Mitochondrial enzyme expression in the hippocampus in relation to Alzheimer-type pathology
Abstract
Recent reports have suggested that mitochondrial dysfunction may contribute to the progression of the pathology of Alzheimer's disease (AD). However, both increases and decreases in the activity of cytochrome oxidase have been described in the hippocampi of AD patients. In this study we used immunohistochemistry and quantitative autoradiographic methods to study the expression pattern of two cytochrome oxidase subunit proteins (nuclear-encoded COX IV and mitochondrial-encoded COX I) in the hippocampus in relation to the development of AD-type pathology. We found heterogeneous expression of both COX subunits in AD with an increased expression of both subunit proteins in healthy, non-tangle-bearing, neurones but absence of both subunit proteins in tangle-bearing neurones. Levels of COX IV but not of COX I were related to the amount of hyperphosphorylated tau accumulated in the same hippocampal region but not to the amount of amyloid deposited in sporadic AD. In Down's syndrome COX I and COX IV were similarly increased in the presence of AD pathology in non-tangle-bearing neurones. However, in these cases levels of enzyme expression were correlated to the amount of amyloid accumulation but not the amount of hyperphosphorylated tau in the hippocampus. We believe that heterogeneity of expression of mitochondrial enzyme proteins between neurones may contribute to the conflicting conclusions in previous reports regarding relative levels of cytochrome oxidase activity in the hippocampus in AD. We hypothesise that the increased mitochondrial enzyme expression in healthy-appearing neurones of AD brains may represent a physiological response to increased functional demand on surviving neurones as a consequence of AD-related neuronal pathology.
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In at least some hippocampal neurons COX subunit protein levels increase.
“In at least some hippocampal neurons COX subunit protein levels also increase [140].”
From Brain aging, Alzheimer's disease, and mitochondria (2011) · cites this paper as [140]
Cites
Aging, energy, and oxidative stress in neurodegenerative diseases
Beal, M. F. (1995) · Annals of Neurology · doi:10.1002/ana.410380304 · Cited by 1,434 · see citing works
Cytochrome oxidase: an endogenous metabolic marker for neuronal activity
Wong-Riley, M. T. T. (1989) · Trends in Neurosciences · doi:10.1016/0166-2236(89)90165-3 · Cited by 1,238 · see citing works
Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain
Mecocci, P., MacGarvey, U., Kaufman, A. E., Koontz, D., Shoffner, J. M., Wallace, D. C., & Beal, M. F. (1993) · Annals of Neurology · doi:10.1002/ana.410340416 · Cited by 757 · see citing works
Evolution of the neuropathology of Alzheimer's disease
Braak, H., & Braak, E. (1996) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1996.tb05866.x · Cited by 710 · see citing works
Brain cytochrome oxidase in Alzheimer's disease
Kish, S. J., Bergeron, C., Rajput, A., Dozic, S., Mastrogiacomo, F., Chang, L., Wilson, J. M., DiStefano, L. M., & Nobrega, J. N. (1992) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1992.tb09439.x · Cited by 537 · see citing works
Cortical Cytochrome Oxidase Activity Is Reduced in Alzheimer's Disease
Mutisya, E. M., Bowling, A. C., & Beal, M. F. (1994) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1994.63062179.x · Cited by 531 · see citing works
Impairment in mitochondrial cytochrome oxidase gene expression in Alzheimer disease.
