Polyunsaturated fatty acids and endocannabinoids in health and disease

References

• Catala A. Five decades with polyunsaturated fatty acids: chemical synthesis, enzymatic formation, lipid peroxidation and its biological effects. J Lipids 2013;2013:710290.
   Google Scholar
• Brown I, Cascio MG, Rotondo D, Pertwee RG, Heys SD, Wahle KW. Cannabinoids and omega-3/6 endocannabinoids as cell death and anticancer modulators. Prog Lipid Res 2013;52(1):80–109.
   Google Scholar
• Bisogno T, Maccarrone M. Endocannabinoid signaling and its regulation by nutrients. BioFactors (Oxford, England) 2014;40(4):373–80.
   PubMed Web of Science ®Google Scholar
• Kim J, Li Y, Watkins BA. Endocannabinoid signaling and energy metabolism: a target for dietary intervention. Nutrition 2011;27(6):624–32.
   PubMed Web of Science ®Google Scholar
• D’Addario C, Di Francesco A, Pucci M, Finazzi Agro A, Maccarrone M. Epigenetic mechanisms and endocannabinoid signalling. FEBS J 2013;280(9):1905–17.
   Google Scholar
• Artmann A, Petersen G, Hellgren LI, Boberg J, Skonberg C, Nellemann C, et al. Influence of dietary fatty acids on endocannabinoid and N-acylethanolamine levels in rat brain, liver and small intestine. Biochim Biophys Acta 2008;1781(4):200–12.
   PubMed Web of Science ®Google Scholar
• Wood JT, Williams JS, Pandarinathan L, Janero DR, Lammi-Keefe CJ, Makriyannis A. Dietary docosahexaenoic acid supplementation alters select physiological endocannabinoid-system metabolites in brain and plasma. J Lipid Res 2010;51(6):1416–23.
   Google Scholar
• Murru E, Banni S, Carta G. Nutritional properties of dietary omega-3-enriched phospholipids. BioMed Res Int 2013;2013:965417.
   Google Scholar
• Silvestri C, Di Marzo V. The endocannabinoid system in energy homeostasis and the etiopathology of metabolic disorders. Cell Metab 2013;17(4):475–90.
   PubMed Web of Science ®Google Scholar
• Pacher P, Kunos G. Modulating the endocannabinoid system in human health and disease – successes and failures. FEBS J 2013;280(9):1918–43.
   PubMed Web of Science ®Google Scholar
• Simopoulos AP. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother 2002;56(8):365–79.
   PubMed Web of Science ®Google Scholar
• Kim J, Li Y, Watkins BA. Fat to treat fat: emerging relationship between dietary PUFA, endocannabinoids, and obesity. Prostaglandins Lipid Mediat 2013;104–105:32–41.
   Web of Science ®Google Scholar
• Fagundo AB, de la Torre R, Jimenez-Murcia S, Aguera Z, Pastor A, Casanueva FF, et al. Modulation of the endocannabinoids N-arachidonoylethanolamine (AEA) and 2-arachidonoylglycerol (2-AG) on executive functions in humans. PLoS ONE 2013;8(6):e66387.
   PubMed Web of Science ®Google Scholar
• Grant WF, Gillingham MB, Batra AK, Fewkes NM, Comstock SM, Takahashi D, et al. Maternal high fat diet is associated with decreased plasma n-3 fatty acids and fetal hepatic apoptosis in nonhuman primates. PLoS ONE 2011;6(2):e17261.
   Google Scholar
• Fride E. Endocannabinoids in the central nervous system – an overview. Prostaglandins Leukot Essent Fatty Acids 2002;66(2–3):221–33.
   PubMed Web of Science ®Google Scholar
• Mechoulam R, Parker LA. The endocannabinoid system and the brain. Ann Rev Psychol 2013;64:21–47.
   PubMed Web of Science ®Google Scholar
• Cascio MG. PUFA-derived endocannabinoids: an overview. Proc Nutr Soc 2013;72(4):451–9.
   Google Scholar
• Popkin BM. Nutrition transition and the global diabetes epidemic. Curr Diabetes Rep 2015;15(9):5.
   Google Scholar
• Conde WL, Monteiro CA. Nutrition transition and double burden of undernutrition and excess of weight in Brazil. Am J Clin Nutr 2014;100(6):1617S–22S.
   PubMed Web of Science ®Google Scholar
• Naughton SS, Mathai ML, Hryciw DH, McAinch AJ. Australia’s nutrition transition 1961-2009: a focus on fats. Br J Nutr 2015;114(3):337–46.
   Google Scholar
• Kearney J. Food consumption trends and drivers. Philos Trans R Soc London Ser B, Biol Sci 2010;365(1554):2793–807.
   PubMed Web of Science ®Google Scholar
• Torres-Fuentes C, Schellekens H, Dinan TG, Cryan JF. A natural solution for obesity: bioactives for the prevention and treatment of weight gain. A review. Nutr Neurosci 2015;18(2):49–65.
   PubMed Web of Science ®Google Scholar
• Cardel M, Lemas DJ, Jackson KH, Friedman JE, Fernandez JR. Higher intake of PUFAs is associated with lower total and visceral adiposity and higher lean mass in a racially diverse sample of children. J Nutr 2015;145(9):2146–52.
   Google Scholar
• Thorsdottir I, Tomasson H, Gunnarsdottir I, Gisladottir E, Kiely M, Parra MD, et al. Randomized trial of weight-loss-diets for young adults varying in fish and fish oil content. Int J Obes (Lond) 2007;31(10):1560–6.
   Google Scholar
• Wang F, Wang Y, Zhu Y, Liu X, Xia H, Yang X, et al. Treatment for 6 months with fish oil-derived n-3 polyunsaturated fatty acids has neutral effects on glycemic control but improves dyslipidemia in type 2 diabetic patients with abdominal obesity: a randomized, double-blind, placebo-controlled trial. Eur J Nutr 2016:1–8. doi: 10.1007/s00394-016-1352-4.
   Google Scholar
• James MJ, Gibson RA, Cleland LG. Dietary polyunsaturated fatty acids and inflammatory mediator production. Am J Clin Nutr 2000;71(1 Suppl):343S–8S.
   PubMed Web of Science ®Google Scholar
• Norris PC, Dennis EA. Omega-3 fatty acids cause dramatic changes in TLR4 and purinergic eicosanoid signaling. Proc Natl Acad Sci USA 2012;109(22):8517–22.
   Google Scholar
• Innis SM. Dietary (n-3) fatty acids and brain development. J Nutr 2007;137(4):855–9.
   PubMed Web of Science ®Google Scholar
• Bigford GE, Del Rossi G. Supplemental substances derived from foods as adjunctive therapeutic agents for treatment of neurodegenerative diseases and disorders. Adv Nutr (Bethesda, MD) 2014;5(4):394–403.
   Google Scholar
• Bosma-den Boer MM, van Wetten ML, Pruimboom L. Chronic inflammatory diseases are stimulated by current lifestyle: how diet, stress levels and medication prevent our body from recovering. Nutr Metab (Lond) 2012;9(1):32.
   Google Scholar
• Larrieu T, Madore C, Joffre C, Laye S. Nutritional n-3 polyunsaturated fatty acids deficiency alters cannabinoid receptor signaling pathway in the brain and associated anxiety-like behavior in mice. J Physiol Biochem 2012;68(4):671–81.
   PubMed Web of Science ®Google Scholar
• Pan JP, Zhang HQ, Wei W, Guo YF, Na X, Cao XH, et al. Some subtypes of endocannabinoid/endovanilloid receptors mediate docosahexaenoic acid-induced enhanced spatial memory in rats. Brain Res 2011;1412:18–27.
   PubMed Web of Science ®Google Scholar
• Straiker A, Mitjavila J, Yin D, Gibson A, Mackie K. Aiming for allosterism: evaluation of allosteric modulators of CB1 in a neuronal model. Pharmacol Res Off J Ital Pharmacol Soc 2015;99:370–6.
   PubMed Web of Science ®Google Scholar
• Lafourcade M, Larrieu T, Mato S, Duffaud A, Sepers M, Matias I, et al. Nutritional omega-3 deficiency abolishes endocannabinoid-mediated neuronal functions. Nat Neurosci 2011;14(3):345–50.
   PubMed Web of Science ®Google Scholar
• Watanabe S, Doshi M, Hamazaki T. n-3 Polyunsaturated fatty acid (PUFA) deficiency elevates and n-3 PUFA enrichment reduces brain 2-arachidonoylglycerol level in mice. Prostaglandins Leukot Essent Fatty Acids 2003;69(1):51–9.
   PubMedGoogle Scholar
• Piscitelli F, Carta G, Bisogno T, Murru E, Cordeddu L, Berge K, et al. Effect of dietary krill oil supplementation on the endocannabinoidome of metabolically relevant tissues from high-fat-fed mice. Nutr Metab (Lond). 2011;8(1):51.
   PubMedGoogle Scholar
• Batetta B, Griinari M, Carta G, Murru E, Ligresti A, Cordeddu L, et al. Endocannabinoids may mediate the ability of (n-3) fatty acids to reduce ectopic fat and inflammatory mediators in obese Zucker rats. J Nutr. 2009;139(8):1495–501.
