Dietary Linoleic Acid Lowering Reduces Lipopolysaccharide-Induced Increase in Brain Arachidonic Acid Metabolism

Ho L, Pieroni C, Winger D, Purohit DP, Aisen PS, Pasinetti GM (1999) Regional distribution of cyclooxygenase-2 in the hippocampal formation in Alzheimer’s disease. J Neurosci Res 57(3):295–303

Suridjan I, Pollock BG, Verhoeff NP, Voineskos AN, Chow T, Rusjan PM, Lobaugh NJ, Houle S, Mulsant BH, Mizrahi R (2015) In-vivo imaging of grey and white matter neuroinflammation in Alzheimer’s disease: a positron emission tomography study with a novel radioligand, [F]-FEPPA. Mol Psychiatry. doi: 10.1038/mp.2015.1 .

Rao J, Chiappelli J, Kochunov P, Regenold WT, Rapoport SI, Hong LE (2014) Is schizophrenia a neurodegenerative disease? Evidence from age-related decline of brain-derived neurotrophic factor in the brains of schizophrenia patients and matched nonpsychiatric controls. Neurodegener Dis. doi: 10.1159/000369214

Primiani CT, Ryan VH, Rao JS, Cam MC, Ahn K, Modi HR, Rapoport SI (2014) Coordinated gene expression of neuroinflammatory and cell signaling markers in dorsolateral prefrontal cortex during human brain development and aging. PLoS One 9(10):e110972. doi: 10.1371/journal.pone.0110972

Esposito G, Giovacchini G, Liow JS, Bhattacharjee AK, Greenstein D, Schapiro M, Hallett M, Herscovitch P et al (2008) Imaging neuroinflammation in Alzheimer’s disease with radiolabeled arachidonic acid and PET. Eur J Nucl Med 49(9):1414–1421. doi: 10.2967/jnumed.107.049619

Hauss-Wegrzyniak B, Dobrzanski P, Stoehr JD, Wenk GL (1998) Chronic neuroinflammation in rats reproduces components of the neurobiology of Alzheimer’s disease. Brain Res 780(2):294–303

Kim WG, Mohney RP, Wilson B, Jeohn GH, Liu B, Hong JS (2000) Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J Neurosci 20(16):6309–6316

Xia Y, Yamagata K, Krukoff TL (2006) Differential expression of the CD14/TLR4 complex and inflammatory signaling molecules following i.c.v. administration of LPS. Brain Res 1095(1):85–95. doi: 10.1016/j.brainres.2006.03.112

Cunningham C, Wilcockson DC, Campion S, Lunnon K, Perry VH (2005) Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J Neurosci 25(40):9275–9284. doi: 10.1523/JNEUROSCI.2614-05.2005

Lee H, Villacreses NE, Rapoport SI, Rosenberger TA (2004) In vivo imaging detects a transient increase in brain arachidonic acid metabolism: a potential marker of neuroinflammation. J Neurochem 91(4):936–945. doi: 10.1111/j.1471-4159.2004.02786.x

Rosenberger TA, Villacreses NE, Weis MT, Rapoport SI (2010) Rat brain docosahexaenoic acid metabolism is not altered by a 6-day intracerebral ventricular infusion of bacterial lipopolysaccharide. Neurochem Int 56(3):501–507. doi: 10.1016/j.neuint.2009.12.010

Thambisetty M, Gallardo KA, Liow JS, Beason-Held LL, Umhau JC, Bhattacharjee AK, Der M, Herscovitch P et al (2012) The utility of (11)C-arachidonate PET to study in vivo dopaminergic neurotransmission in humans. J Cereb Blood Flow Metab 32(4):676–684. doi: 10.1038/jcbfm.2011.171

Wakabayashi S, Freed LM, Chang M, Rapoport SI (1995) In vivo imaging of brain incorporation of fatty acids and of 2-deoxy-D-glucose demonstrates functional and structural neuroplastic effects of chronic unilateral visual deprivation in rats. Brain Res 679(1):110–122

Blanchard HC, Taha AY, Rapoport SI, Yuan ZX (2015) Low-dose aspirin (acetylsalicylate) prevents increases in brain PGE, 15-epi-lipoxin A4 and 8-isoprostane concentrations in 9 month-old HIV-1 transgenic rats, a model for HIV-1 associated neurocognitive disorders. Prostaglandins Leukot Essent Fat Acids. doi: 10.1016/j.plefa.2015.01.002 .

