The role of mitochondrial dysfunction in Alzheimer's disease pathogenesis

To promote new thinking of the pathogenesis of Alzheimer's disease (AD), we examine the central role of mitochondrial dysfunction in AD. Pathologically, AD is characterized by progressive neuronal loss and biochemical abnormalities including mitochondrial dysfunction. Conventional thinking has dictated that AD is driven by amyloid beta pathology, per the Amyloid Cascade Hypothesis. However, the underlying mechanism of how amyloid beta leads to cognitive decline remains unclear. A model correctly identifying the pathogenesis of AD is critical and needed for the development of effective therapeutics. Mitochondrial dysfunction is closely linked to the core pathological feature of AD: neuronal dysfunction. Targeting mitochondria and associated proteins may hold promise for new strategies for the development of disease-modifying therapies. According to the Mitochondrial Cascade Hypothesis, mitochondrial dysfunction drives the pathogenesis of AD, as baseline mitochondrial function and mitochondrial change rates influence the progression of cognitive decline. HIGHLIGHTS: The Amyloid Cascade Model does not readily account for various parameters associated with Alzheimer's disease (AD). A unified model correctly identifying the pathogenesis of AD is greatly needed to inform the development of successful therapeutics. Mitochondria play a key and central role in the maintenance of optimal neuronal and synaptic function, the core pathological feature of AD. Mitochondrial dysfunction may be the primary cause of AD, and is a promising target for new therapeutic strategies.

[1]  D. Cordes,et al.  Brain Entropy During Aging Through a Free Energy Principle Approach , 2021, Frontiers in Human Neuroscience.

[2]  A. Pillai,et al.  Randomized crossover trial of a modified ketogenic diet in Alzheimer’s disease , 2021, Alzheimer's research & therapy.

[3]  Robert A. Harris,et al.  Safety and target engagement profile of two oxaloacetate doses in Alzheimer's patients , 2020, Alzheimer's & dementia : the journal of the Alzheimer's Association.

[4]  Integrated analysis of ultra-deep proteomes in cortex, cerebrospinal fluid and serum reveals a mitochondrial signature in Alzheimer’s disease , 2020, Molecular Neurodegeneration.

[5]  M. Michaelis,et al.  Exploratory analysis of mtDNA haplogroups in two Alzheimer's longitudinal cohorts , 2020, Alzheimer's & dementia : the journal of the Alzheimer's Association.

[6]  Bin Zhang,et al.  Large-scale proteomic analysis of Alzheimer’s disease brain and cerebrospinal fluid reveals early changes in energy metabolism associated with microglia and astrocyte activation , 2019, bioRxiv.

[7]  S. Black,et al.  Preventing dementia by preventing stroke: The Berlin Manifesto , 2019, Alzheimer's & Dementia.

[8]  J. Ko,et al.  Regional hypometabolism in the 3xTg mouse model of Alzheimer's disease , 2019, Neurobiology of Disease.

[9]  R. Graham,et al.  PTCD1 Is Required for Mitochondrial Oxidative-Phosphorylation: Possible Genetic Association with Alzheimer's Disease , 2019, The Journal of Neuroscience.

[10]  R. Paolicelli,et al.  Glial Contribution to Excitatory and Inhibitory Synapse Loss in Neurodegeneration , 2019, Front. Cell. Neurosci..

[11]  M. Z. Cader,et al.  Mitophagy inhibits amyloid-β and tau pathology and reverses cognitive deficits in models of Alzheimer’s disease , 2019, Nature Neuroscience.

[12]  J. Bertran-Gonzalez,et al.  Disease‐associated tau impairs mitophagy by inhibiting Parkin translocation to mitochondria , 2018, The EMBO journal.

[13]  S. An,et al.  Mitochondrial therapeutic interventions in Alzheimer’s disease , 2018, Journal of the Neurological Sciences.

[14]  D. Blackburn,et al.  Ursodeoxycholic Acid Improves Mitochondrial Function and Redistributes Drp1 in Fibroblasts from Patients with Either Sporadic or Familial Alzheimer's Disease , 2018, Journal of molecular biology.

[15]  R. Rizzuto,et al.  Tau localises within mitochondrial sub-compartments and its caspase cleavage affects ER-mitochondria interactions and cellular Ca2+ handling. , 2018, Biochimica et biophysica acta. Molecular basis of disease.

[16]  Colin Smith,et al.  Region-specific depletion of synaptic mitochondria in the brains of patients with Alzheimer’s disease , 2018, Acta Neuropathologica.

