Developmental up-regulation of MnSOD in rat oligodendrocytes confers protection against oxidative injury

European Journal of Neuroscience

Volumn 20, Issue 1, 2004, Pages 29-40

  Baud, Olivier ^a   Haynes, Robin F ^a   Wang, Hong ^a   Folkerth, Rebecca D ^a   Li, Jianrong ^a   Volpe, Joseph J ^a   Rosenberg, Paul A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cerebral palsy; Glutathione; Manganese SOD; Oligodendrocyte; Oxidative stress

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; CYSTINE; GLUTATHIONE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; SUPEROXIDE;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BRAIN MITOCHONDRION; CELL LINEAGE; CELL MATURATION; CELL PROTECTION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NERVE CELL LESION; NEUROPROTECTION; NEWBORN; NONHUMAN; OLIGODENDROGLIA; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION;

ADENOSINE TRIPHOSPHATE; ALDEHYDES; ANIMALS; ANIMALS, NEWBORN; ANTIOXIDANTS; BENZIMIDAZOLES; BLOTTING, WESTERN; CARBOCYANINES; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; CATALASE; CELL COUNT; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; CYSTEINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; FREE RADICALS; GREEN FLUORESCENT PROTEINS; HUMANS; HYDROGEN PEROXIDE; IMMUNOHISTOCHEMISTRY; INFECTION; INTRACELLULAR SPACE; IONOPHORES; LUMINESCENT PROTEINS; MITOCHONDRIA; MYELIN BASIC PROTEINS; O ANTIGENS; OLIGODENDROGLIA; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDE DISMUTASE; TIME FACTORS; UP-REGULATION;

EID: 3142749668     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0953-816X.2004.03451.x     Document Type: Article

References (66)

