Mitochondria are a direct site of Aβ accumulation in Alzheimer's disease neurons: Implications for free radical generation and oxidative damage in disease progression

Human Molecular Genetics

Volumn 15, Issue 9, 2006, Pages 1437-1449

  Manczak, Maria ^a   Anekonda, Thimmappa S ^a   Henson, Edward ^b   Park, Byung S ^a   Quinn, Joseph ^b   Reddy, P Hemachandra ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; CYTOCHROME C OXIDASE; DIGITONIN; FREE RADICAL; HYDROGEN PEROXIDE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN SLICE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE COURSE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG TARGETING; ELECTRON MICROSCOPY; ENZYME ACTIVITY; GENE OVEREXPRESSION; HYPOTHESIS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; TISSUE DISTRIBUTION;

ANIMALIA; MUS MUSCULUS;

EID: 33646152108     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddl066     Document Type: Article

References (59)

1. Selkoe, D.J. (2001) Alzheimer's disease: Genes, proteins, and therapy. Physiol. Rev., 81, 741-766.
2. Mattson, M.P. (2004) Pathways towards and away from Alzheimer's disease. Nature, 430, 631-639.
3. Tanzi, R.E. and Bertram, L. (2005) 20 years of the Alzheimer's disease amyloid hypothesis: A genetic perspective. Cell, 120, 545-555.
4. Reddy, P.H. and McWeeney, S. (2005) Mapping cellular transcriptosomes in autopsied Alzheimer's disease subjects and relevant animal models. Neurobiol. Aging, Published online ahead of print September 9.
5. Walsh, D.M., Klyubin, I., Fadeeva, J.V., Cullen, W.K., Anwyl, R., Wolfe, M.S., Rowan, M.J. and Selkoe, D.J. (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature, 416, 535-539.
6. Hardy, J. and Selkoe, D.J. (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science, 297, 353-356.
7. Sisodia, S.S., Annaert, W., Kim, S.H. and De Strooper, B. (2001) Gamma-secretase: Never more enigmatic. Trends Neurosci., 24 (Suppl. 11), S2-S6.
8. Pappolla, M.A., Omar, R.A., Kim, K.S. and Robakis, N.K. (1992) Immunohistochemical evidence of oxidative [corrected] stress in Alzheimer's disease. Am. J. Pathol., 140, 621-628. Erratum in Am. J. Pathol., (1996) 149, 1770.
9. Bozner, P., Grishko, V., LeDoux, S.P., Wilson, G.L., Chyan, Y.C. and Pappolla, M.A. (1997) The amyloid beta protein induces oxidative damage of mitochondrial DNA. J. Neuropathol. Exp. Neurol., 56, 1356-1362.
10. Pappolla, M.A., Chyan, Y.J., Omar, R.A., Hsiao, K., Perry, G., Smith, M.A. and Bozner, P. (1998) Evidence of oxidative stress and in vivo neurotoxicity of beta-amyloid in a transgenic mouse model of Alzheimer's disease: A chronic oxidative paradigm for testing antioxidant therapies in vivo. Am. J. Pathol., 152, 871-877.
11. Hirai, K., Aliev, G., Nunomura, A., Fujioka, H., Russell, R.L., Atwood, C.S., Johnson, A.B., Kress, Y., Vinters, H.V., Tabaton, M. et al. (2001) Mitochondrial abnormalities in Alzheimer's disease. J. Neurosci., 21, 3017-3023.
12. Swerdlow, R.H. and Khan, S.M. (2004) A 'mitochondrial cascade hypothesis' for sporadic Alzheimer's disease. Med. Hypotheses, 63, 8-20.
13. Manczak, M., Park, B.S., Jung, Y. and Reddy, P.H. (2004) Differential expression of oxidative phosphorylation genes in patients with Alzheimer's disease: Implications for early mitochondrial dysfunction and oxidative damage. Neuromolecular Med., 5, 147-162.
