Redox proteomics studies of in vivo amyloid beta-peptide animal models of Alzheimer's disease: Insight into the role of oxidative stress

Proteomics - Clinical Applications

Volumn 2, Issue 5, 2008, Pages 685-696

  Sultana, Rukhsana ^a,b   Butterfield, D Allan ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Alzheimer's disease; AmyIoid beta peptide; Caenorhabditis elegans; Canine; Oxidative stress

Indexed keywords

ACETYLCYSTEINE; ALPHA ENOLASE; AMYLOID BETA PROTEIN; ASPARTIC PROTEINASE; BETA ACTIN; CALBINDIN; CARBONATE DEHYDRATASE II; CATHEPSIN D; CATHEPSIN E; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; CREATINE KINASE; GLUTAMATE AMMONIA LIGASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; LEVACECARNINE; MULTIDRUG RESISTANCE PROTEIN 1; NEUROPOLYPEPTIDE H3; PEPTIDYLPROLYL ISOMERASE PIN1; PHOSPHOGLYCERATE MUTASE; PHOSPHOGLYCERATE MUTASE 1; POLYPEPTIDE; PROTEIN KINASE C GAMMA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE ALPHA; SNARE PROTEIN; THIOCTIC ACID; TRIOSEPHOSPHATE ISOMERASE; UBIQUITIN THIOLESTERASE; UBIQUITIN THIOLESTERASE L 1; VOLTAGE DEPENDENT ANION CHANNEL 1;

ALZHEIMER DISEASE; ANTIOXIDANT ACTIVITY; CAENORHABDITIS ELEGANS; CELL AGGREGATION; CELL CYCLE; CELL DEATH; CELL FUNCTION; CELL PH; COMPARATIVE STUDY; DOG; ENERGY METABOLISM; EXPERIMENTAL ANIMAL; EXPERIMENTAL MOUSE; IMMUNOPRECIPITATION; IN VIVO STUDY; NERVE DEGENERATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEOMICS; REVIEW; RISK REDUCTION; SENESCENCE ACCELERATED MOUSE;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 44649144568     PISSN: 18628346     EISSN: None     Source Type: Journal    
DOI: 10.1002/prca.200780024     Document Type: Review

References (163)

1. Mirra, S. S., Heyman, A., McKeel, D., Sumi, S. M. et al., The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 1991, 41, 479-486.
2. Mattson, M. P., Gary, D. S., Chan, S. L., Duan, W., Perturbed endoplasmic reticulum function, synaptic apoptosis and the pathogenesis of Alzheimer's disease. Biochemical Society Symposium 2001, 151-162.
3. Butterfield, D. A., Hensley, K., Cole, P., Subramaniam, R. et al., Oxidatively induced structural alteration of glutamine synthetase assessed by analysis of spin label incorporation kinetics: relevance to Alzheimer's disease. J. Neurochem. 1997, 68, 2451-2457.
4. Gahtan, E., Overmier, J. B., Inflammatory pathogenesis in Alzheimer's disease: biological mechanisms and cognitive sequeli. Neurosci. Biobehav. Rev. 1999, 23, 615-633.
5. Poon, H. F., Hensley, K., Thongboonkerd, V., Merchant, M. L. et al., Redox proteomics analysis of oxidatively modified proteins in G93A-SOD1 transgenic mice-a model of familial amyotrophic lateral sclerosis. Free Radic. Biol. Med. 2005, 39, 453-462.
6. Masters, C. L., Cappai, R., Barnham, K. J., Villemagne, V. L., Molecular mechanisms for Alzheimer's disease: implications for neuroimaging and therapeutics. J. Neurochem. 2006, 97, 1700-1725.
7. Butterfield, D. A., Drake, J., Pocernich, C., Castegna, A., Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends Mol. Med. 2001, 7, 548-554.
8. Ingelsson, M., Fukumoto, H., Newell, K. L., Growdon, J. H. et al., Early Abeta accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain. Neurology 2004, 62, 925-931.
9. Butterfield, D. A., Stadtman, E. R., Protein oxidation processes in aging brain. Adv. Cell Aging Gerontol. 1997, 2, 161-191.
10. Sies, H., Cadenas, E., Oxidative stress: damage to intact cells and organs, Philos. Trans. R. Soc. Lond. B Biol. Sci. 1985, 311, 617-631.
11. Mikkelsen, R. B., Wardman, P., Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms, Oncogene 2003, 22, 5734-5754.
12. Thannickal, V. J., Day, R. M., Klinz, S. G., Bastien, M. C. et al., Ras-dependent and -independent regulation of reactive oxygen species by mitogenic growth factors and TGF-beta1, FASEB J. 2000, 14, 1741-1748.
13. Aksenov, M. Y., Aksenova, M. V., Butterfield, D. A., Geddes, J. W., Markesbery, W. R., Protein oxidation in the brain in Alzheimer's disease, Neuroscience 2001, 103, 373-383.
14. Baynes, J. W., Thorpe, S. R., Glycoxidation and lipoxidation in atherogenesis, Free Radi. Biol. Med. 2000, 28, 1708-1716.