   PubMed Web of Science ®Google Scholar
• Kuda O, Rombaldova M, Janovska P, Flachs P, Kopecky J. Cell type-specific modulation of lipid mediator’s formation in murine adipose tissue by omega-3 fatty acids. Biochem Biophys Res Commun 2016;469(3):731–6.
   Google Scholar
• Kim J, Carlson ME, Kuchel GA, Newman JW, Watkins BA. Dietary DHA reduces downstream endocannabinoid and inflammatory gene expression and epididymal fat mass while improving aspects of glucose use in muscle in C57BL/6J mice. Int J Obes (Lond) 2016;40(1):129–37.
   Google Scholar
• Naughton SS, Mathai ML, Hryciw DH, McAinch AJ. Fatty acid modulation of the endocannabinoid system and the effect on food intake and metabolism. Int J Endocrinol 2013;2013:361895.
   Google Scholar
• Bennetzen MF, Nielsen TS, Paulsen SK, Bendix J, Fisker S, Jessen N, et al. Reduced cannabinoid receptor 1 protein in subcutaneous adipose tissue of obese. Eur J Clin Invest 2010;40(2):121–6.
   Google Scholar
• Bluher M, Engeli S, Kloting N, Berndt J, Fasshauer M, Batkai S, et al. Dysregulation of the peripheral and adipose tissue endocannabinoid system in human abdominal obesity. Diabetes 2006;55(11):3053–60.
   PubMed Web of Science ®Google Scholar
• Berger A, Crozier G, Bisogno T, Cavaliere P, Innis S, Di Marzo V. Anandamide and diet: inclusion of dietary arachidonate and docosahexaenoate leads to increased brain levels of the corresponding N-acylethanolamines in piglets. Proc Natl Acad Sci USA 2001;98(11):6402–6.
   PubMedGoogle Scholar
• Moon RJ, Harvey NC, Robinson SM, Ntani G, Davies JH, Inskip HM, et al. Maternal plasma polyunsaturated fatty acid status in late pregnancy is associated with offspring body composition in childhood. J Clin Endocrinol Metab 2013;98(1):299–307.
   Google Scholar
• Heerwagen MJ, Stewart MS, de la Houssaye BA, Janssen RC, Friedman JE. Transgenic increase in N-3/n-6 fatty acid ratio reduces maternal obesity-associated inflammation and limits adverse developmental programming in mice. PLoS ONE 2013;8(6):e67791.
   Google Scholar
• Kim J, Carlson ME, Watkins BA. Docosahexaenoyl ethanolamide improves glucose uptake and alters endocannabinoid system gene expression in proliferating and differentiating C2C12 myoblasts. Front Physiol 2014;5:100.
   PubMed Web of Science ®Google Scholar
• Kim J, Watkins BA. Cannabinoid receptor antagonists and fatty acids alter endocannabinoid system gene expression and COX activity. J Nutr Biochem 2014;25(8):815–23.
   Google Scholar
• Watkins BA, Kim J, Kenny A, Pedersen TL, Pappan KL, Newman JW. Circulating levels of endocannabinoids and oxylipins altered by dietary lipids in older women are likely associated with previously identified gene targets. Biochim Biophys Acta 2016;1861(11):1693–704.
   Google Scholar
• Saunders EF, Reider A, Singh G, Gelenberg AJ, Rapoport SI. Low unesterified:esterified eicosapentaenoic acid (EPA) plasma concentration ratio is associated with bipolar disorder episodes, and omega-3 plasma concentrations are altered by treatment. Bipolar Disord 2015;17(7):729–42.
   Google Scholar
• Friedman AN, Kim J, Kaiser S, Pedersen TL, Newman JW, Watkins BA. Association between plasma endocannabinoids and appetite in hemodialysis patients: a pilot study. Nutr Res (New York, NY) 2016;36(7):658–62.
   Google Scholar
• Fedorova I, Salem N, Jr. Omega-3 fatty acids and rodent behavior. Prostaglandins Leukot Essent Fatty Acids 2006;75(4–5):271–89.
   PubMed Web of Science ®Google Scholar
• Moranis A, Delpech JC, De Smedt-Peyrusse V, Aubert A, Guesnet P, Lavialle M, et al. Long term adequate n-3 polyunsaturated fatty acid diet protects from depressive-like behavior but not from working memory disruption and brain cytokine expression in aged mice. Brain Behav Immun 2012;26(5):721–31.
   Google Scholar
• Liu L, Bartke N, Van Daele H, Lawrence P, Qin X, Park HG, et al. Higher efficacy of dietary DHA provided as a phospholipid than as a triglyceride for brain DHA accretion in neonatal piglets. J Lipid Res 2014;55(3):531–9.
   PubMed Web of Science ®Google Scholar
• Dyall SC, Mandhair HK, Fincham RE, Kerr DM, Roche M, Molina-Holgado F. Distinctive effects of eicosapentaenoic and docosahexaenoic acids in regulating neural stem cell fate are mediated via endocannabinoid signalling pathways. Neuropharmacology 2016;107:387–95.
   Google Scholar
• Matias I, Carta G, Murru E, Petrosino S, Banni S, Di Marzo V. Effect of polyunsaturated fatty acids on endocannabinoid and N-acyl-ethanolamine levels in mouse adipocytes. Biochim Biophys Acta 2008;1781(1–2):52–60.
   PubMed Web of Science ®Google Scholar
• Giuffrida A, Parsons LH, Kerr TM, Rodriguez de Fonseca F, Navarro M, Piomelli D. Dopamine activation of endogenous cannabinoid signaling in dorsal striatum. Nat Neurosci 1999;2(4):358–63.
   PubMed Web of Science ®Google Scholar
• Sugiura T, Waku K. 2-Arachidonoylglycerol and the cannabinoid receptors. Chem Phys Lipids 2000;108(1-2):89–106.
   PubMed Web of Science ®Google Scholar
• Burr GO, Burr MM. Nutrition classics from The journal of biological chemistry 82:345–67, 1929. A new deficiency disease produced by the rigid exclusion of fat from the diet. Nutr Rev 1973;31(8):248–9.
   PubMedGoogle Scholar
• Hansen AE, Burr GO. Essential fatty acids and human nutrition. J Am Med Assoc 1946;132(14):855–9.
   Google Scholar
• Janssen CI, Kiliaan AJ. Long-chain polyunsaturated fatty acids (LCPUFA) from genesis to senescence: the influence of LCPUFA on neural development, aging, and neurodegeneration. Prog Lipid Res 2014;53:1–17.
   PubMed Web of Science ®Google Scholar
• Haast RA, Kiliaan AJ. Impact of fatty acids on brain circulation, structure and function. Prostaglandins Leukot Essent Fatty Acids 2015;92:3–14.
   PubMed Web of Science ®Google Scholar
• Poulose SM, Miller MG, Shukitt-Hale B. Role of walnuts in maintaining brain health with age. J Nutr 2014;144(4 Suppl):561S–6S.
   Google Scholar
• Zhu X, Smith MA, Honda K, Aliev G, Moreira PI, Nunomura A, et al. Vascular oxidative stress in Alzheimer disease. J Neurol Sci 2007;257(1–2):240–6.
   Google Scholar
• Denis I, Potier B, Heberden C, Vancassel S. Omega-3 polyunsaturated fatty acids and brain aging. Curr Opin Clin Nutr Metab Care 2015;18(2):139–46.
   Google Scholar
• 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(1):76–84.
   PubMed Web of Science ®Google Scholar
• Chouinard-Watkins R, Plourde M. Fatty acid metabolism in carriers of apolipoprotein E epsilon 4 allele: is it contributing to higher risk of cognitive decline and coronary heart disease? Nutrients 2014;6(10):4452–71.
   PubMed Web of Science ®Google Scholar
• Salem N, Jr., Vandal M, Calon F. The benefit of docosahexaenoic acid for the adult brain in aging and dementia. Prostaglandins Leukot Essent Fatty Acids 2015;92:15–22.
   Google Scholar
• Nagasawa M, Hara T, Kashino A, Akasaka Y, Ide T, Murakami K. Identification of a functional peroxisome proliferator-activated receptor (PPAR) response element (PPRE) in the human apolipoprotein A-IV gene. Biochem Pharmacol 2009;78(5):523–30.
   Google Scholar
• Xue B, Yang Z, Wang X, Shi H. Omega-3 polyunsaturated fatty acids antagonize macrophage inflammation via activation of AMPK/SIRT1 pathway. PLoS ONE 2012;7(10):e45990.
   Google Scholar
• Bernardo A, Minghetti L. PPAR-gamma agonists as regulators of microglial activation and brain inflammation. Curr Pharm Des 2006;12(1):93–109.
   Google Scholar
• Heneka MT, Landreth GE. PPARs in the brain. Biochim Biophys Acta 2007;1771(8):1031–45.
   PubMed Web of Science ®Google Scholar
• Culman J, Zhao Y, Gohlke P, Herdegen T. PPAR-gamma: therapeutic target for ischemic stroke. Trends Pharmacol Sci 2007;28(5):244–9.
   PubMed Web of Science ®Google Scholar
• Wall R, Ross RP, Fitzgerald GF, Stanton C. Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids. Nutr Rev 2010;68(5):280–9.
