Combination treatment of docosahexaenoic acid (DHA) and all-trans-retinoic acid (ATRA) inhibit IL-17 and RORγt gene expression in PBMCs of patients with relapsing-remitting multiple sclerosis

References

• Tullman MJ. Overview of the epidemiology, diagnosis, and disease progression associated with multiple sclerosis. Am J Manage Care. 2013;19(2):15–20.
   PubMed Web of Science ®Google Scholar
• Hirahara K, Nakayama T. CD4+ T-cell subsets in inflammatory diseases: beyond the Th1/Th2 paradigm. Int Immunol. 2016;28(4):163–171.10.1093/intimm/dxw006
   PubMed Web of Science ®Google Scholar
• Park H, Li Z, Yang XO, et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol. 2005;6(11):1133–1141.10.1038/ni1261
   PubMed Web of Science ®Google Scholar
• Brucklacher-Waldert V, Stuerner K, Kolster M, et al. Phenotypical and functional characterization of T helper 17 cells in multiple sclerosis. Brain. 2009;132(12):3329–3341.10.1093/brain/awp289
   PubMed Web of Science ®Google Scholar
• Noack M, Miossec P. Th17 and regulatory T cell balance in autoimmune and inflammatory diseases. Autoimmun Rev. 2014;13(6):668–677.10.1016/j.autrev.2013.12.004
   PubMed Web of Science ®Google Scholar
• Dos Passos GR, Sato DK, Becker J. Th17 cells pathways in multiple sclerosis and neuromyelitis optica spectrum disorders: pathophysiological and therapeutic implications. Mediators Inflamm. 2016;2016(5314541):6.
   Google Scholar
• Reza Dorosty-Motlagh A, Mohammadzadeh Honarvar N, Sedighiyan M, et al. The molecular mechanisms of vitamin A deficiency in multiple sclerosis. J Mol Neurosci. 2016;60(1):82–90.10.1007/s12031-016-0781-0
   PubMed Web of Science ®Google Scholar
• Harrirchian MH, MohammadzadehHonarvar N, Koohdani F, et al. The effect of vitamin a supplementation on disease progression, cytokine levels and gene expression in multiple sclerotic patients: study protocol for a randomized controlled trial. Acta Med Iran. 2014;52(2):94–100.
   PubMedGoogle Scholar
• Saboor-Yaraghi AA, Harirchian MH, Mohammadzadeh Honarvar N, et al. The effect of vitamin A supplementation on FoxP3 and TGF-β gene expression in Avonex-treated multiple sclerosis patients. J Mol Neurosci. 2015;56(3):608–612.10.1007/s12031-015-0549-y
   PubMed Web of Science ®Google Scholar
• Sezavar H, Saboor-Yaraghi AA, Salehi E, et al. Whether vitamin A supplementation is effective in T-bet and IFN-γ gene expression reduction? Immunol Invest. 2015;44(2):189–198.10.3109/08820139.2014.953635
   PubMed Web of Science ®Google Scholar
• Niemoller TD, Bazan NG. Docosahexaenoic acid neurolipidomics. Prostaglandins Other Lipid Mediators. 2010 Apr;91(3–4):85–89.10.1016/j.prostaglandins.2009.09.005
   PubMed Web of Science ®Google Scholar
• Cunnane SC, Ho SY, Dore-Duffy P, et al. Essential fatty acid and lipid profiles in plasma and erythrocytes in patients with multiple sclerosis. Am J Clin Nutr. 1989;50(4):801–806.
