Apoptosis in Ca2+ reperfusion injury of cultured astrocytes: Roles of Reactive Oxygen Species and NF-κB activation

European Journal of Neuroscience

Volumn 11, Issue 12, 1999, Pages 4204-4212

  Takuma, Kazuhiro ^a   Lee, Eibai ^a   Kidawara, Miyuki ^a   Mori, Koichi ^a   Kimura, Yuji ^b   Baba, Akemichi ^b   Matsuda, Toshio ^b  

^a KOBE GAKUIN UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Caspase; Cell death; Hydrogen peroxide

Indexed keywords

CALCIUM; CASP3 PROTEIN, RAT; CASPASE; CASPASE 3; DNA FRAGMENT; ENZYME INHIBITOR; FLUORESCENT DYE; HYDROGEN PEROXIDE; HYDROXYL RADICAL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; REACTIVE OXYGEN METABOLITE; 1,10 PHENANTHROLINE; CALCIUM ION; CASPASE INHIBITOR; PYRROLIDINE DITHIOCARBAMATE; TACROLIMUS;

AGAR GEL ELECTROPHORESIS; ANIMAL; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN CORTEX; CELL CULTURE; CELL SURVIVAL; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; RAT; REPERFUSION INJURY; WISTAR RAT; ANIMAL CELL; CYTOTOXICITY; NERVE CELL CULTURE; NEWBORN; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; ASTROCYTES; CALCIUM; CASPASE 3; CASPASES; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; DNA FRAGMENTATION; ELECTROPHORESIS, AGAR GEL; ENZYME INHIBITORS; FLUORESCENT DYES; HYDROGEN PEROXIDE; HYDROXYL RADICAL; NF-KAPPA B; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY;

EID: 0033233481     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.1999.00850.x     Document Type: Article

References (67)

