Dissecting the molecular mechanism by which NH2htau and Aβ1-42 peptides impair mitochondrial ANT-1 in Alzheimer disease

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1827, Issue 7, 2013, Pages 848-860

  Bobba, A ^a   Amadoro, G ^b   Petragallo, V A ^a   Calissano, P ^c   Atlante, A ^a  

^a CNR   (Italy)

^b INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

^c EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

Author keywords

amyloid; Adenine nucleotide translocator; Mitochondria; Tau fragment; Thiol group

Indexed keywords

4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; ADENINE NUCLEOTIDE TRANSLOCASE; ADENINE NUCLEOTIDE TRANSLOCASE 1; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; AMYLOID BETA PROTEIN[1-42]; GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; HEXOKINASE; MERSALYL; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUPEROXIDE; TAU PROTEIN; THIOL GROUP; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ENERGY METABOLISM; HISTOPATHOLOGY; HYDROPHILICITY; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; RAT;

ADENINE NUCLEOTIDE TRANSLOCATOR 1; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CELLS, CULTURED; CEREBELLUM; CYTOPLASMIC GRANULES; ENERGY METABOLISM; ENZYME INHIBITORS; MERSALYL; MITOCHONDRIA; MODELS, NEUROLOGICAL; OXYGEN CONSUMPTION; PEPTIDE FRAGMENTS; POLAROGRAPHY; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; SUPEROXIDES; TAU PROTEINS;

EID: 84877860035     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2013.04.001     Document Type: Article

References (96)

