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2019 | 2 | 1 | 7-22
Article title

Multiple sclerosis – new therapeutic directions

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Abstracts
EN
Multiple sclerosis (MS) is a chronic inflammatory and neurodegenerative disease which affects the central nervous system. Currently, there are numerous disease-modifying therapies for this condition. Most of them address the inflammatory aspects of the disease and are most effective in the relapsing-remitting stages of multiple sclerosis. However, none of them can completely stop the progression of MS and they are usually associated with adverse effects. There is an ongoing search for novel approaches that involve different modes of action. Here, we discuss examples of new immunomodulating agents such as antigen-specific therapies, neuroprotectants, regenerative strategies and gut microbiota modification.
Year
Volume
2
Issue
1
Pages
7-22
Physical description
Dates
published
2019-06-04
received
2019-03-18
accepted
2019-05-23
Contributors
References
  • Weinshenker BG. The natural history of multiple sclerosis. Neurol Clin [Internet]. 1995;13(1):119–46. Available from: http://search.ebscohost.com/login.aspx?direct=true&db=mdc&AN=7739500&lang=pl&site=eds-live.
  • The International Multiple Sclerosis Genetics Consortium & The Wellcome Trust Case Control Consortium, Sawcer S, Hellenthal G, Pirinen M, Spencer CCA, Patsopoulos NA, et al. Genetic risk and a primary role for cell-mediated immune mechanisms in multiple sclerosis. Nature [Internet]. 2011;476:214. Available from: https://doi.org/10.1038/nature10251.
  • Correale J, Gaitán MI. Multiple sclerosis and environmental factors: the role of vitamin D, parasites, and Epstein-Barr virus infection. Acta Neurol Scand [Internet]. 2015;132:46–55. Available from: http://doi.wiley.com/10.1111/ane.12431.
  • Yadav SK, Mindur JE, Ito K, Dhib-Jalbut S. Advances in the immunopathogenesis of multiple sclerosis. Curr Opin Neurol [Internet]. 2015;28(3):206–19. Available from: http://content.wkhealth.com/linkback/openurl?sid=WKPTLP:landingpage&an=00019052-201506000-00002.
  • Zhang Q, Vignali DAA. Co-stimulatory and Co-inhibitory Pathways in Autoimmunity. Immunity [Internet]. 2016;44(5):1034–51. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1074761316301467.
  • Claes N, Fraussen J, Stinissen P, Hupperts R, Somers V. B Cells Are Multifunctional Players in Multiple Sclerosis Pathogenesis: Insights from Therapeutic Interventions. Front Immunol [Internet]. 2015;6:642. Available from: http://journal.frontiersin.org/Article/10.3389/fimmu.2015.00642/abstract.
  • Riedhammer C, Weissert R. Antigen Presentation, Autoantigens, and Immune Regulation in Multiple Sclerosis and Other Autoimmune Diseases. Front Immunol [Internet]. 2015;6:322. Available from: http://journal.frontiersin.org/Article/10.3389/fimmu.2015.00322/abstract.
  • Juryńczyk M, Walczak A, Jurewicz A, Jesionek-Kupnicka D, Szczepanik M, Selmaj K. Immune regulation of multiple sclerosis by transdermally applied myelin peptides. Ann Neurol [Internet]. 2010;68(5):593–601. Available from: http://doi.wiley.com/10.1002/ana.22219
  • Walczak A, Siger M, Ciach A, Szczepanik M, Selmaj K. Transdermal Application of Myelin Peptides in Multiple Sclerosis Treatment. JAMA Neurol [Internet]. 2013;70(9):1105. Available from: http://archneur.jamanetwork.com/article.aspx?-doi=10.1001/jamaneurol.2013.3022.
  • Flórez-Grau G, Zubizarreta I, Cabezón R, Villoslada P, Benitez-Ribas D. Tolerogenic Dendritic Cells as a Promising Antigen-Specific Therapy in the Treatment of Multiple Sclerosis and Neuromyelitis Optica From Preclinical to Clinical Trials. Front Immunol [Internet]. 2018;9. Available from: https://www.frontiersin.org/article/10.3389/fimmu.2018.01169/full.
  • Papenfuss TL, Powell ND, McClain MA, Bedarf A, Singh A, Gienapp IE, et al. Estriol generates tolerogenic dendritic cells in vivo that protect against autoimmunity. J Immunol. 2011;186(6):3346–55.