1. Atlante, A., Gagliardi, S., Minervini, G.M., Ciotti, M.T., Marra, E. & Calissano, P. (1997) Glutamates neurotoxicity in rat cerebellar granule cells: a major role for xanthine oxidase in oxygen radical formation. J. Neurochem., 68, 2038-2045.
2. 2+ accumulation. Proc. Natl Acad. Sci. USA, 92, 221-237.
3. Beg, A.A. & Baltimore, D. (1996) An essential role of NF-κB in preventing TNF-α-induced cell death. Science, 274, 782-784.
4. Behl, C., Davis, J.B., Lesiey, R. & Schubert, D. (1994) Hydrogen peroxide mediates amyloid β protein toxicity. Cell, 77, 817-827.
5. Brown, D.G., Sun, X.M. & Cohen, G.M. (1993) Dexamethasone-induced apoptosis involves cleavage of DNA to large fragments prior to internucleosomal fragmentation. J. Biol. Chem., 268, 3037-3039.
6. Burton, K. (1956) A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem. J., 62, 315-323.
7. Buttelli, M.G., Lorenzoni, E. & Stirpe, F. (1973) Milk xanthine oxidase type D (dehydrogenase) and type O (oxidase). Biochem. J., 131, 191-198.
8. Byler, R.M., Sheraman, N.A., Wallner, J.S. & Horwitz, L.D. (1994) Hydrogen peroxide cytotoxicity in cultured cardiac myocytes is iron dependent. Am. J. Physiol., 269, H121-H127.
9. Chapman, R.A. & Tunstall, J. (1987) The calcium paradox of the heart. Prog. Biophys. Mol. Biol., 50, 67-96.
10. Chen, J., Nagayama, T., Jin, K., Stetler, R.A., Zhu, R.L., Graham, S.H. & Simon, R.P. (1998) Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. J. Neurosci., 18, 4914-4928.
11. Cheng, Y. & Sun, A.Y. (1994) Oxidative mechanisms involved in kainate-induced cytotoxicity in cortical neurons. Neurochem. Res., 19, 1557-1564.
12. Chiesa, R., Angeretti, N., Del Bo, R., Lucca, E., Munna, E. & Forloni, G. (1998) Extracellular calcium deprivation in astrocytes: regulation of mRNA expression and apoptosis. J. Neurochem., 70, 1474-1483.
13. Clemens, J.A., Stephenson, D.T., Smalstig, E.B., Dixon, E.P. & Little, S.P. (1997) Global ischemia activates nuclear factor-kappa B in forebrain neurons of rats. Stroke, 28, 1073-1080.
14. Clemens, J.A., Stephenson, D.T., Yin, T., Smalstig, E.B., Panetta, J.A. & Little, S.P. (1998) Drug-induced neuroprotection from global ischemia is associated with prevention of persistent but not transient activation of nuclear factor KB in rats. Stroke, 29, 677-682.
15. Coyle, J.T. & Puttfarcken, P. (1993) Oxidative stress, glutamate, and neurodenerative disorders. Science, 262, 689-695.
16. Dawson, V.L., Dawson, T.M., Bartley, D.A., Uhl, G.R. & Snyder, S.H. (1993) Mechanisms of nitric oxide-mediated neurotoxicity in primary brain culture. J. Neurosci., 13, 2651-2661.
17. Donovan, F.M., Pike, C.J., Cotman, C.W. & Cunningham, D.D. (1997) Thrombin induces apoptosis in cultured neurons and astrocytes via a pathway requiring tyrosine kinase and RhoA activities. J. Neurosci., 17, 5316-5326.
18. Flohé, L., Brigelius-Hohé, R., Saliou, C., Traber, M.G. & Packer, L. (1997) Redox regulation of NF-κB activation. Free Radical Biol. Med., 22, 1115-1126.
19. Frantz, B., Nordby, E.C., Bren, G., Steffan, N., Paya, C.V., Kincaid, R.L., Tocci, M.J., O'Keefe, S.J. & O'Neill, E.A. (1994) Calcineurin acts in synergy with PMA to inactivate IκB/MAD3, an inhibitor of NF-κB. EMBO J., 13, 861-870.
20. Goldman, R., Moshonov, S. & Zor, U. (1998) Generation of reactive oxygen species in a human keratinocyte cell line: role of calcium. Arch. Biochem. Biophys., 350, 10-18.
21. Goodman, Y. & Mattson, M.P. (1996) Ceramide protects hippocampal neurons against excitotoxic and oxidative insults and amyloid β-peptide toxicity. J. Neurochem., 66, 869-872.
22. Grilli, M., Pizzi, M., Memorandum, M. & Spano, P. (1996) Neuroprotection by aspirin and sodium salicylate through blockade of NF-κB activation. Science, 274, 1383-1385.
23. Halliwell, B. (1992) Reactive oxygen species and the central nervous system. J. Neurochem., 59, 1609-1623.
