Skip to main content
Top
Published in: Journal of Neuroinflammation 1/2016

Open Access 01-12-2016 | Review

Role of docosahexaenoic acid in the modulation of glial cells in Alzheimer’s disease

Authors: David Heras-Sandoval, José Pedraza-Chaverri, Jazmin M. Pérez-Rojas

Published in: Journal of Neuroinflammation | Issue 1/2016

Login to get access

Abstract

Docosahexaenoic acid (DHA) is an omega-3 (ω-3) long-chain polyunsaturated fatty acid (LCPUFA) relevant for brain function. It has largely been explored as a potential candidate to treat Alzheimer’s disease (AD). Clinical evidence favors a role for DHA in the improvement of cognition in very early stages of the AD. In response to stress or damage, DHA generates oxygenated derivatives called docosanoids that can activate the peroxisome proliferator-activated receptor γ (PPARγ). In conjunction with activated retinoid X receptors (RXR), PPARγ modulates inflammation, cell survival, and lipid metabolism. As an early event in AD, inflammation is associated with an excess of amyloid β peptide (Aβ) that contributes to neural insult. Glial cells are recognized to be actively involved during AD, and their dysfunction is associated with the early appearance of this pathology. These cells give support to neurons, remove amyloid β peptides from the brain, and modulate inflammation. Since DHA can modulate glial cell activity, the present work reviews the evidence about this modulation as well as the effect of docosanoids on neuroinflammation and in some AD models. The evidence supports PPARγ as a preferred target for gene modulation. The effective use of DHA and/or its derivatives in a subgroup of people at risk of developing AD is discussed.
Literature
2.
go back to reference SanGiovanni JP, Chew EY. The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina. Prog Retin Eye Res. 2005;24:87–138.PubMedCrossRef SanGiovanni JP, Chew EY. The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina. Prog Retin Eye Res. 2005;24:87–138.PubMedCrossRef
3.
go back to reference Pereira H, Barreira L, Figueiredo F, Custódio L, Vizetto-Duarte C, Polo C, et al. Polyunsaturated fatty acids of marine macroalgae: potential for nutritional and pharmaceutical applications. Mar Drugs. 2012;10:1920–35.PubMedPubMedCentralCrossRef Pereira H, Barreira L, Figueiredo F, Custódio L, Vizetto-Duarte C, Polo C, et al. Polyunsaturated fatty acids of marine macroalgae: potential for nutritional and pharmaceutical applications. Mar Drugs. 2012;10:1920–35.PubMedPubMedCentralCrossRef
4.
go back to reference Williams CM, Burdge G. Long-chain n-3 PUFA: plant v. marine sources. Proc Nutr Soc. 2006;65:42–50.PubMedCrossRef Williams CM, Burdge G. Long-chain n-3 PUFA: plant v. marine sources. Proc Nutr Soc. 2006;65:42–50.PubMedCrossRef
5.
go back to reference Morse NL. Benefits of docosahexaenoic acid, folic acid, vitamin D and iodine on foetal and infant brain development and function following maternal supplementation during pregnancy and lactation. Nutrients. 2012;4:799–840.PubMedPubMedCentralCrossRef Morse NL. Benefits of docosahexaenoic acid, folic acid, vitamin D and iodine on foetal and infant brain development and function following maternal supplementation during pregnancy and lactation. Nutrients. 2012;4:799–840.PubMedPubMedCentralCrossRef
6.
go back to reference Carlson SE. Docosahexaenoic acid and arachidonic acid in infant development. Semin Neonatol. 2001;6:437–49.PubMedCrossRef Carlson SE. Docosahexaenoic acid and arachidonic acid in infant development. Semin Neonatol. 2001;6:437–49.PubMedCrossRef
8.
go back to reference Kihara A. Very long-chain fatty acids: elongation, physiology and related disorders. J Biochem. 2012;152:387–95.PubMedCrossRef Kihara A. Very long-chain fatty acids: elongation, physiology and related disorders. J Biochem. 2012;152:387–95.PubMedCrossRef
9.
go back to reference Sprecher H, Luthria DL, Mohammed BS, Baykousheva SP. Reevaluation of the pathways for the biosynthesis of polyunsaturated fatty acids. J Lipid Res. 1995;36:2471–7.PubMed Sprecher H, Luthria DL, Mohammed BS, Baykousheva SP. Reevaluation of the pathways for the biosynthesis of polyunsaturated fatty acids. J Lipid Res. 1995;36:2471–7.PubMed
10.
go back to reference Huffman SL, Harika RK, Eilander A, Osendarp SJ. Essential fats: how do they affect growth and development of infants and young children in developing countries? A literature review. Matern Child Nutr. 2011;Suppl 3:44–65.CrossRef Huffman SL, Harika RK, Eilander A, Osendarp SJ. Essential fats: how do they affect growth and development of infants and young children in developing countries? A literature review. Matern Child Nutr. 2011;Suppl 3:44–65.CrossRef
11.
go back to reference Arterburn LM, Hall EB, Oken H. Distribution, interconversion, and dose response of n-3 fatty acids in humans. Am J Clin Nutr. 2006;83:1467S–76.PubMed Arterburn LM, Hall EB, Oken H. Distribution, interconversion, and dose response of n-3 fatty acids in humans. Am J Clin Nutr. 2006;83:1467S–76.PubMed
12.
go back to reference Rapoport SI, Rao JS, Igarashi M. Brain metabolism of nutritionally essential polyunsaturated fatty acids depends on both the diet and the liver. Prostaglandins Leukot Essent Fatty Acids. 2007;77:251–61.PubMedPubMedCentralCrossRef Rapoport SI, Rao JS, Igarashi M. Brain metabolism of nutritionally essential polyunsaturated fatty acids depends on both the diet and the liver. Prostaglandins Leukot Essent Fatty Acids. 2007;77:251–61.PubMedPubMedCentralCrossRef
13.
go back to reference Rapoport SI, Igarashi M. Can the rat liver maintain normal brain DHA metabolism in the absence of dietary DHA? Prostaglandins Leukot Essent Fatty Acids. 2009;81:119–23.PubMedPubMedCentralCrossRef Rapoport SI, Igarashi M. Can the rat liver maintain normal brain DHA metabolism in the absence of dietary DHA? Prostaglandins Leukot Essent Fatty Acids. 2009;81:119–23.PubMedPubMedCentralCrossRef
14.
go back to reference Gibson RA, Neumann MA, Lien EL, Boyd KA, Tu WC. Docosahexaenoic acid synthesis from alpha-linolenic acid is inhibited by diets high in polyunsaturated fatty acids. Prostaglandins Leukot Essent Fatty Acids. 2013;88:139–46.PubMedCrossRef Gibson RA, Neumann MA, Lien EL, Boyd KA, Tu WC. Docosahexaenoic acid synthesis from alpha-linolenic acid is inhibited by diets high in polyunsaturated fatty acids. Prostaglandins Leukot Essent Fatty Acids. 2013;88:139–46.PubMedCrossRef
15.
go back to reference Bazan NG. Neuroprotectin D1-mediated anti-inflammatory and survival signaling in stroke, retinal degenerations, and Alzheimer’s disease. J Lipid Res. 2009;50 Suppl:S400–5.PubMed Bazan NG. Neuroprotectin D1-mediated anti-inflammatory and survival signaling in stroke, retinal degenerations, and Alzheimer’s disease. J Lipid Res. 2009;50 Suppl:S400–5.PubMed
16.
go back to reference Lauritzen L, Hansen HS, Jørgensen MH, Michaelsen KF. The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog Lipid Res. 2001;40:1–94.PubMedCrossRef Lauritzen L, Hansen HS, Jørgensen MH, Michaelsen KF. The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog Lipid Res. 2001;40:1–94.PubMedCrossRef
17.
go back to reference Rapoport SI, Ramadan E, Basselin M. Docosahexaenoic acid (DHA) incorporation into the brain from plasma as an in vivo biomarker of brain DHA metabolism and neurotransmission. Prostaglandins Other Lipid Mediat. 2011;96:109–13.PubMedPubMedCentralCrossRef Rapoport SI, Ramadan E, Basselin M. Docosahexaenoic acid (DHA) incorporation into the brain from plasma as an in vivo biomarker of brain DHA metabolism and neurotransmission. Prostaglandins Other Lipid Mediat. 2011;96:109–13.PubMedPubMedCentralCrossRef
18.
