Estrogen attenuates oxidative stress-induced apoptosis in C6 glial cells

Brain Research

Volumn 971, Issue 2, 2003, Pages 178-188

  Sur, Pratima ^a   Sribnick, Eric Anthony ^a   Wingrave, James Michael ^a   Nowak, Mark Walter ^a   Ray, Swapan Kumar ^a   Banik, Naren Lal ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

17 Estradiol; Apoptosis; Calcium; Calpain; Caspase 3; Hydrogen peroxide

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; CALCIUM ION; CALPAIN; CASPASE 3; DNA NUCLEOTIDYLEXOTRANSFERASE; ESTROGEN; HYDROGEN PEROXIDE; IONOMYCIN; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; ATTENUATION; BRAIN INJURY; CALCIUM CELL LEVEL; CELL DEATH; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEMYELINATING DISEASE; ENZYME ACTIVITY; GLIA CELL; INCUBATION TIME; NEUROLOGIC DISEASE; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; REDUCTION;

EID: 0037427381     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(03)02349-7     Document Type: Article

References (58)

1. Adams J.M., Cory S. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem. Sci. 26:2001;61-66.
2. 2+ exchanger in C6 glioma cells. J. Neurochem. 74:2000;1505-1513.
3. Asthana S., Baker L.D., Craft S., Stanczyk F.Z., Veith R.C., Raskind M.A., Plymate S.R. High-dose estradiol improves cognition for women with ad: results of a randomized study. Neurology. 57:2001;605-612.
4. Ayres S., Abplanalp W., Liu J.H., Subbiah M.T. Mechanisms involved in the protective effect of estradiol-17β on lipid peroxidation and DNA damage. Am. J. Physiol. 274:1998;E1002-1008.
5. Banik N.L., Chou C.H., Deibler G.E., Krutzch H.C., Hogan E.L. Peptide bond specificity of calpain: proteolysis of human myelin basic protein. J. Neurosci. Res. 37:1994;489-496.
6. Behl C., Skutella T., Lezoualch F., Post A., Widmann M., Newton C.J., Holsboer F. Neuroprotection against oxidative stress by estrogens - structure-activity relationship. Mol. Pharmacol. 51:1997;535-541.
7. Blomgren K., Zhu C., Wang X., Karlsson J.O., Leverin A.L., Bahr B.A., Mallard C., Hagberg H. Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of 'pathological apoptosis'? J. Biol. Chem. 276:2001;10191-10198.
8. Bruce-Keller A.J., Keeling J.L., Keller J.N., Huang F.F., Camondola S., Mattson M.P. Antiinflammatory effects of estrogen on microglial activation. Endocrinology. 141:2000;3646-3656.
9. Buki A., Okonkwo D.O., Wang K.K., Povlishock J.T. Cytochrome c release and caspase activation in traumatic axonal injury. J. Neurosci. 20:2000;2825-2834.
10. Chan S.L., Mattson M.P. Caspase and calpain substrates: roles in synaptic plasticity and cell death. J. Neurosci. Res. 58:1999;167-190.
11. Choi W.S., Lee E.H., Chung C.W., Jung Y.K., Jin B.K., Kim S.U., Oh T.H., Saido T.C., Oh Y.J. Cleavage of bax is mediated by caspase-dependent or -independent calpain activation in dopaminergic neuronal cells: protective role of bcl-2. J. Neurochem. 77:2001;1531-1541.
12. Cotran R.S., Kumar V., Collins T. Robbins Pathologic Basis of Disease. 1999;19 Saunders, Philadelphia.
13. 2+ exchanger increases susceptibility to ischemia/reperfusion injury in male, but not female, transgenic mice. Circ. Res. 83:1998;1215-1223.
14. Daniel P.T. Dissecting the pathways to death. Leukemia. 14:2000;2035-2044.
15. Dare E., Gotz M.E., Zhivotovsky B., Manzo L., Ceccatelli S. Antioxidants J811 and 17β-estradiol protect cerebellar granule cells from methylmercury-induced apoptotic cell death. J. Neurosci. Res. 62:2000;557-565.
16. Dubal D.B., Shughrue P.J., Wilson M.E., Merchenthaler I., Wise P.M. Estradiol modulates bcl-2 in cerebral ischemia: a potential role for estrogen receptors. J. Neurosci. 19:1999;6385-6393.
17. Fitzpatrick J.L., Mize A.L., Wade C.B., Harris J.A., Shapiro R.A., Dorsa D.M. Estrogen-mediated neuroprotection against β-amyloid toxicity requires expression of estrogen receptor α or β and activation of the MAPK pathway. J. Neurochem. 82:2002;674-682.