   PubMed Web of Science ®Google Scholar
• 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.
   Google Scholar
• Marcheselli VL, Hong S, Lukiw WJ, Tian XH, Gronert K, Musto A, et al. Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and pro-inflammatory gene expression. J Biol Chem 2003;278(44):43807–17.
   PubMed Web of Science ®Google Scholar
• Tanaka K, Farooqui AA, Siddiqi NJ, Alhomida AS, Ong WY. Effects of docosahexaenoic acid on neurotransmission. Biomol Ther 2012;20(2):152–7.
   Google Scholar
• Afshordel S, Hagl S, Werner D, Rohner N, Kogel D, Bazan NG, et al. Omega-3 polyunsaturated fatty acids improve mitochondrial dysfunction in brain aging – impact of Bcl-2 and NPD-1 like metabolites. Prostaglandins Leukot Essent Fatty Acids 2015;92:23–31.
   PubMedGoogle Scholar
• Cutuli D, De Bartolo P, Caporali P, Laricchiuta D, Foti F, Ronci M, et al. n-3 polyunsaturated fatty acids supplementation enhances hippocampal functionality in aged mice. Front Aging Neurosci 2014;6:398.
   Google Scholar
• Kaplan RJ, Greenwood CE. Dietary saturated fatty acids and brain function. Neurochem Res 1998;23(5):615–26.
   Google Scholar
• Hashimotodani Y, Ohno-Shosaku T, Kano M. Endocannabinoids and synaptic function in the CNS. Neuroscientist 2007;13(2):127–37.
   Google Scholar
• Ohno-Shosaku T, Maejima T, Kano M. Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 2001;29(3):729–38.
   PubMed Web of Science ®Google Scholar
• Galve-Roperh I, Chiurchiu V, Diaz-Alonso J, Bari M, Guzman M, Maccarrone M. Cannabinoid receptor signaling in progenitor/stem cell proliferation and differentiation. Prog Lipid Res 2013;52(4):633–50.
   PubMed Web of Science ®Google Scholar
• Blankman JL, Cravatt BF. Chemical probes of endocannabinoid metabolism. Pharmacol Rev 2013;65(2):849–71.
   Google Scholar
• De Petrocellis L, Orlando P, Moriello AS, Aviello G, Stott C, Izzo AA, et al. Cannabinoid actions at TRPV channels: effects on TRPV3 and TRPV4 and their potential relevance to gastrointestinal inflammation. Acta Physiol (Oxf) 2012;204(2):255–66.
   PubMed Web of Science ®Google Scholar
• Caterina MJ. TRP channel cannabinoid receptors in skin sensation, homeostasis, and inflammation. ACS Chem Neurosci 2014;5(11):1107–16.
   PubMed Web of Science ®Google Scholar
• Deutsch DG, Glaser ST, Howell JM, Kunz JS, Puffenbarger RA, Hillard CJ, et al. The cellular uptake of anandamide is coupled to its breakdown by fatty-acid amide hydrolase. J Biol Chem 2001;276(10):6967–73.
   Google Scholar
• Day TA, Rakhshan F, Deutsch DG, Barker EL. Role of fatty acid amide hydrolase in the transport of the endogenous cannabinoid anandamide. Mol Pharmacol 2001;59(6):1369–75.
   PubMed Web of Science ®Google Scholar
• Fowler CJ, Jonsson KO, Tiger G. Fatty acid amide hydrolase: biochemistry, pharmacology, and therapeutic possibilities for an enzyme hydrolyzing anandamide, 2-arachidonoylglycerol, palmitoylethanolamide, and oleamide. Biochem Pharmacol 2001;62(5):517–26.
   Google Scholar
• Bisogno T, Hanus L, De Petrocellis L, Tchilibon S, Ponde DE, Brandi I, et al. Molecular targets for cannabidiol and its synthetic analogues: effect on vanilloid VR1 receptors and on the cellular uptake and enzymatic hydrolysis of anandamide. Br J Pharmacol 2001;134(4):845–52.
   PubMed Web of Science ®Google Scholar
• Pascual AC, Gaveglio VL, Giusto NM, Pasquare SJ. Cannabinoid receptor-dependent metabolism of 2-arachidonoylglycerol during aging. Exp Gerontol 2014;55:134–42.
   Google Scholar
• Long JZ, Li W, Booker L, Burston JJ, Kinsey SG, Schlosburg JE, et al. Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects. Nat Chem Biol 2009;5(1):37–44.
   PubMed Web of Science ®Google Scholar
• Kohnz RA, Nomura DK. Chemical approaches to therapeutically target the metabolism and signaling of the endocannabinoid 2-AG and eicosanoids. Chem Soc Rev 2014;43(19):6859–69.
   Google Scholar
• Ahn K, Johnson DS, Cravatt BF. Fatty acid amide hydrolase as a potential therapeutic target for the treatment of pain and CNS disorders. Exp Opin Drug Discov 2009;4(7):763–84.
   PubMed Web of Science ®Google Scholar
• Kerbrat A, Ferre JC, Fillatre P, Ronziere T, Vannier S, Carsin-Nicol B, et al. Acute neurologic disorder from an inhibitor of fatty acid amide hydrolase. N Engl J Med 2016;375(18):1717–25.
   PubMed Web of Science ®Google Scholar
• Fernandez-Ruiz J, Romero J, Velasco G, Tolon RM, Ramos JA, Guzman M. Cannabinoid CB2 receptor: a new target for controlling neural cell survival? Trends Pharmacol Sci 2007;28(1):39–45.
   Google Scholar
• Fernandez-Ruiz J, Moro MA, Martinez-Orgado J. Cannabinoids in neurodegenerative disorders and stroke/brain trauma: from preclinical models to clinical applications. Neurotherapeutics 2015;12(4):793–806.
   PubMed Web of Science ®Google Scholar
• Di Iorio G, Lupi M, Sarchione F, Matarazzo I, Santacroce R, Petruccelli F, et al. The endocannabinoid system: a putative role in neurodegenerative diseases. Int J High Risk Behav Addict 2013;2(3):100–6.
   PubMedGoogle Scholar
• Fernandez-Ruiz J, Romero J, Ramos JA. Endocannabinoids and neurodegenerative disorders: Parkinson’s disease, huntington’s chorea, Alzheimer’s disease, and others. Handb Exp Pharmacol 2015;231:233–59.
   Google Scholar
• Ramirez BG, Blazquez C, Gomez del Pulgar T, Guzman M, de Ceballos ML. Prevention of Alzheimer’s disease pathology by cannabinoids: neuroprotection mediated by blockade of microglial activation. J Neurosci 2005;25(8):1904–13.
   PubMed Web of Science ®Google Scholar
• Janssen B, Vugts DJ, Funke U, Molenaar GT, Kruijer PS, van Berckel BN, et al. Imaging of neuroinflammation in Alzheimer’s disease, multiple sclerosis and stroke: recent developments in positron emission tomography. Biochim Biophys Acta 2016;1862(3):425–41.
   Web of Science ®Google Scholar
• Aso E, Ferrer I. Cannabinoids for treatment of Alzheimer’s disease: moving toward the clinic. Front Pharmacol 2014;5:37.
   PubMed Web of Science ®Google Scholar
• Lastres-Becker I, Molina-Holgado F, Ramos JA, Mechoulam R, Fernandez-Ruiz J. Cannabinoids provide neuroprotection against 6-hydroxydopamine toxicity in vivo and in vitro: relevance to Parkinson’s disease. Neurobiol Dis 2005;19(1–2):96–107.
   Google Scholar
• Garcia-Arencibia M, Gonzalez S, de Lago E, Ramos JA, Mechoulam R, Fernandez-Ruiz J. Evaluation of the neuroprotective effect of cannabinoids in a rat model of Parkinson’s disease: importance of antioxidant and cannabinoid receptor-independent properties. Brain Res 2007;1134(1):162–70.
   PubMed Web of Science ®Google Scholar
• More SV, Choi DK. Promising cannabinoid-based therapies for Parkinson’s disease: motor symptoms to neuroprotection. Mol Neurodegener 2015;10:17.
   PubMed Web of Science ®Google Scholar
• Palazuelos J, Aguado T, Pazos MR, Julien B, Carrasco C, Resel E, et al. Microglial CB2 cannabinoid receptors are neuroprotective in Huntington’s disease excitotoxicity. Brain 2009;132(Pt 11):3152–64.
   Google Scholar
• Kumar P, Kalonia H, Kumar A. Huntington’s disease: pathogenesis to animal models. Pharmacol Rep 2010;62(1):1–14.
   PubMed Web of Science ®Google Scholar
• Pryce G, Ahmed Z, Hankey DJ, Jackson SJ, Croxford JL, Pocock JM, et al. Cannabinoids inhibit neurodegeneration in models of multiple sclerosis. Brain 2003;126(Pt 10):2191–202.
   PubMed Web of Science ®Google Scholar
• de Lago E, Moreno-Martet M, Cabranes A, Ramos JA, Fernandez-Ruiz J. Cannabinoids ameliorate disease progression in a model of multiple sclerosis in mice, acting preferentially through CB1 receptor-mediated anti-inflammatory effects. Neuropharmacology 2012;62(7):2299–308.