  • Mansilla MJ, Sellès‐Moreno C, Fàbregas‐Puig S, Amoedo J, Navarro‐Barriuso J, Teniente‐Serra A, et al. Beneficial effect of tolerogenic dendritic cells pulsed with MOG autoantigen in experimental autoimmune encephalomyelitis. CNS Neurosci Ther. 2015;21(3):222–30.
  • Xie Z-X, Zhang H-L, Wu X-J, Zhu J, Ma D-H, Jin T. Role of the Immunogenic and Tolerogenic Subsets of Dendritic Cells in Multiple Sclerosis. Mediators Inflamm [Internet]. 2015;2015:1–20. Available from: http://www.hindawi.com/journals/mi/2015/513295/.
  • Raϊch-Regué D, Grau-López L, Naranjo-Gómez M, Ramo-Tello C, Pujol-Borrell R, Martínez-Cáceres E, et al. Stable antigen-specific T-cell hyporesponsiveness induced by tolerogenic dendritic cells from multiple sclerosis patients. Eur J Immunol [Internet]. 2012;42(3):771–82. Available from: http://doi.wiley.com/10.1002/eji.201141835.
  • Gross CC, Jonuleit H, Wiendl H. Fulfilling the dream: tolerogenic dendritic cells to treat multiple sclerosis. Eur J Immunol [Internet]. 2012;42(3):569–72. Available from: http://doi.wiley.com/10.1002/eji.201242402
  • Lutterotti A, Yousef S, Sputtek A, Sturner KH, Stellmann J-P, Breiden P, et al. Antigen-Specific Tolerance by Autologous Myelin Peptide-Coupled Cells: A Phase 1 Trial in Multiple Sclerosis. Sci Transl Med [Internet]. 2013;5(188):188ra75-188ra75. Available from: http://stm.sciencemag.org/cgi/doi/10.1126/scitranslmed.3006168.
  • Turley DM, Miller SD. Peripheral Tolerance Induction Using Ethylenecarbodiimide-Fixed APCs Uses both Direct and Indirect Mechanisms of Antigen Presentation for Prevention of Experimental Autoimmune Encephalomyelitis. J Immunol [Internet]. 2007;178(4):2212–20. Available from: http://www.jimmunol.org/cgi/doi/10.4049/jimmunol.178.4.2212.
  • Jenkins MK. Antigen presentation by chemically modified splenocytes induces antigen- specific T cell unresponsiveness in vitro and in vivo. J Exp Med [Internet]. 1987;165(2):302–19. Available from: http://www.jem.org/cgi/doi/10.1084/jem.165.2.302.
  • Getts DR, Turley DM, Smith CE, Harp CT, McCarthy D, Feeney EM, et al. Tolerance Induced by Apoptotic Antigen-Coupled Leukocytes Is Induced by PD-L1+ and IL-10-Producing Splenic Macrophages and Maintained by T Regulatory Cells. J Immunol [Internet]. 2011;187(5):2405–17. Available from: http://www.jimmunol.org/cgi/doi/10.4049/jimmunol.1004175.
  • Garren H, Robinson WH, Krasulová E, Havrdová E, Nadj C, Selmaj K, et al. Phase 2 trial of a DNA vaccine encoding myelin basic protein for multiple sclerosis. Ann Neurol [Internet]. 2008;63(5):611–20. Available from: http://doi.wiley.com/10.1002/ana.21370.
  • Bar-Or A, Vollmer T, Antel J, Arnold DL, Bodner CA, Campagnolo D, et al. Induction of Antigen-Specific Tolerance in Multiple Sclerosis After Immunization With DNA Encoding Myelin Basic Protein in a Randomized, Placebo-Controlled Phase 1/2 Trial. Arch Neurol [Internet]. 2007;64(10):1407. Available from: http://archneur.jamanetwork.com/article.aspx?doi=10.1001/archneur.64.10.nct70002.
  • Vandenbark AA, Chou YK, Whitham R, Mass M, Buenafe A, Liefeld D, et al. Treatment of multiple sclerosis with T–cell receptor peptides: Results of a double–blind pilot trial. Nat Med [Internet]. 1996;2(10):1109–15. Available from: http://www.nature.com/articles/nm1096-1109.