14. Reddy, P.H., McWeeney, S., Park, B.S., Manczak, M., Gutala, R.V., Partovi, D., Jung, Y., Yau, V., Searles, R., Mori, M. and Quinn, J. (2004) 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, 1225-1240.
15. Reddy, P.H., Mani, G., Park, B.S., Jacques, J., Murdoch, G., Whetsell, W., Jr., Kaye, J. and Manczak, M. (2005) Differential loss of synaptic proteins in Alzheimer's disease: Implications for synaptic dysfunction. J. Alzheimers Dis., 7, 103-117.
16. Kitazawa, M., Oddo, S., Yamasaki, T.R., Green, K.N. and LaFerla, F.M. (2005) Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer's disease. J. Neurosci., 25, 8843-8853.
17. Tanzi, R.E. (2005) The synaptic Abeta hypothesis of Alzheimer disease. Nat. Neurosci., 8, 977-979.
18. Oddo, S., Caccamo, A., Tran, L., Lambert, M.P., Glabe, C.G., Klein, W.L. and Laferla, F.M. (2006) Temporal profile of amyloid-beta (Abeta) oligomerization in an in vivo model of Alzheimer disease: A link between Abeta and Tau pathology. J. Biol. Chem., 281, 1599-1604.
19. Butterfield, D.A., Drake, J., Pocernich, C. and Castegna, A. (2001) Evidence of oxidative damage in Alzheimer's disease brain: Central role for amyloid beta-peptide. Trends Mol. Med., 7, 548-554.
20. Reddy, P.H. and Beal, M.F. (2005) Are mitochondria critical in the pathogenesis of Alzheimer's disease? Brain Res. Brain Res. Rev., 49, 618-632.
21. Beal, M.F. (2005) Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol., 58, 495-505.
22. Reddy, P.H. (2006) Amyloid precursor protein-mediated free radicals and oxidative damage: Implications for the development and progression of Alzheimer's disease. J. Neurochem., 96, 1-13.
23. Swerdlow, R.H., Parks, J.K., Cassarino, D.S., Maguire, D.J., Maguire, R.S., Bennett, J.P., Jr., Davis, R.E. and Parker, W.D., Jr. (1997) Cybrids in Alzheimer's disease: A cellular model of the disease? Neurology, 49, 918-925.
24. Khan, S.M., Cassarino, D.S., Abramova, N.N., Keeney, P.M., Borland, M.K., Trimmer, P.A., Krebs, C.T., Bennett, J.C., Parks, J.K., Swerdlow, R.H., Parker, W.D., Jr. and Bennett, J.P., Jr. (2000) Alzheimer's disease cybrids replicate beta-amyloid abnormalities through cell death pathways. Ann. Neurol., 48, 148-155.
25. Casley, C.S., Canevari, L., Land, J.M., Clark, J.B. and Sharpe, M.A. (2002) Beta-amyloid inhibits integrated mitochondrial respiration and key enzyme activities. J. Neurochem., 80, 91-100.
26. Cardoso, S.M., Santos, S., Swerdlow, R.H. and Oliveira, C.R. (2001) Functional mitochondria are required for amyloid beta-mediated neurotoxicity. FASEB J., 15, 1439-1441.
27. Cardoso, S.M., Santana, I., Swerdlow, R.H. and Oliveira, C.R. (2004) Mitochondria dysfunction of Alzheimer's disease cybrids enhances Abeta toxicity. J. Neurochem., 89, 1417-1426.
28. Keil, U., Bonert, A., Marques, C.A., Scherping, I., Weyermann, J., Strosznajder, J.B., Muller-Spahn, F., Haass, C., Czech, C., Pradier, L., Muller, W.E. and Eckert, A. (2004) Amyloid beta-induced changes in nitric oxide production and mitochondrial activity lead to apoptosis. J. Biol. Chem., 279, 50310-50320.
29. Crouch, P.J., Blake, R., Duce, J.A., Ciccotosto, G.D., Li, Q.X., Barnham, K.J., Curtain, C.C., Cherny, R.A., Cappai, R., Dyrks, T., Masters, C.L. and Trounce, I.A. (2005) Copper-dependent inhibition of human cytochrome c oxidase by a dimeric conformer of amyloid-beta 1-42. J. Neurosci., 25, 672-679.