24. He, J., DeCastro, C.M., Vandenbark, G.R., Busciglio, J. & Gabuzda, D. (1997) Astrocyte apoptosis induced by HIV-1 transactivation of the c-kit protooncogene. Proc. Natl Acad. Sci. USA, 94, 3954-3959.
25. Hirata, H., Takahashi, A., Kobayashi, S., Yonehara, S., Sawai, H., Okazaki, T., Yamamoto, K. & Sasada, M. (1998) Caspases are activated in a branched protease cascade and control distinct downstream processes in Fas-induced apoptosis. J. Exp. Med., 187, 587-600.
26. Hu, J. & Van Eldik, L.J. (1996) S100 β induces apoptotic cell death in cultured astrocytes via a nitric oxide-dependent pathway. Biochim. Biophys. Acta, 1313, 239-245.
27. 2 in vitro. Brain Res., 671, 181-186.
28. 2+ exchanger in cells expressing NCX1. J. Biol. Chem., 271, 22391-22397.
29. 2+ influx. J. Immunol., 157, 5277-5283.
30. Kessler, J.A., Ludlam, W.H., Freidin, M.M., Hall, D.H., Michaelson, M.D., Spray, D.C., Dougherty, M. & Batter, D.K. (1993) Cytokine-induced programmed cell death of cultured sympathetic neurons. Neuron, 11, 1123-1132.
31. Kondo, T., Kinouchi, H., Kawase, M. & Yoshimoto, T. (1996) Differential response in the release of hydrogen peroxide between astroglial cells and endothelial cells following hypoxia/reperfusion. Neurosci. Lett., 215, 103-106.
32. Kristian, T., Katsura, K., Gido, G. & Siesjo, B.K. (1994) The influence of pH on cellular calcium influx during ischemia. Brain Res., 641, 295-302.
33. Krueger, B.K., Burne, J.F. & Raff, M.C. (1995) Evidence for large scale astrocyte death in the developing cerebellum. J. Neurosci., 15, 3366-3374.
34. Lancelot, E., Callebert, J., Revaud, M.L., Boulu, R.G. & Plotkine, M. (1995) Detection of hydroxyl radicals in rat striatum during transient focal cerebral ischemia: possible implication in tissue damage. Neurosci. Lett., 197, 85-88.
35. Lee, E., Furukube, T., Miyabe, T., Yamauchi, A. & Kariya, K. (1996) Involvement of histone hyperacetylation in triggering DNA fragmentation of rat thymocytes undergoing apoptosis. FEBS Lett., 395, 183-187.
36. Lee, K.S., Frank, S., Vanderklish, P., Arai, A. & Lynch, G. (1991) Inhibition of proteolysis protects hippocampal neurons from ischemia. Proc. Natl Acad. Sci. USA, 88, 7233-7237.
37. Lin, K.I., Lee, S.H., Narayanan, R., Baraban, J.M., Hardwick, J.M. & Ratan, R.R. (1995) Thiol agents and bcl-2 identify an alphavirus-induced apoptotic pathway that requires activation of NF-κB. J. Cell Biol., 131, 1-14.
38. Linnik, M.D., Zobrist, R.H. & Hatfield, M.D. (1993) Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke, 24, 2002-2009.
39. Liu, X.Z., Xu, X.M., Hu, R., Du, C., Zhang, S.X., McDonald, J.W., Dong, H.X., Wu, Y.J., Fan, G.S., Jacquin, M.F., Hsu, C.Y. & Choi, D.W. (1997) Neuronal and glial apoptosis after traumatic spinal cord injury. J. Neurosci., 17, 5395-5406.
40. Mangoura, D. & Dawson, G. (1998) Programmed cell death in cortical chick embryo astrocytes is associated with activation of protein kinase PK60 and ceramide formation. J. Neurochem., 70, 130-138.
41. Manna, S.K., Zhang, H.J., Yan, T., Oberley, L.W. & Aggarwa, B.B. (1998) Overexpression of manganase superoxide dismutase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-kappaB and activated protein-1. J. Biol. Chem., 273, 13245-13254.
42. 2+ exchanger in reperfusion-induced delayed cell death of cultured rat astrocytes. Eur. J. Neurosci., 8, 951-958.
43. Matsuda, T., Takuma, K., Asano, S., Kishida, Y., Mori, K., Maeda, S. & Baba, A. (1998) Protection by calcineurin inhibitors against reperfusion injury of cultured fat astrocytes. J. Neurochem., 70, 2004-2011.
44. Mello-Filho, A.C. & Meneghini, R. (1991) Iron is the intracellular metal involved in the production of DNA damage by oxygen radicals. Mutat. Res., 251, 109-113.
