Cited by 163Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeurological Disease Mechanisms and Treatments

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High-fat diet-induced deregulation of hippocampal insulin signaling and mitochondrial homeostasis deficiences contribute to Alzheimer disease pathology in rodents

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Petrov, Dmitry, Pedrós, Ignacio, Artiach, Gonzalo, Sureda, Francesc X., Barroso, Emma, Pallàs, Mercè, Casadesús, Gemma, Beas-Zarate, Carlos, Carro, Eva, Ferrer, Isidro, Vazquez-Carrera, Manuel, Folch, Jaume, Camins, Antoni·2015·Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease

DOI 10.1016/j.bbadis.2015.05.004

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Abstract

Global obesity is a pandemic status, estimated to affect over 2 billion people, that has resulted in an enormous strain on healthcare systems worldwide. The situation is compounded by the fact that apart from the direct costs associated with overweight pathology, obesity presents itself with a number of comorbidities, including an increased risk for the development of neurodegenerative disorders. Alzheimer disease (AD), the main cause of senile dementia, is no exception. Spectacular failure of the pharmaceutical industry to come up with effective AD treatment strategies is forcing the broader scientific community to rethink the underlying molecular mechanisms leading to cognitive decline. To this end, the emphasis is once again placed on the experimental animal models of the disease. In the current study, we have focused on the effects of a high-fat diet (HFD) on hippocampal-dependent memory in C57/Bl6 Wild-type (WT) and APPswe/PS1dE9 (APP/PS1) mice, a well-established mouse model of familial AD. Our results indicate that the continuous HFD administration starting at the time of weaning is sufficient to produce β-amyloid-independent, hippocampal-dependent memory deficits measured by a 2-object novel-object recognition test (NOR) in mice as early as 6months of age. Furthermore, the resulting metabolic syndrome appears to have direct effects on brain insulin regulation and mitochondrial function. We have observed pathological changes related to both the proximal and distal insulin signaling pathway in the brains of HFD-fed WT and APP/PS1 mice. These changes are accompanied by a significantly reduced OXPHOS metabolism, suggesting that mitochondria play an important role in hippocampus-dependent memory formation and retention in both the HFD-treated and AD-like rodents at a relatively young age.

