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Current Neuropharmacology

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ISSN (Online): 1875-6190

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Review Article

The Role of Mitochondrial Impairment in Alzheimer´s Disease Neurodegeneration: The Tau Connection

Author(s): Rodrigo A. Quntanilla* and Carola Tapia-Monsalves

Volume 18, Issue 11, 2020

Page: [1076 - 1091] Pages: 16

DOI: 10.2174/1570159X18666200525020259

Price: $65

Abstract

Accumulative evidence has shown that mitochondrial dysfunction plays a pivotal role in the pathogenesis of Alzheimer's disease (AD). Mitochondrial impairment actively contributes to the synaptic and cognitive failure that characterizes AD. The presence of soluble pathological forms of tau like hyperphosphorylated at Ser396 and Ser404 and cleaved at Asp421 by caspase 3, negatively impacts mitochondrial bioenergetics, transport, and morphology in neurons. These adverse effects against mitochondria health will contribute to the synaptic impairment and cognitive decline in AD. Current studies suggest that mitochondrial failure induced by pathological tau forms is likely the result of the opening of the mitochondrial permeability transition pore (mPTP). mPTP is a mitochondrial mega-channel that is activated by increases in calcium and is associated with mitochondrial stress and apoptosis. This structure is composed of different proteins, where Ciclophilin D (CypD) is considered to be the primary mediator of mPTP activation. Also, new studies suggest that mPTP contributes to Aβ pathology and oxidative stress in AD.

Further, inhibition of mPTP through the reduction of CypD expression prevents cognitive and synaptic impairment in AD mouse models. More importantly, tau protein contributes to the physiological regulation of mitochondria through the opening/interaction with mPTP in hippocampal neurons. Therefore, in this paper, we will discuss evidence that suggests an important role of pathological forms of tau against mitochondrial health. Also, we will discuss the possible role of mPTP in the mitochondrial impairment produced by the presence of tau pathology and its impact on synaptic function present in AD.

Keywords: Tau, Mitochondria, oxidative stress, Alzheimer´s disease, mitochondrial permeability transition pore, calcium.

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[1]
Huang, Y.; Mucke, L. Alzheimer mechanisms and therapeutic strategies. Cell, 2012, 148(6), 1204-1222.
[http://dx.doi.org/10.1016/j.cell.2012.02.040] [PMID: 22424230]
[2]
Mucke, L. Neuroscience: Alzheimer’s disease. Nature, 2009, 461(7266), 895-897.
[http://dx.doi.org/10.1038/461895a] [PMID: 19829367]
[3]
Kosik, K.S.; Joachim, C.L.; Selkoe, D.J. Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc. Natl. Acad. Sci. USA, 1986, 83(11), 4044-4048.
[http://dx.doi.org/10.1073/pnas.83.11.4044] [PMID: 2424016]
[4]
Ihara, Y.; Nukina, N.; Miura, R.; Ogawara, M. Phosphorylated tau protein is integrated into paired helical filaments in Alzheimer’s disease. J. Biochem., 1986, 99(6), 1807-1810.
[http://dx.doi.org/10.1093/oxfordjournals.jbchem.a135662] [PMID: 2427509]
[5]
Mandelkow, E-M.; Mandelkow, E. Tau in Alzheimer’s disease. Trends Cell Biol., 1998, 8(11), 425-427.
[http://dx.doi.org/10.1016/S0962-8924(98)01368-3] [PMID: 9854307]
[6]
Tapia-Rojas, C.; Cabezas-Opazo, F.; Deaton, C.A.; Vergara, E.H.; Johnson, G.V.W.; Quintanilla, R.A. It’s all about tau. Prog. Neurobiol., 2019, 175, 54-76.
[http://dx.doi.org/10.1016/j.pneurobio.2018.12.005] [PMID: 30605723]
[7]
Pritchard, S.M.; Dolan, P.J.; Vitkus, A.; Johnson, G.V.W. The toxicity of tau in Alzheimer disease: turnover, targets and potential therapeutics. J. Cell. Mol. Med., 2011, 15(8), 1621-1635.
[http://dx.doi.org/10.1111/j.1582-4934.2011.01273.x] [PMID: 21348938]
[8]
Polanco, J.C.; Li, C.; Bodea, L-G.; Martinez-Marmol, R.; Meunier, F.A.; Götz, J. Amyloid-β and tau complexity — towards improved biomarkers and targeted therapies. Nat. Rev. Neurol., 2017, 1-18.
[PMID: 29242522]
[9]
Dorval, V.; Fraser, P.E. Small ubiquitin-like modifier (SUMO) modification of natively unfolded proteins tau and alpha-synuclein. J. Biol. Chem., 2006, 281(15), 9919-9924.
[http://dx.doi.org/10.1074/jbc.M510127200] [PMID: 16464864]
[10]
Min, S.W.; Cho, S.H.; Zhou, Y.; Schroeder, S.; Haroutunian, V.; Seeley, W.W.; Huang, E.J.; Shen, Y.; Masliah, E.; Mukherjee, C.; Meyers, D.; Cole, P.A.; Ott, M.; Gan, L. Acetylation of tau inhibits its degradation and contributes to tauopathy. Neuron, 2010, 67(6), 953-966.
[http://dx.doi.org/10.1016/j.neuron.2010.08.044] [PMID: 20869593]
[11]
Ledesma, M.D.; Pérez, M.; Colaco, C.; Avila, J. Tau glycation is involved in aggregation of the protein but not in the formation of filaments. Cell. Mol. Biol., 1998, 44(7), 1111-1116.
[PMID: 9846893]
[12]
Takahashi, M.; Tsujioka, Y.; Yamada, T.; Tsuboi, Y.; Okada, H.; Yamamoto, T.; Liposits, Z. Glycosylation of microtubule-associated protein tau in Alzheimer’s disease brain. Acta Neuropathol., 1999, 97(6), 635-641.
[http://dx.doi.org/10.1007/s004010051040] [PMID: 10378383]
[13]
Reynolds, M.R.; Berry, R.W.; Binder, L.I. Nitration in neurodegeneration: deciphering the “Hows” “nYs. Biochemistry, 2007, 46(25), 7325-7336.
[http://dx.doi.org/10.1021/bi700430y] [PMID: 17542619]
[14]
de Calignon, A.; Fox, L.M.; Pitstick, R.; Carlson, G.A.; Bacskai, B.J.; Spires-Jones, T.L.; Hyman, B.T. Caspase activation precedes and leads to tangles. Nature, 2010, 464(7292), 1201-1204.
[http://dx.doi.org/10.1038/nature08890] [PMID: 20357768]
[15]
Tai, H.C.; Wang, B.Y.; Serrano-Pozo, A.; Frosch, M.P.; Spires-Jones, T.L.; Hyman, B.T. Frequent and symmetric deposition of misfolded tau oligomers within presynaptic and postsynaptic terminals in Alzheimer’s disease. Acta Neuropathol. Commun., 2014, 2, 146.
[http://dx.doi.org/10.1186/s40478-014-0146-2] [PMID: 25330988]
[16]
Tai, H.C.; Serrano-Pozo, A.; Hashimoto, T.; Frosch, M.P.; Spires-Jones, T.L.; Hyman, B.T. The synaptic accumulation of hyperphosphorylated tau oligomers in Alzheimer disease is associated with dysfunction of the ubiquitin-proteasome system. Am. J. Pathol., 2012, 181(4), 1426-1435.
[http://dx.doi.org/10.1016/j.ajpath.2012.06.033] [PMID: 22867711]
[17]
Cabezas-Opazo, F.A.; Vergara-Pulgar, K.; Pérez, M.J.; Jara, C.; Osorio-Fuentealba, C.; Quintanilla, R.A. Mitochondrial dysfunction contributes to the pathogenesis of alzheimer’s disease. Oxid. Med. Cell. Longev., 2015. 2015509654
[http://dx.doi.org/10.1155/2015/509654] [PMID: 26221414]
[18]
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(28), 18754-18766.
