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Systematic review and meta-analysis on the role of mitochondrial cytochrome c oxidase in Alzheimer’s disease

Published online by Cambridge University Press:  01 December 2020

Flavio M. Morais
Affiliation:
Graduate Program in Neurosciences, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
Angela M. Ribeiro
Affiliation:
Graduate Program in Neurosciences, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil Department of Biochemistry and Immunology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
Fabricio A. Moreira
Affiliation:
Graduate Program in Neurosciences, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil Department of Pharmacology, Institute of Biological Sciences, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
Pollyanna V. G. Silva*
Affiliation:
Ministerio Público do Estado de Minas Gerais, Belo Horizonte, Brazil
*
Author for correspondence: Pollyanna V. G. Silva, Email: [email protected]

Abstract

Objective:

The present study was designed to test the hypothesis that there is a reduction in the activity of the enzyme cytochrome c oxidase (Cox) in Alzheimer’s disease (AD).

Methods:

Systematic review of literature and meta-analysis were used with data obtained from the PubMed, Scopus, MEDLINE, Lilacs, Eric and Cochrane. The keywords were Alzheimer’s AND Cox AND mitochondria; Alzheimer’s AND Cox AND mitochondria; Alzheimer’s AND complex IV AND mitochondria. A total of 1372 articles were found, 23 of them fitting the inclusion criteria. The data were assembled in an Excel spreadsheet and analysed using the RevMan software. A random effects model was adopted to the estimative of the effect.

Results:

The data shows a significant decrease in the activity of the Cox AD patients and animal models.

Conclusion:

Cox enzyme may be an important molecular component involved in the mechanisms underlying AD. Therefore, this enzyme may represent a possible new biomarker for the disease as a complementary diagnosis and a new treatment target for AD.

Type
Review Article
Copyright
© Scandinavian College of Neuropsychopharmacology 2020

