N-3 PUFAs and neuroinflammatory processes in cognitive disorders

With the ageing population and increased cases of neurodegenerative diseases, there is a crucial need for the development of new nutritional approaches to prevent and delay the onset of cognitive decline. Neuroinflammatory processes contribute to neuronal damage that underpins neurodegenerative disorders. Growing evidence sheds light on the use of dietary n-3 long chain polyunsaturated fatty acids to improve cognitive performances and reduce the neuroinflammatory responses occurring with age and neurodegenerative pathologies. This review will summarise the most recent information related to the impact and mechanisms underlying the neuroinflammatory processes in cognitive disorders. We will also discuss the mechanisms underlying n-3 polyunsaturated fatty acids effect on neuroinflammation and memory decline.

[1]  S. Maier,et al.  Neuroinflammation in the normal aging hippocampus , 2015, Neuroscience.

[2]  Lars Bäckman,et al.  A 2 year multidomain intervention of diet, exercise, cognitive training, and vascular risk monitoring versus control to prevent cognitive decline in at-risk elderly people (FINGER): a randomised controlled trial , 2015, The Lancet.

[3]  W. Gordon,et al.  Corrigendum: Adiponectin receptor 1 conserves docosahexaenoic acid and promotes photoreceptor cell survival , 2015, Nature Communications.

[4]  A. Nadjar,et al.  Dietary n-3 PUFAs Deficiency Increases Vulnerability to Inflammation-Induced Spatial Memory Impairment , 2015, Neuropsychopharmacology.

[5]  A. A. Farooqui,et al.  Synthetic and natural inhibitors of phospholipases A2: their importance for understanding and treatment of neurological disorders. , 2015, ACS chemical neuroscience.

[6]  O. Garaschuk,et al.  Neuroinflammation in Alzheimer's disease , 2015, The Lancet Neurology.

[7]  C. Serhan,et al.  Protectins and maresins: New pro-resolving families of mediators in acute inflammation and resolution bioactive metabolome. , 2015, Biochimica et biophysica acta.

[8]  P. Calder.  Marine omega-3 fatty acids and inflammatory processes: Effects, mechanisms and clinical relevance. , 2015, Biochimica et biophysica acta.

[9]  W. Gordon,et al.  Adiponectin receptor 1 conserves docosahexaenoic acid and promotes photoreceptor cell survival , 2015, Nature Communications.

[10]  J. Palmblad,et al.  Effects of n-3 FA supplementation on the release of proresolving lipid mediators by blood mononuclear cells: the OmegAD study[S] , 2015, Journal of Lipid Research.

[11]  Shauna L. Parkes,et al.  Microglial Activation Enhances Associative Taste Memory through Purinergic Modulation of Glutamatergic Neurotransmission , 2015, The Journal of Neuroscience.

[12]  A. Nadjar,et al.  Transgenic Increase in n-3/n-6 Fatty Acid Ratio Protects Against Cognitive Deficits Induced by an Immune Challenge through Decrease of Neuroinflammation , 2015, Neuropsychopharmacology.

[13]  D. Praticò,et al.  Pharmacologic blockade of 12/15-lipoxygenase ameliorates memory deficits, Aβ and tau neuropathology in the triple-transgenic mice , 2015, Molecular Psychiatry.

[14]  J. Palmblad,et al.  Resolution of inflammation is altered in Alzheimer's disease , 2015, Alzheimer's & Dementia.

[15]  E. Hjorth,et al.  Differential regulation of resolution in inflammation induced by amyloid-β42 and lipopolysaccharides in human microglia. , 2014, Journal of Alzheimer's disease : JAD.

[16]  Jaewoo Choi,et al.  Xanthohumol improved cognitive flexibility in young mice , 2014, Behavioural Brain Research.

[17]  G. Davı̀,et al.  MicroRNA-181b Regulates ALX/FPR2 Receptor Expression and Proresolution Signaling in Human Macrophages* , 2014, The Journal of Biological Chemistry.

[18]  M. Kitazawa,et al.  Restoration of lipoxin A4 signaling reduces Alzheimer's disease-like pathology in the 3xTg-AD mouse model. , 2014, Journal of Alzheimer's disease : JAD.

