Abnormal mitochondrial dynamics and synaptic degeneration as early events in Alzheimer's disease: Implications to mitochondria-targeted antioxidant therapeutics

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 5, 2012, Pages 639-649

  Reddy, P Hemachandra ^a,b   Tripathi, Raghav ^a   Troung, Quang ^a   Tirumala, Karuna ^a   Reddy, Tejaswini P ^a   Anekonda, Vishwanath ^a   Shirendeb, Ulziibat P ^a   Calkins, Marcus J ^a   Reddy, Arubala P ^a   Mao, Peizhong ^a   Manczak, Maria ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Amyloid beta; Amyloid precursor protein; Antioxidant; Primary neuron; Reactive oxygen species

Indexed keywords

ALPHA TOCOPHEROL; AMYLOID BETA PROTEIN; ANTIOXIDANT; APHANORPHINE; CURCUMIN; CYTOCHROME C OXIDASE; DONEPEZIL; GINKGO BILOBA EXTRACT; GLUCOSE; HUPERZINE A; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MITOCHONDRIAL DNA; MITOFUSIN 1; MITOFUSIN 2; PLACEBO; REACTIVE OXYGEN METABOLITE; UBIQUINONE;

ALZHEIMER DISEASE; BIOGENESIS; CELL FUNCTION; CLINICAL EFFECTIVENESS; COGNITION; COGNITIVE DEFECT; COPY NUMBER VARIATION; DISEASE COURSE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; GENETIC SUSCEPTIBILITY; GLUCOSE METABOLISM; GLUCOSE UTILIZATION; HUMAN; LIPID PEROXIDATION; MENTAL TASK; MINI MENTAL STATE EXAMINATION; MITOCHONDRIAL VOLUME; MITOCHONDRION; NERVE CELL; NERVE CELL NECROSIS; NERVE FIBER; NEUROFIBRILLARY TANGLE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVIEW; SYNAPSE; WORKING MEMORY;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTIOXIDANTS; HUMANS; MICE; MICE, TRANSGENIC; MITOCHONDRIA; SYNAPSES;

MUS MUSCULUS;

EID: 84858281225     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2011.10.011     Document Type: Review

References (100)

1. Swerdlow R.H. The neurodegenerative mitochondriopathies. J. Alzheimers Dis. 2009, 17:737-751.
2. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
3. Reddy P.H., Beal M.F. Are mitochondria critical in the pathogenesis of Alzheimer's disease?. Brain Res. Brain Res. Rev. 2005, 49:618-632.
4. Reddy P.H. Mitochondrial medicine for aging and neurodegenerative diseases. Neuromolecular Med. 2008, 10:291-315.
5. Reddy P.H. Role of mitochondria in neurodegenerative diseases: mitochondria as a therapeutic target in Alzheimer's disease. CNS Spectr. 2009, 14:8-13. (discussion 16-8).
6. Krzywanski D.M., Moellering D.R., Fetterman J.L., Dunham-Snary K.J., Sammy M.J., Ballinger S.W. The mitochondrial paradigm for cardiovascular disease susceptibility and cellular function: a complementary concept to Mendelian genetics. Lab. Invest. 2011, 91:1122-1135.
7. Kuzmicic J., Del Campo A., Lopez-Crisosto C., Morales P.E., Pennanen C., Bravo-Sagua R., Hechenleitner J., Zepeda R., Castro P.F., Verdejo H.E., Parra V., Chiong M., Lavandero S. Mitochondrial dynamics: a potential new therapeutic target for heart failure. Rev. Esp. Cardiol. 2011, 64:916-923.
8. Camara A.K., Bienengraeber M., Stowe D.F. Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury. Front. Physiol. 2011, 2:13.
9. Schon E.A., Przedborski S. Mitochondria: the next (neurode)generation. Neuron 2011, 70:1033-1053.
10. Martin L.J. Mitochondrial and cell death mechanisms in neurodegenerative diseases. Pharmaceuticals (Basel) 2010, 3:839-915.
