Interaction between NH2-tau fragment and Aβ in Alzheimer's disease mitochondria contributes to the synaptic deterioration

Neurobiology of Aging

Volumn 33, Issue 4, 2012, Pages 833.e1-833.e25

  Amadoro, Giuseppina ^a   Corsetti, Veronica ^b   Atlante, Anna ^c   Florenzano, Fulvio ^c,d   Capsoni, Simona ^e   Bussani, Rossana ^f   Mercanti, Delio ^c   Calissano, Pietro ^g  

^a INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c CNR   (Italy)

^d IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^e SCUOLA NORMALE SUPERIORE   (Italy)

^f UNIVERSITY OF TRIESTE   (Italy)

^g EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

Author keywords

Alzheimer's disease; A ; Mitochondria; Neurodegeneration; Synapse(s); Tau

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; AMYLOID BETA PROTEIN[1-42]; CYCLOPHILIN D; TAU PROTEIN;

ADULT; AGED; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; HUMAN CELL; HUMAN TISSUE; MITOCHONDRION; NEUROTOXICITY; PRIORITY JOURNAL; PROTEIN INTERACTION; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 84856953764     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.08.001     Document Type: Article

References (183)

1. Aleardi A.M., Benard G., Augereau O., Malgat M., Talbot J.C., Mazat J.P., Letellier T., Dachary-Prigent J., Solaini G.C., Rossignol R. 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 2005, 37:207-225.
2. Amadoro G., Ciotti M.T., Costanzi M., Cestari V., Calissano P., Canu N. NMDA receptor mediates tau-induced neurotoxicity by calpain and ERK/MAPK activation. Proc. Natl. Acad. Sci. U. S. A 2006, 103:2892-2897.
3. Amadoro G., Corsetti V., Stringaro A., Colone M., D'Aguanno S., Meli G., Ciotti M., Sancesario G., Cattaneo A., Bussani R., Mercanti D., Calissano P. A NH2 tau fragment targets neuronal mitochondria at AD synapses: possible implications for neurodegeneration J. Alzheimers Dis 2010, 21:445-470.
4. Amadoro G., Serafino A.L., Barbato C., Ciotti M.T., Sacco A., Calissano P., Canu N. Role of N-terminal tau domain integrity on the survival of cerebellar granule neurons. Cell Death Differ 2004, 11:217-230.
5. Anandatheerthavarada H.K., Biswas G., Robin M.A., Avadhani N.G. Mitochondrial targeting and a novel transmembrane arrest of Alzheimer's amyloid precursor protein impairs mitochondrial function in neuronal cells. J. Cell Biol 2003, 161:41-54.
6. Arendt T. Synaptic degeneration in Alzheimer's disease. Acta Neuropathol 2009, 118:167-179.
7. Arispe N., Pollard H.B., Rojas E. beta-Amyloid Ca(2+)-channel hypothesis for neuronal death in Alzheimer disease. Mol. Cell. Biochem 1994, 140:119-125.
8. Atlante A., Amadoro G., Bobba A., de Bari L., Corsetti V., Pappalardo G., Marra E., Calissano P., Passarella S. A peptide containing residues 26-44 of tau protein impairs mitochondrial oxidative phosphorylation acting at the level of the adenine nucleotide translocator. Biochim. Biophys. Acta 2008, 1777:1289-1300.
9. Atlante A., Bobba A., de Bari L., Fontana F., Calissano P., Marra E., Passarella S. Caspase-dependent alteration of the ADP/ATP translocator triggers the mitochondrial permeability transition which is not required for the low-potassium-dependent apoptosis of cerebellar granule cells. J. Neurochem 2006, 97:1166-1181.
10. Attems J., Jellinger K.A. Hippocampal sclerosis in Alzheimer disease and other dementias. Neurology 2006, 66:775.
11. Avila J., Lucas J.J., Perez M., Hernandez F. Role of tau protein in both physiological and pathological conditions. Physiol. Rev 2004, 84:361-384.
12. Badugu R., Garcia M., Bondada V., Joshi A., Geddes J.W. N terminus of calpain 1 is a mitochondrial targeting sequence. J. Biol. Chem 2008, 283:3409-3417.
13. Baloyannis S.J. Mitochondrial alterations in Alzheimer's disease. J. Alzheimers Dis 2006, 9:119-126.
14. Banaclocha M.M., Hernández A.I., Martínez N., Ferrándiz M.L. N-acetylcysteine protects against age-related increase in oxidized proteins in mouse synaptic mitochondria. Brain Res 1997, 762:256-258.
15. Barelli H., Lebeau A., Vizzavona J., Delaere P., Chevallier N., Drouot C., Marambaud P., Ancolio K., Buxbaum J.D., Khorkova O., Heroux J., Sahasrabudhe S., Martinez J., Warter J.M., Mohr M., Checler F. Characterization of new polyclonal antibodies specific for 40 and 42 amino acid-long amyloid beta peptides: their use to examine the cell biology of presenilins and the immunohistochemistry of sporadic Alzheimer's disease and cerebral amyloid angiopathy cases. Mol. Med 1997, 10:695-707.
