Protective effect of D609 against amyloid-beta1-42-induced oxidative modification of neuronal proteins: Redox proteomics study

Journal of Neuroscience Research

Volumn 84, Issue 2, 2006, Pages 409-417

  Sultana, Rukhsana ^a,b   Newman, Shelley F ^a,b   Abdul, Hafiz Mohmmad ^a,b   Cai, Jian ^c   Pierce, William M ^c   Klein, Jon B ^d   Merchant, Michael ^d   Butterfield, D Allan ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c University of Louisville School of Medicine   (United States)

^d UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Alzheimer's disease; Oxidative stress; Protein carbonyls; Redox proteomics

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; CARBONYL DERIVATIVE; CHAPERONE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MALATE DEHYDROGENASE; PROTEIN 14 3 3 ZETA; PYRUVATE KINASE; TRICYCLO[4.3.0.1]DECAN 9 YL XANTHOGENATE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROPHORESIS; EXPERIMENTAL MODEL; IMAGE ANALYSIS; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; NERVE CELL; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEOMICS; RAT; SEQUENCE ANALYSIS; STATISTICAL ANALYSIS;

14-3-3 PROTEINS; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; BRIDGED COMPOUNDS; CELLS, CULTURED; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; IMAGE PROCESSING, COMPUTER-ASSISTED; MALATE DEHYDROGENASE; MASS SPECTROMETRY; NEURONS; NEUROPROTECTIVE AGENTS; OXIDATION-REDUCTION; PROTEIN CARBONYLATION; PROTEOMICS; PYRUVATE KINASE; RATS; RATS, SPRAGUE-DAWLEY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; THIONES;

EID: 33746397535     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.20876     Document Type: Article

References (74)

