Publication Cover
Neurological Research
A Journal of Progress in Neurosurgery, Neurology and Neurosciences
Volume 41, 2019 - Issue 10
447
Views
21
CrossRef citations to date
0
Altmetric
Articles

Prevention and treatment of experimental autoimmune encephalomyelitis induced mice with 1, 25-dihydroxyvitamin D3

, , , , , & show all
Pages 943-957 | Received 29 Jan 2019, Accepted 25 Jul 2019, Published online: 12 Aug 2019

References

  • Haak S. IL-17A and IL-17F do not contribute vitally to autoimmune neuro-inflammation in mice. J Clin Invest. 2009;119(1):61–69.
  • Haghmorad D, Salehipour Z, Nosratabadi R, et al. Medium-dose estrogen ameliorates experimental autoimmune encephalomyelitis in ovariectomized mice. J Immunotoxicol. 2016;1–12.
  • Aarts SA, Seijkens TT, Kusters PJ, et al. Inhibition of CD40-TRAF6 interactions by the small molecule inhibitor 6877002 reduces neuroinflammation. J Neuroinflammation. 2017;14(1):105.
  • Liu X, He F, Pang R, et al. Interleukin-17 (IL-17)-induced microRNA 873 (miR-873) contributes to the pathogenesis of experimental autoimmune encephalomyelitis by targeting A20 ubiquitin-editing enzyme. J Biol Chem. 2014;289(42):28971–28986.
  • Segal BM. Stage-specific immune dysregulation in multiple sclerosis. J Interferon Cytokine Res. 2014;34(8):633–640.
  • Namjooyan F, Ghanavati R, Majdinasab N, et al. Uses of complementary and alternative medicine in multiple sclerosis. J Tradit Complement Med. 2014;4(3):145–152.
  • Perriard G, Mathias A, Enz L, et al. Interleukin-22 is increased in multiple sclerosis patients and targets astrocytes. J Neuroinflammation. 2015;12(1):119.
  • Croxford AL, Kurschus FC, Waisman A. Mouse models for multiple sclerosis: historical facts and future implications. Biochim Biophys Acta. 2011;1812(2):177–183.
  • Sospedra M, Martin R. Immunology of multiple sclerosis. Annu Rev Immunol. 2005;23:683–747.
  • Domingues HS, Mues M, Lassmann H, et al. Functional and pathogenic differences of Th1 and Th17 cells in experimental autoimmune encephalomyelitis. PLoS One. 2010;5(11):e15531.
  • McCarthy DP, Richards MH, Miller SD. Mouse models of multiple sclerosis: experimental autoimmune encephalomyelitis and Theiler’s virus-induced demyelinating disease. Methods Mol Biol. 2012;900:381–401.
  • Nosratabadi R, Rastin M, Sankian M, et al. Hyperforin-loaded gold nanoparticle alleviates experimental autoimmune encephalomyelitis by suppressing Th1 and Th17 cells and upregulating regulatory T cells. Nanomed. 2016;12(7):1961–1971.
  • Haghmorad D, Mahmoudi MB, Mahmoudi M, et al. Calcium intervention ameliorates experimental model of multiple sclerosis. Oman Med J. 2014;29(3):185–189.
  • Stummvoll GH, DiPaolo RJ, Huter EN, et al. Th1, Th2, and Th17 effector T cell-induced autoimmune gastritis differs in pathological pattern and in susceptibility to suppression by regulatory T cells. J Immunol. 2008;181(3):1908–1916.
  • Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat Med. 2007;13(2):139–145.
  • Panitch HS, Hirsch RL, Haley AS, et al. Exacerbations of multiple sclerosis in patients treated with gamma interferon. Lancet. 1987;1(8538):893–895.
  • Moldovan IR, Rudick RA, Cotleur AC, et al. Interferon gamma responses to myelin peptides in multiple sclerosis correlate with a new clinical measure of disease progression. J Neuroimmunol. 2003;141(1–2):132–140.
  • Lock C, Hermans G, Pedotti R, et al. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med. 2002;8(5):500–508.