[http://dx.doi.org/10.1074/jbc.M808908200] [PMID: 19389700]
[19]
Pérez, M.J.; Vergara-Pulgar, K.; Jara, C.; Cabezas-Opazo, F.; Quintanilla, R.A. Caspase-cleaved tau impairs mitochondrial dynamics in alzheimer’s disease. Mol. Neurobiol., 2018, 55(2), 1004-1018.
[http://dx.doi.org/10.1007/s12035-017-0385-x] [PMID: 28084594]
[20]
Quintanilla, R.A.; Dolan, P.J.; Jin, Y.N.; Johnson, G.V. Truncated tau and Aβ cooperatively impair mitochondria in primary neurons. Neurobiol. Aging, 2012, 33(3), 619.e25-619.e35.
[http://dx.doi.org/10.1016/j.neurobiolaging.2011.02.007] [PMID: 21450370]
[21]
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(23), 4515-4529.
[http://dx.doi.org/10.1093/hmg/ddr381] [PMID: 21873260]
[22]
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(12), 1225-1240.
[http://dx.doi.org/10.1093/hmg/ddh140] [PMID: 15115763]
[23]
Manczak, M.; Reddy, P.H. Abnormal interaction of VDAC1 with amyloid beta and phosphorylated tau causes mitochondrial dysfunction in Alzheimer’s disease. Hum. Mol. Genet., 2012, 21(23), 5131-5146.
[http://dx.doi.org/10.1093/hmg/dds360] [PMID: 22926141]
[24]
Querfurth, H.W.; LaFerla, F.M. Alzheimer’s disease. N. Engl. J. Med., 2010, 362(4), 329-344.
[http://dx.doi.org/10.1056/NEJMra0909142] [PMID: 20107219]
[25]
Busciglio, J.; Lorenzo, A.; Yeh, J.; Yankner, B.A. beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron, 1995, 14(4), 879-888.
[http://dx.doi.org/10.1016/0896-6273(95)90232-5] [PMID: 7718249]
[26]
Clark, L.N.; Poorkaj, P.; Wszolek, Z.; Geschwind, D.H.; Nasreddine, Z.S.; Miller, B.; Li, D.; Payami, H.; Awert, F.; Markopoulou, K.; Andreadis, A.; D’Souza, I.; Lee, V.M.; Reed, L.; Trojanowski, J.Q.; Zhukareva, V.; Bird, T.; Schellenberg, G.; Wilhelmsen, K.C. Pathogenic implications of mutations in the tau gene in pallido-ponto-nigral degeneration and related neurodegenerative disorders linked to chromosome 17. Proc. Natl. Acad. Sci. USA, 1998, 95(22), 13103-13107.
[http://dx.doi.org/10.1073/pnas.95.22.13103] [PMID: 9789048]
[27]
Hutton, M.; Lendon, C.L.; Rizzu, P.; Baker, M.; Froelich, S.; Houlden, H.; Pickering-Brown, S.; Chakraverty, S.; Isaacs, A.; Grover, A.; Hackett, J.; Adamson, J.; Lincoln, S.; Dickson, D.; Davies, P.; Petersen, R.C.; Stevens, M.; de Graaff, E.; Wauters, E.; van Baren, J.; Hillebrand, M.; Joosse, M.; Kwon, J.M.; Nowotny, P.; Che, L.K.; Norton, J.; Morris, J.C.; Reed, L.A.; Trojanowski, J.; Basun, H.; Lannfelt, L.; Neystat, M.; Fahn, S.; Dark, F.; Tannenberg, T.; Dodd, P.R.; Hayward, N.; Kwok, J.B.; Schofield, P.R.; Andreadis, A.; Snowden, J.; Craufurd, D.; Neary, D.; Owen, F.; Oostra, B.A.; Hardy, J.; Goate, A.; van Swieten, J.; Mann, D.; Lynch, T.; Heutink, P. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature, 1998, 393(6686), 702-705.
[http://dx.doi.org/10.1038/31508] [PMID: 9641683]
[28]
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. USA, 2002, 99(9), 6364-6369.
[http://dx.doi.org/10.1073/pnas.092136199] [PMID: 11959919]
[29]
Pallo, S.P.; Johnson, G.V. Tau facilitates Aβ-induced loss of mitochondrial membrane potential independent of cytosolic calcium fluxes in mouse cortical neurons. Neurosci. Lett., 2015, 597, 32-37.
[http://dx.doi.org/10.1016/j.neulet.2015.04.021] [PMID: 25888814]
[30]
Pallo, S.P.; DiMaio, J.; Cook, A.; Nilsson, B.; Johnson, G.V.W. Mechanisms of tau and Aβ-induced excitotoxicity. Brain Res., 2016, 1634, 119-131.
[http://dx.doi.org/10.1016/j.brainres.2015.12.048] [PMID: 26731336]
[31]
Kopeikina, K.J.; Hyman, B.T.; Spires-Jones, T.L. Soluble forms of tau are toxic in Alzheimer’s disease. Transl. Neurosci., 2012, 3(3), 223-233.
[http://dx.doi.org/10.2478/s13380-012-0032-y] [PMID: 23029602]
[32]
Santacruz, K.; Lewis, J.; Spires, T.; Paulson, J.; Kotilinek, L.; Ingelsson, M.; Guimaraes, A.; DeTure, M.; Ramsden, M.; McGowan, E.; Forster, C.; Yue, M.; Orne, J.; Janus, C.; Mariash, A.; Kuskowski, M.; Hyman, B.; Hutton, M.; Ashe, K.H. Tau suppression in a neurodegenerative mouse model improves memory function. Science, 2005, 309(5733), 476-481.
[http://dx.doi.org/10.1126/science.1113694] [PMID: 16020737]
[33]
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(5825), 750-754.
[http://dx.doi.org/10.1126/science.1141736] [PMID: 17478722]
[34]
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(6001), 198.
[http://dx.doi.org/10.1126/science.1194653] [PMID: 20829454]
[35]
Kolarova, M.; García-Sierra, F.; Bartos, A.; Ricny, J.; Ripova, D. Structure and pathology of tau protein in Alzheimer disease. Int. J. Alzheimers Dis., 2012. 2012731526
[http://dx.doi.org/10.1155/2012/731526] [PMID: 22690349]
[36]
Alonso, A.C.; Li, B.; Grundke-Iqbal, I.; Iqbal, K. Mechanism of tau-induced neurodegeneration in Alzheimer disease and related tauopathies. Curr. Alzheimer Res., 2008, 5(4), 375-384.
[http://dx.doi.org/10.2174/156720508785132307] [PMID: 18690834]
[37]
Di Xia. Li, C.; Götz, J. (2015). Pseudophosphorylation of Tau at distinct epitopes or the presence of the P301L mutation targets the microtubule-associated protein Tau to dendritic spines. BBA Mol of Dis, 2015, 1852(5), 913-924.
[http://dx.doi.org/10.1016/j.bbadis.2014.12.017]
[38]
Jin, M.; Shepardson, N.; Yang, T.; Chen, G.; Walsh, D.; Selkoe, D.J. Soluble amyloid β-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc. Natl. Acad. Sci. USA, 2011, 108(14), 5819-5824.
[http://dx.doi.org/10.1073/pnas.1017033108] [PMID: 21421841]
[39]
Jope, R.S.; Johnson, G.V. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci., 2004, 29(2), 95-102.