[19]  Richard P. Bazinet,et al.  Polyunsaturated fatty acids and their metabolites in brain function and disease , 2014, Nature Reviews Neuroscience.

[20]  J. Backs,et al.  Resolvin D1 limits 5-lipoxygenase nuclear localization and leukotriene B4 synthesis by inhibiting a calcium-activated kinase pathway , 2014, Proceedings of the National Academy of Sciences.

[21]  G. Olmos,et al.  Tumor Necrosis Factor Alpha: A Link between Neuroinflammation and Excitotoxicity , 2014, Mediators of inflammation.

[22]  N. Castanon,et al.  Neuropsychiatric Comorbidity in Obesity: Role of Inflammatory Processes , 2014, Front. Endocrinol..

[23]  P. Wong,et al.  Mfsd2a is a transporter for the essential omega-3 fatty acid docosahexaenoic acid , 2014, Nature.

[24]  Q. Wang,et al.  Resolvin D1 Stimulates Alveolar Fluid Clearance through Alveolar Epithelial Sodium Channel, Na,K-ATPase via ALX/cAMP/PI3K Pathway in Lipopolysaccharide-Induced Acute Lung Injury , 2014, The Journal of Immunology.

[25]  S. Yuan,et al.  Resolvin D1 promotes the interleukin-4-induced alternative activation in BV-2 microglial cells , 2014, Journal of Neuroinflammation.

[26]  J. Palmblad,et al.  Transfer of omega‐3 fatty acids across the blood–brain barrier after dietary supplementation with a docosahexaenoic acid‐rich omega‐3 fatty acid preparation in patients with Alzheimer's disease: the OmegAD study , 2014, Journal of internal medicine.

[27]  P. Calder,et al.  Pharmacology and therapeutics of omega-3 polyunsaturated fatty acids in chronic inflammatory disease. , 2014, Pharmacology & therapeutics.

[28]  M. Reilly,et al.  Omega-3 PUFA supplementation and the response to evoked endotoxemia in healthy volunteers. , 2014, Molecular nutrition & food research.

[29]  T. Möller,et al.  Kynurenines in CNS disease: regulation by inflammatory cytokines , 2014, Front. Neurosci..

[30]  N. Castanon,et al.  Lipopolysaccharide-induced brain activation of the indoleamine 2,3-dioxygenase and depressive-like behavior are impaired in a mouse model of metabolic syndrome , 2014, Psychoneuroendocrinology.

[31]  Wei Zhang,et al.  Decreased liver peroxisomal β-oxidation accompanied by changes in brain fatty acid composition in aged rats , 2014, Neurological Sciences.

[32]  F. Bosetti,et al.  Unesterified docosahexaenoic acid is protective in neuroinflammation , 2013, Journal of neurochemistry.

[33]  C. Serhan,et al.  Resolution phase lipid mediators of inflammation: agonists of resolution. , 2013, Current opinion in pharmacology.

[34]  Lin-Xia Zhao,et al.  Spinal injection of docosahexaenoic acid attenuates carrageenan-induced inflammatory pain through inhibition of microglia-mediated neuroinflammation in the spinal cord , 2013, Neuroscience.

[35]  D. Praticò,et al.  5-Lipoxygenase pharmacological blockade decreases tau phosphorylation in vivo: involvement of the cyclin-dependent kinase-5 , 2013, Neurobiology of Aging.

[36]  P. Calder.  n-3 Fatty acids, inflammation and immunity: new mechanisms to explain old actions , 2013, Proceedings of the Nutrition Society.

[37]  F. Heppner,et al.  Functional Impairment of Microglia Coincides with Beta-Amyloid Deposition in Mice with Alzheimer-Like Pathology , 2013, PloS one.

[38]  W. Zhou,et al.  Resolvin D1, an Endogenous Lipid Mediator for Inactivation of Inflammation‐Related Signaling Pathways in Microglial Cells, Prevents Lipopolysaccharide‐Induced Inflammatory Responses , 2013, CNS neuroscience & therapeutics.

