Quantitative proteomics analysis of specific protein expression and oxidative modification in aged senescence-accelerated-prone 8 mice brain

Neuroscience

Volumn 126, Issue 4, 2004, Pages 915-926

  Poon, H F ^a   Castegna, A ^a   Farr, S A ^b,c   Thongboonkerd, V ^d   Lynn, B C ^a,e   Banks, W A ^c   Morley, J E ^c   Klein, J B ^d   Butterfield, D A ^a,e  

^a UNIVERSITY OF KENTUCKY   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF LOUISVILLE SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF KENTUCKY   (United States)

Author keywords

2,4 dinitrophenyl hydrazone; A ; AD; ALS; Alzheimer's disease; amyloid ; amyotrophic lateral sclerosis; CK; collapsin response mediator protein; creatine kinase; CRMP; dihydropyrimidinase like protein 2; DNP; Down syndrome; DRP 2; DS; hsp86

Indexed keywords

CREATINE KINASE; DIHYDROPYRIMIDINASE; DIHYDROPYRIMIDINASE LIKE PROTEIN 2; FODRIN; GLYCINE CLEAVAGE SYSTEM; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 86; LACTATE DEHYDROGENASE; TRIOSEPHOSPHATE ISOMERASE; UNCLASSIFIED DRUG;

AMNESIA; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; LEARNING DISORDER; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SENESCENCE;

AGING; ANIMALS; BLOTTING, WESTERN; BRAIN; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION; MALE; MASS SPECTROMETRY; MICE; MICE, INBRED STRAINS; MICE, NEUROLOGIC MUTANTS; OXIDATIVE STRESS; PROTEINS; PROTEOMICS;

EID: 2942659505     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.04.046     Document Type: Article

References (151)

1. Agrawal A., Shukla R., Tripathi L.M., Pandey V.C., Srimal R.C. Permeability function related to cerebral microvessel enzymes during ageing in rats. Int J Dev Neurosci. 14:1996;87-91
2. Aksenov M., Aksenova M., Butterfield D.A., Markesbery W.R. Oxidative modification of creatine kinase BB in Alzheimer's disease brain. J Neurochem. 74:2000;2520-2527
3. Aksenova M.V., Aksenov M.Y., Carney J.M., Butterfield D.A. Protein oxidation and enzyme activity decline in old brown Norway rats are reduced by dietary restriction. Mech Ageing Dev. 100:1998;157-168
4. Aksenova M.V., Aksenov M.Y., Payne R.M., Trojanowski J.Q., Schmidt M.L., Carney J.M., Butterfield D.A., Markesbery W.R. Oxidation of cytosolic proteins and expression of creatine kinase BB in frontal lobe in different neurodegenerative disorders. Dement Geriatr Cogn Disord. 10:1999;158-165
5. Arimura N., Inagaki N., Chihara K., Menager C., Nakamura N., Amano M., Iwamatsu A., Goshima Y., Kaibuchi K. Phosphorylation of collapsin response mediator protein-2 by Rho-kinase Evidence for two separate signaling pathways for growth cone collapse. J Biol Chem. 275:2000;23973-23980
6. Bahr B.A., Lam N., Lynch G. Changes in the concentrations of tau and other structural proteins in the brains of aged mice. Neurosci Lett. 175:1994;49-52
7. Bahr B.A., Vanderklish P.W., Ha L.T., Tin M.T., Lynch G. Spectrin breakdown products increase with age in telencephalon of mouse brain. Neurosci Lett. 131:1991;237-240
8. Bajo M., Yoo B.C., 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. 21:2001;293-301
9. Banks W.A., Farr S.A., Butt W., Kumar V.B., Franko M.W., Morley J.E. 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 Pharmacol Exp Ther. 297:2001;1113-1121
10. Bergeron C., Beric-Maskarel K., Muntasser S., Weyer L., Somerville M.J., Percy M.E. Neurofilament light and polyadenylated mRNA levels are decreased in amyotrophic lateral sclerosis motor neurons. J Neuropathol Exp Neurol. 53:1994;221-230
11. Brady S.T. Motor neurons and neurofilaments in sickness and in health. Cell. 73:1993;1-3
12. Brugge J.S. Interaction of the Rous sarcoma virus protein pp60src with the cellular proteins pp50 and pp90. Curr Top Microbiol Immunol. 123:1986;1-22