   PubMed Web of Science ®Google Scholar
• Salvati S, Attorri L, Di Benedetto R, et al. Polyunsaturated fatty acids and neurological diseases. Mini Rev Med Chem. 2006;6(11):1201–1211.10.2174/138955706778742740
   PubMed Web of Science ®Google Scholar
• Kong W, Yen JH, Ganea D. Docosahexaenoic acid prevents dendritic cell maturation, inhibits antigen-specific Th1/Th17 differentiation and suppresses experimental autoimmune encephalomyelitis. Brain Behav Immun. 2011 Jul;25(5):872–882.10.1016/j.bbi.2010.09.012
   PubMed Web of Science ®Google Scholar
• Unoda K, Doi Y, Nakajima H, et al. Eicosapentaenoic acid (EPA) induces peroxisome proliferator-activated receptors and ameliorates experimental autoimmune encephalomyelitis. J Neuroimmunol. 2013;256(1–2):7–12.10.1016/j.jneuroim.2012.12.003
   PubMed Web of Science ®Google Scholar
• Pantzaris MC, Loukaides GN, Ntzani EE, et al. A novel oral nutraceutical formula of omega-3 and omega-6 fatty acids with vitamins (PLP10) in relapsing remitting multiple sclerosis: a randomised, double-blind, placebo-controlled proof-of-concept clinical trial. BMJ Open. 2013;3(4):e002170.10.1136/bmjopen-2012-002170
   PubMed Web of Science ®Google Scholar
• Shirani A, Zhao Y, Karim ME, et al. Association between use of interferon beta and progression of disability in patients with relapsing-remitting multiple sclerosis. JAMA. 2012;308(3):247–256.
   PubMed Web of Science ®Google Scholar
• Lublin FD, Reingold SC. Defining the clinical course of multiple sclerosis results of an international survey. Neurology. 1996;46(4):907–911.10.1212/WNL.46.4.907
   PubMed Web of Science ®Google Scholar
• McDonald WI, Compston A, Edan G, et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol. 2001;50(1):121–127.10.1002/(ISSN)1531-8249
   PubMed Web of Science ®Google Scholar
• Kurtzke JF. Rating neurologic impairment in multiple sclerosis an expanded disability status scale (EDSS). Neurology. 1983;33(11):1444–1444.10.1212/WNL.33.11.1444
   PubMed Web of Science ®Google Scholar
• Robledo D, Hernández-Urcera J, Cal RM, et al. Analysis of qPCR reference gene stability determination methods and a practical approach for efficiency calculation on a turbot gonad dataset. BMC Genomics. 2014;15:648.10.1186/1471-2164-15-648
   PubMed Web of Science ®Google Scholar
• Logan J, Edwards kJ, Saunders NA. Real-time PCR: current technology and applications. London: Horizon Scientific Press; 2009.
   Google Scholar
• Haghikia A, Jörg S, Duscha A, et al. Dietary fatty acids directly impact central nervous system autoimmunity via the small intestine. Immunity. 2016;44(4):951–953.10.1016/j.immuni.2016.04.006
   PubMed Web of Science ®Google Scholar
• Axtell RC, Raman C, Steinman L. Type I interferons: beneficial in Th1 and detrimental in Th17 autoimmunity. Clin Rev Allergy Immunol. 2013;44(2):114–120.10.1007/s12016-011-8296-5
   PubMed Web of Science ®Google Scholar
• Río J, Nos C, Tintoré M, et al. Defining the response to interferon-β in relapsing-remitting multiple sclerosis patients. Ann Neurol. 2006;59(2):344–352.10.1002/(ISSN)1531-8249
   PubMed Web of Science ®Google Scholar
• Moynihan J, Moore H. Endocrine and phototransduction effects in the prevention of multiple sclerosis. Med Hypotheses. 2011;77(6):1011–1014.10.1016/j.mehy.2011.08.037
   PubMed Web of Science ®Google Scholar
• Mucida D, Park Y, Kim G, et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science. 2007;317(5835):256–260.10.1126/science.1145697
   PubMed Web of Science ®Google Scholar
• Honarvar NM, Harirchian MH, Koohdani F, et al. The effect of vitamin a supplementation on retinoic acid-related orphan receptor γt (RORγt) and interleukin-17 (IL-17) gene expression in avonex-treated multiple sclerotic patients. J Mol Neurosci. 2013;51(3):749–753.10.1007/s12031-013-0058-9