go back to reference Glomset JA. Role of docosahexaenoic acid in neuronal plasma membranes. Sci STKE. 2006;2006:pe6.PubMed Glomset JA. Role of docosahexaenoic acid in neuronal plasma membranes. Sci STKE. 2006;2006:pe6.PubMed
19.
go back to reference Guesnet P, Alessandri JM. Docosahexaenoic acid (DHA) and the developing central nervous system (CNS)—implications for dietary recommendations. Biochimie. 2011;93:7–12.PubMedCrossRef Guesnet P, Alessandri JM. Docosahexaenoic acid (DHA) and the developing central nervous system (CNS)—implications for dietary recommendations. Biochimie. 2011;93:7–12.PubMedCrossRef
20.
go back to reference Guest J, Garg M, Bilgin A, Grant R. Relationship between central and peripheral fatty acids in humans. Lipids Health Dis. 2013;2:79.CrossRef Guest J, Garg M, Bilgin A, Grant R. Relationship between central and peripheral fatty acids in humans. Lipids Health Dis. 2013;2:79.CrossRef
21.
go back to reference Ouellet M, Emond V, Chen CT, Julien C, Bourasset F, Oddo S, et al. Diffusion of docosahexaenoic and eicosapentaenoic acids through the blood-brain barrier: an in situ cerebral perfusion study. Neurochem Int. 2009;55:476–82.PubMedCrossRef Ouellet M, Emond V, Chen CT, Julien C, Bourasset F, Oddo S, et al. Diffusion of docosahexaenoic and eicosapentaenoic acids through the blood-brain barrier: an in situ cerebral perfusion study. Neurochem Int. 2009;55:476–82.PubMedCrossRef
22.
go back to reference Brossard N, Croset M, Normand S, Pousin J, Lecerf J, Laville M, et al. Human plasma albumin transports [13C] docosahexaenoic acid in two lipid forms to blood cells. J Lipid Res. 1997;38:1571–82.PubMed Brossard N, Croset M, Normand S, Pousin J, Lecerf J, Laville M, et al. Human plasma albumin transports [13C] docosahexaenoic acid in two lipid forms to blood cells. J Lipid Res. 1997;38:1571–82.PubMed
23.
go back to reference Mitchell RW, On NH, Del Bigio MR, Miller DW, Hatch GM. Fatty acid transport protein expression in human brain and potential role in fatty acid transport across human brain microvessel endothelial cells. J Neurochem. 2011;117:735–46.PubMedCrossRef Mitchell RW, On NH, Del Bigio MR, Miller DW, Hatch GM. Fatty acid transport protein expression in human brain and potential role in fatty acid transport across human brain microvessel endothelial cells. J Neurochem. 2011;117:735–46.PubMedCrossRef
24.
go back to reference Ma D, Zhang M, Mori Y, Yao C, Larsen CP, Yamashima T, et al. Cellular localization of epidermal-type and brain-type fatty acid-binding proteins in adult hippocampus and their response to cerebral ischemia. Hippocampus. 2010;20:811–9.PubMed Ma D, Zhang M, Mori Y, Yao C, Larsen CP, Yamashima T, et al. Cellular localization of epidermal-type and brain-type fatty acid-binding proteins in adult hippocampus and their response to cerebral ischemia. Hippocampus. 2010;20:811–9.PubMed
25.
go back to reference Nguyen LN, Ma D, Shui G, Wong P, Cazenave-Gassiot A, Zhang X, et al. Mfsd2a is a transporter for the essential omega-3 fatty acid docosahexaenoic acid. Nature. 2014;509:503–6.PubMedCrossRef Nguyen LN, Ma D, Shui G, Wong P, Cazenave-Gassiot A, Zhang X, et al. Mfsd2a is a transporter for the essential omega-3 fatty acid docosahexaenoic acid. Nature. 2014;509:503–6.PubMedCrossRef
26.
go back to reference Thies F, Pillon C, Moliere P, Lagarde M, Lecerf J. Preferential incorporation of sn-2 lysoPC DHA over unesterified DHA in the young rat brain. Am J Physiol. 1994;267:R1273–9.PubMed Thies F, Pillon C, Moliere P, Lagarde M, Lecerf J. Preferential incorporation of sn-2 lysoPC DHA over unesterified DHA in the young rat brain. Am J Physiol. 1994;267:R1273–9.PubMed
27.
go back to reference Chen S, Subbaiah PV. Regioisomers of phosphatidylcholine containing DHA and their potential to deliver DHA to the brain: role of phospholipase specificities. Lipids. 2013;48:675–86.PubMedCrossRef Chen S, Subbaiah PV. Regioisomers of phosphatidylcholine containing DHA and their potential to deliver DHA to the brain: role of phospholipase specificities. Lipids. 2013;48:675–86.PubMedCrossRef
28.
go back to reference Moore SA, Yoder E, Murphy S, Dutton GR, Spector AA. Astrocytes, not neurons, produce docosahexaenoic acid (22:6 omega-3) and arachidonic acid (20:4 omega-6). J Neurochem. 1991;56:518–24.PubMedCrossRef Moore SA, Yoder E, Murphy S, Dutton GR, Spector AA. Astrocytes, not neurons, produce docosahexaenoic acid (22:6 omega-3) and arachidonic acid (20:4 omega-6). J Neurochem. 1991;56:518–24.PubMedCrossRef
29.
go back to reference Williard DE, Harmon SD, Kaduce TL, Preuss M, Moore SA, Robbins ME, et al. Docosahexaenoic acid synthesis from n-3 polyunsaturated fatty acids in differentiated rat brain astrocytes. J Lipid Res. 2001;42:1368–76.PubMed Williard DE, Harmon SD, Kaduce TL, Preuss M, Moore SA, Robbins ME, et al. Docosahexaenoic acid synthesis from n-3 polyunsaturated fatty acids in differentiated rat brain astrocytes. J Lipid Res. 2001;42:1368–76.PubMed
30.
go back to reference Moore SA. Polyunsaturated fatty acid synthesis and release by brain-derived cells in vitro. J Mol Neurosci. 2001;16(2-3):195–200.PubMedCrossRef Moore SA. Polyunsaturated fatty acid synthesis and release by brain-derived cells in vitro. J Mol Neurosci. 2001;16(2-3):195–200.PubMedCrossRef
31.
go back to reference Bazan NG. Cellular and molecular events mediated by docosahexaenoic acid-derived neuroprotectin D1 signaling in photoreceptor cell survival and brain protection. Prostaglandins Leukot Essent Fatty Acids. 2009;81:205–11.PubMedPubMedCentralCrossRef Bazan NG. Cellular and molecular events mediated by docosahexaenoic acid-derived neuroprotectin D1 signaling in photoreceptor cell survival and brain protection. Prostaglandins Leukot Essent Fatty Acids. 2009;81:205–11.PubMedPubMedCentralCrossRef
32.
go back to reference Tu WC, Cook-Johnson RJ, James MJ, Mühlhäusler BS, Stone DA, Gibson RA. Barramundi (Lates calcarifer) desaturase with Δ6/Δ8 dual activities. Biotechnol Lett. 2012;34:1283–96.PubMedCrossRef Tu WC, Cook-Johnson RJ, James MJ, Mühlhäusler BS, Stone DA, Gibson RA. Barramundi (Lates calcarifer) desaturase with Δ6/Δ8 dual activities. Biotechnol Lett. 2012;34:1283–96.PubMedCrossRef
33.
go back to reference Kim HY, Akbar M, Kim YS. Phosphatidylserine-dependent neuroprotective signaling promoted by docosahexaenoic acid. Prostaglandins Leukot Essent Fatty Acids. 2010;82:165–72.PubMedPubMedCentralCrossRef Kim HY, Akbar M, Kim YS. Phosphatidylserine-dependent neuroprotective signaling promoted by docosahexaenoic acid. Prostaglandins Leukot Essent Fatty Acids. 2010;82:165–72.PubMedPubMedCentralCrossRef
34.
go back to reference Cao D, Kevala K, Kim J, Moon HS, Jun SB, Lovinger D, et al. Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function. J Neurochem. 2009;111:510–21.PubMedPubMedCentralCrossRef Cao D, Kevala K, Kim J, Moon HS, Jun SB, Lovinger D, et al. Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function. J Neurochem. 2009;111:510–21.PubMedPubMedCentralCrossRef
35.
