Is the mitochondrial outermembrane protein VDAC1 therapeutic target for Alzheimer's disease?

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 1, 2013, Pages 67-75

  Reddy, P Hemachandra ^a,b  

^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; Mitochondrial dysfunction; Phoshorylated tau; Voltage dependent anion channel

Indexed keywords

AMYLOID BETA PROTEIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; TAU PROTEIN; VOLTAGE DEPENDENT ANION CHANNEL 1; VOLTAGE DEPENDENT ANION CHANNEL 2; VOLTAGE DEPENDENT ANION CHANNEL 3;

ALZHEIMER DISEASE; APOPTOSIS; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL SURVIVAL; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FERTILITY; HUMAN; MITOCHONDRIAL PERMEABILITY; NERVE CELL PLASTICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; HUMANS; MICE; MITOCHONDRIA; VOLTAGE-DEPENDENT ANION CHANNEL 1;

MUS MUSCULUS;

EID: 84868515517     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.09.003     Document Type: Review

References (99)

1. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 2001, 81:741-766.
2. Mattson M.P. Pathways towards and away from Alzheimer's disease. Nature 2004, 430:631-639.
3. 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.
4. Alzheimer Association Alzheimer's disease: facts and figures 2012.
5. Mao P., Reddy P.H. Aging and amyloid beta-induced oxidative DNA damage and mitochondrial dysfunction in Alzheimer's disease: implications for early intervention and therapeutics. Biochim. Biophys. Acta 2011, 1812:1359-1370.
6. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
7. Nunomura A., Perry G., Aliev G., Hirai K., Takeda A., Balraj E.K., Jones P.K., Ghanbari H., Wataya T., Shimohama S., Chiba S., Atwood C.S., Petersen R.B., Smith M.A. Oxidative damage is the earliest event in Alzheimer disease. J. Neuropathol. Exp. Neurol. 2001, 759-767.
8. 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.
9. Reddy P.H., Tripathi R., Troung Q., Tirumala K., Reddy T.P., Anekonda V., Shirendeb U.P., Calkins M.J., Reddy A.P., Mao P., Manczak M. Abnormal mitochondrial dynamics and synaptic degeneration as early events in Alzheimer's disease: implications to mitochondria-targeted antioxidant therapeutics. Biochim. Biophys. Acta 2012, 1822:639-649.
10. 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.
11. Swerdlow R.H. Brain aging, Alzheimer's disease, and mitochondria. Biochim. Biophys. Acta 2011, 1812:1630-1639.
12. Zhu X., Perry G., Smith M.A., Wang X. Abnormal mitochondrial dynamics in the pathogenesis of Alzheimer's disease. J. Alzheimers Dis. 2012 Apr 24, [Epub ahead of print].
13. Reddy P.H. Amyloid beta, mitochondrial structural and functional dynamics in Alzheimer's disease. Exp. Neurol. 2009, 218:286-292.
14. M. Manczak, P.H. Reddy, Abnormal interaction of VDAC1 with amyloid beta and phosphorylated tau in Alzheimer's disease neurons cause mitochondrial dysfunction, Hum. Mol. Genet. (in press).
15. 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.
16. Reddy P.H. Mitochondrial dysfunction in aging and Alzheimer's disease: strategies to protect neurons. Antioxid. Redox Signal. 2007, 9:1647-1658.
17. 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.
18. Shoshan-Barmatz V., Israelson A., Brdiczka D., Sheu S.S. The voltage-dependent anion channel (VDAC): function in intracellular signalling, cell life and cell death. Curr. Pharm. Des. 2006, 12:2249-2270.
19. Shoshan-Barmatz V., De Pinto V., Zweckstetter M., Raviv Z., Keinan N., Arbel N. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol. Aspects Med. 2010, 31:227-285.
20. Shoshan-Barmatz V., Golan M. Mitochondrial VDAC1: function in cell life and death and a target for cancer therapy. Curr. Med. Chem. 2012, 19:714-735.
21. Shoshan-Barmatz V., Ben-Hail D. VDAC, a multi-functional mitochondrial protein as a pharmacological target. Mitochondrion 2012, 12:24-34.