15. Butterfield, D. A., Amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurode-generation in Alzheimer's disease brain. A review, Free Radic. Res. 2002, 36, 1307-1313.
16. Butterfield, D. A., Perluigi, M., Sultana, R., Oxidative stress in Alzheimer's disease brain: new insights from redox proteomics, Eur. J. Pharmacol. 2006, 545, 39-50.
17. Nakamura, K., Hori T., Sato, N., Sugie, K. et al., Redox regulation of a src family protein tyrosine kinase p56lck in T cells, Oncogene 1993, 8, 3133-3139.
18. Smith, M. A., Perry, G., Alzheimer disease: protein-protein interaction and oxidative stress, Bol. Estud. Med. Biol. 1996, 44, 5-10.
19. Staal, F. J., Anderson, M. T., Staal, G. E., Herzenberg, L. A., Gitler, C., Redox regulation of signal transduction: tyrosine phosphorylation and calcium influx, Proc. Natl. Acad. Sci. USA 1994, 91, 3619-3622.
20. Davies, K. J., Degradation of oxidized proteins by the 20S proteasome, Biochimie 2001, 83, 301-310.
21. Lafon-Cazal, M., Culcasi, M., Gaven, F., Pietri, S., Bockaert, J., Nitric oxide, superoxide and peroxynitrite: putative mediators of NMDA-induced cell death in cerebellar granule cells, Neuropharmacology 1993, 32, 1259-1266.
22. Calabrese, V., Scapagnini, G., Ravagna, A., Bella, R. et al., Disruption of thiol homeostasis and nitrosative stress in the cerebrospinal fluid of patients with active multiple sclerosis: evidence for a protective role of acetylcarnitine, Neurochem. Res. 2003, 28, 1321-1328.
23. Calabrese, V., Sultana, R., Scapagnini, G., Guagliano, E. et al., Nitrosative stress, cellular stress response, and thiol homeostasis in patients with Alzheimer's disease, Antioxid. Redox Signal. 2006, 8, 1975-1986.
24. Uversky, V. N., Yamin, G., Munishkina, L. A., Karymov, M. A. et al., Effects of nitration on the structure and aggregation of alpha-synuclein, Brain Res. 2005, 134, 84-102.
25. Webster, R. P., Macha, S., Brockman, D., Myatt, L., Peroxynitrite treatment in vitro disables catalytic activity of recombinant p38 MAPK, Proteomics 2006, 6, 4838-4844.
26. Levine, R. L., Mosoni, L., Berlett, B. S., Stadtman, E. R. Methionine residues as endogenous antioxidants in proteins, Proc. Natl. Acad. Sci. USA 1996, 93, 15036-15040.
27. Stadtman, E. R., Berlett, B. S., Reactive oxygen-mediated protein oxidation in aging and disease, Chem. Res. Toxicol. 1997, 10, 485-494.
28. Dalle-Donne, I., Scaloni, A., Butterfield, D. A., Redox Proteomics: From protein modifications to cellular dysfunction and diseases, John Wiley and Sons, Hoboken, NJ 2006.
29. Dalle-Donne, I., Scaloni, A., Giustarini, D., Cavarra, E. et al., Proteins as biomarkers of oxidative/nitrosative stress in diseases: the contribution of redox proteomics, Mass Spectrom. Rev. 2005, 24, 55-99.
30. Inai, Y., Nishikimi, M., Increased degradation of oxidized proteins in yeast defective in 26 S proteasome assembly, Arch. Biochem. Biophys. 2002, 404, 279-284.
31. Grune, T., Reinheckel, T., Davies, K. J., Degradation of oxidized proteins in mammalian cells, FASEB J. 1997, 11, 526-534.
32. Stadtman, E. R., Oliver, C. N., Levine, R. L, Fucci, L., Rivett, A. J., Implication of protein oxidation in protein turnover, aging, and oxygen toxicity, Basic Life Sci. 1988, 49, 331-339.
33. Squier, T. C., Oxidative stress and protein aggregation during biological aging, Exp. Gerontol. 2001, 36, 1539-1550.
34. Bader, N., Grune, T., Protein oxidation and proteolysis, Biol. Chem. 2006, 387, 1351-1355.
35. Fucci, L., Oliver, C. N., Coon, M. J., Stadtman, E. R., Inactivation of key metabolic enzymes by mixed-function oxidation reactions: possible implication in protein turnover and ageing, Proc. Natl. Acad. Sci. USA 1983, 80, 1521-1525.
36. Shacter, E., Williams, J. A., Lim, M., Levine, R. L., Differential susceptibility of plasma proteins to oxidative modification: examination by western blot immunoassay, Free Radic. Biol. Med. 1994, 17, 429-437.
37. Keller, J. N., Hanni, K. B., Markesbery, W. H., Impaired proteasome function in Alzheimer's disease, J. Neurochem. 2000, 75, 436-439.
38. Petropoulos, I., Conconi, M., Wang, X., Hoenel, B. et al., Increase of oxidatively modified protein is associated with a decrease of proteasome activity and content in aging epidermal cells, J. Gerontol. A Biol. Sci. Med. Sci. 2000, 55, B220-227.
