Vitamin D down-regulates the expression of some Th17 cell-related cytokines, key inflammatory chemokines, and chemokine receptors in experimental autoimmune encephalomyelitis

References

• Milo R, Miller A. Revised diagnostic criteria of multiple sclerosis. Autoimmun Rev 2014;9972(14):012.
   Google Scholar
• Robinson AP, Harp CT, Noronha A, Miller SD. The experimental autoimmune encephalomyelitis (EAE) model of MS: utility for understanding disease pathophysiology and treatment. Handb Clin Neurol 2014;122:173–89.
   PubMedGoogle Scholar
• Jafarzadeh A, Azizi SV, Nemati M, Khoramdel-Azad H, Shamsizadeh A, Ayoobi F, et al. Ginger extract reduces the expression of IL-17 and IL-23 in the sera and central nervous system of EAE mice. Iran J Immunol 2015;12(4):288–301.
   PubMed Web of Science ®Google Scholar
• Haghmorad D, Mahmoudi MB, Mahmoudi M, Rab SZ, Rastin M, Shegarfi H, et al. Calcium intervention ameliorates experimental model of multiple sclerosis. Oman Med J 2014;29(3):185–89.
   PubMedGoogle Scholar
• Garg N, Smith TW. An update on immunopathogenesis, diagnosis, and treatment of multiple sclerosis. Brain Behav 2015;5(9):e00362.
   PubMed Web of Science ®Google Scholar
• Raphael I, Nalawade S, Eagar TN, Forsthuber TG. T cell subsets and their signature cytokines in autoimmune and inflammatory diseases. Cytokine 2015;74(1):5–17.
   PubMed Web of Science ®Google Scholar
• Buc M. Role of regulatory T cells in pathogenesis and biological therapy of multiple sclerosis. Mediators Inflamm 2013;2013:963748.
   PubMed Web of Science ®Google Scholar
• Jafarzadeh A, Mahdavi R, Jamali M, Hajghani H, Nemati M, Ebrahimi HA. Increased concentrations of interleukin-33 in the serum and cerebrospinal fluid of patients with multiple sclerosis. Oman Med J 2016;31(1):40–45.
   PubMedGoogle Scholar
• Basu R, Hatton RD, Weaver CT. The Th17 family: flexibility follows function. Immunol Rev 2013;252(1):89–103.
   PubMedGoogle Scholar
• Noack M, Miossec P. Th17 and regulatory T cell balance in autoimmune and inflammatory diseases. Autoimmun Rev 2014;13(6):668–77.
   PubMed Web of Science ®Google Scholar
• Zúñiga LA, Jain R, Haines C, Cua DJ. Th17 cell development: from the cradle to the grave. Immunol Rev 2013;252(1):78–88.
   PubMed Web of Science ®Google Scholar
• Annunziato F, Cosmi L, Romagnani S. Human and murine Th17. Curr Opin HIV AIDS 2010;5(2):114–19.
   PubMed Web of Science ®Google Scholar
• Holman DW, Klein RS, Ransohoff RM. The blood–brain barrier, chemokines and multiple sclerosis. Biochim Biophys Acta 2011;1812(2):220–30.
   PubMed Web of Science ®Google Scholar
• Raman D, Sobolik-Delmaire T, Richmond A. Chemokines in health and disease. Exp Cell Res 2011;317(5):575–89.
   PubMed Web of Science ®Google Scholar
• Lee AY, Eri R, Lyons AB, Grimm MC, Korner H. CC chemokine ligand 20 and its cognate receptor CCR6 in mucosal T cell immunology and inflammatory bowel disease: odd couple or axis of evil? Front Immunol 2013;4:194.
   PubMed Web of Science ®Google Scholar
• Williams JL, Holman DW, Klein RS. Chemokines in the balance: maintenance of homeostasis and protection at CNS barriers. Front Cell Neurosci 2014;8:154.
   PubMed Web of Science ®Google Scholar
• Safa A, Rashidinejad HR, Khalili M, Dabiri S, Nemati M, Mohammadi MM, et al. Higher circulating levels of chemokines CXCL10, CCL20 and CCL22 in patients with ischemic heart disease. Cytokine 2016;83:147–57.
