Intraneuronal amyloid β accumulation and oxidative damage to nucleic acids in Alzheimer disease

Neurobiology of Disease

Volumn 37, Issue 3, 2010, Pages 731-737

  Nunomura, Akihiko ^a   Tamaoki, Toshio ^a   Tanaka, Koich ^a   Motohashi, Nobutaka ^a   Nakamura, Masao ^b   Hayashi, Takaaki ^c   Yamaguchi, Haruyasu ^d   Shimohama, Shun ^e   Lee, Hyoung gon ^f   Zhu, Xiongwei ^f   Smith, Mark A ^f   Perry, George ^g  

^a UNIVERSITY OF YAMANASHI   (Japan)

^b ASAHIKAWA MEDICAL COLLEGE   (Japan)

^c HOKKAIDO INSTITUTE OF PUBLIC HEALTH   (Japan)

^d GUNMA UNIVERSITY   (Japan)

^e SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f CASE WESTERN RESERVE UNIVERSITY   (United States)

^g University of San Antonio   (United States)

Author keywords

8 Hydroxyguanosine; Alzheimer disease; Intraneuronal amyloid ; Nucleic acids; Oligomer; Oxidative stress

Indexed keywords

8 HYDROXYGUANINE; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; NUCLEIC ACID;

AGED; ALZHEIMER DISEASE; ANTIBODY SPECIFICITY; ARTICLE; BRAIN TISSUE; CADAVER; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CORRELATION ANALYSIS; CYTOPLASM; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NERVE CELL; OXIDATIVE STRESS; PRIORITY JOURNAL;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; BRAIN; CELL NUCLEUS; CYTOPLASM; CYTOPROTECTION; FEMALE; GUANOSINE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NERVE DEGENERATION; NEURONS; NUCLEIC ACIDS; OXIDATIVE STRESS; PEPTIDE FRAGMENTS;

EID: 75949101857     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2009.12.012     Document Type: Article

References (82)

