Docosahexaenoic acid enhances hippocampal insulin sensitivity to promote cognitive function of aged rats on a high-fat diet

Small, 2011, A pathophysiological framework of hippocampal dysfunction in ageing and disease, Nat Rev Neurosci, 12, 585, 10.1038/nrn3085 Swerdlow, 2007, Is aging part of Alzheimer's disease, or is Alzheimer's disease part of aging?, Neurobiol Aging, 28, 1465, 10.1016/j.neurobiolaging.2006.06.021 Rajagopal, 2016, Functional Deficits Precede Structural Lesions in Mice With High-Fat Diet-Induced Diabetic Retinopathy, Diabetes, 65, 1072, 10.2337/db15-1255 Rao, 2016, Inhibition of ileal bile acid uptake protects against nonalcoholic fatty liver disease in high-fat diet–fed mice, Sci Transl Med, 8, 10.1126/scitranslmed.aaf4823 Kim, 2016, Obesity and cardiovascular disease: friend or foe?, Eur Heart J, 37, 3560, 10.1093/eurheartj/ehv509 Apovian, 2012, Obesity and cardiovascular disease, Circulation, 125, 1178, 10.1161/CIRCULATIONAHA.111.022541 Wolin, 2010, Obesity and cancer, Oncologist, 15, 556, 10.1634/theoncologist.2009-0285 Raider, 2016, A high fat diet alters metabolic and bioenergetic function in the brain: A magnetic resonance spectroscopy study, Neurochem Int, 97, 172, 10.1016/j.neuint.2016.04.008 Langley, 2020, High fat diet consumption results in mitochondrial dysfunction, oxidative stress, and oligodendrocyte loss in the central nervous system, Biochim Biophys Acta Mol Basis Dis, 1866, 165630, 10.1016/j.bbadis.2019.165630 Uranga, 2010, Intersection between metabolic dysfunction, high fat diet consumption, and brain aging, J Neurochem, 114, 344, 10.1111/j.1471-4159.2010.06803.x Kullmann, 2016, Brain Insulin Resistance at the Crossroads of Metabolic and Cognitive Disorders in Humans, Physiol Rev, 96, 1169, 10.1152/physrev.00032.2015 Kullmann, 2020, Central nervous pathways of insulin action in the control of metabolism and food intake, Lancet Diabetes Endocrinol, 8, 524, 10.1016/S2213-8587(20)30113-3 Arnold, 2018, Brain insulin resistance in type 2 diabetes and Alzheimer disease: concepts and conundrums, Nat Rev Neurol, 14, 168, 10.1038/nrneurol.2017.185 Spinelli, 2017, Brain insulin resistance impairs hippocampal synaptic plasticity and memory by increasing GluA1 palmitoylation through FoxO3a, Nat Commun, 8, 10.1038/s41467-017-02221-9 Talbot, 2012, Demonstrated brain insulin resistance in Alzheimer's disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline, J Clin Invest, 122, 1316, 10.1172/JCI59903 Neves, 2018, Brain-Defective Insulin Signaling Is Associated to Late Cognitive Impairment in Post-Septic Mice, Mol Neurobiol, 55, 435, 10.1007/s12035-016-0307-3 Bomfim, 2012, An anti-diabetes agent protects the mouse brain from defective insulin signaling caused by Alzheimer's disease- associated Abeta oligomers, J Clin Invest, 122, 1339, 10.1172/JCI57256 Freiherr, 2013, Intranasal insulin as a treatment for Alzheimer's disease: a review of basic research and clinical evidence, CNS Drugs, 27, 505, 10.1007/s40263-013-0076-8 Scherer, 2021, Brain insulin signalling in metabolic homeostasis and disease, Nat Rev Endocrinol, 17, 468, 10.1038/s41574-021-00498-x Yarchoan, 2014, Repurposing diabetes drugs for brain insulin resistance in Alzheimer disease, Diabetes, 63, 2253, 10.2337/db14-0287 Ramakrishnan, 2009, Role of docosahexaenoic acid in maternal and child mental health, Am J Clin Nutr, 89, 958S, 10.3945/ajcn.2008.26692F K.M. Appleton, P.D. Voyias, H.M. Sallis, S. Dawson, A.R. Ness, R. Churchill, et