[http://dx.doi.org/10.1016/j.tibs.2003.12.004] [PMID: 15102436]
[40]
Spittaels, K.; Van den Haute, C.; Van Dorpe, J.; Geerts, H.; Mercken, M.; Bruynseels, K.; Lasrado, R.; Vandezande, K.; Laenen, I.; Boon, T.; Van Lint, J.; Vandenheede, J.; Moechars, D.; Loos, R.; Van Leuven, F. Glycogen synthase kinase-3beta phosphorylates protein tau and rescues the axonopathy in the central nervous system of human four-repeat tau transgenic mice. J. Biol. Chem., 2000, 275(52), 41340-41349.
[http://dx.doi.org/10.1074/jbc.M006219200] [PMID: 11007782]
[41]
Lucas, J.J.; Hernández, F.; Gómez-Ramos, P.; Morán, M.A.; Hen, R.; Avila, J. Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J., 2001, 20(1-2), 27-39.
[http://dx.doi.org/10.1093/emboj/20.1.27] [PMID: 11226152]
[42]
Terry, R.D.; Masliah, E.; Salmon, D.P.; Butters, N.; DeTeresa, R.; Hill, R.; Hansen, L.A.; Katzman, R. Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol., 1991, 30(4), 572-580.
[http://dx.doi.org/10.1002/ana.410300410] [PMID: 1789684]
[43]
Selkoe, D.J. Alzheimer’s disease is a synaptic failure. Science, 2002, 298(5594), 789-791.
[http://dx.doi.org/10.1126/science.1074069] [PMID: 12399581]
[44]
Davies, P.; Maloney, A.J. Selective loss of central cholinergic neurons in Alzheimer’s disease. Lancet, 1976, 2(8000), 1403.
[http://dx.doi.org/10.1016/S0140-6736(76)91936-X] [PMID: 63862]
[45]
Albuquerque, E.X.; Pereira, E.F.; Alkondon, M.; Rogers, S.W. Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol. Rev., 2009, 89(1), 73-120.
[http://dx.doi.org/10.1152/physrev.00015.2008] [PMID: 19126755]
[46]
Sze, C.I.; Troncoso, J.C.; Kawas, C.; Mouton, P.; Price, D.L.; Martin, L.J. Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease. J. Neuropathol. Exp. Neurol., 1997, 56(8), 933-944.
[http://dx.doi.org/10.1097/00005072-199708000-00011] [PMID: 9258263]
[47]
Ferrer, I.; Gullotta, F. Down’s syndrome and Alzheimer’s disease: dendritic spine counts in the hippocampus. Acta Neuropathol., 1990, 79(6), 680-685.
[http://dx.doi.org/10.1007/BF00294247] [PMID: 2141748]
[48]
Dorostkar, M.M.; Zou, C.; Blazquez-Llorca, L.; Herms, J. Analyzing dendritic spine pathology in Alzheimer’s disease: problems and opportunities. Acta Neuropathol., 2015, 130(1), 1-19.
[http://dx.doi.org/10.1007/s00401-015-1449-5] [PMID: 26063233]
[49]
Kasai, H.; Fukuda, M.; Watanabe, S.; Hayashi-Takagi, A.; Noguchi, J. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci., 2010, 33(3), 121-129.
[http://dx.doi.org/10.1016/j.tins.2010.01.001] [PMID: 20138375]
[50]
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(6), 1067-1081.
[http://dx.doi.org/10.1016/j.neuron.2010.11.030] [PMID: 21172610]
[51]
Zhou, L.; McInnes, J.; Wierda, K.; Holt, M.; Herrmann, A.G.; Jackson, R.J.; Wang, Y-C.; Swerts, J.; Beyens, J.; Miskiewicz, K.; Vilain, S.; Dewachter, I.; Moechars, D.; De Strooper, B.; Spires-Jones, T.L.; De Wit, J.; Verstreken, P. Tau association with synaptic vesicles causes presynaptic dysfunction. Nat. Commun., 2017, 8, 15295.
[http://dx.doi.org/10.1038/ncomms15295] [PMID: 28492240]
[52]
McInnes, J.; Wierda, K.; Snellinx, A.; Bounti, L.; Wang, Y.C.; Stancu, I.C.; Apóstolo, N.; Gevaert, K.; Dewachter, I.; Spires-Jones, T.L.; De Strooper, B.; De Wit, J.; Zhou, L.; Verstreken, P. Synaptogyrin-3 mediates presynaptic dysfunction induced by tau. Neuron, 2018, 97(4), 823-835.e8.
[http://dx.doi.org/10.1016/j.neuron.2018.01.022] [PMID: 29398363]
[53]
Wang, Y.; Balaji, V.; Kaniyappan, S.; Krüger, L.; Irsen, S.; Tepper, K.; Chandupatla, R.; Maetzler, W.; Schneider, A.; Mandelkow, E.; Mandelkow, E-M. The release and trans-synaptic transmission of Tau via exosomes. Mol. Neurodegener., 2017, 12(1), 5-5.
[http://dx.doi.org/10.1186/s13024-016-0143-y] [PMID: 28086931]
[54]
DeVos, S.L.; Corjuc, B.T.; Oakley, D.H.; Nobuhara, C.K.; Bannon, R.N.; Chase, A.; Commins, C.; Gonzalez, J.A.; Dooley, P.M.; Frosch, M.P.; Hyman, B.T. Synaptic tau seeding precedes tau pathology in human alzheimer’s disease brain. Front. Neurosci., 2018, 12, 267.
[http://dx.doi.org/10.3389/fnins.2018.00267] [PMID: 29740275]
[55]
Hatch, R.J.; Wei, Y.; Xia, D.; Götz, J. Hyperphosphorylated tau causes reduced hippocampal CA1 excitability by relocating the axon initial segment. Acta Neuropathol., 2017, 133(5), 717-730.
[http://dx.doi.org/10.1007/s00401-017-1674-1] [PMID: 28091722]
[56]
Mondragón-Rodríguez, S.; Trillaud-Doppia, E.; Dudilot, A.; Bourgeois, C.; Lauzon, M.; Leclerc, N.; Boehm, J. Interaction of endogenous tau protein with synaptic proteins is regulated by N-methyl-D-aspartate receptor-dependent tau phosphorylation. J. Biol. Chem., 2012, 287(38), 32040-32053.
[http://dx.doi.org/10.1074/jbc.M112.401240] [PMID: 22833681]
[57]
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(3), 387-397.
[http://dx.doi.org/10.1016/j.cell.2010.06.036] [PMID: 20655099]
[58]
Roberson, E.D.; Halabisky, B.; Yoo, J.W.; Yao, J.; Chin, J.; Yan, F.; Wu, T.; Hamto, P.; Devidze, N.; Yu, G-Q.; Palop, J.J.; Noebels, J.L.; Mucke, L. Amyloid-β/Fyn-induced synaptic, network, and cognitive impairments depend on tau levels in multiple mouse models of Alzheimer’s disease. J. Neurosci., 2011, 31(2), 700-711.
[http://dx.doi.org/10.1523/JNEUROSCI.4152-10.2011] [PMID: 21228179]
[59]
Shirazi, S.K.; Wood, J.G. The protein tyrosine kinase, fyn, in Alzheimer’s disease pathology. Neuroreport, 1993, 4(4), 435-437.
[http://dx.doi.org/10.1097/00001756-199304000-00024] [PMID: 8388744]
[60]
Basurto-Islas, G.; Luna-Muñoz, J.; Guillozet-Bongaarts, A.L.; Binder, L.I.; Mena, R.; García-Sierra, F. Accumulation of aspartic acid421- and glutamic acid391-cleaved tau in neurofibrillary tangles correlates with progression in Alzheimer disease. J. Neuropathol. Exp. Neurol., 2008, 67(5), 470-483.
[http://dx.doi.org/10.1097/NEN.0b013e31817275c7] [PMID: 18431250]
[61]
Rohn, T.T.; Head, E.; Nesse, W.H.; Cotman, C.W.; Cribbs, D.H. Activation of caspase-8 in the Alzheimer’s disease brain. Neurobiol. Dis., 2001, 8(6), 1006-1016.