16. Bauer M.K., Schubert A., Rocks O., Grimm S. Adenine nucleotide translocase-1, a component of the permeability transition pore, can dominantly induce apoptosis. J. Cell Biol 1999, 147:1493-1502.
17. Billups B., Forsythe I.D. Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J. Neurosci 2002, 22:5840-5847.
18. Blass J.P. Cerebrometabolic abnormalities in Alzheimer's disease. Neurol. Res 2003, 25:556-566.
19. Blennow K., de Leon M.J., Zetterberg H. Alzheimer's disease. Lancet 2006, 368:387-403.
20. Bolte S., Cordelieres F.P. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc 2006, 224:213-232.
21. Boopathi E., Srinivasan S., Fang J.K., Avadhani N.G. Bimodal protein targeting through activation of cryptic mitochondrial targeting signals by an inducible cytosolic endoprotease. Mol. Cell 2008, 32:32-42.
22. Brandt R., Léger J., Lee G. Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. J. Cell Biol 1995, 131:1327-1340.
23. Brown M.R., Sullivan P.G., Geddes J.W. Synaptic mitochondria are more susceptible to Ca2+ overload than nonsynaptic mitochondria. J. Biol. Chem 2006, 281:11658-11668.
24. Bubber P., Haroutunian V., Fisch G., Blass J.P., Gibson G.E. Mitochondrial abnormalities in Alzheimer brain: mechanistic implications. Ann. Neurol 2005, 57:695-703.
25. Burdick D., Soreghan B., Kwon M., Kosmoski J., Knauer M., Henschen A., Yates J., Cotman C., Glabe C. Assembly and aggregation properties of synthetic Alzheimer's A4/beta amyloid peptide analogs. J. Biol. Chem 1992, 267:546-554.
26. Cardoso S.M., Proença M.T., Santos S., Santana I., Oliveira C.R. Cytochrome c oxidase is decreased in Alzheimer's disease platelets. Neurobiol. Aging 2004, 25:105-110.
27. Casley C.S., Canevari L., Land J.M., Clark J.B., Sharpe M.A. Beta-amyloid inhibits integrated mitochondrial respiration and key enzyme activities. J. Neurochem 2002, 80:91-100.
28. Casley C.S., Land J.M., Sharpe M.A., Clark J.B., Duchen M.R., Canevari L. Beta-amyloid fragment 25-35 causes mitochondrial dysfunction in primary cortical neurons. Neurobiol. Dis 2002, 10:258-267.
29. 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.
30. Cente M., Filipcik P., Pevalova M., Novak M. Expression of a truncated tau protein induces oxidative stress in a rodent model of tauopathy. Eur. J. Neurosci 2006, 24:1085-1090.
31. Chagnon P., Bétard C., Robitaille Y., Cholette A., Gauvreau D. Distribution of brain cytochrome oxidase activity in various neurodegenerative diseases. Neuroreport 1995, 6:711-715.
32. Chee F.C., Mudher A., Cuttle M.F., Newman T.A., MacKay D., Lovestone S., Shepherd D. Over-expression of tau results in defective synaptic transmission in Drosophila neuromuscular junctions. Neurobiol. Dis 2005, 20:918-928.
33. Chen J.X., Yan S.D. Pathogenic role of mitochondrial amyloid-beta peptide. Expert Rev. Neurother 2007, 7:1517-1525.
34. Chen J.X., Yan S.S. Role of mitochondrial amyloid-beta in Alzheimer's disease. J. Alzheimers Dis. 2010, 20(suppl):S569-S578.
35. Chen X., Yan S.D. Mitochondrial Abeta: a potential cause of metabolic dysfunction in Alzheimer's disease. IUBMB Life 2006, 58:686-694.
36. Cho K.O., Hunt C.A., Kennedy M.B. The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 1992, 9:929-942.
37. Chong Y.H., Shin Y.J., Lee E.O., Kayed R., Glabe C.G., Tenner A.J. ERK1/2 activation mediates Abeta oligomer-induced neurotoxicity via caspase-3 activation and tau cleavage in rat organotypic hippocampal slice cultures. J. Biol. Chem 2006, 281:20315-20325.
38. Chou J.L., Shenoy D.V., Thomas N., Choudhary P.K., Laferla F.M., Goodman S.R., Breen G.A. Early dysregulation of the mitochondrial proteome in a mouse model of Alzheimer's disease. J Proteomics 2011, 74:466-479.
39. Ciavardelli D., Silvestri E., Viscovo A.D., Bomba M., Gregorio D.D., Moreno M., Ilio C.D., Goglia F., Canzoniero L.M., Sensi S.L. Alterations of brain and cerebellar proteomes linked to Aβ and tau pathology in a female triple-transgenic murine model of Alzheimer's disease. Cell Death. Disorders 2010, 1:e90.
40. Corsetti V., Amadoro G., Gentile A., Capsoni S., Ciotti M.T., Cencioni M.T., Atlante A., Canu N., Rohn T.T., Cattaneo A., Calissano P. Identification of a caspase-derived N-terminal tau fragment in cellular and animal Alzheimer's disease models. Mol. Cell. Neurosci 2008, 38:381-392.
41. 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.