1. P264L/P264L double knock-in mouse model of Alzheimer's disease. Am. J. Pathol 168 (2006) 1608-1618
2. Andorn A.C., and Kalaria R.N. Factors affecting pro- and anti-oxidant properties of fragments of the β-protein precursor (βPP): implication for Alzheimer's disease. J. Alzheimers Dis. 2 (2000) 69-78
3. Atwood C.S., Obrenovich M.E., Liu T., Chan H., Perry G., Smith M.A., and Martins R.N. Amyloid-β: a chameleon walking in two worlds: a review of the trophic and toxic properties of amyloid-β. Brain Res. Brain Res. Rev. 43 (2003) 1-16
4. Baruch-Suchodolsky R., and Fischer B. Soluble amyloid β1-28-copper(I)/copper(II)/Iron(II) complexes are potent antioxidants in cell-free systems. Biochemistry 47 (2008) 7796-7806
5. Bayer T.A., Schafer S., Simons A., Kemmling A., Kamer T., Tepest R., Eckert A., Schüssel K., Eikenberg O., Sturchler-Pierrat C., Abramowski D., Staufenbiel M., and Multhaup G. Dietary Cu stabilizes brain superoxide dismutase 1 activity and reduces amyloid Aβ production in APP23 transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 14187-14192
6. Behl C., Davis J.B., Lesley R., and Schubert D. Hydrogen peroxide mediates amyloid β protein toxicity. Cell 77 (1994) 817-827
7. Bishop G.M., and Robinson S.R. Human Aβ1-42 reduces iron-induced toxicity in rat cerebral cortex. J. Neurosci. Res. 73 (2003) 316-323
8. Butterfield D.A., Poon H.F., St Clair D., Keller J.N., Pierce W.M., Klein J.B., and Markesbery W.R. Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: insights into the development of Alzheimer's disease. Neurobiol. Dis. 22 (2006) 223-232
9. Butterfield D.A., Reed T.T., Perluigi M., De Marco C., Coccia R., Keller J.N., Markesbery W.R., and Sultana R. Elevated levels of 3-nitrotyrosine in brain from subjects with amnestic mild cognitive impairment: implications for the role of nitration in the progression of Alzheimer's disease. Brain Res. 1148 (2007) 243-248
10. Chang Y., Kong Q., Shan X., Tian G., Ilieva H., Cleveland D.W., Rothstein J.D., Borchelt D.R., Wong P.C., and Lin C.L. Messenger RNA oxidation occurs early in disease pathogenesis and promotes motor neuron degeneration in ALS. PLoS ONE 3 8 (2008) e2849
11. Cuajungco M.P., Goldstein L.E., Nunomura A., Smith M.A., Lim J.T., Atwood C.S., Huang X., Farrag Y.W., Perry G., and Bush A.I. Evidence that the β-amyloid plaques of Alzheimer's disease represent the redox-silencing and entombment of Aβ by zinc. J. Biol. Chem. 275 (2000) 19439-19442
12. D'Andrea M.R., Nagele R.G., Wang H.Y., Peterson P.A., and Lee D.H. Evidence that neurones accumulating amyloid can undergo lysis to form amyloid plaques in Alzheimer's disease. Histopathology 38 (2001) 120-134
13. De Felice F.G., Velasco P.T., Lambert M.P., Viola K., Fernandez S.J., Ferreira S.T., and Klein W.L. Aβ oligomers induce neuronal oxidative stress through an N-methyl-d-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J. Biol. Chem. 282 (2007) 11590-11601
14. Ding Q., Markesbery W.R., Chen Q., Li F., and Keller J.N. Ribosome dysfunction is an early event in Alzheimer's disease. J. Neurosci. 25 (2005) 9171-9175
15. Dumont M., Wille E., Stack C., Calingasan N.Y., Beal M.F., and Lin M.T. Reduction of oxidative stress, amyloid deposition, and memory deficit by manganese superoxide dismutase overexpression in a transgenic mouse model of Alzheimer's disease. FASEB J. 23 (2009) 2459-2466
16. Frederikse P.H., Garland D., Zigler Jr. J.S., and Piatigorsky J. Oxidative stress increases production of β-amyloid precursor protein and β-amyloid (Aβ) in mammalian lenses, and Aβ has toxic effects on lens epithelial cells. J. Biol. Chem. 271 (1996) 10169-10174
17. Gouras G.K., Almeida C.G., and Takahashi R.H. Intraneuronal Aβ accumulation and origin of plaques in Alzheimer's disease. Neurobiol. Aging 26 (2005) 1235-1244
18. Gouras G.K., Tsai J., Naslund J., Vincent B., Edgar M., Checler F., Greenfield J.P., Haroutunian V., Buxbaum J.D., Xu H., Greengard P., and Relkin N.R. Intraneuronal Aβ42 accumulation in human brain. Am. J. Pathol. 156 (2000) 15-20
19. Grundke-Iqbal I., Iqbal K., George L., Tung Y.C., Kim K.S., and Wisniewski H.M. Amyloid protein and neurofibrillary tangles coexist in the same neuron in Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 2853-2857