1. D.J. Selkoe Alzheimer's disease is a synaptic failure Science 298 2002 789 791
2. G.E. Gibson, and H.M. Huang Oxidative processes in the brain and non-neuronal tissues as biomarkers of Alzheimer's disease Front. Biosci. 7 2002 d1007 d1015
3. P.I. Moreira, M.S. Santos, and C.R. Oliveira Alzheimer's disease: a lesson from mitochondrial dysfunction Antioxid. Redox Signal. 9 2007 1621 1630
4. P.I. Moreira, M.S. Santos, C.R. Oliveira, J.C. Shenk, A. Nunomura, M.A. Smith, X. Zhu, and G. Perry Alzheimer disease and the role of free radicals in the pathogenesis of the disease Curr. Drug Targets CNS Neurol. Disord. 7 2008 3 10
5. A. Eckert, S. Hauptmann, I. Scherping, V. Rhein, F. Muller-Spahn, J. Götz, and W.E. Muller Soluble beta-amyloid leads to mitochondrial defects in amyloid precursor protein and tau transgenic mice Neurodegener. Dis. 5 2008 157 159
6. B. Su, X. Wang, A. Nunomura, P.I. Moreira, H.G. Lee, G. Perry, M.A. Smith, and X. Zhu Oxidative stress signaling in Alzheimer's disease Curr. Alzheimer Res. 5 2008 525 532
7. S. Hauptmann, I. Scherping, S. Drose, U. Brandt, K.L. Schulz, M. Jendrach, K. Leuner, A. Eckert, and W.E. Muller Mitochondrial dysfunction: an early event in Alzheimer pathology accumulates with age in AD transgenic mice Neurobiol. Aging 30 2009 1574 1586
8. V. Rhein, X. Song, A. Wiesner, L.M. Ittner, G. Baysang, F. Meier, L. Ozmen, H. Bluethmann, S. Dröse, U. Brandt, E. Savaskan, F. Muller-Spahn, C. Czech, J. Götz, and A. Eckert Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice Proc. Natl. Acad. Sci. U. S. A. 106 2009 20057 20062
9. S. Sorbi, E.D. Bird, and J.P. Blass Decreased pyruvate dehydrogenase complex activity in Huntington and Alzheimer brain Ann. Neurol. 1983 13 1983 72 78
10. J.P. Blass Cerebrometabolic abnormalities in Alzheimer's disease Neurol. Res. 25 2003 556 566
11. S.M. Cardoso, M.T. Proenca, S. Santos, I. Santana, and C.R. Oliveira Cytochrome c oxidase is decreased in Alzheimer's disease platelets Neurobiol. Aging 25 2004 105 110
12. J.L. Chou, D.V. Shenoy, N. Thomas, P.K. Choudhary, F.M. Laferla, S.R. Goodman, and G.A. Breen Early dysregulation of the mitochondrial proteome in a mouse model of Alzheimer's disease J. Proteomics 74 2011 466 479
13. P.H. Reddy, and M.F. Beal Amyloid beta, mitochondrial dysfunction and synaptic damage: implications for cognitive decline in aging and Alzheimer's disease Trends Mol. Med. 14 2008 45 53
14. S.W. Scheff, and D.A. Price Alzheimer's disease-related alterations in synaptic density: neocortex and hippocampus J. Alzheimers Dis. 9 2006 101 115
15. J. Yao, R.W. Irwin, L. Zhao, J. Nilsen, R.T. Hamilton, and R.D. Brinton Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease Proc. Natl. Acad. Sci. U. S. A. 106 2009 14670 14675
16. G. Amadoro, M.T. Ciotti, M. Costanzi, V. Cestari, P. Calissano, and N. Canu NMDA receptor mediates tau-induced neurotoxicity by calpain and ERK/MAPK activation Proc. Natl. Acad. Sci. U. S. A. 103 2006 2892 2897
17. A. Atlante, G. Amadoro, A. Bobba, L. de Bari, V. Corsetti, G. Pappalardo, E. Marra, P. Calissano, and S. Passarella 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 1777 2008 1289 1300
18. G. Amadoro, V. Corsetti, A. Atlante, F. Florenzano, S. Capsoni, R. Bussani, D. Mercanti, and P. Calissano Interaction between NH(2)-tau fragment and Aβ in Alzheimer's disease mitochondria contributes to the synaptic deterioration Neurobiol. Aging 33 833 2012 (e1-833.e25)
19. A. Fonyó SH-group reagents as tools in the study of mitochondrial anion transport J. Bioenerg. Biomembr. 10 1978 171 194
20. G. Levi, F. Aloisi, M.T. Ciotti, and V. Gallo Autoradiographic localization and depolarization-induced release of acidic amino acids in differentiating cerebellar granule cell cultures Brain Res. 290 1984 77 86