[17]  M. Pérez,et al.  Contribution of Tau Pathology to Mitochondrial Impairment in Neurodegeneration , 2018, Front. Neurosci..

[18]  Yi Su,et al.  Aerobic glycolysis and tau deposition in preclinical Alzheimer's disease , 2018, Neurobiology of Aging.

[19]  G. Juhász,et al.  Early Presymptomatic Changes in the Proteome of Mitochondria-Associated Membrane in the APP/PS1 Mouse Model of Alzheimer’s Disease , 2018, Molecular Neurobiology.

[20]  F. Kametani,et al.  Reconsideration of Amyloid Hypothesis and Tau Hypothesis in Alzheimer's Disease , 2018, Front. Neurosci..

[21]  M. Shamloo,et al.  Drp1/Fis1 interaction mediates mitochondrial dysfunction, bioenergetic failure and cognitive decline in Alzheimer's disease , 2017, Oncotarget.

[22]  A. McKee,et al.  SIRT3 deregulation is linked to mitochondrial dysfunction in Alzheimer's disease , 2017, Aging cell.

[23]  E. Schon,et al.  A key role for MAM in mediating mitochondrial dysfunction in Alzheimer disease , 2018, Cell Death & Disease.

[24]  L. Lue,et al.  PINK1 signalling rescues amyloid pathology and mitochondrial dysfunction in Alzheimer’s disease , 2017, Brain : a journal of neurology.

[25]  P. Mecocci,et al.  Of Energy and Entropy: The Ineluctable Impact of Aging in Old Age Dementia , 2017, International journal of molecular sciences.

[26]  Z. Khachaturian,et al.  Calcium Hypothesis of Alzheimer's disease and brain aging: A framework for integrating new evidence into a comprehensive theory of pathogenesis , 2017, Alzheimer's & Dementia.

[27]  Ramesh Kandimalla,et al.  Protective effects of reduced dynamin-related protein 1 against amyloid beta-induced mitochondrial dysfunction and synaptic damage in Alzheimer's disease. , 2016, Human molecular genetics.

[28]  Nazanin Mirzaei,et al.  PPARγ-coactivator-1α gene transfer reduces neuronal loss and amyloid-β generation by reducing β-secretase in an Alzheimer’s disease model , 2016, Proceedings of the National Academy of Sciences.

[29]  G. Bu,et al.  Modulation of Mitochondrial Complex I Activity Averts Cognitive Decline in Multiple Animal Models of Familial Alzheimer's Disease , 2015, EBioMedicine.

[30]  R. Swerdlow,et al.  The Alzheimer's disease mitochondrial cascade hypothesis: progress and perspectives. , 2014, Biochimica et biophysica acta.

[31]  G. Pasinetti,et al.  Nicotinamide riboside restores cognition through an upregulation of proliferator-activated receptor-γ coactivator 1α regulated β-secretase 1 degradation and mitochondrial gene expression in Alzheimer's mouse models , 2013, Neurobiology of Aging.

[32]  F. Gunn-Moore,et al.  Is amyloid binding alcohol dehydrogenase a drug target for treating Alzheimer's disease? , 2013, Current Alzheimer research.

[33]  D. Attwell,et al.  Synaptic Energy Use and Supply , 2012, Neuron.

[34]  M. Feany,et al.  Tau Promotes Neurodegeneration via DRP1 Mislocalization In Vivo , 2012, Neuron.

[35]  C. Cotman,et al.  Antioxidants for Alzheimer disease: a randomized clinical trial with cerebrospinal fluid biomarker measures. , 2012, Archives of neurology.

[36]  I. Bezprozvanny,et al.  The dysregulation of intracellular calcium in Alzheimer disease. , 2010, Cell calcium.

[37]  M. Beal,et al.  Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases , 2006, Nature.

[38]  D. Chan Mitochondria: Dynamic Organelles in Disease, Aging, and Development , 2006, Cell.

[39]  Xi Chen,et al.  Materials and Methods Som Text Figs. S1 and S2 Table S1 References Abad Directly Links A␤ to Mitochondrial Toxicity in Alzheimer's Disease , 2022 .

[40]  G. Schellenberg,et al.  Secreted amyloid β–protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease , 1996, Nature Medicine.

[41]  M. Beal,et al.  Cortical Cytochrome Oxidase Activity Is Reduced in Alzheimer's Disease , 1994, Journal of neurochemistry.