30. Aleardi, A.M., Benard, G., Augereau, O., Malgat, M., Talbot, J.C., Mazat, J.P., Letellier, T., Dachary-Prigent, J., Solaini, G.C. and Rossignol, R. (2005) Gradual alteration of mitochondrial structure and function by beta-amyloids: Importance of membrane viscosity changes, energy deprivation, reactive oxygen species production, and cytochrome c release. J. Bioenerg. Biomembr., 37, 207-225.
31. 2 and kainic acid: implications for Alzheimer's disease. J. Neurochem., 96, 1322-1335.
32. Lustbader, J.W., Cirilli, M., Lin, C., Xu, H.W., Takuma, K., Wang, N., Caspersen, C., Chen, X., Pollak, S., Chaney, M. et al. (2004) ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science, 304, 448-452.
33. Smith, M.A., Perry, G., Richey, P.L., Sayre, L.M., Anderson, V.E., Beal, M.F. and Kowall, N. (1996) Oxidative damage in Alzheimer's. Nature, 382, 120-121.
34. Pratico, D., Uryu, K., Leight, S., Trojanoswki, J.Q. and Lee, V.M. (2001) Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J. Neurosci., 21, 4183-4187.
35. Thinakaran, G., Teplow, D.B., Siman, R., Greenberg, B. and Sisodia, S.S. (1996) Metabolism of the 'Swedish' amyloid precursor protein variant in neuro2a (N2a) cells. Evidence that cleavage at the 'beta-secretase' site occurs in the golgi apparatus. J. Biol. Chem., 271, 9390-9397.
36. Kayed, R., Head, E., Thompson, J.L., McIntire, T.M., Milton, S.C., Cotman, C.W. and Glabe, C.G. (2003) Common structure of soluble amyloid oligomers implies common mechanism of athogenesis. Science, 300, 486-489.
37. Schnaitman, C. and Greenawalt, J.W. (1968) Enzymatic properties of the inner and outer membranes of rat liver mitochondria. J. Cell Biol., 38, 158-175.
38. Kuo, Y.M., Emmerling, M.R., Vigo-Pelfrey, C., Kasunic, T.C., Kirkpatrick, J.B., Murdoch, G.H., Ball, M.J. and Roher, A.E. (1996) Water-soluble Abeta (N-40, N-42) oligomers in normal and Alzheimer disease brains. J. Biol. Chem., 271, 4077-4081.
39. Kokubo, H., Kayed, R., Glabe, C.G. and Yamaguchi, H. (2005) Soluble Abeta oligomers ultrastructurally localize to cell processes and might be related to synaptic dysfunction in Alzheimer's disease brain. Brain Res., 1031, 222-228.
40. Caspersen, C., Wang, N., Yao, J., Sosunov, A., Chen, X., Lustbader, J.W., Xu, H.W., Stern, D., McKhann, G. and Yan, S.D. (2005) Mitochondrial Abeta: A potential focal point for neuronal metabolic dysfunction in Alzheimer's disease. FASEB J., 19, 2021-2040.
41. Anandatheerthavarada, H.K., Biswas, G., Robin, M.A. and Avadhani, N.G. (2003) Mitochondrial targeting and a novel transmembrane arrest of Alzheimer's amyloid precursor protein impairs mitochondrial function in neuronal cells. J. Cell Biol., 161, 41-54.
42. Hansson, C.A., Frykman, S., Farmery, M.R., Tjernberg, L.O., Nilsberth, C., Pursglove, S.E., Ito, A., Winblad, B., Cowburn, R.F., Thyberg, J. and Ankarcrona, M. (2004) Nicastrin, presenilin, APH-1 and PEN-2 form active gamma-secretase complexes in mitochondria. J. Biol. Chem., 279, 51654-55160.
43. Helbock, H.J., Beckman, K.B., Shigenaga, M.K., Walter, P.B., Woodall, A.A., Yeo, H.C. and Ames, B.N. (1998) DNA oxidation matters: The HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-guanine. Proc. Natl Acad. Sci. USA, 95, 288-293.
