Hippocampal disruptions of synaptic and astrocyte metabolism are primary events of early amyloid pathology in the 5xFAD mouse model of Alzheimer’s disease
Open accessAbstract
Alzheimer’s disease (AD) is an unremitting neurodegenerative disorder characterized by cerebral amyloid-β (Aβ) accumulation and gradual decline in cognitive function. Changes in brain energy metabolism arise in the preclinical phase of AD, suggesting an important metabolic component of early AD pathology. Neurons and astrocytes function in close metabolic collaboration, which is essential for the recycling of neurotransmitters in the synapse. However, this crucial metabolic interplay during the early stages of AD development has not been sufficiently investigated. Here, we provide an integrative analysis of cellular metabolism during the early stages of Aβ accumulation in the cerebral cortex and hippocampus of the 5xFAD mouse model of AD. Our electrophysiological examination revealed an increase in spontaneous excitatory signaling in the 5xFAD hippocampus. This hyperactive neuronal phenotype coincided with decreased hippocampal tricarboxylic acid (TCA) cycle metabolism mapped by stable 13 C isotope tracing. Particularly, reduced astrocyte TCA cycle activity and decreased glutamine synthesis led to hampered neuronal GABA synthesis in the 5xFAD hippocampus. In contrast, the cerebral cortex of 5xFAD mice displayed an elevated capacity for oxidative glucose metabolism, which may suggest a metabolic compensation in this brain region. We found limited changes when we explored the brain proteome and metabolome of the 5xFAD mice, supporting that the functional metabolic disturbances between neurons and astrocytes are early primary events in AD pathology. In addition, synaptic mitochondrial and glycolytic function was selectively impaired in the 5xFAD hippocampus, whereas non-synaptic mitochondrial function was maintained. These findings were supported by ultrastructural analyses demonstrating disruptions in mitochondrial morphology, particularly in the 5xFAD hippocampus. Collectively, our study reveals complex regional and cell-specific metabolic adaptations in the early stages of amyloid pathology, which may be fundamental for the progressing synaptic dysfunctions in AD.
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Mutations in both APP and PSEN1 cause aberrant APP cleavage and clearance that lead to neuroinflammation, activation of astrocytes and microglia, and changes in bioenergetics.
“Mutations in both APP and PSEN1 cause aberrant APP cleavage and clearance4,47 that lead to neuroinflammation, the activation of astrocytes and microglia, and changes in bioenergetics44,48.”
From Magnetic resonance microscopy maps widespread effects of Alzheimer’s disease on brain structures and behavior in mice (2026) · cites this paper as [44]
The Introduction (page unavailable) links Aβ accumulation to astrocyte changes and early metabolic changes in Alzheimer’s disease. The Discussion (page unavailable) reports altered astrocyte metabolism in 5xFAD mice, but does not establish the claimed chain from aberrant APP cleavage and clearance to neuroinflammation and microglial activation. The cleavage-and-clearance portion also has separate citations in the citing sentence. (LLM, conf=0.85)
Experimental — accuracy not yet measuredOur positive findings contrast sharply with negative findings of the MODEL-AD consortium and other recent studies that have also used T1/T2 MRI and DTI methods.
“Our positive findings contrast sharply with negative findings of the MODEL-AD consortium16 and other recent studies that have also used T1/T2 MRI and DTI methods7,44 (Supplementary Tables 2 and 3).”
From Magnetic resonance microscopy maps widespread effects of Alzheimer’s disease on brain structures and behavior in mice (2026) · cites this paper as [44]
The Materials and methods sections describe metabolic, proteomic, and electron-microscopy analyses, not T1/T2 MRI or DTI. The Discussion passage on regional brain metabolism does not report negative MRI findings or discuss the MODEL-AD consortium. Searches for those terms found no passage in our copy that addresses the attributed claim; page numbers were not available. (LLM, conf=0.76)
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Andersen, J. V., Schousboe, A., & Verkhratsky, A. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102331 · Cited by 259 · see citing works
Self-citationBrain energy metabolism: Astrocytes in neurodegenerative diseases.