11. C.C. Cook, M. Higuchi, The awakening of an advanced malignant cancer: an insult to the mitochondrial genome, Biochim. Biophys. Acta (in press).
12. Wallace D.C. Mitochondria and cancer: Warburg addressed. Cold Spring Harb. Symp. Quant. Biol. 2005, 70:363-374.
13. Reddy P.H., Reddy T.P. Mitochondria as a therapeutic target for aging and neurodegenerative diseases. Curr. Alzheimer Res. 2011, 8:393-409.
14. Reddy P.H., Reddy T.P., Manczak M., Calkins M.J., Shirendeb U., Mao P. Dynamin-related protein 1 and mitochondrial fragmentation in neurodegenerative diseases. Brain Res. Rev. 2011, 67:103-118.
15. Wallace D.C. Mitochondrial diseases in man and mouse. Science 1999, 283:1482-1488.
16. Reddy P.H. Mitochondrial dysfunction in aging and Alzheimer's disease: strategies to protect neurons. Antioxid. Redox Signal. 2007, 9:1647-1658.
17. Chang D.T., Reynolds I.J. Mitochondrial trafficking and morphology in healthy and injured neurons. Prog. Neurobiol. 2006, 80:241-268.
18. Du H., Guo L., Fang F., Chen D., Sosunov A.A., McKhann G.M., Yan Y., Wang C., Zhang H., Molkentin J.D., Gunn-Moore F.J., Vonsattel J.P., Arancio O., Chen J.X., Yan S.D. Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer's disease. Nat. Med. 2008, 14:1097-1105.
19. Lustbader J.W., Cirilli M., Lin C., Xu H.W., Takuma K., Wang N., Caspersen C., Chen X., Pollak S., Chaney M., Trinchese F., Liu S., Gunn-Moore F., Lue L.F., Walker D.G., Kuppusamy P., Zewier Z.L., Arancio O., Stern D., Yan S.S., Wu H. ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science 2004, 304:448-452.
20. L. Devi, M. Ohno, Mitochondrial dysfunction and accumulation of the beta-secretase-cleaved C-terminal fragment of APP in Alzheimer's disease transgenic mice, Neurobiol. Dis. (in press).
21. Anderson S., Bankier A.T., Barrell B.G., de Bruijn M.H., Coulson A.R., Drouin J., Eperon I.C., Nierlich D.P., Roe B.A., Sanger F., Schreier P.H., Smith A.J., Staden R., Young I.G. Sequence and organization of the human mitochondrial genome. Nature 1981, 290:457-465.
22. Van Blerkom J. Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells. Reprod. Biomed. Online 2008, 16:553-569.
23. Boengler K., Heusch G., Schulz R. Nuclear-encoded mitochondrial proteins and their role in cardioprotection. Biochim. Biophys. Acta 2011, 1813:1286-1294.
24. Reddy P.H., Beal M.F. Amyloid beta, mitochondrial dysfunction and synaptic damage implications for cognitive decline in aging and Alzheimer's disease. Trends Mol. Med. 2008, 14:45-53.
25. Mattson M.P. Pathways towards and away from Alzheimer's disease. Nature 2004, 430:631-639.
26. Smith M.A., Perry G., Richey P.L., Sayre L.M., Anderson V.E., Beal M.F., Kowall N. Oxidative damage in Alzheimer's. Nature 1996, 382:120-121.
27. Maurer I., Zierz S., Moller H.J. A selective defect of cytochrome c oxidase is present in brain of Alzheimer disease patients. Neurobiol. Aging 2000, 21:455-462.
28. Hirai K., Aliev G., Nunomura A., Fujioka H., Russell R.L., Atwood C.S., Johnson A.B., Kress Y., Vinters H.V., Tabaton M., Shimohama S., Cash A.D., Siedlak S.L., Harris P.L., Jones P.K., Petersen R.B., Perry G., Smith M.A. Mitochondrial abnormalities in Alzheimer's disease. J. Neurosci. 2001, 21:3017-3023.
