Signal transduction cascades associated with oxidative stress in Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 11, Issue 2, 2007, Pages 143-152

  Petersen, Robert B ^a   Nunomura, Akihiko ^b   Lee, Hyoung Gon ^a   Casadesus, Gemma ^a   Perry, George ^a,c   Smith, Mark A ^a   Zhu, Xiongwei ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b ASAHIKAWA MEDICAL COLLEGE   (Japan)

^c University of San Antonio   (United States)

Author keywords

Alzheimer's disease; Heme oxygenase; Mitochondria; Oxidative stress; Stress activated protein kinase; Transition metals

Indexed keywords

OXYGEN RADICAL; STRESS ACTIVATED PROTEIN KINASE;

ALZHEIMER DISEASE; CYTOPATHOLOGY; CYTOPLASM; DISEASE COURSE; ENZYME ACTIVATION; HUMAN; NEUROPATHOLOGY; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 34347364659     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2007-11202     Document Type: Review

References (119)

1. M.Y. Aksenov, H.M. Tucker, P. Nair, M.V. Aksenova, D.A. Butterfield, S. Estus and W.R. Markesbery, The expression of key oxidative stress-handling genes in different brain regions in Alzheimer's disease, J Mol Neurosci 11 (1998), 151-164.
2. G. Aliev, D. Seyidova, A.K. Raina, M.E. Obrenovich, M.L. Neal, S.L. Siedlak, B.T. Lamb, H. Vinters, J.C. Lamanna, M.A. Smith and G. Perry, Vascular Hypoperfusion, Mitochondria Failure and Oxidative Stress in Alzheimer's Disease, Proc Indian Natl Sci Acad B69 (2003), 209-238.
3. A.J. Anderson, B.J. Cummings and C.W. Cotman, Increased immunoreactivity for Jun- and Fos-related proteins in Alzheimer's disease: association with pathology, Exp Neurol 125 (1994), 286-295.
4. C. Atzori, B. Ghetti, R. Piva, A.N. Srinivasan, P. Zolo, M.B. Delisle, S.S. Mirra and A. Migheli, Activation of the JNK/p38 pathway occurs in diseases characterized by tau protein pathology and is related to tau phosphorylation but not to apoptosis, J Neuropathol Exp Neurol 60 (2001), 1190-1197.
5. C. Behl, J. Davis, G.M. Cole and D. Schubert, Vitamin E protects nerve cells from amyloid beta protein toxicity, Biochem Biophys Res Commun 186 (1992), 944-950.
6. C. Behl, J.B. Davis, R. Lesley and D. Schubert, Hydrogen peroxide mediates amyloid beta protein toxicity, Cell 77 (1994), 817-827.
7. D. Bozyczko-Coyne, T.M. O'Kane, Z.L. Wu, P. Dobrzanski, S. Murthy, J.L. Vaught and R.W. Scott, CEP-1347/KT-7515, an inhibitor of SAPK/JNK pathway activation, promotes survival and blocks multiple events associated with Abeta-induced cortical neuron apoptosis, J Neurochem 77 (2001), 849-863.
8. D.A. Butterfield, J. Drake, C. Pocernich and A. Castegna, Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide, Trends Mol Med 7 (2001), 548-554.
9. A. Castegna, M. Aksenov, M. Aksenova, V. Thongboonkerd, J.B. Klein, W.M. Pierce, R. Booze, W.R. Markesbery and D.A. Butterfield, Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxyterminal hydrolase L-1, Free Radic Biol Med 33 (2002), 562-571.
10. A. Castegna, M. Aksenov, V. Thongboonkerd, J.B. Klein, W.M. Pierce, R. Booze, W.R. Markesbery and D.A. Butterfield, 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.
11. A. Castegna, V. Thongboonkerd, J.B. Klein, B. Lynn, W.R. Markesbery and D.A. Butterfield, Proteomic identification of nitrated proteins in Alzheimer's disease brain, J Neurochem 85 (2003), 1394-1401.
12. R.J. Castellani, P.L. Harris, L.M. Sayre, J. Fujii, N. Taniguchi, M.P. Vitek, H. Founds, C.S. Atwood, G. Perry and M.A. Smith, Active glycation in neurofibrillary pathology of Alzheimer's disease: N(epsilon)-(carboxymethyl) lysine and hexitol-lysine, Free Radic Biol Med 31 (2001), 175-180.