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Seung, T. W., Park, S. K., Kang, J. Y., Kim, J. M., Park, S. H., Kwon, B. S., Lee, C. J., Kang, J. E., Kim, D., Lee, U., et al. (2017) · Food Research International · doi:10.1016/j.foodres.2017.11.063 · Cited by 39
Worsening of memory deficit induced by energy-dense diet in a rat model of early-Alzheimer's disease is associated to neurotoxic Aβ species and independent of neuroinflammation
Adami, P. V. M., Galeano, P., Wallinger, M. L., Quijano, C., Rabossi, A., Pagano, E. S., Olivar, N., Toso, C. R., Cardinali, D. P., Brusco, L. I., et al. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2016.12.014 · Cited by 39
Longitudinal investigation of neuroinflammation and metabolite profiles in the APP swe× PS 1Δe9 transgenic mouse model of Alzheimer's disease
Chaney, A. M., Bauer, M., Bochicchio, D., Smigova, A., Kassiou, M., Davies, K. E., Williams, S. R., & Boutin, H. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14251 · Cited by 38
“Cognitive deficits in these tests have been previously reported in both this (Petrov et al. 2015) and other amyloid-based models of AD (Forster et al. 2013; Daniels et al. 2016; Martins et al. 2017), further supporting the link between pathology burden and cognitive decline.”
Result
High-Fat Diets in Animal Models of Alzheimer’s Disease: How Can Eating Too Much Fat Increase Alzheimer’s Disease Risk?
Valentin‐Escalera, J., Leclerc, M., & Calon, F. (2024) · Journal of Alzheimer s Disease · doi:10.3233/jad-230118 · Cited by 37
Omega-3 fatty acids revert high-fat diet-induced neuroinflammation but not recognition memory impairment in rats
de Andrade, A. M., Fernandes, M. D. C., de Fraga, L. S., Porawski, M., Giovenardi, M., & Guedes, R. P. (2017) · Metabolic Brain Disease · doi:10.1007/s11011-017-0080-7 · Cited by 39
Sugar Consumption Produces Effects Similar to Early Life Stress Exposure on Hippocampal Markers of Neurogenesis and Stress Response
Maniam, J., Antoniadis, C. P., Youngson, N. A., Sinha, J. K., & Morris, M. J. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2015.00086 · Cited by 35
Diabetic phenotype in mouse and humans reduces the number of microglia around β-amyloid plaques
Natunen, T., Martiskainen, H., Marttinen, M., Gabbouj, S., Koivisto, H., Kemppainen, S., Kaipainen, S., Takalo, M., Svobodová, H., Leppänen, L., et al. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00415-2 · Cited by 36
“We successfully induced obesity and diabetic phenotype in all of the mouse lines used by applying a sixmonth TWD regime, starting at the age of 7 months, which is in line with previous reports [13, 16, 20, 82].”
BackgroundResultInfluential
Abscisic Acid Supplementation Rescues High Fat Diet-Induced Alterations in Hippocampal Inflammation and IRSs Expression
Ribes‐Navarro, A., Atef, M., Sánchez‐Sarasúa, S., Beltrán-Bretones, M. T., Olucha-Bordonau, F. E., & Sánchez‐Pérez, A. M. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1091-z · Cited by 35
Chronic consumption of Annona muricata juice triggers and aggravates cerebral tau phosphorylation in wild‐type and MAPT transgenic mice
Rottscholl, R., Haegele, M., Jainsch, B., Xu, H. W., Respondek, G., Höllerhage, M., Rösler, T. W., Bony, E., Ven, J. L., Guérineau, V., et al. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13835 · Cited by 33
Peripheral and Central Effects of Memantine in a Mixed Preclinical Mice Model of Obesity and Familial Alzheimer’s Disease
Ettcheto, M., Sánchez‐López, E., Gómez-Mínguez, Y., Cabrera, H., Busquets, O., Beas‐Zárate, C., García, M. L., Carro, E., Casadesús, G., Auladell, C., et al. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-0868-4 · Cited by 32
High-Fat Diet Leads to Reduced Protein O-GlcNAcylation and Mitochondrial Defects Promoting the Development of Alzheimer’s Disease Signatures
Zuliani, I., Lanzillotta, C., Tramutola, A., Barone, E., Marzia Perluigi, A., Rinaldo, S., Paone, A., Cutruzzolà, F., Bellanti, F., Spinelli, M., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22073746 · Cited by 32
“…Western-style diet [12], thus leading to obesity and T2DM, demonstrated impaired performance in learning and memory tasks, alterations of synaptic integrity, altered CA1-related long-term depression (LTD) and long-term potentiation (LTP), and the development of AD pathological hallmarks [13–16].”
Mechanisms of multiple neurotransmitters in the effects of Lycopene on brain injury induced by Hyperlipidemia
Yang, W., Shen, Z., Wen, S., Wang, W., & Hu, M. (2018) · Lipids in Health and Disease · doi:10.1186/s12944-018-0660-5 · Cited by 32
“[1, 2], but is also closely related to neurodegenerative diseases such as Alzheimer’s disease (AD) [3, 4], Parkinson’s disease [5], and anxiety [6, 7].”
Orexin A attenuates palmitic acid-induced hypothalamic cell death
Duffy, C. M., Nixon, J. P., & Butterick, T. A. (2016) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2016.07.003 · Cited by 31
“Mutations in mitochondrial proteins, impaired mitochondrial dynamics and respiration, and increased ROS production are associated with neurodegenerative diseases such as obesity, Alzheimer's disease, and Parkinson's disease (Cai and Tammineni, 2016; Petrov et al., 2015; Raza et al., 2015; Van Laar and Berman, 2009; Zo…”
Background
A metabolic perspective of late onset Alzheimer’s disease