[http://dx.doi.org/10.1006/nbdi.2001.0449] [PMID: 11741396]
[62]
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(2), 341-354.
[http://dx.doi.org/10.1006/nbdi.2002.0549] [PMID: 12505426]
[63]
Gamblin, T.C.; Chen, F.; Zambrano, A.; Abraha, A.; Lagalwar, S.; Guillozet, A.L.; Lu, M.; Fu, Y.; Garcia-Sierra, F.; LaPointe, N.; Miller, R.; Berry, R.W.; Binder, L.I.; Cryns, V.L. Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer’s disease. Proc. Natl. Acad. Sci. USA, 2003, 100(17), 10032-10037.
[http://dx.doi.org/10.1073/pnas.1630428100] [PMID: 12888622]
[64]
Rissman, R.A.; Poon, W.W.; Blurton-Jones, M.; Oddo, S.; Torp, R.; Vitek, M.P.; LaFerla, F.M.; Rohn, T.T.; Cotman, C.W. Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology. J. Clin. Invest., 2004, 114(1), 121-130.
[http://dx.doi.org/10.1172/JCI200420640] [PMID: 15232619]
[65]
Fasulo, L.; Ugolini, G.; Cattaneo, A. Apoptotic effect of caspase-3 cleaved tau in hippocampal neurons and its potentiation by tau FTDP-mutation N279K. J. Alzheimers Dis., 2005, 7(1), 3-13.
[http://dx.doi.org/10.3233/JAD-2005-7102] [PMID: 15750210]
[66]
Matthews-Roberson, T.A.; Quintanilla, R.A.; Ding, H.; Johnson, G.V. Immortalized cortical neurons expressing caspase-cleaved tau are sensitized to endoplasmic reticulum stress induced cell death. Brain Res., 2008, 1234, 206-212.
[http://dx.doi.org/10.1016/j.brainres.2008.07.111] [PMID: 18718455]
[67]
Kim, Y.; Choi, H.; Lee, W.; Park, H.; Kam, T.I.; Hong, S.H.; Nah, J.; Jung, S.; Shin, B.; Lee, H.; Choi, T.Y.; Choo, H.; Kim, K.K.; Choi, S.Y.; Kayed, R.; Jung, Y.K. Caspase-cleaved tau exhibits rapid memory impairment associated with tau oligomers in a transgenic mouse model. Neurobiol. Dis., 2016, 87, 19-28.
[http://dx.doi.org/10.1016/j.nbd.2015.12.006] [PMID: 26704708]
[68]
Zhao, Y.; Tseng, I.C.; Heyser, C.J.; Rockenstein, E.; Mante, M.; Adame, A.; Zheng, Q.; Huang, T.; Wang, X.; Arslan, P.E.; Chakrabarty, P.; Wu, C.; Bu, G.; Mobley, W.C.; Zhang, Y.W.; St George-Hyslop, P.; Masliah, E.; Fraser, P.; Xu, H. Appoptosin-Mediated Caspase Cleavage of Tau Contributes to Progressive Supranuclear Palsy Pathogenesis. Neuron, 2015, 87(5), 963-975.
[http://dx.doi.org/10.1016/j.neuron.2015.08.020] [PMID: 26335643]
[69]
Zhang, H.; Zhang, Y.W.; Chen, Y.; Huang, X.; Zhou, F.; Wang, W.; Xian, B.; Zhang, X.; Masliah, E.; Chen, Q.; Han, J.D.; Bu, G.; Reed, J.C.; Liao, F.F.; Chen, Y.G.; Xu, H. Appoptosin is a novel pro-apoptotic protein and mediates cell death in neurodegeneration. J. Neurosci., 2012, 32(44), 15565-15576.
[http://dx.doi.org/10.1523/JNEUROSCI.3668-12.2012] [PMID: 23115192]
[70]
Beal, M.F. Mitochondria, oxidative damage, and inflammation in Parkinson’s disease. Ann. N. Y. Acad. Sci., 2003, 991, 120-131.
[http://dx.doi.org/10.1111/j.1749-6632.2003.tb07470.x] [PMID: 12846981]
[71]
Praticò, D.; Clark, C.M.; Liun, F.; Rokach, J.; Lee, V.Y.; Trojanowski, J.Q. Increase of brain oxidative stress in mild cognitive impairment: a possible predictor of Alzheimer disease. Arch. Neurol., 2002, 59(6), 972-976.
[http://dx.doi.org/10.1001/archneur.59.6.972] [PMID: 12056933]
[72]
Nunnari, J.; Suomalainen, A. Mitochondria: in sickness and in health. Cell, 2012, 148(6), 1145-1159.
[http://dx.doi.org/10.1016/j.cell.2012.02.035] [PMID: 22424226]
[73]
Beal, M.F. Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol., 2005, 58(4), 495-505.
[http://dx.doi.org/10.1002/ana.20624] [PMID: 16178023]
[74]
Li, Z.; Okamoto, K.; Hayashi, Y.; Sheng, M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell, 2004, 119(6), 873-887.
[http://dx.doi.org/10.1016/j.cell.2004.11.003] [PMID: 15607982]
[75]
Wang, X.; Su, B.; Fujioka, H.; Zhu, X. Dynamin-like protein 1 reduction underlies mitochondrial morphology and distribution abnormalities in fibroblasts from sporadic Alzheimer’s disease patients. Am. J. Pathol., 2008, 173(2), 470-482.
[http://dx.doi.org/10.2353/ajpath.2008.071208] [PMID: 18599615]
[76]
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(28), 9090-9103.
[http://dx.doi.org/10.1523/JNEUROSCI.1357-09.2009] [PMID: 19605646]
[77]
Sebastián, D.; Palacín, M.; Zorzano, A. Mitochondrial Dynamics: Coupling Mitochondrial Fitness with Healthy Aging. Trends Mol. Med., 2017, 23(3), 201-215.
[http://dx.doi.org/10.1016/j.molmed.2017.01.003] [PMID: 28188102]
[78]
Bertholet, A.M.; Delerue, T.; Millet, A.M.; Moulis, M.F.; David, C.; Daloyau, M.; Arnauné-Pelloquin, L.; Davezac, N.; Mils, V.; Miquel, M.C.; Rojo, M.; Belenguer, P. Mitochondrial fusion/fission dynamics in neurodegeneration and neuronal plasticity. Neurobiol. Dis., 2016, 90, 3-19.
[http://dx.doi.org/10.1016/j.nbd.2015.10.011] [PMID: 26494254]
[79]
Kerr, J.S.; Adriaanse, B.A.; Greig, N.H.; Mattson, M.P.; Cader, M.Z.; Bohr, V.A.; Fang, E.F. Mitophagy and Alzheimer’s Disease: Cellular and Molecular Mechanisms. Trends Neurosci., 2017, 40(3), 151-166.
[http://dx.doi.org/10.1016/j.tins.2017.01.002] [PMID: 28190529]
[80]
Anand, R.; Wai, T.; Baker, M.J.; Kladt, N.; Schauss, A.C.; Rugarli, E.; Langer, T. The i-AAA protease YME1L and OMA1 cleave OPA1 to balance mitochondrial fusion and fission. J. Cell Biol., 2014, 204(6), 919-929.
[http://dx.doi.org/10.1083/jcb.201308006] [PMID: 24616225]
[81]
Bertholet, A.M.; Millet, A.M.; Guillermin, O.; Daloyau, M.; Davezac, N.; Miquel, M.C.; Belenguer, P. OPA1 loss of function affects in vitro neuronal maturation. Brain, 2013, 136(Pt 5), 1518-1533.