go back to reference Hong S, Lu Y, Yang R, Gotlinger KH, Petasis NA, Serhan CN. Resolvin D1, protectin D1, and related docosahexaenoic acid-derived products: analysis via electrospray/low energy tandem mass spectrometry based on spectra and fragmentation mechanisms. J Am Soc Mass Spectrom. 2007;18:128–44.PubMedPubMedCentralCrossRef Hong S, Lu Y, Yang R, Gotlinger KH, Petasis NA, Serhan CN. Resolvin D1, protectin D1, and related docosahexaenoic acid-derived products: analysis via electrospray/low energy tandem mass spectrometry based on spectra and fragmentation mechanisms. J Am Soc Mass Spectrom. 2007;18:128–44.PubMedPubMedCentralCrossRef
36.
go back to reference Ariel A, Li PL, Wang W, Tang WX, Fredman G, Hong S, et al. The docosatriene protectin D1 is produced by TH2 skewing and promotes human T cell apoptosis via lipid raft clustering. J Biol Chem. 2005;280:43079–86.PubMedCrossRef Ariel A, Li PL, Wang W, Tang WX, Fredman G, Hong S, et al. The docosatriene protectin D1 is produced by TH2 skewing and promotes human T cell apoptosis via lipid raft clustering. J Biol Chem. 2005;280:43079–86.PubMedCrossRef
37.
go back to reference Zhao Y, Calon F, Julien C, Winkler JW, Petasis NA, Lukiw WJ, et al. Docosahexaenoic acid-derived neuroprotectin D1 induces neuronal survival via secretase- and PPARγ-mediated mechanisms in Alzheimer’s disease models. PLoS One. 2011;6:e15816.PubMedPubMedCentralCrossRef Zhao Y, Calon F, Julien C, Winkler JW, Petasis NA, Lukiw WJ, et al. Docosahexaenoic acid-derived neuroprotectin D1 induces neuronal survival via secretase- and PPARγ-mediated mechanisms in Alzheimer’s disease models. PLoS One. 2011;6:e15816.PubMedPubMedCentralCrossRef
38.
go back to reference Bordoni A, Di Nunzio M, Danesi F, Biagi PL. Polyunsaturated fatty acids: from diet to binding to PPARs and other nuclear receptors. Genes Nutr. 2006;1:95–106.PubMedPubMedCentralCrossRef Bordoni A, Di Nunzio M, Danesi F, Biagi PL. Polyunsaturated fatty acids: from diet to binding to PPARs and other nuclear receptors. Genes Nutr. 2006;1:95–106.PubMedPubMedCentralCrossRef
39.
go back to reference Picq M, Chen P, Perez M, Michaud M, Véricel E, Guichardant M, et al. DHA metabolism: targeting the brain and lipoxygenation. Mol Neurobiol. 2010;42:48–51.PubMedPubMedCentralCrossRef Picq M, Chen P, Perez M, Michaud M, Véricel E, Guichardant M, et al. DHA metabolism: targeting the brain and lipoxygenation. Mol Neurobiol. 2010;42:48–51.PubMedPubMedCentralCrossRef
40.
go back to reference Chen P, Véricel E, Lagarde M, Guichardant M. Poxytrins, a class of oxygenated products from polyunsaturated fatty acids, potently inhibit blood platelet aggregation. FASEB J. 2011;25:382–8.PubMedCrossRef Chen P, Véricel E, Lagarde M, Guichardant M. Poxytrins, a class of oxygenated products from polyunsaturated fatty acids, potently inhibit blood platelet aggregation. FASEB J. 2011;25:382–8.PubMedCrossRef
41.
go back to reference Serhan CN, Hong S, Gronert K, Colgan SP, Devchand PR, Mirick G, et al. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med. 2002;196:1025–37.PubMedPubMedCentralCrossRef Serhan CN, Hong S, Gronert K, Colgan SP, Devchand PR, Mirick G, et al. Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med. 2002;196:1025–37.PubMedPubMedCentralCrossRef
43.
go back to reference Dyall SC, Michael GJ, Michael-Titus AT. Omega-3 fatty acids reverse age-related decreases in nuclear receptors and increase neurogenesis in old rats. J Neurosci Res. 2010;88:2091–102.PubMedCrossRef Dyall SC, Michael GJ, Michael-Titus AT. Omega-3 fatty acids reverse age-related decreases in nuclear receptors and increase neurogenesis in old rats. J Neurosci Res. 2010;88:2091–102.PubMedCrossRef
44.
go back to reference Itoh T, Yamamoto K. Peroxisome proliferator activated receptor gamma and oxidized docosahexaenoic acids as new class of ligand. Naunyn Schmiedebergs Arch Pharmacol. 2008;377:541–7.PubMedCrossRef Itoh T, Yamamoto K. Peroxisome proliferator activated receptor gamma and oxidized docosahexaenoic acids as new class of ligand. Naunyn Schmiedebergs Arch Pharmacol. 2008;377:541–7.PubMedCrossRef
45.
go back to reference Cimini A, Benedetti E, Cristiano L, Sebastiani P, D'Amico MA, D'Angelo B, et al. Expression of peroxisome proliferator-activated receptors (PPARs) and retinoic acid receptors (RXRs) in rat cortical neurons. Neuroscience. 2005;130:325–37.PubMedCrossRef Cimini A, Benedetti E, Cristiano L, Sebastiani P, D'Amico MA, D'Angelo B, et al. Expression of peroxisome proliferator-activated receptors (PPARs) and retinoic acid receptors (RXRs) in rat cortical neurons. Neuroscience. 2005;130:325–37.PubMedCrossRef
46.
go back to reference Cristiano L, Cimini A, Moreno S, Ragnelli AM, Paola CM. Peroxisome proliferator-activated receptors (PPARs) and related transcription factors in differentiating astrocyte cultures. Neuroscience. 2005;131:577–87.PubMedCrossRef Cristiano L, Cimini A, Moreno S, Ragnelli AM, Paola CM. Peroxisome proliferator-activated receptors (PPARs) and related transcription factors in differentiating astrocyte cultures. Neuroscience. 2005;131:577–87.PubMedCrossRef
47.
go back to reference Aleshin S, Grabeklis S, Hanck T, Sergeeva M, Reiser G. Peroxisome proliferator-activated receptor (PPAR)-gamma positively controls and PPARalpha negatively controls cyclooxygenase-2 expression in rat brain astrocytes through a convergence on PPARbeta/delta via mutual control of PPAR expression levels. Mol Pharmacol. 2009;76:414–24.PubMedCrossRef Aleshin S, Grabeklis S, Hanck T, Sergeeva M, Reiser G. Peroxisome proliferator-activated receptor (PPAR)-gamma positively controls and PPARalpha negatively controls cyclooxygenase-2 expression in rat brain astrocytes through a convergence on PPARbeta/delta via mutual control of PPAR expression levels. Mol Pharmacol. 2009;76:414–24.PubMedCrossRef
48.
go back to reference Holtzman DM, Morris JC, Goate AM. Alzheimer’s disease: the challenge of the second century. Sci Transl Med. 2011;3:77sr1.PubMedPubMedCentral Holtzman DM, Morris JC, Goate AM. Alzheimer’s disease: the challenge of the second century. Sci Transl Med. 2011;3:77sr1.PubMedPubMedCentral
49.
50.
go back to reference Heppner FL, Ransohoff RM, Becher B. Immune attack: the role of inflammation in Alzheimer disease. Nat Rev Neurosci. 2015;16:358–72.PubMedCrossRef Heppner FL, Ransohoff RM, Becher B. Immune attack: the role of inflammation in Alzheimer disease. Nat Rev Neurosci. 2015;16:358–72.PubMedCrossRef
52.
go back to reference Farfara D, Lifshitz V, Frenkel D. Neuroprotective and neurotoxic properties of glial cells in the pathogenesis of Alzheimer’s disease. J Cell Mol Med. 2008;12:762–80.PubMedPubMedCentralCrossRef Farfara D, Lifshitz V, Frenkel D. Neuroprotective and neurotoxic properties of glial cells in the pathogenesis of Alzheimer’s disease. J Cell Mol Med. 2008;12:762–80.PubMedPubMedCentralCrossRef
53.
go back to reference Weitz TM, Town T. Microglia in Alzheimer’s disease: it’s all about context. Int J Alzheimers Dis. 2012;2012:314185.PubMedPubMedCentral Weitz TM, Town T. Microglia in Alzheimer’s disease: it’s all about context. Int J Alzheimers Dis. 2012;2012:314185.PubMedPubMedCentral
55.
go back to reference Rossi D. Astrocyte physiopathology: at the crossroads of intercellular networking, inflammation and cell death. Prog Neurobiol. 2015;130:86–120.PubMedCrossRef Rossi D. Astrocyte physiopathology: at the crossroads of intercellular networking, inflammation and cell death. Prog Neurobiol. 2015;130:86–120.PubMedCrossRef
56.
