Bcl-2 protects isolated plasma and mitochondrial membranes against lipid peroxidation induced by hydrogen peroxide and amyloid β-peptide

Journal of Neurochemistry

Volumn 70, Issue 1, 1998, Pages 31-39

  Bruce Keller, Annadora J ^a   Begley, James G ^a   Fu, Weiming ^a   Butterfield, D Allan ^a,b   Bredesen, Dale E ^c   Hutchins, James B ^d   Hensley, Kenneth ^b   Mattson, Mark P ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c BURNHAM INSTITUTE   (United States)

^d UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

Alzheimer's disease; Apoptosis; Electron paramagnetic resonance spectroscopy; Free radicals; Spin labeling

Indexed keywords

AMYLOID BETA PROTEIN; ANTIOXIDANT; GLUTATHIONE; HYDROGEN PEROXIDE; PROTEIN BCL 2; STEARIC ACID; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ALZHEIMER DISEASE; AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; LIPID PEROXIDATION; MITOCHONDRIAL MEMBRANE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTO ONCOGENE; RAT; SPIN LABELING;

ANIMALIA;

EID: 0031962324     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.70010031.x     Document Type: Article

References (47)

1. Behl C., Davis J., Lesley R., and Schubert D. (1994) Hydrogen peroxide mediates amyloid β amyloid toxicity. Cell 77, 817-827.
2. Borner C., Martinou I., Mattman C., Irmler M., Schaerer E., Martinou J.-C., and Tschopp J. (1994) The protein bcl-2 does not require membrane attachment, but two conserved domains to suppress apoptosis. J. Cell Biol. 126, 1059-1068.
3. Butterfield D. A. (1982) Spin labeling in disease. Biol. Magn. Reson. 4, 1-78.
4. Butterfield D. A., Hensley K., Harris M., Mattson M., and Carney J. (1994) β-Amyloid peptide free radical fragments initiate synaptosomal lipoperoxidation in a sequence specific fashion: implications to Alzheimer's disease. Biochem. Biophys. Res. Commun. 200, 710-715.
5. Carrillo M. C., Kanai S., Nukubo M., and Kitani K. (1991) (-) Deprenyl induces activities of both superoxide dismutase and catalase, but not glutathione peroxidase in the striatum of young male rats. Life Sci. 48, 517-521.
6. Chan P. H. (1994) Oxygen radicals in focal cerebral ischemia. Brain Pathol. 4, 59-65.
7. Eady J. J., Orta T., Dennis M. F., Stratford M. R. L., and Peacock J. H. (1995) Glutathione determination by the Tietze enzymatic recycling assay and its relationship to cellular radiation response. Br. J. Cancer 72, 1089-1095.
8. Ellerby L. M., Ellerby H. M., Park S. M., Holleran A. L., Murphy A. N., Fiskum G., Kane D. J., Testa M. P., Kayalar C., and Bredesen D. E. (1996) Shift of the cellular oxidation-reduction potential in neural cells expressing Bcl-2. J. Neurochem. 67, 1259-1267.
9. Forrest V. J., Kang Y. H., McClain D. E., Robinson D. H., and Ramakrishnan N. (1994) Oxidative stress-induced apoptosis prevented by Trolox. Free Radic. Biol. Med. 16, 675-684.
10. Garcia I., Martinou I., Tsujimoto Y., and Martinou J. C. (1992) Prevention of programmed cell death of sympathetic neurons by bcl-2 proto-oncogene. Science 258, 302-304.
11. Goodman Y., Bruce A. J., Cheng B., and Mattson M. P. (1996) Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid β-peptide toxicity in hippocampal neurons. J. Neurochem. 66, 1836-1844.
12. Guo Q., Sopher B. L., Pham D. G., Furukawa K., Robinson N., Martin G. M., and Mattson M. P. (1997) Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid β-peptide: involvement of calcium and oxyradicals. J. Neurosci. 17, 4212-4222.
13. Hall N. C., Carney J. M., Cheng M. S., and Butterfield D. A. (1994) Ischemia/reperfusion-induced changes in membrane proteins and lipids of gerbil cortical synaptosomes. Neuroscience 64, 81-89.
14. Hensley K., Carney J., Hall N., Shaw W., and Butterfield D. A. (1994) Electron paramagnetic resonance investigations of free radical-induced alterations in neocortical synaptosomal membrane protein infrastructure. Free Radic. Biol. Med. 17, 321-331.
15. Hockenbery D. M., Oltvai Z. N., Xiao-Ming Y., Milliman C. L., and Korsmeyer S. J. (1993) Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75, 241-251.
16. Jacobson M. D. and Raff M. C. (1995) Programmed cell death and Bcl-2 protection in very low oxygen. Nature 374, 814-816.
17. Jacobson M. D., Burne J. F., King M. P., Miyashita T., Reed J. C., and Raff M. C. (1993) Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA. Nature 361, 365-369.
18. Kane D. J., Sarafian T. A., Anton R., Hahn H., Gralla E. B., Valentine J. S., Ord T., and Bredesen D. E. (1993) Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 262, 1274-1277.
19. Kostyuk V. A. and Potapovich A. I. (1989) Superoxide-driven oxidation of quercetin and a simple assay for determination of superoxide dismutase. Biochem. Int. 19, 1117-1124.
