β-Amyloid neurotoxicity in vitro: Evidence of oxidative stress but not protection by antioxidants

Journal of Neurochemistry

Volumn 69, Issue 4, 1997, Pages 1601-1611

  Pike, Christian J ^a   Ramezan Arab, Nima ^a   Cotman, Carl W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer's disease; Antioxidants; Free radicals; Lipid peroxidation; Oxidative stress; Amyloid

Indexed keywords

AMYLOID BETA PROTEIN; ANTIOXIDANT; GALLIC ACID PROPYL ESTER; HYDROGEN PEROXIDE; IRON; PROBUCOL; PROMETHAZINE; REACTIVE OXYGEN METABOLITE; TERT BUTYL HYDROPEROXIDE; TROLOX C;

ALZHEIMER DISEASE; ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN PROTECTION; CHROMOSOME 21; CONTROLLED STUDY; IRON OVERLOAD; LIPID PEROXIDATION; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANIMALIA;

EID: 0030924506     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1997.69041601.x     Document Type: Article

References (73)

1. Araujo D. M. and Cotman C. W. (1992) β-Amyloid stimulates glial cells in vitro to produce growth factors that accumulate in senile plaques in Alzheimer's disease. Brain Res. 569, 141-145.
2. Arispe N., Pollard H. B., and Rojas E. (1993) Giant multilevel cation channels formed by Alzheimer's disease amyloid β-protein [AβP-(1-40 )] in bilayer membranes. Proc. Natl. Acad. Sci. USA 90, 10573-10577.
3. Behl C., Davis J., Cole G. M., and Schubert D. (1992) Vitamin E protects nerve cells from amyloid β protein toxicity. Biochem. Biophys. Res. Commun. 186, 944-950.
4. Behl C., Davis J. B., Klier F. G., and Schubert D. (1994a) Amyloid β peptide induces necrosis rather than apoptosis. Brain Res. 645, 253-264.
5. Behl C., Davis J. B., Lesley R., and Schubert D. (1994b) Hydrogen peroxide mediates amyloid β protein toxicity. Cell 77, 817-827.
6. Bottenstein J. H. and Sato G. H. (1979) Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc. Natl. Acad. Sci. USA 76, 514-517.
7. Brewer G. L. and Cotman C. W. (1989) Survival and growth of hippocampal neurons in defined medium at low density: advantages of a sandwich culture technique or low oxygen. Brain Res. 494, 65-74.
8. Bridges A. B., Scott N. A., and Belch J. J. F. (1991) Probucol, a superoxide free radical scavenger in vitro. Atherosclerosis 89, 263-265.
9. Bruce A. J., Malfroy B., and Baudry M. (1996) β-Amyloid toxicity in organotypic hippocampal cultures: protection by EUK-8, a synthetic catalytic free radical scavenger. Proc. Natl. Acad. Sci. USA 93, 2312-2316.
10. Buc-Calderon P., Latour I., and Roberfroid M. (1991) Biochemical changes in isolated hepatocytes exposed to tert-butyl hydroperoxide. Implications for its cytotoxicity. Cell Biol. Toxicol. 7, 129-143.
11. Burdick D., Soreghan B., Kwon M., Kosmoski J., Knauer M., Henschen A., Yates J., Cotman C., and Glabe C. (1992) Assembly and aggregation properties of synthetic Alzheimer's A4/β amyloid peptide analogs. J. Biol. Chem. 267, 546-554.
12. Busciglio J., Lorenzo A., and Yankner B. A. (1992) Methodological variables in the assessment of beta amyloid neurotoxicity. Neurobiol. Aging 13, 609-612.
13. Busciglio J., Yeh J., and Yankner B. A. (1993) β-Amyloid neurotoxicity in human cortical culture is not mediated by excitotoxins. J. Neurochem. 61, 1565-1568.
14. 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.
15. Café C., Torri C., Bretorelli L., Angeretti N., Lucca E., Forloni G., and Marzatico F. (1996) Oxidative stress after acute and chronic application of β-amyloid fragment 25-35 in cortical cultures. Neurosci. Lett. 203, 61-65.
16. Canning D. R., McKeon R. J., DeWitt D. A., Perry G., Wujek J. R., Frederickson R. C. A., and Silver J. (1993) β-Amyloid of Alzheimer's disease induces reactive gliosis that inhibits axonal outgrowth. Exp. Neurol. 124, 289-298.