[39]  D. Praticò,et al.  Gene Knockout of 5-Lipoxygenase Rescues Synaptic Dysfunction and Improves Memory in the Triple-Transgenic Model of Alzheimer’s Disease , 2013, Molecular Psychiatry.

[40]  E. Epel,et al.  Omega-3 fatty acids, oxidative stress, and leukocyte telomere length: A randomized controlled trial , 2013, Brain, Behavior, and Immunity.

[41]  J. Priestley,et al.  Improved outcome after spinal cord compression injury in mice treated with docosahexaenoic acid , 2013, Experimental Neurology.

[42]  K. Chuang,et al.  Specific Inhibition of p25/Cdk5 Activity by the Cdk5 Inhibitory Peptide Reduces Neurodegeneration In Vivo , 2013, The Journal of Neuroscience.

[43]  Yongqing Hou,et al.  Fish oil enhances intestinal integrity and inhibits TLR4 and NOD2 signaling pathways in weaned pigs after LPS challenge. , 2012, The Journal of nutrition.

[44]  N. Bazan.  Neuroinflammation and Proteostasis are Modulated by Endogenously Biosynthesized Neuroprotectin D1 , 2012, Molecular Neurobiology.

[45]  D. Praticò,et al.  5‐Lipoxygenase gene transfer worsens memory, amyloid, and tau brain pathologies in a mouse model of alzheimer disease , 2012, Annals of neurology.

[46]  Urs Meyer,et al.  Systemic immune challenges trigger and drive Alzheimer-like neuropathology in mice , 2012, Journal of Neuroinflammation.

[47]  J. Godbout,et al.  Lipopolysaccharide-induced interleukin (IL)-4 receptor-α expression and corresponding sensitivity to the M2 promoting effects of IL-4 are impaired in microglia of aged mice , 2012, Brain, Behavior, and Immunity.

[48]  A. Obenaus,et al.  Novel aspirin-triggered neuroprotectin D1 attenuates cerebral ischemic injury after experimental stroke , 2012, Experimental Neurology.

[49]  S. Layé,et al.  Long term adequate n-3 polyunsaturated fatty acid diet protects from depressive-like behavior but not from working memory disruption and brain cytokine expression in aged mice , 2012, Brain, Behavior, and Immunity.

[50]  Dr David Vauzour.  Dietary Polyphenols as Modulators of Brain Functions: Biological Actions and Molecular Mechanisms Underpinning Their Beneficial Effects , 2012, Oxidative medicine and cellular longevity.

[51]  A. Nadjar,et al.  Short-Term Long Chain Omega3 Diet Protects from Neuroinflammatory Processes and Memory Impairment in Aged Mice , 2012, PloS one.

[52]  O. Baker,et al.  Resolvin D1 prevents TNF-α-mediated disruption of salivary epithelial formation. , 2012, American journal of physiology. Cell physiology.

[53]  C. Ulrich,et al.  Fatigue, inflammation, and ω-3 and ω-6 fatty acid intake among breast cancer survivors. , 2012, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[54]  C. Pariante,et al.  Interleukin-1β: A New Regulator of the Kynurenine Pathway Affecting Human Hippocampal Neurogenesis , 2012, Neuropsychopharmacology.

[55]  J. Miranda,et al.  Docosahexaenoic acid pretreatment confers protection and functional improvements after acute spinal cord injury in adult rats. , 2012, Journal of neurotrauma.

[56]  A. Nimmerjahn,et al.  The Role of Microglia in the Healthy Brain , 2011, The Journal of Neuroscience.

[57]  R. Andridge,et al.  Omega-3 supplementation lowers inflammation and anxiety in medical students: A randomized controlled trial , 2011, Brain, Behavior, and Immunity.

[58]  F. Calon,et al.  Accumulation of Dietary Docosahexaenoic Acid in the Brain Attenuates Acute Immune Response and Development of Postischemic Neuronal Damage , 2011, Stroke.

[59]  L. Belayev,et al.  Novel proresolving aspirin-triggered DHA pathway. , 2011, Chemistry & biology.

[60]  P. Barberger‐Gateau,et al.  Chronic Low-Grade Inflammation in Elderly Persons Is Associated with Altered Tryptophan and Tyrosine Metabolism: Role in Neuropsychiatric Symptoms , 2011, Biological Psychiatry.