al., Omega-3 fatty acids for depression in adults. Cochrane Database Syst Rev. 11(2021)CD004692.doi:10.1002/14651858.CD004692.pub5. Cutuli, 2017, Functional and Structural Benefits Induced by Omega-3 Polyunsaturated Fatty Acids During Aging, Curr Neuropharmacol, 15, 534, 10.2174/1570159X14666160614091311 Bazan, 2011, Docosahexaenoic acid signalolipidomics in nutrition: significance in aging, neuroinflammation, macular degeneration, Alzheimer's, and other neurodegenerative diseases, Annu Rev Nutr, 31, 321, 10.1146/annurev.nutr.012809.104635 Bazinet, 2014, Polyunsaturated fatty acids and their metabolites in brain function and disease, Nat Rev Neurosci, 15, 771, 10.1038/nrn3820 Quinn, 2010, Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial, JAMA, 304, 1903, 10.1001/jama.2010.1510 Yurko-Mauro, 2010, Cognitive and cardiovascular benefits of docosahexaenoic acid in aging and cognitive decline, Curr Alzheimer Res, 7, 190, 10.2174/156720510791050911 Luo, 2016, Docosahexaenoic acid attenuates adipose tissue angiogenesis and insulin resistance in high fat diet-fed middle-aged mice via a sirt1-dependent mechanism, Mol Nutr Food Res, 60, 871, 10.1002/mnfr.201500714 Lanza, 2013, Influence of fish oil on skeletal muscle mitochondrial energetics and lipid metabolites during high-fat diet, Am J Physiol Endocrinol Metab, 304, E1391, 10.1152/ajpendo.00584.2012 Storlien, 1987, Fish oil prevents insulin resistance induced by high-fat feeding in rats, Science, 237, 885, 10.1126/science.3303333 Hughey, 2011, Hyperinsulinemic-euglycemic clamp in the conscious rat, J Vis Exp, 10.3791/2432-v Gao, 2016, Long-Term Dietary Alpha-Linolenic Acid Supplement Alleviates Cognitive Impairment Correlate with Activating Hippocampal CREB Signaling in Natural Aging Rats, Mol Neurobiol, 53, 4772, 10.1007/s12035-015-9393-x Gorgich, 2021, Long-term administration of metformin ameliorates age-dependent oxidative stress and cognitive function in rats, Behav Brain Res, 410, 113343, 10.1016/j.bbr.2021.113343 Alvarez, 2007, Anatomical and physiological plasticity of dendritic spines, Annu Rev Neurosci, 30, 79, 10.1146/annurev.neuro.30.051606.094222 Karpova, 2013, Encoding and transducing the synaptic or extrasynaptic origin of NMDA receptor signals to the nucleus, Cell, 152, 1119, 10.1016/j.cell.2013.02.002 Benedict, 2008, Differential sensitivity of men and women to anorexigenic and memory-improving effects of intranasal insulin, J Clin Endocrinol Metab, 93, 1339, 10.1210/jc.2007-2606 Benedict, 2007, Intranasal insulin improves memory in humans: superiority of insulin aspart, Neuropsychopharmacology, 32, 239, 10.1038/sj.npp.1301193 Duda, 2018, Targeting GSK3 signaling as a potential therapy of neurodegenerative diseases and aging, Expert Opin Ther Targets, 22, 833, 10.1080/14728222.2018.1526925 Yamamoto, 2012, Brain insulin resistance accelerates Abeta fibrillogenesis by inducing GM1 ganglioside clustering in the presynaptic membranes, J Neurochem, 121, 619, 10.1111/j.1471-4159.2012.07668.x Stanley, 2016, Changes in insulin and insulin signaling in Alzheimer's disease: cause or consequence?, J Exp Med, 213, 1375, 10.1084/jem.20160493 Biessels, 2015, Hippocampal insulin resistance and cognitive dysfunction, Nat Rev Neurosci, 16, 660, 10.1038/nrn4019 Llorens-Martin, 2014, GSK-3beta, a pivotal kinase in Alzheimer disease, Front Mol Neurosci, 7, 46 Neschen, 2007, n-3 Fatty acids preserve insulin sensitivity in vivo in a peroxisome proliferator-activated receptor-alpha-dependent