Mitochondrial bioenergetics is defective in presymptomatic Tg2576 AD Mice

Merina Varghese, Wei Zhao, Jun Wang, Ann‐Joy Cheng, Xiang Qian, Amna Chaudhry1, Lap Ho, Giulio Maria Pasinetti
1Department of Neurology, The Mount Sinai School of Medicine, New York, NY 10029 USA

Tóm tắt

Abstract

Alzheimer’s disease (AD) is an age-related dementia, with the pathological hallmarks of neuritic plaques and neurofibrillary tangles, brain atrophy and loss of synaptic terminals. Dysfunctional mitochondrial bioenergetics is implicated as a contributing factor to the cognitive decline observed in AD. We hypothesized that, in the presence of the AD neurotoxic peptide beta-amyloid, mitochondrial respiration is impaired early in synaptic terminals, which are vital to cognitive performance, preferentially in cognitive centers of the brain. We compared oxygen consumption in synaptosomal and perikaryal mitochondria prepared from the cerebral cortex and cerebellum of wild type (WT) and AD transgenic Tg2576 mice. Compared to WT mice, Tg2576 mice showed decreased mitochondrial respiration in the cerebral cortex specifically in synaptosomal fraction, while the perikaryal mitochondria were unaffected. Neither mitochondrial fraction was affected in the cerebellum of Tg2576 mice as compared to WT. The occurrence of a bioenergetic defect in synaptic terminals of mice overexpressing mutant beta-amyloid, in particular in an area of the brain important to cognition, points to an early role of mitochondrial defects in the onset of cognitive deficits in AD.

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Tài liệu tham khảo

Duara R., Grady C., Haxby J., Sundaram M., Cutler N. R., Heston L., et al., Positron emission tomography in Alzheimer’s disease, Neurology, 1986, 36, 879–887

Haxby J. V., Grady C. L., Duara R., Schlageter N., Berg G., Rapoport S. I., Neocortical metabolic abnormalities precede nonmemory cognitive defects in early Alzheimer’s-type dementia, Arch Neurol, 1986, 43, 882–885

Butterworth R. F., Besnard A. M., Thiamine-dependent enzyme changes in temporal cortex of patients with Alzheimer’s disease, Metab Brain Dis, 1990, 5, 179–184

Mastrogiacoma F., Lindsay J. G., Bettendorff L., Rice J., Kish S. J., Brain protein and alpha-ketoglutarate dehydrogenase complex activity in Alzheimer’s disease, Ann Neurol, 1996, 39, 592–598

Sorbi S., Bird E. D., Blass J. P., Decreased pyruvate dehydrogenase complex activity in Huntington and Alzheimer brain, Ann Neurol, 1983, 13, 72–78

Perry E. K., Perry R. H., Tomlinson B. E., Blessed G., Gibson P. H., Coenzyme A-acetylating enzymes in Alzheimer’s disease: possible cholinergic ‘compartment’ of pyruvate dehydrogenase, Neurosci Lett, 1980, 18, 105–110

Parker W. D., Parks J., Filley C. M., Kleinschmidtdemasters B. K., Electron-Transport Chain Defects in Alzheimers-Disease Brain, Neurology, 1994, 44, 1090–1096

Maurer I., Zierz S., Moller H. J., A selective defect of cytochrome c oxidase is present in brain of Alzheimer disease patients, Neurobiol Aging, 2000, 21, 455–462

Cottrell D. A., Blakely E. L., Johnson M. A., Ince P. G., Turnbull D. M., Mitochondrial enzyme-deficient hippocampal neurons and choroidal cells in AD, Neurology, 2001, 57, 260–264

Kish S. J., Bergeron C., Rajput A., Dozic S., Mastrogiacomo F., Chang L.J., et al., Brain cytochrome oxidase in Alzheimer’s disease, J Neurochem, 1992, 59, 776–779

Swerdlow R. H., Khan S. M., A “mitochondrial cascade hypothesis” for sporadic Alzheimer’s disease, Med Hypotheses, 2004, 63, 8–20

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, 14670–14675

Dragicevic N., Mamcarz M., Zhu Y. Y., Buzzeo R., Tan J., Arendash G. W., Bradshaw P. C., Mitochondrial amyloid-beta levels are associated with the extent of mitochondrial dysfunction in different brain regions and the degree of cognitive impairment in Alzheimer’s transgenic mice, J Alzheimers Dis, 2010, 20, S535–S550

Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., et al., Correlative memory deficits, A beta elevation, and amyloid plaques in transgenic mice, Science, 1996, 274, 99–102

Brown M. R., Sullivan P. G., Geddes J. W., Synaptic mitochondria are more susceptible to Ca2+ overload than nonsynaptic mitochondria, J Biol Chem, 2006, 281, 11658–11668

Choi S. W., Gerencser A.A., Nicholls D. G., Bioenergetic analysis of isolated cerebrocortical nerve terminals on a microgram scale: spare respiratory capacity and stochastic mitochondrial failure. J Neurochem, 2009, 109, 1179–1191

Wang J., Ho L., Zhao W., Ono K., Rosensweig C., Chen L., et al., Grape-derived polyphenolics prevent Abeta oligomerization and attenuate cognitive deterioration in a mouse model of Alzheimer’s disease, J Neurosci, 2008, 28, 6388–6392

Du H., Guo L., Yan S., Sosunov A. A., McKhann G. M., Yan S. S., Early deficits in synaptic mitochondria in an Alzheimer’s disease mouse model, Proc Natl Acad Sci USA, 2010, 107, 18670–18675

Hansson Petersen C. A., Alikhani N., Behbahani H., Wiehager B., Pavlov P. F., Alafuzoff I., et al., The amyloid beta-peptide is imported into mitochondria via the TOM import machinery and localized to mitochondrial cristae, Proc Natl Acad Sci USA, 2008, 105, 13145–13150

Devi L., Prabhu B. M., Galati D. F., Avadhani N. G., Anandatheerthavarada H. K., Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer’s disease brain is associated with mitochondrial dysfunction, J Neurosci, 2006, 26, 9057–9068

Crouch P. J., Blake R, Duce J. A., Ciccotosto G.D., Li Q.X., Barnham K.J., et al., Copper-dependent inhibition of human cytochrome c oxidase by a dimeric conformer of amyloid-beta 1–42, J Neurosci, 2005, 25, 672–679

Manczak M., Anekonda T.S., Henson E., Park B.S., Quinn J., Reddy P.H., Mitochondria are a direct site of A beta accumulation in Alzheimer’s disease neurons: implications for free radical generation and oxidative damage in disease progression, Hum Mol Genet, 2006, 15, 1437–1449

Lesne S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., et al., A specific amyloid-beta protein assembly in the brain impairs memory, Nature, 2006, 440, 352–357