29. Devi L., Prabhu B.M., Galati D.F., Avadhani N.G., Anandatheerthavarada H.K. Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brain is associated with mitochondrial dysfunction. J. Neurosci. 2006, 26:9057-9068.
30. Caspersen C., Wang N., Yao J., Sosunov A., Chen X., Lustbader J.W., Xu H.W., Stern D., McKhann G., Yan S.D. Mitochondrial Abeta: a potential focal point for neuronal metabolic dysfunction in Alzheimer's disease. FASEB J. 2005, 19:2040-2041.
31. Manczak M., Park B.S., Jung Y., Reddy P.H. Differential expression of oxidative phosphorylation genes in patients with Alzheimer's disease: implications for early mitochondrial dysfunction and oxidative damage. Neuromolecular Med. 2004, 5:147-162.
32. Manczak M., Calkins M.J., Reddy P.H. Impaired mitochondrial dynamics and abnormal interaction of amyloid beta with mitochondrial protein Drp1 in neurons from patients with Alzheimer's disease: implications for neuronal damage. Hum. Mol. Genet. 2011, 20:2495-2509.
33. Parker W.D., Filley C.M., Parks J.K. Cytochrome oxidase deficiency in Alzheimer's disease. Neurology 1990, 40:1302-1303.
34. Reddy P.H., McWeeney S., Park B.S., Manczak M., Gutala R.V., Partovi D., Jung Y., Yau V., Searles R., Mori M., Quinn J. 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. 2004, 13:1225-1240.
35. Manczak M., Anekonda T.S., Henson E., Park B.S., Quinn J., Reddy P.H. Mitochondria are a direct site of A beta accumulation in Alzheimer's disease neurons: implications for free radical generation and oxidative damage in disease progression. Hum. Mol. Genet. 2006, 15:1437-1449.
36. Li F., Calingasan N.Y., Yu F., Mauck W.M., Toidze M., Almeida C.G., Takahashi R.H., Carlson G.A., Flint Beal M., Lin M.T., Gouras G.K. Increased plaque burden in brains of APP mutant MnSOD heterozygous knockout mice. J. Neurochem. 2004, 89:1308-1312.
37. Eckert A., Hauptmann S., Scherping I., Rhein V., Muller-Spahn F., Gotz J., Muller W.E. Soluble beta-amyloid leads to mitochondrial defects in amyloid precursor protein and tau transgenic mice. Neurodegener. Dis. 2008, 5:157-159.
38. Rhein V., Song X., Wiesner A., Ittner L.M., Baysang G., Meier F., Ozmen L., Bluethmann H., Drose S., Brandt U., Savaskan E., Czech C., Gotz J., Eckert A. Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20057-20062.
39. Drago D., Cavaliere A., Mascetra N., Ciavardelli D., di Ilio C., Zatta P., Sensi S.L. Aluminum modulates effects of beta amyloid(1-42) on neuronal calcium homeostasis and mitochondria functioning and is altered in a triple transgenic mouse model of Alzheimer's disease. Rejuvenation Res. 2008, 11:861-871.
40. Resende R., Moreira P.I., Proenca T., Deshpande A., Busciglio J., Pereira C., Oliveira C.R. Brain oxidative stress in a triple-transgenic mouse model of Alzheimer disease. Free Radic. Biol. Med. 2008, 44:2051-2057.
41. Sensi S.L., Rapposelli I.G., Frazzini V., Mascetra N. Altered oxidant-mediated intraneuronal zinc mobilization in a triple transgenic mouse model of Alzheimer's disease. Exp. Gerontol. 2008, 43:488-492.
42. Yao J., Irwin R.W., Zhao L., Nilsen J., Hamilton R.T., Brinton R.D. Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14670-14675.
43. Dragicevic N., Mamcarz M., Zhu Y., Buzzeo R., Tan J., Arendash G.W., Bradshaw P.C. Mitochondrial amyloid-beta levels are associated with the extent of mitochondrial dysfunction in different brain regions and the degree of cognitive impairment in Alzheimer's transgenic mice. J. Alzheimers Dis. 2010, 20(Suppl. 2):S535-S550.