21. A. Atlante, A. Bobba, L. de Bari, F. Fontana, P. Calissano, E. Marra, and S. Passarella 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. 97 2006 1166 1181
22. W.J. Waddell, and C. Hill A simple ultraviolet spectrophotometric method for the determination of protein J. Lab. Clin. Med. 48 1956 311 314
23. A. Atlante, and S. Passarella Detection of reactive oxygen species in primary cultures of cerebellar granule cells Brain Res. Brain Res. Protocol. 4 1999 266 270
24. H.J. Foman, and I. Fridovich Superoxide dismutase: a comparison of rate constants Arch. Biochem. Biophys. 158 1973 396 400
25. K.M. Robinson, M.S. Janes, M. Pehar, J.S. Monette, M.F. Ross, T.M. Hagen, M.P. Murphy, and J.S. Beckman Selective fluorescent imaging of superoxide in vivo using ethidium-based probes Proc. Natl. Acad. Sci. U. S. A. 103 2006 15038 15043
26. W. Yang, and S. Hekimi A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans PLoS Biol. 8 2010 e1000556 10.1371/journal.pbio.1000556
27. C. Batandier, B. Guigas, D. Detaille, M.Y. El-Mir, E. Fontaine, M. Rigoulet, and X.M. Leverve The ROS production induced by a reverse-electron flux at respiratory-chain complex 1 is hampered by metformin J. Bioenerg. Biomembr. 38 2006 33 42
28. V.G. Grivennikova, and A.D. Vinogradov Generation of superoxide by the mitochondrial Complex I Biochim. Biophys. Acta 1757 2006 553 561
29. V. Adam-Vizi, and C. Chinopoulos Bioenergetics and the formation of mitochondrial reactive oxygen species Trends Pharmacol. Sci. 27 2006 639 645
30. + channels Am. J. Physiol. Heart Circ. Physiol. 293 2007 H1400 H1407
31. E. Majima, K. Ikawa, M. Takeda, M. Hashimoto, Y. Shinohara, and H. Terada Translocation of loops regulates transport activity of mitochondrial ADP/ATP carrier deduced from formation of a specific intermolecular disulfide bridge catalyzed by copper-o-phenanthroline J. Biol. Chem. 270 1995 29548 29554
32. A.E. Vercesi, A.J. Kowaltowski, M.T. Grijalba, A.R. Meinicke, and R.F. Castilho The role of reactive oxygen species in mitochondrial permeability transition Biosci. Rep. 17 1997 43 52
33. A.P. Halestrap, K.Y. Woodfield, and C.P. Connern Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase J. Biol. Chem. 272 1997 3346 3354
34. L.I. Leichert, F. Gehrke, H.V. Gudiseva, T. Blackwell, M. Ilbert, A.K. Walker, J.R. Strahler, P.C. Andrews, and U. Jakob Quantifying changes in the thiol redox proteome upon oxidative stress in vivo Proc. Natl. Acad. Sci. U. S. A. 105 2008 8197 8202
35. R.J.A. Wanders, A.K. Groen, C.W.T. Van Roermund, and J.M. Ager Factors determining the relative contribution of the adeninenucleotide translocator and the ADP-regenerating system to the control of oxidative phosphorylation in isolated rat-liver mitochondria Eur. J. Biochem. 142 1984 417 424
36. S. Passarella, A. Atlante, D. Valenti, and L. de Bari The role of mitochondrial transport in energy metabolism Mitochondrion 2 2003 319 343
37. A. Atlante, S. Passarella, E. Quagliariello, G. Moreno, and C. Salet Carrier thiols are targets of Photofrin II photosensitization of isolated rat liver mitochondria J. Photochem. Photobiol. B 7 1990 21 32
38. A. Atlante, A. Bobba, P. Calissano, S. Passarella, and E. Marra The apoptosis/necrosis transition in cerebellar granule cells depends on the mutual relationship of the antioxidant and the proteolytic systems which regulate ROS production and cytochrome c release en route to death J. Neurochem. 84 2003 960 971
39. A. Atlante, L. de Bari, A. Bobba, E. Marra, P. Calissano, and S. Passerella Cytochrome c, released from cerebellar granule cells undergoing apoptosis or excitotoxic death, can generate protonmotive force and drive ATP synthesis in isolated mitochondria J. Neurochem. 86 2003 591 604