17. Chow H. S., Lynch J. J. I., Rose K., and Choi D. W. (1994) Trolox attenuates cortical neuronal injury induced by iron, ultraviolet light, glucose deprivation, or AMPA. Brain Res. 639, 102-108.
18. Colton C. A., Pagan F., Snell J., Cummins A., and Gilbert D. L. (1995) Protection from oxidation enhances the survival of cultured mesencephalic neurons. Exp. Neurol. 132, 54-61.
19. Copani A., Koh J.-Y., and Cotman C. W. (1991) β-Amyloid increases neuronal susceptibility to injury by glucose deprivation. Neuroreport 2, 763-765.
20. Cotman C. W. and Pike C. J. (1994) β-Amyloid and its contributions to neurodegeneration in Alzheimer's disease, in Alzheimer's Disease (Terry R. D., Katzman R., and Bick K., eds), pp. 305-315. Raven Press, New York.
21. Cribbs D. H., Kreng V. M., Anderson A. J., and Cotman C. W. (1996) Cross-linking of concanavalin A receptors on cortical neurons induces programmed cell death. Neuroscience 75, 173-185.
22. Cummings B. J., Pike C. J., Shankle S., and Cotman C. W. (1996) β-Amyloid deposition and other measures of neuropathology predict cognitive status in Alzheimer's disease. Neurobiol. Aging 17, 921-933.
23. Dyrks T., Dyrks E., Hartmann T., Masters C., and Beyreuther K. (1992) Amyloidogenicity of βA4 and βA4-bearing amyloid protein precursor fragments by metal-catalyzed oxidation. J. Biol. Chem. 267, 18210-18217.
24. Forloni G., Chiesa R., Smiroldo S., Verga L., Salmona M., Tagliavini F., and Angeretti N. (1993) Apoptosis mediated neurotoxicity induced by chronic application of β amyloid fragment 25-35. Neuroreport 4, 523-526.
25. Good G. A. and Murphy R. M. (1995) Aggregation state-dependent binding of β-amyloid peptide to protein and lipid components of rat cortical homogenates. Biochem. Biophys. Res. Commun. 207, 209-215.
26. Harris M. E., Hensley K., Butterfield D. A., Leedle R. A., and Carney J. M. (1995) Direct evidence of oxidative injury produced by the Alzheimer's β-amyloid peptide (1-40) in cultured hippocampal neurons. Exp. Neurol. 131, 193-202.
27. Hensley K., Carney J. M., Mattson M. P., Aksenova M., Harris M., Wu J. F., Floyd R. A., and Butterfield D. A. (1994) A model for β-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: relevance to Alzheimer's disease. Proc. Natl. Acad. Sci. USA 91, 3270-3274.
28. Hiramatsu M., Liu J., Edamatsu R., Ohba S., Kadowaki D., and Mori A. (1994) Probucol scavenged 1,1-diphenyl-2-picrylhydrazyl radicals and inhibited formation of thiobarbituric acid reactive substances. Free Radic. Biol. Med. 16, 201-206.
29. Jeding I., Evans P. J., Akanmu D., Dexter D., Spencer J. D., Aruoma O. I., Jenner P., and Halliwell I. (1995) Characterization of the potential antioxidant and pro-oxidant actions of some neuroleptic drugs. Biochem. Pharmacol. 49, 359-365.
30. Koh J.-Y., Yang L. L., and Cotman C. W. (1990) β-Amyloid protein increases the vulnerability of cultured cortical neurons to excitotoxic damage. Brain Res. 533, 315-320.
31. 25-35 peptide-mediated neurotoxicity in rat hippocampal cultures. J. Neurosci. Res. 39, 494-505.
32. Loo D. T., Copani A., Pike C. J., Whittemore E. R., Walencewicz A. J., and Cotman C. W. (1993) Apoptosis is induced by β-amyloid in cultured central nervous system neurons. Proc. Natl. Acad. Sci. USA 90, 7951-7955.
33. Lorenzo A. and Yankner B. A. (1994) β-Amyloid neurotoxicity requires fibril formation and is inhibited by Congo red. Proc. Natl. Acad. Sci. USA 91, 12243-12247.
34. Lovell M. A., Ehmann W. D., Butler S. M., and Markesbery W. R. (1995) Elevated thiobarbituric acid-reactive substances and antioxidant enzyme activity in the brain in Alzheimer's disease. Neurology 45, 1594-1601.