  • Vandenbark AA, Culbertson NE, Bartholomew RM, Huan J, Agotsch M, LaTocha D, et al. Therapeutic vaccination with a trivalent T-cell receptor (TCR) peptide vaccine restores deficient FoxP3 expression and TCR recognition in subjects with multiple sclerosis. Immunology [Internet]. 2008;123(1):66–78. Available from: http://doi.wiley.com/10.1111/j.1365-2567.2007.02703.x.
  • Vandenbark A. TCR Peptide Vaccination in Multiple Sclerosis: Boosting a Deficient Natural Regulatory Network that may Involve TCR-Specific CD4+CD25+ Treg Cells. Curr Drug Target -Inflammation Allergy [Internet]. 2005;4(2):217–29. Available from: http://www.eurekaselect.com/openurl/content.php?genre=article&issn=1568-010X&volume=4&issue=2&spage=217.
  • Streeter HB, Rigden R, Martin KF, Scolding NJ, Wraith DC. Preclinical development and first-in-human study of ATX-MS-1467 for immunotherapy of MS. Neurol - Neuroimmunol Neuroinflammation [Internet]. 2015;2(3):e93. Available from: http://nn.neurology.org/lookup/doi/10.1212/NXI.0000000000000093.
  • Chataway J, Martin K, Barrell K, Sharrack B, Stolt P, Wraith DC. Effects of ATX-MS-1467 immunotherapy over 16 weeks in relapsing multiple sclerosis. Neurology [Internet]. 2018;90(11):e955–62. Available from: http://www.neurology.org/lookup/doi/10.1212/WNL.0000000000005118.
  • Belogurov A, Zakharov K, Lomakin Y, Surkov K, Avtushenko S, Kruglyakov P, et al. CD206-Targeted Liposomal Myelin Basic Protein Peptides in Patients with Multiple Sclerosis Resistant to First-Line Disease-Modifying Therapies: A First-in-Human, Proof-of-Concept Dose-Escalation Study. Neurotherapeutics [Internet]. 2016;13(4):895–904. Available from: http://link.springer.com/10.1007/s13311-016-0448-0.
  • Belogurov AA, Stepanov A V., Smirnov I V., Melamed D, Bacon A, Mamedov AE, et al. Liposome-encapsulated peptides protect against experimental allergic encephalitis. FASEB J [Internet]. 2013;27(1):222–31. Available from: http://www.fasebj.org/doi/10.1096/fj.12-213975.
  • Bielekova B, Goodwin B, Richert N, Cortese I, Kondo T, Afshar G, et al. Encephalitogenic potential of the myelin basic protein peptide (amino acids 83–99) in multiple sclerosis: Results of a phase II clinical trial with an altered peptide ligand. Nat Med [Internet]. 2000;6(10):1167–75. Available from: http://www.nature.com/articles/nm1000_1167.
  • Zhang JZ, Rivera VM, Tejada-Simon M V., Yang D, Hong J, Li S, et al. T cell vaccination in multiple sclerosis: results of a preliminary study. J Neurol [Internet]. 2002;249(2):212–8. Available from: http://link.springer.com/10.1007/PL00007867.
  • Karussis D, Shor H, Yachnin J, Lanxner N, Amiel M, Baruch K, et al. T Cell Vaccination Benefits Relapsing Progressive Multiple Sclerosis Patients: A Randomized, Double-Blind Clinical Trial. Basso AS, editor. PLoS One [Internet]. 2012;7(12):e50478. Available from: https://dx.plos.org/10.1371/journal.pone.0050478.
  • Van der AA A, Hellings N, Medaer R, Gelin G, Palmers Y, Raus J, et al. T cell vaccination in multiple sclerosis patients with autologous CSF-derived activated T cells: results from a pilot study. Clin Exp Immunol [Internet]. 2003;131(1):155–68. Available from: http://doi.wiley.com/10.1046/j.1365-2249.2003.02019.x.
  • Loftus B, Newsom B, Montgomery M, Von Gynz-Rekowski K, Riser M, Inman S, et al. Autologous attenuated T-cell vaccine (Tovaxin®) dose escalation in multiple sclerosis relapsing–remitting and secondary progressive patients nonresponsive to approved immunomodulatory therapies. Clin Immunol [Internet]. 2009 May;131(2):202–15. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1521661609000072.