go back to reference Avila-Muñoz E, Arias C. When astrocytes become harmful: functional and inflammatory responses that contribute to Alzheimer’s disease. Ageing Res Rev. 2014;18:29–40.PubMedCrossRef Avila-Muñoz E, Arias C. When astrocytes become harmful: functional and inflammatory responses that contribute to Alzheimer’s disease. Ageing Res Rev. 2014;18:29–40.PubMedCrossRef
57.
go back to reference Heneka MT, Carson MJ, El Khoury J, Landreth GE, Brosseron F, Feinstein DL, et al. Neuroinflammation in Alzheimer’s disease. Lancet Neurol. 2015;14:388–405.PubMedCrossRef Heneka MT, Carson MJ, El Khoury J, Landreth GE, Brosseron F, Feinstein DL, et al. Neuroinflammation in Alzheimer’s disease. Lancet Neurol. 2015;14:388–405.PubMedCrossRef
58.
go back to reference Lian H, Yang L, Cole A, Sun L, Chiang AC, Fowler SW, et al. NFκB-activated astroglial release of complement C3 compromises neuronal morphology and function associated with Alzheimer’s disease. Neuron. 2015;85:101–15.PubMedPubMedCentralCrossRef Lian H, Yang L, Cole A, Sun L, Chiang AC, Fowler SW, et al. NFκB-activated astroglial release of complement C3 compromises neuronal morphology and function associated with Alzheimer’s disease. Neuron. 2015;85:101–15.PubMedPubMedCentralCrossRef
59.
go back to reference Woodruff TM, Tenner AJ. A commentary on: NFκB-activated astroglial release of complement C3 compromises neuronal morphology and function associated with Alzheimer’s disease. A cautionary note regarding C3aR. Front Immunol. 2015;6:220.PubMedPubMedCentralCrossRef Woodruff TM, Tenner AJ. A commentary on: NFκB-activated astroglial release of complement C3 compromises neuronal morphology and function associated with Alzheimer’s disease. A cautionary note regarding C3aR. Front Immunol. 2015;6:220.PubMedPubMedCentralCrossRef
60.
go back to reference Meyer-Luehmann M, Spires-Jones TL, Prada C, Garcia-Alloza M, de Calignon A, Rozkalne A, et al. Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer’s disease. Nature. 2008;451:720–4.PubMedPubMedCentralCrossRef Meyer-Luehmann M, Spires-Jones TL, Prada C, Garcia-Alloza M, de Calignon A, Rozkalne A, et al. Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer’s disease. Nature. 2008;451:720–4.PubMedPubMedCentralCrossRef
61.
go back to reference Marlatt MW, Bauer J, Aronica E, van Haastert ES, Hoozemans JJ, Joels M, et al. Proliferation in the Alzheimer hippocampus is due to microglia, not astroglia, and occurs at sites of amyloid deposition. Neural Plast. 2014;2014:693851.PubMedPubMedCentral Marlatt MW, Bauer J, Aronica E, van Haastert ES, Hoozemans JJ, Joels M, et al. Proliferation in the Alzheimer hippocampus is due to microglia, not astroglia, and occurs at sites of amyloid deposition. Neural Plast. 2014;2014:693851.PubMedPubMedCentral
62.
go back to reference Rodríguez JJ, Noristanic HN, Hilditchd T, Olabarriad M, Yehd CY, Wittone J, et al. Increased densities of resting and activated microglia in the dentate gyrus follow senile plaque formation in the CA1 subfield of the hippocampus in the triple transgenic model of Alzheimer’s disease. Neurosci Lett. 2013;552:129–34.PubMedCrossRef Rodríguez JJ, Noristanic HN, Hilditchd T, Olabarriad M, Yehd CY, Wittone J, et al. Increased densities of resting and activated microglia in the dentate gyrus follow senile plaque formation in the CA1 subfield of the hippocampus in the triple transgenic model of Alzheimer’s disease. Neurosci Lett. 2013;552:129–34.PubMedCrossRef
63.
go back to reference Mulder SD, Nielsen HM, Blankenstein MA, Eikelenboom P, Veerhuis R. Apolipoproteins E and J interfere with amyloid-beta uptake by primary human astrocytes and microglia in vitro. Glia. 2014;62:493–503.PubMedCrossRef Mulder SD, Nielsen HM, Blankenstein MA, Eikelenboom P, Veerhuis R. Apolipoproteins E and J interfere with amyloid-beta uptake by primary human astrocytes and microglia in vitro. Glia. 2014;62:493–503.PubMedCrossRef
64.
go back to reference Li L, Wu Y, Wang Y, Wu J, Song L, Xian W, et al. Resolvin D1 promotes the interleukin-4-induced alternative activation in BV-2 microglial cells. J Neuroinflammation. 2014;11:72.PubMedPubMedCentralCrossRef Li L, Wu Y, Wang Y, Wu J, Song L, Xian W, et al. Resolvin D1 promotes the interleukin-4-induced alternative activation in BV-2 microglial cells. J Neuroinflammation. 2014;11:72.PubMedPubMedCentralCrossRef
65.
go back to reference Xu J, Storer PD, Chavis JA, Racke MK, Drew PD. Agonists for the peroxisome proliferator-activated receptor-alpha and the retinoid X receptor inhibit inflammatory responses of microglia. J Neurosci Res. 2005;81:403–11.PubMedCrossRef Xu J, Storer PD, Chavis JA, Racke MK, Drew PD. Agonists for the peroxisome proliferator-activated receptor-alpha and the retinoid X receptor inhibit inflammatory responses of microglia. J Neurosci Res. 2005;81:403–11.PubMedCrossRef
66.
go back to reference Manzhulo IV, Ogurtsova OS, Lamash NE, Latyshev NA, Kasyanov SP, Dyuizen IV. Analgetic effect of docosahexaenoic acid is mediated by modulating the microglia activity in the dorsal root ganglia in a rat model of neuropathic pain. Acta Histochem. 2015;117:659–66.PubMedCrossRef Manzhulo IV, Ogurtsova OS, Lamash NE, Latyshev NA, Kasyanov SP, Dyuizen IV. Analgetic effect of docosahexaenoic acid is mediated by modulating the microglia activity in the dorsal root ganglia in a rat model of neuropathic pain. Acta Histochem. 2015;117:659–66.PubMedCrossRef
67.
go back to reference Lu Y, Zhao LX, Cao DL, Gao YJ. Spinal injection of docosahexaenoic acid attenuates carrageenan-induced inflammatory pain through inhibition of microglia-mediated neuroinflammation in the spinal cord. Neuroscience. 2013;241:22–31.PubMedCrossRef Lu Y, Zhao LX, Cao DL, Gao YJ. Spinal injection of docosahexaenoic acid attenuates carrageenan-induced inflammatory pain through inhibition of microglia-mediated neuroinflammation in the spinal cord. Neuroscience. 2013;241:22–31.PubMedCrossRef
68.
69.
go back to reference Pettit LK, Varsanyi C, Tadros J, Vassiliou E. Modulating the inflammatory properties of activated microglia with docosahexaenoic acid and aspirin. Lipids Health Dis. 2013;12:16.PubMedPubMedCentralCrossRef Pettit LK, Varsanyi C, Tadros J, Vassiliou E. Modulating the inflammatory properties of activated microglia with docosahexaenoic acid and aspirin. Lipids Health Dis. 2013;12:16.PubMedPubMedCentralCrossRef
70.
go back to reference De Smedt-Peyrusse V, Sargueil F, Moranis A, Harizi H, Mongrand S, Layé S. Docosahexaenoic acid prevents lipopolysaccharide-induced cytokine production in microglial cells by inhibiting lipopolysaccharide receptor presentation but not its membrane subdomain localization. J Neurochem. 2008;105:296–307.PubMedCrossRef De Smedt-Peyrusse V, Sargueil F, Moranis A, Harizi H, Mongrand S, Layé S. Docosahexaenoic acid prevents lipopolysaccharide-induced cytokine production in microglial cells by inhibiting lipopolysaccharide receptor presentation but not its membrane subdomain localization. J Neurochem. 2008;105:296–307.PubMedCrossRef
71.