18. Garcia-Barcina J.M., Matute C. Ampa-selective glutamate receptor subunits in glial cells of the adult bovine white matter. Brain Res. Mol. Brain Res. 53:1998;270-276.
19. Gavrieli Y., Sherman Y., Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:1992;493-501.
20. Goodman Y., Bruce A.J., Cheng B., Mattson M.P. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid β-peptide toxicity in hippocampal neurons. J. Neurochem. 66:1996;1836-1844.
21. Green P.S., Yang S.H., Simpkins J.W. Neuroprotective effects of phenolic a ring oestrogens. Novartis Found. Symp. 230:2000;202-213.
22. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:1985;3440-3450.
23. Han Y., Weinman S., Boldogh I., Walker R.K., Brasier A.R. Tumor necrosis factor-α-inducible IKBα proteolysis mediated by cytosolic m-calpain. A mechanism parallel to the ubiquitin-proteasome pathway for nuclear factor-KB activation. J. Biol. Chem. 274:1999;787-794.
24. Hansen C.A., Monck J.R., Williamson J.R. Measurement of intracellular free calcium to investigate receptor-mediated calcium signaling. Methods Enzymol. 191:1990;691-706.
25. He Z., He Y.J., Day A.L., Simpkins J.W. Proestrus levels of estradiol during transient global cerebral ischemia improves the histological outcome of the hippocampal ca1 region: perfusion-dependent and -independent mechanisms. J. Neurol. Sci. 193:2002;79-87.
26. Honda K., Shimohama S., Sawada H., Kihara T., Nakamizo T., Shibasaki H., Akaike A. Nongenomic antiapoptotic signal transduction by estrogen in cultured cortical neurons. J. Neurosci. Res. 64:2001;466-475.
27. Hosoda T., Nakajima H., Honjo H. Estrogen protects neuronal cells from amyloid β-induced apoptotic cell death. NeuroReport. 12:2001;1965-1970.
28. Huang Y., Wang K.K. The calpain family and human disease. Trends Mol. Med. 7:2001;355-362.
29. Jacobsson S.O., Rongard E., Stridh M., Tiger G., Fowler C.J. Serum-dependent effects of tamoxifen and cannabinoids upon C6 glioma cell viability. Biochem. Pharmacol. 60:2000;1807-1813.
30. Jin G.F., Hurst J.S., Godley B.F. Hydrogen peroxide stimulates apoptosis in cultured human retinal pigment epithelial cells. Curr. Eye Res. 22:2001;165-173.
31. Kawas C., Resnick S., Morrison A., Brookmeyer R., Corrada M., Zonderman A., Bacal C., Lingle D.D., Metter E. A prospective study of estrogen replacement therapy and the risk of developing Alzheimer's disease: the Baltimore longitudinal study of aging. Neurology. 48:1997;1517-1521.
32. Kim Y.J., Hur E.M., Park T.J., Kim K.T. Nongenomic inhibition of catecholamine secretion by 17β-estradiol in PC12 cells. J. Neurochem. 74:2000;2490-2496.
33. Korsmeyer S.J. Bcl-2 gene family and the regulation of programmed cell death. Cancer Res. 59:1999;1693S-1700S.
34. Lopez T., Lopez-Colome A.M., Ortega A. NMDA receptors in cultured radial glia. FEBS Lett. 405:1997;245-248.
35. McGinnis K.M., Whitton M.M., Gnegy M.E., Wang K.K. Calcium/calmodulin-dependent protein kinase IV is cleaved by caspase-3 and calpain in SH-SY5Y human neuroblastoma cells undergoing apoptosis. J. Biol. Chem. 273:1998;19993-20000.
36. Moosmann B., Behl C. The antioxidant neuroprotective effects of estrogens and phenolic compounds are independent from their estrogenic properties. Proc. Natl Acad. Sci. USA. 96:1999;8867-8872.
37. Nath R., Raser K.J., Stafford D., Hajimohammadreza I., Posner A., Allen H., Talanian R.V., Yuen P., Gilbertsen R.B., Wang K.K. Non-erythroid α-spectrin breakdown by calpain and interleukin 1 β-converting-enzyme-like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis. Biochem. J. 319:1996;683-690.
38. Peden D.B., Dailey L., DeGraff W., Mitchell J.B., Lee J.G., Kaliner M.A., Hohman R.J. Hydrogen peroxide effects on rat mast cell function. Am. J. Physiol. 267:1994;L85-93.