44. Manczak, M., Jung, Y., Park, B.S., Partovi, D. and Reddy, P.H. (2005) Time-course of mitochondrial gene expressions in mice brains: implications for mitochondrial dysfunction, oxidative damage, and cytochrome c in aging. J. Neurochem., 92, 494-504.
45. Migliore, L., Fontana, I., Colognato, R., Coppede, F., Siciliano, G. and Murri, L. (2005) Searching for the role and the most suitable biomarkers of oxidative stress in Alzheimer's disease and in other neurodegenerative diseases. Neurobiol. Aging, 26, 587-595.
46. Pratico, D. (2005) Peripheral biomarkers of oxidative damage in Alzheimer's disease: The road ahead. Neurobiol. Aging, 26, 581-583.
47. Gibson, G.E. and Huang, H.M. (2005) Oxidative stress in Alzheimer's disease. Neurobiol. Aging, 26, 575-578.
48. Beal, M.F. (2005) Oxidative damage as an early marker of Alzheimer's disease and mild cognitive impairment. Neurobiol. Aging, 26, 585-586.
49. Korolainen, M.A., Goldsteins, G., Nyman, T.A., Alafuzoff, I., Koistinaho, J. and Pirttila, T. (2006) Oxidative modification of proteins in the frontal cortex of Alzheimer's disease brain. Neurobiol. Aging, 27, 42-53.
50. Boyd-Kimball, D., Castegna, A., Sultana, R., Poon, H.F., Petroze, R., Lynn, B.C., Klein, J.B. and Butterfield, D.A. (2005) Proteomic identification of proteins oxidized by Abeta(1-42) in synaptosomes: implications for Alzheimer's disease. Brain Res., 1044, 206-215.
51. Bush, A.I., Atwood, C.S., Goldstein, L.E., Huang, X. and Rogers, J. (2000) Could Abeta and AbetaPP be antioxidants? J. Alzheimers Dis., 2, 83-84.
52. Stein, T.D. and Johnson, J.A. (2002) Lack of neurodegeneration in transgenic mice overexpressing mutant amyloid precursor protein is associated with increased levels of transthyretin and the activation of cell survival pathways. J. Neurosci., 22, 7380-7388.
53. Reddy, P.H. Mitochondrial oxidative damage in Aging and Alzheimer's Disease: Implications to mitochondrially targeted antioxidants. J. Biomed. Biotech., in press.
54. Hsiao, K., Chapman, P., Nilsen, S., Eckman, C., Harigaya, Y., Younkin, S., Yang, F. and Cole, G. (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science, 274, 99-102.
55. Lim, G.P., Chu, T., Yang, F., Beech, W., Frautschy, S.A. and Cole, G.M. (2001) The curry spice curcumin reduces oxidative damage and amyloid pathology in an Alzheimer transgenic mouse. J. Neurosci., 21, 8370-8387.
56. Stackman, R.W., Eckenstein, F., Frei, B., Kulhanek, D., Nowlin, J. and Quinn, J.F. (2003) Prevention of age-related spatial memory deficits in a transgenic mouse model of Alzheimer's disease by chronic Ginkgo biloba treatment. Exp. Neurol., 184, 510-520.
57. Bijur, G.N. and Jope, R.S. (2003) Rapid accumulation of Akt in mitochondria following phosphatidylinositol 3-kinase activation. J. Neurochem., 87, 1427-1435.
58. McEnery, M.W., Dawson, T.M., Verma, A., Gurley, D., Colombini, M. and Snyder, S.H. (1993) Mitochondrial voltage-dependent anion channel. Immunochemical and immunohistochemical characterization in rat brain. J. Biol. Chem., 268, 23289-23296.
59. Smith, M.A., Hirai, K., Hsiao, K., Pappolla, M.A., Harris, P.L., Siedlak, S.L., Tabaton, M. and Perry, G. (1998) Amyloid-beta deposition in Alzheimer transgenic mice is associated with oxidative stress. J. Neurochem., 70, 2212-2215.