13. Butterfield D.A., Boyd-Kimball D., Castegna A. Proteomics in Alzheimer's disease: Insights into mechanisms of neurodegeneration. J Neurochem. 86:2003;1313-1327
14. Butterfield D.A., Castegna A. Proteomics for the identification of specially oxidized proteins in brain: Technology and applications to the study of neurodegenerative disorders. Amino Acids. 25:2003;419-425
15. Butterfield D.A., Castegna A., Lauderback C.M., Drake J. Evidence that amyloid beta-peptide-induced lipid peroxidation and its sequelae in Alzheimer's disease brain contribute to neuronal death. Neurobiol Aging. 23:2003;655-664
16. Butterfield D.A., Howard B., Yatin S., Koppal T., Drake J., Hensley K., Aksenov M., Aksenova M., Subramaniam R., Varadarajan S., Harris-White M.E., Pedigo N.W. Jr, Carney J.M. Elevated oxidative stress in models of normal brain aging and Alzheimer's disease. Life Sci. 65:1999;1883-1892
17. 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. 94:1997;674-678
18. Butterfield D.A., Stadtman E.R. Protein oxidation processes in aging brain. Adv Cell Aging Gerontol. 2:1997;161-191
19. Byk T., Dobransky T., Cifuentes-Diaz C., Sobel A. Identification and molecular characterization of Unc-33-like phosphoprotein (Ulip), a putative mammalian homolog of the axonal guidance-associated unc-33 gene product. J Neurosci. 16:1996;688-701
20. Calabrese V., Scapagnini G., Ravagna A., Colombrita C., Spadaro F., Butterfield D.A., Giuffrida Stella A.M. Increased expression of heat shock proteins in rat brain during aging Relationship with mitochondrial function and glutathione redox state. Mech Ageing Dev. 125:2004;325-335
21. Cammarata S., Mancardi G., Tabaton M. Formic acid treatment exposes hidden neurofilament and tau epitopes in abnormal cytoskeletal filaments from patients with progressive supranuclear palsy and Alzheimer's disease. Neurosci Lett. 115:1990;351-355
22. Castegna A., Aksenov M., Aksenova M., Thongboonkerd V., Klein J.B., Pierce W.M., Booze R., Markesbery W.R., Butterfield D.A. 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. 33:2002;562-571
23. Castegna A., Aksenov M., Thongboonkerd V., Klein J.B., Pierce W.M., Booze R., Markesbery W.R., Butterfield D.A. 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. 82:2002;1524-1532
24. Castegna A., Thongboonkerd V., Klein J.B., Lynn B., Markesbery W.R., Butterfield D.A. Proteomic identification of nitrated proteins in Alzheimer's disease brain. J Neurochem. 85:2003;1394-1401
25. Castegna A., Thongboonkerd V., Klein J.B., Lynn B., Markesbery W.R., Butterfield D.A. Proteomic identification of oxidatively modified proteins in gracile axonal dystrophy mice. J Neurochem. 88:2004;1540-1546
26. Chandrasekaran K., Giordano T., Brady D.R., Stoll J., Martin L.J., Rapoport S.I. Impairment in mitochondrial cytochrome oxidase gene expression in Alzheimer disease. Brain Res Mol Brain Res. 24:1994;336-340
27. Chen W., Wieraszko A., Hogan M.V., Yang H.A., Kornecki E., Ehrlich Y.H. Surface protein phosphorylation by ecto-protein kinase is required for the maintenance of hippocampal long-term potentiation. Proc Natl Acad Sci USA. 93:1996;8688-8693
28. Clay S.A., Shore N.A., Landing B.H. Triosephosphate isomerase deficiency A case report with neuropathological findings. Am J Dis Child. 136:1982;800-802
29. Conconi M., Friguet B. Proteasome inactivation upon aging and on oxidation-effect of HSP 90. Mol Biol Rep. 24:1997;45-50
30. Conconi M., Szweda L.I., Levine R.L., Stadtman E.R., Friguet B. Age-related decline of rat liver multicatalytic proteinase activity and protection from oxidative inactivation by heat-shock protein 90. Arch Biochem Biophys. 331:1996;232-240
31. Cote F., Collard J.F., Julien J.P. Progressive neuronopathy in transgenic mice expressing the human neurofilament heavy gene A mouse model of amyotrophic lateral sclerosis. Cell. 73:1993;35-46