39. Pellegrini M., Strasser A. A portrait of the bcl-2 protein family: life, death, and the whole picture. J. Clin. Immunol. 19:1999;365-377.
40. Purnanam K.L., Boustany R.M. Assessment of cell viability and histochemical methods in apoptosis. Hannun Y.A., Boustany R.M. Apoptosis in Neurobiology. 1999;133 CRC Press, New York.
41. Ray S.K., Wilford G.G., Crosby C.V., Hogan E.L., Banik N.L. Diverse stimuli induce calpain overexpression and apoptosis in c6 glioma cells. Brain Res. 829:1999;18-27.
42. Ray S.K., Matzelle D.D., Wilford G.G., Hogan E.L., Banik N.L. Increased calpain expression is associated with apoptosis in rat spinal cord injury: calpain inhibitor provides neuroprotection. Neurochem. Res. 25:2000;1191-1198.
43. 2+ influx upregulate calpain and induce apoptosis in PC12 cells. Brain Res. 852:2000;326-334.
44. Ray S.K., Wilford G.G., Eng L.F., Hogan E.L., Banik N.L. Pathophysiology of central nervous system trauma: proteolytic mechanisms and related therapeutic approaches. Lajtha A., Banik N.L. Role of Proteases in the Pathophysiology of Neurodegenerative Diseases. 2001;199-226 Kluwer, New York.
45. Ray S.K., Matzelle D.D., Wilford G.G., Hogan E.L., Banik N.L. Cell death in spinal cord injury (SCI) requires de novo protein synthesis: calpain inhibitor E-64-d provides neuroprotection in SCI lesion and penumbra. Ann. NY Acad. Sci. 939:2001;436-449.
46. Reed J.C., Jurgensmeier J.M., Matsuyama S. Bcl-2 family proteins and mitochondria. Biochim. Biophys. Acta. 1366:1998;127-137.
47. Seshadri S., Zornberg G.L., Derby L.E., Myers M.W., Jick H., Drachman D.A. Postmenopausal estrogen replacement therapy and the risk of Alzheimer disease. Arch. Neurol. 58:2001;435-440.
48. Shields D.C., Banik N.L. Calcium activated neutral proteinase in demyelinating diseases. Lajtha A., Banik N.L. Role of Proteases in the Pathophysiology of Neurodegenerative Diseases. 2001;25-46 Kluwer, New York.
49. Singer C.A., Figueroa-Masot X.A., Batchelor R.H., Dorsa D.M. The mitogen-activated protein kinase pathway mediates estrogen neuroprotection after glutamate toxicity in primary cortical neurons. J. Neurosci. 19:1999;2455-2463.
50. Sorimachi H., Ishiura S., Suzuki K. Structure and physiological function of calpains. Biochem. J. 328:1997;721-732.
51. Thomas T., Bryant M., Clark L., Garces A., Rhodin J. Estrogen and raloxifene activities on amyloid-β-induced inflammatory reaction. Microvasc. Res. 61:2001;28-39.
52. Wang K.K. Calpain and caspase: can you tell the difference? Trends Neurosci. 23:2000;20-26.
53. Wang K.K., Posmantur R., Nath R., McGinnis K., Whitton M., Talanian R.V., Glantz S.B., Morrow J.S. Simultaneous degradation of αII- and βII-spectrin by caspase 3 (CPP32) in apoptotic cells. J. Biol. Chem. 273:1998;22490-22497.
54. Weaver C.E. Jr., Park-Chung M., Gibbs T.T., Farb D.H. 17β-estradiol protects against NMDA-induced excitotoxicity by direct inhibition of NMDA receptors. Brain Res. 761:1997;338-341.
55. Wong A., Cortopassi G. Mtdna mutations confer cellular sensitivity to oxidant stress that is partially rescued by calcium depletion and cyclosporin A. Biochem. Biophys. Res. Commun. 239:1997;139-145.
56. Varghese J., Radhika G., Sarin A. The role of calpain in caspase activation during etoposide induced apoptosis in T cells. Eur. J. Immunol. 31:2001;2035-2041.
57. Yamaji T., Kagaya A., Uchitomi Y., Yokota N., Yamawaki S. Chronic treatment with antidepressants, verapamil, or lithium inhibits the serotonin-induced intracellular calcium response in individual c6 rat glioma cells. Life Sci. 60:1997;817-823.
58. Yanagisawa K., Sato S., Amaya N., Miyatake T. Degradation of myelin basic protein by calcium-activated neutral protease in human brain and inhibition by E-64 analogue. Neurochem. Res. 8:1983;1285-1293.