42. D'Amelio M., Cavallucci V., Middei S., Marchetti C., Pacioni S., Ferri A., Diamantini A., De Zio D., Carrara P., Battistini L., Moreno S., Bacci A., Ammassari-Teule M., Marie H., Cecconi F. Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nat. Neurosci 2011, 14:69-76.
43. Dahlgren K.N., Manelli A.M., Stine W.B., Baker L.K., Krafft G.A., LaDu M.J. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J. Biol. Chem 2002, 277:32046-32053.
44. David D.C., Hauptmann S., Scherping I., Schuessel K., Keil U., Rizzu P., Ravid R., Dröse S., Brandt U., Müller W.E., Eckert A., Götz J. Proteomic and functional analyses reveal a mitochondrial dysfunction in P301L tau transgenic mice. J. Biol. Chem. 2005, 280:23802-23814.
45. De Felice F.G., Houzel J.C., Garcia-Abreu J., Louzada P.R., Afonso R.C., Meirelles M.N., Lent R., Neto V.M., Ferreira S.T. Inhibition of Alzheimer's disease beta-amyloid aggregation, neurotoxicity, and in vivo deposition by nitrophenols: implications for Alzheimer's therapy. FASEB J 2001, 15:1297-1299.
46. Decker H., Lo K.Y., Unger S.M., Ferreira S.T., Silverman M.A., Silverman M.A. Amyloid-beta peptide oligomers disrupt axonal transport through an NMDA receptor-dependent mechanism that is mediated by glycogen synthase kinase 3beta in primary cultured hippocampal neurons. J. Neurosci 2010, 30:9166-9171.
47. Delacourte A., Sergeant N., Champain D., Wattez A., Maurage C.A., Lebert F., Pasquier F., David J.P. Nonoverlapping but synergetic tau and APP pathologies in sporadic Alzheimer's disease. Neurology 2002, 59:398-407.
48. Deshpande A., Mina E., Glabe C., Busciglio J. Different conformations of amyloid beta induce neurotoxicity by distinct mechanisms in human cortical neurons. J. Neurosci 2006, 26:6011-6018.
49. Devi L., Anandatheerthavarada H.K. Mitochondrial trafficking of APP and alpha synuclein: Relevance to mitochondrial dysfunction in Alzheimer's and Parkinson's diseases. Biochim. Biophys. Acta 2010, 1802:11-19.
50. 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.
51. Devi L., Raghavendran V., Prabhu B.M., Avadhani N.G., Anandatheerthavarada H.K. Mitochondrial import and accumulation of alpha-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. J. Biol. Chem 2008, 283:9089-9100.
52. Diana F.F., Silva Esteves A.R., Oliveira C.R., Cardoso S.M. Mitochondria: the common upstream driver of abeta and tau pathology in Alzheimer's disease. Curr. Alzheimer Res 2011, 8:563-572.
53. 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.
54. 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.
55. Du H., Yan S.S. Mitochondrial medicine for neurodegenerative diseases. Int. J. Biochem. Cell Biol 2010, 42:560-572.
56. Duda J.E., Giasson B.I., Mabon M.E., Miller D.C., Golbe L.I., Lee V.M., Trojanowski J.Q. Concurrence of alpha-synuclein and tau brain pathology in the Contursi kindred. Acta Neuropathol 2002, 104:7-11.
57. Eckert A., Hauptmann S., Scherping I., Meinhardt J., Rhein V., Dröse S., Brandt U., Fändrich M., Müller W.E., Götz J. Oligomeric and fibrillar species of beta-amyloid (A beta 42) both impair mitochondrial function in P301L tau transgenic mice. J. Mol. Med. 2008, 86:1255-1267.
58. Eckert A., Schulz K.L., Rhein V., Götz J. Convergence of amyloid-beta and tau pathologies on mitochondria in vivo. Mol. Neurobiol. 2010, 41:107-114.
59. Escobar-Khondiker M., Höllerhage M., Muriel M.P., Champy P., Bach A., Depienne C., Respondek G., Yamada E.S., Lannuzel A., Yagi T., Hirsch E.C., Oertel W.H., Jacob R., Michel P.P., Ruberg M., Höglinger G.U. Annonacin, a natural mitochondrial complex I inhibitor, causes tau pathology in cultured neurons. J. Neurosci. 2007, 27:7827-7837.
60. Evans R.J., Derkach V., Surprenant A. ATP mediates fast synaptic transmission in mammalian neurons. Nature 1992, 357:503-505.
61. Fein J.A., Sokolow S., Miller C.A., Vinters H.V., Yang F., Cole G.M., Gylys K.H. Co-localization of amyloid beta and tau pathology in Alzheimer's disease synaptosomes. Am. J. Pathol 2008, 172:1683-1692.
62. Fernández-Vizarra P., Fernández A.P., Castro-Blanco S., Serrano J., Bentura M.L., Martínez-Murillo R., Martínez A., Rodrigo J. Intra- and extracellular Abeta and PHF in clinically evaluated cases of Alzheimer's disease. Histol. Histopathol 2004, 19:823-844.
