Neuroinflammatory processes in cognitive disorders: Is there a role for flavonoids and n-3 polyunsaturated fatty acids in counteracting their detrimental effects?

Neurochemistry International

Volumn 89, Issue , 2015, Pages 63-74

  Vauzour, David ^a   Martinsen, Anneloes ^a   Layé, Sophie ^b,c  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b NutriNeuro Bordeaux University   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Alzheimer's disease; Cognitive disorders; Flavonoids; Microglia; n 3 polyunsaturated fatty acids; Neuroinflammation

Indexed keywords

CHEMOKINE; FLAVONOID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; OMEGA 3 FATTY ACID; POLYUNSATURATED FATTY ACID; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; NEUROPROTECTIVE AGENT;

AGING; ALZHEIMER DISEASE; ANTIOXIDANT ACTIVITY; ASTROCYTE; CARDIOVASCULAR FUNCTION; COGNITION; COGNITIVE DEFECT; CYTOKINE PRODUCTION; DEGENERATIVE DISEASE; DIET; DIET SUPPLEMENTATION; HUMAN; INNATE IMMUNITY; MEMORY DISORDER; MICROGLIA; NERVE CELL DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; COGNITION DISORDERS; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; NEURODEGENERATIVE DISEASES;

ANIMALS; BRAIN; COGNITION DISORDERS; FATTY ACIDS, OMEGA-3; FLAVONOIDS; HUMANS; INFLAMMATION MEDIATORS; MICROGLIA; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS;

EID: 84942295644     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2015.08.004     Document Type: Review

References (173)

1. S. Aid, and F. Bosetti Gene expression of cyclooxygenase-1 and Ca(2+)-independent phospholipase A(2) is altered in rat hippocampus during normal aging Brain Res. Bull. 73 2007 108 113
2. S. Aid, and F. Bosetti Targeting cyclooxygenases-1 and -2 in neuroinflammation: therapeutic implications Biochimie 93 2011 46 51
3. C.M. Alfano, I. Imayama, M.L. Neuhouser, J.K. Kiecolt-Glaser, A.W. Smith, K. Meeske, A. McTiernan, L. Bernstein, K.B. Baumgartner, C.M. Ulrich, and R. Ballard-Barbash Fatigue, inflammation, and omega-3 and omega-6 fatty acid intake among breast cancer survivors J. Clin. Oncol. 30 2012 1280 1287
4. C. Andre, J.C. O'Connor, K.W. Kelley, J. Lestage, R. Dantzer, and N. Castanon Spatio-temporal differences in the profile of murine brain expression of proinflammatory cytokines and indoleamine 2,3-dioxygenase in response to peripheral lipopolysaccharide administration J. Neuroimmunol. 200 2008 90 99
5. A. Ariel, and C.N. Serhan Resolvins and protectins in the termination program of acute inflammation Trends Immunol. 28 2007 176 183
6. P. Barberger-Gateau, C. Raffaitin, L. Letenneur, C. Berr, C. Tzourio, J.F. Dartigues, and A. Alperovitch Dietary patterns and risk of dementia: the Three-City cohort study Neurology 69 2007 1921 1930
7. R.M. Barrientos, M.G. Frank, A.M. Hein, E.A. Higgins, L.R. Watkins, J.W. Rudy, and S.F. Maier Time course of hippocampal IL-1 beta and memory consolidation impairments in aging rats following peripheral infection Brain Behav. Immun. 23 2009 46 54
8. R.M. Barrientos, M.M. Kitt, L.R. Watkins, and S.F. Maier Neuroinflammation in the normal aging hippocampus Neuroscience 2015 10.1016/j.neuroscience.2015.03.007
9. N.G. Bazan Cell survival matters: docosahexaenoic acid signaling, neuroprotection and photoreceptors Trends Neurosci. 29 2006 263 271
10. N.G. Bazan, T.N. Eady, L. Khoutorova, K.D. Atkins, S. Hong, Y. Lu, C. Zhang, B. Jun, A. Obenaus, G. Fredman, M. Zhu, J.W. Winkler, N.A. Petasis, C.N. Serhan, and L. Belayev Novel aspirin-triggered neuroprotectin D1 attenuates cerebral ischemic injury after experimental stroke Exp. Neurol. 236 2012 122 130
11. N.G. Bazan, M.F. Molina, and W.C. Gordon Docosahexaenoic acid signalolipidomics in nutrition: significance in aging, neuroinflammation, macular degeneration, Alzheimer's, and other neurodegenerative diseases Annu. Rev. Nutr. 31 2011 321 351
12. R.P. Bazinet, and S. Laye Polyunsaturated fatty acids and their metabolites in brain function and disease Nat. Rev. Neurosci. 15 2014 771 785
13. A.W. Boots, L.C. Wilms, E.L. Swennen, J.C. Kleinjans, A. Bast, and G.R. Haenen In vitro and ex vivo anti-inflammatory activity of quercetin in healthy volunteers Nutrition 24 2008 703 710
14. A. Cagnin, M. Kassiou, S.R. Meikle, and R.B. Banati Positron emission tomography imaging of neuroinflammation Neurotherapeutics 4 2007 443 452
15. P.C. Calder n-3 fatty acids, inflammation and immunity: new mechanisms to explain old actions Proc. Nutr. Soc. 72 2013 326 336
16. P.C. Calder Marine omega-3 fatty acids and inflammatory processes: effects, mechanisms and clinical relevance Biochim. Biophys. Acta 1851 2015 469 484
17. P.C. Calder, and R.F. Grimble Polyunsaturated fatty acids, inflammation and immunity Eur. J. Clin. Nutr. 56 Suppl. 3 2002 S14 S19
18. B.M. Campbell, E. Charych, A.W. Lee, and T. Moller Kynurenines in CNS disease: regulation by inflammatory cytokines Front. Neurosci. 8 2014 12
19. L. Capuron, and A.H. Miller Immune system to brain signaling: neuropsychopharmacological implications Pharmacol. Ther. 130 2011 226 238