44. Wang X., Su B., Siedlak S.L., Moreira P.I., Fujioka H., Wang Y., Casadesus G., Zhu X. Amyloid-beta overproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fission/fusion proteins. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19318-19323.
45. Wang X., Su B., Lee H.G., Li X., Perry G., Smith M.A., Zhu X. Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J. Neurosci. 2009, 29:9090-9103.
46. Manczak M., Mao P., Calkins M.J., Cornea A., Reddy A.P., Murphy M.P., Szeto H.H., Park B., Reddy P.H. Mitochondria-targeted antioxidants protect against amyloid-beta toxicity in Alzheimer's disease neurons. J. Alzheimers Dis. 2010, 20(Suppl. 2):S609-S631.
47. Du H., Guo L., Yan S., Sosunov A.A., McKhann G.M., Yan S.S. Early deficits in synaptic mitochondria in an Alzheimer's disease mouse model. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:18670-18675.
48. Calkins M.J., Manczak M., Mao P., Shirendeb U., Reddy P.H. Impaired mitochondrial biogenesis, defective axonal transport of mitochondria, abnormal mitochondrial dynamics and synaptic degeneration in a mouse model of Alzheimer's disease. Hum. Mol. Genet. 2011, 20:4515-4529.
49. Calkins M.J., Reddy P.H. Assessment of newly synthesized mitochondrial DNA using BrdU labeling in primary neurons from Alzheimer's disease mice: implications for impaired mitochondrial biogenesis and synaptic damage. Biochim. Biophys. Acta 2011, 1812:1182-1189.
50. Calkins M.J., Reddy P.H. Amyloid beta impairs mitochondrial anterograde transport and degenerates synapses in Alzheimer's disease neurons. Biochim. Biophys. Acta 2011, 1812:507-513.
51. Reiman E.M., Caselli R.J., Yun L.S., Chen K., Bandy D., Minoshima S., Thibodeau S.N., Osborne D. Preclinical evidence of Alzheimer's disease in persons homozygous for the epsilon 4 allele for apolipoprotein E. N. Engl. J. Med. 1996, 334:752-758.
52. Mosconi L., de Leon M., Murray J., E.L., Lu J., Javier E., McHugh P., Swerdlow R.H. Reduced mitochondria cytochrome oxidase activity in adult children of mothers with Alzheimer's disease. J. Alzheimers Dis. 2011, 27:483-490.
53. Lin M.T., Simon D.K., Ahn C.H., Kim L.M., Beal M.F. High aggregate burden of somatic mtDNA point mutations in aging and Alzheimer's disease brain. Hum. Mol. Genet. 2002, 11:133-145.
54. Coskun P.E., Beal M.F., Wallace D.C. Alzheimer's brains harbor somatic mtDNA control-region mutations that suppress mitochondrial transcription and replication. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:10726-10731.
55. Coskun P.E., Wyrembak J., Derbereva O., Melkonian G., Doran E., Lott I.T., Head E., Cotman C.W., Wallace D.C. Systemic mitochondrial dysfunction and the etiology of Alzheimer's disease and down syndrome dementia. J. Alzheimers Dis. 2010, 20(Suppl. 2):S293-S310.
56. Lakatos A., Derbeneva O., Younes D., Keator D., Bakken T., Lvova M., Brandon M., Guffanti G., Reglodi D., Saykin A., Weiner M., Macciardi F., Schork N., Wallace D.C., Potkin S.G. Association between mitochondrial DNA variations and Alzheimer's disease in the ADNI cohort. Neurobiol. Aging 2010, 31:1355-1363. Alzheimer's Disease Neuroimaging Initiative.
57. 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. 1994, 24:336-340.
58. Manczak M., Jung Y., Park B.S., Partovi D., Reddy P.H. Time-course of mitochondrial gene expressions in mice brains: implications for mitochondrial dysfunction, oxidative damage, and cytochrome c in aging. J. Neurochem. 2005, 92:494-504.