39. Shringarpure, R., Grune, T., Sitte, N., Davies, K. J., 4-Hydroxynonenal-modified amyloid-beta peptide inhibits the proteasome: possible importance in Alzheimer's disease, Cell. Mol. Life Sci. 2000, 57, 1802-1809.
40. Starke-Reed, P. E., Oliver, C. N., Protein oxidation and proteolysis during aging and oxidative stress, Arch. Biochem. Biophys. 1989, 275, 559-567.
41. Szweda, P. A., Friguet, B., Szweda, L. I., Proteolysis, free radicals, and aging, Free Radic. Biol. Med. 2002, 33, 29-36.
42. Rivett, A. J., Regulation of intracellular protein turnover: covalent modification as a mechanism of marking proteins for degradation, Curr. Top. Cell Regul. 1986, 28, 291-337.
43. Sitte, N., Huber, M., Grune, T., Ladhoff, A. et al., 2000, Proteasome inhibition by lipofuscin/ceroid during postmitotic aging of fibroblasts, FASEB J. 14, 1490-1498.
44. Stadtman, E. R., Levine, H. L., Protein oxidation, Ann. NY Acad Sci. 2000, 899, 191-208.
45. Markesbery, W. H., Oxidative stress hypothesis in Alzheimer's disease, Free Radic. Biol. Med. 1997, 23, 134-147.
46. Butterfield, D. A., beta-Amyloid-associated free radical oxidative stress and neurotoxicity: implications for Alzheimer's disease. Chem. Res. Toxicol. 1997, 10, 495-506.
47. Selkoe, D. J., Alzheimer's disease: genes, proteins, and therapy, Physiol. Rev. 81, 2001, 741-766.
48. Caughey, B., Lansbury, P. T., Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders, Annu. Rev. Neurosci. 2003, 26, 267-298.
49. Yatin, S. M., Varadarajan, S., Link, C. D., Butterfield, D. A., In vitro and in vivo oxidative stress associated with Alzheimer's amyloid beta-peptide (1-42), Neurobiol. Aging 1999, 20, 325-330; discussion 339-342.
50. Boyd-Kimball, D., Sultana, H., Mohmmad-Abdul, H., Butterfield, D. A., Neurotoxicity and oxidative stress in D1M-substituted Alzheimer's A beta(1-42): relevance to N-terminal methionine chemistry in small model peptides, Peptides 2005, 26, 665-673.
51. Sultana, R., Newman, S., Mohmmad-Abdul, H., Keller, J. N., Butterfield, D. A., Protective effect of the xanthate, D609, on Alzheimer's amyloid beta-peptide (1-42)-induced oxidative stress in primary neuronal cells, Free Radic. Res. 2004, 38, 449-458.
52. Drake, J., Link, C. D., Butterfield, D. A., Oxidative stress precedes fibrillar deposition of Alzheimer's disease amyloid beta-peptide (1-42) in a transgenic Caenorhabditis elegans model, Neurobiol. Aging 2003, 24, 415-420.
53. Baglioni, S., Casamenti, F., Bucciantini, M., Luheshi, L. M. et al., Prefibrillar amyloid aggregates could be generic toxins in higher organisms, J. Neurosci. 2006, 26, 8160-8167.
54. Canevari, L., Abramov, A. Y., Duchen, M. R., Toxicity of amyloid beta peptide: tales of calcium, mitochondria, and oxidative stress, Neurochem. Res. 2004, 29, 637-650.
55. Butterfield, D. A., Boyd-Kimball, D., The critical role of methionine 35 in Alzheimer's amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity, Biochim. Biophys. Acta 1703, 2005, 149-156.
56. Boyd-Kimball, D., Sultana, R., Mohmmad-Abdul, H., Butterfield, D. A., Rodent Abeta(1-42) exhibits oxidative stress properties similar to those of human Abeta(1-42): Implications for proposed mechanisms of toxicity, J. Alzheimers Dis. 2004, 6, 515-525.
57. Yatin, S. M., Aksenov, M., Butterfield, D. A., The antioxidant vitamin E modulates amyloid beta-peptide-induced creatine kinase activity inhibition and increased protein oxidation: implications for the free radical hypothesis of Alzheimer's disease, Neurochem. Res. 1999, 24, 427-435.
58. Yatin, S. M., Varadarajan, S., Butterfield, D. A., Vitamin E prevents Alzheimer's amyloid beta-peptide (1-42)-induced neuronal protein oxidation and reactive oxygen species production, J. Alzheimers Dis. 2000, 2, 123-131.
59. Castegna, A., Aksenov, M., Aksenova, M., Thongboonkerd, V. et al., Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1, Free Radic. Biol. Med. 2002, 33, 562-571.
60. Castegna, A., Aksenov, M., Thongboonkerd, V., Klein, J. B. et al., Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71, J. Neurochem. 2002. 82, 1524-1532.