20. L. Capuron, S. Schroecksnadel, C. Feart, A. Aubert, D. Higueret, P. Barberger-Gateau, S. Laye, and D. Fuchs Chronic low-grade inflammation in elderly persons is associated with altered tryptophan and tyrosine metabolism: role in neuropsychiatric symptoms Biol. Psychiatry 70 2011 175 182
21. N. Castanon, J. Lasselin, and L. Capuron Neuropsychiatric comorbidity in obesity: role of inflammatory processes Front. Endocrinol. (Lausanne) 5 2014 74
22. N. Castanon, G. Luheshi, and S. Laye Role of neuroinflammation in the emotional and cognitive alterations displayed by animal models of obesity Front. Neurosci. 9 2015 229
23. R. Cazzola, and B. Cestaro Red wine polyphenols protect n-3 more than n-6 polyunsaturated fatty acid from lipid peroxidation Food Res. Int. 44 2011 3065 3071
24. X. Chen, X. Shi, X. Zhang, H. Lei, S. Long, H. Su, Z. Pei, and R. Huang Scutellarin attenuates hypertension-induced expression of brain Toll-like receptor 4/nuclear factor kappa B Mediat. Inflamm. 2013 2013 432623
25. J. Chu, P.F. Giannopoulos, C. Ceballos-Diaz, T.E. Golde, and D. Pratico 5-Lipoxygenase gene transfer worsens memory, amyloid, and tau brain pathologies in a mouse model of Alzheimer disease Ann. Neurol. 72 2012 442 454
26. J. Chu, J.G. Li, P.F. Giannopoulos, B.E. Blass, W. Childers, M. Abou-Gharbia, and D. Pratico Pharmacologic blockade of 12/15-lipoxygenase ameliorates memory deficits, Abeta and tau neuropathology in the triple-transgenic mice Mol. Psychiatry 2015 10.1038/mp.2014.170
27. J. Chu, and D. Pratico 5-Lipoxygenase pharmacological blockade decreases tau phosphorylation in vivo: involvement of the cyclin-dependent kinase-5 Neurobiol. Aging 34 2013 1549 1554
28. O.K. Chun, S.J. Chung, K.J. Claycombe, and W.O. Song Serum C-reactive protein concentrations are inversely associated with dietary flavonoid intake in U.S. adults J. Nutr. 138 2008 753 760
29. C. Cunningham, D.C. Wilcockson, S. Campion, K. Lunnon, and V.H. Perry Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration J. Neurosci. 25 2005 9275 9284
30. A. Currais, M. Prior, R. Dargusch, A. Armando, J. Ehren, D. Schubert, O. Quehenberger, and P. Maher Modulation of p25 and inflammatory pathways by fisetin maintains cognitive function in Alzheimer's disease transgenic mice Aging Cell 13 2014 379 390
31. R. Dantzer, R.M. Bluthe, G. Gheusi, S. Cremona, S. Laye, P. Parnet, and K.W. Kelley Molecular basis of sickness behavior Ann. N. Y. Acad. Sci. 856 1998 132 138
32. R. Dantzer, J.C. O'Connor, G.G. Freund, R.W. Johnson, and K.W. Kelley From inflammation to sickness and depression: when the immune system subjugates the brain Nat. Rev. Neurosci. 9 2008 46 56
33. S.M. de la Monte Brain insulin resistance and deficiency as therapeutic targets in Alzheimer's disease Curr. Alzheimer Res. 9 2012 35 66
34. V. De Smedt-Peyrusse, F. Sargueil, A. Moranis, H. Harizi, S. Mongrand, and S. Laye Docosahexaenoic acid prevents lipopolysaccharide-induced cytokine production in microglial cells by inhibiting lipopolysaccharide receptor presentation but not its membrane subdomain localization J. Neurochem. 105 2008 296 307
35. J.C. Delpech, C. Madore, C. Joffre, A. Aubert, J.X. Kang, A. Nadjar, and S. Laye Transgenic increase in n-3/n-6 fatty acid ratio protects against cognitive deficits induced by an immune challenge through decrease of neuroinflammation Neuropsychopharmacology 40 2015 525 536
36. J.C. Delpech, N. Saucisse, S.L. Parkes, C. Lacabanne, A. Aubert, F. Casenave, E. Coutureau, N. Sans, S. Laye, G. Ferreira, and A. Nadjar Microglial activation enhances associative taste memory through purinergic modulation of glutamatergic neurotransmission J. Neurosci. 35 2015 3022 3033
37. J.C. Delpech, A. Thomazeau, C. Madore, C. Bosch-Bouju, T. Larrieu, C. Lacabanne, J. Remus-Borel, A. Aubert, C. Joffre, A. Nadjar, and S. Laye Dietary n-3 PUFAs deficiency increases vulnerability to inflammation-induced spatial memory impairment Neuropsychopharmacology 2015 10.1038/npp.2015.127
38. E.E. Devore, J.H. Kang, M.M. Breteler, and F. Grodstein Dietary intakes of berries and flavonoids in relation to cognitive decline Ann. Neurol. 72 2012 135 143
39. R.N. Dilger, and R.W. Johnson Aging, microglial cell priming, and the discordant central inflammatory response to signals from the peripheral immune system J. Leukoc. Biol. 84 2008 932 939
40. A.L. Dinel, C. Andre, A. Aubert, G. Ferreira, S. Laye, and N. Castanon Lipopolysaccharide-induced brain activation of the indoleamine 2,3-dioxygenase and depressive-like behavior are impaired in a mouse model of metabolic syndrome Psychoneuroendocrinology 40 2014 48 59
41. H.C. Dunn, R.R. Ager, D. Baglietto-Vargas, D. Cheng, M. Kitazawa, D.H. Cribbs, and R. Medeiros Restoration of lipoxin A4 signaling reduces Alzheimer's disease-like pathology in the 3xTg-AD mouse model J. Alzheimers Dis. 43 2015 893 903