[http://dx.doi.org/10.1093/brain/awt060] [PMID: 23543485]
[82]
Gratuze, M.; Cisbani, G.; Cicchetti, F.; Planel, E. Is Huntington’s disease a tauopathy? Brain, 2016, 139(Pt 4), 1014-1025.
[http://dx.doi.org/10.1093/brain/aww021] [PMID: 26969684]
[83]
Mckee, A.C.; Daneshvar, D.H. The neuropathology of traumatic brain injury. Handb. Clin. Neurol., 2015, 127, 45-66.
[http://dx.doi.org/10.1016/B978-0-444-52892-6.00004-0] [PMID: 25702209]
[84]
Quintanilla, R.A.; Johnson, G.V.W. Role of mitochondrial dysfunction in the pathogenesis of Huntington’s disease. Brain Res. Bull., 2009, 80(4-5), 242-247.
[http://dx.doi.org/10.1016/j.brainresbull.2009.07.010] [PMID: 19622387]
[85]
McIntosh, G.C.; Jameson, H.D.; Markesbery, W.R. Huntington disease associated with Alzheimer disease. Ann. Neurol., 1978, 3(6), 545-548.
[http://dx.doi.org/10.1002/ana.410030616] [PMID: 150253]
[86]
Myers, R.H.; Sax, D.S.; Schoenfeld, M.; Bird, E.D.; Wolf, P.A.; Vonsattel, J.P.; White, R.F.; Martin, J.B. Late onset of Huntington’s disease. J. Neurol. Neurosurg. Psychiatry, 1985, 48(6), 530-534.
[http://dx.doi.org/10.1136/jnnp.48.6.530] [PMID: 3159849]
[87]
Moss, R.J.; Mastri, A.R.; Schut, L.J. The coexistence and differentiation of late onset Huntington’s disease and Alzheimer’s disease. A case report and review of the literature. J. Am. Geriatr. Soc., 1988, 36(3), 237-241.
[http://dx.doi.org/10.1111/j.1532-5415.1988.tb01807.x] [PMID: 2963060]
[88]
Fernández-Nogales, M.; Cabrera, J.R.; Santos-Galindo, M.; Hoozemans, J.J.; Ferrer, I.; Rozemuller, A.J.; Hernández, F.; Avila, J.; Lucas, J.J. Huntington’s disease is a four-repeat tauopathy with tau nuclear rods. Nat. Med., 2014, 20(8), 881-885.
[http://dx.doi.org/10.1038/nm.3617] [PMID: 25038828]
[89]
Vuono, R.; Winder-Rhodes, S.; de Silva, R.; Cisbani, G.; Drouin-Ouellet, J.; Spillantini, M.G.; Cicchetti, F.; Barker, R.A. The role of tau in the pathological process and clinical expression of Huntington’s disease. Brain, 2015, 138(Pt 7), 1907-1918.
[http://dx.doi.org/10.1093/brain/awv107] [PMID: 25953777]
[90]
Goebel, H.H.; Heipertz, R.; Scholz, W.; Iqbal, K.; Tellez-Nagel, I. Juvenile Huntington chorea: clinical, ultrastructural, and biochemical studies. Neurology, 1978, 28(1), 23-31.
[http://dx.doi.org/10.1212/WNL.28.1.23] [PMID: 145549]
[91]
Stahl, W.L.; Swanson, P.D. Biochemical abnormalities in Huntington’s chorea brains. Neurology, 1974, 24(9), 813-819.
[http://dx.doi.org/10.1212/WNL.24.9.813] [PMID: 4277376]
[92]
Reddy, P.H.; Shirendeb, U.P. Mutant huntingtin, abnormal mitochondrial dynamics, defective axonal transport of mitochondria, and selective synaptic degeneration in Huntington’s disease. Biochim. Biophys. Acta, 2012, 1822(2), 101-110.
[http://dx.doi.org/10.1016/j.bbadis.2011.10.016] [PMID: 22080977]
[93]
Jin, Y.N.; Yu, Y.V.; Gundemir, S.; Jo, C.; Cui, M.; Tieu, K.; Johnson, G.V.W. Impaired mitochondrial dynamics and Nrf2 signaling contribute to compromised responses to oxidative stress in striatal cells expressing full-length mutant huntingtin. PLoS One, 2013, 8(3) e57932
[http://dx.doi.org/10.1371/journal.pone.0057932] [PMID: 23469253]
[94]
Kim, J.; Moody, J.P.; Edgerly, C.K.; Bordiuk, O.L.; Cormier, K.; Smith, K.; Beal, M.F.; Ferrante, R.J. Mitochondrial loss, dysfunction and altered dynamics in Huntington’s disease. Hum. Mol. Genet., 2010, 19(20), 3919-3935.
[http://dx.doi.org/10.1093/hmg/ddq306] [PMID: 20660112]
[95]
Shirendeb, U.; Reddy, A.P.; Manczak, M.; Calkins, M.J.; Mao, P.; Tagle, D.A.; Reddy, P.H. Abnormal mitochondrial dynamics, mitochondrial loss and mutant huntingtin oligomers in Huntington’s disease: implications for selective neuronal damage. Hum. Mol. Genet., 2011, 20(7), 1438-1455.
[http://dx.doi.org/10.1093/hmg/ddr024] [PMID: 21257639]
[96]
Shirendeb, U.P.; Calkins, M.J.; Manczak, M.; Anekonda, V.; Dufour, B.; McBride, J.L.; Mao, P.; Reddy, P.H. Mutant huntingtin’s interaction with mitochondrial protein Drp1 impairs mitochondrial biogenesis and causes defective axonal transport and synaptic degeneration in Huntington’s disease. Hum. Mol. Genet., 2012, 21(2), 406-420.
[http://dx.doi.org/10.1093/hmg/ddr475] [PMID: 21997870]
[97]
Song, W.; Chen, J.; Petrilli, A.; Liot, G.; Klinglmayr, E.; Zhou, Y.; Poquiz, P.; Tjong, J.; Pouladi, M.A.; Hayden, M.R.; Masliah, E.; Ellisman, M.; Rouiller, I.; Schwarzenbacher, R.; Bossy, B.; Perkins, G.; Bossy-Wetzel, E. Mutant huntingtin binds the mitochondrial fission GTPase dynamin-related protein-1 and increases its enzymatic activity. Nat. Med., 2011, 17(3), 377-382.
[http://dx.doi.org/10.1038/nm.2313] [PMID: 21336284]
[98]
Soneson, C.; Fontes, M.; Zhou, Y.; Denisov, V.; Paulsen, J.S.; Kirik, D.; Petersén, A. Early changes in the hypothalamic region in prodromal Huntington disease revealed by MRI analysis. Neurobiol. Dis., 2010, 40, 531-543.
[http://dx.doi.org/10.1016/j.nbd.2010.07.013]
[99]
Costa, V.; Giacomello, M.; Hudec, R.; Lopreiato, R.; Ermak, G.; Lim, D.; Malorni, W.; Davies, K.J.; Carafoli, E.; Scorrano, L. Mitochondrial fission and cristae disruption increase the response of cell models of Huntington’s disease to apoptotic stimuli. EMBO Mol. Med., 2010, 2(12), 490-503.
[http://dx.doi.org/10.1002/emmm.201000102] [PMID: 21069748]
[100]
Ramos-Cejudo, J.; Wisniewski, T.; Marmar, C.; Zetterberg, H.; Blennow, K.; de Leon, M.J.; Fossati, S. Traumatic brain injury and alzheimer’s disease: The cerebrovascular link. EBioMedicine, 2018, 28(C), 21-30.