61. Castegna, A., Thongboonkerd, V., Klein, J. B., Lynn, B. et al., Proteomic identification of nitrated proteins in Alzheimer's disease brain, J. Neurochem. 2003, 85, 1394-1401.
62. Perluigi, M., Fai Poon, H., Hensley, K., Pierce, W. M. et al., Proteomic analysis of 4-hydroxy-2-nonenal-modified proteins in G93A-SOD1 transgenic mice-a model of familial amyotrophic lateral sclerosis, Free Radic. Biol. Med. 2005, 38, 960-968.
63. Perluigi, M., Poon, H. F., Maragos, W., Pierce, W. M. et al., Proteomic analysis of protein expression and oxidative modification in r6/2 transgenic mice: a model of Huntington disease, Mol. Cell. Proteomics 2005, 4, 1849-1861.
64. Poon, H. F., Frasier, M., Shreve, N., Calabrese, V. et al., Mitochondrial associated metabolic proteins are selectively oxidized in A30P alpha-synuclein transgenic mice-a model of familial Parkinson's disease, Neurobiol. Dis. 2005, 18, 492-498.
65. Poon, H. F., Vaishnav, R. A., Getchell, T. V., Getchell, M. L., Butterfield, D. A., Quantitative proteomics analysis of differential protein expression and oxidative modification of specific proteins in the brains of old mice, Neurobiol. Aging 2006, 27, 1010-1019.
66. Sultana, R., Perluigi, M., Butterfield, D. A., Redox proteomics identification of oxidatively modified proteins in Alzheimer's disease brain and in vivo and in vitro models of AD centered around Abeta(1-42), J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2005.
67. Sultana, R., Butterfield, D. A., Oxidatively modified GST and MRP1 in Alzheimer's disease brain: Implications for accumulation of reactive lipid peroxidation products, Neurochem. Res. 2004, 29, 2215-2220.
68. Sultana, R., Boyd-Kimball, D., Poon, H. F., Cai, J. et al., Redox proteomics identification of oxidized proteins in Alzheimer's disease hippocampus and cerebellum: An approach to understand pathological and biochemical alterations in AD, Neurobiol. Aging 2006, 27, 1564-1576.
69. Sultana, R., Poon, H. F., Cai, J., Pierce, W. M. et al., Identification of nitrated proteins in Alzheimer's disease brain using a redox proteomics approach, Neurobiol. Dis. 2006, 22, 76-87.
70. Butterfield, D. A., Reed, T., Newman, S., Sultana, R., Roles of amyloid b-peptide-associated oxidative stress and brain protein modifications in the pathogenesis of Alzheimer's disease and mild cognitive impairment, Free Radic. Biol. Med. 2007, 43, 658-677.
71. Iwangoff, P., Armbruster, R., Enz, A., Meier-Ruge, W., Glycolytic enzymes from human autoptic brain cortex: normal aged and demented cases, Mech. Ageing Dev. 1980, 14, 203-209.
72. Meier-Ruge, W., Iwangoff, P., Reichlmeier, K., Neurochemical enzyme changes in Alzheimer's and Pick's disease, Arch. Gerontol. Geriatr. 1984, 3, 161-165.
73. Messier, C., Gagnon, M., Glucose regulation and cognitive functions: relation to Alzheimer's disease and diabetes, Behav. Brain Res. 1996, 75, 1-11.
74. Rapoport, S.I., In vivo PET imaging and postmortem studies suggest potentially reversible and irreversible stages of brain metabolic failure in Alzheimer's disease, Eur. Arch. Psychiatry Clin. Neurosci. 1999, 249, 46-55.
75. Vanhanen, M., Soininen, H., Glucose intolerance, cognitive impairment and Alzheimer's disease, Curr. Opin. Neurol. 1998, 11, 673-677.
76. Pancholi, V., Multifunctional alpha-enolase: its role in diseases, Cell. Mol. Life Sci. 2001, 58, 902-920.
77. Parnetti, L., Palumbo, B., Cardinali, L., Loreti, F. et al., Cerebrospinal fluid neuron-specific enolase in Alzheimer's disease and vascular dementia, Neurosci. Lett. 1995, 183, 43-45.
78. Choi, J., Levey, A. I., Weintraub, S. T., Rees, H. D. et al., Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases, J. Biol. Chem. 2004, 279, 13256-13264.
79. Choi, J., Rees, H. D., Weintraub, S. T., Levey, A. I. et al., Oxidative modifications and aggregation of Cu,Zn-superoxide dismutase associated with Alzheimer and Parkinson diseases, J. Biol Chem. 2005, 280, 11648-11655.
80. Davies, M. J., Fu, S., Wang, H., Dean, R. T., Stable markers of oxidant damage to proteins and their application in the study of human disease, Free Radic. Biol. Med. 1999, 27, 1151-1163.
81. Lovell, M. A., Gabbita, S. P., Markesbery, W. R., Increased DNA oxidation and decreased levels of repair products in Alzheimer's disease ventricular CSF, J. Neurochem. 1999, 72, 771-776.