  • Foale S, Berry M, Logan A, Fulton D, Ahmed Z. LINGO-1 and AMIGO3, potential therapeutic targets for neurological and dysmyelinating disorders? Neural Regen Res [Internet]. 2017;12(8):1247. Available from: http://www.nrronline.org/text.asp?2017/12/8/1247/213538.
  • Mi S, Hu B, Hahm K, Luo Y, Kam Hui ES, Yuan Q, et al. LINGO-1 antagonist promotes spinal cord remyelination and axonal integrity in MOG-induced experimental autoimmune encephalomyelitis. Nat Med [Internet]. 2007;13(10):1228–33. Available from: http://www.nature.com/articles/nm1664.
  • Sun J-J, Ren Q-G, Xu L, Zhang Z-J. LINGO-1 antibody ameliorates myelin impairment and spatial memory deficits in experimental autoimmune encephalomyelitis mice. Sci Rep [Internet]. 2015;5(1):14235. Available from: http://www.nature.com/articles/srep14235.
  • Klistorner A, Chai Y, Leocani L, Albrecht P, Aktas O, Butzkueven H, et al. Assessment of Opicinumab in Acute Optic Neuritis Using Multifocal Visual Evoked Potential. CNS Drugs [Internet]. 2018;32(12):1159–71. Available from: http://link.springer.com/10.1007/s40263-018-0575-8.
  • Cadavid D, Balcer L, Galetta S, Aktas O, Ziemssen T, Vanopdenbosch L, et al. Safety and efficacy of opicinumab in acute optic neuritis (RENEW): a randomised, placebo-controlled, phase 2 trial. Lancet Neurol [Internet]. 2017;16(3):189–99. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1474442216303775.
  • Mellion M, Edwards KR, Hupperts R, Drulović J, Montalban X, Hartung H-P, et al. Efficacy Results from the Phase 2b SYNERGY Study: Treatment of Disabling Multiple Sclerosis with the Anti-LINGO-1 Monoclonal Antibody Opicinumab (S33.004). Neurology [Internet]. 2017;88(16 Supplement):S33.004. Available from: http://n.neurology.org/content/88/16_Supplement/S33.004.abstract.
  • McCroskery P, Selmaj K, Fernandez O, Grimaldi LME, Silber E, Pardo G, et al. Safety and Tolerability of Opicinumab in Relapsing Multiple Sclerosis: the Phase 2b SYNERGY Trial (P5.369). Neurology [Internet]. 2017;88(16 Supplement):P5.369. Available from: http://n.neurology.org/content/88/16_Supplement/P5.369.abstract.
  • Bieber AJ, Warrington A, Asakura K, Ciric B, Kaveri S V, Pease LR, et al. Human antibodies accelerate the rate of remyelination following lysolecithin-induced demyelination in mice. Glia [Internet]. 2002;37(3):241–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11857682.
  • Warrington AE, Bieber AJ, Ciric B, Pease LR, Van Keulen V, Rodriguez M. A recombinant human IgM promotes myelin repair after a single, very low dose. J Neurosci Res [Internet]. 2007;85(5):967–76. Available from: http://doi.wiley.com/10.1002/jnr.21217.
  • Watzlawik J, Holicky E, Edberg DD, Marks DL, Warrington AE, Wright BR, et al. Human remyelination promoting antibody inhibits apoptotic signaling and differentiation through Lyn kinase in primary rat oligodendrocytes. Glia [Internet]. 2010;58(15):1782–93. Available from: http://doi.wiley.com/10.1002/glia.21048.
  • An Intravenous Infusion Study of rHIgM22 in Patients With Multiple Sclerosis. Clinical Trials Identifier: NCT01803867 [Internet]. [cited 2019 Mar 14]. Available from: https://clinicaltrials.gov/ct2/show/NCT01803867.
  • An Intravenous Infusion Study of rHIgM22 in Patients With Multiple Sclerosis Immediately Following a Relapse. ClinicalTrials.gov Identifier: NCT02398461 [Internet]. [cited 2019 Mar 14]. Available from: https://clinicaltrials.gov/ct2/show/NCT02398461.