[61]  W. Gordon,et al.  Docosahexaenoic acid signalolipidomics in nutrition: significance in aging, neuroinflammation, macular degeneration, Alzheimer's, and other neurodegenerative diseases. , 2011, Annual review of nutrition.

[62]  A. Franklin,et al.  Membrane raft organization is more sensitive to disruption by (n-3) PUFA than nonraft organization in EL4 and B cells. , 2011, The Journal of nutrition.

[63]  G. Oxenkrug.  Interferon-gamma - Inducible Inflammation: Contribution to Aging and Aging-Associated Psychiatric Disorders. , 2011, Aging and disease.

[64]  Andrew H. Miller,et al.  Immune system to brain signaling: neuropsychopharmacological implications. , 2011, Pharmacology & therapeutics.

[65]  P. Tso,et al.  Omega-3 fatty acid deficiency increases constitutive pro-inflammatory cytokine production in rats: relationship with central serotonin turnover. , 2010, Prostaglandins, leukotrienes, and essential fatty acids.

[66]  M. O’Banion,et al.  Neuroinflammatory processes in Alzheimer’s disease , 2010, Journal of Neural Transmission.

[67]  S. Layé.  Polyunsaturated fatty acids, neuroinflammation and well being. , 2010, Prostaglandins, leukotrienes, and essential fatty acids.

[68]  V. Perry,et al.  Microglia in neurodegenerative disease , 2010, Nature Reviews Neurology.

[69]  R. Bazinet,et al.  Genetic Ablation of CD36 Does not Alter Mouse Brain Polyunsaturated Fatty Acid Concentrations , 2010, Lipids.

[70]  Fred H. Gage,et al.  Mechanisms Underlying Inflammation in Neurodegeneration , 2010, Cell.

[71]  W. Harris,et al.  Inverse association of erythrocyte n-3 fatty acid levels with inflammatory biomarkers in patients with stable coronary artery disease: The Heart and Soul Study. , 2009, Atherosclerosis.

[72]  H. Vinters,et al.  β-Amyloid Oligomers Induce Phosphorylation of Tau and Inactivation of Insulin Receptor Substrate via c-Jun N-Terminal Kinase Signaling: Suppression by Omega-3 Fatty Acids and Curcumin , 2009, The Journal of Neuroscience.

[73]  J. W. Rudy,et al.  Time course of hippocampal IL-1 β and memory consolidation impairments in aging rats following peripheral infection , 2009, Brain, Behavior, and Immunity.

[74]  S. Proctor,et al.  Feeding long-chain n-3 polyunsaturated fatty acids to obese leptin receptor-deficient JCR:LA-cp rats modifies immune function and lipid-raft fatty acid composition , 2008, British Journal of Nutrition.

[75]  R. Dantzer,et al.  Uncoupling of interleukin‐6 from its signalling pathway by dietary n‐3‐polyunsaturated fatty acid deprivation alters sickness behaviour in mice , 2008, The European journal of neuroscience.

[76]  Rodney W. Johnson,et al.  Aging, microglial cell priming, and the discordant central inflammatory response to signals from the peripheral immune system , 2008, Journal of leukocyte biology.

[77]  S. Rapoport.  Brain arachidonic and docosahexaenoic acid cascades are selectively altered by drugs, diet and disease. , 2008, Prostaglandins, leukotrienes, and essential fatty acids.

[78]  D. Fuchs,et al.  Chronic immune stimulation correlates with reduced phenylalanine turnover. , 2008, Current drug metabolism.

[79]  R. Dantzer,et al.  Spatio-temporal differences in the profile of murine brain expression of proinflammatory cytokines and indoleamine 2,3-dioxygenase in response to peripheral lipopolysaccharide administration , 2008, Journal of Neuroimmunology.

[80]  R. Bazinet,et al.  The emerging role of docosahexaenoic acid in neuroinflammation. , 2008, Current opinion in investigational drugs.

[81]  F. Gomez-Pinilla,et al.  Brain foods: the effects of nutrients on brain function , 2008, Nature Reviews Neuroscience.