32. Crow J.P., Ye Y.Z., Strong M., Kirk M., Barnes S., Beckman J.S. Superoxide dismutase catalyzes nitration of tyrosines by peroxynitrite in the rod and head domains of neurofilament-L. J Neurochem. 69:1997;1945-1953
33. David S., Shoemaker M., Haley B.E. Abnormal properties of creatine kinase in Alzheimer's disease brain Correlation of reduced enzyme activity and active site photolabeling with aberrant cytosol-membrane partitioning. Brain Res Mol Brain Res. 54:1998;276-287
34. Davies K.J. Degradation of oxidized proteins by the 20S proteasome. Biochimie. 83:2001;301-310
35. el-Mallakh R.S., Egan M., Wyatt R.J. Creatine kinase and enolase Intracellular enzymes serving as markers of central nervous system damage in neuropsychiatric disorders. Psychiatry. 55:1992;392-402
36. Eppenberger H.M., Dawson D.M., Kaplan N.O. The comparative enzymology of creatine kinases: I. Isolation and characterization from chicken and rabbit tissues. J Biol Chem. 242:1967;204-209
37. Farr S.A., Poon H.F., Dogrukol-Ak D., Drake J., Banks W.A., Eyerman E., Butterfield D.A., Morley J.E. The antioxidants alpha-lipoic acid and N-acetylcysteine reverse memory impairment and brain oxidative stress in aged SAMP8 mice. J Neurochem. 84:2003;1173-1183
38. Ferrante F., Amenta F. Enzyme histochemistry of the choroid plexus in old rats. Mech Ageing Dev. 41:1987;65-72
39. Flood J.F., Farr S.A., Kaiser F.E., Morley J.E. Age-related impairment in learning but not memory in SAMP8 female mice. Pharmacol Biochem Behav. 50:1995;661-664
40. Flood J.F., Harris F.J., Morley J.E. Age-related changes in hippocampal drug facilitation of memory processing in SAMP8 mice. Neurobiol Aging. 17:1996;15-24
41. Flood J.F., Morley J.E. Age-related changes in footshock avoidance acquisition and retention in senescence accelerated mouse (SAM). Neurobiol Aging. 14:1993;153-157
42. Fu C., Cao C.M., Xia Q., Yang J., Lu Y. [Reactive oxygen species and mitochondrial K(ATP)-sensitive channels mediated cardioprotection induced by TNF-alpha during hypoxia and reoxygenation]. Sheng Li Xue Bao. 55:2003;284-289
43. Fujii S., Ito K., Osada H., Hamaguchi T., Kuroda Y., Kato H. Extracellular phosphorylation of membrane protein modifies theta burst-induced long-term potentiation in CA1 neurons of guinea-pig hippocampal slices. Neurosci Lett. 187:1995;133-136
44. Fukata Y., Itoh T.J., Kimura T., Menager C., Nishimura T., Shiromizu T., Watanabe H., Inagaki N., Iwamatsu A., Hotani H., Kaibuchi K. CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat Cell Biol. 4:2002;583-591
45. Gelinas S., Chapados C., Beauregard M., Gosselin I., Martinoli M.G. Effect of oxidative stress on stability and structure of neurofilament proteins. Biochem Cell Biol. 78:2000;667-674
46. Gelot A., Moreau J., Khrestchatisky M., Ben Ari Y., Pollard H. Developmental change of alpha-spectrin mRNA in the rat brain. Brain Res Dev Brain Res. 81:1994;240-246
47. Giallongo A., Oliva D., Cali L., Barba G., Barbieri G., Feo S. Structure of the human gene for alpha-enolase. Eur J Biochem. 190:1990;567-573
48. Goldman J.E., Yen S.H., Chiu F.C., Peress N.S. Lewy bodies of Parkinson's disease contain neurofilament antigens. Science. 221:1983;1082-1084
49. Goshima Y., Nakamura F., Strittmatter P., Strittmatter S.M. Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33. Nature. 376:1995;509-514
50. Grune T., Merker K., Sandig G., Davies K.J. Selective degradation of oxidatively modified protein substrates by the proteasome. Biochem Biophys Res Commun. 305:2003;709-718
51. Grune T., Reinheckel T., Davies K.J. Degradation of oxidized proteins in K562 human hematopoietic cells by proteasome. J Biol Chem. 271:1996;15504-15509
52. Gu Y., Ihara Y. Evidence that collapsin response mediator protein-2 is involved in the dynamics of microtubules. J Biol Chem. 275:2000;17917-17920