  • 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.
  • Weiss HA, Millward JM, Owens T. CD8+ T cells in inflammatory demyelinating disease. J Neuroimmunol. 2007;191(1–2):79–85.
  • Salehipour Z, Haghmorad D, Sankian M, et al. Bifidobacterium animalis in combination with human origin of Lactobacillus plantarum ameliorate neuroinflammation in experimental model of multiple sclerosis by altering CD4+ T cell subset balance. Biomed Pharmacothe. 2017;95:1535–1548.
  • Shevach EM. Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity. 2009;30(5):636–645.
  • Moriya M, Nakatsuji Y, Miyamoto K, et al. Edaravone, a free radical scavenger, ameliorates experimental autoimmune encephalomyelitis. Neurosci Lett. 2008;440(3):323–326.
  • O’Brien NC, Charlton B, Cowden WB, et al. Nitric oxide plays a critical role in the recovery of Lewis rats from experimental autoimmune encephalomyelitis and the maintenance of resistance to reinduction. J Immunol. 1999;163(12):6841–6847.
  • Kalman B, Toldy E. Genomic binding sites and biological effects of the vitamin D–VDR complex in multiple sclerosis [corrected]. Neuromolecular Med. 2014;16(2):265–279.
  • Hanwell HE, Banwell B. Assessment of evidence for a protective role of vitamin D in multiple sclerosis. Biochim Biophys Acta. 2011;1812(2):202–212.
  • Iruretagoyena M, Hirigoyen D, Naves R, et al. Immune response modulation by vitamin D: role in systemic lupus erythematosus. Front Immunol. 2015;6.
  • Chang J-H, Cha H-R, Lee D-S, et al. 1,25-Dihydroxyvitamin D3 inhibits the differentiation and migration of T(H)17 cells to protect against experimental autoimmune encephalomyelitis. PLoS One. 2010;5(9):e12925–e.
  • Lefebvre d’Hellencourt C, Montero-Menei CN, Bernard R, et al. Vitamin D3 inhibits proinflammatory cytokines and nitric oxide production by the EOC13 microglial cell line. J Neurosci Res. 2003;71(4):575–582.
  • Mattner F, Smiroldo S, Galbiati F, et al. Inhibition of Th1 development and treatment of chronic-relapsing experimental allergic encephalomyelitis by a non-hypercalcemic analogue of 1,25-dihydroxyvitamin D(3). Eur J Immunol. 2000;30(2):498–508.
  • Soleimani M, Jameie SB, Mehdizadeh M, et al. Vitamin D3 influence the Th1/Th2 ratio in C57BL/6 induced model of experimental autoimmune encephalomyelitis. Iran J Basic Med Sci. 2014;17(10):785–792.
  • Ahangar-Parvin R, Mohammadi-Kordkhayli M, Azizi SV, et al. The modulatory effects of vitamin D on the expression of IL-12 and TGF-β in the spinal cord and serum of mice with experimental autoimmune encephalomyelitis. Iran J Pathol. 2018;13(1):10–22.
  • Chiuso-Minicucci F, Ishikawa LL, Mimura LA, et al. Treatment with vitamin D/MOG association suppresses experimental autoimmune encephalomyelitis. PloS One. 2015;10(5):e0125836.
  • Farias AS, Spagnol GS, Bordeaux-Rego P, et al. Vitamin D3 induces IDO+ tolerogenic DCs and enhances Treg, reducing the severity of EAE. CNS Neurosci Ther. 2013;19(4):269–277.
  • Aranow C. Vitamin D and the immune system. J Investig Med. 2011;59(6):881–886.
  • Chang JH. 1,25-dihydroxyvitamin D(3) inhibits the differentiation and migration of T(H)17 cells to protect against experimental autoimmune encephalomyelitis. ACS Chem Biol. 2010;5(9).
  • Huehnchen P, Prozorovski T, Klaissle P, et al. Modulation of adult hippocampal neurogenesis during myelin-directed autoimmune neuroinflammation. Glia. 2011;59(1):132–142.