   Google Scholar
• Pryce G, Baker D. Endocannabinoids in multiple sclerosis and amyotrophic lateral sclerosis. Handb Exp Pharmacol 2015;231:213–31.
   Google Scholar
• Bilsland LG, Greensmith L. The endocannabinoid system in amyotrophic lateral sclerosis. Curr Pharmaceut Des 2008;14(23):2306–16.
   Google Scholar
• Ludanyi A, Eross L, Czirjak S, Vajda J, Halasz P, Watanabe M, et al. Downregulation of the CB1 cannabinoid receptor and related molecular elements of the endocannabinoid system in epileptic human hippocampus. J Neurosci 2008;28(12):2976–90.
   PubMed Web of Science ®Google Scholar
• Rubino T, Zamberletti E, Parolaro D. Endocannabinoids and mental disorders. Handb Exp Pharmacol 2015;231:261–83.
   Google Scholar
• Chakrabarti B, Persico A, Battista N, Maccarrone M. Endocannabinoid signaling in autism. Neurotherapeutics 2015;12(4):837–47.
   PubMed Web of Science ®Google Scholar
• Fattore L. Synthetic cannabinoids-further evidence supporting the relationship between cannabinoids and psychosis. Biol Psychiatry 2016;79(7):539–48.
   PubMed Web of Science ®Google Scholar
• Campos AC, Fogaca MV, Sonego AB, Guimaraes FS. Cannabidiol, neuroprotection and neuropsychiatric disorders. Pharmacol Res 2016.
   Web of Science ®Google Scholar
• Yarnell S. The use of medicinal Marijuana for posttraumatic stress disorder: a review of the current literature. Primary Care Compan CNS Disord 2015;17(3). doi: 10.4088/PCC.15r01786.
   Google Scholar
• Zlebnik NE, Cheer JF. Beyond the CB1 receptor: is cannabidiol the answer for disorders of motivation? Annu Rev Neurosci 2016;39:1–17. doi: 10.1146/annurev-neuro-070815-014038.
   Google Scholar
• Ashton CH, Moore PB, Gallagher P, Young AH. Cannabinoids in bipolar affective disorder: a review and discussion of their therapeutic potential. J Psychopharmacol 2005;19(3):293–300.
   PubMed Web of Science ®Google Scholar
• Sherif M, Radhakrishnan R, D’Souza DC, Ranganathan M. Human laboratory studies on cannabinoids and psychosis. Biol Psychiatry 2016;79(7):526–38.
   PubMed Web of Science ®Google Scholar
• D’Souza DC. Cannabinoids and psychosis. Int Rev Neurobiol 2007;78:289–326.
   PubMedGoogle Scholar
• Chadwick B, Miller ML, Hurd YL. Cannabis Use during adolescent development: susceptibility to psychiatric illness. Front Psychiatry 2013;4:129.
   PubMedGoogle Scholar
• Bossong MG, Niesink RJ. Adolescent brain maturation, the endogenous cannabinoid system and the neurobiology of cannabis-induced schizophrenia. Prog Neurobiol 2010;92(3):370–85.
   Google Scholar
• Higuera-Matas A, Ucha M, Ambrosio E. Long-term consequences of perinatal and adolescent cannabinoid exposure on neural and psychological processes. Neurosci Biobehav Rev 2015;55:119–46.
   PubMed Web of Science ®Google Scholar
• Lutz B, Marsicano G, Maldonado R, Hillard CJ. The endocannabinoid system in guarding against fear, anxiety and stress. Nat Rev Neurosci 2015;16(12):705–18.
   Web of Science ®Google Scholar
• Broyd SJ, van Hell HH, Beale C, Yucel M, Solowij N. Acute and chronic effects of cannabinoids on human cognition – a systematic review. Biol Psychiatry 2016;79(7):557–67.
   PubMed Web of Science ®Google Scholar
• Zuardi AW, Crippa JA, Hallak JE, Moreira FA, Guimaraes FS. Cannabidiol, a cannabis sativa constituent, as an antipsychotic drug. Braz J Med Biol Res 2006;39(4):421–9.
   PubMed Web of Science ®Google Scholar
• Kogan NM, Mechoulam R. Cannabinoids in health and disease. Dialog Clin Neurosci 2007;9(4):413–30.
   PubMedGoogle Scholar
• Chen R, Zhang J, Fan N, Teng ZQ, Wu Y, Yang H, et al. Delta9-THC-caused synaptic and memory impairments are mediated through COX-2 signaling. Cell 2013;155(5):1154–65.
   Google Scholar
• Iannotti FA, Di Marzo V, Petrosino S. Endocannabinoids and endocannabinoid-related mediators: targets, metabolism and role in neurological disorders. Prog Lipid Res 2016;62:107–28.
   PubMed Web of Science ®Google Scholar
• Nagarkatti P, Pandey R, Rieder SA, Hegde VL, Nagarkatti M. Cannabinoids as novel anti-inflammatory drugs. Future Med Chem 2009;1(7):1333–49.
   PubMed Web of Science ®Google Scholar
• Turcotte C, Chouinard F, Lefebvre JS, Flamand N. Regulation of inflammation by cannabinoids, the endocannabinoids 2-arachidonoyl-glycerol and arachidonoyl-ethanolamide, and their metabolites. J Leukocyte Biol 2015;97(6):1049–70.
   Google Scholar
• Katchan V, David P, Shoenfeld Y. Cannabinoids and autoimmune diseases: a systematic review. Autoimmun Rev 2016;15(6):513–28.
   PubMed Web of Science ®Google Scholar
• Rieder SA, Chauhan A, Singh U, Nagarkatti M, Nagarkatti P. Cannabinoid-induced apoptosis in immune cells as a pathway to immunosuppression. Immunobiology 2010;215(8):598–605.
   PubMed Web of Science ®Google Scholar
• Sanchez-Blazquez P, Rodriguez-Munoz M, Garzon J. The cannabinoid receptor 1 associates with NMDA receptors to produce glutamatergic hypofunction: implications in psychosis and schizophrenia. Front Pharmacol 2014;4:169.
   PubMed Web of Science ®Google Scholar
• Snider NT, Walker VJ, Hollenberg PF. Oxidation of the endogenous cannabinoid arachidonoyl ethanolamide by the cytochrome P450 monooxygenases: physiological and pharmacological implications. Pharmacol Rev 2010;62(1):136–54.
   Google Scholar
• Schlosburg JE, Kinsey SG, Lichtman AH. Targeting fatty acid amide hydrolase (FAAH) to treat pain and inflammation. AAPS J 2009;11(1):39–44.
   Google Scholar
• Piomelli D. More surprises lying ahead. The endocannabinoids keep us guessing. Neuropharmacology 2014;76(Pt B):228–34.
   PubMedGoogle Scholar
• Palomo T, Kostrzewa RM, Beninger RJ, Archer T. Genetic variation and shared biological susceptibility underlying comorbidity in neuropsychiatry. Neurotox Res 2007;12(1):29–42.
   Google Scholar
• Skaper SD, Di Marzo V. Endocannabinoids in nervous system health and disease: the big picture in a nutshell. Philos Trans R Soc London Ser B Biol Sci 2012;367(1607):3193–200.
   Google Scholar
• Cabral GA, Marciano-Cabral F. Cannabinoid receptors in microglia of the central nervous system: immune functional relevance. J Leukocyte Biol 2005;78(6):1192–7.
   PubMed Web of Science ®Google Scholar
• Cabral GA, Raborn ES, Griffin L, Dennis J, Marciano-Cabral F. CB2 receptors in the brain: role in central immune function. Br J Pharmacol 2008;153(2):240–51.
   PubMed Web of Science ®Google Scholar
• Lisboa SF, Gomes FV, Guimaraes FS, Campos AC. Microglial cells as a link between cannabinoids and the immune hypothesis of psychiatric disorders. Front Neurol 2016;7:63.
   Google Scholar
• Hu X, Liou AK, Leak RK, Xu M, An C, Suenaga J, et al. Neurobiology of microglial action in CNS injuries: receptor-mediated signaling mechanisms and functional roles. Prog Neurobiol 2014;119–120:60–84.
   PubMed Web of Science ®Google Scholar
• Wu Y, Dissing-Olesen L, MacVicar BA, Stevens B. Microglia: dynamic mediators of synapse development and plasticity. Trends Immunol 2015;36(10):605–13.
   PubMed Web of Science ®Google Scholar
• Pisanti S, Bifulco M. Endocannabinoid system modulation in cancer biology and therapy. Pharmacol Res 2009;60(2):107–16.
   Google Scholar
• Atwood BK, Wager-Miller J, Haskins C, Straiker A, Mackie K. Functional selectivity in CB(2) cannabinoid receptor signaling and regulation: implications for the therapeutic potential of CB(2) ligands. Mol Pharmacol 2012;81(2):250–63.
   PubMed Web of Science ®Google Scholar
• Deng L, Guindon J, Cornett BL, Makriyannis A, Mackie K, Hohmann AG. Chronic cannabinoid receptor 2 activation reverses paclitaxel neuropathy without tolerance or cannabinoid receptor 1-dependent withdrawal. Biol Psychiatry 2015;77(5):475–87.