   PubMed Web of Science ®Google Scholar
• Jafarzadeh A, Bagherzadeh S, Ebrahimi HA, Hajghani H, Bazrafshani MR, Khosravimashizi A, et al. Higher circulating levels of chemokine CCL20 in patients with multiple sclerosis: evaluation of the influences of chemokine gene polymorphism, gender, treatment and disease pattern. J Mol Neurosci 2014;53(3):500–505.
   PubMed Web of Science ®Google Scholar
• Jafarzadeh A, Fooladseresht H, Minaee K, Bazrafshani MR, Khosravimashizi A, Nemati M, et al. Higher circulating levels of chemokine CCL22 in patients with breast cancer: evaluation of the influences of tumor stage and chemokine gene polymorphism. Tumour Biol 2015;36(2):1163–71.
   PubMedGoogle Scholar
• Jafarzadeh A, Ebrahimi HA, Bagherzadeh S, Zarkesh F, Iranmanesh F, Najafzadeh A, et al. Lower serum levels of Th2-related chemokine CCL22 in women patients with multiple sclerosis: a comparison between patients and healthy women. Inflammation 2014;37(2):604–10.
   PubMed Web of Science ®Google Scholar
• Jafarzadeh A, Jamali M, Mahdavi R, Ebrahimi HA, Hajghani H, Khosravimashizi A, et al. Circulating levels of interleukin-35 in patients with multiple sclerosis: evaluation of the influences of FOXP3 gene polymorphism and treatment program. J Mol Neurosci: MN 2015;55(4):891–97.
   PubMed Web of Science ®Google Scholar
• Mohammadi-Kordkhayli M, Ahangar-Parvin R, Azizi SV, Nemati M, Shamsizadeh A, Khaksari M, et al. Vitamin D modulates the expression of IL-27 and IL-33 in the central nervous system in experimental autoimmune encephalomyelitis (EAE). Iran J Immunol 2015;12(1):35–49.
   PubMed Web of Science ®Google Scholar
• Jafarzadeh A, Keshavarz J, Bagheri-Jamebozorgi M, Nemati M, Frootan R, Shokri F. The association of the vitamin D status with the persistence of anti-HBs antibody at 20years after primary vaccination with recombinant hepatitis B vaccine in infancy. Clin Res Hepatol Gastroenterol 2017;41(1):66–74.
   PubMed Web of Science ®Google Scholar
• Dankers W, Colin EM, van Hamburg JP, Lubberts E. Vitamin D in autoimmunity: molecular mechanisms and therapeutic potential. Front Immunol 2016;7:697.
   PubMed Web of Science ®Google Scholar
• Prietl B, Treiber G, Pieber TR, Amrein K. Vitamin D and immune function. Nutrients 2013;5(7):2502–521.
   PubMed Web of Science ®Google Scholar
• Colotta F, Jansson B, Bonelli F. Modulation of inflammatory and immune responses by vitamin D. J Autoimmun 2017; 85:78–97.
   PubMed Web of Science ®Google Scholar
• Waddell A, Zhao J, Cantorna MT. NKT cells can help mediate the protective effects of 1,25-dihydroxyvitamin D3 in experimental autoimmune encephalomyelitis in mice. Int Immunol 2015;27(5):237–44.
   PubMed Web of Science ®Google Scholar
• Ascherio A, Munger KL, Simon KC. Vitamin D and multiple sclerosis. Lancet Neurol 2010;9(6):599–612.
   PubMed Web of Science ®Google Scholar
• Simpson S, Taylor B, Blizzard L, Ponsonby AL, Pittas F, Tremlett H, et al. Higher 25-hydroxyvitamin D is associated with lower relapse risk in multiple sclerosis. Ann Neurol 2010;68(2):193–203.
   PubMed Web of Science ®Google Scholar
• Farsani ZS, Behmanesh M, Sahraian MA. Interleukin-10 but not transforming growth factor-beta1 gene expression is up-regulated by vitamin D treatment in multiple sclerosis patients. J Neurol Sci 2015;350(1–2):18–23.
   PubMed Web of Science ®Google Scholar
• Sanseverino I, Rinaldi AO, Purificato C, Cortese A, Millefiorini E, Gessani S, et al. CCL2 induction by 1,25(OH)2D3 in dendritic cells from healthy donors and multiple sclerosis patients. J Steroid Biochem Mol Biol 2014;144(Pt A):102–105.
   PubMedGoogle Scholar
• Bartosik-Psujek H, Tabarkiewicz J, Pocinska K, Stelmasiak Z, Rolinski J. Immunomodulatory effects of vitamin D on monocyte-derived dendritic cells in multiple sclerosis. Mult Scler 2010;16(12):1513–16.