63. Galindo M.F., Ikuta I., Zhu X., Casadesus G., Jordán J. Mitochondrial biology in Alzheimer's disease pathogenesis. J. Neurochem 2010, 114:933-945.
64. Gamblin T.C., Berry R.W., Binder L.I. Modeling tau polymerization in vitro: a review and synthesis. Biochemistry 2003, 42:15009-15017.
65. Giasson B.I., Forman M.S., Higuchi M., Golbe L.I., Graves C.L., Kotzbauer P.T., Trojanowski J.Q., Lee V.M. Initiation and synergistic fibrillization of tau and alpha-synuclein. Science 2003, 300:636-640.
66. Gillardon F., Rist W., Kussmaul L., Vogel J., Berg M., Danzer K., Kraut N., Hengerer B. Proteomic and functional alterations in brain mitochondria from Tg2576 mice occur before amyloid plaque deposition. Proteomics 2007, 7:605-616.
67. Giorgi C., De Stefani D., Bononi A., Rizzuto R., Pinton P. Structural and functional link between the mitochondrial network and the endoplasmic reticulum. Int. J. Biochem. Cell Biol 2009, 41:1817-1827.
68. Götz J., Chen F., van Dorpe J., Nitsch R.M. Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils. Science 2001, 293:1491-1495.
69. Götz J., Ittner L.M., Kins S. Do axonal defects in tau and amyloid precursor protein transgenic animals model axonopathy in Alzheimer's disease?. J Neurochem 2006, 98:993-1006.
70. Götz J., Ittner L.M., Schonrock N., Cappai R. An update on the toxicity of Abeta in Alzheimer's disease. Neuropsychiatr. Dis. Treat. 2008, 4:1033-1042.
71. Gouras G.K., Tampellini D., Takahashi R.H., Capetillo-Zarate E. Intraneuronal beta-amyloid accumulation and synapse pathology in Alzheimer's disease. Acta Neuropathol 2010, 119:523-541.
72. Gravina S.A., Ho L., Eckman C.B., Long K.E., Otvos L., Younkin L.H., Suzuki N., Younkin S.G. Amyloid beta protein (A beta) in Alzheimer's disease brain. Biochemical and immunocytochemical analysis with antibodies specific for forms ending at A beta 40 or A beta 42(43). J. Biol. Chem 1995, 270:7013-7016.
73. Guo J.P., Arai T., Miklossy J., McGeer P.L. Abeta and tau form soluble complexes that may promote self aggregation of both into the insoluble forms observed in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A 2006, 103:1953-1958.
74. Hamilton R.L. Lewy bodies in Alzheimer's disease: a neuropathological review of 145 cases using alpha-synuclein immunohistochemistry. Brain Pathol 2000, 10:378-384.
75. 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.
76. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
77. Hauptmann S., Scherping I., Dröse S., Brandt U., Schulz K.L., Jendrach M., Leuner K., Eckert A., Müller W.E. Mitochondrial dysfunction: an early event in Alzheimer pathology accumulates with age in AD transgenic mice. Neurobiol. Aging 2009, 30:1574-1586.
78. Hoover B.R., Reed M.N., Su J., Penrod R.D., Kotilinek L.A., Grant M.K., Pitstick R., Carlson G.A., Lanier L.M., Yuan L.L., Ashe K.H., Liao D. Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron 2010, 68:1067-1081.
79. Hu X., Crick S.L., Bu G., Frieden C., Pappu R.V., Lee J.M. Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc. Natl. Acad. Sci. U. S. A 2009, 106:20324-20329.
80. Israelson A., Arbel N., Da Cruz S., Ilieva H., Yamanaka K., Shoshan-Barmatz V., Cleveland D.W. Misfolded mutant SOD1 directly inhibits VDAC1 conductance in a mouse model of inherited ALS. Neuron 2010, 67:575-587.
81. Ittner L.M., Ke Y.D., Delerue F., Bi M., Gladbach A., van Eersel J., Wölfing H., Chieng B.C., Christie M.J., Napier I.A., Eckert A., Staufenbiel M., Hardeman E., Götz J. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 2010, 142:387-397.
82. Iwatsubo T., Odaka A., Suzuki N., Mizusawa H., Nukina N., Ihara Y. Visualization of A beta 42(43) and Abeta 40 in senile plaques with end-specific A beta monoclonals: evidence that an initially deposited species is A beta 42(43). Neuron 1994, 13:45-53.
83. Iwatsubo T., Saido T.C., Mann D.M., Lee V.M., Trojanowski J.Q. Full-length amyloid-beta (1-42(43)) and amino-terminally modified and truncated amyloid-beta 42(43) deposit in diffuse plaques. Am. J. Pathol 1996, 149:1823-1830.
84. Jan A., Gokce O., Luthi-Carter R., Lashuel H.A. The ratio of monomeric to aggregated forms of Abeta40 and Abeta42 is an important determinant of amyloid-beta aggregation, fibrillogenesis, and toxicity. J. Biol. Chem 2008, 283:28176-28189.
85. Jarrett J.T., Berger E.P., Lansbury P.T. The carboxy terminus of the beta amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease. Biochemistry 1993, 32:4693-4697.
