26 2001 S39 S46
34. B.L. Jacobs, C.A. Fornal Serotonin and motor activity Curr Opin Neurobiol 7 1997 820 825
35. L.B. Jakeman, P. Wei, Z. Guan, B.T. Stokes Brain-derived neurotrophic factor stimulates hindlimb stepping and sprouting of cholinergic fibers after spinal cord injury Exp Neurol 154 1998 170 184
36. M. Joshi, M.G. Fehlings Development and characterization of a novel, graded model of clip compressive spinal cord injury in the mouse: part 2 Quantitative neuroanatomical assessment and analysis of the relationships between axonal tracts, residual tissue, and locomotor recovery J Neurotrauma 19 2002 191 203
37. H. Kamencic, R.W. Griebel, A.W. Lyon, P.G. Paterson, B.H. Juurlink Promoting glutathione synthesis after spinal cord trauma decreases secondary damage and promotes retention of function FASEB J 15 2001 243 250
38. M.Y. Kaynar, M. Hanci, A. Kafadar, K. Gumustas, A. Belce, N. Ciplak The effect of duration of compression on lipid peroxidation after experimental spinal cord injury Neurosurg Rev 21 1998 117 120
39. P. Klatt, S. Lamas Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress Eur J Biochem 267 2000 4928 4944
40. J.D. Kristensen, R. Karlsten, T. Gordh Spinal cord blood flow after intrathecal injection of ropivacaine and bupivacaine with or without epinephrine in rats Acta Anaesthesiol Scand 42 1998 685 690
41. P.L. Kuhn, J.R. Wrathall A mouse model of graded contusive spinal cord injury J Neurotrauma 15 1998 125 140
42. A.J. Lankhorst, M.P. ter Laak, F.P. Hamers, W.H. Gispen Combined treatment with alphaMSH and methylprednisolone fails to improve functional recovery after spinal injury in the rat Brain Res 859 2000 334 340
43. A.J. Lankhorst, M.P. ter Laak, T.J. van Laar, N.L. van Meeteren, J.C. de Groot, L.H. Schrama, F.P. Hamers, W.H. Gispen Effects of enriched housing on functional recovery after spinal cord contusive injury in the adult rat J Neurotrauma 8 2001 203 215
44. M. Larsson, W. Steenbergen, T. Stromberg Influence of optical properties and fiber separation on laser Doppler flowmetry J Biomed Opt 7 2002 236 243
45. M.L. Leski, F. Bao, L. Wu, H. Qian, D. Sun, D. Liu Protein and DNA oxidation in spinal injury: neurofilaments: an oxidation target Free Radic Biol Med 30 2001 613 624
46. D. Liu, X. Ling, J. Wen, J. Liu The role of reactive nitrogen species in secondary spinal cord injury: formation of nitric oxide, peroxynitrite, and nitrated protein J Neurochem 75 2000 2144 2154
47. D. Liu, J. Liu, D. Sun, N.W. Alcock, J. Wen Spinal cord injury increases iron levels: catalytic production of hydroxyl radicals Free Radic Biol Med 34 2003 64 71
48. D. Liu, J. Liu, J. Wen Elevation of hydrogen peroxide after spinal cord injury detected by using the Fenton reaction Free Radic Biol Med 27 1999 478 482
49. D. Liu, T.E. Sybert, H. Qian, J. Liu Superoxide production after spinal injury detected by microperfusion of cytochrome c Free Radic Biol Med 25 1998 298 304
50. B.L. Lopez, J.W. Snyder, D.S. Birenbaum, X.I. Ma N-acetylcysteine enhances endothelium-dependent vasorelaxation in the isolated rat mesenteric artery Ann Emerg Med 32 1998 405 410
51. J. Loscalzo The oxidant stress of hyperhomocyst(e)inemia J Clin Invest 98 1996 5 7
52. J.H. Lucas, D.G. Wheeler, D.G. Emery, S.R. Mallery The endogenous antioxidant glutathione as a factor in the survival of physically injured mammalian spinal cord neurons J Neuropathol Exp Neurol 57 1998 937 954
53. J.H. Lucas, D.G. Wheeler, Z. Guan, Z. Suntres, B.T. Stokes Effect of glutathione augmentation on lipid peroxidation after spinal cord injury J Neurotrauma 19 2002 763 775
54. A.E. Mautes, M.R. Weinzierl, F. Donovan, L.J. Noble Vascular events after spinal cord injury: contribution to secondary pathogenesis Phys Ther 80 2000 673 687