1. Agarwal-Mawal A, Qureshi HY, Cafferty PW, Yuan Z, Han D, Lin R, Paudel HK. 2003. 14-3-3 Connects glycogen synthase kinase-3 beta to tau within a brain microtubule-associated tau phosphorylation complex. J Biol Chem 278:12722-12728.
2. Aksenov M, Aksenova M, Butterfield DA, Markesbery WR. 2000. Oxidative modification of creatine kinase BB in Alzheimer's disease brain. J Neurochem 74:2520-2527.
3. Blacker D, Wilcox MA, Laird NM, Rodes L, Horvath SM, Go RC, Perry R, Watson B Jr, Bassett SS, McInnis MG, Albert MS, Hyman BT, Tanzi RE. 1998. Alpha-2 macroglobulin is genetically associated with Alzheimer disease. Nat Genet 19:357-360.
4. Blass JP, Gibson GE. 1991. The role of oxidative abnormalities in the pathophysiology of Alzheimer's disease. Rev Neurol 147:513-525.
5. 1-42: implications for proposed mechanisms of toxicity. J Alzheimers Dis 6:515-525.
6. 1-42-mediated oxidative stress and neurotoxicity: implications for Alzheimer's disease. J Neurosci Res 79:700-706.
7. 1-42-mediated oxidative stress in neuronal cell culture: a proteomics approach. J Neurosci Res 79:707-713.
8. Butterfield DA. 1997. Beta-amyloid-associated free radical oxidative stress and neurotoxicity: implications for Alzheimer's disease. Chem Res Toxicol 10:495-506.
9. 1-42-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. A review. Free Radic Res 36:1307-1313.
10. Butterfield DA. 2004. Proteomics: a new approach to investigate oxidative stress in Alzheimer's disease brain. Brain Res 1000:1-7.
11. Butterfield DA, Boyd-Kimball D. 2004. Proteomics analysis in Alzheimer's disease: new insights into mechanisms of neurodegeneration. Int Rev Neurobiol 61:159-188.
12. Butterfield DA, Lauderback CM. 2002. 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 32:1050-1060.
13. Butterfield DA, Drake J, Pocernich C, Castegna A. 2001. Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends Mol Med 7:548-554.
14. Butterfield DA, Castegna A, Lauderback CM, Drake J. 2002. Evidence that amyloid beta-peptide-induced lipid peroxidation and its sequelae in Alzheimer's disease brain contribute to neuronal death. Neurobiol Aging 23:655-664.
15. Butterfield DA, Boyd-Kimball D, Castegna A. 2003. Proteomics in Alzheimer's disease: insights into potential mechanisms of neurodegeneration. J Neurochem 86:1313-1327.
16. Castegna A, Aksenov M, Aksenova M, Thongboonkerd V, Klein JB, Pierce WM, Booze R, Markesbery WR, Butterfield DA. 2002a. 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 33:562-571.
17. Castegna A, Aksenov M, Thongboonkerd V, Klein JB, Pierce WM, Booze R, Markesbery WR, Butterfield DA. 2002b. 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 82:1524-1532.
18. Castegna A, Thongboonkerd V, Klein JB, Lynn B, Markesbery WR, Butterfield DA. 2003. Proteomic identification of nitrated proteins in Alzheimer's disease brain. J Neurochem 85:1394-1401.
19. Cooper AJL. 1997. The molecular and genetic basis of neurological disease. Newton, MA: Butterworth-Heinemann. p 1195-1230.
20. Cruts M, van Duijn CM, Backhovens H, Van den Broeck M, Wehnert A, Serneels S, Sherrington R, Hutton M, Hardy J, St. George-Hyslop PH, Hofman A, Van Broeckhoven C. 1998. Estimation of the genetic contribution of presenilin-1 and -2 mutations in a population-based study of presenile Alzheimer disease. Hum Mol Genet 7:43-51.
21. Cummings J, Ward TH, LaCasse E, Lefebvre C, St-Jean M, Durkin J, Ranson M, Dive C. 2005. Validation of pharmacodynamic assays to evaluate the clinical efficacy of an antisense compound (AEG 35156) targeted to the X-linked inhibitor of apoptosis protein XIAP. Br J Cancer 92:532-538.
22. Dahiyat M, Cumming A, Harrington C, Wischik C, Xuereb J, Corrigan F, Breen G, Shaw D, St. Clair D. 1999. Association between Alzheimer's disease and the NOS3 gene. Ann Neurol 46:664-667.
23. Dalle-Donne I, Scaloni A, Butterfield DA. 2006. Redox proteomics. New York: Wiley.
24. Dougherty MK, Morrison DK. 2004. Unlocking the code of 14-3-3. J Cell Sci 117:1875-1884.
25. 1-42 in a transgenic Caenorhabditis elegans model. Neurobiol Aging 24:415-420.
26. Fountoulakis M, Cairns N, Lubec G. 1999. Increased levels of 14-3-3 gamma and epsilon proteins in brain of patients with Alzheimer's disease and Down syndrome. J Neural Transm Suppl 57:323-335.