53. Hamajima N., Matsuda K., Sakata S., Tamaki N., Sasaki M., Nonaka M. A novel gene family defined by human dihydropyrimidinase and three related proteins with differential tissue distribution. Gene. 180:1996;157-163
54. Hamre K.M., Cassell M.D., West J.R. The development of laminar staining for neuron-specific enolase in the rat somatosensory cortex. Brain Res Dev Brain Res. 46:1989;213-220
55. Harada J., Sugimoto M. Activation of caspase-3 in beta-amyloid-induced apoptosis of cultured rat cortical neurons. Brain Res. 842:1999;311-323
56. Harman D. Prolongation of life Role of free radical reactions in aging. J Am Geriatr Soc. 17:1969;721-735
57. Hayes G.M., Howlett D.R., Griffin G.E. Production of beta-amyloid by primary human foetal mixed brain cell cultures and its modulation by exogenous soluble beta-amyloid. Neuroscience. 113:2002;641-646
58. Hedgecock E.M., Culotti J.G., Thomson J.N., Perkins L.A. Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev Biol. 111:1985;158-170
59. Hensley K., Howard B.J., Carney J.M., Butterfield D.A. Membrane protein alterations in rodent erythrocytes and synaptosomes due to aging and hyperoxia. Biochim Biophys Acta. 1270:1995;203-206
60. Hoffman P.N., Cleveland D.W., Griffin J.W., Landes P.W., Cowan N.J., Price D.L. Neurofilament gene expression A major determinant of axonal caliber. Proc Natl Acad Sci USA. 84:1987;3472-3476
61. Hoyer S. Memory function and brain glucose metabolism. Pharmacopsychiatry. 36:(Suppl 1):2003;S62-S67
62. Hrachovina V., Mourek J. [Lactate dehydrogenase and malate dehydrogenase activity in the glial and neuronal fractions of the brain tissue in rats of various ages]. Sb Lek. 92:1990;39-44
63. Hu Y.Y., He S.S., Wang X.C., Duan Q.H., Khatoon S., Iqbal K., Grundke-Iqbal I., Wang J.Z. Elevated levels of phosphorylated neurofilament proteins in cerebrospinal fluid of Alzheimer disease patients. Neurosci Lett. 320:2002;156-160
64. Ikegami S., Shumiya S., Kawamura H. Age-related changes in radial-arm maze learning and basal forebrain cholinergic systems in senescence accelerated mice (SAM). Behav Brain Res. 51:1992;15-22
65. Inai Y., Nishikimi M. Increased degradation of oxidized proteins in yeast defective in 26 S proteasome assembly. Arch Biochem Biophys. 404:2002;279-284
66. Iwangoff P., Armbruster R., Enz A., Meier-Ruge W. Glycolytic enzymes from human autoptic brain cortex Normal aged and demented cases. Mech Ageing Dev. 14:1980;203-209
67. Jensen O.N., Wilm M., Shevchenko A., Mann M. Sample preparation methods for mass spectrometric peptide mapping directly from 2-DE gels. Methods Mol Biol. 112:1999;513-530
68. Johnston-Wilson N.L., Sims C.D., Hofmann J.P., Anderson L., Shore A.D., Torrey E.F., Yolken R.H. Disease-specific alterations in frontal cortex brain proteins in schizophrenia, bipolar disorder, and major depressive disorder The stanley neuropathology consortium. Mol Psychiatry. 5:2000;142-149
69. Kaldis P., Furter R., Wallimann T. The N-terminal heptapeptide of mitochondrial creatine kinase is important for octamerization. Biochemistry. 33:1994;952-959
70. Kato K., Kurobe N., Suzuki F., Morishita R., Asano T., Sato T., Inagaki T. Concentrations of several proteins characteristic of nervous tissue in cerebral cortex of patients with Alzheimer's disease. J Mol Neurosci. 3:1991;95-99
71. Kato K., Suzuki F., Morishita R., Asano T., Sato T. Selective increase in S-100 beta protein by aging in rat cerebral cortex. J Neurochem. 54:1990;1269-1274
72. Kato Y., Hamajima N., Inagaki H., Okamura N., Koji T., Sasaki M., Nonaka M. Post-meiotic expression of the mouse dihydropyrimidinase-related protein 3 (DRP-3) gene during spermiogenesis. Mol Reprod Dev. 51:1998;105-111