   PubMedGoogle Scholar
• da Costa DS, Hygino J, Ferreira TB, Kasahara TM, Barros PO, Monteiro C, et al. Vitamin D modulates different IL-17-secreting T cell subsets in multiple sclerosis patients. J Neuroimmunol 2016;299:8–18.
   PubMed Web of Science ®Google Scholar
• Parastouei K, Mirshafiey A, Eshraghian MR, Shiri-Shahsavar MR, Solaymani-Mohammadi F, Chahardoli R, et al. The effect of 1, 25(OH)2 D3 (calcitriol) alone and in combination with all-trans retinoic acid on ROR-gammat, IL-17, TGF-beta, and FOXP3 gene expression in experimental autoimmune encephalomyelitis. Nutr Neurosci 2016;20:1–9.
   PubMedGoogle Scholar
• Chang JH, Cha HR, Lee DS, Seo KY, Kweon MN. 1,25-Dihydroxyvitamin D3 inhibits the differentiation and migration of T(H)17 cells to protect against experimental autoimmune encephalomyelitis. PloS one 2010;5(12):e12925.
   PubMedGoogle Scholar
• Joshi S, Pantalena LC, Liu XK, Gaffen SL, Liu H, Rohowsky-Kochan C, et al. 1,25-dihydroxyvitamin d(3) ameliorates Th17 autoimmunity via transcriptional modulation of interleukin-17A. Mol Cell Biol 2011;31(17):3653–5669.
   PubMed Web of Science ®Google Scholar
• Zeitelhofer M, Adzemovic MZ, Gomez-Cabrero D, Bergman P, Hochmeister S, N’Diaye M, et al. Functional genomics analysis of vitamin D effects on CD4+ T cells in vivo in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 2017;114(9):E1678–E1687.
   PubMed Web of Science ®Google Scholar
• Jafarzadeh A, Mohammadi-Kordkhayli M, Ahangar-Parvin R, Azizi V, Khoramdel-Azad H, Shamsizadeh A, et al. Ginger extracts influence the expression of IL-27 and IL-33 in the central nervous system in experimental autoimmune encephalomyelitis and ameliorates the clinical symptoms of disease. J Neuroimmunol 2014;276(1–2):80–88.
   PubMed Web of Science ®Google Scholar
• Liu T, Donahue KC, Hu J, Kurnellas MP, Grant JE, Li H, et al. Identification of differentially expressed proteins in experimental autoimmune encephalomyelitis (EAE) by proteomic analysis of the spinal cord. J Proteome Res 2007;6(7):2565–75.
   PubMed Web of Science ®Google Scholar
• Takeuchi C, Yamagata K, Takemiya T. Variation in experimental autoimmune encephalomyelitis scores in a mouse model of multiple sclerosis. World Journal of Neurology 2013;3(3):56–61.
   Google Scholar
• Ni J, Shu YY, Zhu YN, Fu YF, Tang W, Zhong XG, et al. COX-2 inhibitors ameliorate experimental autoimmune encephalomyelitis through modulating IFN-gamma and IL-10 production by inhibiting T-bet expression. J Neuroimmunol 2007;186(1–2):94–103.
   PubMed Web of Science ®Google Scholar
• Rolf L, Muris AH, Hupperts R, Damoiseaux J. Illuminating vitamin D effects on B cells – the multiple sclerosis perspective. Immunology 2016;147(3):275–84.
   PubMed Web of Science ®Google Scholar
• VanAmerongen BM, Dijkstra CD, Lips P, Polman CH. Multiple sclerosis and vitamin D: an update. Eur J Clin Nutr 2004;58(8):1095–109.
   PubMed Web of Science ®Google Scholar
• Farias AS, Spagnol GS, Bordeaux-Rego P, Oliveira CO, Fontana AG, de Paula RF, et al. Vitamin D3 induces IDO+ tolerogenic DCs and enhances Treg, reducing the severity of EAE. CNS Neurosci Ther 2013;19(4):269–77.
   PubMed Web of Science ®Google Scholar
• Xie Z, Chen J, Zheng C, Wu J, Cheng Y, Zhu S, et al. 1,25-dihydroxyvitamin D3-induced dendritic cells suppress experimental autoimmune encephalomyelitis by increasing proportions of the regulatory lymphocytes and reducing T helper type 1 and type 17 cells. Immunology 2015;152(3):414–24.