   PubMed Web of Science ®Google Scholar
• Ternianov A, Perez-Ortiz JM, Solesio ME, Garcia-Gutierrez MS, Ortega-Alvaro A, Navarrete F, et al. Overexpression of CB2 cannabinoid receptors results in neuroprotection against behavioral and neurochemical alterations induced by intracaudate administration of 6-hydroxydopamine. Neurobiol Aging. 2012;33(2):421 e1–16.
   Google Scholar
• Garcia-Gutierrez MS, Manzanares J. Overexpression of CB2 cannabinoid receptors decreased vulnerability to anxiety and impaired anxiolytic action of alprazolam in mice. J Psychopharmacol 2011;25(1):111–20.
   Google Scholar
• Di Marzo V, De Petrocellis L. Endocannabinoids as regulators of transient receptor potential (TRP) channels: a further opportunity to develop new endocannabinoid-based therapeutic drugs. Curr Med Chem 2010;17(14):1430–49.
   PubMed Web of Science ®Google Scholar
• Ferreira LG, Faria RX. TRPing on the pore phenomenon: what do we know about transient receptor potential ion channel-related pore dilation up to now? J Bioenergy Biomembr 2016;48(1):1–12.
   PubMed Web of Science ®Google Scholar
• Lu HC, Mackie K. An introduction to the endogenous cannabinoid system. Biol Psychiatry 2016;79(7):516–25.
   PubMed Web of Science ®Google Scholar
• Haugh O, Penman J, Irving AJ, Campbell VA. The emerging role of the cannabinoid receptor family in peripheral and neuro-immune interactions. Curr Drug Targets 2016;17(16):1834–40.
   Google Scholar
• Chiarlone A, Bellocchio L, Blazquez C, Resel E, Soria-Gomez E, Cannich A, et al. A restricted population of CB1 cannabinoid receptors with neuroprotective activity. Proc Natl Acad Sci USA 2014;111(22):8257–62.
   PubMed Web of Science ®Google Scholar
• Opendak M, Gould E. Adult neurogenesis: a substrate for experience-dependent change. Trends Cognit Sci 2015;19(3):151–61.
   Google Scholar
• Prenderville JA, Kelly AM, Downer EJ. The role of cannabinoids in adult neurogenesis. Br J Pharmacol 2015;172(16):3950–63.
   PubMed Web of Science ®Google Scholar
• Xapelli S, Agasse F, Grade S, Bernardino L, Ribeiro FF, Schitine CS, et al. Modulation of subventricular zone oligodendrogenesis: a role for hemopressin? Front Cell Neurosci 2014;8:59.
   Google Scholar
• Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, et al. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 2008;11(10):1153–61.
   PubMed Web of Science ®Google Scholar
• Diaz-Alonso J, Aguado T, de Salas-Quiroga A, Ortega Z, Guzman M, Galve-Roperh I. CB1 cannabinoid receptor-dependent activation of mTORC1/Pax6 signaling drives Tbr2 expression and basal progenitor expansion in the developing mouse cortex. Cerebral Cortex 2015;25(9):2395–408.
   Google Scholar
• Jin K, Xie L, Kim SH, Parmentier-Batteur S, Sun Y, Mao XO, et al. Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol Pharmacol 2004;66(2):204–8.
   Google Scholar
• Molina-Holgado F, Rubio-Araiz A, Garcia-Ovejero D, Williams RJ, Moore JD, Arevalo-Martin A, et al. CB2 cannabinoid receptors promote mouse neural stem cell proliferation. Eur J Neurosci 2007;25(3):629–34.
   Google Scholar
• Gomez M, Hernandez M, Fernandez-Ruiz J. Cannabinoid signaling system: does it play a function in cell proliferation and migration, neuritic elongation and guidance and synaptogenesis during brain ontogenesis? Cell Adhes Migrat 2008;2(4):246–8.
   PubMed Web of Science ®Google Scholar
• Compagnucci C, Di Siena S, Bustamante MB, Di Giacomo D, Di Tommaso M, Maccarrone M, et al. Type-1 (CB1) cannabinoid receptor promotes neuronal differentiation and maturation of neural stem cells. PLoS ONE 2013;8(1):e54271.
   Google Scholar
• Kim HY, Spector AA. Synaptamide, endocannabinoid-like derivative of docosahexaenoic acid with cannabinoid-independent function. Prostaglandins Leukot Essent Fatty Acids 2013;88(1):121–5.
   Google Scholar
• Kim HY, Spector AA, Xiong ZM. A synaptogenic amide N-docosahexaenoylethanolamide promotes hippocampal development. Prostaglandins Lipid Mediat 2011;96(1–4):114–20.
   Google Scholar
• Rashid MA, Katakura M, Kharebava G, Kevala K, Kim HY. N-docosahexaenoylethanolamine is a potent neurogenic factor for neural stem cell differentiation. J Neurochem 2013;125(6):869–84.
   Google Scholar
• Meijerink J, Balvers M, Witkamp R. N-Acyl amines of docosahexaenoic acid and other n-3 polyunsatured fatty acids - from fishy endocannabinoids to potential leads. Br J Pharmacol 2013;169(4):772–83.
   Google Scholar
• Osei-Hyiaman D, DePetrillo M, Pacher P, Liu J, Radaeva S, Batkai S, et al. Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. J Clin Invest 2005;115(5):1298–305.
   PubMed Web of Science ®Google Scholar
• Cavuoto P, McAinch AJ, Hatzinikolas G, Janovska A, Game P, Wittert GA. The expression of receptors for endocannabinoids in human and rodent skeletal muscle. Biochem Biophys Res Commun 2007;364(1):105–10.
   PubMed Web of Science ®Google Scholar
• You T, Disanzo BL, Wang X, Yang R, Gong D. Adipose tissue endocannabinoid system gene expression: depot differences and effects of diet and exercise. Lipids Health Dis 2011;10:194.
   PubMed Web of Science ®Google Scholar
• Krott LM, Piscitelli F, Heine M, Borrino S, Scheja L, Silvestri C, et al. Endocannabinoid regulation in white and brown adipose tissue following thermogenic activation. J Lipid Res 2016;57(3):464–73.
   Google Scholar
• Boon MR, Kooijman S, van Dam AD, Pelgrom LR, Berbee JF, Visseren CA, et al. Peripheral cannabinoid 1 receptor blockade activates brown adipose tissue and diminishes dyslipidemia and obesity. FASEB J 2014;28(12):5361–75.
   Google Scholar
• Iannotti FA, Silvestri C, Mazzarella E, Martella A, Calvigioni D, Piscitelli F, et al. The endocannabinoid 2-AG controls skeletal muscle cell differentiation via CB1 receptor-dependent inhibition of Kv7 channels. Proc Natl Acad Sci USA 2014;111(24):E2472–81.
   Google Scholar
• Richard D, Guesdon B, Timofeeva E. The brain endocannabinoid system in the regulation of energy balance. Best Pract Res Clin Endocrinol Metabol 2009;23(1):17–32.
   PubMed Web of Science ®Google Scholar
• Jo YH, Chen YJ, Chua SC, Jr, Talmage DA, Role LW. Integration of endocannabinoid and leptin signaling in an appetite-related neural circuit. Neuron 2005;48(6):1055–66.
   Google Scholar
• Huang H, Acuna-Goycolea C, Li Y, Cheng HM, Obrietan K, van den Pol AN. Cannabinoids excite hypothalamic melanin-concentrating hormone but inhibit hypocretin/orexin neurons: implications for cannabinoid actions on food intake and cognitive arousal. J Neurosci 2007;27(18):4870–81.
   Google Scholar
• Cristino L, Busetto G, Imperatore R, Ferrandino I, Palomba L, Silvestri C, et al. Obesity-driven synaptic remodeling affects endocannabinoid control of orexinergic neurons. Proc Natl Acad Sci USA 2013;110(24):E2229–38.
   PubMed Web of Science ®Google Scholar
• Tam J, Cinar R, Liu J, Godlewski G, Wesley D, Jourdan T, et al. Peripheral cannabinoid-1 receptor inverse agonism reduces obesity by reversing leptin resistance. Cell Metab 2012;16(2):167–79.
   PubMed Web of Science ®Google Scholar
• Messina G, Dalia C, Tafuri D, Monda V, Palmieri F, Dato A, et al. Orexin-A controls sympathetic activity and eating behavior. Front Psychol 2014;5:997.
   PubMed Web of Science ®Google Scholar
• Zhou JJ, Yuan F, Zhang Y, Li DP. Upregulation of orexin receptor in paraventricular nucleus promotes sympathetic outflow in obese Zucker rats. Neuropharmacology 2015;99:481–90.
   PubMed Web of Science ®Google Scholar
• Di Marzo V. Endocannabinoids: an appetite for fat. Proc Natl Acad Sci USA 2011;108(31):12567–8.
   Google Scholar
• Deshmukh RR, Sharma PL. Stimulation of accumbens shell cannabinoid CB(1) receptors by noladin ether, a putative endocannabinoid, modulates food intake and dietary selection in rats. Pharmacol Res 2012;66(3):276–82.
   Google Scholar
• Parker KE, McCall JG, McGuirk SR, Trivedi S, Miller DK, Will MJ. Effects of co-administration of 2-arachidonylglycerol (2-AG) and a selective micro-opioid receptor agonist into the nucleus accumbens on high-fat feeding behaviors in the rat. Brain Res 2015;1618:309–15.