Orr SK, Palumbo S, Bosetti F, Mount HT, Kang JX, Greenwood CE, Ma DW, Serhan CN et al (2013) Unesterified docosahexaenoic acid is protective in neuroinflammation. J Neurochem 127(3):378–393. doi: 10.1111/jnc.12392

Domenichiello AF, Chen CT, Trepanier MO, Stavro PM, Bazinet RP (2014) Whole body synthesis rates of DHA from alpha-linolenic acid are greater than brain DHA accretion and uptake rates in adult rats. J Lipid Res 55(1):62–74. doi: 10.1194/jlr.M042275

Hassam AG, Sinclair AJ, Crawford MA (1975) The incorporation of orally fed radioactive gamma-linolenic acid and linoleic acid into the liver and brain lipids of suckling rats. Lipids 10(7):417–420

Scott BL, Bazan NG (1989) Membrane docosahexaenoate is supplied to the developing brain and retina by the liver. Proc Natl Acad Sci U S A 86(8):2903–2907

Strokin M, Sergeeva M, Reiser G (2003) Docosahexaenoic acid and arachidonic acid release in rat brain astrocytes is mediated by two separate isoforms of phospholipase A2 and is differently regulated by cyclic AMP and Ca2+. Br J Pharmacol 139(5):1014–1022. doi: 10.1038/sj.bjp.0705326

Morrow JD, Harris TM, Roberts LJ 2nd (1990) Noncyclooxygenase oxidative formation of a series of novel prostaglandins: analytical ramifications for measurement of eicosanoids. Anal Biochem 184(1):1–10

Waugh RJ, Morrow JD, Roberts LJ 2nd, Murphy RC (1997) Identification and relative quantitation of F2-isoprostane regioisomers formed in vivo in the rat. Free Radic Biol Med 23(6):943–954

Arnold C, Markovic M, Blossey K, Wallukat G, Fischer R, Dechend R, Konkel A, von Schacky C et al (2010) Arachidonic acid-metabolizing cytochrome P450 enzymes are targets of {omega}-3 fatty acids. J Biol Chem 285(43):32720–32733. doi: 10.1074/jbc.M110.118406

Greco A, Ajmone-Cat MA, Nicolini A, Sciulli MG, Minghetti L (2003) Paracetamol effectively reduces prostaglandin E2 synthesis in brain macrophages by inhibiting enzymatic activity of cyclooxygenase but not phospholipase and prostaglandin E synthase. J Neurosci Res 71(6):844–852. doi: 10.1002/jnr.10543

Hong S, Gronert K, Devchand PR, Moussignac RL, Serhan CN (2003) Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. Autacoids in anti-inflammation. J Biol Chem 278(17):14677–14687. doi: 10.1074/jbc.M300218200

Calandria JM, Marcheselli VL, Mukherjee PK, Uddin J, Winkler JW, Petasis NA, Bazan NG (2009) Selective survival rescue in 15-lipoxygenase-1-deficient retinal pigment epithelial cells by the novel docosahexaenoic acid-derived mediator, neuroprotectin D1. J Biol Chem 284(26):17877–17882. doi: 10.1074/jbc.M109.003988

Fischer R, Konkel A, Mehling H, Blossey K, Gapelyuk A, Wessel N, von Schacky C, Dechend R et al (2014) Dietary omega-3 fatty acids modulate the eicosanoid profile in man primarily via the CYP-epoxygenase pathway. J Lipid Res 55(6):1150–1164. doi: 10.1194/jlr.M047357

Niemoller TD, Stark DT, Bazan NG (2009) Omega-3 fatty acid docosahexaenoic acid is the precursor of neuroprotectin D1 in the nervous system. World Rev Nutr Diet 99:46–54. doi: 10.1159/000192994

Igarashi M, Gao F, Kim HW, Ma K, Bell JM, Rapoport SI (2009) Dietary n-6 PUFA deprivation for 15 weeks reduces arachidonic acid concentrations while increasing n-3 PUFA concentrations in organs of post-weaning male rats. Biochim Biophys Acta 1791(2):132–139. doi: 10.1016/j.bbalip.2008.11.002

Kim HW, Rao JS, Rapoport SI, Igarashi M (2011) Dietary n-6 PUFA deprivation downregulates arachidonate but upregulates docosahexaenoate metabolizing enzymes in rat brain. Biochim Biophys Acta 1811(2):111–117. doi: 10.1016/j.bbalip.2010.10.005

Igarashi M, Kim HW, Chang L, Ma K, Rapoport SI (2012) Dietary n-6 polyunsaturated fatty acid deprivation increases docosahexaenoic acid metabolism in rat brain. J Neurochem 120(6):985–997. doi: 10.1111/j.1471-4159.2011.07597.x

Lin LE, Chen CT, Hildebrand KD, Liu Z, Hopperton KE, Bazinet RP (2015) Chronic dietary n-6 PUFA deprivation leads to conservation of arachidonic acid and more rapid loss of DHA in rat brain phospholipids. J Lipid Res 56(2):390–402. doi: 10.1194/jlr.M055590

