Omega-3 fatty acids, pro-inflammatory signaling and neuroprotection

Purpose of reviewTo summarize recent findings that docosahexaenoate (DHA) is the precursor of stereospecific derivatives with anti-inflammatory and cytoprotective properties. Recent findingsThe docosahexaenoate-derived mediator neuroprotectin D1 is formed in retinal pigment epithelial cells when confronted with oxidative stress, in the brain during experimental stroke, and in the human brain from Alzheimer's disease patients as well as in human brain cells in culture. Neuroprotectin D1 displays potent anti-inflammatory and neuroprotective bioactivity. SummaryHere, we summarize recent studies demonstrating that in brain ischemia-reperfusion and in retinal pigment epithelial cells exposed to oxidative stress stereospecific docosahexaenoate-oxygenation pathways are activated and lead to the formation of docosanoid messengers. Two docosahexaenoate-oxygenation pathways were identified: the first is responsible for the formation of the messenger neuroprotectin D1 and the second pathway, which is active in the presence of aspirin, leads to the formation of the resolvin-type mediators (17R-DHA). Neuroprotectin D1 induces antiapoptotic, anti-inflammatory signaling and is neuroprotective.

[1]  Yoshimi Fujii,et al.  Chronic administration of docosahexaenoic acid ameliorates the impairment of spatial cognition learning ability in amyloid beta-infused rats. , 2005, The Journal of nutrition.

[2]  M. Wolfe,et al.  Tumor necrosis factor-alpha, interleukin-1beta, and interferon-gamma stimulate gamma-secretase-mediated cleavage of amyloid precursor protein through a JNK-dependent MAPK pathway. , 2004, The Journal of biological chemistry.

[3]  M. Mattson,et al.  Secreted beta-amyloid precursor protein counteracts the proapoptotic action of mutant presenilin-1 by activation of NF-kappaB and stabilization of calcium homeostasis. , 1998, The Journal of biological chemistry.

[4]  W. Markesbery,et al.  Regional Membrane Phospholipid Alterations in Alzheimer's Disease , 2004, Neurochemical Research.

[5]  M Chopp,et al.  Antibodies against Adhesion Molecules Reduce Apoptosis after Transient Middle Cerebral Artery Occlusion in Rat Brain , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[6]  M. Lazdunski,et al.  Polyunsaturated fatty acids are potent neuroprotectors , 2000, The EMBO journal.

[7]  M. Ball,et al.  Gene expression profiling of 12633 genes in Alzheimer hippocampal CA1: Transcription and neurotrophic factor down‐regulation and up‐regulation of apoptotic and pro‐inflammatory signaling , 2002, Journal of neuroscience research.

[8]  H. Okuyama,et al.  Reversibility of n-3 fatty acid deficiency-induced alterations of learning behavior in the rat: level of n-6 fatty acids as another critical factor. , 2001, Journal of lipid research.

[9]  Takashi Morihara,et al.  A Diet Enriched with the Omega-3 Fatty Acid Docosahexaenoic Acid Reduces Amyloid Burden in an Aged Alzheimer Mouse Model , 2005, The Journal of Neuroscience.

[10]  N. Greig,et al.  Role of cytokines in the gene expression of amyloid beta-protein precursor: identification of a 5'-UTR-binding nuclear factor and its implications in Alzheimer's disease. , 2003, Journal of Alzheimer's disease : JAD.

[11]  N. Bazan,et al.  Membrane docosahexaenoate is supplied to the developing brain and retina by the liver. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Patrick L. McGeer,et al.  Inflammatory processes in Alzheimer's disease , 2003, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[13]  E. Moriguchi,et al.  Prevalence of dementia in the older Japanese‐Brazilian population , 2002, Psychiatry and clinical neurosciences.

[14]  D. Selkoe,et al.  Notch and Presenilin: regulated intramembrane proteolysis links development and degeneration. , 2003, Annual review of neuroscience.

[15]  P. Mukherjee,et al.  Neuroprotectin D1: a docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Takashi Morihara,et al.  Docosahexaenoic Acid Protects from Dendritic Pathology in an Alzheimer's Disease Mouse Model , 2004, Neuron.

