Neurobiology of Aging
Volume 29, Issue 1 , Pages 51-70 , January 2008

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

  • Wycliffe O. Opii

      Affiliations

    • Department of Chemistry, Center of Membrane Sciences, and Sanders-Brown Center on Aging, University of Kentucky, Lexington, KY 40506-0055, United States
  • ,
  • Gururaj Joshi

      Affiliations

    • Department of Chemistry, Center of Membrane Sciences, and Sanders-Brown Center on Aging, University of Kentucky, Lexington, KY 40506-0055, United States
  • ,
  • Elizabeth Head

      Affiliations

    • Institute for Brain Aging and Dementia, Department of Neurology, University of California, Irvine, CA 92697-4540, United States
  • ,
  • N. William Milgram

      Affiliations

    • Division of Life Sciences, University of Toronto, Toronto, Canada M1C 1A4
  • ,
  • Bruce A. Muggenburg

      Affiliations

    • Lovelace Respiratory Research Institute, Albuquerque, NM 87108, United States
  • ,
  • Jon B. Klein

      Affiliations

    • Department of Medicine, Kidney Disease Program, University of Louisville, Louisville, KY, United States
  • ,
  • William M. Pierce

      Affiliations

    • Department of Pharmacology, University of Louisville, Louisville, KY, United States
  • ,
  • Carl W. Cotman

      Affiliations

    • Institute for Brain Aging and Dementia, Department of Neurology, University of California, Irvine, CA 92697-4540, United States
  • ,
  • D. Allan Butterfield

      Affiliations

    • Department of Chemistry, Center of Membrane Sciences, and Sanders-Brown Center on Aging, University of Kentucky, Lexington, KY 40506-0055, United States
    • Corresponding Author InformationCorresponding author. Tel.: +1 859 257 3184; fax: +1 859 257 5876.

Received 21 June 2006 ,Revised 6 September 2006 ,Accepted 14 September 2006.