35. Mark R. J., Blanc E. M., and Mattson M. P. (1996) Amyloid β-peptide and oxidative cellular injury in Alzheimer's disease. Mol Neurobiol. 12, 211-224.
36. 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 induced by amyloid β-peptide. J. Neurochem. 68, 255-264.
37. Mark R. J., Pang Z., Geddes J. W., Uchida K., and Mattson M. P. (1997b) Amyloid β-peptide impairs glucose transport in hippocampal and cortical neurons: involvement of membrane lipid peroxidation. J. Neurosci. 17, 1046-1054.
38. Mattson M. P. and Goodman Y. (1995) Different amyloidogenic peptides share a similar mechanism of neurotoxicity involving reactive oxygen species and calcium. Brain Res. 676, 219-224.
39. Mattson M. P., Cheng B., Davis D., Bryant K., Lieberburg L. and Rydel R. (1992) β-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J. Neurosci. 12, 376-389.
40. Mattson M. P., Tomaselli K. J., and Rydel R. E. (1993) Calcium-destabilizing and neurodegenerative effects of aggregated β-amyloid peptide are attenuated by basic FGF. Brain Res. 621, 35-49.
41. Mattson M. P., Barger S. W., Begley J. G., and Mark R. J. (1995) Calcium, free radicals, and excitotoxic neuronal death in primary cell culture. Methods Cell Biol. 46, 187-216.
42. McGeer P. L. and McGeer E. G. (1995) The inflammatory response system of brain: implications for therapy of Alzheimer and other neurodegenerative disease. Brain Res. Rev. 21, 195-218.
43. Mirzabekov T., Lin M. C., Yuan W. L., Marshall P. J., Carman M., Tomaselli K., Lieberburg I., and Kagan B. L. (1994) Channel formation in planar lipid bilayers by a neurotoxic fragment of the beta-amyloid peptide. Biochem. Biophvs. Res. Commun. 202, 1142-1148.
44. Ohkawa H., Ohishi N., and Yagi K. (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95, 351-358.
45. Pappolla M. A., Omar R. A., Kim K. S., and Robakis N. K. (1992) Immunohistochemical evidence of antioxidant stress in Alzheimer's disease. Am. J. Pathol. 140, 621-628.
46. Pike C. J., Walencewicz A. J., Glabe C. G., and Cotman C. W. (1991) In vitro aging of β-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res. 563, 311-314.
47. Pike C. J., Cummings B. J., and Cotman C. W. (1992) β-Amyloid induces neuritic dystrophy in vitro: similarities with Alzheimer pathology. Neuroreport 3, 769-772.
48. Pike C. J., Burdick D., Walencewicz A. J., Glabe C. G., and Cotman C. W. (1993) Neurodegeneration induced by β-amyloid peptides in vitro: the role of peptide assembly state. J. Neurosci. 13, 1676-1687.
49. Pike C. J., Cummings B. J., Monzavi R., and Cotman C. W. (1994) β-Amyloid-induced changes in cultured astrocytes parallel reactive astrocytosis associated with senile plaques in Alzheimer's disease. Neuroscience 63, 517-531.
50. Pike C. J., Walencewicz-Wasserman A. J., Kosmoski J., Cribbs D. H., Glabe C. G., and Cotman C. W. (1995) Structure-activity analyses of β-amyloid peptides: contributions of the β25-35 region to aggregation and neurotoxicity. J. Neurochem. 64, 253-265.
51. Pike C. J., Vaughan P. J., Cunningham D. D., and Cotman C. W. (1996) Thrombin attenuates neuronal cell death and modulates astrocyte reactivity induced by β-amyloid in vitro. J. Neurochem. 66, 1374-1382.
52. Premkumar D. R. D., Smith M. A., Richey P. L., Petersen R. B., Castellani R., Kutty R. K., Wiggert B., Perry G., and Kalaria R. N. (1995) Induction of heme oxygenase-1 mRNA and protein in neocortex and cerebral vessels in Alzheimer's disease. J. Neurochem. 65, 1399-1402.
53. Probst A., Brunnschweiler H., Lautenschlager C., and Ulrich J. (1987) A special type of senile plaque, possibly an initial stage. Acta Neuropathol. 74, 133-141.