22. Schein S.J., Colombini M., Finkelstein A. Reconstitution in planar lipid bilayers of a voltage-dependent anion-selective channel obtained from paramecium mitochondria. J. Membr. Biol. 1976, 30:99-120.
23. Blachly-Dyson E., Zambronicz E.B., Yu W.H., Adams V., McCabe E.R., Adelman J., Colombini M., Forte M. Cloning and functional expression in yeast of two human isoforms of the outer mitochondrial membrane channel, the voltage-dependent anion channel. J. Biol. Chem. 1993, 268:1835-1841.
24. Blachly-Dyson E., Baldini A., Litt M., McCabe E.R., Forte M. Human genes encoding the voltage-dependent anion channel (VDAC) of the outer mitochondrial membrane: mapping and identification of two new isoforms. Genomics 1994, 20:62-67.
25. Hodge T., Colombini M. Regulation of metabolite flux through voltage-gating of VDAC channels. J. Membr. Biol. 1997, 157:271-279.
26. Rostovtseva T., Colombini M. VDAC channels mediate and gate the flow of ATP: implications for the regulation of mitochondrial function. Biophys. J. 1997, 72:1954-1962.
27. Blachly-Dyson E., Forte M. VDAC channels. IUBMB Life 2001, 52:113-118.
28. Colombini M. VDAC structure, selectivity, and dynamics. Biochim. Biophys. Acta 2012, 1818:1457-1465.
29. Sampson M.J., Lovell R.S., Davison D.B., Craigen W.J. A novel mouse mitochondrial voltage-dependent anion channel gene localizes to chromosome 8. Genomics 1996, 36:192-196.
30. Sampson M.J., Lovell R.S., Craigen W.J. Isolation, characterization, and mapping of two mouse mitochondrial voltage-dependent anion channel isoforms. Genomics 1996, 33:283-288.
31. Messina A., Reina S., Guarino F., De Pinto V. VDAC isoforms in mammals. Biochim. Biophys. Acta 2012, 1818:1466-1476.
32. Young M.J., Bay D.C., Hausner G., Court D.A. The evolutionary history of mitochondrial porins. BMC Evol. Biol. 2007, 7:31.
33. Saccone C., Caggese C., D'Erchia A.M., Lanave C., Oliva M., Pesole G. Molecular clock and gene function. J. Mol. Evol. 2003, 57:S277-S285.
34. Craigen W.J., Graham B.H. Genetic strategies for dissecting mammalian and Drosophila voltage-dependent anion channel functions. J. Bioenerg. Biomembr. 2008, 40:207-212.
35. Yamamoto T., Yamada A., Watanabe M., Yoshimura Y., Yamazaki N., Yoshimura Y., Yamauchi T., Kataoka M., Nagata T., Terada H., Shinohara Y. VDAC1, having a shorter N-terminus than VDAC2 but showing the same migration in an SDS-polyacrylamide gel, is the predominant form expressed in mitochondria of various tissues. J. Proteome Res. 2006, 5:3336-3344.
36. Sampson M.J., Ross L., Decker W.K., Craigen W.J. A novel isoform of the mitochondrial outer membrane protein VDAC3 via alternative splicing of a 3-base exon. Functional characteristics and subcellular localization. J. Biol. Chem. 1998, 273:30482-30486.
37. Krauskopf A., Eriksson O., Craigen W.J., Forte M.A., Bernardi P. Properties of the permeability transition in VDAC1(-/-) mitochondria. Biochim. Biophys. Acta 2006, 1757:590-595.
38. Raghavan A., Sheiko T., Graham B.H., Craigen W.J. Voltage-dependant anion channels: novel insights into isoform function through genetic models. Biochim. Biophys. Acta 2012, 1818:1477-1485.
39. Shimizu S., Narita M., Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogeniccytochrome c by the mitochondrial channel VDAC. Nature 1993, 399:483-487.
40. Xu X., Decker W., Sampson M.J., Craigen W.J., Colombini M. Mouse VDAC isoforms expressed in yeast: channel properties and their roles in mitochondrial outer membrane permeability. J. Membr. Biol. 1999, 170:89-102.
41. Benz R. Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins. Biochim. Biophys. Acta 1994, 1197:167-196.
42. Colombini M., Blachly-Dyson E., Forte M. VDAC, a channel in the outer mitochondrial membrane. Ion Channels 1996, 4:169-202.
43. Duan S., Hajek P., Lin C., Shin S.K., Attardi G., Chomyn A. Mitochondrial outer membrane permeability change and hypersensitivity to digitonin early in staurosporine-induced apoptosis. J. Biol. Chem. 2003, 278:1346-1353.