40. P. Bénit, S. Goncalves, E. Philippe Dassa, J.J. Brière, G. Martin, and P. Rustin Three spectrophotometric assays for the measurement of the five respiratory chain complexes in minuscule biological samples Clin. Chim. Acta 374 2006 81 86
41. H. Atamna, and W.H. Frey II Mechanisms of mitochondrial dysfunction and energy deficiency in Alzheimer's disease Mitochondrion 7 2007 297 310
42. X. Wang, B. Su, H. Fujioka, and X. Zhu Dynamin-like protein 1 reduction underlies mitochondrial morphology and distribution abnormalities in fibroblasts from sporadic Alzheimer's disease patients Am. J. Pathol. 173 2008 470 482
43. M.J. Calkins, M. Manczak, P. Mao, U. Shirendeb, and P.H. Reddy 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. 20 2011 4515 4529
44. E. Cadenas, and K.J. Davies Mitochondrial free radical generation, oxidative stress, and aging Free Radic. Biol. Med. 29 2000 222 230
45. A. Atlante, P. Calissano, A. Bobba, A. Azzariti, E. Marra, and S. Passarella Cytochrome c is released from mitochondria in a reactive oxygen species (ROS)-dependent fashion and can operate as a ROS scavenger and as a respiratory substrate in cerebellar neurons undergoing excitotoxic death J. Biol. Chem. 275 2000 37159 37166
46. 2 formation by rat heart mitochondria on substrate availability and donor age J. Bioenerg. Biomembr. 29 1997 89 95
47. S.S. Korshunov, V.P. Skulachev, and A.A. Starkov High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria FEBS Lett. 416 1997 15 18
48. Q. Chen, E.J. Vazquez, S. Moghaddas, C.L. Hoppel, and E.J. Lesnefsky Production of reactive oxygen species by mitochondria: central role of complex III J. Biol. Chem. 278 2003 36027 36031
49. A. Atlante, L. de Bari, A. Bobba, E. Marra, and S. Passarella Transport and metabolism of l-lactate occur in mitochondria from cerebellar granule cells and are modified in cells undergoing low potassium dependent apoptosis Biochim. Biophys. Acta 1767 2007 1285 1299
50. A. Atlante, S. Gagliardi, E. Marra, P. Calissano, and S. Passarella Glutamate neurotoxicity in rat cerebellar granule cells involves cytochrome c release from mitochondria and mitochondrial shuttle impairment J. Neurochem. 73 1999 237 246
51. A. Eckert, K. Schmitt, and J. Götz Mitochondrial dysfunction - the beginning of the end in Alzheimer's disease? Separate and synergistic modes of tau and amyloid-β toxicity Alzheimers Res. Ther. 3 2011 15
52. P. Calissano, C. Matrone, and G. Amadoro Apoptosis and in vitro Alzheimer disease neuronal models Commun. Integr. Biol. 2 2009 163 169
53. D. Sepulveda-Falla, J. Matschke, C. Bernreuther, C. Hagel, B. Puig, A. Villegas, G. Garcia, J. Zea, B. Gomez-Mancilla, I. Ferrer, F. Lopera, and M. Glatzel Deposition of hyperphosphorylated tau in cerebellum of PS1 E280A Alzheimer's disease Brain Pathol. 21 2011 452 463
54. J. Kuan, and M.H. Saier Jr. The mitochondrial carrier family of transport proteins: structural, functional, and evolutionary relationships Crit. Rev. Biochem. Mol. Biol. 28 1993 209 233
55. 2 +: correlation with mitochondrial permeability transition Biochim. Biophys. Acta 1318 1997 395 402
56. G. McStay, S.J. Clarke, and A.P. Halestrap 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. 367 2002 541 548
57. + transport by free fatty acids, which is further stimulated by mersalyl J. Biol. Chem. 269 1994 27329 27336
58. E. Majima, H. Koike, Y.M. Hong, Y. Shinohara, and H. Terada Characterization of cysteine residues of mitochondrial ADP/ATP carrier with the SH-reagents eosin 5-maleimide and N-ethylmaleimide J. Biol. Chem. 268 1993 22181 22187