   Web of Science ®Google Scholar
• Smolders J, Thewissen M, Peelen E, Menheere P, Tervaert JW, Damoiseaux J, et al. Vitamin D status is positively correlated with regulatory T cell function in patients with multiple sclerosis. PloS one 2009;4(8):e6635.
   PubMed Web of Science ®Google Scholar
• Sloka S, Zhornitsky S, Silva C, Metz LM, Yong VW. 1,25-Dihydroxyvitamin D3 protects against immune-mediated killing of neurons in culture and in experimental autoimmune encephalomyelitis. PloS one 2015;10(12):e0144084.
   PubMed Web of Science ®Google Scholar
• Grishkan IV, Fairchild AN, Calabresi PA, Gocke AR. 1,25-Dihydroxyvitamin D3 selectively and reversibly impairs T helper-cell CNS localization. Proc Natl Acad Sci U S A 2013;110(52):21101–106.
   PubMed Web of Science ®Google Scholar
• Shirazi HA, Rasouli J, Ciric B, Rostami A, Zhang GX. 1,25-Dihydroxyvitamin D3 enhances neural stem cell proliferation and oligodendrocyte differentiation. Exp Mol Pathol 2015;98(2):240–45.
   PubMed Web of Science ®Google Scholar
• Lemire JM, Archer DC. 1,25-dihydroxyvitamin D3 prevents the in vivo induction of murine experimental autoimmune encephalomyelitis. J Clin Invest 1991;87(3):1103–07.
   PubMed Web of Science ®Google Scholar
• Cantorna MT, Hayes CE, DeLuca HF. 1,25-Dihydroxyvitamin D3 reversibly blocks the progression of relapsing encephalomyelitis, a model of multiple sclerosis. Proc Natl Acad Sci U S A 1996;93(15):7861–64.
   PubMed Web of Science ®Google Scholar
• Hayes CE, Hubler SL, Moore JR, Barta LE, Praska CE, Nashold FE. Vitamin D actions on CD4(+) T cells in autoimmune disease. Front Immunol 2015;6:100.
   PubMed Web of Science ®Google Scholar
• Sloka S, Silva C, Wang J, Yong VW. Predominance of Th2 polarization by vitamin D through a STAT6-dependent mechanism. J Neuroinflammation 2011;8:56.
   PubMed Web of Science ®Google Scholar
• Mayne CG, Spanier JA, Relland LM, Williams CB, Hayes CE. 1,25-Dihydroxyvitamin D3 acts directly on the T lymphocyte vitamin D receptor to inhibit experimental autoimmune encephalomyelitis. Eur J Immunol 2011;41(3):822–32.
   PubMed Web of Science ®Google Scholar
• Becher B, Segal BM. T(H)17 cytokines in autoimmune neuro-inflammation. Curr Opin Immunol 2011;23(6):707–12.
   PubMed Web of Science ®Google Scholar
• Ghaffari SA, Nemati M, Hajghani H, Ebrahimi H, Sheikhi A, Jafarzadeh A. Circulating concentrations of interleukin (IL)-17 in patients with multiple sclerosis: evaluation of the effects of gender, treatment, disease patterns and IL-23 receptor gene polymorphisms. Iran J Neurol 2017;16(1):15–25.
   PubMed Web of Science ®Google Scholar
• Qu N, Xu M, Mizoguchi I, Furusawa J, Kaneko K, Watanabe K, et al. Pivotal roles of T-helper 17-related cytokines, IL-17, IL-22, and IL-23, in inflammatory diseases. Clin Dev Immunol 2013;2013:968549.
   PubMed Web of Science ®Google Scholar
• Murphy AC, Lalor SJ, Lynch MA, Mills KH. Infiltration of Th1 and Th17 cells and activation of microglia in the CNS during the course of experimental autoimmune encephalomyelitis. Brain Behav Immun 2010;24(4):641–51.
   PubMed Web of Science ®Google Scholar
• Etesam Z, Nemati M, Ebrahimizadeh MA, Ebrahimi HA, Hajghani H, Khalili T, et al. Altered expression of specific transcription factors of Th17 (RORgammat, RORalpha) and treg lymphocytes (FOXP3) by peripheral blood mononuclear cells from patients with multiple sclerosis. J Mol Neurosci: MN 2016;60(1):94–101.