45. Nash, T. (1953) The colorimetric estimation of formaldehyde by means of the Hantzsch reaction. Biochem. J., 55, 416-421.
46. Nicholson, D.W., Ali, A., Thomberry, N.A., Vaillancourt, J.P., Ding, C.K., Gallant, M., Gareau, Y., Griffin, P.R., Labelle, M., Lazenbnik, Y.A., Munday, N.A., Raju, S.M., Smulson, M.E., Yamin, T., Yu, V.L. & Miller, D.K. (1995) Identification arid inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature, 376, 37-43.
47. Olanow, C.W. (1993) A radical hypothesis for neurodegeneration. Trends Neurosci., 16, 439-444.
48. 2+ and reactive oxygen intermediates as messengers. FEBS Lett., 392, 129-136.
49. Papadopoulos, M., Koumenis, I.L., Yuan, T.Y. & Giffard, R.G. (1998) Increasing vulnerability of astrocytes to oxidative injury with age despite constant antioxidant defenses. Neuroscience, 82, 915-925.
50. Perez-Velazquez, J.L., Frantseva, M.V. & Carlen, P.L. (1997) In vitro ischemia promotes glutamate-mediated free radical generation and intracellular calcium accumulation in hippocampal pyramidal neurons. J. Neurosci., 17, 9085-9094.
51. Petito, C.K., Olarte, J.P., Roberts, B., Nowak, T.S. Jr & Pulsinelli, W.A. (1998) Selective glial vulnerability following transient global ischemia in rat brain. J. Neuropathol. Exp. Neurol., 57, 231-238.
52. Portera-Cailliau, C., Hedreen, J.C., Price, D.L. & Koliatsos, V.E. (1995) Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J. Neurosci., 15, 3775-3787.
53. Rano, T.A., Timkey, T., Petersoh, E.P., Rotonda, J., Nicholson, D.W., Becker, J.W., Chapman, K.T. & Thomberry, N.A. (1997) A combinatorial approach for determining protease specificities: application to interleukin-1β converting enzyme (ICE). Chem. Biol., 4, 149-155.
54. Schneider, A., Martin-Villalba, A., Weih, F., Vogel, J., Wirth, T. & Schwaninger, M. (1999) NF-κB is activated and promotes cell death in focal cerebral ischemia. Nature Med., 5, 554-559.
55. Schreiber, E., Matthias, P., Muller, M.M. & Schaffner, W. (1989) Rapid detection of octamer binding proteins with 'mini extracts', prepared from a small number of cells. Nucleic Acid Res., 11, 6419.
56. Shatrov, V.A., Lehmann, V. & Chouaib, S. (1997) Sphingosine-1-phosphate mobilizes intracellular calcium and activates transcription factor NF-κB in U937 cells. Biochem. Biophys. Res. Commun., 234, 121-124.
57. Siemkowicz, E. & Hansen, A.J. (1981) Brain extracellular ion composition and EEG activity following 10 minutes ischemia in normo- and hyperglycemic rats. Stroke, 12, 236-240.
58. + in the hippocampus during recovery from short-term, transient ischemia. J. Cereb. Blood Flow Metab., 12, 759-772.
59. Simonson, S.G., Zhang, J., Canada, A.T. Jr, Su, Y.F., Benveniste, H. & Piantadosi, C.A. (1993) Hydrogen peroxide production by monoamine oxidase during ischemia-reperfusion in the rat brain. J. Cereb. Blood Flow Metab., 13, 125-134.
60. Slater, T.F. (1984) Free-radical mechanisms in tissue injury. Biochem. J., 222, 1-15.
61. 2+-dependent signal transduction pathways. J. Immunol., 155, 4685-4691.
62. Suzumura, A., Sawada, M., Yamamoto, H. & Marunouchi, T. (1993) Transforming growth factor-β suppresses activation and proliferation of microglia in vitro. J. Immunol., 151, 2150-2158.
63. 2+ exchanger. Glia, 12, 336-342.
64. Tong, L., Toliver-Kinsky, T., Taglialatela, G., Werrbach-Perez, K., Wood, T. & Perez-Polo, J.R. (1998) J. Neurochem., 71, 447-459.
65. Van Antwerp, D.J., Martin, S.J., Kafri, T., Green, D.R. & Verma, I.M. (1996) Suppression of TNF-α-induced apoptosis by NF-κB. Science, 274, 787-789.
66. Watson, A.J.M., Askew, J.N. & Sandle, G.I. (1994) Characterisation of oxidative injury to an intestinal cell line (HT-29) by hydrogen peroxide. Gut, 35, 1575-1581.
67. Zimmerman, A.N.E. & Hulsmann, W.G. (1966) Paradoxical influence of calcium ions on the permeability of the cell membranes of the isolated rat heart. Nature, 211, 646-647.