27. Fucci L, Oliver CN, Coon MJ, Stadtman ER. 1983. Inactivation of key metabolic enzymes by mixed-function oxidation reactions: possible implication in protein turnover and ageing. Proc Natl Acad Sci U S A 80:1521-1525.
28. Goate A, Chartier-Harlin MC, Mullan M, Brown J, Crawford F, Fidani L, Giuffra L, Haynes A, Irving N, James L, Mant R, Newton P, Rooke K, Roques P, Talbot C, Pericak-Vance M, Roses A, Williamson R, Rossor M, Owen M, Hardy J. 1991. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349:704-706.
29. Grimes CA, Jope RS. 2001. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog Neurobiol 65:391-426.
30. Hashiguchi M, Sobue K, Paudel HK. 2000. 14-3-3 Zeta is an effector of tau protein phosphorylation. J Biol Chem 275:25247-25254.
31. Hensley K, Hall N, Subramaniam R, Cole P, Harris M, Aksenov M, Aksenova M, Gabbita SP, Wu JF, Carney JM, Lovell M, Markesbery WR, Butterfield DA. 1995. Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation. J Neurochem 65:2146-2156.
32. Hernandez F, Cuadros R, Avila J. 2004. Zeta 14-3-3 protein favours the formation of human tau fibrillar polymers. Neurosci Lett 357:143-146.
33. Hernandez-Fonseca K, Montiel T, Massieu L. 2005. Inhibition of glyceraldehydes-3-phoshate dehydrogenase by oxidative stress during metabolic inhibition leads to neuronal death in cultured hippocampal neurons. Soc Neurosci Abstr 35.
34. Hurst JK, Barrette WC Jr. 1989. Leukocytic oxygen activation and microbicidal oxidative toxins. Crit Rev Biochem Mol Biol 24:271-328.
35. 2 or 2, 2-azobis-(2-amidinopropane) dihydrochloride by the glutathione mimetic tricyclodecan-9-yl-xanthogenate. Free Radic Biol Med 38:1023-1031.
36. Lauderback CM, Hackett JM, Huang FF, Keller JN, Szweda LI, Markesbery WR, Butterfield DA. 2001. 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 78:413-416.
37. Lauderback CM, Drake J, Zhou D, Hackett JM, Castegna A, Kanski J, Tsoras M, Varadarajan S, Butterfield DA. 2003. Derivatives of xanthic acid are novel antioxidants: application to synaptosomes. Free Radic Res 37:355-365.
38. Layfield R, Fergusson J, Aitken A, Lowe J, Landon M, Mayer RJ. 1996. Neurofibrillary tangles of Alzheimer's disease brains contain 14-3-3 proteins. Neurosci Lett 209:57-60.
39. Levine RL, Williams JA, Stadtman ER, Shacter E. 1994. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346-357.
40. Levy-Lahad E, Lahad A, Wijsman EM, Bird TD, Schellenberg GD. 1995. Apolipoprotein E genotypes and age of onset in early-onset familial Alzheimer's disease. Ann Neurol 38:678-680.
41. Liu R, Choi J. 2000. Age-associated decline in gamma-glutamylcysteine synthetase gene expression in rats. Free Radic Biol Med 28:566-574.
42. Lovell MA, Xie C, Markesbery WR. 2001. Acrolein is increased in Alzheimer's disease brain and is toxic to primary hippocampal cultures. Neurobiol Aging 22:187-194.
43. Lovell MA, Xiong S, Markesbery WR, Lynn BC. 2005. Quantitative proteomic analysis of mitochondria from primary neuron cultures treated with amyloid beta peptide. Neurochem Res 30:113-122.
44. Markesbery WR. 1997. Oxidative stress hypothesis in Alzheimer's disease. Free Radic Biol Med 23:134-147.
45. Markesbery WR, Lovell MA. 1998. Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiol Aging 19:33-36.
46. Maurer MH, Feldmann RE Jr, Bromme JO, Kalenka A. 2005. Comparison of statistical approaches for the analysis of proteome expression data of differentiating neural stem cells. J Proteome Res 4:96-100.
47. Meda L, Cassatella MA, Szendrei GI, Otvos L Jr, Baron P, Villalba M, Ferrari D, Rossi F. 1995. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 374:647-650.
48. Messier C, Gagnon M. 2000. Glucose regulation and brain aging. J Nutr Health Aging 4:208-213.
49. Mohmmad Abdul H, Wenk GL, Gramling M, Hauss-Wegrzyniak B, Butterfield DA. 2004. APP and PS-1 mutations induce brain oxidative stress independent of dietary cholesterol: implications for Alzheimer's disease. Neurosci Lett 368:148-150.
50. 1-42-induced oxidative stress. Neuroscience (in press).
51. Pocernich CB, Sultana R, Mohmmad Abdul H, Nath A, Butterfield DA. 2005. HIV-dementia, Tat-induced oxidative stress and antioxidant therapeutic considerations. Brain Res Brain Res Rev 50:14-26.