59. Butterfield D.A., Drake J., Pocernich C., Castegna A. Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends Mol. Med. 2001, 7:548-554.
60. Smith M.A., Hirai K., Hsiao K., Pappolla M.A., Harris P.L., Siedlak S.L., Tabaton M., Perry G. Amyloid-beta deposition in Alzheimer transgenic mice is associated with oxidative stress. J. Neurochem. 1998, 70:2212-2215.
61. Pratico D., Uryu K., Leight S., Trojanoswki J.Q., Lee V.M. Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J. Neurosci. 2001, 21:4183-4187.
62. 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., Trounce I.A. Copper-dependent inhibition of human cytochrome c oxidase by a dimeric conformer of amyloid-beta1-42. J. Neurosci. 2005, 25:672-679.
63. Hansson Petersen C.A., Alikhani N., Behbahani H., Wiehager B., Pavlov P.F., Alafuzoff I., Leinonen V., Ito A., Winblad B., Glaser E., Ankarcrona M. The amyloid beta-peptide is imported into mitochondria via the TOM import machinery and localized to mitochondrial cristae. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13145-13150.
64. Zhao X.L., Wang W.A., Tan J.X., Huang J.K., Zhang X., Zhang B.Z., Wang Y.H., YangCheng H.Y., Zhu H.L., Sun X.J., Huang F.D. Expression of beta-amyloid induced age-dependent presynaptic and axonal changes in Drosophila. J. Neurosci. 2010, 30:1512-1522.
65. Rui Y., Tiwari P., Xie Z., Zheng J.Q. Acute impairment of mitochondrial trafficking by beta-amyloid peptides in hippocampal neurons. J. Neurosci. 2006, 26:10480-10487.
66. Wang X., Perry G., Smith M.A., Zhu X. Amyloid-beta-derived diffusible ligands cause impaired axonal transport of mitochondria in neurons. Neurodegener. Dis. 2010, 7:56-59.
67. Nakashima H., Ishihara T., Yokota O., Terada S., Trojanowski J.Q., Lee V.M., Kuroda S. Effects of alpha-tocopherol on an animal model of tauopathies. Free Radic. Biol. Med. 2004, 37:176-186.
68. Conte V., Uryu K., Fujimoto S., Yao Y., Rokach J., Longhi L., Trojanowski J.Q., Lee V.M., McIntosh T.K., Pratico D. Vitamin E reduces amyloidosis and improves cognitive function in Tg2576 mice following repetitive concussive brain injury. J. Neurochem. 2004, 90:758-764.
69. Sung S., Yao Y., Uryu K., Yang H., Lee V.M., Trojanowski J.Q., Pratico D. Early vitamin E supplementation in young but not aged mice reduces Abeta levels and amyloid deposition in a transgenic model of Alzheimer's disease. FASEB J. 2004, 18:323-325.
70. Matsubara E., Bryant-Thomas T., Pacheco Quinto J., Henry T.L., Poeggeler B., Herbert D., Cruz-Sanchez F., Chyan Y.J., Smith M.A., Perry G., Shoji M., Abe K., Leone A., Grundke-Ikbal I., Wilson G.L., Ghiso J., Williams C., Refolo L.M., Pappolla M.A., Chain D.G., Neria E. Melatonin increases survival and inhibits oxidative and amyloid pathology in a transgenic model of Alzheimer's disease. J. Neurochem. 2003, 85:1101-1108.
71. Stackman R.W., Eckenstein F., Frei B., Kulhanek D., Nowlin J., Quinn J.F. Prevention of age-related spatial memory deficits in a transgenic mouse model of Alzheimer's disease by chronic Ginkgo biloba treatment. Exp. Neurol. 2003, 184:510-520.
72. Yang F., Lim G.P., Begum A.N., Ubeda O.J., Simmons M.R., Ambegaokar S.S., Chen P.P., Kayed R., Glabe C.G., Frautschy S.A., Cole G.M. Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J. Biol. Chem. 2005, 280:5892-5901.