manner, Diabetes, 56, 1034, 10.2337/db06-1206 Takeda, 2010, Diabetes-accelerated memory dysfunction via cerebrovascular inflammation and Abeta deposition in an Alzheimer mouse model with diabetes, Proc Natl Acad Sci U S A, 107, 7036, 10.1073/pnas.1000645107 Rosales-Corral, 2015, Diabetes and Alzheimer disease, two overlapping pathologies with the same background: oxidative stress, Oxid Med Cell Longev, 2015, 1, 10.1155/2015/985845 Perluigi, 2014, Redox proteomics and the dynamic molecular landscape of the aging brain, Ageing Res Rev, 13, 75, 10.1016/j.arr.2013.12.005 Manolopoulos, 2010, Linking Alzheimer's disease to insulin resistance: the FoxO response to oxidative stress, Mol Psychiatry, 15, 1046, 10.1038/mp.2010.17 Bloch-Damti, 2005, Proposed mechanisms for the induction of insulin resistance by oxidative stress, Antioxid Redox Signal, 7, 1553, 10.1089/ars.2005.7.1553 Rains, 2011, Oxidative stress, insulin signaling, and diabetes, Free Radic Biol Med, 50, 567, 10.1016/j.freeradbiomed.2010.12.006 Tong, 2005, Oxidative stress potentiates BACE1 gene expression and Abeta generation, J Neural Transm (Vienna), 112, 455, 10.1007/s00702-004-0255-3 Gao, 2016, Maternal DHA supplementation protects rat offspring against impairment of learning and memory following prenatal exposure to valproic acid, J Nutr Biochem, 35, 87, 10.1016/j.jnutbio.2016.07.003 Johansson, 2015, The marine n-3 PUFA DHA evokes cytoprotection against oxidative stress and protein misfolding by inducing autophagy and NFE2L2 in human retinal pigment epithelial cells, Autophagy, 11, 1636, 10.1080/15548627.2015.1061170 Mayo, 2014, Regulation of astrocyte activation by glycolipids drives chronic CNS inflammation, Nat Med, 20, 1147, 10.1038/nm.3681 Heppner, 2005, Experimental autoimmune encephalomyelitis repressed by microglial paralysis, Nat Med, 11, 146, 10.1038/nm1177 Domínguez-González, 2018, Regional vulnerability to lipoxidative damage and inflammation in normal human brain aging, Exp Gerontol, 111, 218, 10.1016/j.exger.2018.07.023 Matt, 2016, Neuro-immune dysfunction during brain aging: new insights in microglial cell regulation, Curr Opin Pharmacol, 26, 96, 10.1016/j.coph.2015.10.009 Esiri, 2007, Ageing and the brain, J Pathol, 211, 181, 10.1002/path.2089 Kim, 2019, Microglial UCP2 Mediates Inflammation and Obesity Induced by High-Fat Feeding, Cell Metab, 30, 952, 10.1016/j.cmet.2019.08.010 Denver, 2018, Sustained high-fat diet modulates inflammation, insulin signalling and cognition in mice and a modified xenin peptide ameliorates neuropathology in a chronic high-fat model, Diabetes Obes Metab, 20, 1166, 10.1111/dom.13210 Xu, 2019, Melatonin alleviates cognition impairment by antagonizing brain insulin resistance in aged rats fed a high-fat diet, J Pineal Res, 67, 10.1111/jpi.12584 Thaler, 2012, Obesity is associated with hypothalamic injury in rodents and humans, J Clin Invest, 122, 153, 10.1172/JCI59660 Liu, 2014, The role of inflammasome in Alzheimer's disease, Ageing Res Rev, 15, 6, 10.1016/j.arr.2013.12.007 T. Schmidt-Glenewinkel and M. Figueiredo-Pereira, Inflammation as a Mediator of Oxidative Stress and UPS Dysfunction, in The Proteasome in Neurodegeneration, L. Stefanis and J.N. Keller, Editors. 