59. M. Klingenberg The ADP and ATP transport in mitochondria and its carrier Biochem. Biophys. Acta 1778 2008 1978 2021
60. J.R. Aprille, and G.K. Asimakis Postnatal development of rat liver mitochondria: state 3 respiration, adenine nucleotide translocase activity, and the net accumulation of adenine nucleotides Arch. Biochem. Biophys. 201 1980 564 575
61. J. Austin, and J.R. Aprille Carboxyatractyloside-insensitive influx and efflux of adenine nucleotides in rat liver mitochondria J. Biol. Chem. 259 1984 154 160
62. J.K. Pollak, and R. Sutton The differentiation of animal mitochondria during development Trends Biochem. Sci. 5 1980 23 27
63. C. Fiore, V. Trezeguet, A. Le Saux, P. Roux, C. Schwimmer, A.C. Dianoux, F. Noel, G.J. Lauquin, G. Brandolin, and P.V. Vignais The mitochondrial ADP/ATP carrier: structural, physiological and pathological aspects Biochimie 80 1998 137 150
64. M. Le Bras, M.V. Clément, S. Pervaiz, and C. Brenner Reactive oxygen species and the mitochondrial signaling pathway of cell death Histol. Histopathol. 20 2005 205 219
65. G. Moreno, K. Poussin, F. Ricchelli, and C. Salet The effects of singlet oxygen produced by photodynamic action on the mitochondrial permeability transition differ in accordance with the localization of the sensitizer Arch. Biochem. Biophys. 386 2001 243 250
66. A. Atlante, S. Passarella, E. Quagliariello, G. Moreno, and C. Salet Haematoporphyrin derivative (Photofrin II) photosensitization of isolated mitochondria: inhibition of ADP/ATP translocator J. Photochem. Photobiol. B 4 1989 35 46
67. D.A. Butterfield Amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. A review Free Radic. Res. 36 2002 1307 1313
68. R. Naylor, A.F. Hill, and K.J. Barnham Neurotoxicity in Alzheimer's disease: is covalently crosslinked A-beta responsible? Eur. Biophys. J. 37 2008 265 268
69. K.J. Barnham, G.D. Ciccotosto, A.K. Tickler, F.E. Ali, D.G. Smith, N.A. Williamson, Y.H. Lam, D. Carrington, D. Tew, G. Kocak, I. Volitakis, F. Separovic, C.J. Barrow, J.D. Wade, C.L. Masters, R.A. Cherny, C.C. Curtain, A.I. Bush, and R. Cappai Neurotoxic, redox-competent Alzheimer's beta-amyloid is released from lipid membrane by methionine oxidation J. Biol. Chem. 278 2003 42959 42965
70. M.S. Lustgarten, A. Bhattacharya, F.L. Muller, Y.C. Jang, T. Shimizu, T. Shirasawa, A. Richardson, and H. Van Remmen Complex I generated, mitochondrial matrix-directed superoxide is released from the mitochondria through voltage dependent anion channels Biochem. Biophys. Res. Commun. 422 2012 515 521
71. R.S. Balaban, S. Nemoto, and T. Finkel Mitochondria, oxidants, and aging Cell 120 2005 483 495
72. J. Park, J. Lee, and C. Choi Mitochondrial network determines intracellular ROS dynamics and sensitivity to oxidative stress through switching inter-mitochondrial messengers PLoS One 6 2011 3211
73. T.V. Votyakova, and I.J. Reynolds ΔΨ-Dependent and -independent production of reactive oxygen species by rat brain mitochondria J. Neurochem. 79 2001 266 277
74. T.R. Hurd, T.A. Prime, M.E. Harbour, K.S. Lilley, and M.P. Murphy Detection of reactive oxygen species-sensitive thiol proteins by redox difference gel electrophoresis: implications for mitochondrial redox signaling J. Biol. Chem. 282 2007 22040 22051
75. T.S. Chang, C.S. Cho, S. Park, S. Yu, S.W. Kang, and S.G. Rhee Peroxiredoxin III, a mitochondrion-specific peroxidase, regulates apoptotic signaling by mitochondria J. Biol. Chem. 279 2004 41975 41984
76. +-dependent isocitrate dehydrogenase activity by glutathionylation J. Biol. Chem. 280 2005 10846 10854
77. C.C. Dahm, K. Moore, and M.P. Murphy Persistent S-nitrosation of complex I and other mitochondrial membrane proteins by S-nitrosothiols but not nitric oxide or peroxynitrite: implications for the interaction of nitric oxide with mitochondria J. Biol. Chem. 281 2006 10056 10065