go back to reference Antonietta Ajmone-Cat M, Lavinia Salvatori M, De Simone R, Mancini M, Biagioni S, Bernardo A, et al. Docosahexaenoic acid modulates inflammatory and antineurogenic functions of activated microglial cells. J Neurosci Res. 2012;90:575–87.PubMedCrossRef Antonietta Ajmone-Cat M, Lavinia Salvatori M, De Simone R, Mancini M, Biagioni S, Bernardo A, et al. Docosahexaenoic acid modulates inflammatory and antineurogenic functions of activated microglial cells. J Neurosci Res. 2012;90:575–87.PubMedCrossRef
73.
go back to reference Saka HA, Valdivia R. Emerging roles for lipid droplets in immunity and host-pathogen interactions. Annu Rev Cell Dev Biol. 2012;28:411–37.PubMedCrossRef Saka HA, Valdivia R. Emerging roles for lipid droplets in immunity and host-pathogen interactions. Annu Rev Cell Dev Biol. 2012;28:411–37.PubMedCrossRef
74.
go back to reference Chang PK, Khatchadourian A, McKinney RA, Maysinger D. Docosahexaenoic acid (DHA): a modulator of microglia activity and dendritic spine morphology. J Neuroinflammation. 2015;12:34.PubMedPubMedCentralCrossRef Chang PK, Khatchadourian A, McKinney RA, Maysinger D. Docosahexaenoic acid (DHA): a modulator of microglia activity and dendritic spine morphology. J Neuroinflammation. 2015;12:34.PubMedPubMedCentralCrossRef
75.
go back to reference Mirza M, Volz C, Karlstetter M, Langiu M, Somogyi A, Ruonala MO, et al. Progressive retinal degeneration and glial activation in the CLN6 (nclf) mouse model of neuronal ceroid lipofuscinosis: a beneficial effect of DHA and curcumin supplementation. PLoS One. 2013;8:e75963.PubMedPubMedCentralCrossRef Mirza M, Volz C, Karlstetter M, Langiu M, Somogyi A, Ruonala MO, et al. Progressive retinal degeneration and glial activation in the CLN6 (nclf) mouse model of neuronal ceroid lipofuscinosis: a beneficial effect of DHA and curcumin supplementation. PLoS One. 2013;8:e75963.PubMedPubMedCentralCrossRef
76.
go back to reference Hjorth E, Zhu M, Toro VC, Vedin I, Palmblad J, Cederholm T, et al. Omega-3 fatty acids enhance phagocytosis of Alzheimer’s disease-related amyloid-β42 by human microglia and decrease inflammatory markers. J Alzheimers Dis. 2013;35:697–713.PubMed Hjorth E, Zhu M, Toro VC, Vedin I, Palmblad J, Cederholm T, et al. Omega-3 fatty acids enhance phagocytosis of Alzheimer’s disease-related amyloid-β42 by human microglia and decrease inflammatory markers. J Alzheimers Dis. 2013;35:697–713.PubMed
77.
go back to reference Lu DY, Tsao YY, Leung YM, Su KP. Docosahexaenoic acid suppresses neuroinflammatory responses and induces heme oxygenase-1 expression in BV-2 microglia: implications of antidepressant effects for ω-3 fatty acids. Neuropsychopharmacology. 2010;35:2238–48.PubMedPubMedCentralCrossRef Lu DY, Tsao YY, Leung YM, Su KP. Docosahexaenoic acid suppresses neuroinflammatory responses and induces heme oxygenase-1 expression in BV-2 microglia: implications of antidepressant effects for ω-3 fatty acids. Neuropsychopharmacology. 2010;35:2238–48.PubMedPubMedCentralCrossRef
78.
go back to reference Ebert S, Weigelt K, Walczak Y, Drobnik W, Mauerer R, Hume DA, et al. Docosahexaenoic acid attenuates microglial activation and delays early retinal degeneration. Neurochem. 2009;110:1863–75.CrossRef Ebert S, Weigelt K, Walczak Y, Drobnik W, Mauerer R, Hume DA, et al. Docosahexaenoic acid attenuates microglial activation and delays early retinal degeneration. Neurochem. 2009;110:1863–75.CrossRef
79.
go back to reference Chang CY, Kuan YH, Li JR, Chen WY, Ou YC, Pan HC, et al. Docosahexaenoic acid reduces cellular inflammatory response following permanent focal cerebral ischemia in rats. J Nutr Biochem. 2013;24:2127–37.PubMedCrossRef Chang CY, Kuan YH, Li JR, Chen WY, Ou YC, Pan HC, et al. Docosahexaenoic acid reduces cellular inflammatory response following permanent focal cerebral ischemia in rats. J Nutr Biochem. 2013;24:2127–37.PubMedCrossRef
80.
go back to reference Hjorth E, Freund-Levi Y. Immunomodulation of microglia by docosahexaenoic acid and eicosapentaenoic acid. Curr Opin Clin Nutr Metab Care. 2012;15:134–43.PubMed Hjorth E, Freund-Levi Y. Immunomodulation of microglia by docosahexaenoic acid and eicosapentaenoic acid. Curr Opin Clin Nutr Metab Care. 2012;15:134–43.PubMed
81.
go back to reference Becerir C, Kılıç İ, Sahin Ö, Özdemir Ö, Tokgün O, Özdemir B, et al. The protective effect of docosahexaenoic acid on the bilirubin neurotoxicity. J Enzyme Inhib Med Chem. 2013;28:801–7.PubMedCrossRef Becerir C, Kılıç İ, Sahin Ö, Özdemir Ö, Tokgün O, Özdemir B, et al. The protective effect of docosahexaenoic acid on the bilirubin neurotoxicity. J Enzyme Inhib Med Chem. 2013;28:801–7.PubMedCrossRef
82.
go back to reference Gupta S, Knight AG, Gupta S, Keller JN, Bruce-Keller AJ. Saturated long-chain fatty acids activate inflammatory signaling in astrocytes. J Neurochem. 2012;120:1060–71.PubMedPubMedCentral Gupta S, Knight AG, Gupta S, Keller JN, Bruce-Keller AJ. Saturated long-chain fatty acids activate inflammatory signaling in astrocytes. J Neurochem. 2012;120:1060–71.PubMedPubMedCentral
83.
go back to reference Begum G, Kintner D, Liu Y, Cramer SW, Sun D. DHA inhibits ER Ca2+ release and ER stress in astrocytes following in vitro ischemia. J Neurochem. 2012;120:622–30.PubMedPubMedCentralCrossRef Begum G, Kintner D, Liu Y, Cramer SW, Sun D. DHA inhibits ER Ca2+ release and ER stress in astrocytes following in vitro ischemia. J Neurochem. 2012;120:622–30.PubMedPubMedCentralCrossRef
84.
go back to reference Grintal B, Champeil-Potokar G, Lavialle M, Vancassel S, Breton S, Denis I. Inhibition of astroglial glutamate transport by polyunsaturated fatty acids: evidence for a signalling role of docosahexaenoic acid. Neurochem Int. 2009;54:535–43.PubMedCrossRef Grintal B, Champeil-Potokar G, Lavialle M, Vancassel S, Breton S, Denis I. Inhibition of astroglial glutamate transport by polyunsaturated fatty acids: evidence for a signalling role of docosahexaenoic acid. Neurochem Int. 2009;54:535–43.PubMedCrossRef
85.
go back to reference Latour A, Grintal B, Champeil-Potokar G, Hennebelle M, Lavialle M, Dutar P, et al. Omega-3 fatty acids deficiency aggravates glutamatergic synapse and astroglial aging in the rat hippocampal CA1. Aging Cell. 2013;12:76–84.PubMedCrossRef Latour A, Grintal B, Champeil-Potokar G, Hennebelle M, Lavialle M, Dutar P, et al. Omega-3 fatty acids deficiency aggravates glutamatergic synapse and astroglial aging in the rat hippocampal CA1. Aging Cell. 2013;12:76–84.PubMedCrossRef
86.
go back to reference Sheets KG, Jun B, Zhou Y, Zhu M, Petasis NA, Gordon WC, et al. Microglial ramification and redistribution concomitant with the attenuation of choroidal neovascularization by neuroprotectin D1. Mol Vis. 2013;19:1747–59.PubMedPubMedCentral Sheets KG, Jun B, Zhou Y, Zhu M, Petasis NA, Gordon WC, et al. Microglial ramification and redistribution concomitant with the attenuation of choroidal neovascularization by neuroprotectin D1. Mol Vis. 2013;19:1747–59.PubMedPubMedCentral
87.