55. A.L. McKenzie, J.J. Hall, N. Aihara, K. Fukuda, L.J. Noble Immunolocalization of endothelin in the traumatized spinal cord: relationship to blood-spinal cord barrier breakdown J Neurotrauma 12 1995 257 268
56. C.D. Mills, K.M. Johnson, C.E. Hulsebosch Role of group II and group III metabotropic glutamate receptors in spinal cord injury Exp Neurol 173 2002 153 167
57. C.D. Mills, K.M. Johnson, C.E. Hulsebosch Group I metabotropic glutamate receptors in spinal cord injury: roles in neuroprotection and the development of chronic central pain J Neurotrauma 19 2002 23 42
58. A.N. Obeid, N.J. Barnett, G. Dougherty, G. Ward A critical review of laser Doppler flowmetry J Med Eng Technol 14 1990 178 181
59. E. Park, A.A. Velumian, M.G. Fehlings The role of excitotoxicity in secondary mechanisms of spinal cord injury: a review with an emphasis on the implications for white matter degeneration J Neurotrauma 21 2004 754 774
60. V. Pointillart, M.E. Petitjean, L. Wiart, J.M. Vital, P. Lassie, M. Thicoipe, P. Dabadie Pharmacological therapy of spinal cord injury during the acute phase Spinal Cord 38 2000 71 76
61. P.G. Popovich, Z. Guan, P. Wei, I. Huitinga, N. van Rooijen, B.T. Stokes Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury Exp Neurol 158 1999 351 365
62. A. Prasad, N.P. Andrews, F.A. Padder, M. Husain, A.A. Quyyumi Glutathione reverses endothelial dysfunction and improves nitric oxide bioavailability J Am Coll Cardiol 34 1999 507 514
63. A.G. Rabchevsky, I. Fugaccia, A.F. Turner, D.A. Blades, M.P. Mattson, S.W. Scheff Basic fibroblast growth factor (bFGF) enhances functional recovery following severe spinal cord injury to the rat Exp Neurol 164 2000 280 291
64. A.G. Rabchevsky, I. Fugaccia, P.G. Sullivan, D.A. Blades, S.W. Scheff Efficacy of methylprednisolone therapy for the injured rat spinal cord J Neurosci Res 68 2002 7 18
65. M.G. Ribotta, J. Provencher, D. Feraboli-Lohnherr, S. Rossignol, A. Privat, D. Orsal Activation of locomotion in adult chronic spinal rats is achieved by transplantation of embryonic raphe cells reinnervating a precise lumbar level J Neurosci 20 2000 5144 5152
66. M. Rizzardini, M. Lupi, S. Bernasconi, A. Mangolini, L. Cantoni Mitochondrial dysfunction and death in motor neurons exposed to the glutathione-depleting agent ethacrynic acid J Neurol Sci 207 2003 51 58
67. M.K. Robinson, M.S. Ahn, J.D. Rounds, J.A. Cook, D.O. Jacobs, D.W. Wilmore Parenteral glutathione monoester enhances tissue antioxidant stores JPEN J Parenter Enteral Nutr 16 1992 413 418
68. L.J. Rosenberg, Y.D. Teng, J.R. Wrathall Effects of the sodium channel blocker tetrodotoxin on acute white matter pathology after experimental contusive spinal cord injury J Neurosci 19 1999 6122 6133
69. S. Rossignol, C. Chau, E. Brustein, N. Giroux, L. Bouyer, H. Barbeau, T.A. Reader Pharmacological activation and modulation of the central pattern generator for locomotion in the cat Ann NY Acad Sci 860 1998 346 359
70. S.K. Salzman, R. Acosta, G. Beck, J. Madden, B. Boxer, E.H. Ohlstein Spinal endothelin content is elevated after moderate local trauma in the rat to levels associated with locomotor dysfunction after intrathecal injection J Neurotrauma 13 1996 93 101
71. C. Santoscoy, C. Rios, R.E. Franco-Bourland, E. Hong, G. Bravo, G. Rojas, G. Guizar-Sahagun Lipid peroxidation by nitric oxide supplements after spinal cord injury: effect of antioxidants in rats Neurosci Lett 330 2002 94 98
72. M. Sato, L.J. Noble Involvement of the endothelin receptor subtype A in neuronal pathogenesis after traumatic brain injury Brain Res 809 1998 39 49
73. S.W. Scheff, D.A. Saucier, M.E. Cain A statistical method for analyzing rating scale data: the BBB locomotor score J Neurotrauma 19 2002 1251 1260