86. Jellinger K.A. Basic mechanisms of neurodegeneration: a critical update. J. Cell. Mol. Med 2010, 14:457-487.
87. Jellinger K.A., Attems J. Does striatal pathology distinguish Parkinson disease with dementia and dementia with Lewy bodies?. Acta Neuropathol 2006, 112:253-260.
88. Jensen P.H., Hager H., Nielsen M.S., Hojrup P., Gliemann J., Jakes R. Alpha-synuclein binds to Tau and stimulates the protein kinase A-catalyzed tau phosphorylation of serine residues 262 and 356. J. Biol. Chem 1999, 274:25481-25489.
89. Johnson G.V., Stoothoff W.H. Tau phosphorylation in neuronal cell function and dysfunction. J. Cell Sci 2004, 117:5721-5729.
90. Kalaitzakis M.E., Pearce R.K. The morbid anatomy of dementia in Parkinson's disease. Acta Neuropathol 2009, 118:587-598.
91. Kalaitzakis M.E., Pearce R.K., Gentleman S.M. Clinical correlates of pathology in the claustrum in Parkinson's disease and dementia with Lewy bodies. Neurosci. Lett 2009, 461:12-15.
92. Kamal A., Almenar-Queralt A., LeBlanc J.F., Roberts E.A., Goldstein L.S. Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 2001, 414:643-648.
93. King M.E., Kan H.M., Baas P.W., Erisir A., Glabe C.G., Bloom G.S. Tau-dependent microtubule disassembly initiated by prefibrillar beta-amyloid. J. Cell Biol 2006, 175:541-546.
94. Kinnally K.W., Peixoto P.M., Ryu S.Y., Dejean L.M. Is mPTP the gatekeeper for necrosis, apoptosis, or both?. Biochim. Biophys. Acta 2011, 1813:616-622.
95. Kuperstein I., Broersen K., Benilova I., Rozenski J., Jonckheere W., Debulpaep M., Vandersteen A., Segers-Nolten I., Van Der Werf K., Subramaniam V., Braeken D., Callewaert G., Bartic C., D'Hooge R., Martins I.C., Rousseau F., Schymkowitz J., De Strooper B. Neurotoxicity of Alzheimer's disease Aβ peptides is induced by small changes in the Aβ42 to Aβ40 ratio. EMBO J 2010, 29:3408-3420.
96. Lee J., Schriner S.E., Wallace D.C. Adenine nucleotide translocator 1 deficiency increases resistance of mouse brain and neurons to excitotoxic insults. Biochim. Biophys. Acta 2009, 1787:364-370.
97. Leung A.W., Varanyuwatana P., Halestrap A.P. The mitochondrial phosphate carrier interacts with cyclophilin D and may play a key role in the permeability transition. J. Biol. Chem 2008, 283:26312-26323.
98. Levi G., Aloisi F., Ciotti M.T., Gallo V. Autoradiographic localization and depolarization-induced release of acidic amino acids in differentiating cerebellar granule cell cultures. Brain Res 1984, 290:77-86.
99. Lewis J., Dickson D.W., Lin W.L., Chisholm L., Corral A., Jones G., Yen S.H., Sahara N., Skipper L., Yager D., Eckman C., Hardy J., Hutton M., McGowan E. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 2001, 293:1487-1491.
100. Liang N.J.T., Duda J.E. Does striatal pathology distinguish DLB from PDD?. Mov. Disord 2006, 21:S69-S70.
101. Lienhard G.E., Secemski I.I. 1,5-di (adenosine-5') pentaphosphate, a potent multisubstrate inhibitor of adenylate kinase. J. Biol. Chem 1973, 248:1121-1123.
102. Liu G., Zhang C., Yin J., Li X., Cheng F., Li Y., Yang H., Uéda K., Chan P., Yu S. alpha-Synuclein is differentially expressed in mitochondria from different rat brain regions and dose-dependently down-regulates complex I activity. Neurosci. Lett 2009, 454:187-192.
103. Lorenzo A., Yankner B.A. Beta-amyloid neurotoxicity requires fibril formation and is inhibited by congo red. Proc. Natl. Acad. Sci. U. S. A 1994, 91:12243-12247.
104. 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.
105. Maas T., Eidenmüller J., Brandt R. Interaction of tau with the neural membrane cortex is regulated by phosphorylation at sites that are modified in paired helical filaments. J. Biol. Chem 2000, 275:15733-15740.
106. Magnani E., Fan J., Gasparini L., Golding M., Williams M., Schiavo G., Goedert M., Amos L.A., Spillantini M.G. Interaction of tau protein with the dynactin complex. EMBO J 2007, 26:4546-4554.
107. 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.
108. 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. Neuromol. Med 2004, 5:147-162.
109. Martin L., Latypova X., Terro F. Post-translational modifications of tau protein: implications for Alzheimer's disease. Neurochem. Int 2011, 58:458-471.
110. Martinez M., Hernández A.I., Martínez N., Ferrándiz M.L. Age-related increase in oxidized proteins in mouse synaptic mitochondria. Brain Res 1996, 731:246-248.
111. Matsuo E.S., Shin R.W., Billingsley M.L., Van deVoorde A., O'Connor M., Trojanowski J.Q., Lee V.M. Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau. Neuron 1994, 13:989-1002.