73. Morris M.C., Beckett L.A., Scherr P.A., Hebert L.E., Bennett D.A., Field T.S., Evans D.A. Vitamin E and vitamin C supplement use and risk of incident Alzheimer disease. Alzheimer Dis. Assoc. Disord. 1998, 12:121-126.
74. Morris M.C., Evans D.A., Bienias J.L., Tangney C.C., Wilson R.S. Vitamin E and cognitive decline in older persons. Arch. Neurol. 2002, 59:1125-1132.
75. Morris M.C., Evans D.A., Tangney C.C., Bienias J.L., Wilson R.S., Aggarwal N.T., Scherr P.A. Relation of the tocopherol forms to incident Alzheimer disease and to cognitive change. Am. J. Clin. Nutr. 2005, 81:508-514.
76. Grundman M., Petersen R.C., Ferris S.H., Thomas R.G., Aisen P.S., Bennett D.A., Foster N.L., Jack C.R., Galasko D.R., Doody R., Kaye J., Sano M., Mohs R., Gauthier S., Kim H.T., Jin S., Schultz A.N., Schafer K., Mulnard R., van Dyck C.H., Mintzer J., Zamrini E.Y., Cahn-Weiner D., Thal L.J. Mild cognitive impairment can be distinguished from Alzheimer disease and normal aging for clinical trials. Arch. Neurol. 2004, 61:59-66. Alzheimer's Disease Cooperative Study.
77. Cornelli U. Treatment of Alzheimer's disease with a cholinesterase inhibitor combined with antioxidants. Neurodegener. Dis. 2010, 7:193-202.
78. Schneider L.S., Raman R., Schmitt F.A., Doody R.S., Insel P., Clark C.M., Morris J.C., Reisberg B., Petersen R.C., Ferris S.H. Characteristics and performance of a modified version of the ADCS-CGIC CIBIC+ for mild cognitive impairment clinical trials. Alzheimer Dis. Assoc. Disord. 2009, 23:260-267.
79. Lu P.H., Edland S.D., Teng E., Tingus K., Petersen R.C., Cummings J.L. Donepezil delays progression to AD in MCI subjects with depressive symptoms. Neurology 2009, 72:2115-2121. Alzheimer's Disease Cooperative Study Group.
80. Lloret A., Badia M.C., Mora N.J., Pallardo F.V., Alonso M.D., Vina J. Vitamin E paradox in Alzheimer's disease: it does not prevent loss of cognition and may even be detrimental. J. Alzheimers Dis. 2009, 17:143-149.
81. Pratico D. Evidence of oxidative stress in Alzheimer's disease brain and antioxidant therapy: lights and shadows. Ann. N. Y. Acad. Sci. 2008, 1147:70-78.
82. Isaac M.G., Quinn R., Tabet N. Vitamin E for Alzheimer's disease and mild cognitive impairment. Cochrane Database Syst. Rev. 2008, (3):CD002854.
83. DeCarli C., Frisoni G.B., Clark C.M., Harvey D., Grundman M., Petersen R.C., Thal L.J., Jin S., Jack C.R., Scheltens P. Qualitative estimates of medial temporal atrophy as a predictor of progression from mild cognitive impairment to dementia. Arch. Neurol. 2007, 64:108-115. Alzheimer's Disease Cooperative Study Group.
84. Burns A., O'Brien J., Auriacombe S., Ballard C., Broich K., Bullock R., Feldman H., Ford G., Knapp M., McCaddon A., Iliffe S., Jacova C., Jones R., Lennon S., McKeith I., Orgogozo J.M., Purandare N., Richardson M., Ritchie C., Thomas A., Warner J., Wilcock G., Wilkinson D. Clinical practice with anti-dementia drugs: a consensus statement from British Association for Psychopharmacology. J. Psychopharmacol. 2006, 20:732-755. BAP Dementia Consensus group, British Association for PsychopharmacologyBritish Association for Psychopharmacology.