[17]  N. Bazan,et al.  Strong nuclear factor‐κB‐DNA binding parallels cyclooxygenase‐2 gene transcription in aging and in sporadic alzheimer's disease superior temporal lobe neocortex , 1998, Journal of neuroscience research.

[18]  C. Clish,et al.  Novel Functional Sets of Lipid-Derived Mediators with Antiinflammatory Actions Generated from Omega-3 Fatty Acids via Cyclooxygenase 2–Nonsteroidal Antiinflammatory Drugs and Transcellular Processing , 2000, The Journal of experimental medicine.

[19]  Kevin A Roth,et al.  Bcl-2 family regulation of neuronal development and neurodegeneration. , 2004, Biochimica et biophysica acta.

[20]  Y. Kitamura,et al.  Apoptotic cell death in neurons and glial cells: implications for Alzheimer's disease. , 1999, Japanese journal of pharmacology.

[21]  K. Sugioka,et al.  Chronic administration of docosahexaenoic acid improves reference memory-related learning ability in young rats , 1999, Neuroscience.

[22]  S. Kimber,et al.  Expression of 11 members of the BCL‐2 family of apoptosis regulatory molecules during human preimplantation embryo development and fragmentation , 2004, Molecular reproduction and development.

[23]  Motoi Tamura,et al.  Effect of the long-term feeding of dietary lipids on the learning ability, fatty acid composition of brain stem phospholipids and synaptic membrane fluidity in adult mice: a comparison of sardine oil diet with palm oil diet , 1998, Mechanisms of Ageing and Development.

[24]  N. Bazan,et al.  Effect of Bicuculline‐Induced Status Epilepticus on Prostaglandins and Hydroxyeicosatetraenoic Acids in Rat Brain Subcellular Fractions , 1987, Journal of neurochemistry.

[25]  Song‐Pyo Hong,et al.  Novel Docosanoids Inhibit Brain Ischemia-Reperfusion-mediated Leukocyte Infiltration and Pro-inflammatory Gene Expression* , 2003, Journal of Biological Chemistry.

[26]  B. Sacchetti,et al.  Astrocyte modulation of in vitro β‐amyloid neurotoxicity , 2004, Glia.

[27]  M. Lynch,et al.  Age-related changes in synaptic function: analysis of the effect of dietary supplementation with ω-3 fatty acids , 1999, Neuroscience.

[28]  R. Itzhaki,et al.  The significance of environmental factors in the etiology of Alzheimer's disease. , 2002, Journal of Alzheimer's disease : JAD.

[29]  Bente Pakkenberg,et al.  Neocortical Glial Cell Numbers in Alzheimer’s Disease , 2003, Dementia and Geriatric Cognitive Disorders.

[30]  A. Hofman,et al.  Dietary fat intake and the risk of incident dementia in the Rotterdam study , 1997, Annals of neurology.

[31]  W. Klein,et al.  Selective neuronal degeneration induced by soluble oligomeric amyloid beta‐protein , 2003, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[32]  M. Goldberg,et al.  Amyloid-β Peptides Are Cytotoxic to Oligodendrocytes , 2001, The Journal of Neuroscience.

[33]  T. Montine,et al.  Lipid peroxidation in aging brain and Alzheimer's disease. , 2002, Free radical biology & medicine.

[34]  J. Sweatt,et al.  Protein Kinase Inhibition by ω-3 Fatty Acids* , 2001, The Journal of Biological Chemistry.

[35]  N. Bazan.  Neuroprotectin D1 (NPD1): A DHA‐Derived Mediator that Protects Brain and Retina Against Cell Injury‐Induced Oxidative Stress , 2005, Brain pathology.

[36]  D. Bennett,et al.  Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. , 2003, Archives of neurology.

[37]  M. Hori,et al.  Contribution of microglia/macrophages to expansion of infarction and response of oligodendrocytes after focal cerebral ischemia in rats. , 2000, Stroke.

[38]  N. Bazan,et al.  Cyclooxygenase-2 and Presenilin-1 Gene Expression Induced by Interleukin-1β and Amyloid β42 Peptide Is Potentiated by Hypoxia in Primary Human Neural Cells* , 2002, The Journal of Biological Chemistry.