74. S.W. Scheff, A.G. Rabchevsky, I. Fugaccia, J.A. Main, J.E. Lumpp Jr Experimental modeling of spinal cord injury: characterization of a force-defined injury device J Neurotrauma 20 2003 179 193
75. L.H. Sekhon, M.G. Fehlings Epidemiology, demographics, and pathophysiology of acute spinal cord injury Spine 26 2001 S2 S12
76. T. Takami, M. Oudega, J.R. Bethea, P.M. Wood, N. Kleitman, M.B. Bunge Methylprednisolone and interleukin-10 reduce gray matter damage in the contused Fischer rat thoracic spinal cord but do not improve functional outcome J Neurotrauma 19 2002 653 666
77. D. Taskiran, T. Tanyalcin, E.Y. Sozmen, G.O. Peker, V. Gulmen, S. Cagli, L. Kanit, G. Tekeli, E. Barcin, M. Zileli, F.Z. Kutay The effects of melatonin on the antioxidant systems in experimental spinal injury Int J Neurosci 104 2000 63 73
78. C.H. Tator Update on the pathophysiology and pathology of acute spinal cord injury Brain Pathol 5 1995 407 413
79. C.H. Tator, M.G. Fehlings Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms J Neurosurg 75 1991 15 26
80. M. Uesugi, Y. Kasuya, H. Hama, M. Yamamoto, K. Hayashi, T. Masaki, K. Goto Endogenous endothelin-1 initiates astrocytic growth after spinal cord injury Brain Res 728 1996 255 259
81. M. Utsugi, K. Dobashi, Y. Koga, Y. Shimizu, T. Ishizuka, K. Iizuka, J. Hamuro, T. Nakazawa, M. Mori Glutathione redox regulates lipopolysaccharide- induced IL-12 production through p38 mitogen-activated protein kinase activation in human monocytes: role of glutathione redox in IFN-gamma priming of IL-12 production J Leukoc Biol 71 2002 339 347
82. N.L. Van Meeteren, R. Eggers, A.J. Lankhorst, W.H. Gispen, F.P. Hamers Locomotor recovery after spinal cord contusion injury in rats is improved by spontaneous exercise J Neurotrauma 20 2003 1029 1037
83. V. Varga, Z. Jenei, R. Janaky, P. Saransaari, S.S. Oja Glutathione is an endogenous ligand of rat brain N-methyl-d-aspartate (NMDA) and 2-amino-3-hydroxy-5-methyl-4-isoxazolepropionate (AMPA) receptors Neurochem Res 22 1997 1165 1171
84. P. Villa, A. Saccani, A. Sica, P. Ghezzi Glutathione protects mice from lethal sepsis by limiting inflammation and potentiating host defense J Infect Dis 185 2002 1115 1120
85. N. Weidner, A. Ner, N. Salimi, M.H. Tuszynski Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury Proc Natl Acad Sci USA 98 2001 3513 3518
86. N. Weiss, Y.Y. Zhang, S. Heydrick, C. Bierl, J. Loscalzo Overexpression of cellular glutathione peroxidase rescues homocyst(e)ine-induced endothelial dysfunction Proc Natl Acad Sci USA 98 2001 12503 12508
87. J.E. Wells, R.J. Hurlbert, M.G. Fehlings, V.W. Yong Neuroprotection by minocycline facilitates significant recovery from spinal cord injury in mice Brain 126 2003 1628 1637
88. J. Wernerman, F. Hammarqvist Modulation of endogenous glutathione availability Curr Opin Clin Nutr Metab Care 2 1999 487 492
89. H. Westergren, M. Farooque, Y. Olsson, A. Holtz Spinal cord blood flow changes following systemic hypothermia and spinal cord compression injury: an experimental study in the rat using Laser-Doppler flowmetry Spinal Cord 39 2001 74 84
90. R. Westmark, L.J. Noble, K. Fukuda, N. Aihara, A.L. McKenzie Intrathecal administration of endothelin-1 in the rat: impact on spinal cord blood flow and the blood-spinal cord barrier Neurosci Lett 192 1995 173 176
91. W.F. Young, R.H. Rosenwasser, U.S. Vasthare, R.F. Tuma Preservation of post-compression spinal cord function by infusion of hypertonic saline J Neurosurg Anesthesiol 6 1994 122 127
92. W. Young, E.S. Flamm Effect of high-dose corticosteroid therapy on blood flow, evoked potentials, and extracellular calcium in experimental spinal injury J Neurosurg 57 1982 667 673