44. Vander Heiden M.G., Chandel N.S., Li X.X., Schumacker P.T., Colombini M., Thompson C.B. Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:4666-4671.
45. Rostovtseva T.K., Antonsson B., Suzuki M., Youle R.J., Colombini M., Bezrukov S.M. Bid, but not Bax, regulates VDAC channels. J. Biol. Chem. 2004, 279:13575-13583.
46. Rostovtseva T.K., Bezrukov S.M. VDAC inhibition by tubulin and its physiological implications. Biochim. Biophys. Acta 2012, 1818:1526-1535.
47. Kerner J., Lee K., Tandler B., Hoppel C.L. VDAC proteomics: post-translation modifications. Biochim. Biophys. Acta 2012, 1818:1520-1525.
48. Lemasters J.J., Holmuhamedov E.L., Czerny C., Zhong Z., Maldonado E.N. Regulation of mitochondrialfunction by voltage dependent anion channels in ethanol metabolism and the Warburg effect. Biochim. Biophys. Acta 2012, 1818:1536-1544.
49. Baines C.P., Son C.X., Zheng Y.T., Wang G.W., Zhang J., Wang O.L., Guo Y., Bolli R., Cardwell E.M., Ping P. Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ. Res. 2003, 92:873-880.
50. Pastorino J.G., Hoek J.B., Shulga N. Activation of glycogen synthase kinase 3beta disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapy-induced cytotoxicity. Cancer Res. 2005, 65:10545-10554.
51. Wu S., Sampson M.J., Decker W.K., Craigen W.J. Each mammalian mitochondrial outer membrane porin protein is dispensable: effects on cellular respiration. Biochim. Biophys. Acta 1999, 1452:68-78.
52. Weeber E.J., Levy M., Sampson M.J., Anflous K., Armstrong D.L., Brown S.E., Sweatt J.D., Craigen W.J. The role of mitochondrial porins and the permeability transition pore in learning and synaptic plasticity. J. Biol. Chem. 2002, 277:18891-18897.
53. Cheng E.H., Sheiko T.V., Fisher J.K., Craigen W.J., Korsmeyer S.J. VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 2003, 301:513-517.
54. Jr W.D., Parker C.M., Filley J.K.Parks Cytochrome oxidase deficiency in Alzheimer's disease. Neurology 1990, 40:1302-1303.
55. 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.
56. Maurer I., Zierz S., Möller H.J. A selective defect of cytochrome c oxidase is present in brain of Alzheimer disease patients. Neurobiol. Aging 2000, 21:455-462.
57. 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.
58. 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.
59. 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.
60. 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.
61. 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.
62. 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.
63. 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(2004):1308-1312.
64. Eckert A., Hauptmann S., Scherping I., Rhein V., Müller-Spahn F., Götz J., Müller W.E. Soluble beta amyloid leads to mitochondrial defects in amyloid precursor protein and tau transgenic mice. Neurodegener. Dis. 2008, 5:157-159.
65. 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.
66. Caspersen C., Wang N., Yao J., Sosunov A., Chen X., Lustbader J.W., Xu H.W., Stern D., McKhann G., Yan S.S. Mitochondrial Abeta: a potential focal point for neuronal metabolic dysfunction in Alzheimer's disease. FASEB J. 2005, 19:2040-2041.
67. 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.
68. 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.
69. 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.
70. Manczak M., Mao P., Calkins C.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:S609-S631.
71. 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. 2010, 20:4515-4529.
72. 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.
73. Diana A., Simić G., Sinforiani E., Orrù N., Pichiri G., Bono G. Mitochondria morphology and DNA content upon sublethal exposure to beta-amyloid(1-42) peptide. Coll. Antropol. 2008, 32:51-58.