42. R. Farzaneh-Far, W.S. Harris, S. Garg, B. Na, and M.A. Whooley Inverse association of erythrocyte n-3 fatty acid levels with inflammatory biomarkers in patients with stable coronary artery disease: the Heart and Soul Study Atherosclerosis 205 2009 538 543
43. A.M. Fenn, C.J. Henry, Y. Huang, A. Dugan, and J.P. Godbout Lipopolysaccharide-induced interleukin (IL)-4 receptor-alpha expression and corresponding sensitivity to the M2 promoting effects of IL-4 are impaired in microglia of aged mice Brain Behav. Immun. 26 2012 766 777
44. S. Ferdinandusse, S. Denis, P.A. Mooijer, Z. Zhang, J.K. Reddy, A.A. Spector, and R.J. Wanders Identification of the peroxisomal beta-oxidation enzymes involved in the biosynthesis of docosahexaenoic acid J. Lipid Res. 42 2001 1987 1995
45. J.F. Ferguson, C.K. Mulvey, P.N. Patel, R.Y. Shah, J. Doveikis, W. Zhang, J. Tabita-Martinez, K. Terembula, M. Eiden, A. Koulman, J.L. Griffin, N.N. Mehta, R. Shah, K.J. Propert, W.L. Song, and M.P. Reilly Omega-3 PUFA supplementation and the response to evoked endotoxemia in healthy volunteers Mol. Nutr. Food Res. 58 2014 601 613
46. L. Ferrucci, A. Cherubini, S. Bandinelli, B. Bartali, A. Corsi, F. Lauretani, A. Martin, C. Andres-Lacueva, U. Senin, and J.M. Guralnik Relationship of plasma polyunsaturated fatty acids to circulating inflammatory markers J. Clin. Endocrinol. Metab. 91 2006 439 446
47. J.D. Figueroa, K. Cordero, K. Baldeosingh, A.I. Torrado, R.L. Walker, J.D. Miranda, and M.D. Leon Docosahexaenoic acid pretreatment confers protection and functional improvements after acute spinal cord injury in adult rats J. Neurotrauma 29 2012 551 566
48. L. Fratiglioni, S. Paillard-Borg, and B. Winblad An active and socially integrated lifestyle in late life might protect against dementia Lancet Neurol. 3 2004 343 353
49. L. Fratiglioni, B. Winblad, and E. von Strauss Prevention of Alzheimer's disease and dementia. Major findings from the Kungsholmen Project Physiol. Behav. 92 2007 98 104
50. G. Fredman, L. Ozcan, S. Spolitu, J. Hellmann, M. Spite, J. Backs, and I. Tabas Resolvin D1 limits 5-lipoxygenase nuclear localization and leukotriene B4 synthesis by inhibiting a calcium-activated kinase pathway Proc. Natl. Acad. Sci. U. S. A. 111 2014 14530 14535
51. R. Freese, O. Vaarala, A.M. Turpeinen, and M. Mutanen No difference in platelet activation or inflammation markers after diets rich or poor in vegetables, berries and apple in healthy subjects Eur. J. Nutr. 43 2004 175 182
52. F. Frenois, M. Moreau, J. O'Connor, M. Lawson, C. Micon, J. Lestage, K.W. Kelley, R. Dantzer, and N. Castanon Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior Psychoneuroendocrinology 32 2007 516 531
53. Y. Freund Levi, I. Vedin, T. Cederholm, H. Basun, G. Faxen Irving, M. Eriksdotter, E. Hjorth, M. Schultzberg, B. Vessby, L.O. Wahlund, N. Salem Jr., and J. Palmblad 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. 275 2014 428 436
54. K. Fritsche Fatty acids as modulators of the immune response Annu. Rev. Nutr. 26 2006 45 73
55. P.F. Giannopoulos, J. Chu, Y.B. Joshi, M. Sperow, J.G. Li, L.G. Kirby, and D. Pratico Gene knockout of 5-lipoxygenase rescues synaptic dysfunction and improves memory in the triple-transgenic model of Alzheimer's disease Mol. Psychiatry 19 2014 511 518
56. S. Gillette-Guyonnet, M. Secher, and B. Vellas Nutrition and neurodegeneration: epidemiological evidence and challenges for future research Br. J. Clin. Pharmacol. 75 2013 738 755
57. B. Giunta, H. Hou, Y. Zhu, J. Salemi, A. Ruscin, R.D. Shytle, and J. Tan Fish oil enhances anti-amyloidogenic properties of green tea EGCG in Tg2576 mice Neurosci. Lett. 471 2010 134 138
58. C.K. Glass, K. Saijo, B. Winner, M.C. Marchetto, and F.H. Gage Mechanisms underlying inflammation in neurodegeneration Cell 140 2010 918 934
59. J.P. Godbout, J. Chen, J. Abraham, A.F. Richwine, B.M. Berg, K.W. Kelley, and R.W. Johnson Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system FASEB J. 19 2005 1329 1331
60. J. Gonzalez-Gallego, M.V. Garcia-Mediavilla, S. Sanchez-Campos, and M.J. Tunon Fruit polyphenols, immunity and inflammation Br. J. Nutr. 104 Suppl. 3 2010 S15 S27
61. S.K. Ha, P. Lee, J.A. Park, H.R. Oh, S.Y. Lee, J.H. Park, E.H. Lee, J.H. Ryu, K.R. Lee, and S.Y. Kim Apigenin inhibits the production of NO and PGE2 in microglia and inhibits neuronal cell death in a middle cerebral artery occlusion-induced focal ischemia mice model Neurochem. Int. 52 2008 878 886
62. B. Halliwell Oxidative stress and neurodegeneration: where are we now? J. Neurochem. 97 2006 1634 1658
63. U.K. Hanisch, and H. Kettenmann Microglia: active sensor and versatile effector cells in the normal and pathologic brain Nat. Neurosci. 10 2007 1387 1394
64. R.J. Hardman, G. Kennedy, H. Macpherson, A.B. Scholey, and A. Pipingas A randomised controlled trial investigating the effects of Mediterranean diet and aerobic exercise on cognition in cognitively healthy older people living independently within aged care facilities: the Lifestyle Intervention in Independent Living Aged Care (LIILAC) study protocol [ACTRN12614001133628] Nutr. J. 14 2015 53