Chandrasekaran, K., Giordano, T., Brady, D., Stoll, J., Martin, L. J., & Rapoport, S. (1994) · Brain Research. Molecular Brain Research · doi:10.1016/0169-328x(94)90147-3 · Cited by 221 · see citing works
Rapidly progressing atrophy of medial temporal lobe in Alzheimer's disease
Jobst, K. A., Smith, A. D., Szatmari, M., Esiri, M. M., Jaskowski, A., Hindley, N., McDonald, B., & Molyneux, A. J. (1994) · The Lancet · doi:10.1016/s0140-6736(94)92028-1 · Cited by 215 · see citing works
Threshold Effects and Control of Oxidative Phosphorylation in Nonsynaptic Rat Brain Mitochondria
Davey, G. P., & Clark, J. B. (1996) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1996.66041617.x · Cited by 209 · see citing works
Magistretti, P. J., & Pellerin, L. (1996) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1996.tb34449.x · Cited by 159 · see citing works
Cavelier, L. B., JAZIN, E. E., Eriksson, I., Prince, J. A., Båve, U., Oreland, L., & Gyllensten, U. B. (1995) · Genomics · doi:10.1006/geno.1995.1234 · Cited by 157 · see citing works
Cytochrome C Oxidase in Alzheimer's Disease Brain: Purification and Characterization
Parker, W. D., & Parks, J. K. (1995) · Neurology · doi:10.1212/wnl.45.3.482 · Cited by 142 · see citing works
Takahashi, M., Tomizawa, K., Kato, R., Sato, K., Uchida, T., Fujita, S., & Imahori, K. (1994) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1994.63010245.x · Cited by 129 · see citing works
Cytochrome c Oxidase Deficiency
DiMauro, S., Lombès, A., Nakase, H., Mita, S., Fabrizi, G. M., Bonilla, E., Miranda, A. F., Vivo, D. C. D., & Schon, E. A. (1990) · Pediatric Research · doi:10.1203/00006450-199011000-00025 · Cited by 116 · see citing works
Hevner, R., & Wong-Riley, M. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-11-03884.1989 · Cited by 114 · see citing works
Simonian, N. A., & Hyman, B. T. (1994) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199409000-00010 · Cited by 108 · see citing works
Hevner, R., & Wong-Riley, M. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-07-01942.1991 · Cited by 100 · see citing works
Functional Alterations in Alzheimerʼs Disease
Simonian, N. A., & Hyman, B. T. (1993) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199311000-00004 · Cited by 89 · see citing works
Oxidative metabolism deficiencies in brains of patients with Alzheimer's disease
Hoyer, S. (1996) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1996.tb05868.x · Cited by 88 · see citing works
Neuronal activity and early neurofibrillary tangles in Alzheimer's disease
Hatanpaa, K. J., Brady, D. R., Stoll, J., Rapoport, S. I., & Chandrasekaran, K. (1996) · Annals of Neurology · doi:10.1002/ana.410400310 · Cited by 67 · see citing works
Altered mitochondrial membrane fluidity in AD brain
Mecocci, P., Cherubini, A., Beal, M. F., Cecchetti, R., Chionne, F., Polidori, M. C., Romano, G., & Senin, U. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)12509-x · Cited by 56 · see citing works
Reichmann, H., Fhirke, S., Hebenstreit, G. F., Schrubar, H., & Riederer, P. F. (1993) · Journal of Neurology · doi:10.1007/bf00839971 · Cited by 51 · see citing works
Age-Associated Changes of Mitochondrial Translation and Respiratory Function in Mouse Brain
Takai, D., Inoue, K., Shisa, H., Kagawa, Y., & Hayashi, J. (1995) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1995.2826 · Cited by 38 · see citing works
Richard, S., Brion, J., Couck, A. M., & Flament-Durand, J. (1989) · PubMed · Cited by 31 · see citing works
Nicoletti, V. G., Tendi, E. A., Lalicata, C., Reale, S., Costa, A., Villa, R. F., Ragusa, N., & Stella, A. M. G. (1995) · Neurochemical Research · doi:10.1007/bf00970595 · Cited by 31 · see citing works
Functional alterations in neural circuits in Alzheimer's disease