13. K. Chandrasekaran, T. Giordano, D.R. Brady, J. Stoll, L.J. Martin and S.I. Rapoport, Impairment in mitochondrial cytochrome oxidase gene expression in Alzheimer's disease, Brain Res Mol Brain Res 24 (1994), 336-340.
14. C.A. Colton and D.L. Gilbert, Production of superoxide anions by a CNS macrophage, the microglia, FEBS Lett 223 (1987), 284-288.
15. J.R. Connor, B.S. Snyder, P. Arosio, D.A. Loeffler and P. LeWitt, Aquantitative analysis of isoferritins in select regions of aged, parkinsonian, and Alzheimer's diseased brains, J Neurochem 65 (1995), 717-724.
16. D.A. Cottrell, E.L. Blakely, M.A. Johnson, P.G. Ince and D.M. Turnbull, Mitochondrial enzyme-deficient hippocampal neurons and choroidal cells in AD, Neurology 57 (2001), 260-264.
17. P. Cras, M.A. Smith, P.L. Richey, S.L. Siedlak, P. Mulvihill and G. Perry, Extracellular neurofibrillary tangles reflect neuronal loss and provide further evidence of extensive protein cross-linking in Alzheimer's disease, Acta Neuropathol 89 (1995), 291-295.
18. C.E. Cross, B. Halliwell, E.T. Borish, W.A. Pryor, B.N. Ames, R.L. Saul, J.M. McCord and D. Harman, Oxygen radicals and human disease, Ann Intern Med 107 (1987), 526-545.
19. T. Dunckley, T.G. Beach, K.E. Ramsey, A. Grover, D. Mastroeni, D.G. Walker, B.J. LaFleur, K.D. Coon, K.M. Brown, R. Caselli, W. Kukull, R. Higdon, D. McKeel, J.C. Morris, C. Hulette, D. Schmechel, E.M. Reiman, J. Rogers and D.A. Stephan, Gene expression correlates of neurofibrillary tangles in Alzheimer's disease, Neurobiol Aging 27 (2006), 1359-1371.
20. I. Ferrer, R. Blanco, M. Carmona and B. Puig, Phosphorylated mitogen-activated protein kinase (MAPK/ERK-P), protein kinase of 38 kDa (p38-P), stress-activated protein kinase (SAPK/JNK-P), and calcium/calmodulin-dependent kinase II (CaM kinase II) are differentially expressed in tau deposits in neurons and glial cells in tauopathies, J Neural Transm 108 (2001), 1397-1415.
21. G.E. Gibson, K.F. Sheu and J.P. Blass, Abnormalities of mitochondrial enzymes in Alzheimer's disease, J Neural Transm 105 (1998), 855-870.
22. P.F. Good, D.P. Perl, L.M. Bierer and J. Schmeidler, Selective accumulation of aluminum and iron in the neurofibrillary tangles of Alzheimer's disease: a laser microprobe (LAMMA) study, Ann Neurol 31 (1992), 286-292.
23. P.F. Good, P. Werner, A. Hsu, C.W. Olanow and D.P. Perl, Evidence of neuronal oxidative damage in Alzheimer's disease, Am J Pathol 149 (1996), 21-28.
24. A.W. Hartzler, X. Zhu, S.L. Siedlak, R.J. Castellani, J. Avila, G. Perry and M.A. Smith, The p38 pathway is activated in Pick disease and progressive supranuclear palsy: a mechanistic link between mitogenic pathways, oxidative stress, and tau, Neurobiology of Aging 23 (2002), 855-859.
25. K. Hensley, R.A. Floyd, N.Y. Zheng, R. Nael, K.A. Robinson, X. Nguyen, Q.N. Pye, C.A. Stewart, J. Geddes, W.R. Markesbery, E. Patel, G.V. Johnson and G. Bing, p38 kinase is activated in the Alzheimer's disease brain, J Neurochem 72 (1999), 2053-2058.
26. K.E. Heslop, M.A. Goss-Sampson, D.P. Muller and G. Curzon, Serotonin metabolism and release in frontal cortex of rats on a vitamin E-deficient diet, J Neurochem 66 (1996), 860-864.
27. K. Hirai, G. Aliev, A. Nunomura, H. Fujioka, R.L. Russell, C.S. Atwood, A.B. Johnson, Y. Kress, H.V. Vinters, M. Tabaton, S. Shimohama, A.D. Cash, S.L. Siedlak, P.L. Harris, P.K. Jones, R.B. Petersen, G. Perry and M.A. Smith, Mitochondrial abnormalities in Alzheimer's disease, J. Neurosci. 21 (2001), 3017-3023.