65. L. Harrington, C.V. Srikanth, R. Antony, S.J. Rhee, A.L. Mellor, H.N. Shi, and B.J. Cherayil Deficiency of indoleamine 2,3-dioxygenase enhances commensal-induced antibody responses and protects against Citrobacter rodentium-induced colitis Infect. Immun. 76 2008 3045 3053
66. M.T. Heneka, M.J. Carson, J.E. Khoury, G.E. Landreth, F. Brosseron, D.L. Feinstein, A.H. Jacobs, T. Wyss-Coray, J. Vitorica, R.M. Ransohoff, K. Herrup, S.A. Frautschy, B. Finsen, G.C. Brown, A. Verkhratsky, K. Yamanaka, J. Koistinaho, E. Latz, A. Halle, G.C. Petzold, T. Town, D. Morgan, M.L. Shinohara, V.H. Perry, C. Holmes, N.G. Bazan, D.J. Brooks, S. Hunot, B. Joseph, N. Deigendesch, O. Garaschuk, E. Boddeke, C.A. Dinarello, J.C. Breitner, G.M. Cole, D.T. Golenbock, and M.P. Kummer Neuroinflammation in Alzheimer's disease Lancet Neurol. 14 2015 388 405
67. M.T. Heneka, M.K. O'Banion, D. Terwel, and M.P. Kummer Neuroinflammatory processes in Alzheimer's disease J. Neural Transm. 117 2010 919 947
68. F.L. Heppner, R.M. Ransohoff, and B. Becher Immune attack: the role of inflammation in Alzheimer disease Nat. Rev. Neurosci. 16 2015 358 372
69. M.T. Herrero, C. Estrada, L. Maatouk, and S. Vyas Inflammation in Parkinson's disease: role of glucocorticoids Front. Neuroanat. 9 2015 32
70. E. Hjorth, M. Zhu, V.C. Toro, I. Vedin, J. Palmblad, T. Cederholm, Y. Freund-Levi, G. Faxen-Irving, L.O. Wahlund, H. Basun, M. Eriksdotter, and M. Schultzberg Omega-3 fatty acids enhance phagocytosis of Alzheimer's disease-related amyloid-beta42 by human microglia and decrease inflammatory markers J. Alzheimers Dis. 35 2013 697 713
71. W.L. Huang, V.R. King, O.E. Curran, S.C. Dyall, R.E. Ward, N. Lal, J.V. Priestley, and A.T. Michael-Titus A combination of intravenous and dietary docosahexaenoic acid significantly improves outcome after spinal cord injury Brain 130 2007 3004 3019
72. S. Huhn, S. Kharabian Masouleh, M. Stumvoll, A. Villringer, and A.V. Witte Components of a Mediterranean diet and their impact on cognitive functions in aging Front. Aging Neurosci. 7 2015 132
73. N. Jia, K. Han, J.J. Kong, X.M. Zhang, S. Sha, G.R. Ren, and Y.P. Cao (-)-Epigallocatechin-3-gallate alleviates spatial memory impairment in APP/PS1 mice by restoring IRS-1 signaling defects in the hippocampus Mol. Cell Biochem. 380 2013 211 218
74. M. Jung, S. Triebel, T. Anke, E. Richling, and G. Erkel Influence of apple polyphenols on inflammatory gene expression Mol. Nutr. Food Res. 53 2009 1263 1280
75. C.H. Kang, Y.H. Choi, S.K. Moon, W.J. Kim, and G.Y. Kim Quercetin inhibits lipopolysaccharide-induced nitric oxide production in BV2 microglial cells by suppressing the NF-kappaB pathway and activating the Nrf2-dependent HO-1 pathway Int. Immunopharmacol. 17 2013 808 813
76. T.K. Kao, Y.C. Ou, S.L. Raung, C.Y. Lai, S.L. Liao, and C.J. Chen Inhibition of nitric oxide production by quercetin in endotoxin/cytokine-stimulated microglia Life Sci. 86 2010 315 321
77. A. Karlsen, L. Retterstol, P. Laake, I. Paur, S.K. Bohn, L. Sandvik, and R. Blomhoff Anthocyanins inhibit nuclear factor-kappaB activation in monocytes and reduce plasma concentrations of pro-inflammatory mediators in healthy adults J. Nutr. 137 2007 1951 1954
78. E. Kesse-Guyot, L. Fezeu, V.A. Andreeva, M. Touvier, A. Scalbert, S. Hercberg, and P. Galan Total and specific polyphenol intakes in midlife are associated with cognitive function measured 13 years later J. Nutr. 142 2012 76 83
79. J.K. Kiecolt-Glaser, M.A. Belury, R. Andridge, W.B. Malarkey, and R. Glaser Omega-3 supplementation lowers inflammation and anxiety in medical students: a randomized controlled trial Brain Behav. Immun. 25 2011 1725 1734
80. J.K. Kiecolt-Glaser, M.A. Belury, K. Porter, D.Q. Beversdorf, S. Lemeshow, and R. Glaser Depressive symptoms, omega-6:omega-3 fatty acids, and inflammation in older adults Psychosom. Med. 69 2007 217 224
81. J.K. Kiecolt-Glaser, E.S. Epel, M.A. Belury, R. Andridge, J. Lin, R. Glaser, W.B. Malarkey, B.S. Hwang, and E. Blackburn Omega-3 fatty acids, oxidative stress, and leukocyte telomere length: a randomized controlled trial Brain Behav. Immun. 28 2013 16 24
82. V.F. Labrousse, A. Nadjar, C. Joffre, L. Costes, A. Aubert, S. Gregoire, L. Bretillon, and S. Laye Short-term long chain omega3 diet protects from neuroinflammatory processes and memory impairment in aged mice PLoS One 7 2012 e36861
83. M. Lalancette-Hebert, G. Gowing, A. Simard, Y.C. Weng, and J. Kriz Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain J. Neurosci. 27 2007 2596 2605
84. M. Lalancette-Hebert, C. Julien, P. Cordeau, I. Bohacek, Y.C. Weng, F. Calon, and J. Kriz Accumulation of dietary docosahexaenoic acid in the brain attenuates acute immune response and development of postischemic neuronal damage Stroke 42 2011 2903 2909
85. S. Laye Polyunsaturated fatty acids, neuroinflammation and well being Prostaglandins Leukot. Essent. Fat. Acids 82 2010 295 303