  • Wootla B, Denic A, Watzlawik JO, Warrington AE, Rodriguez M. A single dose of a neuron-binding human monoclonal antibody improves brainstem NAA concentrations, a biomarker for density of spinal cord axons, in a model of progressive multiple sclerosis. J Neuroinflammation [Internet]. 2015;12(1):83. Available from: http://www.jneuroinflammation.com/content/12/1/83.
  • Cho YK, Kim G, Park S, Sim JH, Won YJ, Hwang CH, et al. Erythropoietin promotes oligodendrogenesis and myelin repair following lysolecithin-induced injury in spinal cord slice culture. Biochem Biophys Res Commun [Internet]. 2012;417(2):753–9. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0006291X11022388.
  • Gyetvai G, Hughes T, Wedmore F, Roe C, Heikal L, Ghezzi P, et al. Erythropoietin Increases Myelination in Oligodendrocytes: Gene Expression Profiling Reveals Early Induction of Genes Involved in Lipid Transport and Metabolism. Front Immunol [Internet]. 2017;8. Available from: http://journal.frontiersin.org/article/10.3389/fimmu.2017.01394/full.
  • Ehrenreich H, Fischer B, Norra C, Schellenberger F, Stender N, Stiefel M, et al. Exploring recombinant human erythropoietin in chronic progressive multiple sclerosis. Brain [Internet]. 2007 Oct;130(10):2577–88. Available from: https://academic.oup.com/brain/article-lookup/doi/10.1093/brain/awm203.
  • Schreiber K, Magyari M, Sellebjerg F, Iversen P, Garde E, Madsen CG, et al. High-dose erythropoietin in patients with progressive multiple sclerosis: a randomized, placebo-controlled, phase 2 trial. Mult Scler J. 2017;23(5):675–85.
  • Mameli G, Madeddu G, Mei A, Uleri E, Poddighe L, Delogu LG, et al. Activation of MSRV-type endogenous retroviruses during infectious mononucleosis and Epstein-Barr virus latency: the missing link with multiple sclerosis? PLoS One [Internet]. 2013 Nov 13;8(11):e78474–e78474. Available from: http://search.ebscohost.com/login.aspx?direct=true&db=mdc&AN=24236019&lang=pl&site=eds-live.
  • Dolei A. The aliens inside us: HERV-W endogenous retroviruses and multiple sclerosis. Mult Scler J [Internet]. 2018;24(1):42–7. Available from: http://journals.sagepub.com/doi/10.1177/1352458517737370.
  • Clinical Trial Assessing the HERV-W Env Antagonist GNbAC1 for Efficacy in MS (CHANGE-MS). Clinical Trials.gov Identifier: NCT02782858 [Internet]. [cited 2019 May 27]. Available from: https://clinicaltrials.gov/ct2/show/NCT02782858.
  • Daniel Kantor, MD. Update on CHANGE-MS: Clinical Trial Results for GNbAC1.Is the cause of MS within us?[Internet]. Practical Neurology. 2018 june [cited 2019 Mar 14]. Available from: https://practicalneurology.com/articles/2018-june/update-on-change-ms-clinical-trial-results-for-gnbac1.
  • Curtin F, Perron H, Kromminga A, Porchet H, Lang AB. Preclinical and early clinical development of GNbAC1, a humanized IgG4 monoclonal antibody targeting endogenous retroviral MSRV-Env protein. MAbs [Internet]. 2015;7(1):265–75. Available from: http://www.tandfonline.com/doi/full/10.4161/19420862.2014.985021.
  • Domperidone in Secondary Progressive Multiple Sclerosis (SPMS). ClinicalTrials.gov Identifier: NCT02308137 [Internet]. Available from: https://clinicaltrials.gov/ct2/show/NCT02308137.
  • Zhornitsky S, Yong VW, Weiss S, Metz LM. Prolactin in multiple sclerosis. Mult Scler J [Internet]. 2013;19(1):15–23. Available from: http://journals.sagepub.com/doi/10.1177/1352458512458555.
  • Zhornitsky S, Johnson TA, Metz LM, Weiss S, Yong V. Prolactin in combination with interferon-β reduces disease severity in an animal model of multiple sclerosis. J Neuroinflammation [Internet]. 2015;12(1):55. Available from: http://www.jneuroinflammation.com/content/12/1/55.