Chen, Z., Yuan, Z., Yang, S., Zhu, Y., Xue, M., Zhang, J., & Leng, L. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13982 · Cited by 153 · see citing works
Andersen, J. V., & Schousboe, A. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15811 · Cited by 152 · see citing works
Self-citationThe Glutamate/ GABA ‐Glutamine Cycle: Insights, Updates, and Advances
Andersen, J. V. (2025) · Journal of Neurochemistry · doi:10.1111/jnc.70029 · Cited by 156 · see citing works
Self-citationInflammatory aspects of Alzheimer’s disease
Lucena, P. B., & Heneka, M. T. (2024) · Acta Neuropathologica · doi:10.1007/s00401-024-02790-2 · Cited by 143 · see citing works
Axonal energy metabolism, and the effects in aging and neurodegenerative diseases
Yang, S., Park, J. H., & Lu, H.-C. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00634-3 · Cited by 94 · see citing works
Glucose metabolism, neural cell senescence and Alzheimer's disease
Wang, Q., Duan, L., Li, X., Wang, Y., Guo, W., Guan, F., & Ma, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084351 · Cited by 90 · see citing works
Glial Glutamine Homeostasis in Health and Disease
Andersen, J. V., & Schousboe, A. (2022) · Neurochemical Research · doi:10.1007/s11064-022-03771-1 · Cited by 88 · see citing works
Self-citationNaia, L., Shimozawa, M., Bereczki, E., Li, X., Liu, J., Jiang, R., Giraud, R., Leal, N. S., Pinho, C. M., Berger, E., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02289-4 · Cited by 79 · see citing works
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Lei, W., Cheng, Y., Liu, X., Gao, J., Zhu, Z., Ding, W., Xu, X., Li, Y., Ling, Z., Jiang, R., et al. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1582119 · Cited by 68 · see citing works
Astrocytes regulate inhibitory neurotransmission through GABA uptake, metabolism, and recycling
Andersen, J. V., Schousboe, A., & Wellendorph, P. (2023) · Essays in Biochemistry · doi:10.1042/ebc20220208 · Cited by 55 · see citing works
Self-citationAstrocytic modulation of neuronal signalling
Purushotham, S. S., & Buskila, Y. (2023) · Frontiers in Network Physiology · doi:10.3389/fnetp.2023.1205544 · Cited by 54 · see citing works
Wang, W., Zhao, F., Lu, Y., Siedlak, S. L., Fujioka, H., Feng, H., Perry, G. L., & Zhu, X. (2023) · Acta Neuropathologica Communications · doi:10.1186/s40478-023-01552-7 · Cited by 49 · see citing works
Golgi fragmentation – One of the earliest organelle phenotypes in Alzheimer’s disease neurons
Haukedal, H., Corsi, G. I., Gadekar, V. P., Doncheva, N. T., Kedia, S., de Haan, N., Chandrasekaran, A., Jensen, P., Schiønning, P., Vallin, S., et al. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1120086 · Cited by 37 · see citing works
Self-citationAstrocytes: The Stars in Neurodegeneration?
Dittlau, K. S., & Freude, K. (2024) · Biomolecules · doi:10.3390/biom14030289 · Cited by 38 · see citing works
Self-citationNeural Metabolic Networks: Key Elements of Healthy Brain Function
Madrer, N., Perera, N. D., Uccelli, N. A., Abbondanza, A., Andersen, J. V., Carsana, E. V., Demmings, M. D., Fernandez, R. F., de Fragas, M. G., Gbadamosi, I., et al. (2025) · Journal of Neurochemistry · doi:10.1111/jnc.70084 · Cited by 35 · see citing works
Self-citationThe neural basis of neuropsychiatric symptoms in Alzheimer’s disease
Zhang, N. K., Zhang, S. K., Zhang, L. I., Tao, H. W., & Zhang, G. (2024) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2024.1487875 · Cited by 35 · see citing works
Quintanilla‐Sánchez, C., Schmitt, F. W., Curdt, N., Westhoff, A. C., Bänfer, I. W. H., Bayer, T. A., & Bouter, Y. (2023) · Biomedicines · doi:10.3390/biomedicines11020599 · Cited by 32 · see citing works
Zhukov, O., He, C., Soylu-Kucharz, R., Cai, C., Lauritzen, A. D., Aldana, B. I., Björkqvist, M., Lauritzen, M., & Kucharz, K. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1089005 · Cited by 32 · see citing works
Self-citationComerota, M. M., Gedam, M., Xiong, W., Jin, F., Deng, L., Wang, M. C., Wang, J., & Zheng, H. (2023) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00648-x · Cited by 31 · see citing works
Zhu, Z., Lu, J., Wang, S., Peng, W., Yang, Y., Chen, C., Zhou, X. J., Yang, X., Xin, W., Chen, X., et al. (2022) · Aging Cell · doi:10.1111/acel.13587 · Cited by 28 · see citing works
Zhou, H., Li, H., Gowravaram, N., Quan, M., Kausar, N., & Gomperts, S. N. (2022) · Scientific Reports · doi:10.1038/s41598-022-25364-2 · Cited by 28 · see citing works
Potential Retinal Biomarkers in Alzheimer’s Disease
García-Bermúdez, M. Y., Vohra, R., Freude, K., van Wijngaarden, P., Martin, K. R. G., Thomsen, M. S., Aldana, B. I., & Kolko, M. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242115834 · Cited by 30 · see citing works