78. E.R. Taylor, F. Hurrell, R.J. Shannon, T.K. Lin, J. Hirst, and M.P. Murphy Reversible glutathionylation of complex I increases mitochondrial superoxide formation J. Biol. Chem. 278 2003 19603 19610
79. M. Klingenberg Molecular aspects of the adenine nucleotide carrier from mitochondria Arch. Biochem. Biophys. 270 1989 1 14
80. E. Majima, Y. Shinohara, N. Yamaguchi, Y. Hong, and H. Terada Importance of loops of mitochondrial ADP/ATP carrier for its transport activity deduced from reactivities of its cysteine residues with the sulfhydryl reagent eosin-5-maleimide Biochemistry 33 1994 9530 9536
81. P.V. Vignais, and P.M. Vignais Effect of SH reagents on atractyloside binding to mitochondria and ADP translocation. Potentiation by ADP and its prevention by uncoupler FCCP FEBS Lett. 26 1972 27 31
82. M.A. Smith, J.A. Joseph, and G. Perry Arson: tracking the culprit in Alzheimer's disease Ann. N. Y. Acad. Sci. 924 2000 35 38
83. M.A. Smith, C.S. Atwood, J.A. Joseph, and G. Perry Predicting the failure of the amyloid-beta vaccine Lancet 359 2002 1864 1865
84. J. Joseph, B. Shukitt-Hale, N.A. Denisova, A. Martin, G. Perry, and M.A. Smith Copernicus revisited: amyloid beta in Alzheimer's disease Neurobiol. Aging 22 2001 131 146
85. C.A. Rottkamp, C.S. Atwood, J.A. Joseph, A. Nunomura, G. Perry, and M.A. Smith The state versus amyloid-β: the trial of the most wanted criminal in Alzheimer disease Peptides 23 2002 1333 1341
86. C. Hureau, and P. Faller Abeta-mediated ROS production by Cu ions: structural insights, mechanisms and relevance to Alzheimer's disease Biochimie 91 2009 1212 1217
87. K. Leuner, T. Schütt, C. Kurz, S.H. Eckert, C. Schiller, A. Occhipinti, S. Mai, M. Jendrach, G.P. Eckert, S.E. Kruse, R.D. Palmiter, U. Brandt, S. Dröse, I. Wittig, M. Willem, C. Haass, A.S. Reichert, and W.E. Müller Mitochondrion-derived reactive oxygen species lead to enhanced amyloid beta formation Antioxid. Redox Signal. 16 2012 1421 1433
88. J.A. Fein, S. Sokolow, C.A. Miller, H.V. Vinters, F. Yang, G.M. Cole, and K.H. Gylys Co-localization of amyloid beta and tau pathology in Alzheimer's disease synaptosomes Am. J. Pathol. 172 2008 1683 1692
89. J. Busciglio, A. Lorenzo, J. Yeh, and B.A. Yankner βeta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding Neuron 14 1995 879 888
90. W.H. Zheng, S. Bastianetto, F. Mennicken, W. Ma, and S. Kar Amyloid beta peptide induces tau phosphorylation and loss of cholinergic neurons in rat primary septal cultures J. Neurosci. 115 2002 201 211
91. K.B. Rank, A.M. Pauley, K. Bhattacharya, Z. Wang, D.B. Evans, T. Fleck, J.A. Johnston, and S.K. Sharma Direct interaction of soluble human recombinant Abeta 1-42 results in tau aggregation and hyperphosphorylation by tau protein kinase II FEBS Lett. 514 2002 263 268
92. J.P. Guo, T. Arai, J. Miklossy, and P.L. McGeer 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. 103 2006 1953 1958
93. M. Rapoport, H.N. Dawson, L.I. Binder, M.P. Vitek, and A. Ferreira Tau is essential for beta-amyloid-induced neurotoxicity Proc. Natl. Acad. Sci. U. S. A. 99 2002 6364 6369
94. E.D. Roberson, K. Scearce-Levie, J.J. Palop, F. Yan, I.H. Cheng, T. Wu, H. Gerstein, G.Q. Yu, and L. Mucke Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model Science 316 2007 750 754
95. H.N. Dawson, A. Ferreira, M.V. Eyster, N. Ghoshal, L.I. Binder, and M.P. Vitek Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice J. Cell Sci. 114 2001 1179 1187
96. A. Gómez-Ramos, M. Díaz-Hernández, R. Cuadros, F. Hernández, and J. Avila Extracellular tau is toxic to neuronal cells FEBS Lett. 580 2006 4842 4850