[http://dx.doi.org/10.1016/j.ebiom.2018.01.021] [PMID: 29396300]
[101]
McKee, A.C.; Cairns, N.J.; Dickson, D.W.; Folkerth, R.D.; Keene, C.D.; Litvan, I.; Perl, D.P. Stein; T. D.; Vonsattel, J. P.; Stewart, W.; Tripodis, Y.; Crary, J.F.; Bieniek, K.F.; Dams- O’Connor, K.; Alvarez, V.E.; Gordon, W. A.; Group, T. C. The first NINDS/NIBIB con- sensus meeting to define neuropathological criteria for the diagnosis of chronic traumatic encephalopathy. Acta Neuropathol., 2016, 131, 75-86.
[http://dx.doi.org/10.1007/s00401-015-1515-z] [PMID: 26667418]
[102]
Washington, P.M.; Morffy, N.; Parsadanian, M.; Zapple, D.N.; Burns, M.P. Experimental traumatic brain injury induces rapid aggregation and oligomerization of amyloid-beta in an Alzheimer’s disease mouse model. J. Neurotrauma, 2014, 31(1), 125-134.
[http://dx.doi.org/10.1089/neu.2013.3017] [PMID: 24050316]
[103]
Abisambra, J.F.; Scheff, S. Brain injury in the context of tauopathies. J. Alzheimers Dis., 2014, 40(3), 495-518.
[http://dx.doi.org/10.3233/JAD-131019] [PMID: 24496078]
[104]
Benaroya, H. Brain energetics, mitochondria, and traumatic brain injury. Rev. Neurosci., 2020, 31(4), 363-390.
[http://dx.doi.org/10.1515/revneuro-2019-0086] [PMID: 32004148]
[105]
Di Pietro, V.; Lazzarino, G.; Amorini, A.M.; Signoretti, S.; Hill, L.J.; Porto, E.; Tavazzi, B.; Lazzarino, G.; Belli, A. Fusion or fission: The destiny of mitochondria in traumatic brain injury of different severities. Sci. Rep., 2017, 7(1), 9189.
[http://dx.doi.org/10.1038/s41598-017-09587-2] [PMID: 28835707]
[106]
Fischer, T.D.; Hylin, M.J.; Zhao, J.; Moore, A.N.; Waxham, M.N.; Dash, P.K. Altered Mitochondrial Dynamics and TBI Pathophysiology. Front. Syst. Neurosci., 2016, 10, 29.
[http://dx.doi.org/10.3389/fnsys.2016.00029] [PMID: 27065821]
[107]
Wu, Q.; Xia, S.X.; Li, Q.Q.; Gao, Y.; Shen, X.; Ma, L.; Zhang, M.Y.; Wang, T.; Li, Y.S.; Wang, Z.F.; Luo, C.L.; Tao, L.Y. Mitochondrial division inhibitor 1 (Mdivi-1) offers neuroprotection through diminishing cell death and improving functional outcome in a mouse model of traumatic brain injury. Brain Res., 2016, 1630, 134-143.
[http://dx.doi.org/10.1016/j.brainres.2015.11.016] [PMID: 26596858]
[108]
Wu, Q.; Gao, C.; Wang, H.; Zhang, X.; Li, Q.; Gu, Z.; Shi, X.; Cui, Y.; Wang, T.; Chen, X.; Wang, X.; Luo, C.; Tao, L. Mdivi-1 alleviates blood-brain barrier disruption and cell death in experimental traumatic brain injury by mitigating autophagy dysfunction and mitophagy activation. Int. J. Biochem. Cell Biol., 2018, 94(94), 44-55.
[http://dx.doi.org/10.1016/j.biocel.2017.11.007] [PMID: 29174311]
[109]
Nisoli, E.; Clementi, E.; Paolucci, C.; Cozzi, V.; Tonello, C.; Sciorati, C.; Bracale, R.; Valerio, A.; Francolini, M.; Moncada, S.; Carruba, M.O. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science, 2003, 299(5608), 896-899.
[http://dx.doi.org/10.1126/science.1079368] [PMID: 12574632]
[110]
Cleeter, M.W.; Cooper, J.M.; Darley-Usmar, V.M.; Moncada, S.; Schapira, A.H. Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett., 1994, 345(1), 50-54.
[http://dx.doi.org/10.1016/0014-5793(94)00424-2] [PMID: 8194600]
[111]
Clementi, E.; Brown, G.C.; Feelisch, M.; Moncada, S. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc. Natl. Acad. Sci. USA, 1998, 95(13), 7631-7636.
[http://dx.doi.org/10.1073/pnas.95.13.7631] [PMID: 9636201]
[112]
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(4), 605-616.
[http://dx.doi.org/10.1002/pmic.200600728] [PMID: 17309106]
[113]
Chen, G.; Chen, K.S.; Knox, J.; Inglis, J.; Bernard, A.; Martin, S.J.; Justice, A.; McConlogue, L.; Games, D.; Freedman, S.B.; Morris, R.G. A learning deficit related to age and beta-amyloid plaques in a mouse model of Alzheimer’s disease. Nature, 2000, 408(6815), 975-979.
[http://dx.doi.org/10.1038/35050103] [PMID: 11140684]
[114]
Reddy, P.H.; Manczak, M.; Yin, X. Mitochondria-division inhibitor 1 protects against amyloid-β induced mitochondrial fragmentation and synaptic damage in alzheimer’s disease. J. Alzheimers Dis., 2017, 58(1), 147-162.
[http://dx.doi.org/10.3233/JAD-170051] [PMID: 28409745]
[115]
Hollenbeck, P.J.; Saxton, W.M. The axonal transport of mitochondria. J. Cell Sci., 2005, 118(Pt 23), 5411-5419.
[http://dx.doi.org/10.1242/jcs.02745] [PMID: 16306220]
[116]
Guo, X.; Macleod, G.T.; Wellington, A.; Hu, F.; Panchumarthi, S.; Schoenfield, M.; Marin, L.; Charlton, M.P.; Atwood, H.L.; Zinsmaier, K.E. The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron, 2005, 47(3), 379-393.
[http://dx.doi.org/10.1016/j.neuron.2005.06.027] [PMID: 16055062]
[117]
Glater, E.E.; Megeath, L.J.; Stowers, R.S.; Schwarz, T.L. Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent. J. Cell Biol., 2006, 173(4), 545-557.
[http://dx.doi.org/10.1083/jcb.200601067] [PMID: 16717129]
[118]
Fransson, S.; Ruusala, A.; Aspenström, P. The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochem. Biophys. Res. Commun., 2006, 344(2), 500-510.
[http://dx.doi.org/10.1016/j.bbrc.2006.03.163] [PMID: 16630562]
[119]
Stowers, R.S.; Megeath, L.J.; Górska-Andrzejak, J.; Meinertzhagen, I.A.; Schwarz, T.L. Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron, 2002, 36(6), 1063-1077.
[http://dx.doi.org/10.1016/S0896-6273(02)01094-2] [PMID: 12495622]
[120]
Stokin, G.B.; Lillo, C.; Falzone, T.L.; Brusch, R.G.; Rockenstein, E.; Mount, S.L.; Raman, R.; Davies, P.; Masliah, E.; Williams, D.S.; Goldstein, L.S. Axonopathy and transport deficits early in the pathogenesis of Alzheimer’s disease. Science, 2005, 307(5713), 1282-1288.
[http://dx.doi.org/10.1126/science.1105681] [PMID: 15731448]
[121]
Iijima-Ando, K.; Hearn, S.A.; Shenton, C.; Gatt, A.; Zhao, L.; Iijima, K. Mitochondrial mislocalization underlies Abeta42-induced neuronal dysfunction in a Drosophila model of Alzheimer’s disease. PLoS One, 2009, 4(12) e8310
[http://dx.doi.org/10.1371/journal.pone.0008310] [PMID: 20016833]
[122]
Quintanilla, R.A.; von Bernhardi, R.; Godoy, J.A.; Inestrosa, N.C.; Johnson, G.V. Phosphorylated tau potentiates Aβ-induced mitochondrial damage in mature neurons. Neurobiol. Dis., 2014, 71(C), 260-269.