Self-citationKetone body metabolism and cardiometabolic implications for cognitive health
Fulghum, K., Salathe, S. F., Davis, X. C., Thyfault, J. P., Puchalska, P., & Crawford, P. A. (2024) · npj Metabolic Health and Disease · doi:10.1038/s44324-024-00029-y · Cited by 27 · see citing works
St‐Pierre, M., Carrier, M., Ibáñez, F. G., Khakpour, M., Wallman, M., Parent, M., & Tremblay, M. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02752-7 · Cited by 26 · see citing works
Latest assessment methods for mitochondrial homeostasis in cognitive diseases
You, W., Li, Y., Liu, K., Mi, X., Li, Y., Guo, X., & Li, Z. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.382222 · Cited by 27 · see citing works
Westi, E. W., Jakobsen, E., Voss, C. M., Bak, L. K., Pinborg, L. H., Aldana, B. I., & Andersen, J. V. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-03053-5 · Cited by 26 · see citing works
Self-citationProgress of Astrocyte-Neuron Crosstalk in Central Nervous System Diseases
Zhang, Y., Wang, Z., Xu, F., Liu, Z., Zhao, Y., Yang, L. Z., & Fang, W. (2024) · Neurochemical Research · doi:10.1007/s11064-024-04241-6 · Cited by 28 · see citing works
AI-driven framework to map the brain metabolome in three dimensions
Ma, X., Shedlock, C. J., Medina, T., Ribas, R. A., Clarke, H. A., Hawkinson, T. R., Dande, P. K., Golamari, H. K. R., Wu, L., Ziani, B., et al. (2025) · Nature Metabolism · doi:10.1038/s42255-025-01242-9 · Cited by 24 · see citing works
Self-citationWesti, E. W., Andersen, J. V., & Aldana, B. I. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106145 · Cited by 23 · see citing works
Self-citationGlutamate dehydrogenase: Potential therapeutic targets for neurodegenerative disease
Pan, C., Mao, S., Xiong, Z., Chen, Z., & Xu, N. (2023) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2023.175733 · Cited by 23 · see citing works
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Yusoff, A. A. M., & Khair, S. Z. N. M. (2024) · Reviews in the Neurosciences · doi:10.1515/revneuro-2024-0080 · Cited by 22 · see citing works
Current Advances in Mitochondrial Targeted Interventions in Alzheimer’s Disease
de Sousa, T. S., Moreira, P. I., & Cardoso, S. (2023) · Biomedicines · doi:10.3390/biomedicines11092331 · Cited by 21 · see citing works
Baringer, S. L., Lukacher, A. S., Palsa, K., Kim, H., Lippmann, E. S., Spiegelman, V. S., Simpson, I. A., & Connor, J. R. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15954 · Cited by 20 · see citing works
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Self-citationKong, Y., Maschio, C., Shi, X., Yao, B., Xie, F., Zuo, C., Konietzko, U., Shi, K., Rominger, A., Xiao, J., et al. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04106-7 · Cited by 17 · see citing works
Noncanonical regulation of imprinted gene Igf2 by amyloid-beta 1–42 in Alzheimer’s disease
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Potassium homeostasis during disease progression of Alzheimer's disease
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Self-citationHIF-1α Pathway Orchestration by LCN2: A Key Player in Hypoxia-Mediated Colitis Exacerbation
Yang, Y.-H., Yan, F., Shi, P.-S., Yang, L.-C., & Cui, D. (2024) · Inflammation · doi:10.1007/s10753-024-01990-y · Cited by 11 · see citing works
Walker, V. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26157328 · Cited by 11 · see citing works
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Self-citationAmeen, A. O., Nielsen, S. W., Kjær, M. W., Andersen, J. V., Westi, E., Freude, K., & Aldana, B. (2024) · Journal of Cerebral Blood Flow and Metabolism · doi:10.1177/0271678x241270457 · Cited by 11 · see citing works
Self-citationLopes, C. R., Silva, J. S., Santos, J., Rodrigues, M. S., Madeira, D., Oliveira, A., Moreira-de-Sá, A., Lourenço, V. S., Gonçalves, F. Q., Silva, H. B. L., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24086968 · Cited by 10 · see citing works
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Correlations of blood and brain NMR metabolomics with Alzheimer’s disease mouse models
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CNS Mitochondria‐Derived Vesicle in Blood: Potential Biomarkers for Brain Mitochondria Dysfunction
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Disrupted astrocyte-neuron signaling reshapes brain activity in epilepsy and Alzheimer’s disease
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Spatial and cellular composition of lung fibrosis induced by multi-walled carbon nanotubes
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Emerging roles of astrocytes in hippocampal circuitry and behavior
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Fueling Alzheimer’s Disease: Where Does Immunometabolism Stand?