References 

  1. Adams JC. Fascin protrusions in cell interactions. Trends Cardiovasc Med. 2004;14(6):221–226
  2. Adams JC. Roles of fascin in cell adhesion and motility. Curr Opin Cell Biol. 2004;16(5):590–596
  3. Adlard PA, Perreau VM, Pop V, Cotman CW. Voluntary exercise decreases amyloid load in a transgenic model of Alzheimer's disease. J Neurosci. 2005;25(17):4217–4221
  4. Aksenova MV, Aksenov MY, Carney JM, Butterfield DA. Protein oxidation and enzyme activity decline in old brown Norway rats are reduced by dietary restriction. Mech Ageing Dev. 1998;100(2):157–168
  5. Aksenov MY, Aksenova MV, Markesbery WR, Butterfield DA. Amyloid beta-peptide (1–40)-mediated oxidative stress in cultured hippocampal neurons. Protein carbonyl formation, CK BB expression, and the level of Cu, Zn, and Mn SOD mRNA. J Mol Neurosci. 1998;10(3):181–192
  6. Aksenova MV, Aksenov MY, Payne RM, Trojanowski JQ, Schmidt ML, Carney JM, et al. Oxidation of cytosolic proteins and expression of creatine kinase BB in frontal lobe in different neurodegenerative disorders. Dement Geriatr Cogn Disord. 1999;10(2):158–165
  7. Aksenov M, Aksenova M, Butterfield DA, Markesbery WR. Oxidative modification of creatine kinase BB in Alzheimer's disease brain. J Neurochem. 2000;74(6):2520–2527
  8. Bajo M, Yoo BC, Cairns N, Gratzer M, Lubec G. Neurofilament proteins NF-L, NF-M and NF-H in brain of patients with Down syndrome and Alzheimer's disease. Amino Acids. 2001;21(3):293–301
  9. Bergeron C, Beric-Maskarel K, Muntasser S, Weyer L, Somerville MJ, Percy ME. Neurofilament light and polyadenylated mRNA levels are decreased in amyotrophic lateral sclerosis motor neurons. J Neuropathol Exp Neurol. 1994;53(3):221–230
  10. Bickford PC, Gould T, Briederick L, Chadman K, Pollock A, Young D, et al. Antioxidant-rich diets improve cerebellar physiology and motor learning in aged rats. Brain Res. 2000;866(1–2):211–217
  11. Boero J, Qin W, Cheng J, Woolsey TA, Strauss AW, Khuchua Z. Restricted neuronal expression of ubiquitous mitochondrial creatine kinase: changing patterns in development and with increased activity. Mol Cell Biochem. 2003;244(1–2):69–76
  12. Boyd-Kimball D, Sultana R, Poon HF, Mohmmad-Abdul H, Lynn BC, Klein JB, et al. Gamma-glutamylcysteine ethyl ester protection of proteins from Abeta(1–42)-mediated oxidative stress in neuronal cell culture: a proteomics approach. J Neurosci Res. 2005;79(5):707–713
  13. Boyd-Kimball D, Sultana R, Poon HF, Lynn BC, Casamenti F, Pepeu G, et al. Proteomic identification of proteins specifically oxidized by intracerebral injection of amyloid beta-peptide (1–42) into rat brain: implications for Alzheimer's disease. Neuroscience. 2005;132(2):313–324
  14. Boyd-Kimball D, Castegna A, Sultana R, Poon HF, Petroze R, Lynn BC, et al. Proteomic identification of proteins oxidized by Abeta(1–42) in synaptosomes: implications for Alzheimer's disease. Brain Res. 2005;1044(2):206–215
  15. Butterfield DA, Stadtman ER. Protein oxidation processes in aging brain. Adv Cell Aging Gerontol. 1997;2:161–191
  16. Butterfield DA, 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(12):548–554
  17. Butterfield DA, Kanski J. Brain protein oxidation in age-related neurodegenerative disorders that are associated with aggregated proteins. Mech Ageing Dev. 2001;122(9):945–962
  18. Butterfield DA, Lauderback CM. Lipid peroxidation and protein oxidation in Alzheimer's disease brain: potential causes and consequences involving amyloid beta-peptide-associated free radical oxidative stress. Free Radic Biol Med. 2002;32(11):1050–1060
  19. Butterfield DA, Griffin S, Munch G, Pasinetti GM. Amyloid beta-peptide and amyloid pathology are central to the oxidative stress and inflammatory cascades under which Alzheimer's disease brain exists. J Alzheimers Dis. 2002;4(3):193–201