86. S. Laye, P. Parnet, E. Goujon, and R. Dantzer Peripheral administration of lipopolysaccharide induces the expression of cytokine transcripts in the brain and pituitary of mice Brain Res. Mol. Brain Res. 27 1994 157 162
87. J.J. Legos, R.F. Tuma, and F.C. Barone Pharmacological interventions for stroke: failures and future Expert Opin. Investig. Drugs 11 2002 603 614
88. J. Li, L. Ye, X. Wang, J. Liu, Y. Wang, Y. Zhou, and W. Ho (-)-Epigallocatechin gallate inhibits endotoxin-induced expression of inflammatory cytokines in human cerebral microvascular endothelial cells J. Neuroinflammation 9 2012 161
89. L. Li, Y. Wu, Y. Wang, J. Wu, L. Song, W. Xian, S. Yuan, L. Pei, and Y. Shang Resolvin D1 promotes the interleukin-4-induced alternative activation in BV-2 microglial cells J. Neuroinflammation 11 2014 72
90. S.N. Lim, W. Huang, J.C. Hall, A.T. Michael-Titus, and J.V. Priestley Improved outcome after spinal cord compression injury in mice treated with docosahexaenoic acid Exp. Neurol. 239 2013 13 27
91. C.C. Liu, J. Hu, C.W. Tsai, M. Yue, H.L. Melrose, T. Kanekiyo, and G. Bu Neuronal LRP1 regulates glucose metabolism and insulin signaling in the brain J. Neurosci. 35 2015 5851 5859
92. Y. Liu, F. Chen, J. Odle, X. Lin, S.K. Jacobi, H. Zhu, Z. Wu, and Y. Hou Fish oil enhances intestinal integrity and inhibits TLR4 and NOD2 signaling pathways in weaned pigs after LPS challenge J. Nutr. 142 2012 2017 2024
93. Y. Liu, X. Fu, N. Lan, S. Li, J. Zhang, S. Wang, C. Li, Y. Shang, T. Huang, and L. Zhang Luteolin protects against high fat diet-induced cognitive deficits in obesity mice Behav. Brain Res. 267 2014 178 188
94. Y. Lu, L.X. Zhao, D.L. Cao, and Y.J. Gao Spinal injection of docosahexaenoic acid attenuates carrageenan-induced inflammatory pain through inhibition of microglia-mediated neuroinflammation in the spinal cord Neuroscience 241 2013 22 31
95. W.J. Lukiw, J.G. Cui, V.L. Marcheselli, M. Bodker, A. Botkjaer, K. Gotlinger, C.N. Serhan, and N.G. Bazan A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease J. Clin. Invest. 115 2005 2774 2783
96. A.M. Lynch, D.J. Loane, A.M. Minogue, R.M. Clarke, D. Kilroy, R.E. Nally, O.J. Roche, F. O'Connell, and M.A. Lynch Eicosapentaenoic acid confers neuroprotection in the amyloid-beta challenged aged hippocampus Neurobiol. Aging 28 2007 845 855
97. A.M. Lynch, M. Moore, S. Craig, P.E. Lonergan, D.S. Martin, and M.A. Lynch Analysis of interleukin-1 beta-induced cell signaling activation in rat hippocampus following exposure to gamma irradiation. Protective effect of eicosapentaenoic acid J. Biol. Chem. 278 2003 51075 51084
98. Q.L. Ma, F. Yang, E.R. Rosario, O.J. Ubeda, W. Beech, D.J. Gant, P.P. Chen, B. Hudspeth, C. Chen, Y. Zhao, H.V. Vinters, S.A. Frautschy, and G.M. Cole Beta-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 J. Neurosci. 29 2009 9078 9089
99. A.L. Macready, T.W. George, M.F. Chong, D.S. Alimbetov, Y. Jin, A. Vidal, J.P. Spencer, O.B. Kennedy, K.M. Tuohy, A.M. Minihane, M.H. Gordon, and J.A. Lovegrove Flavonoid-rich fruit and vegetables improve microvascular reactivity and inflammatory status in men at risk of cardiovascular disease-FLAVURS: a randomized controlled trial Am. J. Clin. Nutr. 99 2014 479 489
100. C. Madore, A. Nadjar, J.C. Delpech, A. Sere, A. Aubert, C. Portal, C. Joffre, and S. Laye Nutritional n-3 PUFAs deficiency during perinatal periods alters brain innate immune system and neuronal plasticity-associated genes Brain Behav. Immun. 41 2014 22 31
101. V.L. Marcheselli, P.K. Mukherjee, M. Arita, S. Hong, R. Antony, K. Sheets, J.W. Winkler, N.A. Petasis, C.N. Serhan, and N.G. Bazan Neuroprotectin D1/protectin D1 stereoselective and specific binding with human retinal pigment epithelial cells and neutrophils Prostaglandins Leukot. Essent. Fat. Acids 82 2010 27 34
102. P.L. McGeer, and E.G. McGeer NSAIDs and Alzheimer disease: epidemiological, animal model and clinical studies Neurobiol. Aging 28 2007 639 647
103. R.K. McNamara, R. Jandacek, T. Rider, P. Tso, A. Cole-Strauss, and J.W. Lipton Omega-3 fatty acid deficiency increases constitutive pro-inflammatory cytokine production in rats: relationship with central serotonin turnover Prostaglandins Leukot. Essent. Fat. Acids 83 2010 185 191
104. S.N. Meydani, A.H. Lichtenstein, P.J. White, S.H. Goodnight, C.E. Elson, M. Woods, S.L. Gorbach, and E.J. Schaefer Food use and health effects of soybean and sunflower oils J. Am. Coll. Nutr. 10 1991 406 428
105. B. Michaeli, M.M. Berger, J.P. Revelly, L. Tappy, and R. Chiolero Effects of fish oil on the neuro-endocrine responses to an endotoxin challenge in healthy volunteers Clin. Nutr. 26 2007 70 77
106. R. Mingam, A. Moranis, R.M. Bluthe, V. De Smedt-Peyrusse, K.W. Kelley, P. Guesnet, M. Lavialle, R. Dantzer, and S. Laye Uncoupling of interleukin-6 from its signalling pathway by dietary n-3-polyunsaturated fatty acid deprivation alters sickness behaviour in mice Eur. J. Neurosci. 28 2008 1877 1886
107. A.M. Minogue, A.M. Lynch, D.J. Loane, C.E. Herron, and M.A. Lynch Modulation of amyloid-beta-induced and age-associated changes in rat hippocampus by eicosapentaenoic acid J. Neurochem. 103 2007 914 926