20. Gyure K.A., Durham R., Stewart W.F., Smialek J.E., and Troncoso J.C. Intraneuronal β-amyloid precedes development of amyloid plaques in Down syndrome. Arch. Pathol. Lab. Med. 125 (2001) 489-492
21. Haass C., and Selkoe D.J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide. Nat. Rev. Mol. Cell Biol. 8 (2007) 101-112
22. Hayashi T., Shishido N., Nakayama K., Nunomura A., Smith M.A., Perry G., and Nakamura M. Lipid peroxidation and 4-hydroxy-2-nonenal formation by copper ion bound to amyloid-β peptide. Free Rad. Biol. Med. 43 (2007) 1552-1559
23. Hensley K., Carney J.M., Mattson M.P., Aksenova M., Harris M., Wu J.F., Floyd R.A., and Butterfield D.A. A model for β-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: relevance to Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 3270-3274
24. Kamal A., Almenar-Queralt A., LeBlanc J.F., Roberts E.A., and Goldstein L.S. Kinesin-mediated axonal transport of a membrane compartment containing β-secretase and presenilin-1 requires APP. Nature 414 (2001) 643-648
25. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., and Glabe C.G. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300 (2003) 486-489
26. Keller J.N., Schmitt F.A., Scheff S.W., Ding Q., Chen Q., Butterfield D.A., and Markesbery W.R. Evidence of increased oxidative damage in subjects with mild cognitive impairment. Neurology 64 (2005) 1152-1156
27. Khachaturian Z.S. Diagnosis of Alzheimer's disease. Arch. Neurol. 42 (1985) 1097-1105
28. Klein J.A., Longo-Guess C.M., Rossmann M.P., Seburn K.L., Hurd R.E., Frankel W.N., Bronson R.T., and Ackerman S.L. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 419 (2002) 367-374
29. Kokubo H., Kayed R., Glabe C.G., and Yamaguchi H. Soluble Aβ oligomers ultrastructurally localize to cell processes and might be related to synaptic dysfunction in Alzheimer's disease brain. Brain Res. 1031 (2005) 222-228
30. Kontush A. Amyloid-β: an antioxidant that becomes a pro-oxidant and critically contributes to Alzheimer's disease. Free Radic. Biol. Med. 31 (2001) 1120-1131
31. Kontush A., Berndt C., Weber W., Akopyan V., Arlt S., Schippling S., and Beisiegel U. Amyloid-β is an antioxidant for lipoproteins in cerebrospinal fluid and plasma. Free Radic. Biol. Med. 30 (2001) 119-128
32. Lacor P.N., Buniel M.C., Chang L., Fernandez S.J., Gong Y., Viola K.L., Lambert M.P., Velasco P.T., Bigio E.H., Finch C.E., Krafft G.A., and Klein W.L. Synaptic targeting by Alzheimer's-related amyloid β oligomers. J. Neurosci. 24 (2004) 10191-10200
33. LaFerla F.M., Green K.N., and Oddo S. Intracellular amyloid-β in Alzheimer's disease. Nat. Rev. Neurosci. 8 (2007) 499-509
34. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., and Klein W.L. Diffusible, nonfibrillar ligands derived from Aβ1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U. S. A. 26 (1998) 6448-6453
35. Li F., Calingasan N.Y., Yu F., Mauck W.M., Toidze M., Almeida C.G., Takahashi R.H., Carlson G.A., Beal F.M., Lin M.T., and Gouras G.K. Increased plaque burden in brains of APP mutant MnSOD heterozygous knockout mice. J. Neurochem. 89 (2004) 1308-1312
36. Lord A., Kalimo H., Eckman C., Zhang X.Q., Lannfelt L., and Nilsson L.N. The Arctic Alzheimer mutation facilitates early intraneuronal Aβ aggregation and senile plaque formation in transgenic mice. Neurobiol. Aging 27 (2006) 67-77
37. Lovell M.A., and Markesbery W.R. Oxidatively modified RNA in mild cognitive impairment. Neurobiol. Dis. 29 (2008) 169-175
38. Luo Y., Sunderland T., Roth G.S., and Wolozin B. Physiological levels of β-amyloid peptide promote PC12 cell proliferation. Neurosci. Lett. 217 (1996) 125-128
39. Mark R.J., Lovell M.A., Markesbery W.R., Uchida K., and Mattson M.P. A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J. Neurochem. 68 (1997) 255-264
40. Markesbery W.R., Kryscio R.J., Lovell M.A., and Morrow J.D. Lipid peroxidation is an early event in the brain in amnestic mild cognitive impairment. Ann. Neurol. 58 (2005) 730-735
41. Mirra S.S., Heyman A., McKeel D., Sumi S.M., Crain B.J., Brownlee L.M., Vogel F.S., Hughes J.P., van Belle G., and Berg L. The consortium to establish a registry for Alzheimer's disease (CERAD). II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41 (1991) 479-486
42. Misonou H., Morishima-Kawashima M., and Ihara Y. Oxidative stress induces intracellular accumulation of amyloid β-protein (Aβ) in human neuroblastoma cells. Biochemistry 39 (2000) 6951-6959