[82]  J. Palmblad,et al.  Effects of docosahexaenoic acid-rich n-3 fatty acid supplementation on cytokine release from blood mononuclear leukocytes: the OmegAD study. , 2008, The American journal of clinical nutrition.

[83]  Cai Song,et al.  Long-chain polyunsaturated fatty acids modulate interleukin-1beta-induced changes in behavior, monoaminergic neurotransmitters, and brain inflammation in rats. , 2008, The Journal of nutrition.

[84]  A. Mellor,et al.  Deficiency of Indoleamine 2,3-Dioxygenase Enhances Commensal-Induced Antibody Responses and Protects against Citrobacter rodentium-Induced Colitis , 2008, Infection and Immunity.

[85]  S. Mongrand,et al.  Docosahexaenoic acid prevents lipopolysaccharide‐induced cytokine production in microglial cells by inhibiting lipopolysaccharide receptor presentation but not its membrane subdomain localization , 2008, Journal of neurochemistry.

[86]  V. King,et al.  A combination of intravenous and dietary docosahexaenoic acid significantly improves outcome after spinal cord injury. , 2007, Brain : a journal of neurology.

[87]  M. Lynch,et al.  Modulation of amyloid‐β‐induced and age‐associated changes in rat hippocampus by eicosapentaenoic acid , 2007, Journal of neurochemistry.

[88]  H. Kettenmann,et al.  Microglia: active sensor and versatile effector cells in the normal and pathologic brain , 2007, Nature Neuroscience.

[89]  B. Winblad,et al.  Prevention of Alzheimer's disease and dementia. Major findings from the Kungsholmen Project , 2007, Physiology & Behavior.

[90]  Richard B. Banati,et al.  Positron emission tomography imaging of neuroinflammation , 2007, Neurotherapeutics.

[91]  F. Bosetti,et al.  Gene expression of cyclooxygenase-1 and Ca2+-independent phospholipase A2 is altered in rat hippocampus during normal aging , 2007, Brain Research Bulletin.

[92]  R. Dantzer,et al.  Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior , 2007, Psychoneuroendocrinology.

[93]  Dana Kilroy,et al.  Eicosapentaenoic acid confers neuroprotection in the amyloid-β challenged aged hippocampus , 2007, Neurobiology of Aging.

[94]  Patrick L. McGeer,et al.  NSAIDs and Alzheimer disease: Epidemiological, animal model and clinical studies , 2007, Neurobiology of Aging.

[95]  P. Calder,et al.  Differential immunomodulation with long-chain n-3 PUFA in health and chronic disease , 2007, Proceedings of the Nutrition Society.

[96]  S. Lemeshow,et al.  Depressive Symptoms, omega-6:omega-3 Fatty Acids, and Inflammation in Older Adults , 2007, Psychosomatic medicine.

[97]  C. Serhan,et al.  Resolvins and protectins in the termination program of acute inflammation. , 2007, Trends in immunology.

[98]  C. Serhan.  Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. , 2007, Annual review of immunology.

[99]  G. Gowing,et al.  Selective Ablation of Proliferating Microglial Cells Exacerbates Ischemic Injury in the Brain , 2007, The Journal of Neuroscience.

[100]  N. Bazan,et al.  Omega-3 fatty acids, pro-inflammatory signaling and neuroprotection , 2007, Current opinion in clinical nutrition and metabolic care.

[101]  M. Berger,et al.  Effects of fish oil on the neuro-endocrine responses to an endotoxin challenge in healthy volunteers. , 2007, Clinical nutrition.

[102]  J. Wallace,et al.  Resolution of in flammation: state of the art, definitions and terms , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[103]  K. Fritsche.  Fatty acids as modulators of the immune response. , 2006, Annual review of nutrition.

[104]  N. Bazan.  Cell survival matters: docosahexaenoic acid signaling, neuroprotection and photoreceptors , 2006, Trends in Neurosciences.

[105]  P. Calder,et al.  Dose-related effects of eicosapentaenoic acid on innate immune function in healthy humans: a comparison of young and older men. , 2006, The American journal of clinical nutrition.

