Superoxide dismutase deficiency enhances superoxide levels in brain tissues during oxygenation and hypoxia-reoxygenation

Journal of Neuroscience Research

Volumn 89, Issue 4, 2011, Pages 601-610

  Sasaki, Toru ^a   Shimizu, Takahiko ^a   Koyama, Tomoko ^a,b   Sakai, Masanobu ^a,b   Uchiyama, Satoshi ^a   Kawakami, Satoru ^a   Noda, Yoshihiro ^a   Shirasawa, Takuji ^a,c   Kojima, Shuji ^b  

^a TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

^b TOKYO UNIVERSITY OF SCIENCE   (Japan)

^c JUNTENDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Brain slices; Chemiluminescence; Hypoxia reoxygenation; Superoxide; Superoxide dismutase deficiency

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; MANGANESE SUPEROXIDE DISMUTASE; SUPEROXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HYPOXIA; BRAIN LEVEL; CYTOPLASM; ENZYME ACTIVITY; MITOCHONDRION; MOUSE; NONHUMAN; OXYGENATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REOXYGENATION; REPERFUSION INJURY;

ANIMALS; BRAIN; CYTOPLASM; HYPOXIA, BRAIN; LUMINESCENCE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA; ORGAN CULTURE TECHNIQUES; REPERFUSION INJURY; SUPEROXIDE DISMUTASE; SUPEROXIDES;

EID: 79751481756     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22581     Document Type: Article

References (72)