  20. Butterfield DA, Castegna A, Drake J, Scapagnini G, Calabrese V. Vitamin E and neurodegenerative disorders associated with oxidative stress. Nutr Neurosci. 2002;5(4):229–239
  21. Butterfield DA, Boyd-Kimball D, Castegna A. Proteomics in Alzheimer's disease: insights into potential mechanisms of neurodegeneration. J Neurochem. 2003;86(6):1313–1327
  22. Butterfield DA. Proteomics: a new approach to investigate oxidative stress in Alzheimer's disease brain. Brain Res. 2004;1000(1–2):1–7
  23. Butterfield DA, Boyd-Kimball D. Amyloid beta-peptide(1–42) contributes to the oxidative stress and neurodegeneration found in Alzheimer disease brain. Brain Pathol. 2004;14(4):426–432
  24. Butterfield DA, 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. 2005;1703(2):149–156
  25. Butterfield DA, Poon HF, St Clair D, Keller JN, Pierce WM, Klein JB, 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
  26. Calabrese V, Scapagnini G, Ravagna A, Colombrita C, Spadaro F, Butterfield DA, et al. Increased expression of heat shock proteins in rat brain during aging: relationship with mitochondrial function and glutathione redox state. Mech Ageing Dev. 2004;125(4):325–335
  27. Calabrese V, Butterfield DA, Stella AM. Nutritional antioxidants and the heme oxygenase pathway of stress tolerance: novel targets for neuroprotection in Alzheimer's disease. Ital J Biochem. 2003;52(4):177–181
  28. Calabrese V, Stella AM, Butterfield DA, Scapagnini G. Redox regulation in neurodegeneration and longevity: role of the heme oxygenase and HSP70 systems in brain stress tolerance. Antioxid Redox Signal. 2004;6(5):895–913
  29. Calabrese V, Giuffrida Stella AM, Calvani M, Butterfield DA. Acetylcarnitine and cellular stress response: roles in nutritional redox homeostasis and regulation of longevity genes. J Nutr Biochem. 2006;17(2):73–88
  30. Callahan H, Ikeda-Douglas C, Head E, Cotman CW, Milgram NW. Development of a protocol for studying object recognition memory in the dog. Prog Neuro-Psychopharmacol Biol Psychiatry. 2000;24(5):693–707
  31. Cao G, Verdon CP, Wu AH, Wang H, Prior RL. Automated assay of oxygen radical absorbance capacity with the COBAS FARA II. Clin Chem. 1995;41(12 Pt 1):1738–1744
  32. Castegna A, Aksenov M, Thongboonkerd V, Klein JB, Pierce WM, Booze R, 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(6):1524–1532
  33. Castegna A, Aksenov M, Aksenova M, Thongboonkerd V, Klein JB, Pierce WM, 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(4):562–571
  34. Castegna A, Thongboonkerd V, Klein JB, Lynn B, Markesbery WR, Butterfield DA. Proteomic identification of nitrated proteins in Alzheimer's disease brain. J Neurochem. 2003;85(6):1394–1401
  35. Castegna A, Thongboonkerd V, Klein J, Lynn BC, Wang YL, Osaka H, et al. Proteomic analysis of brain proteins in the gracile axonal dystrophy (gad) mouse, a syndrome that emanates from dysfunctional ubiquitin carboxyl-terminal hydrolase L-1, reveals oxidation of key proteins. J Neurochem. 2004;88(6):1540–1546
  36. Chan AD, Nippak PM, Murphey H, Ikeda-Douglas CJ, Muggenburg B, Head E, et al. Visuospatial impairments in aged canines (Canis familiaris): the role of cognitive-behavioral flexibility. Behav Neurosci. 2002;116(3):443–454
  37. Chen K, Gunter K, Maines MD. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J Neurochem. 2000;75(1):304–313
  38. Chuang DM, Hough C, Senatorov VV. Glyceraldehyde-3-phosphate dehydrogenase, apoptosis, and neurodegenerative diseases. Annu Rev Pharmacol Toxicol. 2005;45:269–290
  39. Conrad CC, Choi J, Malakowsky CA, Talent JM, Dai R, Marshall P, et al. Identification of protein carbonyls after two-dimensional electrophoresis. Proteomics. 2001;1(7):829–834