73. Kawamata T., Akiguchi I., Maeda K., Tanaka C., Higuchi K., Hosokawa M., Takeda T. Age-related changes in the brains of senescence-accelerated mice (SAM) Association with glial and endothelial reactions. Microsc Res Tech. 43:1998;59-67
74. Keller A., Berod A., Dussaillant M., Lamande N., Gros F., Lucas M. Coexpression of alpha and gamma enolase genes in neurons of adult rat brain. J Neurosci Res. 38:1994;493-504
75. Koyasu S., Nishida E., Kadowaki T., Matsuzaki F., Iida K., Harada F., Kasuga M., Sakai H., Yahara I. Two mammalian heat shock proteins, HSP90 and HSP100, are actin-binding proteins. Proc Natl Acad Sci USA. 83:1986;8054-8058
76. 2+-calmodulin-regulated actin-binding protein. J Biol Chem. 264:1989;15083-15087
77. Krekoski C.A., Parhad I.M., Fung T.S., Clark A.W. Aging is associated with divergent effects on Nf-L and GFAP transcription in rat brain. Neurobiol Aging. 17:1996;833-841
78. Kumar V.B., Farr S.A., Flood J.F., Kamlesh V., Franko M., Banks W.A., Morley J.E. Site-directed antisense oligonucleotide decreases the expression of amyloid precursor protein and reverses deficits in learning and memory in aged SAMP8 mice. Peptides. 21:2000;1769-1775
79. Kumar V.B., Vyas K., Franko M., Choudhary V., Buddhiraju C., Alvarez J., Morley J.E. Molecular cloning, expression, and regulation of hippocampal amyloid precursor protein of senescence accelerated mouse (SAMP8). Biochem Cell Biol. 79:2001;57-67
80. Lai J.C., White B.K., Buerstatte C.R., Haddad G.G., Novotny E.J. Jr, Behar K.L. Chronic hypoxia in development selectively alters the activities of key enzymes of glucose oxidative metabolism in brain regions. Neurochem Res. 28:2003;933-940
81. Lee M.K., Xu Z., Wong P.C., Cleveland D.W. Neurofilaments are obligate heteropolymers in vivo. J Cell Biol. 122:1993;1337-1350
82. Lee S.J. Expression of HSP86 in male germ cells. Mol Cell Biol. 10:1990;3239-3242
83. Leto T.L., Fortugno-Erikson D., Barton D., Yang-Feng T.L., Francke U., Harris A.S., Morrow J.S., Marchesi V.T., Benz E.J. Jr. Comparison of nonerythroid alpha-spectrin genes reveals strict homology among diverse species. Mol Cell Biol. 8:1988;1-9
84. Levine R.L., Williams J.A., Stadtman E.R., Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 233:1994;346-357
85. Lubec G., Nonaka M., Krapfenbauer K., Gratzer M., Cairns N., Fountoulakis M. Expression of the dihydropyrimidinase related protein 2 (DRP-2) in Down syndrome and Alzheimer's disease brain is downregulated at the mRNA and dysregulated at the protein level. J Neural Transm Suppl. 57:1999;161-177
86. Lushchak V.I., Bahnjukova T.V., Storey K.B. Effect of hypoxia on the activity and binding of glycolytic and associated enzymes in sea scorpion tissues. Braz J Med Biol Res. 31:1998;1059-1067
87. Lynch G., Baudry M. The biochemistry of memory A new and specific hypothesis. Science. 224:1984;1057-1063
88. Maekawa M., Sudo K., Kitajima M., Matsuura Y., Li S.S., Kanno T. Analysis of a genetic mutation in an electrophoretic variant of the human lactate dehydrogenase-B(H) subunit. Hum Genet. 91:1993;423-426
89. Manetto V., Sternberger N.H., Perry G., Sternberger L.A., Gambetti P. Phosphorylation of neurofilaments is altered in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol. 47:1988;642-653
90. Marangos P.J., Schmechel D.E. Neuron specific enolase, a clinically useful marker for neurons and neuroendocrine cells. Annu Rev Neurosci. 10:1987;269-295
91. Matts R.L., Hurst R. Evidence for the association of the heme-regulated eIF-2 alpha kinase with the 90-kDa heat shock protein in rabbit reticulocyte lysate in situ. J Biol Chem. 264:1989;15542-15547
92. Maxwell G.D., Whitehead M.C., Connolly S.M., Marangos P.J. Development of neuron-specific enolase immunoreactivity in avian nervous tissue in vivo and in vitro. Brain Res. 255:1982;401-418