   PubMed Web of Science ®Google Scholar
• Kimura A, Kishimoto T. IL-6: regulator of Treg/Th17 balance. Eur J Immunol 2010;40(7):1830–35.
   PubMed Web of Science ®Google Scholar
• Neve A, Corrado A, Cantatore FP. Immunomodulatory effects of vitamin D in peripheral blood monocyte-derived macrophages from patients with rheumatoid arthritis. Clin Exp Med 2014;4(3): 275–83.
   Google Scholar
• Derkow K, Kruger C, Dembny P, Lehnardt S. Microglia induce neurotoxic IL-17+ gammadelta T cells dependent on TLR2, TLR4, and TLR9 activation. PloS one 2015;10(8):e0135898.
   PubMed Web of Science ®Google Scholar
• Jadidi-Niaragh F, Mirshafiey A. Th17 cell, the new player of neuroinflammatory process in multiple sclerosis. Scand J Immunol 2011;74(1):1–13.
   PubMed Web of Science ®Google Scholar
• Feng X, Lv C, Wang F, Gan K, Zhang M, Tan W. Modulatory effect of 1,25-dihydroxyvitamin D 3 on IL1 beta-induced RANKL, OPG, TNF alpha , and IL-6 expression in human rheumatoid synoviocyte MH7A. Clin Dev Immunol 2013;2013:160123.
   PubMedGoogle Scholar
• Croxford AL, Kulig P, Becher B. IL-12-and IL-23 in health and disease. Cytokine Growth Factor Rev 2014;25(4):415–21.
   PubMed Web of Science ®Google Scholar
• Klein A, Schwartz H, Sagi-Assif O, Meshel T, Izraely S, Ben Menachem S, et al. Astrocytes facilitate melanoma brain metastasis via secretion of IL-23. J Pathol 2015;236(1):116–27.
   PubMed Web of Science ®Google Scholar
• Columba-Cabezas S, Serafini B, Ambrosini E, Sanchez M, Penna G, Adorini L, et al. Induction of macrophage-derived chemokine/CCL22 expression in experimental autoimmune encephalomyelitis and cultured microglia: implications for disease regulation. J Neuroimmunol 2002;130(1–2):10–21.
   PubMed Web of Science ®Google Scholar
• Ding X, Cao F, Cui L, Ciric B, Zhang GX, Rostami A. IL-9 signaling affects central nervous system resident cells during inflammatory stimuli. Exp Mol Pathol 2015;99(3):570–74.
   PubMed Web of Science ®Google Scholar
• Galimberti D, Fenoglio C, Comi C, Scalabrini D, De Riz M, Leone M, et al. MDC/CCL22 intrathecal levels in patients with multiple sclerosis. Mult Scler 2008;14(4):547–49.
   PubMedGoogle Scholar
• Dogan R-NE, Long N, Forde E, Dennis K, Kohm AP, Miller SD, et al. CCL22 regulates experimental autoimmune encephalomyelitis by controlling inflammatory macrophage accumulation and effector function. J Leukoc Biol 2011;89(1):93–104.
   PubMed Web of Science ®Google Scholar
• Leibowitz SM, Yan J. NF-kappaB pathways in the pathogenesis of multiple sclerosis and the therapeutic implications. Front Mol Neurosci 2016;9:84.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Sonobe Y, Akahori T, Jin S, Kawanokuchi J, Noda M, et al. IL-9 promotes Th17 cell migration into the central nervous system via CC chemokine ligand-20 produced by astrocytes. J Immunol 2011;186(7):4415–21.
   PubMed Web of Science ®Google Scholar
• Meares GP, Ma X, Qin H, Benveniste EN. Regulation of CCL20 expression in astrocytes by IL-6 and IL-17. Glia 2012;60(5):771–81.
   PubMed Web of Science ®Google Scholar
• Ambrosini E, Columba-Cabezas S, Serafini B, Muscella A, Aloisi F. Astrocytes are the major intracerebral source of macrophage inflammatory protein-3alpha/CCL20 in relapsing experimental autoimmune encephalomyelitis and in vitro. Glia 2003;41(3):290–300.
   PubMed Web of Science ®Google Scholar
• Boontanrart M, Hall SD, Spanier JA, Hayes CE, Olson JK. Vitamin D3 alters microglia immune activation by an IL-10 dependent SOCS3 mechanism. J Neuroimmunol 2016;292:126–36.
   PubMed Web of Science ®Google Scholar