[http://dx.doi.org/10.1016/j.nbd.2014.08.016] [PMID: 25134729]
[123]
Stoothoff, W.; Jones, P.B.; Spires-Jones, T.L.; Joyner, D.; Chhabra, E.; Bercury, K.; Fan, Z.; Xie, H.; Bacskai, B.; Edd, J.; Irimia, D.; Hyman, B.T. Differential effect of three-repeat and four-repeat tau on mitochondrial axonal transport. J. Neurochem., 2009, 111(2), 417-427.
[http://dx.doi.org/10.1111/j.1471-4159.2009.06316.x] [PMID: 19686388]
[124]
Vossel, K.A.; Xu, J.C.; Fomenko, V.; Miyamoto, T.; Suberbielle, E.; Knox, J.A.; Ho, K.; Kim, D.H.; Yu, G.Q.; Mucke, L. Tau reduction prevents Aβ-induced axonal transport deficits by blocking activation of GSK3β. J. Cell Biol., 2015, 209(3), 419-433.
[http://dx.doi.org/10.1083/jcb.201407065] [PMID: 25963821]
[125]
Shahpasand, K.; Uemura, I.; Saito, T.; Asano, T.; Hata, K.; Shibata, K.; Toyoshima, Y.; Hasegawa, M.; Hisanaga, S. Regulation of mitochondrial transport and inter-microtubule spacing by tau phosphorylation at the sites hyperphosphorylated in Alzheimer’s disease. J. Neurosci., 2012, 32(7), 2430-2441.
[http://dx.doi.org/10.1523/JNEUROSCI.5927-11.2012] [PMID: 22396417]
[126]
Niewidok, B.; Igaev, M.; Sündermann, F.; Janning, D.; Bakota, L.; Brandt, R. Presence of a carboxy-terminal pseudorepeat and disease-like pseudohyperphosphorylation critically influence tau’s interaction with microtubules in axon-like processes. Mol. Biol. Cell, 2016, 27(22), 3537-3549.
[http://dx.doi.org/10.1091/mbc.e16-06-0402] [PMID: 27582388]
[127]
Jonas, E.A.; Porter, G.A., Jr; Beutner, G.; Mnatsakanyan, N.; Alavian, K.N. Cell death disguised: The mitochondrial permeability transition pore as the c-subunit of the F(1)F(O) ATP synthase. Pharmacol. Res., 2015, 99, 382-392.
[http://dx.doi.org/10.1016/j.phrs.2015.04.013] [PMID: 25956324]
[128]
Pérez, M.J.; Quintanilla, R.A. Development or disease: duality of the mitochondrial permeability transition pore. Dev. Biol., 2017, 426(1), 1-7.
[http://dx.doi.org/10.1016/j.ydbio.2017.04.018] [PMID: 28457864]
[129]
Bonora, M.; Bononi, A.; De Marchi, E.; Giorgi, C.; Lebiedzinska, M.; Marchi, S.; Patergnani, S.; Rimessi, A.; Suski, J.M.; Wojtala, A.; Wieckowski, M.R.; Kroemer, G.; Galluzzi, L.; Pinton, P. Role of the c subunit of the FO ATP synthase in mitochondrial permeability transition. Cell Cycle, 2013, 12(4), 674-683.
[http://dx.doi.org/10.4161/cc.23599] [PMID: 23343770]
[130]
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(10), 1097-1105.
[http://dx.doi.org/10.1038/nm.1868] [PMID: 18806802]
[131]
Du, H.; Guo, L.; Zhang, W.; Rydzewska, M.; Yan, S. Cyclophilin D deficiency improves mitochondrial function and learning/memory in aging Alzheimer disease mouse model. Neurobiol. Aging, 2011, 32(3), 398-406.
[http://dx.doi.org/10.1016/j.neurobiolaging.2009.03.003] [PMID: 19362755]
[132]
Du, H.; Yan, S.S. Mitochondrial permeability transition pore in Alzheimer’s disease: cyclophilin D and amyloid beta. Biochim. Biophys. Acta, 2010, 1802(1), 198-204.
[http://dx.doi.org/10.1016/j.bbadis.2009.07.005] [PMID: 19616093]
[133]
Guo, L.; Du, H.; Yan, S.; Wu, X.; McKhann, G.M.; Chen, J.X.; Yan, S.S. Cyclophilin D deficiency rescues axonal mitochondrial transport in Alzheimer’s neurons. PLoS One, 2013, 8(1) e54914
[http://dx.doi.org/10.1371/journal.pone.0054914] [PMID: 23382999]
[134]
Gauba, E.; Chen, H.; Guo, L.; Du, H. Cyclophilin D deficiency attenuates mitochondrial F1Fo ATP synthase dysfunction via OSCP in Alzheimer’s disease. Neurobiol. Dis., 2019, 121, 138-147.
[http://dx.doi.org/10.1016/j.nbd.2018.09.020] [PMID: 30266287]
[135]
Pérez, M.J.; Ponce, D.P.; Osorio-Fuentealba, C.; Behrens, M.I.; Quintanilla, R.A. Mitochondrial bioenergetics is altered in fibroblasts from patients with sporadic alzheimer’s disease. Front. Neurosci., 2017, 11, 553-553.
[http://dx.doi.org/10.3389/fnins.2017.00553] [PMID: 29056898]
[136]
Pérez, M.J.; Ponce, D.P.; Aránguiz, A.; Behrens, M.I.; Quintanilla, R.A. Mitochondrial permeability transition pore contributes to mitochondrial dysfunction in fibroblasts of patients with sporadic Alzheimer’s disease. Redox Biol., 2018, 19, 290-300.
[http://dx.doi.org/10.1016/j.redox.2018.09.001] [PMID: 30199818]
[137]
Johri, A.; Beal, M.F. Mitochondrial dysfunction in neurodegenerative diseases. J. Pharmacol. Exp. Ther., 2012, 342(3), 619-630.
[http://dx.doi.org/10.1124/jpet.112.192138] [PMID: 22700435]
[138]
Pérez, M.J.; Jara, C.; Quintanilla, R.A. Contribution of tau pathology to mitochondrial impairment in neurodegeneration. Front. Neurosci., 2018, 12, 441.
[http://dx.doi.org/10.3389/fnins.2018.00441] [PMID: 30026680]
[139]
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. USA, 2009, 106(34), 14670-14675.
[http://dx.doi.org/10.1073/pnas.0903563106] [PMID: 19667196]
[140]
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(9), 3017-3023.
[http://dx.doi.org/10.1523/JNEUROSCI.21-09-03017.2001] [PMID: 11312286]
[141]
Li, X.C.; Hu, Y.; Wang, Z.H.; Luo, Y.; Zhang, Y.; Liu, X.P.; Feng, Q.; Wang, Q.; Ye, K.; Liu, G.P.; Wang, J.Z. Human wild-type full-length tau accumulation disrupts mitochondrial dynamics and the functions via increasing mitofusins. Sci. Rep., 2016, 6, 24756.
[http://dx.doi.org/10.1038/srep24756] [PMID: 27099072]
[142]
Schulz, K.L.; Eckert, A.; Rhein, V.; Mai, S.; Haase, W.; Reichert, A.S.; Jendrach, M.; Müller, W.E.; Leuner, K. A new link to mitochondrial impairment in tauopathies. Mol. Neurobiol., 2012, 46(1), 205-216.
[http://dx.doi.org/10.1007/s12035-012-8308-3] [PMID: 22847631]
[143]
Manczak, M.; Reddy, P.H. Abnormal interaction between the mitochondrial fission protein Drp1 and hyperphosphorylated tau in Alzheimer’s disease neurons: implications for mitochondrial dysfunction and neuronal damage. Hum. Mol. Genet., 2012, 21(11), 2538-2547.