74. Schmidt C., Lepsverdize E., Chi S.L., Das A.M., Pizzo S.V., Dityatev A., Schachner M. Amyloid precursor protein and amyloid beta-peptide bind to ATP synthase and regulate its activity at the surface of neural cells. Mol. Psychiatry 2008, 13:953-969.
75. Matsumoto K., Akao Y., Yi H., Shamoto-Nagai M., Maruyama W., Naoi M. Overexpression of amyloid precursor protein induces susceptibility to oxidative stress in human neuroblastoma SH-SY5Y cells. J. Neural Transm. 2006, 113:125-135.
76. 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.
77. 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.
78. 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.
79. Chandrasekaran K., Hatanpää K., Rapoport S.I., Brady B.R. Decreased expression of nuclear and mitochondrial DNA-encoded genes of oxidative phosphorylation in association neocortex in Alzheimer disease. Brain Res. Mol. Brain Res. 1997, 44:99-104.
80. Simonian N.A., Hyman B.T. Functional alterations in Alzheimer's disease: selective loss of mitochondrial-encoded cytochrome oxidase mRNA in the hippocampal formation. J. Neuropathol. Exp. Neurol. 1994, 53:508-512.
81. Gibson G.E., Sheu K.F., Blass J.P. Abnormalities of mitochondrial enzymes in Alzheimer disease. J. Neural Transm. 1998, 105:855-870.
82. Wang J., Xiong S., Xie C., MarkesberY W.R., Lovell M.A. Increased oxidative damage in nuclear and mitochondrial DNA in Alzheimer's disease. J. Neurochem. 2005, 93:953-962.
83. Sultana R., Boyd-Kimball D., Cai J., Pierce W.M., Klein J.B., Merchant M., Butterfield D.A. Proteomics analysis of the Alzheimer's disease hippocampal proteome. J. Alzheimers Dis. 2007, 11:153-164.
84. Du H.L., 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.
85. 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.
86. Devi L., Ohno M. Mitochondrial dysfunction and accumulation of the β-secretase-cleaved C-terminal fragment of APP in Alzheimer's disease transgenic mice. Neurobiol. Dis. 2012, 45:417-424.
87. 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.
88. 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.
89. 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.
90. Keil U., Bonert A., Marques C.A., Strosznajder J.B., Müller-Spahn F., Müller W.E., Eckert A. Elevated nitric oxide production mediates beta-amyloid-induced mitochondria failure. Pol. J. Pharmacol. 2004, 56:631-634.
91. Park H.J., Kim S.S., Seong Y.M., Kim K.H., Goo H.G., Yoon E.J., Min do S., Kang S., Rhim H. Beta-amyloid precursor protein is a direct cleavage target of HtrA2 serine protease. Implications for the physiological function of HtrA2 in the mitochondria. J. Biol. Chem. 2006, 281:34277-34287.
92. Amadoro G., Corsetti V., Ciotti M.T., Florenzano F., Capsoni S., Amato G., Calissano P. Endogeno Aβ causes cell death via early tau hyperphosphorylation. Neurobiol. Aging 2011, 32:969-990.
93. 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.
94. 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.
95. 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.
96. Cuadrado-Tejedor M., Vilariño M., Cabodevilla F., Del Río J., Frechilla D., Pérez-Mediavilla A. Enhanced expression of the voltage-dependent anion channel 1 (VDAC1) in Alzheimer's disease transgenic mice: an insight into the pathogenic effects of amyloid-β. J. Alzheimers Dis. 2011, 23:195-206.
97. Thinnes F.P. Apoptogenic interactions of plasmalemmal type-1 VDAC and Aβ peptides via GxxxG motifs induce Alzheimer's disease - a basic model of apoptosis?. Wien. Med. Wochenschr. 2011, 161:274-276.
98. Ramírez C.M., González M., Díaz M., Alonso R., Ferrer I., Santpere G., Puig B., Meyer G., Marin R. VDAC and ERalpha interaction in caveolae from human cortex is altered in Alzheimer's disease. Mol. Cell. Neurosci. 2009, 42:172-183.
99. Reddy P.H. Abnormal tau, mitochondrial dysfunction, impaired axonal transport of mitochondria, and synaptic deprivation in Alzheimer's disease. Brain Res. 2011, 1415:136-148.