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References

Aleardi, AM, Benard, G, Augereau, O, Malgat, M, Talbot, JC, Mazat, JP, Letellier, T, Dachary-Prigent, J, Solaini, GC, and Rossignol, R (2005) 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. Journal of Bioenergetics and Biomembranes 37, 207225.CrossRefGoogle ScholarPubMed
Avetisyan, AV, Samokhin, AN, Alexandrova, IY, Zinovkin, RA, Simonyan, RA, and Bobkova, NV (2016) Mitochondrial dysfunction in neocortex and hippocampus of olfactory bulbectomized mice, a model of Alzheimer’s disease. Biochemistry (Mosc) 81, 615623.CrossRefGoogle Scholar
Beal, MF (1995) Aging, energy, and oxidative stress in neurodegenerative diseases. Annals of Neurology 38, 357366.CrossRefGoogle ScholarPubMed
Bobba, A, Amadoro, G, Valenti, D, Corsetti, V, Lassandro, R, and Atlante, A (2013) Mitochondrial respiratory chain Complexes I and IV are impaired by β-amyloid via direct interaction and through Complex I-dependent ROS production, respectively. Mitochondrion 13, 298311.CrossRefGoogle ScholarPubMed
Borenstein, M (2009). Introduction to Meta-Analysis. John Wiley & Sons.CrossRefGoogle Scholar
Bowling, AC, Mutisya, EM, Walker, LC, Price, DL, Cork, LC, and Beal, MF (1993) Age-dependent impairment of mitochondrial function in primate brain. Journal of Neurochemistry 60, 19641967.CrossRefGoogle ScholarPubMed
Cardoso, SM, Proença, MT, Santos, S, Santana, I, and Oliveira, CR (2004) Cytochrome c oxidase is decreased in Alzheimer’s disease platelets. Neurobiology of Aging 25, 105110.CrossRefGoogle ScholarPubMed
Cassano, T, Serviddio, G, Gaetani, S, Romano, A, Dipasquale, P, Cianci, S, Bellanti, F, Laconca, L, Romano, AD, Padalino, I, LaFerla, FM, Nicoletti, F, Cuomo, V, and Vendemiale, G (2012) Glutamatergic alterations and mitochondrial impairment in a murine model of Alzheimer disease. Neurobiology of Aging 33, 1121.e1–12.CrossRefGoogle Scholar
Cavallucci, V, Ferraina, C, and D’Amelio, M (2013) Key role of mitochondria in Alzheimer’s disease synaptic dysfunction. Current Pharmaceutical Design 19, 64406450.CrossRefGoogle ScholarPubMed
Crouch, PJ, Barnham, KJ, Duce, JA, Blake, RE, Masters, CL, and Trounce, IA (2006) Copper-dependent inhibition of cytochrome c oxidase by Abeta(1-42) requires reduced methionine at residue 35 of the Abeta peptide. Journal of Neurochemistry 99, 226236.CrossRefGoogle ScholarPubMed
Crouch, PJ, Blake, R, Duce, JA, Ciccotosto, GD, Li, QX, Barnham, KJ, Curtain, CC, Cherny, RA, Cappai, R, Dyrks, T, Masters, CL, and Trounce, IA (2005) Copper-dependent inhibition of human cytochrome c oxidase by a dimeric conformer of amyloid-beta1-42. Journal of Neuroscience 25, 672679.CrossRefGoogle ScholarPubMed
Delbarba, A, Abate, G, Prandelli, C, Marziano, M, Buizza, L, Arce Varas, N, Novelli, A, Cuetos, F, Martinez, C, Lanni, C, Memo, M, and Uberti, D (2016) Mitochondrial Alterations in Peripheral Mononuclear Blood Cells from Alzheimer’s Disease and Mild Cognitive Impairment Patients. Oxidative Medicine and Cellular Longevity, 2016.CrossRefGoogle Scholar
Diaz, F, Fukui, H, Garcia, S, and Moraes, CT (2006) Cytochrome c oxidase is required for the assembly/stability of respiratory complex I in mouse fibroblasts. Molecular and Cellular Biology 26, 48724881.CrossRefGoogle ScholarPubMed
Du, H, Guo, L, Fang, F, Chen, D, Sosunov, AA, McKhann, GM, Yan, Y, Wang, C, Zhang, H, Molkentin, JD, Gunn-Moore, FJ, Vonsattel, JP, Arancio, O, Chen, JX, and Yan, SD (2008) Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer’s disease. Naure Medicine 14, 10971105.Google ScholarPubMed