[39]  J. H. Boo,et al.  Interferon gamma stimulates beta-secretase expression and sAPPbeta production in astrocytes. , 2003, Biochemical and biophysical research communications.

[40]  R. Turner,et al.  Interleukin-1 and Nitric Oxide Increase NADPH Oxidase Activity in Human Coronary Artery Smooth Muscle Cells , 2003, Medical Principles and Practice.

[41]  A. LeBlanc,et al.  Selective cytotoxicity of intracellular amyloid β peptide1–42 through p53 and Bax in cultured primary human neurons , 2002, The Journal of cell biology.

[42]  Michael T. Heneka,et al.  Inflammatory processes in Alzheimer's disease , 2007, Journal of Neuroimmunology.

[43]  R. Busto,et al.  Systemic fatty acid responses to transient focal cerebral ischemia: influence of neuroprotectant therapy with human albumin , 2002, Journal of neurochemistry.

[44]  F. Wahl,et al.  Kinetics of polymorphonuclear neutrophil infiltration after a traumatic brain injury in rat. , 1999, Neuroreport.

[45]  Marta I. Aveldan˜o,et al.  Differential lipid deacylation during brain ischemia in a homeotherm and a poikilotherm. Content and composition of free fatty acids and triacylglycerols , 1975, Brain Research.

[46]  G. Lynch,et al.  Amyloid β protein is internalized selectively by hippocampal field CA1 and causes neurons to accumulate amyloidogenic carboxyterminal fragments of the amyloid precursor protein , 1998 .

[47]  M. Mattson,et al.  Secreted β-Amyloid Precursor Protein Counteracts the Proapoptotic Action of Mutant Presenilin-1 by Activation of NF-κB and Stabilization of Calcium Homeostasis* , 1998, The Journal of Biological Chemistry.

[48]  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.

[49]  M. Wolfe,et al.  Tumor Necrosis Factor-α, Interleukin-1β, and Interferon-γ Stimulate γ-Secretase-mediated Cleavage of Amyloid Precursor Protein through a JNK-dependent MAPK Pathway* , 2004, Journal of Biological Chemistry.

[50]  S. Hossain,et al.  Chronic Administration Of Docosahexaenoic Acid Improves The Performance Of Radial Arm Maze Task In Aged Rats , 2001, Clinical and experimental pharmacology & physiology.

[51]  P. Mukherjee,et al.  Neuroprotectin D 1 : A docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress , 2004 .

[52]  Jean-François Dartigues,et al.  Fish, meat, and risk of dementia: cohort study , 2002, BMJ : British Medical Journal.

[53]  W. Gordon,et al.  Docosahexaenoic acid utilization during rod photoreceptor cell renewal , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  M. Lynch,et al.  Age-related changes in synaptic function: analysis of the effect of dietary supplementation with omega-3 fatty acids. , 1999, Neuroscience.

[55]  G. Patton,et al.  Low serum docosahexaenoic acid is a significant risk factor for alzheimer’s dementia , 2007, Lipids.

[56]  C. Serhan,et al.  Resolvins , 2002, The Journal of experimental medicine.

[57]  Y. Koshino,et al.  Correlation between astrocyte apoptosis and Alzheimer changes in gray matter lesions in Alzheimer's disease. , 2005, Journal of Alzheimer's disease : JAD.

[58]  N. Bazan,et al.  Differential lipid deacylation during brain ischemia in a homeotherm and a poikilotherm. Content and composition of free fatty acids and triacylglycerols. , 1975, Brain research.

[59]  B. Slotnick,et al.  Cognitive deficits in docosahexaenoic acid-deficient rats. , 2002, Behavioral neuroscience.

[60]  N. Bazan,et al.  Docosahexaenoic acid (22:6, n-3) is metabolized to lipoxygenase reaction products in the retina. , 1984, Biochemical and biophysical research communications.

[61]  B. Halliwell,et al.  F4 ‐ Isoprostanes as Specific Marker of Docosahexaenoic Acid Peroxidation in Alzheimer's Disease , 1999, Journal of neurochemistry.

[62]  K. Tarte,et al.  The Bcl‐2 family member Bfl‐1/A1 is strongly repressed in normal and malignant plasma cells but is a potent anti‐apoptotic factor for myeloma cells , 2004, British journal of haematology.