82. Arendt, T., Bruckner, M. K., Gertz, H. J., Marcova, L., Cortical distribution of neurofibrillary tangles in Alzheimer's disease matches the pattern of neurons that retain their capacity of plastic remodelling in the adult brain, Neuroscience 1998, 83, 991-1002.
83. Hanks, S. D., Flood, D. G., Region-specific stability of dendritic extent in normal human aging and regression in Alzheimer's disease. J. CA1 of hippocampus, Brain Res. 1991, 540, 63-82.
84. Coleman, P. D., Flood, D. G., Neuron numbers and dendritic extent in normal aging and Alzheimer's disease, Neurobiol. Aging 1987, 8, 521-545.
85. Butterfield, D. A., Abdul, H. M., Opii, W., Newman, S. F. et al., Pin1 in Alzheimer's disease, J. Neurochem. 2006, 98, 1697-1706.
86. Butterfield, D. A., Poon, H. F., St Clair, D., Keller, J. N. et al., Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: insights into the development of Alzheimer's disease, Neurobiol. Dis. 2006, 22, 223-232.
87. Gong, C. X., Grundke-Iqbal, I., Iqbal, K., Dephosphorylation of Alzheimer's disease abnormally phosphorylated tau by protein phosphatase-2A, Neuroscience 1994, 81, 765-772.
88. Zambrano, C. A., Egana, J. T., Nunez, M. T., Maccioni, R. B., Gonzalez-Billault, C., Oxidative stress promotes tau dephosphorylation in neuronal cells: the roles of cdk5 and PP1, Free Radic. Biol. Med. 2004, 36, 1393-1402.
89. Wang, J. Z., Grundke-Iqbal, I., Iqbal, K., Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration, Eur. J. Neurosci. 2007, 25, 59-68.
90. Lavoie, S. B., Albert, A. L., Vincent, M., [Unexpected roles of the peptidyl-prolyl cis/trans isomerase Pin 1], Med. Sci. (Paris) 2003, 19, 1251-1258.
91. Zhou, X. Z., Kops, O., Werner, A., Lu, P. J. et al., Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins, Mol. Cell 2000, 6, 873-883.
92. Holzer, M., Gartner, U., Stobe, A., Hartig, W. et al., Inverse association of Pin1 and tau accumulation in Alzheimer's disease hippocampus, Acta Neuropathologica 2002, 104, 471-481.
93. Ramakrishnan, P., Dickson, D. W., Davies, P., Pin1 colocalization with phosphorylated tau in Alzheimer's disease and other tauopathies, Neurobiol. Dis. 2003, 14, 251-264.
94. Pastorino, L., Sun, A., Lu, P. J., Zhou, X. Z. et al., The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-beta production, Nature 2006, 440, 528-534.
95. Hensley, K., Hall, N., Subramaniam, R., Cole, P. et al., Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation, J. Neurochem. 1995, 65, 2146-2156.
96. Lauderback, C. M., Hackett, J. M., Huang, F. F., Keller, J. N. et al., The glial glutamate transporter, GLT-1, is oxidatively modified by 4-hydroxy-2-nonenal in the Alzheimer's disease brain: the role of Abeta1-42, J. Neurochem. 2001, 78, 413-416.
97. Boyd-Kimball, D., Poon, H. F., Lynn, B. C., Cai, J. et al., Proteomic identification of proteins specifically oxidized in Caenorhabditis elegans expressing human Abeta(1-42): implications for Alzheimer's disease, Neurobiol. Aging 2006, 27, 1239-1249.
98. Opii, W. O., Joshi, G., Head, E., Milgram, N. W. et al., Proteomic identification of brain proteins in the canine model of human aging following a long-term treatment with antioxidants and a program of behavioral enrichment: Relevance to Alzheimer's disease, Neurobiol. Aging 2006.
99. Poon, H. F., Castegna, A., Farr, S. A., Thongboonkerd, V. et al., Quantitative proteomics analysis of specific protein expression and oxidative modification in aged senescence-accelerated-prone 8 mice brain, Neuroscience 2004, 126, 915-926.
100. Poon, H. F., Farr, S. A., Banks, W. A., Pierce, W. M. et al., Proteomic identification of less oxidized brain proteins in aged senescence-accelerated mice following administration of antisense oligonucleotide directed at the Abeta region of amyloid precursor protein, Brain Res. 2005, 138, 8-16.
101. Poon, H. F., Farr, S. A., Thongboonkerd, V., Lynn, B. C. et al., Proteomic analysis of specific brain proteins in aged SAMP8 mice treated with alpha-lipoic acid: implications for aging and age-related neurodegenerative disorders, Neurochem. Int. 2005, 46, 159-168.
102. Link, C. D., Expression of human beta-amyloid peptide in transgenic Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA, 1995, 92, 9368-9372.
103. Link, C. D., Transgenic invertebrate models of age-associated neurodegenerative diseases, Mech. Ageing Dev. 2001, 122, 1639-1649.
104. Fay, D. S., Fluet, A., Johnson, C. J., Link, C. D., In vivo aggregation of beta-amyloid peptide variants, J. Neurochem. 1998, 71, 1616-1625.