28. X. Huang, M.P. Cuajungco, C.S. Atwood, M.A. Hartshorn, J.D. Tyndall, G.R. Hanson, K.C. Stokes, M. Leopold, G. Multhaup, L.E. Goldstein, R.C. Scarpa, A.J. Saunders, J. Lim, R.D. Moir, C. Glabe, E.F. Bowden, C.L. Masters, D.P. Fairlie, R.E. Tanzi and A.I. Bush, Cu(II) potentiation of alzheimer abeta neurotoxicity. Correlation with cell-free hydrogen peroxide production and metal reduction, J Biol Chem 274 (1999), 37111-37116.
29. J.H. Jang and Y.J. Surh, β-Amyloid induces oxidative DNA damage and cell death through activation of c-Jun N terminal kinase, Ann N Y Acad Sci 973 (2002), 228-236.
30. S.C. Kao, A.M. Krichevsky, K.S. Kosik and L.H. Tsai, BACE1 suppression by RNA interference in primary cortical neurons, J Biol Chem 279 (2004), 1942-1949.
31. J.N. Keller, R.J. Mark, A.J. Bruce, E. Blanc, J.D. Rothstein, K. Uchida, G. Waeg and M.P. Mattson, 4-Hydroxynonenal, an aldehydic product of membrane lipid peroxidation, impairs glutamate transport and mitochondrial function in synaptosomes, Neuroscience 80 (1997), 685-696.
32. H.G. Lee, G. Casadesus, X. Zhu, A. Takeda, G. Perry and M.A. Smith, Challenging the amyloid cascade hypothesis: senile plaques and amyloid-beta as protective adaptations to Alzheimer's disease, Ann N Y Acad Sci 1019 (2004), 1-4.
33. H.G. Lee, G. Perry, P.I. Moreira, M.R. Garrett, Q. Liu, X. Zhu, A. Takeda, A. Nunomura and M.A. Smith, Tau phosphorylation in Alzheimer's disease: pathogen or protector?, Trends Mol Med 11 (2005), 164-169.
34. S.C. Lee, M.L. Zhao, A. Hirano and D.W. Dickson, Inducible nitric oxide synthase immunoreactivity in the Alzheimer's disease hippocampus: association with Hirano bodies, neurofibrillary tangles, and senile plaques, J Neuropathol Exp Neurol 58 (1999), 1163-1169.
35. B.P. Lockhart, C. Benicourt, J.L. Junien and A. Privat, Inhibitors of free radical formation fail to attenuate direct beta- amyloid25-35 peptide-mediated neurotoxicity in rat hippocampal cultures, J Neurosci Res 39 (1994), 494-505.
36. D.A. Loeffler, J.R. Connor, P.L. Juneau, B.S. Snyder, L. Kanaley, A.J. DeMaggio, H. Nguyen, C.M. Brickman and P.A. LeWitt, Transferrin and iron in normal, Alzheimer's disease, and Parkinson's disease brain regions, J Neurochem 65 (1995), 710-724.
37. M.A. Lovell, J.L. Smith and W.R. Markesbery, Elevated zinc transporter-6 in mild cognitive impairment, Alzheimer's disease, and pick disease, J Neuropathol Exp Neurol 65 (2006), 489-498.
38. M. Manczak, B.S. Park, Y. Jung and P.H. Reddy, Differential expression of oxidative phosphorylation genes in patients with Alzheimer's disease: implications for early mitochondrial dysfunction and oxidative damage, Neuromolecular Med 5 (2004), 147-162.
39. R.J. Mark, M.A. Lovell, W.R. Markesbery, K. Uchida and M.P. Mattson, A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid beta-peptide, J Neurochem 68 (1997), 255-264.
40. R.J. Mark, Z. Pang, J.W. Geddes, K. Uchida and M.P. Mattson, Amyloid beta-peptide impairs glucose transport in hippocampal and cortical neurons: involvement of membrane lipid peroxidation, J Neurosci 17 (1997), 1046-1054.
41. W.R. Markesbery and M.A. Lovell, Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease, Neurobiol Aging 19 (1998), 33-36.
42. M. Marlatt, H.G. Lee, G. Perry, M.A. Smith and X. Zhu, Sources and mechanisms of cytoplasmic oxidative damage in Alzheimer's disease, Acta Neurobiol Exp (Wars) 64 (2004), 81-87.