Simonian, N. A., & Hyman, B. T. (1995) · Neurobiology of Aging · doi:10.1016/0197-4580(95)00034-c · Cited by 23 · see citing works
Liu, S., & Wong‐Riley, M. T. T. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00043-i · Cited by 22 · see citing works
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Wallace, D. C. (2005) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.110304.095751 · Cited by 3,185 · see citing works
Oxidative stress and mitochondrial dysfunction in Alzheimer’s disease
Wang, X., Wang, W., Li, L., Perry, G., Lee, H.-G., & Zhu, X. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.10.015 · Cited by 1,357 · see citing works
The Alzheimer’s disease mitochondrial cascade hypothesis: progress and perspectives
Swerdlow, R. H., Burns, J. M., & Khan, S. M. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.09.010 · Cited by 786 · see citing works
History and progress of hypotheses and clinical trials for Alzheimer’s disease
Liu, P.-P., Xie, Y., Meng, X.-Y., & Kang, J.-S. (2019) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-019-0063-8 · Cited by 723 · see citing works
Neurofibrillary Tangles, Amyloid, and Memory in Aging and Mild Cognitive Impairment
Guillozet-Bongaarts, A. L., Weıntraub, S., Mash, D. C., & Mesulam, M. M. (2003) · Archives of Neurology · doi:10.1001/archneur.60.5.729 · Cited by 572 · see citing works
Coskun, P. E., Beal, M. F., & Wallace, D. C. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403649101 · Cited by 556 · see citing works
Oxidative stress signalling in Alzheimer's disease
Zhu, X., Raina, A. K., Lee, H., Casadesús, G., Smith, M. A., & Perry, G. L. (2004) · Brain Research · doi:10.1016/j.brainres.2004.01.012 · Cited by 390 · see citing works
Oxidative Stress Signaling in Alzheimers Disease
Su, B., Wang, X., Nunomura, A., Moreira, P., Lee, H.-G., Perry, G., Smith, M., & Zhu, X. (2008) · Current Alzheimer Research · doi:10.2174/156720508786898451 · Cited by 344 · see citing works
Causes of oxidative stress in Alzheimer disease
Zhu, X., Su, B., Wang, X., Smith, M. A., & Perry, G. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7218-4 · Cited by 336 · see citing works
Evangelou, N. (2001) · Brain · doi:10.1093/brain/124.9.1813 · Cited by 324 · see citing works
Mitochondrial Dysfunctions in Neurodegenerative Diseases: Relevance to Alzheimer’s Disease
Hroudová, J., Singh, N., & Fišar, Z. (2014) · BioMed Research International · doi:10.1155/2014/175062 · Cited by 319 · see citing works
Brain aging, Alzheimer's disease, and mitochondria
Swerdlow, R. H. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2011.08.012 · Cited by 306 · see citing works
“In at least some hippocampal neurons COX subunit protein levels also increase [140].”
BackgroundAbnormal mitochondrial dynamics and neurodegenerative diseases
Su, B., Wang, X., Zheng, L., Perry, G. L., Smith, M. A., & Zhu, X. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2009.09.013 · Cited by 289 · see citing works
Mitochondrial DNA damage as a mechanism of cell loss in Alzheimer's disease
de la Monte, S. M., Luong, T., Neely, T. R., Robinson, D., & Wands, J. R. (2000) · Laboratory Investigation · doi:10.1038/labinvest.3780140 · Cited by 227 · see citing works
Bhatia, V., & Sharma, S. (2020) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2020.117253 · Cited by 226 · see citing works
Swerdlow, R. H. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4149 · Cited by 203 · see citing works
Mitochondrial dysfunction: the missing link between aging and sporadic Alzheimer’s disease
Grimm, A., Friedland, K., & Eckert, A. (2015) · Biogerontology · doi:10.1007/s10522-015-9618-4 · Cited by 182 · see citing works
Driver, J. A. (2014) · Biogerontology · doi:10.1007/s10522-014-9523-2 · Cited by 182 · see citing works