go back to reference Abdelmoaty S, Wigerblad G, Bas DB, Codeluppi S, Fernandez-Zafra T, El-Awady e-S, et al. Spinal actions of lipoxin A4 and 17(R)-resolvin D1 attenuate inflammation-induced mechanical hypersensitivity and spinal TNF release. PLoS One. 2013;8:e75543.PubMedPubMedCentralCrossRef Abdelmoaty S, Wigerblad G, Bas DB, Codeluppi S, Fernandez-Zafra T, El-Awady e-S, et al. Spinal actions of lipoxin A4 and 17(R)-resolvin D1 attenuate inflammation-induced mechanical hypersensitivity and spinal TNF release. PLoS One. 2013;8:e75543.PubMedPubMedCentralCrossRef
88.
go back to reference Mizwicki MT, Liu G, Fiala M, Magpantay L, Sayre J, Siani A, et al. 1α, 25-dihydroxyvitamin D3 and resolvin D1 retune the balance between amyloid-β phagocytosis and inflammation in Alzheimer’s disease patients. J Alzheimers Dis. 2013;34:155–70.PubMedPubMedCentral Mizwicki MT, Liu G, Fiala M, Magpantay L, Sayre J, Siani A, et al. 1α, 25-dihydroxyvitamin D3 and resolvin D1 retune the balance between amyloid-β phagocytosis and inflammation in Alzheimer’s disease patients. J Alzheimers Dis. 2013;34:155–70.PubMedPubMedCentral
89.
go back to reference Yamanaka M, Ishikawa T, Griep A, Axt D, Kummer MP, Heneka MT. PPARγ/RXRα-induced and CD36-mediated microglial amyloid-β phagocytosis results in cognitive improvement in amyloid precursor protein/presenilin 1 mice. J Neurosci. 2012;32:17321–31.PubMedCrossRef Yamanaka M, Ishikawa T, Griep A, Axt D, Kummer MP, Heneka MT. PPARγ/RXRα-induced and CD36-mediated microglial amyloid-β phagocytosis results in cognitive improvement in amyloid precursor protein/presenilin 1 mice. J Neurosci. 2012;32:17321–31.PubMedCrossRef
90.
go back to reference Bahety P, Tan YM, Hong Y, Zhang L, Chan EC, Ee PL. Metabotyping of docosahexaenoic acid-treated Alzheimer’s disease cell model. PLoS One. 2014;9:e90123.PubMedPubMedCentralCrossRef Bahety P, Tan YM, Hong Y, Zhang L, Chan EC, Ee PL. Metabotyping of docosahexaenoic acid-treated Alzheimer’s disease cell model. PLoS One. 2014;9:e90123.PubMedPubMedCentralCrossRef
91.
go back to reference Seo J, Barhoumi R, Johnson AE, Lupton JR, Chapkin RS. Docosahexaenoic acid selectively inhibits plasma membrane targeting of lipidated proteins. FASEB J. 2006;20:770–2.PubMed Seo J, Barhoumi R, Johnson AE, Lupton JR, Chapkin RS. Docosahexaenoic acid selectively inhibits plasma membrane targeting of lipidated proteins. FASEB J. 2006;20:770–2.PubMed
92.
go back to reference Raza Shaikh S, Brown DA. Models of plasma membrane organization can be applied to mitochondrial membranes to target human health and disease with polyunsaturated fatty acids. Prostaglandins Leukot Essent Fatty Acids. 2013;88:21–5.PubMedCrossRef Raza Shaikh S, Brown DA. Models of plasma membrane organization can be applied to mitochondrial membranes to target human health and disease with polyunsaturated fatty acids. Prostaglandins Leukot Essent Fatty Acids. 2013;88:21–5.PubMedCrossRef
93.
go back to reference Grimm MO, Kuchenbecker J, Grösgen S, Burg VK, Hundsdörfer B, Rothhaar TL, et al. Docosahexaenoic acid reduces amyloid beta production via multiple pleiotropic mechanisms. J Biol Chem. 2011;286:14028–39.PubMedPubMedCentralCrossRef Grimm MO, Kuchenbecker J, Grösgen S, Burg VK, Hundsdörfer B, Rothhaar TL, et al. Docosahexaenoic acid reduces amyloid beta production via multiple pleiotropic mechanisms. J Biol Chem. 2011;286:14028–39.PubMedPubMedCentralCrossRef
94.
go back to reference Fabelo N, Martín V, Marín R, Moreno D, Ferrer I, Díaz M. Altered lipid composition in cortical lipid rafts occurs at early stages of sporadic Alzheimer’s disease and facilitates APP/BACE1 interactions. Neurobiol Aging. 2014;35:1801–12.PubMedCrossRef Fabelo N, Martín V, Marín R, Moreno D, Ferrer I, Díaz M. Altered lipid composition in cortical lipid rafts occurs at early stages of sporadic Alzheimer’s disease and facilitates APP/BACE1 interactions. Neurobiol Aging. 2014;35:1801–12.PubMedCrossRef
95.
go back to reference Oksman M, Iivonen H, Hogyes E, Amtul Z, Penke B, Leenders I, et al. Impact of different saturated fatty acid, polyunsaturated fatty acid and cholesterol containing diets on beta-amyloid accumulation in APP/PS1 transgenic mice. Neurobiol Dis. 2006;23:563–72.PubMedCrossRef Oksman M, Iivonen H, Hogyes E, Amtul Z, Penke B, Leenders I, et al. Impact of different saturated fatty acid, polyunsaturated fatty acid and cholesterol containing diets on beta-amyloid accumulation in APP/PS1 transgenic mice. Neurobiol Dis. 2006;23:563–72.PubMedCrossRef
96.
go back to reference Eckert GP, Chang S, Eckmann J, Copanaki E, Hagl S, Hener U, et al. Liposome-incorporated DHA increases neuronal survival by enhancing non-amyloidogenic APP processing. Biochim Biophys Acta. 1808;2011:236–43. Eckert GP, Chang S, Eckmann J, Copanaki E, Hagl S, Hener U, et al. Liposome-incorporated DHA increases neuronal survival by enhancing non-amyloidogenic APP processing. Biochim Biophys Acta. 1808;2011:236–43.
97.
go back to reference Torres M, Price SL, Fiol-Deroque MA, Marcilla-Etxenike A, Ahyayauch H, Barceló-Coblijn G, et al. Membrane lipid modifications and therapeutic effects mediated by hydroxydocosahexaenoic acid on Alzheimer’s disease. Biochim Biophys Acta. 1838;2014:1680–92. Torres M, Price SL, Fiol-Deroque MA, Marcilla-Etxenike A, Ahyayauch H, Barceló-Coblijn G, et al. Membrane lipid modifications and therapeutic effects mediated by hydroxydocosahexaenoic acid on Alzheimer’s disease. Biochim Biophys Acta. 1838;2014:1680–92.
99.
go back to reference Hashimoto M, Katakura M, Hossain S, Rahman A, Shimada T, Shido O. Docosahexaenoic acid withstands the Aβ (25-35)-induced neurotoxicity in SH-SY5Y cells. J Nutr Biochem. 2011;22:22–9.PubMedCrossRef Hashimoto M, Katakura M, Hossain S, Rahman A, Shimada T, Shido O. Docosahexaenoic acid withstands the Aβ (25-35)-induced neurotoxicity in SH-SY5Y cells. J Nutr Biochem. 2011;22:22–9.PubMedCrossRef
100.
go back to reference Sublimi Saponetti M, Grimaldi M, Scrima M, Albonetti C, Nori SL, Cucolo A. Aggregation of Aβ (25-35) on DOPC and DOPC/DHA bilayers: an atomic force microscopy study. PLoS One. 2014;9:e115780.PubMedPubMedCentralCrossRef Sublimi Saponetti M, Grimaldi M, Scrima M, Albonetti C, Nori SL, Cucolo A. Aggregation of Aβ (25-35) on DOPC and DOPC/DHA bilayers: an atomic force microscopy study. PLoS One. 2014;9:e115780.PubMedPubMedCentralCrossRef
101.
go back to reference Calon F, Lim GP, Yang F, Morihara T, Teter B, Ubeda O, et al. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer’s disease mouse model. Neuron. 2004;43:633–45.PubMedPubMedCentralCrossRef Calon F, Lim GP, Yang F, Morihara T, Teter B, Ubeda O, et al. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer’s disease mouse model. Neuron. 2004;43:633–45.PubMedPubMedCentralCrossRef
102.
go back to reference Calon F, Cole G. Neuroprotective action of omega-3 polyunsaturated fatty acids against neurodegenerative diseases: evidence from animal studies. Prostaglandins Leukot Essent Fat Acids. 2007;77:287–93.CrossRef Calon F, Cole G. Neuroprotective action of omega-3 polyunsaturated fatty acids against neurodegenerative diseases: evidence from animal studies. Prostaglandins Leukot Essent Fat Acids. 2007;77:287–93.CrossRef
103.