  40. Cotman CW, Head E, Muggenburg BA, Zicker S, Milgram NW. Brain aging in the canine: a diet enriched in antioxidants reduces cognitive dysfunction. Neurobiol Aging. 2002;23(5):809–818
  41. Crow JP, Ye YZ, Strong M, Kirk M, Barnes S, Beckman JS. Superoxide dismutase catalyzes nitration of tyrosines by peroxynitrite in the rod and head domains of neurofilament-L. J Neurochem. 1997;69(5):1945–1953
  42. Cummings BJ, Su JH, Cotman CW, White R, Russell MJ. Beta-amyloid accumulation in aged canine brain: a model of early plaque formation in Alzheimer's disease. Neurobiol Aging. 1993;14(6):547–560
  43. Cummings BJ, Head E, Afagh AJ, Milgram NW, Cotman CW. Beta-amyloid accumulation correlates with cognitive dysfunction in the aged canine. Neurobiol Learn Mem. 1996;66(1):11–23
  44. Cummings BJ, Head E, Ruehl W, Milgram NW, Cotman CW. The canine as an animal model of human aging and dementia. Neurobiol Aging. 1996;17(2):259–268
  45. Drake J, Sultana R, Aksenova M, Calabrese V, Butterfield DA. Elevation of mitochondrial glutathione by gamma-glutamylcysteine ethyl ester protects mitochondria against peroxynitrite-induced oxidative stress. J Neurosci Res. 2003;74(6):917–927
  46. Eckles-Smith K, Clayton D, Bickford P, Browning MD. Caloric restriction prevents age-related deficits in LTP and in NMDA receptor expression. Brain Res Mol Brain Res. 2000;78(1–2):154–162
  47. Farr SA, Poon HF, Dogrukol-Ak D, Drake J, Banks WA, Eyerman E, 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(5):1173–1183
  48. Gutteridge JM, Halliwell B. Free radicals and antioxidants in the year 2000. A historical look to the future. Ann NY Acad Sci. 2000;899:136–147
  49. Habig WH, Jakoby WB. Glutathione S-transferases (rat and human). Meth Enzymol. 1981;77:218–231
  50. Hara MR, Cascio MB, Sawa A. GAPDH as a sensor of NO stress. Biochim Biophys Acta. 2006;1762(5):502–509
  51. Head E, Callahan H, Muggenburg BA, Cotman CW, Milgram NW. Visual-discrimination learning ability and beta-amyloid accumulation in the dog. Neurobiol Aging. 1998;19(5):415–425
  52. Head E, McCleary R, Hahn FF, Milgram NW, Cotman CW. Region-specific age at onset of beta-amyloid in dogs. Neurobiol Aging. 2000;21(1):89–96
  53. Head E, Torp R. Insights into Abeta and presenilin from a canine model of human brain aging. Neurobiol Dis. 2002;9(1):1–10
  54. Head E, Liu J, Hagen TM, Muggenburg BA, Milgram NW, Ames BN, et al. Oxidative damage increases with age in a canine model of human brain aging. J Neurochem. 2002;82(2):375–381
  55. Hensley K, Carney JM, Mattson MP, Aksenova M, Harris M, Wu JF, et al. A model for beta-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: relevance to Alzheimer disease. Proc Natl Acad Sci USA. 1994;91(8):3270–3274
  56. Hensley K, Hall N, Subramaniam R, Cole P, Harris M, Aksenov M, et al. Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation. J. Neurochem. 1995;65:2146–2156
  57. Hensley K, Butterfield DA, Hall N, Cole P, Subramaniam R, Mark R, et al. Reactive oxygen species as causal agents in the neurotoxicity of the Alzheimer's disease-associated amyloid beta peptide. Ann NY Acad Sci. 1996;786:120–134
  58. Heydari AR, Wu B, Takahashi R, Strong R, Richardson A. Expression of heat shock protein 70 is altered by age and diet at the level of transcription. Mol Cell Biol. 1993;13(5):2909–2918
  59. Hodges PE, Carrico PM, Hogan JD, O’Neill KE, Owen JJ, Mangan M, et al. Annotating the human proteome: the Human Proteome Survey Database (HumanPSD) and an in-depth target database for G protein-coupled receptors (GPCR-PD) from Incyte Genomics. Nucl Acids Res. 2002;30(1):137–141
  60. Hoffman PN, Cleveland DW, Griffin JW, Landes PW, Cowan NJ, Price DL. Neurofilament gene expression: a major determinant of axonal calibre. Proc Natl Acad Sci USA. 1987;84(10):3472–3476