Freeman, L. R., & Keller, J. N. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2011.12.009 · Cited by 173 · see citing works
Coskun, P. E., Wyrembak, J., Derbereva, O., Melkonian, G., Doran, E. W., Lott, I. T., Head, E., Cotman, C. W., & Wallace, D. C. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-100351 · Cited by 158 · see citing works
Hua, T., Kiran, S., Li, Y., & Sang, Q. A. (2022) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2022.128884 · Cited by 155 · see citing works
Oxidative Imbalance in Alzheimer's Disease
Zhu, X., Lee, H., Casadesús, G., Ávila, J., Drew, K. L., Perry, G. L., & Smith, M. A. (2005) · Molecular Neurobiology · doi:10.1385/mn:31:1-3:205 · Cited by 146 · see citing works
Filippini, N., Rao, A., Wetten, S., Gibson, R. A., Borrie, M., Guzman, D., Kertesz, A., Loy-English, I., Williams, J., Nichols, T., et al. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.10.003 · Cited by 143 · see citing works
Alzheimer's disease: the amyloid hypothesis and the Inverse Warburg effect
Demetrius, L., Magistretti, P. J., & Pellerin, L. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2014.00522 · Cited by 142 · see citing works
Birnbaum, J. H., Wanner, D., Gietl, A. F., Saake, A., Kündig, T. M., Hock, C., Nitsch, R. M., & Tackenberg, C. (2018) · Stem Cell Research · doi:10.1016/j.scr.2018.01.019 · Cited by 135 · see citing works
Silva, D. F., Selfridge, J. E., Lu, J., E, L., Roy, N., Hutfles, L., Burns, J. M., Michaelis, E. K., Yan, S., Cardoso, S. M., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt247 · Cited by 133 · see citing works
Yoo, B. C., Fountoulakis, M., Cairns, N. J., & Lübec, G. (2001) · Electrophoresis · doi:10.1002/1522-2683(200101)22:1 · Cited by 129 · see citing works
Mitochondria in Alzheimer's disease
Swerdlow, R. H., & Kish, S. J. (2002) · International review of neurobiology · doi:10.1016/s0074-7742(02)53013-0 · Cited by 126 · see citing works
Mitochondrial failures in Alzheimer's disease
Zhu, X., Smith, M. A., Perry, G. L., & Aliev, G. M. (2004) · American Journal of Alzheimer s Disease & Other Dementias® · doi:10.1177/153331750401900611 · Cited by 120 · see citing works
Mitochondrial Dynamics in Alzheimerʼs Disease
Bonda, D., Wang, X., Perry, G. L., Smith, M. A., & Zhu, X. (2010) · Drugs & Aging · doi:10.2165/11532140-000000000-00000 · Cited by 106 · see citing works
Preciados, M., Yoo, C., & Roy, D. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17122086 · Cited by 105 · see citing works
Salminen, A., Haapasalo, A., Kauppinen, A., Kaarniranta, K., Soininen, H. S., & Hiltunen, M. O. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.05.001 · Cited by 105 · see citing works
Signal Transduction Cascades Associated with Oxidative Stress in Alzheimer's Disease
Petersen, R. B., Nunomura, A., Lee, H., Casadesús, G., Perry, G. L., Smith, M. A., & Zhu, X. (2007) · Journal of Alzheimer s Disease · doi:10.3233/jad-2007-11202 · Cited by 99 · see citing works
Amadoro, G., Corsetti, V., Atlante, A., Florenzano, F., Capsoni, S., Bussani, R., Mercanti, D., & Calissano, P. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.08.001 · Cited by 94 · see citing works
Mitochondrial Abnormalities in Alzheimer’s Disease
Silva, D. F., Selfridge, J. E., Lu, J., E, L., Cardoso, S. M., & Swerdlow, R. H. (2012) · Advances in Pharmacology · doi:10.1016/b978-0-12-394816-8.00003-9 · Cited by 86 · see citing works
Trimmer, P. A., Keeney, P. M., Borland, M. K., Simon, F. A., Almeida, J., Swerdlow, R. H., Parks, J. K., Parker, W. D., & Bennett, J. P. (2003) · Neurobiology of Disease · doi:10.1016/j.nbd.2003.09.011 · Cited by 84 · see citing works
The Alzheimer’s Disease Mitochondrial Cascade Hypothesis: A Current Overview