93. Meier-Ruge W., Iwangoff P., Reichlmeier K. Neurochemical enzyme changes in Alzheimer's and Pick's disease. Arch Gerontol Geriatr. 3:1984;161-165
94. Minturn J.E., Fryer H.J., Geschwind D.H., Hockfield S. TOAD-64, a gene expressed early in neuronal differentiation in the rat, is related to unc-33, a C. elegans gene involved in axon outgrowth. J Neurosci. 15:1995;6757-6766
95. Miyamoto M. Characteristics of age-related behavioral changes in senescence-accelerated mouse SAMP8 and SAMP10. Exp Gerontol. 32:1997;139-148
96. Miyata Y., Yahara I. The 90-kDa heat shock protein, HSP90, binds and protects casein kinase II from self-aggregation and enhances its kinase activity. J Biol Chem. 267:1992;7042-7047
97. Miyata Y., Yahara I. Interaction between casein kinase II and the 90-kDa stress protein, HSP90. Biochemistry. 34:1995;8123-8129
98. Mizuno Y., Ohta K. Regional distributions of thiobarbituric acid-reactive products, activities of enzymes regulating the metabolism of oxygen free radicals, and some of the related enzymes in adult and aged rat brains. J Neurochem. 46:1986;1344-1352
99. Moore S.K., Kozak C., Robinson E.A., Ullrich S.J., Appella E. Murine 86- and 84-kDa heat shock proteins, cDNA sequences, chromosome assignments, and evolutionary origins. J Biol Chem. 264:1989;5343-5351
100. Moore S.K., Rijli F., Appella E. Characterization of the mouse 84-kD heat shock protein gene family. DNA Cell Biol. 9:1990;387-400
101. Morley J.E., Farr S.A., Kumar V.B., Banks W.A. Alzheimer's disease through the eye of a mouse Acceptance lecture for the 2001 gayle a. Olson and Richard D. Olson prize Peptides. 23:2002;589-599
102. Morley J.E., Kumar V.B., Bernardo A.E., Farr S.A., Uezu K., Tumosa N., Flood J.F. Beta-amyloid precursor polypeptide in SAMP8 mice affects learning and memory. Peptides. 21:2000;1761-1767
103. Munoz D.G., Greene C., Perl D.P., Selkoe D.J. Accumulation of phosphorylated neurofilaments in anterior horn motoneurons of amyotrophic lateral sclerosis patients. J Neuropathol Exp Neurol. 47:1988;9-18
104. Nardai G., Csermely P., Soti C. Chaperone function and chaperone overload in the aged A preliminary analysis. Exp Gerontol. 37:2002;1257-1262
105. Nomura Y., Yamanaka Y., Kitamura Y., Arima T., Ohnuki T., Oomura Y., Sasaki K., Nagashima K., Ihara Y. Senescence-accelerated mouse Neurochemical studies on aging. Ann NY Acad Sci. 786:1996;410-418
106. Ohta A., Hirano T., Yagi H., Tanaka S., Hosokawa M., Takeda T. Behavioral characteristics of the SAM-P/8 strain in Sidman active avoidance task. Brain Res. 498:1989;195-198
107. Okabe S., Miyasaka H., Hirokawa N. Dynamics of the neuronal intermediate filaments. J Cell Biol. 121:1993;375-386
108. Okatani Y., Wakatsuki A., Reiter R.J., Miyahara Y. Melatonin reduces oxidative damage of neural lipids and proteins in senescence-accelerated mouse. Neurobiol Aging. 23:2002;639-644
109. Ozaki M., Haga S., Zhang H.Q., Irani K., Suzuki S. Inhibition of hypoxia/reoxygenation-induced oxidative stress in HGF-stimulated antiapoptotic signaling Role of pi3-k and akt kinase upon rac1. Cell Death Differ. 10:2003;508-515
110. Pasterkamp R.J., Giger R.J., Verhaagen J. Regulation of semaphorin III/collapsin-1 gene expression during peripheral nerve regeneration. Exp Neurol. 153:1998;313-327
111. Perdew G.H. Association of the Ah receptor with the 90-kDa heat shock protein. J Biol Chem. 263:1988;13802-13805
112. Perdew G.H., Hord N., Hollenback C.E., Welsh M.J. Localization and characterization of the 86- and 84-kDa heat shock proteins in Hepa 1c1c7 cells. Exp Cell Res. 209:1993;350-356
113. Poon, HF, Calabrese, V, Scapagnini, G, Butterfield, DA (2004) Free radicals: key to brain aging and heme oxygenase as a cellular response to oxidative stress. J Gerontol, Part A, 59:478-493.