  61. Hultsch DF, Hertzog C, Small BJ, Dixon RA. Use it or lose it: engaged lifestyle as a buffer of cognitive decline in aging?. Psychol Aging. 1999;14(2):245–263
  62. Ji LL. Exercise-induced modulation of antioxidant defense. Ann NY Acad Sci. 2002;959:82–92
  63. Johnstone EM, Chaney MO, Norris FH, Pascual R, Little SP. 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 Mol Brain Res. 1991;10(4):299–305
  64. Joseph JA, Denisova N, Fisher D, Bickford P, Prior R, Cao G. Age-related neurodegeneration and oxidative stress: putative nutritional intervention. Neurol Clin. 1998;16(3):747–755
  65. Joseph JA, Shukitt-Hale B, Denisova NA, Prior RL, Cao G, Martin A, et al. Long-term dietary strawberry, spinach, or vitamin E supplementation retards the onset of age-related neuronal signal-transduction and cognitive behavioral deficits. J Neurosci. 1998;18(19):8047–8055
  66. Koufen P, Stark G. Free radical induced inactivation of creatine kinase: sites of interaction, protection, and recovery. Biochim Biophys Acta. 2000;1501(1):44–50
  67. Kureishy N, Sapountzi V, Prag S, Anilkumar N, Adams JC. Fascins, and their roles in cell structure and function. Bioessays. 2002;24(4):350–361
  68. Lauderback CM, Hackett JM, Huang FF, Keller JN, Szweda LI, Markesbery WR, 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(2):413–416
  69. Laurin D, Verreault R, Lindsay J, MacPherson K, Rockwood K. Physical activity and risk of cognitive impairment and dementia in elderly persons. Arch Neurol. 2001;58(3):498–504
  70. Liochev SI, Fridovich I. Copper- and zinc-containing superoxide dismutase can act as a superoxide reductase and a superoxide oxidase. J Biol Chem. 2000;275(49):38482–38485
  71. Lovell MA, Ehmann WD, Butler SM, Markesbery WR. Elevated thiobarbituric acid-reactive substances and antioxidant enzyme activity in the brain in Alzheimer's disease. Neurology. 1995;45(8):1594–1601
  72. Lovell MA, Xie C, Markesbery WR. Decreased glutathione transferase activity in brain and ventricular fluid in Alzheimer's disease. Neurology. 1998;51(6):1562–1566
  73. Lovell MA, Gabbita SP, Markesbery WR. Increased DNA oxidation and decreased levels of repair products in Alzheimer's disease ventricular CSF. J Neurochem. 1999;72(2):771–776
  74. Markesbery WR. Oxidative stress hypothesis in Alzheimer's disease. Free Radic Biol Med. 1997;23(1):134–147
  75. Maurer MH, Feldmann RE, Bromme JO, Kalenka A. Comparison of statistical approaches for the analysis of proteome expression data of differentiating neural stem cells. J Proteome Res. 2005;4(1):96–100
  76. Mecocci P, MacGarvey U, Kaufman AE, Koontz D, Shoffner JM, Wallace DC, et al. Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain. Ann Neurol. 1993;34(4):609–616
  77. Milgram NW, Adams B, Callahan H, Head E, Mackay B, Thirlwell C, et al. Landmark discrimination learning in the dog. Learn Mem. 1999;6(1):54–61
  78. Milgram NW, Zicker SC, Head E, Muggenburg BA, Murphey H, Ikeda-Douglas C, et al. Dietary enrichment counteracts age-associated cognitive dysfunction in canines. Neurobiol Aging. 2002;23:737–745
  79. Milgram NW, Head E, Zicker SC, Ikeda-Douglas C, Murphey H, Muggenberg BA, et al. Long-term treatment with antioxidants and a program of behavioral enrichment reduces age-dependent impairment in discrimination and reversal learning in beagle dogs. Exp Gerontol. 2004;39(5):753–765
  80. Milgram NW, Head E, Zicker SC, Ikeda-Douglas CJ, Murphey H, Muggenburg B, et al. Learning ability in aged beagle dogs is preserved by behavioral enrichment and dietary fortification: a two-year longitudinal study. Neurobiol Aging. 2005;26(1):77–90
  81. Perham RN. The fructose-1,6-bisphosphate aldolases: same reaction, different enzymes. Biochem Soc Trans. 1990;18(2):185–187