2006, Springer US: Boston, MA. p. 105-131. Maphis, 2015, Reactive microglia drive tau pathology and contribute to the spreading of pathological tau in the brain, Brain, 138, 1738, 10.1093/brain/awv081 Devassy, 2016, Omega-3 Polyunsaturated Fatty Acids and Oxylipins in Neuroinflammation and Management of Alzheimer Disease, Adv Nutr, 7, 905, 10.3945/an.116.012187 L.D. Harvey, Y. Yin, I.Y. Attarwala, G. Begum, J. Deng, H.Q. Yan, et al., Administration of DHA Reduces Endoplasmic Reticulum Stress-Associated Inflammation and Alters Microglial or Macrophage Activation in Traumatic Brain Injury. ASN Neuro. 7(2015).doi:10.1177/1759091415618969. Kuda, 2017, Bioactive metabolites of docosahexaenoic acid, Biochimie, 136, 12, 10.1016/j.biochi.2017.01.002 Joffre, 2019, N-3 Polyunsaturated Fatty Acids and the Resolution of Neuroinflammation, Front Pharmacol, 10, 1022, 10.3389/fphar.2019.01022 Viola, 2015, Amyloid beta oligomers in Alzheimer's disease pathogenesis, treatment, and diagnosis, Acta Neuropathol, 129, 183, 10.1007/s00401-015-1386-3 Gravitz, 2011, Drugs: a tangled web of targets, Nature, 475, S9, 10.1038/475S9a Morris, 2011, The many faces of tau, Neuron, 70, 410, 10.1016/j.neuron.2011.04.009 Jansen, 2015, Prevalence of cerebral amyloid pathology in persons without dementia: a meta-analysis, JAMA, 313, 1924, 10.1001/jama.2015.4668 Mandal, 2010, Comprehensive nuclear magnetic resonance studies on interactions of amyloid-beta with different molecular sized anesthetics, J Alzheimers Dis, 22, 27, 10.3233/JAD-2010-101128 Jin, 2011, Soluble amyloid beta-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration, Proc Natl Acad Sci U S A, 108, 5819, 10.1073/pnas.1017033108 He, 2018, Amyloid-beta plaques enhance Alzheimer's brain tau-seeded pathologies by facilitating neuritic plaque tau aggregation, Nat Med, 24, 29, 10.1038/nm.4443 Barthélemy, 2020, A soluble phosphorylated tau signature links tau, amyloid and the evolution of stages of dominantly inherited Alzheimer's disease, Nat Med, 26, 398, 10.1038/s41591-020-0781-z Gao, 2016, Chronic alpha-linolenic acid treatment alleviates age-associated neuropathology: Roles of PERK/eIF2alpha signaling pathway, Brain Behav Immun, 57, 314, 10.1016/j.bbi.2015.09.012 Green, 2007, Dietary docosahexaenoic acid and docosapentaenoic acid ameliorate amyloid-beta and tau pathology via a mechanism involving presenilin 1 levels, J Neurosci, 27, 4385, 10.1523/JNEUROSCI.0055-07.2007 Lim, 2005, A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model, J Neurosci, 25, 3032, 10.1523/JNEUROSCI.4225-04.2005 Grimm, 2016, Eicosapentaenoic acid and docosahexaenoic acid increase the degradation of amyloid-beta by affecting insulin-degrading enzyme, Biochem Cell Biol, 94, 534, 10.1139/bcb-2015-0149 Wang, 2009, Coexistences of insulin signaling-related proteins and choline acetyltransferase in neurons, Brain Res, 1249, 237, 10.1016/j.brainres.2008.10.046 Rivera, 2005, Insulin and insulin-like growth factor expression and function deteriorate with progression of Alzheimer's disease: link to brain reductions in acetylcholine, J Alzheimers Dis, 8, 247, 10.3233/JAD-2005-8304 Marini, 2008, Hormesis: a promising strategy to sustain endogenous neuronal survival pathways against neurodegenerative disorders, Ageing Res Rev, 7, 21, 10.1016/j.arr.2007.07.003 Xu, 2010, Memory Impairment in Cognitively Impaired Aged Rats Associated With Decreased Hippocampal CREB Phosphorylation: Reversal by Procyanidins Extracted From the Lotus Seedpod, J. Gerontology Series a-Biological Sci. Medical Sci., 65A, 933 Grimes, 2001, CREB DNA binding activity is inhibited by glycogen synthase kinase-3 beta and facilitated by lithium, J Neurochem, 78, 1219, 10.1046/j.1471-4159.2001.00495.x