Swerdlow, R. H. (2023) · Journal of Alzheimer s Disease · doi:10.3233/jad-221286 · Cited by 83 · see citing works
ATP Synthase and Mitochondrial Bioenergetics Dysfunction in Alzheimer’s Disease
Patro, S., Ratna, S., Yamamoto, H. A., Ebenezer, A. T., Ferguson, D. S., Kaur, A., McIntyre, B. C., Snow, R., & Solesio, M. E. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222011185 · Cited by 74 · see citing works
Oxidative Stress and Mitochondrial Dysfunction in Down’s Syndrome: Relevance to Aging and Dementia
Coskun, P. E., & Busciglio, J. A. (2012) · Current Gerontology and Geriatrics Research · doi:10.1155/2012/383170 · Cited by 73 · see citing works
Neuronal plasticity and stressor toxicity during aging
Brewer, G. J. (2000) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00121-2 · Cited by 71 · see citing works
Membrane-disordering effects of β-amyloid peptides
Müller, W. E. G., Kirsch, C., & Eckert, G. P. (2001) · Biochemical Society Transactions · doi:10.1042/bst0290617 · Cited by 69 · see citing works
Effects of aging and β-amyloid on the properties of brain synaptic and mitochondrial membranes
Eckert, G. P., Wood, W. G., & Müller, W. E. G. (2001) · Journal of Neural Transmission · doi:10.1007/s007020170024 · Cited by 57 · see citing works
Hypoxia and GABA shunt activation in the pathogenesis of Alzheimer's disease
Salminen, A., Jouhten, P., Sarajärvi, T., Haapasalo, A., & Hiltunen, M. O. (2015) · Neurochemistry International · doi:10.1016/j.neuint.2015.11.005 · Cited by 54 · see citing works
Redox signaling and metabolism in Alzheimer's disease
Holubiec, M. I., Gellert, M., & Hanschmann, E.-M. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.1003721 · Cited by 52 · see citing works
Relationship Between Mitochondria and α-Synuclein
Reeve, A. K. (2012) · Archives of Neurology · doi:10.1001/archneurol.2011.2675 · Cited by 49 · see citing works
Sex differences in Alzheimer’s disease: metabolic reprogramming and therapeutic intervention
Demetrius, L., Eckert, A., & Grimm, A. (2021) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2021.09.004 · Cited by 50 · see citing works
Cerebrometabolic abnormalities in Alzheimer's disease
Blass, J. P. (2003) · Neurological Research · doi:10.1179/016164103101201995 · Cited by 49 · see citing works
Brain pyrimidine nucleotide synthesis and Alzheimer disease
Pesini, A., Iglesias, E., Bayona‐Bafaluy, M. P., Garrido-Pérez, N., Meade, P., Gaudó, P., Jiménez-Salvador, I., Andrés‐Benito, P., Montoya, J., Ferrer, I., et al. (2019) · Aging · doi:10.18632/aging.102328 · Cited by 46 · see citing works
Evidence of oxidative stress-induced BNIP3 expression in amyloid beta neurotoxicity
Zhang, S., Zhang, Z., Sandhu, G., Ma, X., Yang, X., Geiger, J. D., & Kong, J. (2007) · Brain Research · doi:10.1016/j.brainres.2006.12.086 · Cited by 43 · see citing works
Rapoport, S. I. (2003) · Neurotoxicity Research · doi:10.1007/bf03033167 · Cited by 41 · see citing works
Dietary Lipids in the Aetiology of Alzheimer???s Disease
Cooper, J. L. (2003) · Drugs & Aging · doi:10.2165/00002512-200320060-00001 · Cited by 41 · see citing works
Strazielle, C., Jazi, R., Verdier, Y., Qian, S., & Lalonde, R. (2009) · Neurochemistry International · doi:10.1016/j.neuint.2009.08.005 · Cited by 41 · see citing works
Krügel, U., Bigl, V., Eschrich, K., & Bigl, M. (2001) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(01)00010-7 · Cited by 36 · see citing works
Metal attenuating therapies in neurodegenerative disease
Mot, A. I., Wedd, A. G., Sinclair, L., Brown, D. R., Collins, S. J., & Brazier, M. W. (2011) · Expert Review of Neurotherapeutics · doi:10.1586/ern.11.170 · Cited by 31 · see citing works
Mitochondrial DNA Manipulations Affect Tau Oligomerization