1. Almeida, A., Delgado-Esteban, M., Bolanos, J.P. & Medina, J.M. (2002) Oxygen and glucose deprivation induces mitochondrial dysfunction and oxidative stress in neurones but not in astrocytes in primary culture. J. Neurochem., 81, 207-217.
2. Back, S.A., Gan, X., Li, Y., Rosenberg, P.A. & Volpe, J.J. (1998) Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J. Neurosci., 18, 6241-6253.
3. Back, S.A., Han, B.H., Luo, N.L., Chricton, C.A., Xanthoudakis, S., Tam, J., Arvin, K.L. & Holtzman, D.M. (2002) Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J. Neurosci., 22, 455-463.
4. Back, S.A., Khan, R., Gan, X., Rosenberg, P.A. & Volpe, J.J. (1999) A new Alamar Blue viability assay to rapidly quantify oligodendrocyte death. J. Neurosci. Meth., 91, 47-54.
5. Bernardo, A., Greco, A., Levi, G. & Minghetti, L. (2003) Differential lipid peroxidation, Mn superoxide, and bcl-2 expression contribute to the maturation-dependent vulnerability of oligodendrocytes to oxidative stress. J. Neuropathol. Exp. Neurol., 62, 509-519.
6. Bianca, R.V., Wayman, N.S., McDonald, M.C., Pinto, A., Shape, M.A., Chatterjee, P.K. & Thiemermann, C. (2002) Superoxide dismutase mimetic with catalase activity, EUK-134, attenuates the multiple organ injury and dysfunction caused by endotoxin in the rat. Medical Sci. Monit., 8, BR1-7.
7. Bindokas, V.P., Jordan, J., Lee, C.C. & Miller, R.J. (1996) Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J. Neurosci., 16, 1324-1336.
8. Boveris, A. & Chance, B. (1973) The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem. J., 134, 707-716.
9. Bruce-Keller, A.J., Geddes, J.W., Knapp, P.E., McFall, R.W., Keller, J.N., Holtsberg, F.W., Parthasarathy, S., Steiner, S.M. & Mattson, M.P. (1999) Anti-death properties of TNF against metabolic poisoning: mitochondrial stabilization by MnSOD. J. Neuroimmunol., 93, 53-71.
10. Busciglio, J. & Yankner, B.A. (1995) Apoptosis and increased generation of reactive oxygen species in Down's syndrome neurons in vitro. Nature, 378, 776-779.
11. Carter, W.O., Narayanan, P.K. & Robinson, J.P. (1994) Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells. J. Leukoc. Biol., 55, 253-258.
12. Castilho, R.F., Ward, M.W. & Nicholls, D.G. (1999) Oxidative stress, mitochondrial function, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurochem., 72, 1394-1401.
13. Chance, B., Sies, H. & Boveris, A. (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev., 59, 527-605.
14. Christianson, D.W. (1997) Structural chemistry and biology of manganese metalloenzymes. Prog. Biophys. Molec. Biol., 67, 217-252.
15. Coyle, J.T. & Puttfarcken, P. (1993) Oxidative stress, glutamate, and neurodegenerative disorders. Science, 262, 689-695.
16. De Leo, M.E., Borrello, S., Passantino, M., Palazzotti, B., Mordente, A., Daniele, A., Filippini, V., Galeotti, T. & Masullo, C. (1998) Oxidative stress and overexpression of manganese superoxide dismutase in patients with Alzheimer's disease. Neurosci. Lett., 250, 173-176.
17. Ditelberg, J.S., Sheldon, R.A., Epstein, C.J. & Ferriero, D.M. (1996) Brain injury after perinatal hypoxia-ischemia is exacerbated in copper/zinc superoxide dismutase transgenic mice. Pediatr. Res., 39, 204-208.
18. Dugan, L.L., Sensi, S.L., Canzoniero, L.M., Handran, S.D., Rothman, S.M., Lin, T.S., Goldberg, M.P. & Choi, D.W. (1995) Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J. Neurosci., 15, 6377-6388.
19. Epperly, M.W., Sikora, C.A., DeFilippi, S.J., Gretton, J.A., Zhan, Q., Kufe, D.W. & Greenberger, J.S. (2002) Manganese superoxide dismutase (SOD2) inhibits radiation-induced apoptosis by stabilization of the mitochondrial membrane. Radiat. Res., 157, 568-577.
20. Fagni, L., Lafon-Cazal, M., Rondouin, G., Manzoni, O., Lerner-Natoli, M. & Bockaert, J. (1994) The role of free radicals in NMDA-dependent neurotoxicity. Prog. Brain Res., 103, 381-390.
21. Floreani, M., Skaper, S.D., Facci, L., Lipartiti, M. & Giusti, P. (1997) Melatonin maintains glutathione homeostasis in kainic acid-exposed rat brain tissues. FASEB J., 11, 1309-1315.
22. Follett, P.L., Rosenberg, P.A., Volpe, J.J. & Jensen, F.E. (2000) NBQX attenuates excitotoxic injury in developing white matter. J. Neurosci., 20, 9235-9241.
23. Fridovich, I. (1995) Superoxide radical and superoxide dismutases. Annu. Rev. Biochem., 64, 97-112.
24. Fullerton, H.J., Ditelberg, J.S., Chen, S.F., Sarco, D.P., Chan, P.H., Epstein, C.J. & Ferriero, D.M. (1998) Copper/zinc superoxide dismutase transgenic brain accumulates hydrogen peroxide after perinatal hypoxia ischemia. Ann. Neurol., 44, 357-364.