105. Link, C. D., Cypser, J. R., Johnson, C. J., Johnson, T. E., Direct observation of stress response in Caenorhabditis elegans using a reporter transgene. Cell Stress Chap., 1999, 4, 235-242.
106. Vanfleteren, J. R., Oxidative stress and ageing in Caenorhabditis elegans, Biochem. J. 1993, 292, 605-608.
107. Wu, Y., Luo, Y., Transgenic C. elegans as a model in Alzheimer's research, Curr. Alz. Res. 2005, 2, 37-45.
108. Lovell, M. A., Xie, C., Markesbery, W. R., Decreased glutathione transferase activity in brain and ventricular fluid in Alzheimer's disease, Neurology 1998 51, 1562-1566.
109. Boyd-Kimball, D., Castegna, A., Sultana, R., Poon, H. F. et al., Proteomic identification of proteins oxidized by Abeta(1-42) in synaptosomes: implications for Alzheimer's disease, Brain Res. 2005, 1044, 206-215.
110. Wu, Y., Wu, Z., Butko, P., Christen, Y. et al., Amyloid-beta-induced pathological behaviors are suppressed by Ginkgo biloba extract EGb 761 and ginkgolides in transgenic Caenorhabditis elegans, J. Neurosci. 2006, 26, 13102-13113.
111. Brown, M. K., Evans, J. L., Luo, Y., Beneficial effects of natural antioxidants EGCG and alpha-lipoic acid on life span and age-dependent behavioral declines in Caenorhabditis elegans, Pharmacol. Biochem. Behav. 2006, 85, 620-628.
112. Miyamoto, M., Characteristics of age-related behavioral changes in senescence-accelerated mouse SAMP8 and SAMP10, Exp. Gerontol. 1997, 32, 139-148.
113. Takeda, T., Hosakawa, M., Higuchi, K., Senescence-accelerated mouse (SAM): a novel murine model of senescence, Exp. Gerontol. 1997, 32, 105-109.
114. Flood, J. F., Morley, J. E., Learning and memory in the SAMP8 mouse, Neurosci. Biobehav. Rev. 1998, 22, 1-20.
115. Kawamata, T., Akiguchi, I., Maeda, K., Tanaka, C. et al., Age-related changes in the brains of senescence-accelerated mice (SAM): association with glial and endothelial reactions, Microsc. Res. Tech. 1998, 43, 59-67.
116. Morley, J. E., The SAMP8 mouse: a model of Alzheimer disease?, Biogerontology 2002, 3, 57-60.
117. Morley, J. E., Kumar, V. B., Bernardo, A. E., Farr, S. A. et al., Beta-amyloid precursor polypeptide in SAMP8 mice affects learning and memory, Peptides 2000, 21, 1761-1767.
118. Takemura, M., Nakamura, S., Akiguchi, I., Ueno, M. et al., Beta/A4 proteinlike immunoreactive granular structures in the brain of senescence-accelerated mouse, Am. J. Pathol. 1993, 142, 1887-1897.
119. Butterfield, D. A., Howard, B. J., Yatin, S., Allen, K. L., Carney, J. M., Free radical oxidation of brain proteins in accelerated senescence and its modulation by N-tert-butyl-alpha-phenylnitrone, Proc. Natl. Acad. Sci. USA 1997, 94, 674-678.
120. Fujibayashi, Y., Yamamoto, S., Waki, A., Konishi, J., Yonekura, Y., Increased mitochondrial DNA deletion in the brain of SAMP8, a mouse model for spontaneous oxidative stress brain, Neurosci. Lett. 254, 1998, 109-112.
121. Nishikawa, T., Takahashi, J. A., Fujibayashi, Y., Fujisawa, H. et al., An early stage mechanism of the age-associated mitochondrial dysfunction in the brain of SAMP8 mice; an age-associated neurodegeneration animal model, Neurosci. Lett. 1998, 254, 69-72.
122. Liu, J., Mori, A., Age-associated changes in superoxide dismutase activity, thiobarbituric acid reactivity and reduced glutathione level in the brain and liver in senescence accelerated mice (SAM): a comparison with ddY mice, Mech. Ageing Dev. 1993, 71, 23-30.
123. Sato, E., Oda, N., Ozaki, N., Hashimota, S. et al., Early and transient increase in oxidative stress in the cerebral cortex of senescence-accelerated mouse, Mech. Ageing Dev. 1996, 86, 105-114.
124. Petursdottir, A. L., Farr, S. A., Marley, J. E., Banks, W. A., Skuladottir, G. V., Lipid peroxidation in brain during aging in the senescence-accelerated mouse (SAM), Neurobiol. Aging 2007, 28, 1170-1178.
125. Okatani, Y., Wakatsuki, A., Reiter, R. J., Miyahara, V., Melatonin reduces oxidative damage of neural lipids and proteins in senescence-accelerated mouse, Neurobiol. Aging 2002, 23, 639-644.
126. Nabeshi, H., Oikawa, S., Inoue, S., Nishino, K., Kawanishi, S., Proteomic analysis for protein carbonyl as an indicator of oxidative damage in senescence-accelerated mice, Free Radic. Res. 2006, 40, 1173-1181.