  • Laurenti L, Innocenti I, Autore F, Sica S, Efremov DG. New developments in the management of chronic lymphocytic leukemia: role of ofatumumab. Onco Targets Ther [Internet]. 2016;9:421–9. Available from: https://www.dovepress.com/new-developments-in-the-management-of-chronic-lymphocytic-leukemia-rol-peer-reviewed-article-OTT.
  • Quattrocchi E, Østergaard M, Taylor PC, van Vollenhoven RF, Chu M, Mallett S, et al. Safety of Repeated Open-Label Treatment Courses of Intravenous Ofatumumab, a Human Anti-CD20 Monoclonal Antibody, in Rheumatoid Arthritis: Results from Three Clinical Trials. Chopra A, editor. PLoS One [Internet]. 2016;11(6):e0157961. Available from: https://dx.plos.org/10.1371/journal.pone.0157961.
  • Sorensen PS, Lisby S, Grove R, Derosier F, Shackelford S, Havrdova E, et al. Safety and efficacy of ofatumumab in relapsing-remitting multiple sclerosis: A phase 2 study. Neurology [Internet]. 2014;82(7):573–81. Available from: http://www.neurology.org/cgi/doi/10.1212/WNL.0000000000000125.
  • Bar-Or A, Grove RA, Austin DJ, Tolson JM, VanMeter SA, Lewis EW, et al. Subcutaneous ofatumumab in patients with relapsing-remitting multiple sclerosis. Neurology [Internet]. 2018;90(20):e1805–14. Available from: http://www.neurology.org/lookup/doi/10.1212/WNL.0000000000005516.
  • Agius MA, Klodowska-Duda G, Maciejowski M, Potemkowski A, Li J, Patra K, et al. Safety and tolerability of inebilizumab (MEDI-551), an anti-CD19 monoclonal antibody, in patients with relapsing forms of multiple sclerosis: Results from a phase 1 randomised, placebo-controlled, escalating intravenous and subcutaneous dose study. Mult Scler J [Internet]. 2019;25(2):235–45. Available from: http://journals.sagepub.com/doi/10.1177/1352458517740641.
  • Silk M, Nantz E. Efficacy and Safety of Tabalumab in Patients with Relapsing-Remitting Multiple Sclerosis: A Randomized, Double-Blind, Placebo-Controlled Study (P3.397). Neurology [Internet]. 2018;90(15 Supplement):P3.397. Available from: http://n.neurology.org/content/90/15_Supplement/P3.397.abstract.
  • Kolbinger F, Huppertz C, Mir A, Padova F. IL-17A and Multiple Sclerosis: Signaling Pathways, Producing Cells and Target Cells in the Central Nervous System. Curr Drug Targets [Internet]. 2016;17(16):1882–93. Available from: http://www.eurekaselect.com/openurl/content.php?genre=article&issn=1389-4501&volume=17&issue=16&spage=1882.
  • Cingoz O. Ustekinumab. MAbs [Internet]. 2009;1(3):216–21. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20069753.
  • Hart BA t., Brok HPM, Remarque E, Benson J, Treacy G, Amor S, et al. Suppression of Ongoing Disease in a Nonhuman Primate Model of Multiple Sclerosis by a Human-Anti-Human IL-12p40 Antibody. J Immunol [Internet]. 2005;175(7):4761–8. Available from: http://www.jimmunol.org/cgi/doi/10.4049/jimmunol.175.7.4761.
  • Brok HPM, van Meurs M, Blezer E, Schantz A, Peritt D, Treacy G, et al. Prevention of Experimental Autoimmune Encephalomyelitis in Common Marmosets Using an Anti-IL-12p40 Monoclonal Antibody. J Immunol [Internet]. 2002;169(11):6554–63. Available from: http://www.jimmunol.org/cgi/doi/10.4049/jimmunol.169.11.6554.
  • Segal BM, Constantinescu CS, Raychaudhuri A, Kim L, Fidelus-Gort R, Kasper LH. Repeated subcutaneous injections of IL12/23 p40 neutralising antibody, ustekinumab, in patients with relapsing-remitting multiple sclerosis: a phase II, double-blind, placebo-controlled, randomised, dose-ranging study. Lancet Neurol [Internet]. 2008;7(9):796–804. Available from: https://linkinghub.elsevier.com/retrieve/pii/S147444220870173X.