108. A. Moranis, J.C. Delpech, V. De Smedt-Peyrusse, A. Aubert, P. Guesnet, M. Lavialle, C. Joffre, and S. Laye 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 Brain Behav. Immun. 26 2012 721 731
109. A. Nanri, D. Yoshida, T. Yamaji, T. Mizoue, R. Takayanagi, and S. Kono Dietary patterns and C-reactive protein in Japanese men and women Am. J. Clin. Nutr. 87 2008 1488 1496
110. R.K. Narayan, M.E. Michel, B. Ansell, A. Baethmann, A. Biegon, M.B. Bracken, M.R. Bullock, S.C. Choi, G.L. Clifton, C.F. Contant, W.M. Coplin, W.D. Dietrich, J. Ghajar, S.M. Grady, R.G. Grossman, E.D. Hall, W. Heetderks, D.A. Hovda, J. Jallo, R.L. Katz, N. Knoller, P.M. Kochanek, A.I. Maas, J. Majde, D.W. Marion, A. Marmarou, L.F. Marshall, T.K. McIntosh, E. Miller, N. Mohberg, J.P. Muizelaar, L.H. Pitts, P. Quinn, G. Riesenfeld, C.S. Robertson, K.I. Strauss, G. Teasdale, N. Temkin, R. Tuma, C. Wade, M.D. Walker, M. Weinrich, J. Whyte, J. Wilberger, A.B. Young, and L. Yurkewicz Clinical trials in head injury J. Neurotrauma 19 2002 503 557
111. G. Neurauter, K. Schrocksnadel, S. Scholl-Burgi, B. Sperner-Unterweger, C. Schubert, M. Ledochowski, and D. Fuchs Chronic immune stimulation correlates with reduced phenylalanine turnover Curr. Drug Metab. 9 2008 622 627
112. T. Ngandu, J. Lehtisalo, A. Solomon, E. Levalahti, S. Ahtiluoto, R. Antikainen, L. Backman, T. Hanninen, A. Jula, T. Laatikainen, J. Lindstrom, F. Mangialasche, T. Paajanen, S. Pajala, M. Peltonen, R. Rauramaa, A. Stigsdotter-Neely, T. Strandberg, J. Tuomilehto, H. Soininen, and M. Kivipelto 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 Lancet 385 2015 2255 2263
113. L.N. Nguyen, D. Ma, G. Shui, P. Wong, A. Cazenave-Gassiot, X. Zhang, M.R. Wenk, E.L. Goh, and D.L. Silver Mfsd2a is a transporter for the essential omega-3 fatty acid docosahexaenoic acid Nature 509 2014 503 506
114. S.U. Noh, and Y.M. Park The effect of green tea polyphenols on macrophage migration inhibitory factor-associated steroid resistance Br. J. Dermatol. 166 2012 653 657
115. O. Odusanwo, S. Chinthamani, A. McCall, M.E. Duffey, and O.J. Baker Resolvin D1 prevents TNF-alpha-mediated disruption of salivary epithelial formation Am. J. Physiol. Cell Physiol. 302 2012 C1331 C1345
116. G. Olmos, and J. Llado Tumor necrosis factor alpha: a link between neuroinflammation and excitotoxicity Mediat. Inflamm. 2014 2014 861231
117. W.Y. Ong, T. Farooqui, G. Kokotos, and A.A. Farooqui Synthetic and natural inhibitors of phospholipases A2: their importance for understanding and treatment of neurological disorders ACS Chem. Neurosci. 6 6 2015 814 831
118. S.K. Orr, and R.P. Bazinet The emerging role of docosahexaenoic acid in neuroinflammation Curr. Opin. Investig. Drugs 9 2008 735 743
119. S.K. Orr, S. Palumbo, F. Bosetti, H.T. Mount, J.X. Kang, C.E. Greenwood, D.W. Ma, C.N. Serhan, and R.P. Bazinet Unesterified docosahexaenoic acid is protective in neuroinflammation J. Neurochem. 127 2013 378 393
120. G. Oxenkrug Interferon-gamma-inducible inflammation: contribution to aging and aging-associated psychiatric disorders Aging Dis. 2 2011 474 486
121. V.H. Perry, J.A. Nicoll, and C. Holmes Microglia in neurodegenerative disease Nat. Rev. Neurol. 6 2010 193 201
122. A.M. Pierdomenico, A. Recchiuti, F. Simiele, M. Codagnone, V.C. Mari, G. Davi, and M. Romano MicroRNA-181b regulates ALX/FPR2 receptor expression and proresolution signaling in human macrophages J. Biol. Chem. 290 2015 3592 3600
123. Z. Qu, F. Meng, H. Zhou, J. Li, Q. Wang, F. Wei, J. Cheng, C.M. Greenlief, D.B. Lubahn, G.Y. Sun, S. Liu, and Z. Gu NitroDIGE analysis reveals inhibition of protein S-nitrosylation by epigallocatechin gallates in lipopolysaccharide-stimulated microglial cells J. Neuroinflammation 11 2014 17
124. S.I. Rapoport Brain arachidonic and docosahexaenoic acid cascades are selectively altered by drugs, diet and disease Prostaglandins Leukot. Essent. Fat. Acids 79 2008 153 156
125. S.S. Raza, M.M. Khan, A. Ahmad, M. Ashafaq, F. Islam, A.P. Wagner, M.M. Safhi, and F. Islam Neuroprotective effect of naringenin is mediated through suppression of NF-kappaB signaling pathway in experimental stroke Neuroscience 230 2013 157 171
126. D. Rees, E.A. Miles, T. Banerjee, S.J. Wells, C.E. Roynette, K.W. Wahle, and P.C. Calder Dose-related effects of eicosapentaenoic acid on innate immune function in healthy humans: a comparison of young and older men Am. J. Clin. Nutr. 83 2006 331 342
127. K. Rezai-Zadeh, J. Ehrhart, Y. Bai, P.R. Sanberg, P. Bickford, J. Tan, and R.D. Shytle Apigenin and luteolin modulate microglial activation via inhibition of STAT1-induced CD40 expression J. Neuroinflammation 5 2008 41
128. D.S. Rice, J.M. Calandria, W.C. Gordon, B. Jun, Y. Zhou, C.M. Gelfman, S. Li, M. Jin, E.J. Knott, B. Chang, A. Abuin, T. Issa, D. Potter, K.A. Platt, and N.G. Bazan Adiponectin receptor 1 conserves docosahexaenoic acid and promotes photoreceptor cell survival Nat. Commun. 6 2015 6228