Ettcheto, M., Cano, A. C., Busquets, O., Manzine, P. R., Sánchez‐López, E., Castro-Torres, R. D., Beas‐Zárate, C., Verdaguer, E., García, M. L., Olloquequi, J., et al. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104255 · Cited by 31
Mitochondria in Alzheimer’s Disease and Diabetes-Associated Neurodegeneration: License to Heal!
Cardoso, S., Correia, S. C., Carvalho, C., & Moreira, P. I. (2017) · Handbook of experimental pharmacology · doi:10.1007/164_2017_3 · Cited by 29
Physical exercise consequences on memory in obesity: A systematic review
Sousa, R. A. L. D., Santos, L. G., Lopes, P. M., Cavalcante, B. R. R., Caria, A. C. I., & Cassilhas, R. C. (2021) · Obesity Reviews · doi:10.1111/obr.13298 · Cited by 29
Obesity and neuroinflammatory phenotype in mice lacking endothelial megalin
Bartolomé, F. B., Antequera, D., Tavares, E., Pascual, C., Maldonado, R., Camins, A., & Carro, E. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0800-2 · Cited by 30
“Obesity has been linked to mitochondrial alterations, [14, 15].”
Background
Role of c-Jun N-Terminal Kinases (JNKs) in Epilepsy and Metabolic Cognitive Impairment
Busquets, O., Ettcheto, M., Cano, A. C., Manzine, P. R., Sánchez‐López, E., Espinosa-Jiménez, T., Verdaguer, E., Castro-Torres, R. D., Beas‐Zárate, C., Sureda, F. X., et al. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms21010255 · Cited by 28
Diabesity and brain disturbances: A metabolic perspective
Cardoso, S., & Moreira, P. I. (2018) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2018.10.002 · Cited by 31
Evaluation of the neuroprotective effect of donepezil in type 2 diabetic rats
Gomaa, A. A., Makboul, R. M., El‐Mokhtar, M. A., Abdel‐Rahman, E. A., Ahmed, E. A., & Nicola, M. A. (2020) · Fundamental and Clinical Pharmacology · doi:10.1111/fcp.12585 · Cited by 26
Neuroprotective role of alendronate against APP processing and neuroinflammation in mice fed a high fat diet
Zameer, S., Alam, M. M., Hussain, S., Vohora, D., Ali, J., Najmi, A. K., & Akhtar, M. (2020) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.04.010 · Cited by 26
Lipoic acid improves neuronal insulin signalling and rescues cognitive function regulating VGlut1 expression in high-fat-fed rats: Implications for Alzheimer's disease
Rodriguez‐Perdigon, M., Solas, M., Moreno-Aliaga, M. J., & Ramírez, M. J. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2016.01.004 · Cited by 26
Disruption of leptin signalling in a mouse model of Alzheimer’s disease
King, A. E., Brain, A., Hanson, K., Dittmann, J., Vickers, J. C., & Fernández-Martos, C. M. (2018) · Metabolic Brain Disease · doi:10.1007/s11011-018-0203-9 · Cited by 27
Tetrahydrobiopterin Improves Recognition Memory in the Triple-Transgenic Mouse Model of Alzheimer’s Disease, Without Altering Amyloid-β and Tau Pathologies
Fanet, H., Tournissac, M., Leclerc, M., Caron, V., Tremblay, C., Vancassel, S., & Calon, F. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-200637 · Cited by 24
Metformin attenuates vascular pathology by increasing expression of insulin-degrading enzyme in a mixed model of cerebral amyloid angiopathy and type 2 diabetes mellitus
Inoue, Y., Masuda, T., Misumi, Y., Ando, Y., & Ueda, M. (2021) · Neuroscience Letters · doi:10.1016/j.neulet.2021.136136 · Cited by 25
A high fat, sugar, and salt Western diet induces motor‐muscular and sensory dysfunctions and neurodegeneration in mice during aging: Ameliorative action of metformin
Hong, S., Nagayach, A., Lü, Y., Peng, H., Duong, Q.-V., Pham, N. B., Vuong, C. A., & Bazan, N. G. (2021) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13726 · Cited by 24
Inflammation, Nitro-Oxidative Stress, Impaired Autophagy, and Insulin Resistance as a Mechanistic Convergence Between Arterial Stiffness and Alzheimer’s Disease
Hendrickx, J. O., Martinet, W., Dam, D. V., & Meyer, G. R. Y. D. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.651215 · Cited by 28
Animal Models of Alzheimer’s Disease
Newman, M., Kretzschmar, D., Khan, I., Chen, M., Verdile, G., & Lardelli, M. T. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809468-6.00040-1 · Cited by 25
Diabesity and Brain Energy Metabolism: The Case of Alzheimer’s Disease
Cardoso, S., Seiça, R. M. F., & Moreira, P. I. (2017) · Advances in neurobiology · doi:10.1007/978-3-319-63260-5_5 · Cited by 24
High-fat diet induced discrepant peripheral and central nervous systems insulin resistance in APPswe/PS1dE9 and wild-type C57BL/6J mice
Guo, Y., Ma, X., Li, P., Dong, S., Huang, X., Ren, X., & Yuan, L. (2020) · Aging · doi:10.18632/aging.202262 · Cited by 21
“We speculate that the HFD-mediated elevation of peripheral insulin might neutralize or counteract the existed selfcompensatory activation of insulin signaling in brain of APP/PS1 mice [39], and ultimately inhibit the activation of insulin receptor and its downstream targets.”
Background
Circulating Insulin-Like Growth Factor I is Involved in the Effect of High Fat Diet on Peripheral Amyloid β Clearance
Herrero-Labrador, R., Trueba-Sáiz, Á., Martinez‐Rachadell, L., de Sevilla, M. E. F., Zegarra-Valdivia, J. A., Pignatelli, J., Díaz-Pacheco, S., Fernandez, A. M., & Torres‐Alemán, I. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21249675 · Cited by 22
“Further, previous studies using the APP/PS1 mouse model of AD had shown that HFD interferes with central and peripheral insulin signaling [55], which is largely shared by IGF-I.”
Mitochondrial Ultrastructure and Glucose Signaling Pathways Attributed to the Kv1.3 Ion Channel