43. Mori C., Spooner E.T., Wisniewski K.E., Wisniewski T.M., Yamaguchi H., Saido T.C., Tolan D.R., Selkoe D.J., and Lemere CA. Intraneuronal Aβ42 accumulation in Down syndrome brain. Amyloid 9 (2002) 88-102
44. 2 catalytically but quench hydroxyl radicals. Biochemistry 47 (2008) 11653-11664
45. Nakamura M., Shishido N., Nunomura A., Smith M.A., Perry G., Hayashi Y., Nakayama K., and Hayashi T. Three histidine residues of amyloid β peptide control the redox activity of copper and iron. Biochemistry 46 (2007) 12737-12743
46. Nunomura A., Castellani R.J., Zhu X., Moreira P.I., Perry G., and Smith M.A. Involvement of oxidative stress in Alzheimer disease. J. Neuropathol. Exp. Neurol. 65 (2006) 631-641
47. Nunomura A., Chiba S., Lippa C.F., Cras P., Kalaria R.N., Takeda A., Honda K., Smith M.A., and Perry G. Neuronal RNA oxidation is a prominent feature of familial Alzheimer's disease. Neurobiol. Dis. 17 (2004) 108-113
48. Nunomura A., Hofer T., Moreira P.I., Castellani R.J., Smith M.A., and Perry G. RNA oxidation in Alzheimer disease and related neurodegenerative disorders. Acta Neuropathol. 118 (2009) 151-166
49. Nunomura A., Moreira P.I., Takeda A., Smith M.A., and Perry G. Oxidative RNA damage and neurodegeneration. Curr. Med. Chem. 14 (2007) 2968-2975
50. Nunomura A., Perry G., Aliev G., Hirai K., Takeda A., Balraj E.K., Jones P.K., Ghanbari H., Wataya T., Shimohama S., Chiba S., Atwood C.S., Petersen R.B., and Smith M.A. Oxidative damage is the earliest event in Alzheimer disease. J. Neuropathol. Exp. Neurol. 60 (2001) 759-767
51. Nunomura A., Perry G., Pappolla M.A., Friedland R.P., Hirai K., Chiba S., and Smith M.A. Neuronal oxidative stress precedes amyloid-β deposition in Down syndrome. J. Neuropathol. Exp. Neurol. 59 (2000) 1011-1017
52. Nunomura A., Perry G., Pappolla M.A., Wade R., Hirai K., Chiba S., and Smith M.A. RNA oxidation is a prominent feature of vulnerable neurons in Alzheimer's disease. J. Neurosci. 19 (1999) 1959-1964
53. Oakley H., Cole S.L., Logan S., Maus E., Shao P., Craft J., Guillozet-Bongaarts A., Ohno M., Disterhoft J., Van Eldik L., Berry R., and Vassar R. Intraneuronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J. Neurosci. 26 (2006) 10129-10140
54. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., and LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Aβ and synaptic dysfunction. Neuron 39 (2003) 409-421
55. Paola D., Domenicotti C., Nitti M., Vitali A., Borghi R., Cottalasso D., Zaccheo D., Odetti P., Strocchi P., Marinari U.M., Tabaton M., and Pronzato M.A. Oxidative stress induces increase in intracellular amyloid β-protein production and selective activation of βI and βII PKCs in NT2 cells. Biochem. Biophys. Res. Commun. 268 (2000) 642-646
56. Plant L.D., Boyle J.P., Smith I.F., Peers C., and Pearson H.A. The production of amyloid β peptide is a critical requirement for the viability of central neurons. J. Neurosci. 23 (2003) 5531-5535
57. Praticò D., Uryu K., Leight S., Trojanoswki J.Q., and Lee V.M. Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J. Neurosci. 21 (2001) 4183-4187
58. Puzzo D., Privitera L., Leznik E., Fà M., Staniszewski A., Palmeri A., and Arancio O. Picomolar amyloid-β positively modulates synaptic plasticity and memory in hippocampus. J. Neurosci. 28 (2008) 14537-14545
59. Resende R., Moreira P.I., Proença T., Deshpande A., Busciglio J., Pereira C., and Oliveira C.R. Brain oxidative stress in a triple-transgenic mouse model of Alzheimer disease. Free Radic. Biol. Med. 44 (2008) 2051-2057
60. Schubert D., Behl C., Lesley R., Brack A., Dargusch R., Sagara Y., and Kimura H. Amyloid peptides are toxic via a common oxidative mechanism. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 1989-1993
61. Shan X., Chang Y., and Lin C.L. Messenger RNA oxidation is an early event preceding cell death and causes reduced protein expression. FASEB J. 21 (2007) 2753-2764
62. Shan X., and Lin C.L. Quantification of oxidized RNAs in Alzheimer's disease. Neurobiol. Aging 27 (2006) 657-662
63. Shan X., Tashiro H., and Lin C.L. The identification and characterization of oxidized RNAs in Alzheimer's disease. J. Neurosci. 23 (2003) 4913-4921
64. Shen C., Chen Y., Liu H., Zhang K., Zhang T., Lin A., and Jing N. Hydrogen peroxide promotes Aβ production through JNK-dependent activation of γ-secretase. J. Biol. Chem. 283 (2008) 17721-17730