  82. Perluigi M, Poon HF, Maragos W, Pierce WM, Klein JB, Calabrese V, 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(12):1849–1861
  83. Perluigi M, Poon HF, Hensley K, Pierce WM, Klein JB, Calabrese V, 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(7):960–968
  84. Petersen RC, Thomas RG, Grundman M, Bennett D, Doody R, Ferris S, et al. Vitamin E and donepezil for the treatment of mild cognitive impairment. N Engl J Med. 2005;352(23):2379–2388
  85. Pocernich CB, Butterfield DA. Acrolein inhibits NADH-linked mitochondrial enzyme activity: implications for Alzheimer's disease. Neurotox Res. 2003;5(7):515–520
  86. Poon HF, Joshi G, Sultana R, Farr SA, Banks WA, Morley JE, et al. Antisense directed at the Abeta region of APP decreases brain oxidative markers in aged senescence accelerated mice. Brain Res. 2004;1018(1):86–96
  87. Poon HF, Castegna A, Farr SA, Thongboonkerd V, Lynn BC, Banks WA, et al. Quantitative proteomics analysis of specific protein expression and oxidative modification in aged senescence-accelerated-prone 8 mice brain. Neuroscience. 2004;126(4):915–926
  88. Poon HF, Vaishnav RA, Butterfield DA, Getchell ML, Getchell TV. Proteomic identification of differentially expressed proteins in the aging murine olfactory system and transcriptional analysis of the associated genes. J Neurochem. 2005;94(2):380–392
  89. Poon HF, Farr SA, Thongboonkerd V, Lynn BC, Banks WA, Morley JE, 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(2):159–168
  90. Poon HF, Frasier M, Shreve N, Calabrese V, Wolozin B, Butterfield DA. Mitochondrial associated metabolic proteins are selectively oxidized in A30P alpha-synuclein transgenic mice—a model of familial Parkinson's disease. Neurobiol Dis. 2005;18(3):492–498
  91. Poon HF, Hensley K, Thongboonkerd V, Merchant ML, Lynn BC, Pierce WM, 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(4):453–462
  92. Poon HF, Vaishnav RA, Getchell TV, Getchell ML, Butterfield DA. 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
  93. Poon HF, Shepherd HM, Reed TT, Calabrese V, Stella AM, Pennisi G, et al. Proteomics analysis provides insight into caloric restriction mediated oxidation and expression of brain proteins associated with age-related impaired cellular processes: mitochondrial dysfunction, glutamate dysregulation and impaired protein synthesis. Neurobiol Aging. 2006;27:1020–1034
  94. Rakhit R, Cunningham P, Furtos-Matei A, Dahan S, Qi XF, Crow JP, et al. Oxidation-induced misfolding and aggregation of superoxide dismutase and its implications for amyotrophic lateral sclerosis. J Biol Chem. 2002;277(49):47551–47556
  95. Schlattner U, Forstner M, Eder M, Stachowiak O, Fritz-Wolf K, Wallimann T. Functional aspects of the X-ray structure of mitochondrial creatine kinase: a molecular physiology approach. Mol Cell Biochem. 1998;184(1–2):125–140
  96. Selkoe DJ, Bell DS, Podlisny MB, Price DL, Cork LC. Conservation of brain amyloid proteins in aged mammals and humans with Alzheimer's disease. Science. 1987;235(4791):873–877
  97. Selverstone Valentine J, Doucette PA, Zittin Potter S. Copper–zinc superoxide dismutase and amyotrophic lateral sclerosis. Annu Rev Biochem. 2005;74:563–593
  98. Singh SP, Janecki AJ, Srivastava SK, Awasthi S, Awasthi YC, Xia SJ, et al. Membrane association of glutathione S-transferase mGSTA4-4, an enzyme that metabolizes lipid peroxidation products. J Biol Chem. 2002;277(6):4232–4239
  99. Smith CD, Carney JM, Starke-Reed PE, Oliver CN, Stadtman ER, Floyd RA, et al. Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease. Proc Natl Acad Sci USA. 1991;88(23):10540–10543
  100. Stachowiak O, Dolder M, Wallimann T, Richter C. Mitochondrial creatine kinase is a prime target of peroxynitrite-induced modification and inactivation. J Biol Chem. 1998;273(27):16694–16699