Duval, S and Tweedie, R (2000). Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56, 455463.CrossRefGoogle ScholarPubMed
Fang, D, Zhang, Z, Li, H, Yu, Q, Douglas, JT, Bratasz, A, Kuppusamy, P, and Yan, SS (2016) Increased electron paramagnetic resonance signal correlates with mitochondrial dysfunction and oxidative stress in an Alzheimer’s disease mouse brain. Journal of Alzheimer’s Disease 51, 571580.CrossRefGoogle Scholar
Freitas, EV, Py, L, Cançado, FAX, Doll, J, and Gorzoni, ML (2013). Tratado de geriatria e gerontologia.Google Scholar
Gibson, GE, Sheu, KF, and Blass, JP (1998) Abnormalities of mitochondrial enzymes in Alzheimer disease. Journal of Neural Transmission (Vienna) 105, 855870.CrossRefGoogle ScholarPubMed
Greilberger, J, Koidl, C, Greilberger, M, Lamprecht, M, Schroecksnadel, K, Leblhuber, F, Fuchs, D, and Oettl, K (2008) Malondialdehyde, carbonyl proteins and albumin-disulphide as useful oxidative markers in mild cognitive impairment and Alzheimer’s disease. Free Radical Research 42, 633638.CrossRefGoogle ScholarPubMed
Guo, L, Du, H, Zhang, W, Rydzewska, M, and Yan, S (2011) Cyclophilin D deficiency improves mitochondrial function and learning/memory in aging Alzheimer disease mouse model. Neurobiology of Aging 32, 398406.Google Scholar
Hernández-Zimbrón, LF and Rivas-Arancibia, S (2015) Oxidative stress caused by ozone exposure induces β-amyloid 1-42 overproduction and mitochondrial accumulation by activating the amyloidogenic pathway. Neuroscience 304, 340348.CrossRefGoogle ScholarPubMed
Hou, DR, Wang, Y, Xue, L, Tian, Y, Chen, K, Song, Z, and Yang, QD (2008) Effect of polygonum multiflorum on the fluidity of the mitochondria membrane and activity of COX in the hippocampus of rats with Abeta 1-40-induced Alzheimer’s diseas. Journal of Central South University 33, 987992.Google Scholar
Hu, Y, Li, XC, Wang, ZH, Luo, Y, Zhang, X, Liu, XP, Feng, Q, Wang, Q, Yue, Z, Chen, Z, Ye, K, Wang, JZ, and Liu, GP (2016) Tau accumulation impairs mitophagy via increasing mitochondrial membrane potential and reducing mitochondrial Parkin. Oncotarget 7, 1735617368.CrossRefGoogle ScholarPubMed
Jiao, Y, Zhang, Y, Wei, Y, Liu, Z, An, W, and Guo, M (2012) Direct observation of internalization and ROS generation of amyloid β-peptide in neuronal cells at subcellular resolution. Chembiochem 13, 23352338.CrossRefGoogle ScholarPubMed
Kadenbach, B and Hüttemann, M (2015) The subunit composition and function of mammalian cytochrome c oxidase. Mitochondrion 24, 6476.CrossRefGoogle ScholarPubMed
Kalra, J, Kumar, P, Majeed, AB, and Prakash, A (2016) Modulation of LOX and COX pathways via inhibition of amyloidogenesis contributes to mitoprotection against β-amyloid oligomer-induced toxicity in an animal model of Alzheimer’s disease in rats. Pharmacology Biochemistry Behavior 146, 112.CrossRefGoogle Scholar
Kanamori, T, Nishimaki, K, Asoh, S, Ishibashi, Y, Takata, I, Kuwabara, T, Taira, K, Yamaguchi, H, Sugihara, S, Yamazaki, T, Ihara, Y, Nakano, K, Matuda, S, and Ohta, S (2003) Truncated product of the bifunctional DLST gene involved in biogenesis of the respiratory chain. The EMBO Journal 22, 29132923.CrossRefGoogle ScholarPubMed
Kaur, N, Dhiman, M, Perez-Polo, JR, and Mantha, AK (2015) Ginkgolide B revamps neuroprotective role of apurinic/apyrimidinic endonuclease 1 and mitochondrial oxidative phosphorylation against Aβ25-35 -induced neurotoxicity in human neuroblastoma cells. Journal of Neuroscience Research 93, 938947.CrossRefGoogle ScholarPubMed