Weidling, I. W., Wilkins, H., Koppel, S. J., Hutfles, L. J., Wang, X., Kalani, A., Menta, B. W., Ryan, B. J., Ortiz, J. P., Gamblin, T. C., et al. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-200286 · Cited by 31 · see citing works
Somatostatin and the pathophysiology of Alzheimer’s disease
Almeida, V. N. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102270 · Cited by 30 · see citing works
Zhou, L., Diefenbach, E., Crossett, B., Tran, S. L., Ng, T., Rizos, H., Rua, R., Wang, B., Kapur, A., Gandhi, K. S., et al. (2010) · Molecular Neurodegeneration · doi:10.1186/1750-1326-5-27 · Cited by 30 · see citing works
Strazielle, C., Sturchler, C., Staufenbiel, M., & Lalonde, R. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00037-x · Cited by 30 · see citing works
Mechanisms of neuronal death in Down’s syndrome
Nagy, Z. (1999) · Springer eBooks · doi:10.1007/978-3-7091-6380-1_15 · Cited by 29 · see citing works
Butterfield, D. A., Favia, M., Spera, I., Campanella, A., Lanza, M., & Castegna, A. (2022) · Molecules · doi:10.3390/molecules27030951 · Cited by 28 · see citing works
The cognitive impact of nutritional homocysteinemia in Apolipoprotein-E deficient mice
Troen, A. M., Shukitt‐Hale, B., Chao, W., Albuquerque, B., Smith, D. E., Selhub, J., & Rosenberg, I. H. (2006) · Journal of Alzheimer s Disease · doi:10.3233/jad-2006-9403 · Cited by 28 · see citing works
Preventing Alzheimer's disease by means of natural selection
Demetrius, L., & Driver, J. A. (2014) · Journal of The Royal Society Interface · doi:10.1098/rsif.2014.0919 · Cited by 24 · see citing works
Alterations in mitochondrial number and function in Alzheimer’s disease fibroblasts
Gray, N. E., & Quinn, J. F. (2015) · Metabolic Brain Disease · doi:10.1007/s11011-015-9667-z · Cited by 21 · see citing works
Coskun, P. E., Helguera, P. R., Nemati, Z., Bohannan, R. C., Thomas, J., Samuel, S. E., Argueta, J., Doran, E. W., Wallace, D. C., Lott, I. T., et al. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-160278 · Cited by 19 · see citing works
Bioenergetics and lipid metabolism in Alzheimer's disease: From cell biology to systemic health
Maioli, S., Nalvarte, I., Ankarcrona, M., Schultzberg, M., Zuloaga, K. L., Goikolea, J., Visser, P. J., Strooper, B. D., Winblad, B., Pizzo, P., et al. (2025) · Journal of Internal Medicine · doi:10.1111/joim.70036 · Cited by 18 · see citing works
Mitochondrial Drugs for Alzheimer Disease
Bonda, D., Wang, X., Gustaw‐Rothenberg, K., Perry, G. L., Smith, M. A., & Zhu, X. (2009) · Pharmaceuticals · doi:10.3390/ph2030287 · Cited by 16 · see citing works
Smith, M., Nagy, Z., Barnetson, L. P. D., King, E. M., & Esiri, M. M. (2000) · Acta Neuropathologica · doi:10.1007/s004010051197 · Cited by 16 · see citing works
Energy Metabolism is Compromised in Skeletal Muscle of Rats Chronically-Treated with Glutaric Acid
Ferreira, G. C., Schuck, P. F., Viegas, C. M., Tonin, A. M., Latini, A., Dutra‐Filho, C. S., Wyse, Â. T. D. S., Wannmacher, C. M. D., Vargas, C. R., & Wajner, M. (2007) · Metabolic Brain Disease · doi:10.1007/s11011-006-9043-0 · Cited by 14 · see citing works
RECENT ADVANCES IN ALZHEIMER'S DISEASE: CAUSES AND TREATMENT
Kaur, K., Kaur, R., & Kaur, M. (2016) · International Journal of Pharmacy and Pharmaceutical Sciences · Cited by 14 · see citing works
Casademont, J., Rodríguez‐Santiago, B., Miró, Ò., Beato, A., López, S., Nunes, V., & Cardellach, F. (2005) · Aging Clinical and Experimental Research · doi:10.1007/bf03337713 · Cited by 14 · see citing works
Cancer and Alzheimer’s Inverse Correlation: an Immunogenetic Analysis
Bhardwaj, A., Liyanage, S. I., & Weaver, D. F. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03260-8 · Cited by 13 · see citing works
Strazielle, C., Dumont, M., Fukuchi, K.-I., & Lalonde, R. (2004) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2004.03.009 · Cited by 8 · see citing works