[106]  S. Bandinelli,et al.  Relationship of plasma polyunsaturated fatty acids to circulating inflammatory markers. , 2006, The Journal of clinical endocrinology and metabolism.

[107]  D. Mostofsky,et al.  Essential fatty acids and the brain: From infancy to aging , 2005, Neurobiology of Aging.

[108]  V. Perry,et al.  Central and Systemic Endotoxin Challenges Exacerbate the Local Inflammatory Response and Increase Neuronal Death during Chronic Neurodegeneration , 2005, The Journal of Neuroscience.

[109]  Charles N Serhan,et al.  A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease. , 2005, The Journal of clinical investigation.

[110]  Jing Chen,et al.  Exaggerated neuroinflammation and sickness behavior in aged mice after activation of the peripheral innate immune system , 2005 .

[111]  N. Sparkman,et al.  Effects of intraperitoneal lipopolysaccharide on Morris maze performance in year-old and 2-month-old female C57BL/6J mice , 2005, Behavioural Brain Research.

[112]  L. Lannfelt,et al.  Transgenic model of Alzheimer's disease , 2005 .

[113]  B. Winblad,et al.  An active and socially integrated lifestyle in late life might protect against dementia , 2004, The Lancet Neurology.

[114]  B. Leonard,et al.  Dietary Ethyl-eicosapentaenoic Acid but not Soybean Oil Reverses Central Interleukin-1-induced Changes in Behavior, Corticosterone and Immune Response in Rats , 2004, Stress.

[115]  M. Lynch,et al.  Analysis of Interleukin-1β-induced Cell Signaling Activation in Rat Hippocampus following Exposure to Gamma Irradiation , 2003, Journal of Biological Chemistry.

[116]  D. Mostofsky,et al.  The role of polyunsaturated fatty acids in restoring the aging neuronal membrane , 2002, Neurobiology of Aging.

[117]  S. Ferdinandusse,et al.  Identification of the peroxisomal beta-oxidation enzymes involved in the biosynthesis of docosahexaenoic acid. , 2001, Journal of lipid research.

[118]  P. Calder,et al.  Polyunsaturated fatty acids, inflammation, and immunity , 2001, Lipids.

[119]  R. Dantzer,et al.  Peripheral administration of lipopolysaccharide induces the expression of cytokine transcripts in the brain and pituitary of mice. , 1994, Brain research. Molecular brain research.

[120]  A. Lichtenstein,et al.  Food use and health effects of soybean and sunflower oils. , 1991, Journal of the American College of Nutrition.

[121]  Polyunsaturated Fatty Acids , 2020, Encyclopedia of Behavioral Medicine.

[122]  A. Nadjar,et al.  Named Series : Diet , Inflammation and the Brain Nutritional n-3 PUFAs deficiency during perinatal periods alters brain innate immune system and neuronal plasticity-associated genes , 2014 .

[123]  J. Palmblad,et al.  Omega-3 fatty acids enhance phagocytosis of Alzheimer's disease-related amyloid-β42 by human microglia and decrease inflammatory markers. , 2013, Journal of Alzheimer's disease : JAD.

[124]  Cornelis J Stam,et al.  Efficacy of Souvenaid in mild Alzheimer's disease: results from a randomized, controlled trial. , 2012, Journal of Alzheimer's disease : JAD.

[125]  S. Monte.  Brain Insulin Resistance and Deficiency as Therapeutic Targets in Alzheimer's Disease , 2012 .

[126]  F. Bosetti,et al.  Targeting cyclooxygenases-1 and -2 in neuroinflammation: Therapeutic implications. , 2011, Biochimie.

[127]  P. Mukherjee,et al.  Neuroprotectin D1/protectin D1 stereoselective and specific binding with human retinal pigment epithelial cells and neutrophils. , 2010, Prostaglandins, leukotrienes, and essential fatty acids.

[128]  P. Calder.  Marine omega-3 fatty acids and inflammation , 2010 .

[129]  R. Dantzer,et al.  From inflammation to sickness and depression: when the immune system subjugates the brain , 2008, Nature Reviews Neuroscience.

[130]  R. Holman,et al.  Polyunsaturated fatty acids , 1977 .