Basselin M, Kim HW, Chen M, Ma K, Rapoport SI, Murphy RC, Farias SE (2010) Lithium modifies brain arachidonic and docosahexaenoic metabolism in rat lipopolysaccharide model of neuroinflammation. J Lipid Res 51(5):1049–1056. doi: 10.1194/jlr.M002469

Basselin M, Villacreses NE, Lee HJ, Bell JM, Rapoport SI (2007) Chronic lithium administration attenuates up-regulated brain arachidonic acid metabolism in a rat model of neuroinflammation. J Neurochem 102(3):761–772. doi: 10.1111/j.1471-4159.2007.04593.x

Kellom M, Basselin M, Keleshian VL, Chen M, Rapoport SI, Rao JS (2012) Dose-dependent changes in neuroinflammatory and arachidonic acid cascade markers with synaptic marker loss in rat lipopolysaccharide infusion model of neuroinflammation. BMC Neurosci 13:50. doi: 10.1186/1471-2202-13-50

Montine TJ, Milatovic D, Gupta RC, Valyi-Nagy T, Morrow JD, Breyer RM (2002) Neuronal oxidative damage from activated innate immunity is EP2 receptor-dependent. J Neurochem 83(2):463–470

Ramsden CE, Ringel A, Majchrzak-Hong SF, Yang J, Blanchard H, Zamora D, Loewke JD, Rapoport SI, Hibbeln JR, Davis JM, Hammock BD, Taha AY (2016) Dietary linoleic acid-induced alterations in pro- and anti-nociceptive lipid autacoids: Implications for idiopathic pain syndromes? Mol Pain. 12. doi: 10.1177/1744806916636386

Guesnet P, Lallemand SM, Alessandri JM, Jouin M, Cunnane SC (2011) alpha-Linolenate reduces the dietary requirement for linoleate in the growing rat. Prostaglandins Leukot Essent Fatty Acids 85(6):353–360. doi: 10.1016/j.plefa.2011.08.003

Reeves PG, Nielsen FH, Fahey GC Jr (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123(11):1939–1951

Demar JC Jr, Ma K, Chang L, Bell JM, Rapoport SI (2005) alpha-Linolenic acid does not contribute appreciably to docosahexaenoic acid within brain phospholipids of adult rats fed a diet enriched in docosahexaenoic acid. J Neurochem 94(4):1063–1076. doi: 10.1111/j.1471-4159.2005.03258.x

Deutsch J, Rapoport SI, Purdon AD (1997) Relation between free fatty acid and acyl-CoA concentrations in rat brain following decapitation. Neurochem Res 22(7):759–765

Bazinet RP, Lee HJ, Felder CC, Porter AC, Rapoport SI, Rosenberger TA (2005) Rapid high-energy microwave fixation is required to determine the anandamide (N-arachidonoylethanolamine) concentration of rat brain. Neurochem Res 30(5):597–601

Cheon Y, Park JY, Modi HR, Kim HW, Lee HJ, Chang L, Rao JS, Rapoport SI (2011) Chronic olanzapine treatment decreases arachidonic acid turnover and prostaglandin E(2) concentration in rat brain. J Neurochem 119(2):364–376. doi: 10.1111/j.1471-4159.2011.07410.x

Washizaki K, Smith QR, Rapoport SI, Purdon AD (1994) Brain arachidonic acid incorporation and precursor pool specific activity during intravenous infusion of unesterified [3H]arachidonate in the anesthetized rat. J Neurochem 63(2):727–736

Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1):497–509

Skipski VP, Good JJ, Barclay M, Reggio RB (1968) Quantitative analysis of simple lipid classes by thin-layer chromatography. Biochim Biophys Acta 152(1):10–19

Skipski VP, Barclay M, Reichman ES, Good JJ (1967) Separation of acidic phospholipids by one-dimensional thin-layer chromatography. Biochim Biophys Acta 137(1):80–89

Robinson PJ, Noronha J, DeGeorge JJ, Freed LM, Nariai T, Rapoport SI (1992) A quantitative method for measuring regional in vivo fatty-acid incorporation into and turnover within brain phospholipids: review and critical analysis. Brain Res Brain Res Rev 17(3):187–214

DeMar JC Jr, Lee HJ, Ma K, Chang L, Bell JM, Rapoport SI, Bazinet RP (2006) Brain elongation of linoleic acid is a negligible source of the arachidonate in brain phospholipids of adult rats. Biochim Biophys Acta 1761(9):1050–1059

Radin NS (1981) Extraction of tissue lipids with a solvent of low toxicity. Methods Enzymol 72:5–7