129. B.D. Rockett, A. Franklin, M. Harris, H. Teague, A. Rockett, and S.R. Shaikh Membrane raft organization is more sensitive to disruption by (n-3) PUFA than nonraft organization in EL4 and B cells J. Nutr. 141 2011 1041 1048
130. A. Rodriguez-Mateos, D. Vauzour, C.G. Krueger, D. Shanmuganayagam, J. Reed, L. Calani, P. Mena, D. Del Rio, and A. Crozier Bioavailability, bioactivity and impact on health of dietary flavonoids and related compounds: an update Arch. Toxicol. 88 2014 1803 1853
131. J.M. Rubio-Perez, and J.M. Morillas-Ruiz Serum cytokine profile in Alzheimer's disease patients after ingestion of an antioxidant beverage CNS Neurol. Disord. Drug Targets 12 2013 1233 1241
132. M.R. Ruth, S.D. Proctor, and C.J. Field 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 Br. J. Nutr. 101 2009 1341 1350
133. J. Salas-Salvado, A. Garcia-Arellano, R. Estruch, F. Marquez-Sandoval, D. Corella, M. Fiol, E. Gomez-Gracia, E. Vinoles, F. Aros, C. Herrera, C. Lahoz, J. Lapetra, J.S. Perona, D. Munoz-Aguado, M.A. Martinez-Gonzalez, and E. Ros Components of the Mediterranean-type food pattern and serum inflammatory markers among patients at high risk for cardiovascular disease Eur. J. Clin. Nutr. 62 2008 651 659
134. P. Scheltens, J.W. Twisk, R. Blesa, E. Scarpini, C.A. von Arnim, A. Bongers, J. Harrison, S.H. Swinkels, C.J. Stam, H. de Waal, R.J. Wurtman, R.L. Wieggers, B. Vellas, and P.J. Kamphuis Efficacy of Souvenaid in mild Alzheimer's disease: results from a randomized, controlled trial J. Alzheimers Dis. 31 2012 225 236
135. C.N. Serhan Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways Annu. Rev. Immunol. 25 2007 101 137
136. C.N. Serhan, S.D. Brain, C.D. Buckley, D.W. Gilroy, C. Haslett, L.A. O'Neill, M. Perretti, A.G. Rossi, and J.L. Wallace Resolution of inflammation: state of the art, definitions and terms FASEB J. 21 2007 325 332
137. C.N. Serhan, and N. Chiang Resolution phase lipid mediators of inflammation: agonists of resolution Curr. Opin. Pharmacol. 13 2013 632 640
138. C.N. Serhan, G. Fredman, R. Yang, S. Karamnov, L.S. Belayev, N.G. Bazan, M. Zhu, J.W. Winkler, and N.A. Petasis Novel proresolving aspirin-triggered DHA pathway Chem. Biol. 18 2011 976 987
139. Z. Shu, B. Yang, H. Zhao, B. Xu, W. Jiao, Q. Wang, Z. Wang, and H. Kuang Tangeretin exerts anti-neuroinflammatory effects via NF-kappaB modulation in lipopolysaccharide-stimulated microglial cells Int. Immunopharmacol. 19 2014 275 282
140. B. Shukitt-Hale, F.C. Lau, A.N. Carey, R.L. Galli, E.L. Spangler, D.K. Ingram, and J.A. Joseph Blueberry polyphenols attenuate kainic acid-induced decrements in cognition and alter inflammatory gene expression in rat hippocampus Nutr. Neurosci. 11 2008 172 182
141. J.W. Sijben, and P.C. Calder Differential immunomodulation with long-chain n-3 PUFA in health and chronic disease Proc. Nutr. Soc. 66 2007 237 259
142. F. Sofi, R. Abbate, G.F. Gensini, and A. Casini Accruing evidence on benefits of adherence to the Mediterranean diet on health: an updated systematic review and meta-analysis Am. J. Clin. Nutr. 92 2010 1189 1196
143. B.J. Song, A. Elbert, T. Rahman, S.K. Orr, C.T. Chen, M. Febbraio, and R.P. Bazinet Genetic ablation of CD36 does not alter mouse brain polyunsaturated fatty acid concentrations Lipids 45 2010 291 299
144. C. Song, B.E. Leonard, and D.F. Horrobin Dietary ethyl-eicosapentaenoic acid but not soybean oil reverses central interleukin-1-induced changes in behavior, corticosterone and immune response in rats Stress 7 2004 43 54
145. C. Song, M.S. Manku, and D.F. Horrobin Long-chain polyunsaturated fatty acids modulate interleukin-1beta-induced changes in behavior, monoaminergic neurotransmitters, and brain inflammation in rats J. Nutr. 138 2008 954 963
146. N.L. Sparkman, L.A. Martin, W.S. Calvert, and G.W. Boehm Effects of intraperitoneal lipopolysaccharide on Morris maze performance in year-old and 2-month-old female C57BL/6J mice Behav. Brain Res. 159 2005 145 151
147. K. Suk, H. Lee, S.S. Kang, G.J. Cho, and W.S. Choi Flavonoid baicalein attenuates activation-induced cell death of brain microglia J. Pharmacol. Exp. Ther. 305 2003 638 645
148. J.R. Sundaram, C.P. Poore, N.H. Sulaimee, T. Pareek, A.B. Asad, R. Rajkumar, W.F. Cheong, M.R. Wenk, G.S. Dawe, K.H. Chuang, H.C. Pant, and S. Kesavapany Specific inhibition of p25/Cdk5 activity by the Cdk5 inhibitory peptide reduces neurodegeneration in vivo J. Neurosci. 33 2013 334 343
149. C.C. Tangney, M.J. Kwasny, H. Li, R.S. Wilson, D.A. Evans, and M.C. Morris Adherence to a Mediterranean-type dietary pattern and cognitive decline in a community population Am. J. Clin. Nutr. 93 2011 601 607
150. M.E. Tremblay, B. Stevens, A. Sierra, H. Wake, A. Bessis, and A. Nimmerjahn The role of microglia in the healthy brain J. Neurosci. 31 2011 16064 16069
151. D. Vauzour Dietary polyphenols as modulators of brain functions: biological actions and molecular mechanisms underpinning their beneficial effects Oxid. Med. Cell Longev. 2012 2012 914273