127. Colas, D., Gharib, A., Bezin, L., Morales, A. et al., Regional age-related changes in neuronal nitric oxide synthase (nNOS), messenger RNA levels and activity in SAMP8 brain, BMC neuroscience 2006, 7, 81.
128. Inada, K., Yokoi, I., Kabuto, H., Habu, H. et al., Age-related increase in nitric oxide synthase activity in senescence accelerated mouse brain and the effect of long-term administration of superoxide radical scavenger, Mech. Ageing Dev. 1996, 89, 95-102.
129. Kumar, V. B., Farr, S. A., Flood, J. F., Kamlesh, V. et al., Site-directed antisense oligonucleotide decreases the expression of amyloid precursor protein and reverses deficits in learning and memory in aged SAMP8 mice, Peptides 2000, 21, 1769-1775.
130. Perez, R. G., Soriana, S., Hayes, J. D., Ostaszewski, B. et al., Mutagenesis identifies new signals for beta-amyloid precursor protein endocytosis, turnover, and the generation of secreted fragments, including Abeta42, J. Biol. Chem. 1999, 274, 18851-18856.
131. Kumar, V. B., Vyas, K., Franko, M., Choudhary, V. et al., Molecular cloning, expression, and regulation of hippocampal amyloid precursor protein of senescence accelerated mouse (SAMP8), Biochem. Cell. Biol. = Biochimie et Biologie Cellulaire 2001, 79, 57-67.
132. Banks, W. A., Farr, S. A., Butt, W., Kumar, V. B. et al., Delivery across the blood-brain barrier of antisense directed against amyloid beta: reversal of learning and memory deficits in mice overexpressing amyloid precursor protein, J. Pharm. Exp. Therap. 2001. 297, 1113-1121.
133. Banks, W. A., Robinson, S. M., Verma, S., Morley, J. E., Efflux of human and mouse amyloid beta proteins 1-40 and 1-42 from brain: impairment in a mouse model of Alzheimer's disease, Neuroscience 2003, 121, 487-492.
134. Poon, H. F., Joshi, G., Sultana, R., Farr, S. A. et al., Antisense directed at the Abeta region of APP decreases brain oxidative markers in aged senescence accelerated mice, Brain Res. 2004, 1018, 86-96.
135. Miyazaki, H., Okuma, Y., Nomura, J., Nagashima, K., Nomura, Y., Age-related alterations in the expression of glial cell line-derived neurotrophic factor in the senescence-accelerated mouse brain, J. Pharm. Sci. 2003, 92, 28-34.
136. Kurokawa, T., Sato, E., Inoue, A., Ishibashi, S., Evidence that glucose metabolism is decreased in the cerebrum of aged female senescence-accelerated mouse; possible involvement of a low hexokinase activity, Neurosci. Lett. 1996, 214, 45-48.
137. Shimano, Y., [Studies on aging through analysis of the glucose metabolism related to the ATP-production of the senescence accelerated mouse (SAM)], [Hokkaido igaku zasshi] The Hokkaido J. Med. Sci. 1998, 73, 557-569.
138. Farr, S. A., Poon, H. F., Dogrukol-Ak, D., Drake, J. et al., The antioxidants alpha-lipoic acid and N-acetylcysteine reverse memory impairment and brain oxidative stress in aged SAMP8 mice, J. Neurochem. 2003, 84, 1173-1183.
139. Armbrecht, H. J., Boltz, M. A., Kumar, V. B., Flood, J. F., Morley, J. E., Effect of age on calcium-dependent proteins in hippocampus of senescence-accelerated mice, Brain Res. 1999, 842, 287-293.
140. Amano, T., Nakanishi, H., Oka, M., Yamamoto, K., Increased expression of cathepsins E and D in reactive microglial cells associated with spongiform degeneration in the brain stem of senescence-accelerated mouse, Exp. Neurol. 1995, 136, 171-182.
141. Yasui, F., Matsugo, S., Ishibashi, M., Kajita, T. et al., Effects of chronic acetyl-L-carnitine treatment on brain lipid hydroperoxide level and passive avoidance learning in senescence-accelerated mice, Neurosci. Lett. 2002, 334, 177-180.
142. Saigoh, K., Wang, Y. L., Suh, J. G., Yamanishi, T. et al., Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice, Nat. Genet. 1999, 23, 47-51.
143. Yamazaki, K., Wakasugi, N., Tomita, T., Kikuchi, T. et al., Gracile axonal dystrophy (GAD), a new neurological mutant in the mouse, Proc. Soc. Exp. Biol. Med. 1988, 187, 209-215.
144. Ichihara, N., Wu, J., Chui, D. H., Yamazaki, K. et al., Axonal degeneration promotes abnormal accumulation of amyloid beta-protein in ascending gracile tract of gracile axonal dystrophy (GAD) mouse, Brain Res. 1995, 695, 173-178.
