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Volume 17, Number 8, Issue of April 15, 1997 pp. 2653-2657
Copyright ©1997 Society for Neuroscience

Widespread Peroxynitrite-Mediated Damage in Alzheimer's Disease

Received Aug. 26, 1996; accepted Jan. 22, 1997.

Mark A. Smith1, Peggy L. Richey Harris1, Lawrence M. Sayre2, Joseph S. Beckman3, and George Perry1

1 Institute of Pathology and 2 Department of Chemistry, Case Western Reserve University, Cleveland, Ohio 44106, and 3 Department of Anesthesiology, School of Medicine, University of Alabama, Birmingham, Alabama 35233

Increasing evidence suggests that oxidative damage to proteins and other macromolecules is a salient feature of the pathology of Alzheimer's disease. Establishing the source of oxidants is key to understanding what role they play in the pathogenesis of Alzheimer's disease, and one way to examine this issue is to determine which oxidants are involved in damage.

In this study, we examine whether peroxynitrite, a powerful oxidant produced from the reaction of superoxide with nitric oxide, is involved in Alzheimer's disease. Peroxynitrite is a source of hydroxyl radical-like reactivity, and it directly oxidizes proteins and other macromolecules with resultant carbonyl formation from side-chain and peptide-bond cleavage. Although carbonyl formation is a major oxidative modification induced by peroxynitrite, nitration of tyrosine residues is an indicator of peroxynitrite involvement. In brain tissue from cases of Alzheimer's disease, we found increased protein nitration in neurons, including but certainly not restricted to those containing neurofibrillary tangles (NFTs). Conversely, nitrotyrosine was undetectable in the cerebral cortex of age-matched control brains. This distribution is essentially identical to that of free carbonyls.

These findings provide strong evidence that peroxynitrite is involved in oxidative damage of Alzheimer's disease. Moreover, the widespread occurrence of nitrotyrosine in neurons suggests that oxidative damage is not restricted to long-lived polymers such as NFTs, but instead reflects a generalized oxidative stress that is important in disease pathogenesis.

Key words: Alzheimer's disease; carbonyls; glycation; nitrotyrosine; oxidative stress; protein modification