25. Gonzalez-Zulueta, M., Ensz, L.M., Mukhina, G., Lebovitz, R.M., Zwacka, R.M., Engelhardt, J.F., Oberley, L.W., Dawson, V.L. & Dawson, T.M. (1998) Manganese superoxide dismutase protects nNOS neurons from NMDA and nitric oxide-mediated neurotoxicity. J. Neurosci., 18, 2040-2055.
26. Halliwell, B. & Gutteridge, J.M.C. (1999) Free Radicals in Biology and Medicine, 3rd edn. Oxford University Press, Oxford, UK, 140-146.
27. Haynes, R.L., Folkerth, R.D., Keefe, R.J., Sung, I., Swzeda, L.I., Rosenberg, P.A., Volpe, J.J. & Kinney, H.C. (2003) Nitrosative and oxidative injury to premyelinating OLs in periventricular leukomalacia. J. Neuropathol. Exp. Neurol., 62, 441-450.
28. Huang, J. & Philbert, M.A. (1995) Distribution of glutathione and glutathione-related enzyme systems in mitochondria and cytosol of cultured cerebellar astrocytes and granule cells. Brain Res., 680, 16-22.
29. Juurlink, B.H. & Sweeney, M.I. (1997) Mechanisms that result in damage during and following cerebral ischemia. Neurosci. Biobehav. Rev., 21, 121-128.
30. Khand, F.D., Gordge, M.P., Robertson, W.G., Noronha-Dutra, A.A. & Hothersall, J.S. (2002) Mitochondrial superoxide production during oxalate-mediated oxidative stress in renal epithelial cells. Free Radic. Biol. Med., 32, 1339-1350.
31. Kulkarni-Narla, A., Getchell, T.V. & Getchell, M.L. (1997) Differential expression of manganese and copper-zinc dismutases in the olfactory and vomeronasal receptor neurons of rats during ontogeny. J. Comp. Neurol., 381, 31-40.
32. Li, Y., Maher, P. & Schubert, D. (1997) A role for 12-lipoxygenase in nerve cell death caused by glutathion depletion. Neuron, 19, 453-463.
33. Li, Y., Copin, J.C., Reola, R.F., Calagui, B., Gobbel, G.T., Chen, S.F., Sato, S., Epstein, C.J. & Chan, P.H. (1998) Reduced mitochondrial manganese-superoxide dismutase activity exacerbates glutamate toxicity in cultured mouse cortical neurons. Brain Res., 814, 164-170.
34. Li, J., Lin, J.C., Wang, H., Peterson, J.W., Furie, B.C., Furie, B., Booth, S.L., Volpe, J.J. & Rosenberg, P.A. (2003) Novel role of vitamin K in preventing oxidative injury to developing OLs and neurons. J. Neurosci., 23, 5816-5826.
35. Li, Q., Sanlioglu, S., Li, S., Ritchie, T., Oberley, L. & Engelhardt, J.F. (2001) GPx-1 gene delivery modulates NFkappaB activation following diverse environmental injuries through a specific subunit of the IKK complex. Antioxid. Redox Signal, 3, 415-432.
36. Liang, L.P., Ho, Y.S. & Patel, M. (2000) Mitochondrial superoxide production in kainate-induced hippocampal damage. Neuroscience, 101, 563-570.
37. Luetjens, C.M., Bui, N.T., Sengpiel, B., Munstermann, G., Poppe, M., Krohn, A.J., Bauerbach, E., Krieglstein, J. & Prehn, J.H. (2000) Delayed mitochondrial dysfunction in excitotoxic neuron death: cytochrome c release and a secondary increase in superoxide production. J. Neurosci., 20, 5715-5723.
38. Maiorino, M., Roveri, A., Coassin, M. & Ursini, F. (1988) Kinetic mechanism and substrate specificity of glutathione peroxidase activity of ebselen (PZ51). Biochem. Pharmacol., 37, 2267-2271.
39. McCarthy, K.D. & de Vellis, J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol., 85, 890-902.
40. McDonald, M.C., d'Emmanuele di Villa Bianca, R., Wayman, N.S., Pinto, A., Sharpe, M.A., Cuzzocrea, S., Chatterjee, P.K. & Thiemermann, C. (2003) A superoxide dismutase mimetic with catalase activity (EUK-8) reduces the organ injury in endotoxic shock. Eur. J. Pharmacol., 466, 181-189.
41. Melov, S., Schneider, J.A., Day, B.J., Hinerfeld, D., Coskun, P., Mirra, S.S., Crapo, J.D. & Wallace, D.C. (1998) A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat. Genet., 18, 159-163.
42. Mitchell, P. (1966) Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol. Rev. Camb. Philos. Soc., 41, 445-502.
43. Murphy, T.H., Miyamoto, M., Sastre, A., Schnaar, R.L. & Coyle, J.T. (1989) Glutamate toxicity in a neuronal cell line involves inhibition of cystine transport leading to oxidative stress. Neuron, 2, 1547-1558.
44. Murphy, T.H., Schnaar, R.L. & Coyle, J.T. (1990) Immature cortical neurons are uniquely sensitive to glutamate toxicity by inhibition of cystine uptake. FASEB J., 4, 1624-1633.
45. Naqui, A., Chance, B. & Cadenas, E. (1986) Reactive oxygen intermediates in biochemistry. Annu. Rev. Biochem., 55, 137-166.
46. Oka, A., Belliveau, M.J., Rosenberg, P.A. & Volpe, J.J. (1993) Vulnerability of oligodendroglia to glutamate: pharmacology, mechanisms, and prevention. J. Neurosci., 13, 1441-1453.