1. Asimakis GK, Lick S, Patterson C. 2002. Postischemic recovery of contractile function is impaired in SOD2(+/-) but not SOD1(+/-) mouse hearts. Circulation 105: 981-986.
2. Baker MS, Gebicki JM. 1984. The effect of pH on the conversion of superoxide to hydroxyl free radicals. Arch Biochem Biophys 234: 258-264.
3. Becker LB, vanden Hoek TL, Shao ZH, Li CQ, Schumacker PT. 1999. Generation of superoxide in cardiomyocytes during ischemia before reperfusion. Am J Physiol 277: H2240-H2246.
4. Beckman KB, Ames BN. 1998. Mitochondrial aging: open questions. Ann N Y Acad Sci 854: 118-127.
5. Bejma J, Ji LL. 1999. Aging and acute exercise enhance free radical generation in rat skeletal muscle. J Appl Physiol 87: 465-470.
6. Brennan LA, Steinhorn RH, Wedgwood S, Mata-Greenwood E, Roark EA, Russell JA, Black SM. 2003. Increased superoxide generation is associated with pulmonary hypertension in fetal lambs: a role for NADPH oxidase. Circ Res 92: 683-691.
7. Carlsson LM, Jonsson J, Edlund T, Marklund SL. 1995. Mice lacking extracellular superoxide dismutase are more sensitive to hyperoxia. Proc Natl Acad Sci U S A 92: 6264-6268.
8. Chan PH. 2005. Mitochondrial dysfunction and oxidative stress as determinants of cell death/survival in stroke. Ann N Y Acad Sci 1042: 203-209.
9. Chan PH, Kawase M, Murakami K, Chen SF, Li Y, Calagui B, Reola L, Carlson E, Epstein CJ. 1998. Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J Neurosci 18: 8292-8299.
10. Chang LY, Slot JW, Geuze HJ, Crapo JD. 1988. Molecular immunocytochemistry of the CuZn superoxide dismutase in rat hepatocytes. J Cell Biol 107: 2169-2179.
11. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ. 2003. Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278: 36027-36031.
12. Cortopassi GA, Wong A. 1999. Mitochondria in organismal aging and degeneration. Biochim Biophys Acta 1410: 183-193.
13. Elchuri S, Oberley TD, Qi W, Eisenstein RS, Jackson Roberts L, Van Remmen H, Epstein CJ, Huang TT. 2005. CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 24: 367-380.
14. Fabian RH, Kent TA. 1999. Superoxide anion production during reperfusion is reduced by an antineutrophil antibody after prolonged cerebral ischemia. Free Radic Biol Med 26: 355-361.
15. Fiskum G, Murphy AN, Beal MF. 1999. Mitochondria in neurodegeneration: acute ischemia and chronic neurodegenerative diseases. J Cereb Blood Flow Metab 19: 351-369.
16. Fleming JE, Reveillaud I, Niedzwiecki A. 1992. Role of oxidative stress in Drosophila aging. Mutat Res 275: 267-279.
17. Frederiks WM, Vreeling-Sindelárová H. 2002. Ultrastructural localization of xanthine oxidoreductase activity in isolated rat liver cells. Acta Histochem 104: 29-37.
18. Fujimura M, Morita-Fujimura Y, Kawase M, Copin JC, Calagui B, Epstein CJ, Chan PH. 1999. Manganese superoxide dismutase mediates the early release of mitochondrial cytochrome C and subsequent DNA fragmentation after permanent focal cerebral ischemia in mice. J Neurosci 19: 3414-3422.
19. Granger DN, Rutili G, McCord JM. 1981. Superoxide radicals in feline intestinal ischemia. Gastroenterology 81: 22-29.
20. Harik SI, Lust WD, Jones SC, Lauro KL, Pundik S, LaManna JC. 1995. Brain glucose metabolism in hypobaric hypoxia. J Appl Physiol 79: 136-140.
21. Huang J, Philbert MA. 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.
22. Ikegami T, Suzuki Y, Shimizu T, Isono K, Koseki H, Shirasawa T. 2002. Model mice for tissue-specific deletion of the manganese superoxide dismutase (MnSOD) gene. Biochem Biophys Res Commun 296: 729-736.
23. Inarrea P, Moini H, Rettori D, Han D, Martinez J, Garcia I, Fernandez-Vizarra E, Iturralde M, Cadenas E. 2005. Redox activation of mitochondrial intermembrane space Cu, Zn-superoxide dismutase. Biochem J 387: 203-209.
24. Inauen W, Payne DK, Kvietys PR, Granger DN. 1990. Hypoxia/reoxygenation increases the permeability of endothelial cell monolayers: role of oxygen radicals. Free Radic Biol Med 9: 219-223.
25. Jones SA, O'Donnell VB, Wood JD, Broughton JP, Hughes EJ, Jones OT. 1996. Expression of phagocyte NADPH oxidase components in human endothelial cells. Am J Physiol 271: H1626-H634.