   PubMed Web of Science ®Google Scholar
• DiPatrizio NV, Astarita G, Schwartz G, Li X, Piomelli D. Endocannabinoid signal in the gut controls dietary fat intake. Proc Natl Acad Sci USA 2011;108(31):12904–8.
   PubMed Web of Science ®Google Scholar
• Krashes MJ, Lowell BB, Garfield AS. Melanocortin-4 receptor-regulated energy homeostasis. Nat Neurosci 2016;19(2):206–19.
   PubMed Web of Science ®Google Scholar
• Koch M, Varela L, Kim JG, Kim JD, Hernandez-Nuno F, Simonds SE, et al. Hypothalamic POMC neurons promote cannabinoid-induced feeding. Nature 2015;519(7541):45–50.
   Google Scholar
• Ravinet Trillou C, Delgorge C, Menet C, Arnone M, Soubrie P. CB1 cannabinoid receptor knockout in mice leads to leanness, resistance to diet-induced obesity and enhanced leptin sensitivity. Int J Obes Relat Metab Disord 2004;28(4):640–8.
   PubMed Web of Science ®Google Scholar
• Kola B, Farkas I, Christ-Crain M, Wittmann G, Lolli F, Amin F, et al. The orexigenic effect of ghrelin is mediated through central activation of the endogenous cannabinoid system. PLoS ONE 2008;3(3):e1797.
   Google Scholar
• Lage R, Parisi C, Seoane-Collazo P, Ferno J, Mazza R, Bosch F, et al. Lack of hypophagia in CB1 null mice is associated to decreased hypothalamic POMC and CART expression. Int J Neuropsychopharmacol 2015;18(9). doi:10.1093/ijnp/pyv011.
   Google Scholar
• Rorato R, Miyahara C, Antunes-Rodrigues J, Elias LL. Tolerance to hypophagia induced by prolonged treatment with a CB1 antagonist is related to the reversion of anorexigenic neuropeptide gene expression in the hypothalamus. Regulat Pept 2013;182:12–8.
   Google Scholar
• Agudo J, Martin M, Roca C, Molas M, Bura AS, Zimmer A, et al. Deficiency of CB2 cannabinoid receptor in mice improves insulin sensitivity but increases food intake and obesity with age. Diabetologia 2010;53(12):2629–40.
   PubMed Web of Science ®Google Scholar
• Di Marzo V, Goparaju SK, Wang L, Liu J, Batkai S, Jarai Z, et al. Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 2001;410(6830):822–5.
   PubMed Web of Science ®Google Scholar
• Bosier B, Bellocchio L, Metna-Laurent M, Soria-Gomez E, Matias I, Hebert-Chatelain E, et al. Astroglial CB1 cannabinoid receptors regulate leptin signaling in mouse brain astrocytes. Mol Metab 2013;2(4):393–404.
   PubMed Web of Science ®Google Scholar
• Flak JN, Myers MG, Jr. Minireview: CNS mechanisms of leptin action. Mol Endocrinol (Baltimore, MD) 2016;30(1):3–12.
   PubMed Web of Science ®Google Scholar
• Malcher-Lopes R, Buzzi M. Glucocorticoid-regulated crosstalk between arachidonic acid and endocannabinoid biochemical pathways coordinates cognitive-, neuroimmune-, and energy homeostasis-related adaptations to stress. Vitamins Hormones 2009;81:263–313.
   Google Scholar
• Munzberg H, Flier JS, Bjorbaek C. Region-specific leptin resistance within the hypothalamus of diet-induced obese mice. Endocrinology 2004;145(11):4880–9.
   PubMed Web of Science ®Google Scholar
• Ahima RS. Editorial: molecular obesity research: lessons learned? Mol Endocrinol (Baltimore, MD) 2014;28(6):785–9.
   Google Scholar
• Tekeleselassie AW, Goh YM, Rajion MA, Motshakeri M, Ebrahimi M. A high-fat diet enriched with low omega-6 to omega-3 fatty acid ratio reduced fat cellularity and plasma leptin concentration in Sprague-Dawley rats. Scienti World J 2013;2013:757593.
   Google Scholar
• Haslam DW, James WP. Obesity. Lancet 2005;366(9492):1197–209.
   PubMed Web of Science ®Google Scholar
• Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA 2014;311(8):806–14.
   PubMed Web of Science ®Google Scholar
• Flegal KM, Kit BK, Orpana H, Graubard BI. Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and meta-analysis. JAMA 2013;309(1):71–82.
   PubMed Web of Science ®Google Scholar
• Heppenstall C, Bunce S, Smith JC. Relationships between glucose, energy intake and dietary composition in obese adults with type 2 diabetes receiving the cannabinoid 1 (CB1) receptor antagonist, rimonabant. Nutr J 2012;11:1210.
   Google Scholar
• Pi-Sunyer FX, Aronne LJ, Heshmati HM, Devin J, Rosenstock J. Effect of rimonabant, a cannabinoid-1 receptor blocker, on weight and cardiometabolic risk factors in overweight or obese patients: RIO-North America: a randomized controlled trial. JAMA 2006;295(7):761–75.
   PubMed Web of Science ®Google Scholar
• Burch J, McKenna C, Palmer S, Norman G, Glanville J, Sculpher M, et al. Rimonabant for the treatment of overweight and obese people. Health Technol Assess 2009;13(Suppl 3):13–22.
   Google Scholar
• Jbilo O, Ravinet-Trillou C, Arnone M, Buisson I, Bribes E, Peleraux A, et al. The CB1 receptor antagonist rimonabant reverses the diet-induced obesity phenotype through the regulation of lipolysis and energy balance. FASEB J 2005;19(11):1567–9.
   PubMed Web of Science ®Google Scholar
• Nogueiras R, Veyrat-Durebex C, Suchanek PM, Klein M, Tschop J, Caldwell C, et al. Peripheral, but not central, CB1 antagonism provides food intake-independent metabolic benefits in diet-induced obese rats. Diabetes 2008;57(11):2977–91.
   PubMed Web of Science ®Google Scholar
• Quarta C, Bellocchio L, Mancini G, Mazza R, Cervino C, Braulke LJ, et al. CB(1) signaling in forebrain and sympathetic neurons is a key determinant of endocannabinoid actions on energy balance. Cell Metab 2010;11(4):273–85.
   PubMed Web of Science ®Google Scholar
• Cota D, Marsicano G, Tschop M, Grubler Y, Flachskamm C, Schubert M, et al. The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J Clin Invest 2003;112(3):423–31.
   PubMed Web of Science ®Google Scholar
• Iannotti FA, Piscitelli F, Martella A, Mazzarella E, Allara M, Palmieri V, et al. Analysis of the ‘endocannabinoidome’ in peripheral tissues of obese Zucker rats. Prostaglandins Leukot Essent Fatty Acids 2013;89(2–3):127–35.
   Google Scholar
• Pagano C, Pilon C, Calcagno A, Urbanet R, Rossato M, Milan G, et al. The endogenous cannabinoid system stimulates glucose uptake in human fat cells via phosphatidylinositol 3-kinase and calcium-dependent mechanisms. J Clin Endocrinol Metab 2007;92(12):4810–9.
   PubMed Web of Science ®Google Scholar
• Matias I, Bisogno T, Di Marzo V. Endogenous cannabinoids in the brain and peripheral tissues: regulation of their levels and control of food intake. Int J Obes (Lond) 2006;30(Suppl 1):S7–12.
   PubMedGoogle Scholar
• Di Marzo V. CB(1) receptor antagonism: biological basis for metabolic effects. Drug Discov Today 2008;13(23-24):1026–41.
   Google Scholar
• Karvela A, Rojas-Gil AP, Samkinidou E, Papadaki H, Pappa A, Georgiou G, et al. Endocannabinoid (EC) receptor, CB1, and EC enzymes’ expression in primary adipocyte cultures of lean and obese pre-pubertal children in relation to adiponectin and insulin. J Pediatr Endocrinol Metab 2010;23(10):1011–24.
   Google Scholar
• Deveaux V, Cadoudal T, Ichigotani Y, Teixeira-Clerc F, Louvet A, Manin S, et al. Cannabinoid CB2 receptor potentiates obesity-associated inflammation, insulin resistance and hepatic steatosis. PLoS ONE 2009;4(6):e5844.
   PubMedGoogle Scholar
• Labbe SM, Caron A, Lanfray D, Monge-Rofarello B, Bartness TJ, Richard D. Hypothalamic control of brown adipose tissue thermogenesis. Front Syst Neurosci 2015;9:175.
   Google Scholar
• Verty AN, Evetts MJ, Crouch GJ, McGregor IS, Stefanidis A, Oldfield BJ. The cannabinoid receptor agonist THC attenuates weight loss in a rodent model of activity-based anorexia. Neuropsychopharmacology 2011;36(7):1349–58.
   Google Scholar
• Verty AN, Allen AM, Oldfield BJ. The effects of rimonabant on brown adipose tissue in rat: implications for energy expenditure. Obesity (Silver Spring, Md) 2009;17(2):254–61.