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J. E. Duda, B. I. Giasson, Q. Chen, T. L. Gur, H. I. Hurtig, M. B. Stern, S. M. Gollomp, H. Ischiropoulos, V. M.-Y. Lee, and J. Q. Trojanowski
Widespread Nitration of Pathological Inclusions in Neurodegenerative Synucleinopathies
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Subacute NO generation induced by Alzheimer's {beta}-amyloid in the living brain: reversal by inhibition of the inducible NO synthase
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C.-i. Lee, X. Liu, and J. L. Zweier
Regulation of Xanthine Oxidase by Nitric Oxide and Peroxynitrite
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K. T. Akama and L. J. Van Eldik
beta -Amyloid Stimulation of Inducible Nitric-oxide Synthase in Astrocytes Is Interleukin-1beta - and Tumor Necrosis Factor-alpha (TNFalpha )-dependent, and Involves a TNFalpha Receptor-associated Factor- and NFkappa B-inducing Kinase-dependent Signaling Mechanism
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A. Takeda, G. Perry, N. G. Abraham, B. E. Dwyer, R. K. Kutty, J. T. Laitinen, R. B. Petersen, and M. A. Smith
Overexpression of Heme Oxygenase in Neuronal Cells, the Possible Interaction with Tau
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Y. Christen
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P. Baron, D. Galimberti, L. Meda, E. Prat, E. Scarpini, G. Conti, M. Moggio, A. Prelle, and G. Scarlato
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J. A. Hinson, S. L. Michael, S. G. Ault, and N. R. Pumford
Western Blot Analysis for Nitrotyrosine Protein Adducts in Livers of Saline-Treated and Acetaminophen-Treated Mice
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D. G. Munoz and H. Feldman
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G. Bartzokis, D. Sultzer, J. Cummings, L. E. Holt, D. B. Hance, V. W. Henderson, and J. Mintz
In Vivo Evaluation of Brain Iron in Alzheimer Disease Using Magnetic Resonance Imaging
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Peroxynitrite Inactivates Tryptophan Hydroxylase via Sulfhydryl Oxidation. COINCIDENT NITRATION OF ENZYME TYROSYL RESIDUES HAS MINIMAL IMPACT ON CATALYTIC ACTIVITY
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Y. Rong, S. R. Doctrow, G. Tocco, and M. Baudry
EUK-134, a synthetic superoxide dismutase and catalase mimetic, prevents oxidative stress and attenuates kainate-induced neuropathology
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R. W. Vandivier, A. Eidsath, S. M. Banks, H. L. Preas II, S. B. Leighton, P. J. Godin, A. F. Suffredini, and R. L. Danner
Down-Regulation of Nitric Oxide Production by Ibuprofen in Human Volunteers
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S. I. Dikalov, M. P. Vitek, K. R. Maples, and R. P. Mason
Amyloid beta  Peptides Do Not Form Peptide-derived Free Radicals Spontaneously, but Can Enhance Metal-catalyzed Oxidation of Hydroxylamines to Nitroxides
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In Vivo Disposition of 3-Nitro-L-Tyrosine in Rats: Implications on Tracking Systemic Peroxynitrite Exposure
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A. Nunomura, G. Perry, M. A. Pappolla, R. Wade, K. Hirai, S. Chiba, and M. A. Smith
RNA Oxidation Is a Prominent Feature of Vulnerable Neurons in Alzheimer's Disease
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Increased poly(ADP-ribosyl)ation of nuclear proteins in Alzheimer's disease
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K. Hensley, M. L. Maidt, Z. Yu, H. Sang, W. R. Markesbery, and R. A. Floyd
Electrochemical Analysis of Protein Nitrotyrosine and Dityrosine in the Alzheimer Brain Indicates Region-Specific Accumulation
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G. M. Murphy Jr., L. Yang, and B. Cordell
Macrophage Colony-stimulating Factor Augments beta -Amyloid-induced Interleukin-1, Interleukin-6, and Nitric Oxide Production by Microglial Cells
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N. Y. Calingasan, L. C. H. Park, L. L. Calo, R. R. Trifiletti, S. E. Gandy, and G. E. Gibson
Induction of Nitric Oxide Synthase and Microglial Responses Precede Selective Cell Death Induced by Chronic Impairment of Oxidative Metabolism
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Inactivation of tyrosine hydroxylase by nitration following exposure to peroxynitrite and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)
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D. R. McDonald, M. E. Bamberger, C. K. Combs, and G. E. Landreth
beta -Amyloid Fibrils Activate Parallel Mitogen-Activated Protein Kinase Pathways in Microglia and THP1 Monocytes
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Nitric Oxide-Dependent Production of cGMP Supports the Survival of Rat Embryonic Motor Neurons Cultured with Brain-Derived Neurotrophic Factor
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Amyloid beta -peptide stimulates nitric oxide production in astrocytes through an NFkappa B-dependent mechanism
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M. A. Smith, L. M. Sayre, V. E. Anderson, P. L.R. Harris, M. F. Beal, N. Kowall, and G. Perry
Cytochemical Demonstration of Oxidative Damage in Alzheimer Disease by Immunochemical Enhancement of the Carbonyl Reaction with 2,4-Dinitrophenylhydrazine
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A. G. Estevez, N. Spear, S. M. Manuel, R. Radi, C. E. Henderson, L. Barbeito, and J. S. Beckman
Nitric Oxide and Superoxide Contribute to Motor Neuron Apoptosis Induced by Trophic Factor Deprivation
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Uric acid, a natural scavenger of peroxynitrite, in experimental allergic encephalomyelitis and multiple sclerosis
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J. N. Keller, M. S. Kindy, F. W. Holtsberg, D. K. St. Clair, H.-C. Yen, A. Germeyer, S. M. Steiner, A. J. Bruce-Keller, J. B. Hutchins, and M. P. Mattson
Mitochondrial Manganese Superoxide Dismutase Prevents Neural Apoptosis and Reduces Ischemic Brain Injury: Suppression of Peroxynitrite Production, Lipid Peroxidation, and Mitochondrial Dysfunction
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J. H. Morrison and P. R. Hof
Life and Death of Neurons in the Aging Brain
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Iron accumulation in Alzheimer disease is a source of redox-generated free radicals
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M. P. Cuajungco, L. E. Goldstein, A. Nunomura, M. A. Smith, J. T. Lim, C. S. Atwood, X. Huang, Y. W. Farrag, G. Perry, and A. I. Bush
Evidence that the beta -Amyloid Plaques of Alzheimer's Disease Represent the Redox-silencing and Entombment of Abeta by Zinc
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J. M. Souza, B. I. Giasson, Q. Chen, V. M.-Y. Lee, and H. Ischiropoulos
Dityrosine Cross-linking Promotes Formation of Stable alpha -Synuclein Polymers. IMPLICATION OF NITRATIVE AND OXIDATIVE STRESS IN THE PATHOGENESIS OF NEURODEGENERATIVE SYNUCLEINOPATHIES
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W. Wang, S. Wang, L. Yan, P. Madara, A. Del Pilar Cintron, R. A. Wesley, and R. L. Danner
Superoxide Production and Reactive Oxygen Species Signaling by Endothelial Nitric-oxide Synthase
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M. J. LaDu, J. A. Shah, C. A. Reardon, G. S. Getz, G. Bu, J. Hu, L. Guo, and L. J. Van Eldik
Apolipoprotein E Receptors Mediate the Effects of beta -Amyloid on Astrocyte Cultures
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