43. R.N. Martins, C.G. Harper, G.B. Stokes and C.L. Masters, Increased cerebral glucose-6-phosphate dehydrogenase activity in Alzheimer's disease may reflect oxidative stress, J Neurochem 46 (1986), 1042-1045.
44. I. Maurer, S. Zierz and H.J. Moller, A selective defect of cytochrome c oxidase is present in brain of Alzheimer's disease patients, Neurobiol Aging 21 (2000), 455-462.
45. P. Mecocci, U. MacGarvey and M.F. Beal, Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease, Ann Neurol 36 (1994), 747-751.
46. P. Mecocci, M.F. Beal, R. Cecchetti, M.C. Polidori, A. Cherubini, F. Chionne, L. Avellini, G. Romano and U. Senin, Mitochondrial membrane fluidity and oxidative damage to mitochondrial DNA in aged and AD human brain, Mol Chem Neuropathol 31 (1997), 53-64.
47. K. Mielke and T. Herdegen, JNK and p38 stresskinases - degenerative effectors of signal- transduction-cascades in the nervous system, Prog Neurobiol 61 (2000), 45-60.
48. P.I. Moreira, X. Zhu, H.G. Lee, K. Honda, M.A. Smith and G. Perry, The (un)balance between metabolic and oxidative abnormalities and cellular compensatory responses in Alzheimer's disease, Mech Ageing Dev 127 (2006), 501-506.
49. Y. Morishima, Y. Gotoh, J. Zieg, T. Barrett, H. Takano, R. Flavell, R.J. Davis, Y. Shirasaki and M.E. Greenberg, Beta-amyloid induces neuronal apoptosis via a mechanism that involves the c-Jun N-terminal kinase pathway and the induction of Fas ligand, J Neurosci 21 (2001), 7551-7560.
50. R. Morsch, W. Simon and P.D. Coleman, Neurons may live for decades with neurofibrillary tangles, J Neuropathol Exp Neurol 58 (1999), 188-197.
51. Z. Nagy, M.M. Esiri, M. LeGris and P.M. Matthews, Mitochondrial enzyme expression in the hippocampus in relation to Alzheimer-type pathology, Acta Neuropathol (Berl) 97 (1999), 346-354.
52. A. Nunomura, G. Perry, M.A. Pappolla, R. Wade, K. Hirai, S. Chiba and M.A. Smith, RNA oxidation is a prominent feature of vulnerable neurons in Alzheimer's disease, J Neurosci 19 (1999), 1959-1964.
53. A. Nunomura, G. Perry, M.A. Pappolla, R.P. Friedland, K. Hirai, S. Chiba and M.A. Smith, Neuronal oxidative stress precedes amyloid-beta deposition in Down syndrome, J Neuropathol Exp Neurol 59 (2000), 1011-1017.
54. A. Nunomura, G. Perry, G. Aliev, K. Hirai, A. Takeda, E.K. Balraj, P.K. Jones, H. Ghanbari, T. Wataya, S. Shimohama, S. Chiba, C.S. Atwood, R.B. Petersen and M.A. Smith, Oxidative damage is the earliest event in Alzheimer's disease, J Neuropathol Exp Neurol 60 (2001), 759-767.
55. P. Odetti, G. Angelini, D. Dapino, D. Zaccheo, S. Garibaldi, F. Dagna-Bricarelli, G. Piombo, G. Perry, M. Smith, N. Traverso and M. Tabaton, Early glycoxidation damage in brains from Down's syndrome, Biochem. Biophys. Res. Commun. 243 (1998), 849-851.
56. D. Paola, C. Domenicotti, M. Nitti, A. Vitali, R. Borghi, D. Cottalasso, D. Zaccheo, P. Odetti, P. Strocchi, U.M. Marinari, M. Tabaton and M.A. Pronzato, Oxidative stress induces increase in intracellular amyloid beta-protein production and selective activation of betaI and betaII PKCs in NT2 cells, Biochem Biophys Res Commun 268 (2000), 642-646.
57. M.A. Pappolla, R.A. Omar, K.S. Kim and N.K. Robakis, Immunohistochemical evidence of oxidative [corrected] stress in Alzheimer's disease, Am J Pathol 140 (1992), 621-628.
58. W.D. Parker, Jr., N.J. Mahr, C.M. Filley, J.K. Parks, D. Hughes, D.A. Young and C.M. Cullum, Reduced platelet cytochrome c oxidase activity in Alzheimer's disease, Neurology 44 (1994), 1086-1090.