Keil, U, Bonert, A, Marques, CA, Scherping, I, Weyermann, J, Strosznajder, JB, Müller-Spahn, F, Haass, C, Czech, C, Pradier, L, Müller, WE, and Eckert, A (2004) Amyloid beta-induced changes in nitric oxide production and mitochondrial activity lead to apoptosis. Journal of Biological Chemistry 279, 5031050320.CrossRefGoogle Scholar
Lahmy, V, Long, R, Morin, D, Villard, V, and Maurice, T (2015) Mitochondrial protection by the mixed muscarinic/σ1 ligand ANAVEX2-73, a tetrahydrofuran derivative, in Aβ25-35 peptide-injected mice, a nontransgenic Alzheimer’s disease model. Frontiers in Cellular Neuroscience 8, 463.CrossRefGoogle ScholarPubMed
Malmström, BG (1990) Cytochrome oxidase: some unsolved problems and controversial issues. Archives of Biochemistry and Biophysics 280, 233241.CrossRefGoogle ScholarPubMed
Mancuso, M, Filosto, M, Bosetti, F, Ceravolo, R, Rocchi, A, Tognoni, G, Manca, ML, Solaini, G, Siciliano, G, and Murri, L (2003) Decreased platelet cytochrome c oxidase activity is accompanied by increased blood lactate concentration during exercise in patients with Alzheimer disease. Experimental Neurology 182, 421426.CrossRefGoogle ScholarPubMed
Maurer, I, Zierz, S, and Möller, HJ (2000) A selective defect of cytochrome c oxidase is present in brain of Alzheimer disease patients. Neurobiology of Aging 21, 455462.CrossRefGoogle ScholarPubMed
Meunier, J, Ieni, J, and Maurice, T (2006) The anti-amnesic and neuroprotective effects of donepezil against amyloid beta25-35 peptide-induced toxicity in mice involve an interaction with the sigma1 receptor. British Journal of Pharmacology 149, 9981012.CrossRefGoogle ScholarPubMed
Mutisya, EM, Bowling, AC, and Beal, MF (1994) Cortical cytochrome oxidase activity is reduced in Alzheimer’s disease. Journal of Neurochemistry 63, 21792184.CrossRefGoogle ScholarPubMed
OMS (2017) Dementia. Factsheet 362.Google Scholar
Paradies, G, Ruggiero, FM, Petrosillo, G, and Quagliariello, E (1993) Age-dependent decrease in the cytochrome c oxidase activity and changes in phospholipids in rat-heart mitochondria. Archives of Gerontology and Geriatrics 16, 263272.CrossRefGoogle ScholarPubMed
Paradies, G, Ruggiero, FM, Petrosillo, G, and Quagliariello, E (1998) Peroxidative damage to cardiac mitochondria: cytochrome oxidase and cardiolipin alterations. FEBS Letters 424, 155158.CrossRefGoogle ScholarPubMed
Parker, WD, Parks, J, Filley, CM, and Kleinschmidt-DeMasters, BK (1994) Electron transport chain defects in Alzheimer’s disease brain. Neurology 44, 10901096.CrossRefGoogle ScholarPubMed
Pedrós, I, Petrov, D, Allgaier, M, Sureda, F, Barroso, E, Beas-Zarate, C, Auladell, C, Pallàs, M, Vázquez-Carrera, M, Casadesús, G, Folch, J, and Camins, A (2014) Early alterations in energy metabolism in the hippocampus of APPswe/PS1dE9 mouse model of Alzheimer’s disease. Biochimica et Biophysica Acta 1842, 15561566.CrossRefGoogle ScholarPubMed
Pierron, D, Wildman, DE, Hüttemann, M, Markondapatnaikuni, GC, Aras, S, and Grossman, LI (2012) Cytochrome c oxidase: evolution of control via nuclear subunit addition. Biochimica et Biophysica Acta 1817, 590597.CrossRefGoogle ScholarPubMed
Rak, M, Bénit, P, Chrétien, D, Bouchereau, J, Schiff, M, El-Khoury, R, Tzagoloff, A, and Rustin, P (2016) Mitochondrial cytochrome c oxidase deficiency. Clinical Science (Lond) 130, 393407.CrossRefGoogle ScholarPubMed
Readnower, RD, Sauerbeck, AD, and Sullivan, PG (2011) Mitochondria, Amyloid β, and Alzheimer’s disease. International Journal of Alzheimer’s Disease 2011, 104545.Google ScholarPubMed
Rettberg, JR, Yao, J, and Brinton, RD (2014) Estrogen: a master regulator of bioenergetic systems in the brain and body. Frontiers in Neuroendocrinology 35, 830.CrossRefGoogle ScholarPubMed