54. Rogers J., Webster S., Lue L. F., Brachova L., Civin W. H., Emmerling M., Shivers B., Walker D., and McGeer P. (1996) Inflammation and Alzheimer's disease pathogenesis. Neurobiol. Aging 17, 681-686.
55. Rozemuller J. M., Eikelenboom P., Stam F. C., Beyreuther K., and Masters C. L. (1989) A4 protein in Alzheimer's disease: primary and secondary cellular events in extracellular amyloid deposition. J. Neuropathol. Exp. Neurol 48, 674-691.
56. Sano M., Ernesto C., Thomas R. G., Klauber M. R., Schaffer K., Grundman M., Woodbury P., Growdon J., Cotman C. W., Pfeiffer E., Schneider L. S., and Thai L. J. (1997) A controlled trial of selegiline, alpha-tocopherol, or both as treatment for Alzheimer's disease. N. Engl. J. Med. 336, 1216-1222.
57. Schubert D. and Chevion M. (1995) The role of iron in beta amyloid toxicity. Biochem. Biophys. Res. Commun. 216, 702-707.
58. Schubert D., Behl C., Leley R., Brack A., Dargusch R., Sagara Y., and Kimura H. (1995) Amyloid peptides are toxic via a common oxidative mechanism. Proc. Natl. Acad. Sci. USA 92, 1989-1993.
59. Selkoe D. J. (1996) Amyloid β-protein and the genetics of Alzheimer's disease. J. Biol. Chem. 271, 18295-18298.
60. Simmons L. K., May P. C., Tomaselli K. J., Rydel R. E., Fuson K. S., Brigham E. F., Wright S., Lieberburg I., Becker G. W., Brems D. N., and Li W. Y. (1994) Secondary structure of amyloid β peptide correlates with neurotoxic activity in vitro. Mol. Pharmacol. 45, 373-379.
61. Smith C. D., Carney J. M., Starke-Reed P. E., Oliver C. N., Stadtman E. R., Floyd R. A., and Markesbery W. R. (1991) Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer's disease. Proc. Natl. Acad. Sci. USA 88, 10540-10543.
62. Smith M. A., Sayre L. M., Monnier V. M., and Perry G. (1995) Radical AGEing in Alzheimer's disease. Trends Neurosci. 18, 172-176.
63. Smith M. A., Richey Harris P. L., Sayre L. M., Beckman J. S., and Perry G. (1997) Widespread peroxynitrite-mediated damage in Alzheimer's disease. J. Neurosci. 17, 2653-2657.
64. Terzi E., Holzemann G., and Seelig J. (1995) Self-association of beta-amyloid peptide (1-40) in solution and binding to lipid membranes. J. Mol. Biol. 252, 633-642.
65. Thomas T., Thomas G., McLendon C., Sutton T., and Mullan M. (1996) β-Amyloid-mediated vasoactivity and vascular endothelial damage. Nature 380, 168-171.
66. Tomiyama T., Shoji A., Kataoka K., Suwa Y., Asano S., Kaneko H., and Endo N. (1996) Inhibition of amyloid β protein aggregation and neurotoxicity by rifampicin. J. Biol. Chem. 271, 6839-6844.
67. Van Nostrand W. E., Davis-Salinas J., and Saporito-Irwin S. M. (1996) Amyloid β-protein induces the cerebrovascular cellular pathology of Alzheimer's disease and related disorders. Ann. NY Acad. Sci. 777, 297-302.
68. 2+ channel blockers attenuate β-amyloid peptide toxicity to cortical neurons in culture. J. Neurochem. 62, 372-375.
69. Wisniewski H. M. and Terry R. D. (1973) Reexamination of the pathogenesis of the senile plaque, in Progress in Neuropathology (Zimmerman H. M., ed), pp. 1-26. Grune and Stratton, New York.
70. Wu T. W., Fung K. P., Zeng L. H., Wu J., and Nakamura H. (1994) Propyl gallate as a hepatoprotector in vitro and in vivo. Biochem. Pharmacol. 48, 419-422.
71. Yan S. D., Chen X., Fu J., Chen M., Zhu H., Roher A., Slattery T., Zhao L., Nagashima M., Morser J., Migheli A., Nawroth P., Stern D., and Schmidt A. M. (1996) RAGE and amyloid-β peptide neurotoxicity in Alzheimer's disease. Nature 382, 685-691.
72. Yankner B. A. (1996) Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 16, 921-932.
73. 2 generation. J. Neurochem. 67, 1595-1606.