59. W.D. Parker, Jr., J. Parks, C.M. Filley and B.K. Kleinschmidt-DeMasters, Electron transport chain defects in Alzheimer's disease brain, Neurology 44 (1994), 1090-1096.
60. A.G. Pearson, U.T. Byrne, G.A. MacGibbon, R.L. Faull and M. Dragunow, Activated c-Jun is present in neurofibrillary tangles in Alzheimer's disease brains, Neurosci Lett 398 (2006), 246-250.
61. J.J. Pei, E. Braak, H. Braak, I. Grundke-Iqbal, K. Iqbal, B. Winblad and R.F. Cowburn, Localization of active forms of C-jun kinase (JNK) and p38 kinase in Alzheimer's disease brains at different stages of neurofibrillary degeneration, J Alzheimers's Dis 3 (2001), 41-48.
62. J.J. Pei, H. Braak, W.L. An, B. Winblad, R.F. Cowburn, K. Iqbal and I. Grundke-Iqbal, Up-regulation of mitogen-activated protein kinases ERK1/2 and MEK1/2 is associated with the progression of neurofibrillary degeneration in Alzheimer's disease, Brain Res Mol Brain Res 109 (2002), 45-55.
63. M. Perez, R. Cuadros, M.A. Smith, G. Perry and J. Avila, Phosphorylated, but not native, tau protein assembles following reaction with the lipid peroxidation product, 4-hydroxy-2-nonenal, FEBS Lett 486 (2000), 270-274.
64. G. Perry, A. Nunomura, P. Lucassen, H. Lassmann and M.A. Smith, Apoptosis and Alzheimer's disease, Science 282 (1998), 1268-1269.
65. G. Perry and M.A. Smith, Is oxidative damage central to the pathogenesis of Alzheimer's disease? Acta Neurol Belg 98 (1998), 175-179.
66. G. Perry, X. Zhu and M.A. Smith, Do neurons have a choice in death?, Am J Pathol 158 (2001), 1-2.
67. G. Perry, A. Nunomura, K. Hirai, X. Zhu, M. Perez, J. Avila, R.J. Castellani, C.S. Atwood, G. Aliev, L.M. Sayre, A. Takeda and M.A. Smith, Is oxidative damage the fundamental pathogenic mechanism of Alzheimer's and other neurodegenerative diseases?, Free Radic Biol Med 33 (2002), 1475-1479.
68. G. Perry, M.A. Taddeo, A. Nunomura, X. Zhu, T. Zenteno-Savin, K.L. Drew, S. Shimohama, J. Avila, R.J. Castellani and M.A. Smith, Comparative biology and pathology of oxidative stress in Alzheimer and other neurodegenerative diseases: beyond damage and response, Comp Biochem Physiol C Toxicol Pharmacol 133 (2002), 507-513.
69. G. Perry, A. Nunomura, A.K. Raina, G. Aliev, S.L. Siedlak, P.L. Harris, G. Casadesus, R.B. Petersen, W. Bligh-Glover, E. Balraj, G.J. Petot and M.A. Smith, A metabolic basis for Alzheimer's disease, Neurochem Res 28 (2003), 1549-1552.
70. G. Perry, M.A. Taddeo, R.B. Petersen, R.J. Castellani, P.L. Harris, S.L. Siedlak, A.D. Cash, Q. Liu, A. Nunomura, C.S. Atwood and M.A. Smith, Adventiously-bound redox active iron and copper are at the center of oxidative damage in Alzheimer's disease, Biometals 16 (2003), 77-81.
71. D.J. Pinero, J. Hu and J.R. Connor, Alterations in the interaction between iron regulatory proteins and their iron responsive element in normal and Alzheimer's diseased brains, Cell Mol Biol (Noisy-le-grand) 46 (2000), 761-776.
72. D. Praprotnik, M.A. Smith, P.L. Richey, H.V. Vinters and G. Perry, Plasma membrane fragility in dystrophic neurites in senile plaques of Alzheimer's disease: an index of oxidative stress, Acta Neuropathol 91 (1996), 1-5.
73. D. Pratico, K. Uryu, S. Leight, J.Q. Trojanoswki and V.M. Lee, Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis, J Neurosci 21 (2001), 4183-4187.
74. D.R. Premkumar, M.A. Smith, P.L. Richey, R.B. Petersen, R. Castellani, R.K. Kutty, B. Wiggert, G. Perry and R.N. Kalaria, Induction of heme oxygenase-1 mRNA and protein in neocortex and cerebral vessels in Alzheimer's disease, J Neurochem 65 (1995), 1399-1402.