Rhein, V, Baysang, G, Rao, S, Meier, F, Bonert, A, Müller-Spahn, F, and Eckert, A (2009) Amyloid-Beta leads to impaired cellular respiration, energy production and mitochondrial electron chain complex activities in human neuroblastoma cells. Cellular and Molecular Neurobiology 29, 10631071.CrossRefGoogle ScholarPubMed
Rhein, V, Giese, M, Baysang, G, Meier, F, Rao, S, Schulz, KL, Hamburger, M, and Eckert, A (2010) Ginkgo biloba extract ameliorates oxidative phosphorylation performance and rescues abeta-induced failure. PLoS One 5, e12359.CrossRefGoogle ScholarPubMed
Rodrigues, CL and Ziegelmann, PK (2010) Metanálise: um guia prático.Google Scholar
Saada, A, Edvardson, S, Shaag, A, Chung, WK, Segel, R, Miller, C, Jalas, C, and Elpeleg, O (2012) Combined OXPHOS complex I and IV defect, due to mutated complex I assembly factor C20ORF7. Journal of Inherited Metabolic Disease 35, 125131.CrossRefGoogle ScholarPubMed
Seo, JS, Lee, KW, Kim, TK, Baek, IS, Im, JY, and Han, PL (2011) Behavioral stress causes mitochondrial dysfunction via ABAD up-regulation and aggravates plaque pathology in the brain of a mouse model of Alzheimer disease. Free Radical Biology & Medicine 50, 15261535.CrossRefGoogle ScholarPubMed
Shi, L and Lin, L (2019) The trim-and-fill method for publication bias: practical guidelines and recommendations based on a large database of meta-analyses. Medicine 98.CrossRefGoogle Scholar
Simonian, NA and Hyman, BT (1993) Functional alterations in Alzheimer’s disease: diminution of cytochrome oxidase in the hippocampal formation. Journal of Neuropathology & Experimental Neurology 52, 580585.CrossRefGoogle ScholarPubMed
Sohal, RS (1993) Aging, cytochrome oxidase activity, and hydrogen peroxide release by mitochondria. Free Radical Biology & Medicine 14, 583588.CrossRefGoogle ScholarPubMed
Srinivasan, S and Avadhani, NG (2012) Cytochrome c oxidase dysfunction in oxidative stress. Free Radical Biology & Medicine 53, 12521263.CrossRefGoogle ScholarPubMed
Swerdlow, RH, Burns, JM, and Khan, SM (2010) The Alzheimer’s disease mitochondrial cascade hypothesis. Journal of Alzheimer’s Disease 20, 265279.CrossRefGoogle ScholarPubMed
Walls, KC, Coskun, P, Gallegos-Perez, JL, Zadourian, N, Freude, K, Rasool, S, Blurton-Jones, M, Green, KN, and LaFerla, FM (2012) Swedish Alzheimer mutation induces mitochondrial dysfunction mediated by HSP60 mislocalization of amyloid precursor protein (APP) and beta-amyloid. Journal of Biological Chemistry 287, 3031730327.CrossRefGoogle ScholarPubMed
Warburg, O and Negelein, E (1929) Biochemistry Z 214, 64.Google Scholar
Whitehead, A (2002) Meta-Analysis of Controlled Clinical Trials . John Wiley & Sons.CrossRefGoogle Scholar
Yang, TT, Hsu, CT, and Kuo, YM (2009) Cell-Derived soluble oligomers of human amyloid-beta peptides disturb cellular homeostasis and induce apoptosis in primary hippocampal neurons. Journal of Neural Transmission (Vienna) 116, 15611569.CrossRefGoogle ScholarPubMed
Yao, J, Rettberg, JR, Klosinski, LP, Cadenas, E, and Brinton, RD (2011) Shift in brain metabolism in late onset Alzheimer’s disease: implications for biomarkers and therapeutic interventions. Molecular Aspects of Medicine 32, 247–57.CrossRefGoogle ScholarPubMed
Zhao, H, Wu, H, He, J, Zhuang, J, Liu, Z, Yang, Y, Huang, L, and Zhao, Z (2016) Frontal cortical mitochondrial dysfunction and mitochondria-related β-amyloid accumulation by chronic sleep restriction in mice. Neuroreport 27, 916922.CrossRefGoogle ScholarPubMed