go back to reference Lim GP, Calon F, Morihara T, Yang F, Teter B, Ubeda O, et al. A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model. J Neurosci. 2005;25:3032–40.PubMedCrossRef Lim GP, Calon F, Morihara T, Yang F, Teter B, Ubeda O, et al. A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model. J Neurosci. 2005;25:3032–40.PubMedCrossRef
104.
go back to reference Arsenault D, Julien C, Tremblay C, Calon F. DHA improves cognition and prevents dysfunction of entorhinal cortex neurons in 3xTg-AD mice. PLoS One. 2011;6:e17397.PubMedPubMedCentralCrossRef Arsenault D, Julien C, Tremblay C, Calon F. DHA improves cognition and prevents dysfunction of entorhinal cortex neurons in 3xTg-AD mice. PLoS One. 2011;6:e17397.PubMedPubMedCentralCrossRef
105.
go back to reference Perez SE, Berg BM, Moore KA, He B, Counts SE, Fritz JJ, et al. DHA diet reduces AD pathology in young APPswe/PS1 delta E9 transgenic mice: possible gender effects. J Neurosci Res. 2010;88:1026–40.PubMedPubMedCentral Perez SE, Berg BM, Moore KA, He B, Counts SE, Fritz JJ, et al. DHA diet reduces AD pathology in young APPswe/PS1 delta E9 transgenic mice: possible gender effects. J Neurosci Res. 2010;88:1026–40.PubMedPubMedCentral
106.
go back to reference Hashimoto M, Tozawa R, Katakura M, Shahdat H, Haque AM, Tanabe Y, et al. Protective effects of prescription n-3 fatty acids against impairment of spatial cognitive learning ability in amyloid β-infused rats. Food Funct. 2011;2:386–94.PubMedCrossRef Hashimoto M, Tozawa R, Katakura M, Shahdat H, Haque AM, Tanabe Y, et al. Protective effects of prescription n-3 fatty acids against impairment of spatial cognitive learning ability in amyloid β-infused rats. Food Funct. 2011;2:386–94.PubMedCrossRef
107.
go back to reference Green KN, Martinez-Coria H, Khashwji H, Hall EB, Yurko-Mauro KA, Ellis L, et al. Dietary docosahexaenoic acid and docosapentaenoic acid ameliorate amyloid-beta and tau pathology via a mechanism involving presenilin 1 levels. J Neurosci. 2007;27:4385–95.PubMedCrossRef Green KN, Martinez-Coria H, Khashwji H, Hall EB, Yurko-Mauro KA, Ellis L, et al. Dietary docosahexaenoic acid and docosapentaenoic acid ameliorate amyloid-beta and tau pathology via a mechanism involving presenilin 1 levels. J Neurosci. 2007;27:4385–95.PubMedCrossRef
108.
go back to reference Hooijmans CR, Rutters F, Dederen PJ, Gambarota G, Veltien A, van Groen T, et al. Changes in cerebral blood volume and amyloid pathology in aged Alzheimer APP/PS1 mice on a docosahexaenoic acid (DHA) diet or cholesterol enriched typical western diet (TWD). Neurobiol Dis. 2007;28:16–29.PubMedCrossRef Hooijmans CR, Rutters F, Dederen PJ, Gambarota G, Veltien A, van Groen T, et al. Changes in cerebral blood volume and amyloid pathology in aged Alzheimer APP/PS1 mice on a docosahexaenoic acid (DHA) diet or cholesterol enriched typical western diet (TWD). Neurobiol Dis. 2007;28:16–29.PubMedCrossRef
109.
go back to reference Fiol-deRoque MA, Gutierrez-Lanza R, Terés S, Torres M, Barceló P, Rial RV, et al. Cognitive recovery and restoration of cell proliferation in the dentate gyrus in the 5XFAD transgenic mice model of Alzheimer’s disease following 2-hydroxy-DHA treatment. Biogerontology. 2013;14:763–75.PubMedCrossRef Fiol-deRoque MA, Gutierrez-Lanza R, Terés S, Torres M, Barceló P, Rial RV, et al. Cognitive recovery and restoration of cell proliferation in the dentate gyrus in the 5XFAD transgenic mice model of Alzheimer’s disease following 2-hydroxy-DHA treatment. Biogerontology. 2013;14:763–75.PubMedCrossRef
110.
go back to reference Vedin I, Cederholm T, Freund-Levi Y, Basun H, Garlind A, Irving GF, et al. Effects of DHA-rich n-3 fatty acid supplementation on gene expression in blood mononuclear leukocytes: the OmegAD study. PLoS One. 2012;7:e35425.PubMedPubMedCentralCrossRef Vedin I, Cederholm T, Freund-Levi Y, Basun H, Garlind A, Irving GF, et al. Effects of DHA-rich n-3 fatty acid supplementation on gene expression in blood mononuclear leukocytes: the OmegAD study. PLoS One. 2012;7:e35425.PubMedPubMedCentralCrossRef
111.
go back to reference Freund Levi Y, Vedin I, Cederholm T, Basun H, Faxén Irving G, Eriksdotter M, 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. J Intern Med. 2014;275:428–36.PubMedCrossRef Freund Levi Y, Vedin I, Cederholm T, Basun H, Faxén Irving G, Eriksdotter M, 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. J Intern Med. 2014;275:428–36.PubMedCrossRef
113.
go back to reference Quinn JF, Raman R, Thomas RG, Yurko-Mauro K, Nelson EB, Van Dyck C, et al. Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial. JAMA. 2010;304:1903–11.PubMedPubMedCentralCrossRef Quinn JF, Raman R, Thomas RG, Yurko-Mauro K, Nelson EB, Van Dyck C, et al. Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial. JAMA. 2010;304:1903–11.PubMedPubMedCentralCrossRef
114.
go back to reference Chouinard-Watkins R, Rioux-Perreault C, Fortier M, Tremblay-Mercier J, Zhang Y, et al. Disturbance in uniformly 13C-labelled DHA metabolism in elderly human subjects carrying the apoE ε4 allele. Br J Nutr. 2013;110:1751–9.PubMedCrossRef Chouinard-Watkins R, Rioux-Perreault C, Fortier M, Tremblay-Mercier J, Zhang Y, et al. Disturbance in uniformly 13C-labelled DHA metabolism in elderly human subjects carrying the apoE ε4 allele. Br J Nutr. 2013;110:1751–9.PubMedCrossRef
115.
go back to reference Vandal M, Alata W, Tremblay C, Rioux-Perreault C, Salem Jr N, Calon F, et al. Reduction in DHA transport to the brain of mice expressing human APOE4 compared to APOE2. J Neurochem. 2014;129:516–26.PubMedCrossRef Vandal M, Alata W, Tremblay C, Rioux-Perreault C, Salem Jr N, Calon F, et al. Reduction in DHA transport to the brain of mice expressing human APOE4 compared to APOE2. J Neurochem. 2014;129:516–26.PubMedCrossRef
116.
go back to reference Conway V, Allard MJ, Minihane AM, Jackson KG, Lovegrove JA, Plourde M. Postprandial enrichment of triacylglycerol-rich lipoproteins with omega-3 fatty acids: lack of an interaction with apolipoprotein E genotype? Lipids Health Dis. 2014;13:148.PubMedPubMedCentralCrossRef Conway V, Allard MJ, Minihane AM, Jackson KG, Lovegrove JA, Plourde M. Postprandial enrichment of triacylglycerol-rich lipoproteins with omega-3 fatty acids: lack of an interaction with apolipoprotein E genotype? Lipids Health Dis. 2014;13:148.PubMedPubMedCentralCrossRef
117.
go back to reference Dang TM, Conway V, Plourde M. Disrupted fatty acid distribution in HDL and LDL according to apolipoprotein E allele. Nutrition. 2015;31:807–12.PubMedCrossRef Dang TM, Conway V, Plourde M. Disrupted fatty acid distribution in HDL and LDL according to apolipoprotein E allele. Nutrition. 2015;31:807–12.PubMedCrossRef
118.