β‐Apptists and Tauists, it is time for a sermon from the book of biogenesis
Swerdlow, R. H. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07561.x · Cited by 8 · see citing works
Booker, S. A., Campbell, G. R., Mysiak, K. S., Brophy, P., Kind, P. C., Mahad, D., & Wyllie, D. J. A. (2017) · The Journal of Physiology · doi:10.1113/jp273581 · Cited by 7 · see citing works
Wallace, D. C., Lott, M. T., & Procaccio, V. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-383834-6.00013-6 · Cited by 7 · see citing works
Mitochondrial Effects of Hydromethylthionine, Rivastigmine and Memantine in Tau-Transgenic Mice
Kondak, C., Leith, M., Baddeley, T. C., Santos, R. X., Harrington, C. R., Wischik, C. M., Riedel, G., & Klein, J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241310810 · Cited by 5 · see citing works
ECSIT prevents Alzheimer’s disease pathology by regulating neuronal mitochondrial ROS and mitophagyPreprint
Lepelley, A., Vaughn, L. S., Staniszewski, A., Zhang, H., Du, F., Koppensteiner, P., Tomljanovic, Z., Carneiro, F. R. G., Teich, A. F., Ninan, I., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.01.09.900407 · Cited by 3 · see citing works
Sex differences in brain glucose metabolism and Alzheimer's disease risk and progression
Ramezan, M., Demetriou, A., Burke, S. N., Nalvarte, I., & Shin, A. C. (2026) · Alzheimer s & Dementia · doi:10.1002/alz.71491 · Cited by 2 · see citing works
Role of Mitochondria in Alzheimer s Disease
Ortiz, G. G., Pacheco-Moisés, F. P., García-Trejo, J. D. J., Rocio, E., Miguel, A., Jose, A., Irma, E., Arias‐Merino, E. D., & de la Ros, A. C. (2011) · InTech eBooks · doi:10.5772/16713
Mechanisms of Mitochondrial Defects in Gulf War Syndrome
Shoffner, J. M. (2010) · doi:10.21236/ada536634
Stages of Brain Functional Failure in Alzheimer’s Disease
Rapoport, S. I. (2007) · Humana Press eBooks · doi:10.1007/978-1-59259-888-5_10
Meier-Ruge, W. A., Bertoni–Freddari, C., & Fattoretti, P. (2004) · Springer eBooks · doi:10.1007/978-3-642-18741-4_5
Mechanisms of Mitochondrial Defects in Gulf War Syndrome
Shoffner, J. M. (2011) · doi:10.21236/ada554016
Oxidative Stress Associated Signal Transduction Cascades in Alzheimer Disease
Petersen, R. B., Nunomura, A., Lee, H., Casadesús, G., Perry, G. L., Smith, M. A., & Zhu, X. (2009) · Contemporary clinical neuroscience · doi:10.1007/978-1-60327-342-8_8
- Authors
- Nagy, Z., Esiri, M. M., LeGris, M., & Matthews, P. M.
- Affiliations
- University of Oxford (GB)
- Venue
- Acta Neuropathologica
- Published
- 1999-04-04
- Volume
- 97
- Issue
- 4
- Pages
- 346-354
- ISSN
- 0001-6322 (ISSN-L)
- 1432-0533
- OpenAlex
- W2040258716
- Cited by
- 85
- References
- 27
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 3 · 2021: 2 · 2020: 4 · 2019: 2 · 2018: 1 · 2017: 1 · 2016: 3 · 2015: 5 · 2014: 3 · 2013: 4 · 2012: 3
- FWCI
- 1.89
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Acta Neuropathologica (publishedVersion)
- PubMed (publishedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
- Funders
- Bristol-Myers Squibb
- Buddhist Tzu Chi Medical Foundation
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- Alzheimer's disease, mitochondrial dysfunction, cytochrome c oxidase, cytochrome c oxidase subunit IV, coxI, hippocampus, hyperphosphorylated tau, amyloid deposition, Down syndrome, neuronal heterogeneity
- MeSH terms
- Adolescent, Adult, Aged, Aged, 80 and over, Alzheimer Disease, Autoradiography, Cell Nucleus, Child, Child, Preschool, Electron Transport Complex IV, Down Syndrome, Hippocampus, Humans, Infant, Infant, Newborn, Isoenzymes, Middle Aged, Mitochondria, Neurons, Neurofibrillary Tangles, Fluorescent Antibody Technique, Indirect, Plaque, Amyloid
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