85. Sparks D.L., Sabbagh M., Connor D., Soares H., Lopez J., Stankovic G., Johnson-Traver S., Ziolkowski C., Browne P. Statin therapy in Alzheimer's disease. Acta Neurol. Scand. Suppl. 2006, 185:78-86.
86. Ciabattoni G., Porreca E., Di Febbo C., Di Iorio A., Paganelli R., Bucciarelli T., Pescara L., Del Re L., Giusti C., Falco A., Sau A., Patrono C., Davi G. Determinants of platelet activation in Alzheimer's disease. Neurobiol. Aging 2007, 28:336-342.
87. Pham D.Q., Plakogiannis R. Vitamin E supplementation in Alzheimer's disease, Parkinson's disease, tardive dyskinesia, and cataract: Part 2. Ann. Pharmacother. 2005, 39:2065-2072.
88. Boothby L.A., Doering P.L. Vitamin C and vitamin E for Alzheimer's disease. Ann. Pharmacother. 2005, 39:2073-2080.
89. Petersen R.C., Thomas R.G., Grundman M., Bennett D., Doody R., Ferris S., Galasko D., Jin S., Kaye J., Levey A., Pfeiffer E., Sano M., van Dyck C.H., Thal L.J. Vitamin E and donepezil for the treatment of mild cognitive impairment. N. Engl. J. Med. 2005, 352:2379-2388. Alzheimer's Disease Cooperative Study Group.
90. Rafii M.S., Walsh S., Little J.T., Behan K., Reynolds B., Ward C., Jin S., Thomas R., Aisen P.S. A phase II trial of huperzine A in mild to moderate Alzheimer disease. Neurology 2011, 76:1389-1394. Alzheimer's Disease Cooperative Study.
91. Szeto H.H. Mitochondria-targeted peptide antioxidants: novel neuroprotective agents. AAPS J. 2006, 8:E521-E531.
92. Reddy P.H. Mitochondrial oxidative damage in aging and Alzheimer's disease: implications for mitochondrially targeted antioxidant therapeutics. J. Biomed. Biotechnol. 2006, 2006:31372.
93. Sheu S.S., Nauduri D., Anders M.W. Targeting antioxidants to mitochondria: a new therapeutic direction. Biochim. Biophys. Acta 2006, 1762:256-265.
94. Murphy M.P., Smith R.A. Targeting antioxidants to mitochondria by conjugation to lipophilic cations. Annu. Rev. Pharmacol. Toxicol. 2007, 47:629-656.
95. Szeto H.H. Cell-permeable, mitochondrial-targeted, peptide antioxidants. AAPS J. 2006, 8:E277-E283.
96. Szeto H.H. Development of mitochondria-targeted aromatic-cationic peptides for neurodegenerative diseases. Ann. N. Y. Acad. Sci. 2008, 1147:112-121.
97. Cho J., Won K., Wu D., Soong Y., Liu S., Szeto H.H., Hong M.K. Potent mitochondria-targeted peptides reduce myocardial infarction in rats. Coron. Artery Dis. 2007, 18:215-220.
98. Thomas D.A., Stauffer C., Zhao K., Yang H., Sharma V.K., Szeto H.H., Suthanthiran M. Mitochondrial targeting with antioxidant peptide SS-31 prevents mitochondrial depolarization, reduces islet cell apoptosis, increases islet cell yield, and improves posttransplantation function. J. Am. Soc. Nephrol. 2007, 18:213-222.
99. Cho S., Szeto H.H., Kim E., Kim H., Tolhurst A.T., Pinto J.T. A novel cell-permeable antioxidant peptide, SS31, attenuates ischemic brain injury by down-regulating CD36. J. Biol. Chem. 2007, 282:4634-4642.
100. Petri S., Kiaei M., Damiano M., Hiller A., Wille E., Manfredi G., Calingasan N.Y., Szeto H.H., Beal M.F. Cell-permeable peptide antioxidants as a novel therapeutic approach in a mouse model of amyotrophic lateral sclerosis. J. Neurochem. 2006, 98:1141-1148.