Kovach, C. P., Al Koborssy, D., Huang, Z., Chelette, B. M., Fadool, J. M., & Fadool, D. A. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00178 · Cited by 20
“Similar effects of high-fat diet on mitochondrial function have been observed in the central nervous system (Petrov et al., 2015).”
Background
Astaxanthin Esters as Functional Food: A Review of Their Nutrition, Phytochemical Structure, Biological Features, and Food Industry Prospects
Wang, Y., Chen, L., Zhao, J., Xia, G., Liu, Z., & Shi, H.-Q. L. W.-M. (2024) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.4c00765 · Cited by 20
Sweet Mitochondria: A Shortcut to Alzheimer’s Disease
Moreira, P. I. (2018) · Journal of Alzheimer’s Disease · doi:10.3233/jad-170931 · Cited by 20
Long-Term Ingestion of Sicilian Black Bee Chestnut Honey and/or D-Limonene Counteracts Brain Damage Induced by High Fat-Diet in Obese Mice
Terzo, S., Calvi, P., Nuzzo, D., Picone, P., Allegra, M., Mulè, F., & Amato, A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043467 · Cited by 19
Dietary composition affects the development of cognitive deficits in WT and Tg AD model mice
Kadish, I., Kumar, A., Beitnere, U., Jennings, E., McGilberry, W., & van Groen, T. (2016) · Experimental Gerontology · doi:10.1016/j.exger.2016.05.003 · Cited by 20
The exposome from neurodevelopment to neurodegeneration: A narrative review
Dallere, S., Rasà, D. M., Pavarino, G., Schellino, R., Vercelli, A., & Boido, M. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106247 · Cited by 21
Assessment of Cognitive Impairment in a Mouse Model of High-Fat Diet-Induced Metabolic Stress with Touchscreen-Based Automated Battery System
Lee, S., Kim, J. Y., Kim, E., Seo, K. Y., Kang, Y. J., Kim, J. Y., Kim, C. H., Song, H., Saksida, L. M., & Lee, J. E. (2018) · Experimental Neurobiology · doi:10.5607/en.2018.27.4.277 · Cited by 18
“According to previous studies, HFD increases hippocampal oxidative stress, which reduces NF-E2related factor 2 signaling [24], causes mitochondrial homeostasis deficiency [25], and impairs hippocampus-dependent memory function [26].”
Background
Fluoxetine administration in juvenile overfed rats improves hypothalamic mitochondrial respiration and REDOX status and induces mitochondrial biogenesis transcriptional expression
Braz, G. R. F., Silva, S. C. D. A., Pedroza, A. A. D. S., de Lemos, M. D. T. B., de Lima, F. A. S., da Silva, A. I., & Lagranha, C. J. (2020) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2020.173200 · Cited by 18
Insulin deficiency, but not resistance, exaggerates cognitive deficits in transgenic mice expressing human amyloid and tau proteins. Reversal by Exendin‐4 treatment
King, M. R., Anderson, N. J., Deciu, M., Guernsey, L. S., Cundiff, M., Hajizadeh, S., & Jolivalt, C. G. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24706 · Cited by 18
“In addition, Petrov et al (Petrov et al., 2015) showed that phosphorylated tau levels were not increased and alterations in cerebral amyloid levels did not play a critical role in memory loss of APP-PS1 transgenic mice when fed HFD from weaning for 6 months.”
Background
Inhibition of ANGPTL8 protects against diabetes-associated cognitive dysfunction by reducing synaptic loss via the PirB signaling pathway
Meng, X., Li, D., Kan, R., Xiang, Y., Pan, L., Guo, Y., Yu, P., Luo, P., Zou, H., Huang, L. T., et al. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03183-8 · Cited by 19
“According to previous studies, neuroinflammation and memory impairment occurred in mice fed a HFD for 4–6 months [24, 25] and db/db mice fed a ND for over 6 months [26–28].”
Method
Hypothalamic-pituitary-adrenal (HPA) axis activity and anxiety-like behavior during aging: A test of the glucocorticoid cascade hypothesis in amyloidogenic APPswe/PS1dE9 mice
Harris, B. N., Roberts, B. R., DiMarco, G. M., Maldonado, K. A., Okwunwanne, Z., Savonenko, A. V., & Soto, P. L. (2022) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2022.114126 · Cited by 19
Pleiotrophin deficiency protects against high-fat diet-induced neuroinflammation: Implications for brain mitochondrial dysfunction and aberrant protein aggregation
Cañeque‐Rufo, H., Sánchez‐Alonso, M. G., Zuccaro, A., Sevillano, J., Ramos, P., & Herradón, G. (2022) · Food and Chemical Toxicology · doi:10.1016/j.fct.2022.113578 · Cited by 14
High-fat diet feeding triggers a regenerative response in the adult zebrafish brain
Azbazdar, Y., Poyraz, Y. K., Özalp, Ö., Nazli, D., Ipekgil, D., Cucun, G., & Özhan, G. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03210-4 · Cited by 15
“In addition to its adverse effects on the liver (Lian et al., 2020), dietary changes including HFD have been associated with brain disorders including dementia, Alzheimer’s disease, and Parkinson’s disease (Morris et al., 2010; Pistell et al., 2010; Petrov et al., 2015; Nuzzo et al., 2018).”
Background
Effect of Aruncus dioicus var. kamtschaticus Extract on Neurodegeneration Improvement: Ameliorating Role in Cognitive Disorder Caused by High-Fat Diet Induced Obesity
Park, S. B., Kang, J. Y., Kim, J. M., Park, S. K., Yoo, S. K., Lee, U., Kim, D., & Heo, H. J. (2019) · Nutrients · doi:10.3390/nu11061319 · Cited by 15
“CNS-IR that is caused by peripheral-IR induces insulin deficiency and hyperglycemia in the brain, resulting in damage to mitochondrial metabolism and neuronal apoptosis, and further causing excessive levels of oxidative stress [7,23,25].”
BackgroundInfluential