26. Kim GW, Kondo T, Noshita N, Chan PH. 2002. Manganese superoxide dismutase deficiency exacerbates cerebral infarction after focal cerebral ischemia/reperfusion in mice: implications for the production and role of superoxide radicals. Stroke 33: 809-815.
27. Kinouchi H, Epstein CJ, Mizui T, Carlson E, Chen SF, Chan PH. 1991. Attenuation of focal cerebral ischemic injury in transgenic mice overexpressing CuZn superoxide dismutase. Proc Natl Acad Sci U S A 88: 11158-11162.
28. Kirsch JR, Helfaer MA, Lange DG, Traystman RJ. 1992. Evidence for free radical mechanisms of brain injury resulting from ischemia/reperfusion-induced events. J Neurotrauma 9( Suppl 1): S157-S163.
29. Koistinaho J, Chan PH. 2000. Spreading depression-induced cyclooxygenase-2 expression in the cortex. Neurochem Res 25: 645-651.
30. Kondo T, Reaume AG, Huang TT, Carlson E, Murakami K, Chen SF, Hoffman EK, Scott RW, Epstein CJ, Chan PH. 1997. Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J Neurosci 17: 4180-4189.
31. Kondo Y, Sasaki T, Sato Y, Amano A, Aizawa S, Iwama M, Handa S, Shimada N, Fukuda M, Akita M, Lee J, Jeong K, Maruyama N. 2008. Vitamin C depletion increases superoxide generation in brains of SMP30/GNL knockout mice. Biochem Biophys Res Commun 377: 291-296.
32. Kostrominova TY, Pasyk KA, Van Remmen H, Richardson AG, Faulkner JA. 2007. Adaptive changes in structure of skeletal muscles from adult Sod1 homozygous knockout mice. Cell Tissue Res 327: 595-605.
33. Ku HH, Brunk UT, Sohal RS. 1993. Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species. Free Radic Biol Med 15: 621-627.
34. Landis GN, Tower J. 2005. Superoxide dismutase evolution and life span regulation. Mech Ageing Dev 126: 365-379.
35. Lebovitz RM, Zhang H, Vogel H, Cartwright JJr, Dionne L, Lu N, Huang S, Matzuk MM. 1996. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci U S A 93: 9782-9787.
36. Li C, Jackson RM. 2002. Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol 282: C227-C241.
37. Li Y, Huang TT, Carlson EJ, Melov S, Ursell PC, Olson JL, Noble LJ, Yoshimura MP, Berger C, Chan PH, Wallace DC, Epstein CJ. 1995. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 11: 376-381.
38. Li Y, Zhu H, Kuppusamy P, Roubaud V, Zweier JL, Trush MA. 1998. Validation of lucigenin (bis-N-methylacridinium) as a chemilumigenic probe for detecting superoxide anion radical production by enzymatic and cellular systems. J Biol Chem 273: 2015-2023.
39. 2 formation. Free Radic Biol Med 42: 1465-1469.
40. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
41. Luft R. 1994. The development of mitochondrial medicine. Proc Natl Acad Sci U S A 91: 8731-8738.
42. Margaill I, Plotkine M, Lerouet D. 2005. Antioxidant strategies in the treatment of stroke. Free Radic Biol Med 39: 429-443.
43. Martz D, Rayos G, Schielke GP, Betz AL. 1989. Allopurinol and dimethylthiourea reduce brain infarction following middle cerebral artery occlusion in rats. Stroke 20: 488-494.
44. Murakami K, Kondo T, Kawase M, Li Y, Sato S, Chen SF, Chan PH. 1998. 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: 205-213.
45. Nojiri H, Shimizu T, Funakoshi M, Yamaguchi O, Zhou H, Kawakami S, Ohta Y, Sami M, Tachibana T, Ishikawa H, Kurosawa H, Kahn RC, Otsu K, Shirasawa T. 2006. Oxidative stress causes heart failure with impaired mitochondrial respiration. J Biol Chem 281: 33789-33801.
46. Okado-Matsumoto A, Fridovich I. 2001. Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J Biol Chem 276: 38388-38393.
47. Panchenko LF, Brusov OS, Gerasimov AM, Loktaeva TD. 1975. Intramitochondrial localization and release of rat liver superoxide dismutase. FEBS Lett 55: 84-87.
48. Phillis JW, Sen S, Cao X. 1994. Amflutizole, a xanthine oxidase inhibitor, inhibits free radical generation in the ischemic/reperfused rat cerebral cortex. Neurosci Lett 169: 188-190.
49. Rao PV, Maddala R, John F, Zigler JS. 2004. Expression of nonphagocytic NADPH oxidase system in the ocular lens. Mol Vis 1910: 112-121.
50. Rembish SJ, Trush MA. 1994. Further evidence that lucigenin-derived chemiluminescence monitors mitochondrial superoxide generation in rat alveolar macrophages. Free Radic Biol Med 17: 117-126.