65. Smith M.A., Casadesus G., Joseph J.A., and Perry G. Amyloid-β and tau serve antioxidant functions in the aging and Alzheimer brain. Free Radic. Biol. Med. 33 (2002) 1194-1199
66. Sternberger L.A. Immunocytochemistry. 3rd ed (1986), Wiley, New York
67. Sung S., Yao Y., Uryu K., Yang H., Lee V.M., Trojanowski J.Q., and Praticò D. Early vitamin E supplementation in young but not aged mice reduces Aβ levels and amyloid deposition in a transgenic model of Alzheimer's disease. FASEB J. 18 (2004) 323-325
68. Tabner B.J., El-Agnaf O.M., Turnbull S., German M.J., Paleologou K.E., Hayashi Y., Cooper L.J., Fullwood N.J., and Allsop D. Hydrogen peroxide is generated during the very early stages of aggregation of the amyloid peptides implicated in Alzheimer disease and familial British dementia. J. Biol. Chem. 280 (2005) 35789-35792
69. Takahashi R., Almeida C.G., Kearney P.F., Yu F., Lin M.T., Milner T.A., and Gouras G.K. Oligomerization of Alzheimer's β-amyloid within processes and synapses of cultured neurons and brain. J. Neurosci. 24 (2004) 3592-3599
70. Tamagno E., Guglielmotto M., Aragno M., Borghi R., Autelli R., Giliberto L., Muraca G., Danni O., Zhu X., Smith M.A., Perry G., Jo D.G., Mattson M.P., and Tabaton M. Oxidative stress activates a positive feedback between the γ- and β-secretase cleavages of the β-amyloid precursor protein. J. Neurochem. 104 (2008) 683-695
71. Tamagno E., Parola M., Bardini P., Piccini A., Borghi R., Guglielmotto M., Santoro G., Davit A., Danni O., Smith M.A., Perry G., and Tabaton M. β-Site APP cleaving enzyme up-regulation induced by 4-hydroxynonenal is mediated by stress-activated protein kinases pathways. J. Neurochem. 92 (2005) 628-636
72. Tong Y., Zhou W., Fung V., Christensen M.A., Qing H., Sun X., and Song W. Oxidative stress potentiates BACE1 gene expression and Aβ generation. J. Neural. Transm. 112 (2005) 455-469
73. Walsh D.M., Hartley D.M., Kusumoto Y., Fezoui Y., Condron M.M., Lomakin A., Benedek G.B., Selkoe D.J., and Teplow D.B. Amyloid β-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J. Biol. Chem. 274 (1999) 45-52
74. Walter M.F., Mason P.E., and Mason R.P. Alzheimer's disease amyloid β peptide 25-35 inhibits lipid peroxidation as a result of its membrane interactions. Biochem. Biophys. Res. Commun. 233 (1997) 760-764
75. Wang J., Markesbery W.R., and Lovell M.A. Increased oxidative damage in nuclear and mitochondrial DNA in mild cognitive impairment. J. Neurochem. 96 (2006) 825-832
76. Wegiel J., Kuchna I., Nowicki K., Frackowiak J., Mazur-Kolecka B., Imaki H., Wegiel J., Mehta P.D., Silverman W.P., Reisberg B., Deleon M., Wisniewski T., Pirttilla T., Frey H., Lehtimäki T., Kivimäki T., Visser F.E., Kamphorst W., Potempska A., Bolton D., Currie J.R., and Miller D.L. Intraneuronal Aβ immunoreactivity is not a predictor of brain amyloidosis-β or neurofibrillary degeneration. Acta Neuropathol. 113 (2007) 389-402
77. Wirths O., Multhaup G., Czech C., Blanchard V., Moussaoui S., Tremp G., Pradier L., Beyreuther K., and Bayer T.A. Intraneuronal Aβ accumulation precedes plaque formation in β-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci. Lett. 306 (2001) 116-120
78. Yan S.D., Yan S.F., Chen X., Fu J., Chen M., Kuppusamy P., Smith M.A., Perry G., Godman G.C., Nawroth P., Zweier J.L., and Stern D. Non-enzymatically glycated tau in Alzheimer's disease induces neuronal oxidant stress resulting in cytokine gene expression and release of amyloid β-peptide. Nat. Med. 1 (1995) 693-699
79. Yankner B.A., Duffy L.K., and Kirschner D.A. Neurotrophic and neurotoxic effects of amyloid β protein: reversal by tachykinin neuropeptides. Science 250 (1990) 279-282
80. Yin B., Whyatt R.M., Perera F.P., Randall M.C., Cooper T.B., and Santella R.M. Determination of 8-hydroxydeoxyguanosine by an immunoaffinity chromatography-monoclonal antibody-based ELISA. Free Radic. Biol. Med. 18 (1995) 1023-1032
81. Zhang J., Perry G., Smith M.A., Robertson D., Olson S.J., Graham D.G., and Montine T.J. Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am. J. Pathol. 154 (1999) 1423-1429
82. Zou K., Gong J.S., Yanagisawa K., and Michikawa M. A novel function of monomeric amyloid β-protein serving as an antioxidant molecule against metal-induced oxidative damage. J. Neurosci. 22 (2002) 4833-4841