  101. Stevens MJ, Obrosova I, Cao X, Van Huysen C, Greene DA. Effects of dl-alpha-lipoic acid on peripheral nerve conduction, blood flow, energy metabolism, and oxidative stress in experimental diabetic neuropathy. Diabetes. 2000;49(6):1006–1015
  102. Studzinski CM, Christie LA, Araujo JA, Burnham WM, Head E, Cotman CW, et al. Visuospatial function in the beagle dog: an early marker of cognitive decline in a model of human aging and dementia. Neurobiol Learn Mem. 2006;
  103. Su MY, Head E, Brooks WM, Wang Z, Muggenburg BA, Adam GE, et al. Magnetic resonance imaging of anatomic and vascular characteristics in a canine model of human aging. Neurobiol Aging. 1998;19(5):479–485
  104. Sultana R, Butterfield DA. Oxidatively modified GST and MRP1 in Alzheimer's disease brain: implications for accumulation of reactive lipid peroxidation products. Neurochem Res. 2004;29(12):2215–2220
  105. Sultana R, Ravagna A, Mohmmad-Abdul H, Calabrese V, Butterfield DA. Ferulic acid ethyl ester protects neurons against amyloid beta-peptide(1–42)-induced oxidative stress and neurotoxicity: relationship to antioxidant activity. J Neurochem. 2005;92(4):749–758
  106. Sultana R, Poon HF, Cai J, Pierce WM, Merchant M, Klein JB, et al. Identification of nitrated proteins in Alzheimer's disease brain using a redox proteomics approach. Neurobiol Dis. 2006;22:76–87
  107. Takahashi M, Dore S, Ferris CD, Tomita T, Sawa A, Wolosker H, et al. Amyloid precursor proteins inhibit heme oxygenase activity and augment neurotoxicity in Alzheimer's disease. Neuron. 2000;28(2):461–473
  108. Tapp PD, Siwak CT, Estrada J, Head E, Muggenburg BA, Cotman CW, et al. Size and reversal learning in the beagle dog as a measure of executive function and inhibitory control in aging. Learn Mem. 2003;10(1):64–73
  109. Tapp D, Siwak CT, Zicker SC, Head E, Muggenburg BA, Cotman CW, et al. An antioxidant enriched diet improves concept learning in aged dogs. Soc Neurosci Abstr. 2003;[abstract 836.12]
  110. Tapp PD, Siwak CT, Gao FQ, Chiou JY, Black SE, Head E, et al. Frontal lobe volume, function, and beta-amyloid pathology in a canine model of aging. J Neurosci. 2004;24(38):8205–8213
  111. Tapp PD, Head K, Head E, Milgram NW, Muggenburg BA, Su MY. Application of an automated voxel-based morphometry technique to assess regional gray and white matter brain atrophy in a canine model of aging. Neuroimage. 2006;29(1):234–244
  112. Thongboonkerd V, McLeish KR, Arthur JM, Klein JB. Proteomic analysis of normal human urinary proteins isolated by acetone precipitation or ultracentrifugation. Kidney Int. 2002;62(4):1461–1469
  113. Tyrrell R. Redox regulation and oxidant activation of heme oxygenase-1. Free Radic Res. 1999;31(4):335–340
  114. Valentine JS. Do oxidatively modified proteins cause ALS?. Free Radic Biol Med. 2002;33(10):1314–1320
  115. van Praag H, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci. 1999;2(3):266–270
  116. Varadarajan S, Kanski J, Aksenova M, Lauderback C, Butterfield DA. Different mechanisms of oxidative stress and neurotoxicity for Alzheimer's A beta(1–42) and A beta(25–35). J Am Chem Soc. 2001;123(24):5625–5631
  117. Wallimann T, Dolder M, Schlattner U, Eder M, Hornemann T, O’Gorman E, et al. Some new aspects of creatine kinase (CK): compartmentation, structure, function and regulation for cellular and mitochondrial bioenergetics and physiology. Biofactors. 1998;8(3–4):229–234
  118. Wu B, Gu MJ, Heydari AR, Richardson A. The effect of age on the synthesis of two heat shock proteins in the hsp70 family. J Gerontol. 1993;48(2):B50–B56

PII: S0197-4580(06)00347-2

doi: 10.1016/j.neurobiolaging.2006.09.012

Neurobiology of Aging
Volume 29, Issue 1 , Pages 51-70 , January 2008