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5xFAD mutations induce hearing impairment in the Ahl-corrected 5xFAD mice
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Central cytometabolic functional vascular coupling in health and disease
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Fueling Brain Inhibition: Integrating GABAergic Neurotransmission and Energy Metabolism
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NMR metabolomics in genetically engineered mouse models
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Impaired docking and recycling of synaptic vesicles in inherited lysosomal sphingolipidoses
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Self-citationAltered Metabolic Signaling and Potential Therapies in Polyglutamine Diseases
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Metabolic Regulation as a Potential Therapeutic Approach for Alzheimer's Disease
Zhong, J., Sun, J., & Zhou, B. (2025) · Current Alzheimer Research · doi:10.2174/0115672050379410250421065857
Wegener, A. J., Stadtler, H., Fulenwider, H. D., Glasper, E. R., & Neigh, G. N. (2025) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2025.101087
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Han, Y., Zeng, X., Hua, L., Quan, X., Chen, Y., Zhou, M., Chuang, Y., Li, Y., Wang, S., Shen, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26669625
Wang, W., Zhao, F., Lu, Y., Siedlak, S. L., Fujioka, H., Feng, H., Perry, G., & Zhu, X. (2024) · Figshare · doi:10.6084/m9.figshare.26579702
Han, Y., Zeng, X., Hua, L., Quan, X., Chen, Y., Zhou, M., Chuang, Y., Li, Y., Wang, S., Shen, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26669616
Han, Y., Zeng, X., Hua, L., Quan, X., Chen, Y., Zhou, M., Chuang, Y., Li, Y., Wang, S., Shen, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26669631
- Authors
- Andersen, J. V., Skotte, N. H., Christensen, S. K., Polli, F. S., Shabani, M., Markussen, K. H., Haukedal, H., Westi, E. W., Diaz-delCastillo, M., Sun, R. C., Kohlmeier, K. A., Schousboe, A., Gentry, M. S., Tanila, H., Freude, K. K., Aldana, B. I., Mann, M., & Waagepetersen, H. S.
- Affiliations
- University of Copenhagen (DK)
- Scripps Research Institute (US)
- Kerman University of Medical Sciences (IR)
- University of Kentucky (US)
- University of Eastern Finland (FI)
- Corresponding author
- Andersen, Jens V.
- Waagepetersen, Helle S.
- ORCID
- Venue
- Cell Death & Disease
- Published
- 2021-10-16
- Volume
- 12
- Issue
- 11
- Pages
- 954-954
- ISSN
- 2041-4889 (ISSN-L)
- PMC
- PMC8520528
- OpenAlex
- W3206998885
- Cited by
- 104
- References
- 82
- Citations by year
- 2026: 15 · 2025: 28 · 2024: 21 · 2023: 30 · 2022: 10
- FWCI
- 11.15
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Cell Death and Disease (publishedVersion, cc-by)
- SSRN Electronic Journal (acceptedVersion)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, cc-by)
- University of Southern Denmark Research Portal (University of Southern Denmark) (acceptedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Hørslev-Fonden (203866)
- Lundbeckfonden (R333‐2019‐1244, NNF14CC0001, R211-2015-3062, R338-2019-2997, R208‐2015‐2859)
- Novo Nordisk (NNF14CC0001, NNF15CC0001)
- Augustinus Fonden (18-1624)
- Novo Nordisk Fonden (NNF 14CC0001, NNF18OC0052369, NNF15CC0001)
- Grosserer L. F. Foghts Fond
- H. Lundbeck A/S
- National Institutes of Health
- National Institute on Aging (R01AG066653)
- National Institute of Neurological Disorders and Stroke (R35NS116824)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- Alzheimer's disease, 5xFAD mice, amyloid-beta deposition, hippocampus, astrocytes, neuronal metabolism, TCA cycle, glutamine synthesis, GABA synthesis, glucose oxidation, mitochondrial dysfunction, glycolysis, synaptic dysfunction, neuronal hyperexcitability, cerebral cortex, brain energy metabolism, 13C isotope tracing
- MeSH terms
- Alzheimer Disease, Amyloid, Animals, Astrocytes, Cerebral Cortex, Citric Acid Cycle, Disease Models, Animal, Energy Metabolism, Glucose, Glutamine, Glycolysis, Hippocampus, Male, Mice, Transgenic, Mitochondria, Synapses, Signal Transduction, Neurotransmitter Agents, Proteome, Metabolome
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