   PubMed Web of Science ®Google Scholar
• Weaver KL, Ivester P, Seeds M, et al. Effect of dietary fatty acids on inflammatory gene expression in healthy humans. J Biol Chem. 2009;284(23):15400–15407.10.1074/jbc.M109.004861
   PubMed Web of Science ®Google Scholar
• Pizato N, Bonatto S, Piconcelli M. Fish oil alters T-lymphocyte proliferation and macrophage responses in Walker 256 tumor-bearing rats. Nutrition. 2006 Apr;22(4):425–432.10.1016/j.nut.2005.11.001
   PubMed Web of Science ®Google Scholar
• Harris TJ, Grosso JF, Yen HR, et al. Cutting edge: An in vivo requirement for STAT3 signaling in TH17 development and TH17-dependent autoimmunity. J Immunol. 2007;179(7):4313–4317.10.4049/jimmunol.179.7.4313
   PubMed Web of Science ®Google Scholar
• Monk JM, Hou TY, Turk HF, et al. n3 PUFAs reduce mouse CD4+ T-cell ex vivo polarization into Th17 cells. J Nutr. 2013;143(9):1501–1508.10.3945/jn.113.178178
   PubMed Web of Science ®Google Scholar
• Harbige L, Yeatman N, Amor S, et al. Prevention of experimental autoimmune encephalomyelitis in Lewis rats by a novel fungal source of γ-linolenic acid. Br J Nutr. 1995;74(05):701–715.10.1079/BJN19950173
   PubMed Web of Science ®Google Scholar
• Millar JH, Zilkha K, Langman M, et al. Double-blind trial of linoleate supplementation of the diet in multiple sclerosis. Br Med J. 1973;1(5856):765–768.10.1136/bmj.1.5856.765
   PubMed Web of Science ®Google Scholar
• Weinstock-Guttman B, Baier M, Park Y, et al. Low fat dietary intervention with omega-3 fatty acid supplementation in multiple sclerosis patients. Prostaglandins Leukotrienes Essent Fatty Acids. 2005;73(5):397–404.10.1016/j.plefa.2005.05.024
   PubMed Web of Science ®Google Scholar
• Torkildsen O, Wergeland S, Bakke S, et al. ω-3 fatty acid treatment in multiple sclerosis (OFAMS Study): a randomized, double-blind, placebo-controlled trial. Arch Neurol. 2012;69(8):1044–1051.
   PubMed Web of Science ®Google Scholar
• Urquiza AM, Liu S, Sjöberg M, et al. Docosahexaenoic acid, a ligand for the retinoid X receptor in mouse brain. Science. 2000;290(5499):2140–2144.10.1126/science.290.5499.2140
   PubMed Web of Science ®Google Scholar
• Dawson MI, Xia Z. The retinoid X receptors and their ligands. Biochim Biophys Acta. 2012;1821(1):21–56.10.1016/j.bbalip.2011.09.014
   PubMed Web of Science ®Google Scholar
• Berger H, Végran F, Chikh M, et al. SOCS3 transactivation by PPARγ prevents IL-17-driven cancer growth. Cancer Res. 2013;73(12):3578–3590.10.1158/0008-5472.CAN-12-4018
   PubMed Web of Science ®Google Scholar
• Chandraratna RA, Noelle RJ, Nowak EC. Treatment with retinoid X receptor agonist IRX4204 ameliorates experimental autoimmune encephalomyelitis. Am J Transl Res. 2016;8(2):1016–1026.
   PubMed Web of Science ®Google Scholar
• Shiri-Shahsavar MR, Mirshafiee A, Parastouei K, et al. A novel combination of docosahexaenoic acid, all-trans retinoic acid, and 1, 25-dihydroxyvitamin D3 reduces T-bet gene expression, serum interferon gamma, and clinical scores but promotes PPARγ gene expression in experimental autoimmune encephalomyelitis. J Mol Neurosci. 2016;60(4):498–508.10.1007/s12031-016-0834-4
   PubMed Web of Science ®Google Scholar
• Levin AA, Sturzenbecker LJ, Kazmer S, et al. 9-cis retinoic acid stereoisomer binds and activates the nuclear receptor RXRα. Nature. 1992;355(6358):359–361.10.1038/355359a0
   PubMed Web of Science ®Google Scholar
• Diab A, Hussain RZ, Lovett-Racke AE, et al. Ligands for the peroxisome proliferator-activated receptor-γ and the retinoid X receptor exert additive anti-inflammatory effects on experimental autoimmune encephalomyelitis. J Neuroimmunol. 2004;148(1–2):116–126.10.1016/j.jneuroim.2003.11.010
   PubMed Web of Science ®Google Scholar