51. Sasaki T. 2004. In vivo and in vitro molecular imaging techniques to clarify the mechanism of oxidative stress related to brain aging and neurodegenerative diseases. Curr Med Chem Central Nerv Syst Agents 4: 61-69.
52. Sasaki T, Fujibayashi Y, Senda M. 1998. Distribution of glutathione and technetium-99m-meso-HMPAO in normal and diethyl maleate-treated mouse brain mitochondria. J Nucl Med 39: 2178-2183.
53. Sasaki T, Iwamoto A, Tsuboi H, Watanabe Y. 2006. Development of real-time bioradiographic system for functional and metabolic imaging in living brain tissue. Brain Res 1077: 161-169.
54. Sasaki T, Unno K, Tahara S, Shimada A, Chiba Y, Hoshino M, Kaneko T. 2008. Age-related increase of superoxide generation in the brains of mammals and birds. Aging Cell 7: 459-469.
55. Sasaki T, Unno K, Tahara S, Kaneko T. 2010. Age-related increase of reactive oxygen generation in the brains of mammals and birds: Is reactive oxygen a signaling molecule to determine the aging process and life span? Geriatr Gerontol Int 10: S10-S24.
56. Sato Y, Kajiyama S, Amano A, Kondo Y, Sasaki T, Handa S, Takahashi R, Fukui M, Hasegawa G, Nakamura N, Fujinawa H, Mori T, Ohta M, Obayashi H, Maruyama N, Ishigami A. 2008. Hydrogen-rich pure water prevents superoxide formation in brain slices of vitamin C-depleted SMP30/GNL knockout mice. Biochem Biophys Res Commun 375: 346-350.
57. Schurr A, West CA, Rigor BM. 1988. Lactate-supported synaptic function in the rat hippocampal slice preparation. Science 240: 1326-1328.
58. Sentman ML, Granström M, Jakobson H, Reaume A, Basu S, Marklund SL. 2006. Phenotypes of mice lacking extracellular superoxide dismutase and copper- and zinc-containing superoxide dismutase. J Biol Chem 281: 6904-6909.
59. Shigenaga MK, Hagen TM, Ames BN. 1994. Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci U S A 91: 10771-10778.
60. Sims NR, Anderson MF. 2002. Mitochondrial contributions to tissue damage in stroke. Neurochem Int 40: 511-526.
61. Soboll S, Scholz R, Heldt HW. 1978. Subcellular metabolite concentrations. Dependence of mitochondrial and cytosolic ATP systems on the metabolic state of perfused rat liver. Eur J Biochem 87: 377-390.
62. Sugawara T, Noshita N, Lewen A, Gasche Y, Ferrand-Drake M, Fujimura M, Morita-Fujimura Y, Chan PH. 2002. Overexpression of copper/zinc superoxide dismutase in transgenic rats protects vulnerable neurons against ischemic damage by blocking the mitochondrial pathway of caspase activation. J Neurosci 22: 209-217.
63. Suzuki K, Miyazawa N, Nakata T, Seo HG, Sugiyama T, Taniguchi N. 1993. High copper and iron levels and expression of Mn-superoxide dismutase in mutant rats displaying hereditary hepatitis and hepatoma (LEC rats). Carcinogenesis 14: 1881-1884.
64. Takahashi MA, Asada K. 1983. Superoxide anion permeability of phospholipid membranes and chloroplast thylakoids. Arch Biochem Biophys 226: 558-566.
65. Taylor MD, Mellert TK, Parmentier JL, Eddy LJ. 1985. Pharmacological protection of reoxygenation damage to in vitro brain slice tissue. Brain Res 347: 268-273.
66. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schutz G. 1999. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23: 99-103.
67. Uchiyama S, Shimizu T, Shirasawa T. 2006. CuZn-SOD deficiency causes ApoB degradation and induces hepatic lipid accumulation by impaired lipoprotein secretion in mice. J Biol Chem 281: 31713-31719.
68. Van Den Munckhof RJ, Vreeling-Sindelarova H, Schellens JP, Van Noorden CJ, Frederiks WM. 1995. Ultrastructural localization of xanthine oxidase activity in the digestive tract of the rat. Histochem J 27: 897-905.
69. van Manen HJ, van Bruggen R, Roos D, Otto C. 2006. Single-cell optical imaging of the phagocyte NADPH oxidase. Antioxid Redox Signal 8: 1509-1522.
70. Vanfleteren JR, De Vreese A. 1996. Rate of aerobic metabolism and superoxide production rate potential in the nematode Caenorhabditis elegans. J Exp Zool 274: 93-100.
71. Weisiger RA, Fridovich I. 1973. Mitochondrial superoxide simutase. Site of synthesis and intramitochondrial localization. J Biol Chem 248: 4793-4796.
72. Xiong Y, Shie FS, Zhang J, Lee CP, Ho YS. 2005. Prevention of mitochondrial dysfunction in post-traumatic mouse brain by superoxide dismutase. J Neurochem 95: 732-744.