112. Mattson M.P., Gleichmann M., Cheng A. Mitochondria in neuroplasticity and neurological disorders. Neuron 2008, 60:748-766.
113. Mc Stay G.P., Clarke S.J., Halestrap A.P. Role of critical thiol groups on the matrix surface of the adenine nucleotide translocase in the mechanism of the mitochondrial permeability transition pore. Biochem. J 2002, 367:541-548.
114. Melov S., Adlard P.A., Morten K., Johnson F., Golden T.R., Hinerfeld D., Schilling B., Mavros C., Masters C.L., Volitakis I., Li Q.X., Laughton K., Hubbard A., Cherny R.A., Gibson B., Bush A.I. Mitochondrial oxidative stress causes hyperphosphorylation of tau. PLoS One 2007, 2:e536.
115. Miller K.E., Sheetz M.P. Axonal mitochondrial transport and potential are correlated. J. Cell Sci 2004, 117:2791-2804.
116. Morais V.A., De Strooper B. Mitochondria dysfunction and neurodegenerative disorders: cause or consequence. J. Alzheimers Dis 2010, 20:S255-S263.
117. Morrison J.H., Hof P.R. Life and death of neurons in the aging brain. Science 1997, 278:412-419.
118. Mukrasch M.D., Bibow S., Korukottu J., Jeganathan S., Biernat J., Griesinger C., Mandelkow E., Zweckstetter M. Structural polymorphism of 441-residue tau at single residue resolution. PLoS Biol 2009, 7:e34.
119. Müller W.E., Kirsch C., Eckert G.P. Membrane-disordering effects of beta-amyloid peptides. Biochem. Soc. Trans 2001, 29:617-623.
120. Naga K.K., Sullivan P.G., Geddes J.W. High cyclophilin D content of synaptic mitochondria results in increased vulnerability to permeability transition. J. Neurosci 2007, 27:7469-7475.
121. Nagy Z., Esiri M.M., LeGris M., Matthews P.M. Mitochondrial enzyme expression in the hippocampus in relation to Alzheimer-type pathology. Acta Neuropathol 1999, 97:346-354.
122. Näslund J., Schierhorn A., Hellman U., Lannfelt L., Roses A.D., Tjernberg L.O., Silberring J., Gandy S.E., Winblad B., Greengard P., Nordstedt C., Terenius L. Relative abundance of Alzheimer A beta amyloid peptide variants in Alzheimer disease and normal aging. Proc. Natl. Acad. Sci. U. S. A 1994, 91:8378-8382.
123. Neupert W., Herrmann J.M. Translocation of proteins into mitochondria. Annu. Rev. Biochem 2007, 76:723-749.
124. O'Leary J.C., Koren J., Dickey C.A. Neuronal life span versus health span: principles of natural selection at work in the degenerating brain. J. Mol. Neurosci. 2011, in press.
125. Oddo S., Billings L., Kesslak J.P., Cribbs D.H., LaFerla F.M. Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 2004, 43:321-332.
126. Oddo S., Caccamo A., Cheng D., Jouleh B., Torp R., LaFerla F.M. Genetically augmenting tau levels does not modulate the onset or progression of Abeta pathology in transgenic mice. J. Neurochem 2007, 102:1053-1063.
127. Oddo S., Caccamo A., Kitazawa M., Tseng B.P., LaFerla F.M. Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol. Aging 2003, 24:1063-1070.
128. Ono K., Yamada M. Low-n oligomers as therapeutic targets of Alzheimer's disease. J. Neurochem 2011, 117:19-28.
129. Parihar M.S., Brewer G.J. Mitoenergetic failure in Alzheimer disease. Am. J. Physiol. Cell Physiol 2007, 292:C8-C23.
130. Passarella S., Atlante A., Valenti D., de Bari L. The role of mitochondrial transport in energy metabolism. Mitochondrion 2003, 2:319-343.
131. Perreault S., Bousquet O., Lauzon M., Paiement J., Leclerc N. Increased association between rough endoplasmic reticulum membranes and mitochondria in transgenic mice that express P301L tau. J. Neuropathol. Exp. Neurol 2009, 68:503-514.
132. Piccini A., Russo C., Gliozzi A., Relini A., Vitali A., Borghi R., Giliberto L., Armirotti A., D'Arrigo C., Bachi A., Cattaneo A., Canale C., Torrassa S., Saido T.C., Markesbery W., Gambetti P., Tabaton M. beta-amyloid is different in normal aging and in Alzheimer disease. J. Biol. Chem 2005, 280:34186-34192.
133. Pigino G., Morfini G., Atagi Y., Deshpande A., Yu C., Jungbauer L., SaDu M., Busciglio J., Brady S. Disruption of fast axonal transport is a pathogenic mechanism for intraneuronal amyloid beta. Proc. Natl. Acad. Sci. U. S. A 2009, 106:5907-5912.
134. Pike C.J., Burdick D., Walencewicz A.J., Glabe C.G., Cotman C.W. Neurodegeneration induced by beta-amyloid peptides in vitro: the role of peptide assembly state. J. Neurosci 1993, 13:1676-1687.