75. A.K. Raina, A. Hochman, X. Zhu, C.A. Rottkamp, A. Nunomura, S.L. Siedlak, H. Boux, R.J. Castellani, G. Perry and M.A. Smith, Abortive apoptosis in Alzheimer's disease, Acta Neuropathol (Berl) 101 (2001), 305-310.
76. P.H. Reddy, S. McWeeney, B.S. Park, M. Manczak, R.V. Gutala, D. Partovi, Y. Jung, V. Yau, R. Searles, M. Mori and J. Quinn, Gene expression profiles of transcripts in amyloid precursor protein transgenic mice: up-regulation of mitochondrial metabolism and apoptotic genes is an early cellular change in Alzheimer's disease, Hum. Mol. Genet. 13 (2004), 1225-1240.
77. K. Renkawek, G.J. Bosman and W.W. de Jong, Expression of small heat-shock protein hsp 27 in reactive gliosis in Alzheimer's disease and other types of dementia, Acta Neuropathol (Berl) 87 (1994), 511-519.
78. C.A. Rottkamp, A.K. Raina, X. Zhu, E. Gaier, A.I. Bush, C.S. Atwood, M. Chevion, G. Perry and M.A. Smith, Redoxactive iron mediates amyloid-beta toxicity, Free Radic Biol Med 30 (2001), 447-450.
79. R.L. Russell, S.L. Siedlak, A.K. Raina, J.M. Bautista, M.A. Smith and G. Perry, Increased neuronal glucose-6-phosphate dehydrogenase and sulfhydryl levels indicate reductive compensation to oxidative stress in Alzheimer's disease, Arch Biochem Biophys 370 (1999), 236-239.
80. M.J. Savage, Y.G. Lin, J.R. Ciallella, D.G. Flood and R.W. Scott, Activation of c-Jun N-terminal kinase and p38 in an Alzheimer's disease model is associated with amyloid deposition, J Neurosci 22 (2002), 3376-3385.
81. L.M. Sayre, D.A. Zelasko, P.L. Harris, G. Perry, R.G. Salomon and M.A. Smith, 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease, J Neurochem 68 (1997), 2092-2097.
82. M. Shoji, N. Iwakami, S. Takeuchi, M. Waragai, M. Suzuki, I. Kanazawa, C.F. Lippa, S. Ono and H. Okazawa, JNK activation is associated with intracellular beta-amyloid accumulation, Brain Res Mol Brain Res 85 (2000), 221-233.
83. M.A. Smith, R.K. Kutty, P.L. Richey, S.D. Yan, D. Stern, G.J. Chader, B. Wiggert, R.B. Petersen and G. Perry, Heme oxygenase-1 is associated with the neurofibrillary pathology of Alzheimer's disease, Am J Pathol 145 (1994), 42-47.
84. M.A. Smith, R.K. Kutty, P.L. Richey, S.D. Yan, D. Stern, G.J. Chader, B. Wiggert, R.B. Petersen and G. Perry, Heme oxygenase-1 is associated with the neurofibrillary pathology of Alzheimer's disease, Am J Pathol 145 (1994), 42-47.
85. M.A. Smith, S. Taneda, P.L. Richey, S. Miyata, S.D. Yan, D. Stern, L.M. Sayre, V.M. Monnier and G. Perry, Advanced Maillard reaction end products are associated with Alzheimer's disease pathology, Proc Natl Acad Sci USA 91 (1994), 5710-5714.
86. M.A. Smith, L.M. Sayre, V.M. Monnier and G. Perry, Radical AGEing in Alzheimer's disease, Trends Neurosci 18 (1995), 172-176.
87. M.A. Smith, G. Perry, P.L. Richey, L.M. Sayre, V.E. Anderson, M.F. Beal and N. Kowall, Oxidative damage in Alzheimer's, Nature 382 (1996), 120-121.
88. M.A. Smith, S.L. Siedlak, P.L. Richey, R.H. Nagaraj, A. Elhammer and G. Perry, Quantitative solubilization and analysis of insoluble paired helical filaments from Alzheimer's disease, Brain Res 717 (1996), 99-108.
89. M.A. Smith, P.L. Harris, L.M. Sayre and G. Perry, Iron accumulation in Alzheimer's disease is a source of redox-generated free radicals, Proc Natl Acad Sci USA 94 (1997), 9866-9868.