[http://dx.doi.org/10.1093/hmg/dds072] [PMID: 22367970]
[144]
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(25), 23802-23814.
[http://dx.doi.org/10.1074/jbc.M500356200] [PMID: 15831501]
[145]
Lopes, S.; Teplytska, L.; Vaz-Silva, J.; Dioli, C.; Trindade, R.; Morais, M. Tau deletion prevents stress-induced dendritic atrophy in prefrontal cortex: Role of synaptic mitochondria. Cereb. Cortex, 2016, 27(4), 2580-2591.
[http://dx.doi.org/10.1093/cercor/bhw057] [PMID: 27073221]
[146]
Jara, C.; Aránguiz, A.; Cerpa, W.; Tapia-Rojas, C.; Quintanilla, R.A. Genetic ablation of tau improves mitochondrial function and cognitive abilities in the hippocampus. Redox Biol., 2018, 18, 279-294.
[http://dx.doi.org/10.1016/j.redox.2018.07.010] [PMID: 30077079]
[147]
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(4), 1085-1090.
[http://dx.doi.org/10.1111/j.1460-9568.2006.04986.x] [PMID: 16930434]
[148]
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(6) e536
[http://dx.doi.org/10.1371/journal.pone.0000536] [PMID: 17579710]
[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. USA, 2009, 106(47), 20057-20062.
[http://dx.doi.org/10.1073/pnas.0905529106] [PMID: 19897719]
[150]
Liska, D.J. The detoxification enzyme systems. Altern. Med. Rev., 1998, 3(3), 187-198.
[PMID: 9630736]
[151]
Itoh, K.; Chiba, T.; Takahashi, S.; Ishii, T.; Igarashi, K.; Katoh, Y.; Oyake, T.; Hayashi, N.; Satoh, K.; Hatayama, I.; Yamamoto, M.; Nabeshima, Y. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun., 1997, 236(2), 313-322.
[http://dx.doi.org/10.1006/bbrc.1997.6943] [PMID: 9240432]
[152]
Venugopal, R.; Jaiswal, A.K. Nrf1 and Nrf2 positively and c-Fos and Fra1 negatively regulate the human antioxidant response element-mediated expression of NAD(P)H:quinone oxidoreductase1 gene. Proc. Natl. Acad. Sci. USA, 1996, 93(25), 14960-14965.
[http://dx.doi.org/10.1073/pnas.93.25.14960] [PMID: 8962164]
[153]
Dodson, M.; de la Vega, M.R.; Cholanians, A.B.; Schmidlin, C.J.; Chapman, E.; Zhang, D.D. Modulating NRF2 in disease: Timing is everything. Annu. Rev. Pharmacol. Toxicol., 2019, 59, 555-575.
[http://dx.doi.org/10.1146/annurev-pharmtox-010818-021856] [PMID: 30256716]
[154]
Jo, C.; Gundemir, S.; Pritchard, S.; Jin, Y.N.; Rahman, I.; Johnson, G.V. Nrf2 reduces levels of phosphorylated tau protein by inducing autophagy adaptor protein NDP52. Nat. Commun., 2014, 5, 3496.
[http://dx.doi.org/10.1038/ncomms4496] [PMID: 24667209]
[155]
Lavich, I.C.; de Freitas, B.S.; Kist, L.W.; Falavigna, L.; Dargél, V.A.; Köbe, L.M.; Aguzzoli, C.; Piffero, B.; Florian, P.Z.; Bogo, M.R.; de Lima, M.N.; Schröder, N. Sulforaphane rescues memory dysfunction and synaptic and mitochondrial alterations induced by brain iron accumulation. Neuroscience, 2015, 301, 542-552.
[http://dx.doi.org/10.1016/j.neuroscience.2015.06.025] [PMID: 26112383]
[156]
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(12), 548-554.
[http://dx.doi.org/10.1016/S1471-4914(01)02173-6] [PMID: 11733217]
[157]
Maccioni, R.B.; Muñoz, J.P.; Barbeito, L. The molecular bases of Alzheimer’s disease and other neurodegenerative disorders. Arch. Med. Res., 2001, 32(5), 367-381.
[http://dx.doi.org/10.1016/S0188-4409(01)00316-2] [PMID: 11578751]
[158]
Sayre, L.M.; Smith, M.A.; Perry, G. Chemistry and biochemistry of oxidative stress in neurodegenerative disease. Curr. Med. Chem., 2001, 8(7), 721-738.
[http://dx.doi.org/10.2174/0929867013372922] [PMID: 11375746]
[159]
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, 60(8), 759-767.
[http://dx.doi.org/10.1093/jnen/60.8.759] [PMID: 11487050]
[160]
McManus, M.J.; Murphy, M.P.; Franklin, J.L. The mitochondria-targeted antioxidant MitoQ prevents loss of spatial memory retention and early neuropathology in a transgenic mouse model of Alzheimer’s disease. J. Neurosci., 2011, 31(44), 15703-15715.
[http://dx.doi.org/10.1523/JNEUROSCI.0552-11.2011] [PMID: 22049413]
[161]
Amadoro, G.; Corsetti, V.; Atlante, A.; Florenzano, F.; Capsoni, S.; Bussani, R.; Mercanti, D.; Calissano, P. Interaction between NH(2)-tau fragment and Aβ in Alzheimer’s disease mitochondria contributes to the synaptic deterioration. Neurobiol. Aging, 2012, 33(4), 833.e1-833.e25.
[http://dx.doi.org/10.1016/j.neurobiolaging.2011.08.001] [PMID: 21958963]
[162]
Cieri, D.; Vicario, M.; Vallese, F.; D’Orsi, B.; Berto, P.; Grinzato, A.; Catoni, C.; De Stefani, D.; Rizzuto, R.; Brini, M.; Calì, T. Tau localises within mitochondrial sub-compartments and its caspase cleavage affects ER-mitochondria interactions and cellular Ca2+ handling. Biochim. Biophys. Acta Mol. Basis Dis., 2018, 1864(10), 3247-3256.
[http://dx.doi.org/10.1016/j.bbadis.2018.07.011] [PMID: 30006151]
[163]
Baines, C.P.; Kaiser, R.A.; Purcell, N.H.; Blair, N.S.; Osinska, H.; Hambleton, M.A.; Brunskill, E.W.; Sayen, M.R.; Gottlieb, R.A.; Dorn, G.W.; Robbins, J.; Molkentin, J.D. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature, 2005, 434(7033), 658-662.
[http://dx.doi.org/10.1038/nature03434] [PMID: 15800627]
[164]
Hom, J.R.; Quintanilla, R.A.; Hoffman, D.L.; de Mesy Bentley, K.L.; Molkentin, J.D.; Sheu, S.S.; Porter, G.A., Jr The permeability transition pore controls cardiac mitochondrial maturation and myocyte differentiation. Dev. Cell, 2011, 21(3), 469-478.
[http://dx.doi.org/10.1016/j.devcel.2011.08.008] [PMID: 21920313]
[165]
Briston, T.; Selwood, D.L.; Szabadkai, G.; Duchen, M.R. Mitochondrial Permeability Transition: A Molecular Lesion with Multiple Drug Targets. Trends Pharmacol. Sci., 2019, 40(1), 50-70.
[http://dx.doi.org/10.1016/j.tips.2018.11.004] [PMID: 30527591]
[166]
Camilleri, A.; Ghio, S.; Caruana, M.; Weckbecker, D.; Schmidt, F.; Kamp, F. Tau-induced mitochondrial membrane perturbation is dependent upon cardiolipin BBA - Biomembranes, 2020, 1862(2), 183064..
[http://dx.doi.org/10.1016/j.bbamem.2019.183064]

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