20. Krafewski S., Tanaka S., Takayama S., Schibler M. J., Fenton W., and Reed J. C. (1993) Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res. 53, 4701-4714.
21. Kruman I., Bruce-Keller A. J., Bredesen D. E., Waeg G., and Mattson M. P. (1997) Evidence that 4-hydroxynonenal mediates oxidative stress-induced apoptosis. J. Neurosci. 17, 5097-5108.
22. 2+ fluxes. Proc. Natl. Acad. Sci. USA 91, 6569-6573.
23. Linnik M. D., Zobrist R. H., and Hatfield M. D. (1993) Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24, 2002-2009.
24. Lithgow T., van Driel R., Bertram J. F., and Strasser A. (1994) The protein product of the oncogene bcl-2 is a component of the nuclear envelope, the endoplasmic reticulum, and the outer mitochondrial membrane. Cell Growth Differ. 5, 411-417.
25. Loo D. T., Copani A., Pike C. J., Whittemore E. R., Walencewicz A. J., and Cotman C. W. (1993) Apoptosis is induced by beta-amyloid in cultured central nervous system neurons. Proc. Natl. Acad. Sci. USA 90, 7951-7955.
26. MacManus J. P., Buchan A. M., Hill I. E., Rasquinha I., and Preston E. (1993) Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci. Lett. 164, 89-92.
27. Mah S. P., Zhong L. T., Liu Y., Roghani A., Edwards R. H., and Bredesen D. E. (1993) The protooncogene bcl-2 inhibits apoptosis in PC12 cells. J. Neurochem. 60, 1183-1186.
28. 2+ homeostasis and cell death. J. Neurosci. 15, 6239-6249.
29. Mark R. J., Lovell M. A., Markesbery W. R., Uchida K., and Mattson M. P. (1997a) A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death by amyloid β-peptide. J. Neurochem. 68, 255-264.
30. Mark R. J., Pang Z., Geddes J. W., Uchida K., and Mattson M. P. (1997b) Amyloid β-peptide impairs glucose uptake in hippocampal and cortical neurons; involvement of membrane lipid peroxidation. J. Neurosci. 17, 1046-1054.
31. Mason R. P., Estermeier J. D., Kelly J. S., and Mason P. E. (1996) Alzheimer's disease amyloid β-peptide 25-35 is located in the membrane hydrocarbon core: x-ray diffraction analyses. Biochem. Biophys. Res. Commun. 222, 78-82.
32. Murphy A. N., Bredesen D. E., Cortopassi G., Wang E., and Fiskum G. (1996) Bcl-2 potentiates the maximal calcium capacity of neural cell mitochondria. Proc. Natl. Acad. Sci. USA 93, 9893-9898.
33. Myers K. M., Fiskum G., Liu Y., Simmens S. J., Bredesen D. E., and Murphy A. N. (1995) Bcl-2 protects neural cells from cyanide/aglycemia-induced lipid oxidation, mitochondrial injury, and loss of viability. J. Neurochem. 65, 2432-2440.
34. Newmeyer D. G., Farschon D. M., and Reed J. C. (1994) Cell-free apoptosis in xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79, 353-364.
35. Nguyen M., Branton P. E., Walton P. A., Oltvai Z. N., Korsmeyer S. J., and Shore G. C. (1994) Role of membrane anchor domain of Bcl-2 in suppression of apoptosis caused by E1B-defective adenovirus. J. Biol. Chem. 269, 16521-16528.
36. Paglia D. E. and Valentine W. N. (1967) Studies on the qualitative and quantitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Invest. 70, 158-169.
37. Petit P. X., Susin S. A., Zamzami N., Mignotte B., and Kroemer G. (1996) Mitochondria and programmed cell death - back to the future. FEBS Lett. 396, 7-13.
38. Reed J. C. (1994) Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124, 1-6.
39. Richter C., Schweizer M., Cossarizza A., and Franceschi C. (1996) Control of apoptosis by the cellular ATP level. FEBS Lett. 378, 107-110.
40. Sentman C. L., Shutter J. R., Hockenbery D., Kanagawa O., and Korsmeyer S. J. (1991) bcl-2 inhibits multiple forms of apoptosis but not negative selection in thymocytes. Cell 67, 879-888.
41. Srinivasan A., Foster L. M., Testa M.-P., Ord T., Keane R. W., Bredesen D. E., and Kayalar C. (1996) Bcl-2 expression in neural cells blocks activation of ICE/CED-3 family proteases during apoptosis. J. Neurosci. 16, 5654-5660.
42. Su J. H., Anderson A. J., Cummings B., and Cotman C. W. (1994) Immunocytochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 5, 2529-2533.
43. Whittemore E. R., Loo D. T., and Cotman C. W. (1994) Exposure to hydrogen peroxide induces cell death via apoptosis in cultured rat cortical neurons. Neuroreport 5, 1485-1488.
44. Zaleska M. M., Nagy K., and Floyd R. A. (1989) Iron-induced lipid peroxidation and inhibition of dopamine synthesis in striatal synaptosomes. Neurochem. Res. 14, 597-605.
45. 0 ATPase δ-subunit is regulated by platelet-derived growth factor in mouse cortical neurons in vitro. J. Neurochem. 65, 2812-2815.
46. Zhong L. T., Kane D. J., and Bredesen D. E. (1993) Bcl-2 blocks glutamate toxicity in neural cell lines. Mol. Brain Res. 19, 353-355.
47. Zhou Y., Gopalakrishnan V., and Richardson J. S. (1996) Actions of neurotoxic β-amyloid on calcium homeostasis and viability of PC12 cells are blocked by antioxidants but not by calcium channel antagonists. J. Neurochem. 67, 1419-1425.