  • Mosayebi G, Haghmorad D, Namaki S, et al. Therapeutic effect of EDTA in experimental model of multiple sclerosis. Immunopharmacol Immunotoxicol. 2010;32(2):321–326.
  • Pedersen LB, Nashold FE, Spach KM, et al. 1,25-dihydroxyvitamin D3 reverses experimental autoimmune encephalomyelitis by inhibiting chemokine synthesis and monocyte trafficking. J Neurosci Res. 2007;85(11):2480–2490.
  • Horstmann L, Schmid H, Heinen AP, et al. Inflammatory demyelination induces glia alterations and ganglion cell loss in the retina of an experimental autoimmune encephalomyelitis model. J Neuroinflammation. 2013;10:120.
  • Nashold FE, Spach KM, Spanier JA, et al. Estrogen controls vitamin D3-mediated resistance to experimental autoimmune encephalomyelitis by controlling vitamin D3 metabolism and receptor expression. J Immunol. 2009;183(6):3672–3681.
  • Marques CD, Dantas AT, Fragoso TS, et al. The importance of vitamin D levels in autoimmune diseases. Rev Bras Reumatol Engl Ed. 2010;50(1):67–80.
  • Fernandes de Abreu DA, Landel V, Feron F. Seasonal, gestational and postnatal influences on multiple sclerosis: the beneficial role of a vitamin D supplementation during early life. J Neurol Sci. 2011;311(1–2):64–68.
  • Huseby ES, Huseby PG, Shah S, et al. Pathogenic CD8 T cells in multiple sclerosis and its experimental models. Front Immunol. 2012;3.
  • Yang C, He D, Yin C, et al. Inhibition of interferon regulatory factor 4 suppresses Th1 and Th17 cell differentiation and ameliorates experimental autoimmune encephalomyelitis. Scand J Immunol. 2015;82(4):345–351.
  • Nygardas M, Aspelin C, Paavilainen H, et al. Treatment of experimental autoimmune encephalomyelitis in SJL/J mice with a replicative HSV-1 vector expressing interleukin-5. Gene Ther. 2011;18(7):646–655.
  • Ruuls SR, Sedgwick JD. Cytokine-directed therapies in multiple sclerosis and experimental autoimmune encephalomyelitis. Immunol Cell Biol. 1998;76(1):65–73.
  • Haghmorad D, Amini AA, Mahmoudi MB, et al. Pregnancy level of estrogen attenuates experimental autoimmune encephalomyelitis in both ovariectomized and pregnant C57BL/6 mice through expansion of Treg and Th2 cells. J Neuroimmunol. 2014;277(1–2):85–95.
  • Haghmorad D, Mahmoudi MB, Salehipour Z, et al. Hesperidin ameliorates immunological outcome and reduces neuroinflammation in the mouse model of multiple sclerosis. J Neuroimmunol. 2017;302:23–33.
  • Bettelli E, Das MP, Howard ED, et al. IL-10 is critical in the regulation of autoimmune encephalomyelitis as demonstrated by studies of IL-10- and IL-4-deficient and transgenic mice. J Immunol. 1998;161(7):3299–3306.
  • Speck S, Lim J, Shelake S, et al. TGF-beta signaling initiated in dendritic cells instructs suppressive effects on Th17 differentiation at the site of neuroinflammation. PLos One. 2014;9(7):e102390.
  • Zhang X, Koldzic DN, Izikson L, et al. IL‐10 is involved in the suppression of experimental autoimmune encephalomyelitis by CD25+ CD4+ regulatory T cells. Int Immunol. 2004;16(2):249–256.
  • Jamshidian A, Shaygannejad V, Pourazar A, et al. Biased Treg/Th17 balance away from regulatory toward inflammatory phenotype in relapsed multiple sclerosis and its correlation with severity of symptoms. J Neuroimmunol. 2013;262(1–2):106–112.
  • Lemire JM, Archer DC. 1,25-dihydroxyvitamin D3 prevents the in vivo induction of murine experimental autoimmune encephalomyelitis. J Clin Invest. 1991;87(3):1103–1107.