47. Pfeiffer, S.E., Warrington, A.E. & Bansal, R. (1993) The oligodendrocyte and its many cellular processes. Trends Cell. Biol., 3, 191-197.
48. Rizzardini, M., Lupi, M., Bernasconi, S., Mangolini, A. & Cantoni, L. (2003) Mitochondrial dysfunction and death in motor neurons exposed to the glutathione-depleting agent ethacrynic acid. J. Neurol. Sci., 207, 51-58.
49. Rosenberg, P.A., Dai, W., Gan, X.D., Ali, S., Fu, J., Back, S.A., Sanchez, R.M., Segal, M.M., Follett, P.L., Jensen, F.E. & Volpe, J.J. (2003) Mature myelin basic protein-expressing oligodendrocytes are insensitive to kainate toxicity. J. Neurosci. Res., 71, 237-245.
50. Rosenberg, P.A., Li. Y., Le, M. & Zhang, Y. (2000) Nitric oxide-stimulated increase in extracellular adenosine accumulation in rat forebrain neurons in culture is associated with ATP hydrolysis and inhibition of adenosine kinase activity. J. Neurosci., 20, 6294-6301.
51. Salvioli, S., Ardizzoni, A., Franceschi, C. & Cossarizza, A. (1997) JC-1, but not DiOC6 (3) or rhodamine 123, is a reliable fluorescent probe to assess delta psi changes in intact cells: implications for studies on mitochondrial functionality during apoptosis. FEBS Lett., 411, 77-82.
52. Schinder, A.F., Olson, E.C., Spitzer, N.C. & Montal, M. (1996) Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J. Neurosci., 16, 6125-6133.
53. Sengpiel, B., Preis, E., Krieglstein, J. & Prehn, J.H. (1998) NMDA-induced superoxide production and neurotoxicity in cultured rat hippocampal neurons: role of mitochondria. Eur. J. Neurosci., 10, 1903-1910.
54. Seyfried, J., Soldner, F., Schulz, J.B., Klockgether, T., Kovar, K.A. & Wullner, U. (1999) Differential effects of 1-buthionine sulfoxime and ethacrynic acid on glutathione levels and mitochondrial function in PC12 cells. Neurosci. Lett., 264, 1-4.
55. Shivakumar, B.R., Kolluri, S.V. & Ravindranath, V. (1995) Glutathione and protein thiol homeostasis in brain during reperfusion after cerebral ischemia. J. Pharmacol. Exp. Ther., 274, 1167-1173.
56. Staniek, K., Gille, L., Kozlov, A.V. & Nohl, H. (2002) Mitochondrial superoxide radical formation is controlled by electron bifurcation to the high and low potential pathways. Free Radic. Res., 36, 381-387.
57. Tan, S., Sagara, Y., Liu, Y., Maher, P. & Schubert, D. (1998) The regulation of reactive oxygen species production during programmed cell death. J. Cell. Biol., 141, 1423-1432.
58. Vander Heiden, M., Chandel, N.S., Williamson, E.K., Schumaker, P.T. & Thompson, C.B. (1997) Bcl-xL regulates the membrane potential and Volume homeostasis of mitochondria. Cell, 91, 627-637.
59. Voest, E.E., van Faassen, E. & Marx, J.J. (1993) An electron paramagnetic resonance study of the antioxidant properties of the nitroxide free radical TEMPO. Free Radic. Biol. Med., 15, 589-595.
60. Wallin, C., Puka-Sundvall, M., Hagberg, H., Weber, S.G. & Sandberg, M. (2000) Alterations in glutathione and amino acid concentrations after hypoxia-ischemia in the immature rat brain. Brain Res. Dev. Brain Res., 125, 51-60.
61. White, R.J. & Reynolds, I.J. (1996) Mitochondrial depolarization in glutamate-stimulated neurons: an eraly signal specific to excitotoxin exposure. J. Neurosci., 16, 5688-5697.
62. Wullner, U., Seyfried, J., Groscurth, P., Beinroth, S., Winter, S., Gleichmann, M., Heneka, M., Loschmann, P., Schulz, J.B., Weller, M. & Klockgether, T. (1999) Glutathione depletion and neuronal cell death: the role of reactive oxygen intermediates and mitochondrial function. Brain Res., 826, 53-62.
63. Yamamoto, M., Sakamoto, N., Iwai, A., Yatsugi, S., Hidaka, K., Noguchi, K. & Yuasa, T. (1993) Protective actions of YM737, a new glutathione analog. against cerebral ischemia in rats. Res. Commun. Chem. Pathol. Pharmacol., 81, 221-232.
64. Yonezawa, M., Back, S.A., Gan, X., Rosenberg, P.A. & Volpe, J.J. (1996) Cystine deprivation induced oligodendroglial death: rescue by free radical scavengers and by a diffusible glial factor. J. Neurochem., 67, 566-573.
65. Zwacka, R.M., Dudus, L., Epperly, M.W., Greenberger, J.S. & Engelhardt, J.F. (1998b) Redox gene therapy protects human IB-3 lung epithelial cells against ionizing radition-induced apoptosis. Hum. Gene Ther., 9, 1381-1386.
66. Zwacka, R.M., Zhou, W., Zhang, Y., Darby, C.J., Dudus, L., Halldorson, J., Oberley, L. & Engelhardt, J.F. (1998a) Redox gene therapy for ischemia/ reperfusion injury of the liver reduces AP1 and NF-kappaB activation. Nat. Med., 4, 698-704.