52. Poon HF, Farr SA, Thongboonkerd V, Lynn BC, Banks WA, Morley JE, Klein JB, Butterfield DA. 2005. 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 46:159-168.
53. Scheltens P, Korf ES. 2000. Contribution of neuroimaging in the diagnosis of Alzheimer's disease and other dementias. Curr Opin Neurol 13:391-396.
54. Schonberger SJ, Edgar PF, Kydd R, Faull RL, Cooper GJ. 2001. Proteomic analysis of the brain in Alzheimer's disease: molecular phenotype of a complex disease process. Proteomics 1:1519-1528.
55. Shacter E, Williams JA, Lim M, Levine RL. 1994. Differential susceptibility of plasma proteins to oxidative modification: examination by western blot immunoassay. Free Radic Biol Med 17:429-437.
56. Sherrington R, Rogaev EI, Liang Y, Rogaeva EA, Levesque G, Ikeda M, Chi H, Lin C, Li G, Holman K, Tsuda T, Mar L, Foncin J-F, Bruni AC, Montesi MP, Sorbi S, Rainero I, Pinessi L, Nee L, Chumakov I, Pollen D, Brookes A, Sanseau P, Polinsky RJ, Wasco W, Da Silva HAR, Haines JL, Pericak-Vance MA, Tanzi RE, Roses AD, Fraser E, Rommens JM, St. George-Hyslop PH. 1995. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375(6534):754-760.
57. Slooter AJ, Cruts M, Kalmijn S, Hofman A, Breteler MM, Van Broeckhoven C, van Duijn CM. 1998. Risk estimates of dementia by apolipoprotein E genotypes from a population-based incidence study: the Rotterdam Study. Arch Neurol 55:964-968.
58. Smith MA, Taneda S, Richey PL, Miyata S, Yan SD, Stern D, Sayre LM, Monnier VM, Perry G. 1994. Advanced Maillard reaction end products are associated with Alzheimer disease pathology. Proc Natl Acad Sci U S A 91:5710-5714.
59. Smith MA, Richey Harris PL, Sayre LM, Beckman JS, Perry G. 1997. Widespread peroxynitrite-mediated damage in Alzheimer's disease. J Neurosci 17:2653-2657.
60. Stadtman ER, Oliver CN, Starke-Reed PE, Rhee SG. 1993. Age-related oxidation reaction in proteins. Toxicol Ind Health 9:187-196.
61. Subramaniam R, Roediger F, Jordan B, Mattson MP, Keller JN, Waeg G, Butterfield DA. 1997. The lipid peroxidation product, 4-hydroxy-2-trans-nonenal, alters the conformation of cortical synaptosomal membrane proteins. J Neurochem 69:1161-1169.
62. 1-42-induced oxidative stress in primary neuronal cells. Free Radic Res 38:449-458.
63. Sultana R, Boyd-Kimball D, Poon HF, Cai J, Pierce WM, Klein JB, Markesbery WR, Zhou XZ, Lu KP, Butterfield DA. 2005a. Oxidative modification and down-regulation of Pin1 in Alzheimer's disease hippocampus: a redox proteomics analysis. Neurobiol Aging, doi: 10.1016/jneurobiolaging.2005.05.005.
64. Sultana R, Boyd-Kimball D, Poon HF, Cai J, Pierce WM, Klein JB, Merchant M, Markesbery WR, Butterfield DA. 2005b. 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 doi: 10.1016/jneuro biolaging.2005.09.021.
65. 1-42. J Chromatogr B Analyt Technol Biomed Life Sci 833:3-11.
66. Takahashi Y. 2003. The 14-3-3 proteins: gene, gene expression, and function. Neurochem Res 28:1265-1273.
67. Thongboonkerd V, Luengpailin J, Cao J, Pierce WM, Cai J, Klein JB, Doyle RJ. 2002. Fluoride exposure attenuates expression of Streptococcus pyogenes virulence factors, J Biol Chem 277:16599-16605.
68. Vanhanen M, Soininen H. 1998. Glucose intolerance, cognitive impairment and Alzheimer's disease. Curr Opin Neurol 11:673-677.
69. Varadarajan S, Yatin S, Aksenova M, Butterfield DA. 2000. Review: Alzheimer's amyloid beta-peptide-associated free radical oxidative stress and neurotoxicity. J Struct Biol 130:184-208.
70. Wang Q, Woltjer RL, Cimino PJ, Pan C, Montine KS, Zhang J, Montine TJ. 2005. Proteomic analysis of neurofibrillary tangles in Alzheimer disease identifies GAPDH as a detergent-insoluble paired helical filament tau binding protein. FASEB J 19:869-871.
71. Yatin SM, Aksenov M, Butterfield DA. 1999a. 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 24:427-435.
72. 1-42. Neurobiol Aging 20:325-330; discussion 339-342.
73. Yatin SM, Yatin M, Aulick T, Ain KB, Butterfield DA. 1999c. Alzheimer's amyloid beta-peptide associated free radicals increase rat embryonic neuronal polyamine uptake and ornithine decarboxylase activity: protective effect of vitamin E. Neurosci Lett 263:17-20.
74. 1-42-induced neuronal protein oxidation and reactive oxygen species production. J Alzheimers Dis 2:123-131.