  • Longbrake EE, Racke MK. Why did IL-12/IL-23 antibody therapy fail in multiple sclerosis? Expert Rev Neurother [Internet]. 2009;9(3):319–21. Available from: http://www.tandfonline.com/doi/full/10.1586/14737175.9.3.319.
  • Havrdová E, Belova A, Goloborodko A, Tisserant A, Wright A, Wallstroem E, et al. Activity of secukinumab, an anti-IL-17A antibody, on brain lesions in RRMS: results from a randomized, proof-of-concept study. J Neurol [Internet]. 2016;263(7):1287–95. Available from: http://link.springer.com/10.1007/s00415-016-8128-x.
  • Serada S, Fujimoto M, Mihara M, Koike N, Ohsugi Y, Nomura S, et al. IL-6 blockade inhibits the induction of myelin antigen-specific Th17 cells and Th1 cells in experimental autoimmune encephalomyelitis. Proc Natl Acad Sci [Internet]. 2008;105(26):9041–6. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas.0802218105.
  • Beauchemin P, Carruthers R. MS arising during Tocilizumab therapy for rheumatoid arthritis. Mult Scler J [Internet]. 2016;22(2):254–6. Available from: http://journals.sagepub.com/doi/10.1177/1352458515623862.
  • Codarri L, Gyülvészi G, Tosevski V, Hesske L, Fontana A, Magnenat L, et al. RORγt drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat Immunol [Internet]. 2011;12(6):560–7. Available from: http://www.nature.com/articles/ni.2027.
  • Li R, Rezk A, Miyazaki Y, Hilgenberg E, Touil H, Shen P, et al. Proinflammatory GM-CSF–producing B cells in multiple sclerosis and B cell depletion therapy. Sci Transl Med [Internet]. 2015;7(310):310ra166-310ra166. Available from: http://stm.sciencemag.org/lookup/doi/10.1126/scitranslmed.aab4176.
  • Constantinescu CS, Asher A, Fryze W, Kozubski W, Wagner F, Aram J, et al. Randomized phase 1b trial of MOR103, a human antibody to GM-CSF, in multiple sclerosis. Neurol - Neuroimmunol Neuroinflammation [Internet]. 2015;2(4):e117. Available from: http://nn.neurology.org/lookup/doi/10.1212/NXI.0000000000000117.
  • Waxman SG. Mechanisms of Disease: sodium channels and neuroprotection in multiple sclerosis-current status. Nat Clin Pract Neurol [Internet]. 2008;4(3):159–69. Available from: http://www.nature.com/articles/ncpneuro0735.
  • Dutta R, Trapp BD. Mechanisms of neuronal dysfunction and degeneration in multiple sclerosis. Prog Neurobiol [Internet]. 2011;93(1):1–12. Available from: https://linkinghub.elsevier.com/retrieve/pii/S030100821000170X.
  • Kapoor R, Furby J, Hayton T, Smith KJ, Altmann DR, Brenner R, et al. Lamotrigine for neuroprotection in secondary progressive multiple sclerosis: a randomised, double-blind, placebo-controlled, parallel-group trial. Lancet Neurol [Internet]. 2010;9(7):681–8. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1474442210701319.
  • Gnanapavan S, Grant D, Morant S, Furby J, Hayton T, Teunissen CE, et al. Biomarker Report from the Phase II Lamotrigine Trial in Secondary Progressive MS – Neurofilament as a Surrogate of Disease Progression. Derfuss T, editor. PLoS One [Internet]. 2013;8(8):e70019. Available from: https://dx.plos.org/10.1371/journal.pone.0070019.
  • Raftopoulos R, Hickman SJ, Toosy A, Sharrack B, Mallik S, Paling D, et al. Phenytoin for neuroprotection in patients with acute optic neuritis: a randomised, placebo-controlled, phase 2 trial. Lancet Neurol [Internet]. 2016;15(3):259–69. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1474442216000041.
  • Lidster K, Jackson SJ, Ahmed Z, Munro P, Coffey P, Giovannoni G, et al. Neuroprotection in a Novel Mouse Model of Multiple Sclerosis. Villoslada P, editor. PLoS One [Internet]. 2013;8(11):e79188. Available from: https://dx.plos.org/10.1371/journal.pone.0079188.
  • Cheah BC, Vucic S, Krishnan A V, Kiernan MC. Riluzole, neuroprotection and amyotrophic lateral sclerosis. Curr Med Chem [Internet]. 2010;17(18):1942–199. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20377511.