90. M.A. Smith, P.L. Richey Harris, L.M. Sayre, J.S. Beckman and G. Perry, Widespread peroxynitrite-mediated damage in Alzheimer's disease, J Neurosci 17 (1997), 2653-2657.
91. M.A. Smith, L.M. Sayre, V.E. Anderson, P.L. Harris, M.F. Beal, N. Kowall and G. Perry, Cytochemical demonstration of oxidative damage in Alzheimer's disease by immunochemical enhancement of the carbonyl reaction with 2,4-dinitrophenylhydrazine, J Histochem Cytochem 46 (1998), 731-735.
92. M.A. Smith, K. Wehr, P.L. Harris, S.L. Siedlak, J.R. Connor and G. Perry, Abnormal localization of iron regulatory protein in Alzheimer's disease, Brain Res 788 (1998), 232-236.
93. M.A. Smith, X. Zhu, Z. Sun and G. Perry, Activation of c-Jun in Alzheimer's disease, J. Neuropathol Exp Neurol 60 (2001), 546.
94. M.A. Smith, G. Casadesus, J.A. Joseph and G. Perry, Amyloid-beta and tau serve antioxidant functions in the aging and Alzheimer brain, Free Radic Biol Med 33 (2002), 1194-1199.
95. Y.J. Suzuki, H.J. Forman and A. Sevanian, Oxidants as stimulators of signal transduction, Free Radic Biol Med 22 (1997), 269-285.
96. A. Takeda, G. Perry, N.G. Abraham, B.E. Dwyer, R.K. Kutty, J.T. Laitinen, R.B. Petersen and M.A. Smith, Overexpression of heme oxygenase in neuronal cells, the possible interaction with Tau, J Biol Chem 275 (2000), 5395-5399.
97. A. Takeda, M.A. Smith, J. Avila, A. Nunomura, S.L. Siedlak, X. Zhu, G. Perry and L.M. Sayre, In Alzheimer's disease, heme oxygenase is coincident with Alz50, an epitope of tau induced by 4-hydroxy-2-nonenal modification, J Neurochem 75 (2000), 1234-1241.
98. A. Takeda, M.A. Smith, J. Avila, A. Nunomura, S.L. Siedlak, X. Zhu, G. Perry and L.M. Sayre, In Alzheimer's disease, heme oxygenase is coincident with Alz50, an epitope of tau induced by 4-hydroxy-2-nonenal modification, J Neurochem 75 (2000), 1234-1241.
99. E. Tamagno, P. Bardini, A. Obbili, A. Vitali, R. Borghi, D. Zaccheo, M.A. Pronzato, O. Danni, M.A. Smith, G. Perry and M. Tabaton, Oxidative stress increases expression and activity of BACE in NT2 neurons, Neurobiol Dis 10 (2002), 279-288.
100. E. Tamagno, M. Parola, P. Bardini, A. Piccini, R. Borghi, M. Guglielmotto, G. Santoro, A. Davit, O. Danni, M.A. Smith, G. Perry and M. Tabaton, Beta-site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinases pathways, J Neurochem 92 (2005), 628-636.
101. C.M. Troy, S.A. Rabacchi, Z. Xu, A.C. Maroney, T.J. Connors, M.L. Shelanski and L.A. Greene, beta-Amyloid-induced neuronal apoptosis requires c-Jun N-terminal kinase activation, J Neurochem 77 (2001), 157-164.
102. C. Velez-Pardo, G.G. Ospina and M. Jimenez del Rio, Abeta[25-35] peptide and iron promote apoptosis in lymphocytes by an oxidative stress mechanism: involvement of H2O2, caspase-3, NF-kappaB, p53 and c-Jun, Neurotoxicology 23 (2002), 351-365.
103. M.P. Vitek, K. Bhattacharya, J.M. Glendening, E. Stopa, H. Vlassara, R. Bucala, K. Manogue and A. Cerami, Advanced glycation end products contribute to amyloidosis in Alzheimer's disease, Proc Natl Acad Sci USA 91 (1994), 4766-4770.
104. T. Wataya, A. Nunomura, M.A. Smith, S.L. Siedlak, P.L. Harris, S. Shimohama, L.I. Szweda, M.A. Kaminski, J. Avila, D.L. Price, D.W. Cleveland, L.M. Sayre and G. Perry, High molecular weight neurofilament proteins are physiological substrates of adduction by the lipid peroxidation product hydroxynonenal, J Biol Chem 277 (2002), 4644-4648.