Authors: Petrov, D., Pedrós, I., Artiach, G., Sureda, F. X., Barroso, E., Pallàs, M., Casadesús, G., Beas-Zarate, C., Carro, E., Ferrer, I., Vazquez-Carrera, M., Folch, J., & Camins, A.
Affiliations: Biomedical Research Networking Center on Neurodegenerative Diseases (ES)
Centro de Investigación Biomédica en Red Diabetes y Enfermedades Metabólicas Asociadas (ES)
Kent State University (US)
Research Institute Hospital 12 de Octubre (ES)
Corresponding author: Camins, Antoni
ORCID: Sureda, Francesc X.
Barroso, Emma
Pallàs, Mercè
Casadesús, Gemma
Carro, Eva
Folch, Jaume
Camins, Antoni
Venue: Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease
Publisher: Elsevier BV
Published: 2015-09
Volume: 1852
Issue: 9
Pages: 1687-1699
ISSN: 0925-4439 (ISSN-L)
DOI: 10.1016/j.bbadis.2015.05.004
OpenAlex: W256530927
Cited by: 163
References: 78
Citations by year: 2026: 6 · 2025: 4 · 2024: 15 · 2023: 14 · 2022: 14 · 2021: 19 · 2020: 17 · 2019: 14 · 2018: 24 · 2017: 10 · 2016: 22 · 2015: 3
FWCI: 14.47
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 366 d)
Locations: Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease (publishedVersion)
PubMed (publishedVersion)
Funders: Generalitat de Catalunya (2009/SGR00853)
Spanish Ministerio de Ciencia e Innovación (SAF2011-23631, SAF2012-39852-C02-01, SAF2012-30708)
CONACYT (Mexico) (0177594)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
Keywords: high-fat diet, Alzheimer's disease, hippocampus, insulin signaling, mitochondrial homeostasis, metabolic syndrome, obesity, APP/PS1 mice, novel object recognition, hippocampal-dependent memory, oxidative phosphorylation, neurodegeneration

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High-fat diet-induced deregulation of hippocampal insulin signaling and mitochondrial homeostasis deficiences contribute to Alzheimer disease pathology in rodents

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