152. D. Vauzour Effect of flavonoids on learning, memory and neurocognitive performance: relevance and potential implications for Alzheimer's disease pathophysiology J. Sci. Food Agric. 94 2014 1042 1056
153. I. Vedin, T. Cederholm, Y. Freund Levi, H. Basun, A. Garlind, G. Faxen Irving, M.E. Jonhagen, B. Vessby, L.O. Wahlund, and J. Palmblad Effects of docosahexaenoic acid-rich n-3 fatty acid supplementation on cytokine release from blood mononuclear leukocytes: the OmegAD study Am. J. Clin. Nutr. 87 2008 1616 1622
154. Q. Wang, X. Zheng, Y. Cheng, Y.L. Zhang, H.X. Wen, Z. Tao, H. Li, Y. Hao, Y. Gao, L.M. Yang, F.G. Smith, C.J. Huang, and S.W. Jin 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 J. Immunol. 192 2014 3765 3777
155. X. Wang, E. Hjorth, I. Vedin, M. Eriksdotter, Y. Freund-Levi, L.O. Wahlund, T. Cederholm, J. Palmblad, and M. Schultzberg Effects of n-3 FA supplementation on the release of proresolving lipid mediators by blood mononuclear cells: the OmegAD study J. Lipid Res. 56 2015 674 681
156. X. Wang, M. Zhu, E. Hjorth, V. Cortes-Toro, H. Eyjolfsdottir, C. Graff, I. Nennesmo, J. Palmblad, M. Eriksdotter, K. Sambamurti, J.M. Fitzgerald, C.N. Serhan, A.C. Granholm, and M. Schultzberg Resolution of inflammation is altered in Alzheimer's disease Alzheimers Dement. 11 2015 40 50 e41-42
157. J. Warford, Q.R. Jones, M. Nichols, V. Sullivan, H.P. Rupasinghe, and G.S. Robertson The flavonoid-enriched fraction AF4 suppresses neuroinflammation and promotes restorative gene expression in a mouse model of experimental autoimmune encephalomyelitis J. Neuroimmunol. 268 2014 71 83
158. M.E. Widlansky, S.J. Duffy, N.M. Hamburg, N. Gokce, B.A. Warden, S. Wiseman, J.F. Keaney Jr., B. Frei, and J.A. Vita Effects of black tea consumption on plasma catechins and markers of oxidative stress and inflammation in patients with coronary artery disease Free Radic. Biol. Med. 38 2005 499 506
159. R.J. Williams, J.P. Spencer, and C. Rice-Evans Flavonoids: antioxidants or signalling molecules? Free Radic. Biol. Med. 36 2004 838 849
160. S.S. Wu, and S.J. Frucht Treatment of Parkinson's disease: what's on the horizon? CNS Drugs 19 2005 723 743
161. M.X. Xu, B.C. Tan, W. Zhou, T. Wei, W.H. Lai, J.W. Tan, and J.H. Dong Resolvin D1, an endogenous lipid mediator for inactivation of inflammation-related signaling pathways in microglial cells, prevents lipopolysaccharide-induced inflammatory responses CNS Neurosci. Ther. 19 2013 235 243
162. L. Yang, Y. Zhang, S. Wang, W. Zhang, and R. Shi Decreased liver peroxisomal beta-oxidation accompanied by changes in brain fatty acid composition in aged rats Neurol. Sci. 35 2014 289 293
163. C.M. Yates, P.C. Calder, and G. Ed Rainger Pharmacology and therapeutics of omega-3 polyunsaturated fatty acids in chronic inflammatory disease Pharmacol. Ther. 141 2014 272 282
164. C.H. Yeh, M.L. Yang, C.Y. Lee, C.P. Yang, Y.C. Li, C.J. Chen, and Y.H. Kuan Wogonin attenuates endotoxin-induced prostaglandin E2 and nitric oxide production via Src-ERK1/2-NFkappaB pathway in BV-2 microglial cells Environ. Toxicol. 29 2014 1162 1170
165. S. Yehuda, S. Rabinovitz, R.L. Carasso, and D.I. Mostofsky The role of polyunsaturated fatty acids in restoring the aging neuronal membrane Neurobiol. Aging 23 2002 843 853
166. S. Yehuda, S. Rabinovitz, and D.I. Mostofsky Essential fatty acids and the brain: from infancy to aging Neurobiol. Aging 26 Suppl. 1 2005 98 102
167. K.A. Youdim, B. Shukitt-Hale, and J.A. Joseph Flavonoids and the brain: interactions at the blood-brain barrier and their physiological effects on the central nervous system Free Radic. Biol. Med. 37 2004 1683 1693
168. L. Yu, C. Chen, L.F. Wang, X. Kuang, K. Liu, H. Zhang, and J.R. Du Neuroprotective effect of kaempferol glycosides against brain injury and neuroinflammation by inhibiting the activation of NF-kappaB and STAT3 in transient focal stroke PLoS One 8 2013 e55839
169. D.R. Zamzow, V. Elias, L.L. Legette, J. Choi, J.F. Stevens, and K.R. Magnusson Xanthohumol improved cognitive flexibility in young mice Behav. Brain Res. 275 2014 1 10
170. X. Zhou, P. Gan, L. Hao, L. Tao, J. Jia, B. Gao, J.Y. Liu, L.T. Zheng, and X. Zhen Antiinflammatory effects of orientin-2″-O-galactopyranoside on lipopolysaccharide-stimulated microglia Biol. Pharm. Bull. 37 2014 1282 1294
171. M. Zhu, X. Wang, M. Schultzberg, and E. Hjorth Differential regulation of resolution in inflammation induced by amyloid-beta42 and lipopolysaccharides in human microglia J. Alzheimers Dis. 43 2015 1237 1250
172. Y. Zhu, P.C. Bickford, P. Sanberg, B. Giunta, and J. Tan Blueberry opposes beta-amyloid peptide-induced microglial activation via inhibition of p44/42 mitogen-activation protein kinase Rejuvenation Res. 11 2008 891 901
173. P.A. Zunszain, C. Anacker, A. Cattaneo, S. Choudhury, K. Musaelyan, A.M. Myint, S. Thuret, J. Price, and C.M. Pariante Interleukin-1beta: a new regulator of the kynurenine pathway affecting human hippocampal neurogenesis Neuropsychopharmacology 37 2012 939 949