105. W. Wei, X. Wang and J.W. Kusiak, Signaling events in amyloid beta-peptide-induced neuronal death and insulin-like growth factor I protection, J Biol Chem 277 (2002), 17649-17656.
106. S.D. Yan, S.F. Yan, X. Chen, J. Fu, M. Chen, P. Kuppusamy, M.A. Smith, G. Perry, G.C. Godman, P. Nawroth and et al., Non-enzymatically glycated tau in Alzheimer's disease induces neuronal oxidant stress resulting in cytokine gene expression and release of amyloid beta-peptide, Nat Med 1 (1995), 693-699.
107. S.D. Yan, X. Chen, J. Fu, M. Chen, H. Zhu, A. Roher, T. Slattery, L. Zhao, M. Nagashima, J. Morser, A. Migheli, P. Nawroth, D. Stern and A.M. Schmidt, RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease, Nature 382 (1996), 685-691.
108. X. Zhu, C.A. Rottkamp, H. Boux, A. Takeda, G. Perry and M.A. Smith, Activation of p38 kinase links tau phosphorylation, oxidative stress, and cell cycle-related events in Alzheimer's disease, J Neuropathol Exp Neurol 59 (2000), 880-888.
109. X. Zhu, R.J. Castellani, A. Takeda, A. Nunomura, C.S. Atwood, G. Perry and M.A. Smith, Differential activation of neuronal ERK, JNK/SAPK and p38 in Alzheimer's disease: the 'two hit' hypothesis, Mech Ageing Dev 123 (2001), 39-46.
110. X. Zhu, R.J. Castellani, A. Takeda, A. Nunomura, C.S. Atwood, G. Perry and M.A. Smith, Differential activation of neuronal ERK, JNK/SAPK and p38 in Alzheimer's disease: the 'two hit' hypothesis, Mech Ageing Dev 123 (2001), 39-46.
111. X. Zhu, A.K. Raina, C.A. Rottkamp, G. Aliev, G. Perry, H. Boux and M.A. Smith, Activation and redistribution of c-jun N-terminal kinase/stress activated protein kinase in degenerating neurons in Alzheimer's disease, J Neurochem 76 (2001), 435-441.
112. X. Zhu, A.K. Raina, C.A. Rottkamp, G. Aliev, G. Perry, H. Boux and M.A. Smith, Activation and redistribution of c-Jun N-terminal kinase/stress activated protein kinase in degenerating neurons in Alzheimer's disease, J Neurochem 76 (2001), 435-441.
113. X. Zhu, C.A. Rottkamp, K. Zevez, C.S. Atwood, G. Perry and M.A. Smith, Metal-Mediated amyloid-beta toxicity acts through the activation of JNK/SAPK pathway in Alzheimer's disease, Free Radic Biol Med 31 (2001), S65.
114. X. Zhu, H.-G. Lee, G. Perry, A.K. Raina and M.A. Smith, The MAPK Pathways in Alzheimer's Disease, NeuroSignals 11 (2002), 270-281.
115. X. Zhu, A.K. Raina, H.G. Lee, M. Chao, A. Nunomura, M. Tabaton, R.B. Petersen, G. Perry and M.A. Smith, Oxidative stress and neuronal adaptation in Alzheimer's disease: the role of SAPK pathways, Antioxid Redox Signal 5 (2003), 571-576.
116. X. Zhu, A.K. Raina, G. Perry and M.A. Smith, Alzheimer's disease: the two-hit hypothesis, Lancet Neurol 3 (2004), 219-226.
117. X. Zhu, Y. Wang, O. Ogawa, H.G. Lee, A.K. Raina, S.L. Siedlak, P.L. Harris, H. Fujioka, S. Shimohama, M. Tabaton, C.S. Atwood, R.B. Petersen, G. Perry and M.A. Smith, Neuroprotective properties of Bcl-w in Alzheimer's disease, J Neurochem 89 (2004), 1233-1240.
118. X. Zhu, G. Perry, P.I. Moreira, G. Aliev, A.D. Cash, K. Hirai and V.A. Smith, Mitochondrial abnormalities and oxidative imbalance in Alzheimer's disease, J Alzheimers Dis 9 (2006), 147-153.
119. X. Zhu, A.K. Raina, G. Perry and M.A. Smith, Apoptosis in Alzheimer's disease: a mathematical improbability, Curr Alzheimer Res 3 (2006), 393-396.