114. Pratt W.B. Interaction of hsp90 with steroid receptors Organizing some diverse observations and presenting the newest concepts. Mol Cell Endocrinol. 74:1990;C69-C76
115. Rebbe N.F., Hickman W.S., Ley T.J., Stafford D.W., Hickman S. Nucleotide sequence and regulation of a human 90-kDa heat shock protein gene. J Biol Chem. 264:1989;15006-15011
116. Roberts R. Purification of canine myocardial mitochondrial creatine kinase. Experientia. 36:1980;632-634
117. Rose D.W., Welch W.J., Kramer G., Hardesty B. Possible involvement of the 90-kDa heat shock protein in the regulation of protein synthesis. J Biol Chem. 264:1989;6239-6244
118. Rosenberg R.N. The molecular and genetic basis of AD The end of the beginning: the 2000 wartenberg lecture. Neurology. 54:2000;2045-2054
119. Sakai I., Sharief F.S., Pan Y.C., Li S.S. The cDNA and protein sequences of human lactate dehydrogenase B. Biochem J. 248:1987;933-936
120. Schlegel J., Wyss M., Eppenberger H.M., Wallimann T. Functional studies with the octameric and dimeric form of mitochondrial creatine kinase Differential ph-dependent association of the two oligomeric forms with the inner mitochondrial membrane. J Biol Chem. 265:1990;9221-9227
121. Schmidt M.L., Murray J., Lee V.M., Hill W.D., Wertkin A., Trojanowski J.Q. Epitope map of neurofilament protein domains in cortical and peripheral nervous system Lewy bodies. Am J Pathol. 139:1991;53-65
122. Schonberger S.J., Edgar P.F., Kydd R., Faull R.L., Cooper G.J. Proteomic analysis of the brain in Alzheimer's disease Molecular phenotype of a complex disease process. Proteomics. 1:2001;1519-1528
123. Schurr A., Payne R.S., Miller J.J., Rigor B.M. Brain lactate is an obligatory aerobic energy substrate for functional recovery after hypoxia Further in vitro validation. J Neurochem. 69:1997;423-426
124. Schurr A., Payne R.S., Miller J.J., Rigor B.M. Brain lactate, not glucose, fuels the recovery of synaptic function from hypoxia upon reoxygenation An in vitro study. Brain Res. 744:1997;105-111
125. Sheline C.T., Choi D.W. Neuronal death in cultured murine cortical cells is induced by inhibition of GAPDH and triosephosphate isomerase. Neurobiol Dis. 5:1998;47-54
126. 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. 73:1998;557-569
127. Sobel B.E., Shell W.E., Klein M.S. An isoenzyme of creatine phosphokinase associated with rabbit heart mitochondria. J Mol Cell Cardiol. 4:1972;367-380
128. Sudo K., Maekawa M., Kanno T., Li S.S., Akizuki S., Magara T. Premature termination mutations in two patients with deficiency of lactate dehydrogenase H(B) subunit. Clin Chem. 40:1994;1567-1570
129. Takeda S., Okabe S., Funakoshi T., Hirokawa N. Differential dynamics of neurofilament-H protein and neurofilament-L protein in neurons. J Cell Biol. 127:1994;173-185
130. Takeda T., Hosokawa M., Takeshita S., Irino M., Higuchi K., Matsushita T., Tomita Y., Yasuhira K., Hamamoto H., Shimizu K., Ishii M., Yamamuro T. A new murine model of accelerated senescence. Mech Ageing Dev. 17:1981;183-194
131. Tholey G., Ledig M., Mandel P. Modifications in energy metabolism during the development of chick glial cells and neurons in culture. Neurochem Res. 7:1982;27-36
132. Thongboonkerd V., Luengpailin J., Cao J., Pierce W.M., Cai J., Klein J.B., Doyle R.J. Fluoride exposure attenuates expression of Streptococcus pyogenes virulence factors. J Biol Chem. 277:2002;16599-16605
133. Toyoshima I., Yamamoto A., Masamune O., Satake M. Phosphorylation of neurofilament proteins and localization of axonal swellings in motor neuron disease. J Neurol Sci. 89:1989;269-277