145. Lowe, J., McDermott, H., Landon, M., Mayer, R. J., Wilkinson, K. D., Ubiquitin carboxyl-terminal hydrolase (PGP 9.5) is selectively present in ubiquitinated inclusion bodies characteristic of human neurodegenerative diseases, J. Pathol. 1990, 761, 153-160.
146. Leroy, E., Boyer, R., Auburger, G., Leube, B. et al., The ubiquitin pathway in Parkinson's disease, Nature 1998, 395, 451-452.
147. Bonin, M., Poths, S., Osaka, H., Wang, Y. L. et al., Micro-array expression analysis of gad mice implicates involvement of Parkinson's disease associated UCH-L1 in multiple metabolic pathways, Brain Res. 2004, 126, 88-97.
148. Castegna, A., Thongboonkerd, V., Klein, J., Lynn, B.C. et al., Proteome analysis of brain proteins in the gracile axoryl dystrophy ( gad) mouse, a syndrome that emanates from dysfunctional ubiquitin carbaxy-terminal hydrolase L-1, reveals oxidation of key proteins. J. Neurochem 2004, 88, 1540-1546.
149. Studzinski, C. M., Araujo, J. A., Milgram, N. W., The canine model of human cognitive aging and dementia: pharmacological validity of the model for assessment of human cognitive-enhancing drugs, Progress Neuro-psychopharmacol. Biol. Psychiatry 29, 2005, 489-498.
150. Cummings, B. J., Su, J. H., Cotman, C. W., White, R., Russell, M. J., Beta-amyloid accumulation in aged canine brain: a model of early plaque formation in Alzheimer's disease, Neurobiol. Aging 1993, 14, 547-560.
151. Ball, M. J., MacGregor, J., Fyfe, I. M., Rapoport, S. I., London, E. D., Paucity of morphological changes in the brains of ageing beagle dogs: further evidence that Alzheimer lesions are unique for primate central nervous system, Neurobiol. Aging 1983, 4, 127-131.
152. Johnstone, E. M., Chaney, M. O., Norris, F. H., Pascual, R., Little, S. P., Conservation of the sequence of the Alzheimer's disease amyloid peptide in dog, polar bear and five other mammals by cross-species polymerase chain reaction analysis, Brain Res. 1991, 10, 299-305.
153. Head, E., Callahan, H., Muggenburg, B. A., Cotman, C. W., Milgram, N. W., Visual-discrimination learning ability and beta-amyloid accumulation in the dog, Neurobiol. Aging 1998, 19, 415-425.
154. Kimotsuki, T., Nagaoka, T., Yasuda, M., Tamahara, S. et al., Changes of magnetic resonance imaging on the brain in beagle dogs with aging, J. Vet. Med. Sci./Jap. Soci. Vet. Sci. 2005, 67, 961-967.
155. Tapp, P. D., Siwak, C. T., Gao, F. Q., Chiou, J. Y. et al., Frontal lobe volume, function, and beta-amyloid pathology in a canine model of aging, J. Neurosci. 2004, 24, 8205-8213.
156. Carrillo, M. C., Ivy, G. O., Milgram, N. W., Head, E. et al., (-)Deprenyl increases activities of superoxide dismutase (SOD) in striatum of dog brain, Life Sci. 1994, 54, 1483-1489.
157. Rofina, J. E., Singh, K., Skoumalova-Vesela, A., van Ederen, A. M. et al., Histochemical accumulation of oxidative damage products is associated with Alzheimer-like pathology in the canine, Amytoid 2004, 11, 90-100.
158. Papaioannou, N., Tooten, P. C., van Ederen, A. M., Bohl, J. R. et al., Immunohistochemical investigation of the brain of aged dogs. I. Detection of neurofibrillary tangles and of 4-hydroxynonenal protein, an oxidative damage product, in senile plaques, Amytoid 2001, 8, 11-21.
159. Opii, W. O., Joshi, G., Head, E., Milgram, N. W. et al., Proteomic identification of brain proteins in the canine model of human aging following a long-term treatment with anti-oxidants and a program of behavioral enrichment: Relevance to Alzheimer's disease, Neurobiol. Aging 2008, 29, 51-70.
160. Skoumalova, A., Rofina, J., Schwippelova, Z., Gruys, E., Wilhelm, J., The role of free radicals in canine counterpart of senile dementia of the Alzheimer type, Exp. Gerontol. 2003, 38, 711-719.
161. Cotman, C. W., Head, E., Muggenburg, B. A., Zicker, S., Milgram, N. W., Brain aging in the canine: a diet enriched in antioxidants reduces cognitive dysfunction, Neurobiol. Aging 2002, 23, 809-818.
162. Milgram, N. W., Head, E., Zicker, S. C., Ikeda-Douglas, C.,J. et al., Learning ability in aged beagle dogs is preserved by behavioral enrichment and dietary fortification: a two-year longitudinal study, Neurobiol. Aging 2005, 28, 77-90.
163. Kitani, K., Kanai, S., Ivy, G. O., Carrillo, M. C., Assessing the effects of deprenyl on longevity and antioxidant defenses in different animal models, Ann. NY Acad. Sci. 1998, 854, 291-306.