   Google Scholar
• Bajzer M, Olivieri M, Haas MK, Pfluger PT, Magrisso IJ, Foster MT, et al. Cannabinoid receptor 1 (CB1) antagonism enhances glucose utilisation and activates brown adipose tissue in diet-induced obese mice. Diabetologia. 2011;54(12):3121–31.
   Google Scholar
• Matias I, Petrosino S, Racioppi A, Capasso R, Izzo AA, Di Marzo V. Dysregulation of peripheral endocannabinoid levels in hyperglycemia and obesity: effect of high fat diets. Mol Cell Endocrinol 2008;286(1–2 Suppl 1):S66–78.
   PubMed Web of Science ®Google Scholar
• Dodd GT, Mancini G, Lutz B, Luckman SM. The peptide hemopressin acts through CB1 cannabinoid receptors to reduce food intake in rats and mice. J Neurosci 2010;30(21):7369–76.
   Google Scholar
• Dodd GT, Worth AA, Hodkinson DJ, Srivastava RK, Lutz B, Williams SR, et al. Central functional response to the novel peptide cannabinoid, hemopressin. Neuropharmacology 2013;71:27–36.
   Google Scholar
• Vickers SP, Webster LJ, Wyatt A, Dourish CT, Kennett GA. Preferential effects of the cannabinoid CB1 receptor antagonist, SR 141716, on food intake and body weight gain of obese (fa/fa) compared to lean Zucker rats. Psychopharmacology 2003;167(1):103–11.
   Google Scholar
• Hildebrandt AL, Kelly-Sullivan DM, Black SC. Antiobesity effects of chronic cannabinoid CB1 receptor antagonist treatment in diet-induced obese mice. Eur J Pharmacol 2003;462(1–3):125–32.
   Google Scholar
• Bensaid M, Gary-Bobo M, Esclangon A, Maffrand JP, Le Fur G, Oury-Donat F, et al. The cannabinoid CB1 receptor antagonist SR141716 increases Acrp30 mRNA expression in adipose tissue of obese fa/fa rats and in cultured adipocyte cells. Mol Pharmacol 2003;63(4):908–14.
   PubMed Web of Science ®Google Scholar
• Banni S, Di Marzo V. Effect of dietary fat on endocannabinoids and related mediators: consequences on energy homeostasis, inflammation and mood. Mol Nutr Food Res 2010;54(1):82–92.
   PubMed Web of Science ®Google Scholar
• Kelly OJ, Gilman JC, Kim Y, Ilich JZ. Long-chain polyunsaturated fatty acids may mutually benefit both obesity and osteoporosis. Nutr Res (New York, NY) 2013;33(7):521–33.
   Google Scholar
• Bergstrom S, Samuelsson B. Prostaglandins. Annu Rev Biochem 1965;34:101–8.
   PubMed Web of Science ®Google Scholar
• Anggard E, Samuelsson B. Biosynthesis of prostaglandins from arachidonic acid in Guinea Pig lung. Prostaglandins and related factors 38. J Biol Chem 1965;240(9):3518–21.
   PubMed Web of Science ®Google Scholar
• Vane JR. Inhibition of prostaglandin synthesis as a mechanism of action of aspirin-like drugs. Nat New Biol 1971;231:232–5.
   PubMedGoogle Scholar
• Moncada S, Ferreira SH, Vane JR. Inhibition of prostaglandin biosynthesis as the mechanism of analgesia of aspirin-like drugs in the dog knee joint. Eur J Pharmacol 1975;31(2):250–60.
   Google Scholar
• Flower RJ, Blackwell GJ. Anti-inflammatory steroids induce biosynthesis of a phospholipase A2 inhibitor which prevents prostaglandin generation. Nature 1979;278(5703):456–9.
   Google Scholar
• Henderson WR. The role of leukotrienes in inflammation. Ann Intern Med 1994;121(9):684–97.
   PubMed Web of Science ®Google Scholar
• Peters-Golden M, Henderson WR, Jr. Leukotrienes. New Engl J Med 2007;357(18):1841–54.
   PubMed Web of Science ®Google Scholar
• Simmons DL, Botting RM, Hla T. Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev 2004;56(3):387–437.
   PubMed Web of Science ®Google Scholar
• Murakami M, Kudo I. Recent advances in molecular biology and physiology of the prostaglandin E2-biosynthetic pathway. Prog Lipid Res 2004;43(1):3–35.
   Google Scholar
• Yui K, Imataka G, Nakamura H, Ohara N, Naito Y. Eicosanoids derived from arachidonic acid and their family prostaglandins and cyclooxygenase in psychiatric disorders. Curr Neuropharmacol 2015;13(6):776–85.
   PubMed Web of Science ®Google Scholar
• Yagami T, Koma H, Yamamoto Y. Pathophysiological roles of cyclooxygenases and prostaglandins in the central nervous system. Mol Neurobiol 2016;53(7):4754–71.
   PubMed Web of Science ®Google Scholar
• Serhan CN, Yacoubian S, Yang R. Anti-Inflammatory and proresolving lipid mediators. Annu Rev Pathol: Mechan Dis 2008;3(1):279–312.
   PubMedGoogle Scholar
• Sandig H, Pease JE, Sabroe I. Contrary prostaglandins: the opposing roles of PGD2 and its metabolites in leukocyte function. J Leukoc Biol 2007;81(2):372–82.
   Google Scholar
• Bisogno T, Maurelli S, Melck D, De Petrocellis L, Di Marzo V. Biosynthesis, uptake, and degradation of anandamide and palmitoylethanolamide in leukocytes. J Biol Chem 1997;272(6):3315–23.
   Google Scholar
• Matias I, Pochard P, Orlando P, Salzet M, Pestel J, Di Marzo V. Presence and regulation of the endocannabinoid system in human dendritic cells. Eur J Biochem 2002;269(15):3771–8.
   Google Scholar
• Di Marzo V. Endocannabinoids: synthesis and degradation. In: Amara SG, Bamberg E, Fleischmann B, Gudermann T, Hebert SC, Jahn R, et al., (eds.). Reviews of physiology biochemistry and pharmacology. Berlin, Heidelberg: Springer Berlin Heidelberg; 2008. p. 1–24.
   Google Scholar
• Pacher P, Mechoulam R. Is lipid signaling through cannabinoid 2 receptors part of a protective system? Prog Lipid Res 2011;50(2):193–211.
   PubMed Web of Science ®Google Scholar
• Oh DY, Talukdar S, Bae EJ, Imamura T, Morinaga H, Fan W, et al. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 2010;142(5):687–98.
   PubMed Web of Science ®Google Scholar
• Li H, Ruan XZ, Powis SH, Fernando R, Mon WY, Wheeler DC, et al. EPA and DHA reduce LPS-induced inflammation responses in HK-2 cells: evidence for a PPAR- g dependent mechanism. Kidney Int 2005;67(3):867–74.
   PubMed Web of Science ®Google Scholar
• Dong L, Zou H, Yuan C, Hong YH, Kuklev DV, Smith WL. Different fatty acids compete with arachidonic acid for binding to the allosteric or catalytic subunits of cyclooxygenases to regulate prostanoid synthesis. J Biol Chem 2015.
   Web of Science ®Google Scholar
• Strasser T, Fischer S, Weber PC. Leukotriene B5 is formed in human neutrophils after dietary supplementation with icosapentaenoic acid. Proc Natl Acad Sci 1985;82(5):1540–3.
   Google Scholar
• Levy BD, Serhan CN. Resolution of acute inflammation in the lung. Annu Rev Physiol 2014;76:467–92.
   PubMed Web of Science ®Google Scholar
• Serhan CN. Treating inflammation and infection in the 21st century: new hints from decoding resolution mediators and mechanisms. FASEB J 2017;31(4):1273–88.
   PubMed Web of Science ®Google Scholar
• Fung A, Vizcaychipi M, Lloyd D, Wan Y, Ma D. Central nervous system inflammation in disease related conditions: mechanistic prospects. Brain Res 2012;1446:144–55.
   Google Scholar
• Lyman M, Lloyd DG, Ji X, Vizcaychipi MP, Ma D. Neuroinflammation: the role and consequences. Neurosci Res 2014;79:1–12.
   PubMed Web of Science ®Google Scholar
• Trépanier MO, Hopperton KE, Orr SK, Bazinet RP. N-3 polyunsaturated fatty acids in animal models with neuroinflammation: an update. Eur J Pharmacol 2016;785:187–206.
   Google Scholar
• Leyrolle Q, Layé S, Nadjar As. N-3 PUFAs and neuroinflammatory processes in cognitive disorders. OCL 2016;23(1):D103.
   Google Scholar
• Calder PC. Long-chain n-3 fatty acids and inflammation: potential application in surgical and trauma patients. Braz J Med Biol Res 2003;36(4):433–46.
   Google Scholar
• Breitner JC, Baker LD, Montine TJ, Meinert CL, Lyketsos CG, Ashe KH, et al. Extended results of the Alzheimer’s disease anti-inflammatory prevention trial. Alzheimer’s Dementia 2011;7(4):402–11.
   PubMed Web of Science ®Google Scholar
• Klegeris A, McGeer PL. Non-steroidal anti-inflammatory drugs (NSAIDs) and other anti-inflammatory agents in the treatment of neurodegenerative disease. Curr Alzheimer Res 2005;2(3):355–65.