134. Trapp B.D., Marangos P.J., Webster H.D. Immunocytochemical localization and developmental profile of neuron specific enolase (NSE) and non-neuronal enolase (NNE) in aggregating cell cultures of fetal rat brain. Brain Res. 220:1981;121-130
135. Troost D., Sillevis Smitt P.A., de Jong J.M., Swaab D.F. Neurofilament and glial alterations in the cerebral cortex in amyotrophic lateral sclerosis. Acta Neuropathol (Berl). 84:1992;664-673
136. Ulrich J., Anderton B.H., Probst A. Alzheimer dementia A study of the senile plaque with antisera and a monoclonal antibody specific for neurofilament proteins. Acta Histochem Suppl. 34:1987;115-121
137. Ulrich J., Haugh M., Anderton B.H., Probst A., Lautenschlager C., His B. Alzheimer dementia and Pick's disease Neurofibrillary tangles and pick bodies are associated with identical phosphorylated neurofilament epitopes. Acta Neuropathol (Berl). 73:1987;240-246
138. Vanderklish P.W., Bahr B.A. The pathogenic activation of calpain A marker and mediator of cellular toxicity and disease states. Int J Exp Pathol. 81:2000;323-339
139. Wallimann T., Wyss M., Brdiczka D., Nicolay K., Eppenberger H.M. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands The 'phosphocreatine circuit' for cellular energy homeostasis. Biochem J. 281:(Pt 1):1992;21-40
140. Wang L.H., Strittmatter S.M. A family of rat CRMP genes is differentially expressed in the nervous system. J Neurosci. 16:1996;6197-6207
141. Weitzdoerfer R., Fountoulakis M., Lubec G. Aberrant expression of dihydropyrimidinase related proteins-2, -3 and -4 in fetal Down syndrome brain. J Neural Transm Suppl. 61:2001;95-107
142. Welch W.J. Mammalian stress response Cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol Rev. 72:1992;1063-1081
143. Whitehead M.C., Marangos P.J., Connolly S.M., Morest D.K. Synapse formation is related to the onset of neuron-specific enolase immunoreactivity in the avian auditory and vestibular systems. Dev Neurosci. 5:1982;298-307
144. Wieraszko A., Ehrlich Y.H. On the role of extracellular ATP in the induction of long-term potentiation in the hippocampus. J Neurochem. 63:1994;1731-1738
145. Wyss M., Smeitink J., Wevers R.A., Wallimann T. Mitochondrial creatine kinase A key enzyme of aerobic energy metabolism. Biochim Biophys Acta. 1102:1992;119-166
146. Yagi H., Katoh S., Akiguchi I., Takeda T. Age-related deterioration of ability of acquisition in memory and learning in senescence accelerated mouse Sam-p/8 as an animal model of disturbances in recent memory. Brain Res. 474:1988;86-93
147. Yamazaki Y., Kaneko K., Fujii S., Kato H., Ito K. Long-term potentiation and long-term depression induced by local application of ATP to hippocampal CA1 neurons of the guinea pig. Hippocampus. 13:2003;81-92
148. Yasui F., Matsugo S., Ishibashi M., Kajita T., Ezashi Y., Oomura Y., Kojo S., Sasaki K. Effects of chronic acetyl-L-carnitine treatment on brain lipid hydroperoxide level and passive avoidance learning in senescence-accelerated mice. Neurosci Lett. 334:2002;177-180
149. 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. 24:1999;427-435
150. Zhang H., Sternberger N.H., Rubinstein L.J., Herman M.M., Binder L.I., Sternberger L.A. Abnormal processing of multiple proteins in Alzheimer disease. Proc Natl Acad Sci USA. 86:1989;8045-8049
151. Ziemiecki A., Catelli M.G., Joab I., Moncharmont B. Association of the heat shock protein hsp90 with steroid hormone receptors and tyrosine kinase oncogene products. Biochem Biophys Res Commun. 138:1986;1298-1307