Yang HC, Mosior M, Johnson CA, Chen Y, Dennis EA (1999) Group-specific assays that distinguish between the four major types of mammalian phospholipase A2. Anal Biochem 269(2):278–288

Quan N, Whiteside M, Herkenham M (1998) Cyclooxygenase 2 mRNA expression in rat brain after peripheral injection of lipopolysaccharide. Brain Res 802(1–2):189–197

Fraga D, Zanoni CI, Zampronio AR, Parada CA, Rae GA, Souza GE (2016) Endocannabinoids, through opioids and prostaglandins, contribute to fever induced by key pyrogenic mediators. Brain Behav Immun 51:204–211. doi: 10.1016/j.bbi.2015.08.014

Rabin O, Deutsch J, Grange E, Pettigrew KD, Chang MC, Rapoport SI, Purdon AD (1997) Changes in cerebral acyl-CoA concentrations following ischemia-reperfusion in awake gerbils. J Neurochem 68(5):2111–2118

Tchelingerian JL, Quinonero J, Booss J, Jacque C (1993) Localization of TNF alpha and IL-1 alpha immunoreactivities in striatal neurons after surgical injury to the hippocampus. Neuron 10(2):213–224

Rosczyk HA, Sparkman NL, Johnson RW (2008) Neuroinflammation and cognitive function in aged mice following minor surgery. Exp Gerontol 43(9):840–846. doi: 10.1016/j.exger.2008.06.004

Xu J, Chalimoniuk M, Shu Y, Simonyi A, Sun AY, Gonzalez FA, Weisman GA, Wood WG et al (2003) Prostaglandin E2 production in astrocytes: regulation by cytokines, extracellular ATP, and oxidative agents. Prostaglandins Leukot Essent Fatty Acids 69(6):437–448

Kaplanski J, Nassar A, Sharon-Granit Y, Jabareen A, Kobal SL, Azab AN (2014) Lithium attenuates lipopolysaccharide-induced hypothermia in rats. Eur Rev Med Pharmacol Sci 18(12):1829–1837

Contreras MA, Greiner RS, Chang MC, Myers CS, Salem N Jr, Rapoport SI (2000) Nutritional deprivation of alpha-linolenic acid decreases but does not abolish turnover and availability of unacylated docosahexaenoic acid and docosahexaenoyl-CoA in rat brain. J Neurochem 75(6):2392–2400

Taha AY, Chang L, Chen M (2016) Threshold changes in rat brain docosahexaenoic acid incorporation and concentration following graded reductions in dietary alpha-linolenic acid. Prostaglandins Leukot Essent Fatty Acids 105:26–34. doi: 10.1016/j.plefa.2015.12.002

Matsumoto H, Naraba H, Murakami M, Kudo I, Yamaki K, Ueno A, Oh-ishi S (1997) Concordant induction of prostaglandin E2 synthase with cyclooxygenase-2 leads to preferred production of prostaglandin E2 over thromboxane and prostaglandin D2 in lipopolysaccharide-stimulated rat peritoneal macrophages. Biochem Biophys Res Commun 230(1):110–114. doi: 10.1006/bbrc.1996.5894

Milatovic D, Zaja-Milatovic S, Montine KS, Horner PJ, Montine TJ (2003) Pharmacologic suppression of neuronal oxidative damage and dendritic degeneration following direct activation of glial innate immunity in mouse cerebrum. J Neurochem 87(6):1518–1526

Milatovic D, Zaja-Milatovic S, Montine KS, Shie FS, Montine TJ (2004) Neuronal oxidative damage and dendritic degeneration following activation of CD14-dependent innate immune response in vivo. J Neuroinflammation 1(1):20. doi: 10.1186/1742-2094-1-20

Gogtay NJ (2010) Principles of sample size calculation. Indian J Ophthalmol 58(6):517–518. doi: 10.4103/0301-4738.71692

Ramsden CE, Faurot KR, Zamora D, Suchindran CM, Macintosh BA, Gaylord S, Ringel A, Hibbeln JR et al (2013) Targeted alteration of dietary n-3 and n-6 fatty acids for the treatment of chronic headaches: a randomized trial. Pain 154(11):2441–2451. doi: 10.1016/j.pain.2013.07.028

Ramsden CE, Faurot KR, Zamora D, Palsson OS, MacIntosh BA, Gaylord S, Taha AY, Rapoport SI et al (2015) Targeted alterations in dietary n-3 and n-6 fatty acids improve life functioning and reduce psychological distress among patients with chronic headache: a secondary analysis of a randomized trial. Pain 156(4):587–596. doi: 10.1097/01.j.pain.0000460348.84965.47