   PubMedGoogle Scholar
• Szekely CA, Thorne JE, Zandi PP, Ek M, Messias E, Breitner JCS, et al. Nonsteroidal anti-inflammatory drugs for the prevention of Alzheimer’s disease: a systematic review. Neuroepidemiology 2004;23(4):159–69.
   PubMed Web of Science ®Google Scholar
• Martin BK, Meinert CL, Breitner JCS, the ARG. Double placebo design in a prevention trial for Alzheimer’s disease. Controll Clin Trials 2002;23(1):93–9.
   PubMedGoogle Scholar
• The Alzheimer’s Disease Anti-inflammatory Prevention Trial Research G. Results of a follow-up study to the randomized Alzheimer’s Disease Anti-inflammatory Prevention Trial (ADAPT). Alzheimer’s Dementia 2013;9(6):714–23.
   Google Scholar
• Blom MAA, van Twillert MGH, de Vries SC, Engels F, Finch CE, Veerhuis R, et al. NSAIDS inhibit the IL-1á-induced IL-6 release from human post-mortem astrocytes: the involvement of prostaglandin E2. Brain Res 1997;777(1–2):210–8.
   Google Scholar
• Wang P, Guan PP, Wang T, Yu X, Guo JJ, Wang ZY. Aggravation of Alzheimer’s disease due to the COX-2-mediated reciprocal regulation of IL-1β and Aβ between glial and neuron cells. Aging Cell 2014;13(4):605–15.
   Web of Science ®Google Scholar
• Kawano T, Anrather J, Zhou P, Park L, Wang G, Frys KA, et al. Prostaglandin E2 EP1 receptors: downstream effectors of COX-2 neurotoxicity. Nat Med 2006;12(2):225–9.
   Google Scholar
• An Y, Belevych N, Wang Y, Zhang H, Herschman H, Chen Q, et al. Neuronal and nonneuronal COX-2 expression confers neurotoxic and neuroprotective phenotypes in response to excitotoxin challenge. J Neurosci Res 2014;92(4):486–95.
   Google Scholar
• van Leyen K. Lipoxygenase: An emerging target for stroke therapy. CNS Neurol Disord Drug Targets 2013;12(2):191–9.
   Google Scholar
• Praticò D, Zhukareva V, Yao Y, Uryu K, Funk CD, Lawson JA, et al. 12/15-Lipoxygenase is increased in Alzheimer’s disease: possible involvement in brain oxidative stress. Am J Pathol 2004;164(5):1655–62.
   Google Scholar
• Wang H, Li J, Follett PL, Zhang Y, Cotanche DA, Jensen FE, et al. 12-Lipoxygenase plays a key role in cell death caused by glutathione depletion and arachidonic acid in rat oligodendrocytes. Eur J Neurosci 2004;20(8):2049–58.
   Google Scholar
• Yu GL, Wei EQ, Wang ML, Zhang WP, Zhang SH, Weng JQ, et al. Pranlukast, a cysteinyl leukotriene receptor-1 antagonist, protects against chronic ischemic brain injury and inhibits the glial scar formation in mice. Brain Res 2005;1053(1–2):116–25.
   Google Scholar
• Zhao CZ, Zhao B, Zhang XY, Huang XQ, Shi WZ, Liu HL, et al. Cysteinyl leukotriene receptor 2 is spatiotemporally involved in neuron injury, astrocytosis and microgliosis after focal cerebral ischemia in rats. Neuroscience 2011;189:1–11.
   Google Scholar
• Ye XH, Wu Y, Guo PP, Wang J, Yuan SY, Shang Y, et al. Lipoxin A4 analogue protects brain and reduces inflammation in a rat model of focal cerebral ischemia reperfusion. Brain Res 2010;1323:174–83.
   PubMed Web of Science ®Google Scholar
• Wu L, Miao S, Zou LB, Wu P, Hao H, Tang K, et al. Lipoxin A4 inhibits 5-lipoxygenase translocation and leukotrienes biosynthesis to exert a neuroprotective effect in cerebral ischemia/reperfusion injury. J Mol Neurosci 2012;48(1):185–200.
   PubMed Web of Science ®Google Scholar
• Lukiw WJ, Cui JG, Marcheselli VL, Bodker M, Botkjaer A, Gotlinger K, et al. A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease. J Clin Invest 2005;115(10):2774–83.
   PubMed Web of Science ®Google Scholar
• Bitarafan S, Harirchian MH, Nafissi S, Sahraian MA, Togha M, Siassi F, et al. Dietary intake of nutrients and its correlation with fatigue in multiple sclerosis patients. Iran J Neurol 2014;13(1):28–32.
   PubMedGoogle Scholar
• Samson RD, Barnes CA. Impact of aging brain circuits on cognition. Eur J Neurosci 2013;37(12):1903–15.
   PubMed Web of Science ®Google Scholar
• Cunnane S, Nugent S, Roy M, Courchesne-Loyer A, Croteau E, Tremblay S, et al. Brain fuel metabolism, aging, and Alzheimer’s disease. Nutrition 2011;27(1):3–20.
   PubMed Web of Science ®Google Scholar
• Landgrave-Gomez J, Mercado-Gomez O, Guevara-Guzman R. Epigenetic mechanisms in neurological and neurodegenerative diseases. Front Cell Neurosci 2015;9:58.
   PubMed Web of Science ®Google Scholar
• Madore C, Nadjar A, Delpech JC, Sere A, Aubert A, Portal C, et al. Nutritional n-3 PUFAs deficiency during perinatal periods alters brain innate immune system and neuronal plasticity-associated genes. Brain Behav Immun 2014;41:22–31.
   PubMed Web of Science ®Google Scholar
• Chen S, Zhang H, Pu H, Wang G, Li W, Leak RK, et al. n-3 PUFA supplementation benefits microglial responses to myelin pathology. Sci Rep 2015;4:2705.
   Web of Science ®Google Scholar
• Cardoso HD, dos Santos Junior EF, de Santana DF, Goncalves-Pimentel C, Angelim MK, Isaac AR, et al. Omega-3 deficiency and neurodegeneration in the substantia nigra: involvement of increased nitric oxide production and reduced BDNF expression. Biochim Biophys Acta 2014;1840(6):1902–12.
   PubMed Web of Science ®Google Scholar
• Passos PP, Borba JM, Rocha-de-Melo AP, Guedes RC, da Silva RP, Filho WT, et al. Dopaminergic cell populations of the rat substantia nigra are differentially affected by essential fatty acid dietary restriction over two generations. J Chem Neuroanat 2012;44(2):66–75.
   Google Scholar
• Lee HJ, Han J, Jang Y, Kim SJ, Park JH, Seo KS, et al. Docosahexaenoic acid prevents paraquat-induced reactive oxygen species production in dopaminergic neurons via enhancement of glutathione homeostasis. Biochem Biophys Res Commun 2015;457(1):95–100.
   Google Scholar
• Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell 2013;153(6):1194–217.
   PubMed Web of Science ®Google Scholar
• Swerdlow RH. Brain aging, Alzheimer’s disease, and mitochondria. Biochim Biophys Acta 2011;1812(12):1630–9.
   PubMed Web of Science ®Google Scholar
• Zoncu R, Efeyan A, Sabatini DM. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 2011;12(1):21–35.
   PubMed Web of Science ®Google Scholar
• Cornu M, Albert V, Hall MN. mTOR in aging, metabolism, and cancer. Curr Opin Genet Dev 2013;23(1):53–62.
   PubMed Web of Science ®Google Scholar
• Perluigi M, Di Domenico F, Butterfield DA. mTOR signaling in aging and neurodegeneration: At the crossroad between metabolism dysfunction and impairment of autophagy. Neurobiol Dis 2015;84:39–49.
   PubMed Web of Science ®Google Scholar
• Mi W, van Wijk N, Cansev M, Sijben JW, Kamphuis PJ. Nutritional approaches in the risk reduction and management of Alzheimer’s disease. Nutrition 2013;29(9):1080–9.
   PubMed Web of Science ®Google Scholar
• Tomi M, Zhao Y, Thamotharan S, Shin BC, Devaskar SU. Early life nutrient restriction impairs blood-brain metabolic profile and neurobehavior predisposing to Alzheimer’s disease with aging. Brain Res 2013;1495:61–75.
   Google Scholar
• Bazinet RP, Laye S. Polyunsaturated fatty acids and their metabolites in brain function and disease. Nat Rev Neurosci 2014;15(12):771–85.
   PubMed Web of Science ®Google Scholar
• Balvers MG, Verhoeckx KC, Plastina P, Wortelboer HM, Meijerink J, Witkamp RF. Docosahexaenoic acid and eicosapentaenoic acid are converted by 3T3-L1 adipocytes to N-acyl ethanolamines with anti-inflammatory properties. Biochim Biophys Acta 2010;1801(10):1107–14.
   Google Scholar
• Simopoulos AP. Evolutionary aspects of diet: the omega-6/omega-3 ratio and the brain. Mol Neurobiol 2011;44(2):203–15.
   PubMed Web of Science ®Google Scholar
• Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR, et al. Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 1990;87(5):1932–6.
   PubMed Web of Science ®Google Scholar