  • Sloka S, Silva C, Wang J, et al. Predominance of Th2 polarization by vitamin D through a STAT6-dependent mechanism. J Neuroinflammation. 2011;8(1):56.
  • Chang SH, Chung Y, Dong C. Vitamin D suppresses Th17 cytokine production by inducing C/EBP homologous protein (CHOP) expression. J Biol Chem. 2010;285(50):38751–38755.
  • Joshi S, Pantalena LC, Liu XK, et al. 1,25-dihydroxyvitamin D(3) ameliorates Th17 autoimmunity via transcriptional modulation of interleukin-17A. Mol Cell Biol. 2011;31(17):3653–3669.
  • Mohammadi-Kordkhayli M, Ahangar-Parvin R, Azizi SV, et al. Vitamin D modulates the expression of IL-27 and IL-33 in the central nervous system in Experimental Autoimmune Encephalomyelitis (EAE). Iranian J Immunol. 2015;12(1):35–49.
  • Wergeland S, Torkildsen Ø, Myhr K-M, et al. Dietary vitamin D3 supplements reduce demyelination in the cuprizone model. PLoS One. 2011;6(10):e26262–e.
  • Adzemovic MZ, Zeitelhofer M, Hochmeister S, et al. Efficacy of vitamin D in treating multiple sclerosis-like neuroinflammation depends on developmental stage. Exp Neurol. 2013;249:39–48.
  • Wittke A, Weaver V, Mahon BD, et al. Vitamin D receptor-deficient mice fail to develop experimental allergic asthma. J Immunol. 2004;173(5):3432–3436.
  • Gocke AR, Hussain RZ, Yang Y, et al. Transcriptional modulation of the immune response by peroxisome proliferator-activated receptor-α agonists in autoimmune disease. J Immunol. 2009;182(7):4479–4487.
  • Fernando V, Omura S, Sato F, et al. Regulation of an autoimmune model for multiple sclerosis in Th2-biased GATA3 transgenic mice. Int J Mol Sci. 2014;15(2):1700–1718.
  • Martinez NE, Sato F, Omura S, et al. RORγt, but not T-bet, overexpression exacerbates an autoimmune model for multiple sclerosis. J Neuroimmunol. 2014;276:142–149.
  • Liu T, Shi Y, Du J, et al. Vitamin D treatment attenuates 2,4,6-trinitrobenzene sulphonic acid (TNBS)-induced colitis but not oxazolone-induced colitis. Sci Rep. 2016;6:32889.
  • Yang Y, Weiner J, Liu Y, et al. T-bet is essential for encephalitogenicity of both Th1 and Th17 cells. J Exp Med. 2009;206(7):1549–1564.
  • Lovett-Racke AE, Yang Y, Racke MK. Th1 versus Th17: are T cell cytokines relevant in multiple sclerosis? Biochim Biophys Acta. 2011;1812(2):246–251.
  • Letourneau S, Hernandez L, Faris AN, et al. Evaluating the effects of estradiol on endothelial nitric oxide stimulated by erythrocyte-derived ATP using a microfluidic approach. Anal Bioanal Chem. 2010;397(8):3369–3375.
  • Ysmail-Dahlouk L, Nouari W, Aribi M. 1,25-dihydroxyvitamin D3 down-modulates the production of proinflammatory cytokines and nitric oxide and enhances the phosphorylation of monocyte-expressed STAT6 at the recent-onset type 1 diabetes. Immunol Lett. 2016;179:122–130.
  • Dulla YA, Kurauchi Y, Hisatsune A, et al. Regulatory mechanisms of vitamin D3 on production of nitric oxide and pro-inflammatory cytokines in microglial BV-2 cells. Neurochem Res. 2016;41:2848–2858.
  • La Flamme AC, Patton EA, Bauman B, et al. IL-4 plays a crucial role in regulating oxidative damage in the liver during schistosomiasis. J Immunol. 2001;166(3):1903–1911.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.