go back to reference Terwel D, Steffensen KR, Verghese PB, Kummer MP, Gustafsson JÅ, Holtzman DM, et al. Critical role of astroglial apolipoprotein E and liver X receptor-α expression for microglial Aβ phagocytosis. J Neurosci. 2011;31:7049–59.PubMedCrossRef Terwel D, Steffensen KR, Verghese PB, Kummer MP, Gustafsson JÅ, Holtzman DM, et al. Critical role of astroglial apolipoprotein E and liver X receptor-α expression for microglial Aβ phagocytosis. J Neurosci. 2011;31:7049–59.PubMedCrossRef
119.
go back to reference Casali BT, Corona AW, Mariani MM, Karlo JC, Ghosal K, Landreth GE. Omega-3 fatty acids augment the actions of nuclear receptor agonists in a mouse model of Alzheimer’s disease. J Neurosci. 2015;35:9173–81.PubMedPubMedCentralCrossRef Casali BT, Corona AW, Mariani MM, Karlo JC, Ghosal K, Landreth GE. Omega-3 fatty acids augment the actions of nuclear receptor agonists in a mouse model of Alzheimer’s disease. J Neurosci. 2015;35:9173–81.PubMedPubMedCentralCrossRef
120.
go back to reference Tai LM, Koster KP, Luo J, Lee SH, Wang YT, Collins NC, et al. Amyloid-β pathology and APOE genotype modulate retinoid X receptor agonist activity in vivo. J Biol Chem. 2014;289:30538–55.PubMedPubMedCentralCrossRef Tai LM, Koster KP, Luo J, Lee SH, Wang YT, Collins NC, et al. Amyloid-β pathology and APOE genotype modulate retinoid X receptor agonist activity in vivo. J Biol Chem. 2014;289:30538–55.PubMedPubMedCentralCrossRef
121.
go back to reference Conquer JA, Tierney MC, Zecevic J, Bettger WJ, Fisher RH. Fatty acid analysis of blood plasma of patients with Alzheimer’s disease, other types of dementia, and cognitive impairment. Lipids. 2000;35:1305–12.PubMedCrossRef Conquer JA, Tierney MC, Zecevic J, Bettger WJ, Fisher RH. Fatty acid analysis of blood plasma of patients with Alzheimer’s disease, other types of dementia, and cognitive impairment. Lipids. 2000;35:1305–12.PubMedCrossRef
122.
go back to reference Tully AM, Roche HM, Doyle R, Fallon C, Bruce I, Lawlor B, et al. Low serum cholesteryl ester-docosahexaenoic acid levels in Alzheimer’s disease: a case-control study. Br J Nutr. 2003;89:483–9.PubMedCrossRef Tully AM, Roche HM, Doyle R, Fallon C, Bruce I, Lawlor B, et al. Low serum cholesteryl ester-docosahexaenoic acid levels in Alzheimer’s disease: a case-control study. Br J Nutr. 2003;89:483–9.PubMedCrossRef
123.
go back to reference Wang W, Shinto L, Connor WE, Quinn JF. Nutritional biomarkers in Alzheimer’s disease: the association between carotenoids, n-3 fatty acids, and dementia severity. J Alzheimers Dis. 2008;13:31–8.PubMed Wang W, Shinto L, Connor WE, Quinn JF. Nutritional biomarkers in Alzheimer’s disease: the association between carotenoids, n-3 fatty acids, and dementia severity. J Alzheimers Dis. 2008;13:31–8.PubMed
124.
go back to reference Astarita G, Jung KM, Berchtold NC, Nguyen VQ, Gillen DL, Head E, et al. Deficient liver biosynthesis of docosahexaenoic acid correlates with cognitive impairment in Alzheimer’s disease. PLoS One. 2010;5:e12538.PubMedPubMedCentralCrossRef Astarita G, Jung KM, Berchtold NC, Nguyen VQ, Gillen DL, Head E, et al. Deficient liver biosynthesis of docosahexaenoic acid correlates with cognitive impairment in Alzheimer’s disease. PLoS One. 2010;5:e12538.PubMedPubMedCentralCrossRef
125.
go back to reference Plourde M, Fortier M, Vandal M, Tremblay-Mercier J, Freemantle E, Bégin M, et al. Unresolved issues in the link between docosahexaenoic acid and Alzheimer’s disease. Prostaglandins Leukot Essent Fatty Acids. 2007;77:301–8.PubMedCrossRef Plourde M, Fortier M, Vandal M, Tremblay-Mercier J, Freemantle E, Bégin M, et al. Unresolved issues in the link between docosahexaenoic acid and Alzheimer’s disease. Prostaglandins Leukot Essent Fatty Acids. 2007;77:301–8.PubMedCrossRef
126.
go back to reference Cole GM, Frautschy SA. Docosahexaenoic acid protects from amyloid and dendritic pathology in an Alzheimer’s disease mouse model. Nutr Health. 2006;18:249–59.PubMedCrossRef Cole GM, Frautschy SA. Docosahexaenoic acid protects from amyloid and dendritic pathology in an Alzheimer’s disease mouse model. Nutr Health. 2006;18:249–59.PubMedCrossRef
127.
go back to reference McGahon BM, Martin DS, Horrobin DF, Lynch MA. Age-related changes in synaptic function: analysis of the effect of dietary supplementation with ω-3 fatty acids. Neuroscience. 1999;94:305–14.PubMedCrossRef McGahon BM, Martin DS, Horrobin DF, Lynch MA. Age-related changes in synaptic function: analysis of the effect of dietary supplementation with ω-3 fatty acids. Neuroscience. 1999;94:305–14.PubMedCrossRef
128.
go back to reference Lee LK, Shahar S, Chin AV, Yusoff NA. Docosahexaenoic acid-concentrated fish oil supplementation in subjects with mild cognitive impairment (MCI): a 12-month randomised, double-blind, placebo-controlled trial. Psychopharmacology (Berl). 2013;225:605–12.CrossRef Lee LK, Shahar S, Chin AV, Yusoff NA. Docosahexaenoic acid-concentrated fish oil supplementation in subjects with mild cognitive impairment (MCI): a 12-month randomised, double-blind, placebo-controlled trial. Psychopharmacology (Berl). 2013;225:605–12.CrossRef
129.
go back to reference Fiala M, Halder RC, Sagong B, Ross O, Sayre J, Porter V, et al. ω-3 supplementation increases amyloid-β phagocytosis and resolvin D1 in patients with minor cognitive impairment. FASEB J. 2015;29:2681–9.PubMedCrossRef Fiala M, Halder RC, Sagong B, Ross O, Sayre J, Porter V, et al. ω-3 supplementation increases amyloid-β phagocytosis and resolvin D1 in patients with minor cognitive impairment. FASEB J. 2015;29:2681–9.PubMedCrossRef
130.
go back to reference Daiello LA, Gongvatana A, Dunsiger S, Cohen RA, Ott BR, Alzheimer’s Disease Neuroimaging Initiative. Association of fish oil supplement use with preservation of brain volume and cognitive function. Alzheimers Dement. 2015;11:226–35.PubMedCrossRef Daiello LA, Gongvatana A, Dunsiger S, Cohen RA, Ott BR, Alzheimer’s Disease Neuroimaging Initiative. Association of fish oil supplement use with preservation of brain volume and cognitive function. Alzheimers Dement. 2015;11:226–35.PubMedCrossRef
131.
go back to reference Jernerén F, Elshorbagy AK, Oulhaj A, Smith SM, Refsum H, Smith AD. Brain atrophy in cognitively impaired elderly: the importance of long-chain ω-3 fatty acids and B vitamin status in a randomized controlled trial. Am J Clin Nutr. 2015;102:215–21.PubMedCrossRef Jernerén F, Elshorbagy AK, Oulhaj A, Smith SM, Refsum H, Smith AD. Brain atrophy in cognitively impaired elderly: the importance of long-chain ω-3 fatty acids and B vitamin status in a randomized controlled trial. Am J Clin Nutr. 2015;102:215–21.PubMedCrossRef
132.
go back to reference van Neerven S, Kampmann E, Mey J. RAR/RXR and PPAR/RXR signaling in neurological and psychiatric diseases. Prog Neurobiol. 2008;85:433–51.PubMedCrossRef van Neerven S, Kampmann E, Mey J. RAR/RXR and PPAR/RXR signaling in neurological and psychiatric diseases. Prog Neurobiol. 2008;85:433–51.PubMedCrossRef
Metadata
Title
Role of docosahexaenoic acid in the modulation of glial cells in Alzheimer’s disease
Authors
David Heras-Sandoval
José Pedraza-Chaverri
Jazmin M. Pérez-Rojas
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2016
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/s12974-016-0525-7

Other articles of this Issue 1/2016

Journal of Neuroinflammation 1/2016 Go to the issue