135. Pillot T., Goethals M., Vanloo B., Talussot C., Brasseur R., Vandekerckhove J., Rosseneu M., Lins L. Fusogenic properties of the C-terminal domain of the Alzheimer beta-amyloid peptide. J. Biol. Chem 1996, 271:28757-28765.
136. Quintanilla R.A., Dolan P.J., Jin Y.N., Johnson G.V. Truncated tau and Aβ cooperatively impair mitochondria in primary neurons. Neurobiol. Aging 2011, in press.
137. Quintanilla R.A., Matthews-Roberson T.A., Dolan P.J., Johnson G.V. Caspase-cleaved tau expression induces mitochondrial dysfunction in immortalized cortical neurons: implications for the pathogenesis of Alzheimer disease. J. Biol. Chem 2009, 284:18754-18766.
138. Raghavan R., Khin-Nu C., Brown A., Irving D., Ince P.G., Day K., Tyrer S.P., Perry R.H. Detection of Lewy bodies in Trisomy 21 (Down's syndrome). Can. J. Neurol. Sci 1993, 20:48-51.
139. Rapoport M., Dawson H.N., Binder L.I., Vitek M.P., Ferreira A. Tau is essential to beta -amyloid-induced neurotoxicity. Proc. Natl. Acad. Sci. U. S. A 2002, 99:6364-6369.
140. Reddy P.H. Amyloid beta, mitochondrial structural and functional dynamics in Alzheimer's disease. Exp. Neurol 2009, 218:286-292.
141. 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.
142. Reddy P.H., Manczak M., Mao P., Calkins M.J., Reddy A.P., Shirendeb U. Amyloid-beta and mitochondria in aging and Alzheimer's disease: implications for synaptic damage and cognitive decline. J. Alzheimers Dis 2010, 20:S499-S512.
143. Reifert J., Hartung-Cranston D., Feinstein S.C. Amyloid beta-mediated cell death of cultured hippocampal neurons reveals extensive Tau fragmentation without increased full-length tau phosphorylation. J. Biol. Chem 2011, 286:20797-20811.
144. Ren R., Zhang Y., Li B., Wu Y., Li B. Effect of β-amyloid (25-35) on mitochondrial function and expression of mitochondrial permeability transition pore proteins in rat hippocampal neurons. J. Cell. Biochem 2011, 112:1450-1457.
145. Rendon A., Jung D., Jancsik V. Interaction of microtubules and microtubule-associated proteins (MAPs) with rat brain mitochondria. Biochem. J 1990, 15:555-556.
146. Reynolds M.R., Berry R.W., Binder L.I. Site-specific nitration differentially influences tau assembly in vitro. Biochemistry 2005, 44:13997-14009.
147. Reynolds M.R., Lukas T.J., Berry R.W., Binder L.I. Peroxynitrite-mediated tau modifications stabilize preformed filaments and destabilize microtubules through distinct mechanisms. Biochemistry 2006, 45:4314-4326.
148. Reynolds M.R., Reyes J.F., Fu Y., Bigio E.H., Guillozet-Bongaarts A.L., Berry R.W., Binder L.I. Tau nitration occurs at tyrosine 29 in the fibrillar lesions of Alzheimer's disease and other tauopathies. J. Neurosci 2006, 26:10636-10645.
149. Rhein V., Song X., Wiesner A., Ittner L.M., Baysang G., Meier F., Ozmen L., Bluethmann H., Dröse S., Brandt U., Savaskan E., Czech C., Götz 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.
150. Ribé E.M., Pérez M., Puig B., Gich I., Lim F., Cuadrado M., Sesma T., Catena S., Sánchez B., Nieto M., Gómez-Ramos P., Morán M.A., Cabodevilla F., Samaranch L., Ortiz L., Pérez A., Ferrer I., Avila J., Gómez-Isla T. Accelerated amyloid deposition, neurofibrillary degeneration and neuronal loss in double mutant APP/tau transgenic mice. Neurobiol. Dis 2005, 20:814-822.
151. Roberson E.D., Scearce-Levie K., Palop J.J., Yan F., Cheng I.H., Wu T., Gerstein H., Yu G.Q., Mucke L. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 2007, 316:750-754.
152. Robin M.A., Anandatheerthavarada H.K., Biswas G., Sepuri N.B., Gordon D.M., Pain D., Avadhani N.G. Bimodal targeting of microsomal CYP2E1 to mitochondria through activation of an N-terminal chimeric signal by cAMP-mediated phosphorylation. J. Biol. Chem 2002, 277:40583-40593.
153. Rohn T.T., Rissman R.A., Davis M.C., Kim Y.E., Cotman C.W., Head E. Caspase-9 activation and caspase cleavage of tau in the Alzheimer's disease brain. Neurobiol. Dis 2002, 11:341-354.
154. 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.
155. Scheff S.W., Price D.A. Alzheimer's disease-related alterations in synaptic density: neocortex and hippocampus. J. Alzheimers Dis 2006, 9:101-115.
156. Scheff S.W., Price D.A., Schmitt F.A., Mufson E.J. Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment. Neurobiol. Aging 2006, 27:1372-1384.
157. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
158. Shipton O.A., Leitz J.R., Dworzak J., Acton C.E., Tunbridge E.M., Denk F., Dawson H.N., Vitek M.P., Wade-Martins R., Paulsen O., Vargas-Caballero M. Tau protein is required for amyloid {beta}-induced Impairment of hippocampal long-term potentiation. J. Neurosci 2011, 31:1688-1692.
159. Singh P., Suman S., Chandna S., Das T.K. Possible role of amyloid-beta, adenine nucleotide translocase and cyclophilin-D interaction in mitochondrial dysfunction of Alzheimer's disease. Bioinformation 2009, 3:440-445.
160. Sorbi S., Bird E.D., Blass J.P. Decreased pyruvate dehydrogenase complex activity in Huntington and Alzheimer brain. Ann. Neurol 1983, 13:72-78.
161. Spillantini M.G., Goedert M. Tau protein pathology in neurodegenerative diseases. Trends Neurosci 1998, 21:428-433.
162. Sultan A., Nesslany F., Violet M., Bégard S., Loyens A., Talahari S., Mansuroglu Z., Marzin D., Sergeant N., Humez S., Colin M., Bonnefoy E., Buée L., Galas M.C. Nuclear tau, a key player in neuronal DNA protection. J. Biol. Chem 2011, 286:4566-4575.
163. Takahashi R.H., Capetillo-Zarate E., Lin M.T., Milner T.A., Gouras G.K. Co-occurrence of Alzheimer's disease beta-amyloid and tau pathologies at synapses. Neurobiol. Aging 2010, 31:1145-1152.
164. Takuma K., Yao J., Huang J., Xu H., Chen X., Luddy J., Trillat A.C., Stern D.M., Arancio O., Yan S.S. ABAD enhances Abeta-induced cell stress via mitochondrial dysfunction. FASEB J 2005, 19:597-598.
165. Terry R.D. Cell death or synaptic loss in Alzheimer disease. J. Neuropathol. Exp. Neurol 2000, 59:1118-1119.
166. Thies E., Mandelkow E.M. Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1. J. Neurosci 2007, 27:2896-2907.
167. Trojanowski J.Q. Emerging Alzheimer's disease therapies: focusing on the future. Neurobiol. Aging 2002, 23:985-990.
168. Tsigelny I.F., Crews L., Desplats P., Shaked G.M., Sharikov Y., Mizuno H., Spencer B., Rockenstein E., Trejo M., Platoshyn O., Yuan J.X., Masliah E. Mechanisms of hybrid oligomer formation in the pathogenesis of combined Alzheimer's and Parkinson's diseases. PLoS One 2008, 3:e3135.
169. Verstreken P., Ly C.V., Venken K.J., Koh T.W., Zhou Y., Bellen H.J. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 2005, 47:365-378.
170. Vossel K.A., Zhang K., Brodbeck J., Daub A.C., Sharma P., Finkbeiner S., Cui B., Mucke L. Tau reduction prevents Abeta-induced defects in axonal transport. Science 2010, 330:198.
171. Waddell W.J., Hill C. A simple ultraviolet spectrophotometric method for the determination of protein. J. Lab. Clin. Med 1956, 48:311-314.
172. Wanders R.J., Groen A.K., Van Roermund C.W., Tager J.M. Factors determining the relative contribution of the adenine-nucleotide translocator and the ADP-regenerating system to the control of oxidative phosphorylation in isolated rat-liver mitochondria. Eur. J. Biochem 1984, 142:417-424.
173. 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.
174. 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.
175. 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.
176. Wemmie J.A., Chen J., Askwith C.C., Hruska-Hageman A.M., Price M.P., Nolan B.C., Yoder P.G., Lamani E., Hoshi T., Freeman J.H., Welsh M.J. The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron 2002, 34:463-477.
177. Yankner B.A., Lu T. Amyloid beta-protein toxicity and the pathogenesis of Alzheimer disease. J. Biol. Chem 2009, 284:4755-4759.
178. Yao J., Du H., Yan S., Fang F., Wang C., Lue L.F., Guo L., Chen D., Stern D.M., Gunn Moore F.J., Xi Chen J., Arancio O., Yan S.S. Inhibition of amyloid-beta (Abeta) peptide-binding alcohol dehydrogenase-Abeta interaction reduces Abeta accumulation and improves mitochondrial function in a mouse model of Alzheimer's disease. J. Neurosci 2011, 31:2313-2320.
179. 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.
180. Younkin S.G. Evidence that A beta 42 is the real culprit in Alzheimer's disease. Ann. Neurol 1995, 37:287-288.
181. Zempel H., Thies E., Mandelkow E., Mandelkow E.M. Abeta oligomers cause localized Ca(2+) elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation, and destruction of microtubules and spines. J. Neurosci 2010, 30:11938-11950.
182. Zhivotovsky B., Samali A., Gahm A., Orrenius S. Caspases: their intracellular localization and translocation during apoptosis. Cell Death Differ 1999, 6:644-651.
183. Zinchuk V., Grossenbacher-Zinchuk O. Recent advances in quantitative colocalization analysis: focus on neuroscience. Prog Histochem Cytochem 2009, 44:125-172.