  • Connick P, De Angelis F, Parker RA, Plantone D, Doshi A, John N, et al. Multiple Sclerosis-Secondary Progressive Multi-Arm Randomisation Trial (MS-SMART): a multiarm phase IIb randomised, double-blind, placebo-controlled clinical trial comparing the efficacy of three neuroprotective drugs in secondary progressive multiple scl. BMJ Open [Internet]. 2018;8(8):e021944. Available from: http://bmjopen.bmj.com/lookup/doi/10.1136/bmjopen-2018-021944.
  • Morsali D, Bechtold D, Lee W, Chauhdry S, Palchaudhuri U, Hassoon P, et al. Safinamide and flecainide protect axons and reduce microglial activation in models of multiple sclerosis. Brain [Internet]. 2013;136(4):1067–82. Available from: https://academic.oup.com/brain/article-lookup/doi/10.1093/brain/awt041.
  • McKee JB, Cottriall CL, Elston J, Epps S, Evangelou N, Gerry S, et al. Amiloride does not protect retinal nerve fibre layer thickness in optic neuritis in a phase 2 randomised controlled trial. Mult Scler J [Internet]. 2019;25(2):246–55. Available from: http://journals.sagepub.com/doi/10.1177/1352458517742979.
  • Zhang F, Zhou H, Wilson BC, Shi J-S, Hong J-S, Gao H-M. Fluoxetine protects neurons against microglial activation-mediated neurotoxicity. Parkinsonism Relat Disord [Internet]. 2012;18:S213–7. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1353802011700669.
  • Cambron M, Mostert J, Haentjens P, D’Hooghe M, Nagels G, Willekens B, et al. Fluoxetine in Progressive Multiple Sclerosis (FLUOX-PMS): study protocol for a randomized controlled trial. Trials [Internet]. 2014;15(1):37. Available from: https://trialsjournal.biomedcentral.com/articles/10.1186/1745-6215-15-37.
  • Comi G. CONCERTO: a placebo-controlled trial of oral laquinimod in patients with relapsing-remitting multiple sclerosis [Internet]. ECTRIMS Online Library. 2017 [cited 2019 Mar 14]. Available from: concerto: a placebo-controlled trial of oral laquinimod in patients with relapsing-remitting multiple sclerosis.
  • A Phase 2 Clinical Study in Subjects With Primary Progressive Multiple Sclerosis to Assess the Efficacy, Safety and Tolerability of Two Oral Doses of Laquinimod Either of 0.6 mg/Day or 1.5mg/Day (Experimental Drug) as Compared to Placebo. ClinicalTrials.g [Internet]. [cited 2019 Mar 14]. Available from: https://clinicaltrials.gov/ct2/show/NCT02284568.
  • Mishra MK, Wang J, Keough MB, Fan Y, Silva C, Sloka S, et al. Laquinimod reduces neuroaxonal injury through inhibiting microglial activation. Ann Clin Transl Neurol [Internet]. 2014;1(6):409–22. Available from: http://doi.wiley.com/10.1002/acn3.67.
  • Wilmes AT, Reinehr S, Kühn S, Pedreiturria X, Petrikowski L, Faissner S, et al. Laquinimod protects the optic nerve and retina in an experimental autoimmune encephalomyelitis model. J Neuroinflammation [Internet]. 2018;15(1):183. Available from: https://jneuroinflammation.biomedcentral.com/articles/10.1186/s12974-018-1208-3.
  • Gentile A, Musella A, De Vito F, Fresegna D, Bullitta S, Rizzo FR, et al. Laquinimod ameliorates excitotoxic damage by regulating glutamate re-uptake. J Neuroinflammation [Internet]. 2018;15(1):5. Available from: https://jneuroinflammation.biomedcentral.com/articles/10.1186/s12974-017-1048-6.
  • Tikka TM, Koistinaho JE. Minocycline Provides Neuroprotection Against N-Methyl-D-aspartate Neurotoxicity by Inhibiting Microglia. J Immunol [Internet]. 2001;166(12):7527–33. Available from: http://www.jimmunol.org/cgi/doi/10.4049/jimmunol.166.12.7527.
  • Yang Y, Salayandia VM, Thompson JF, Yang LY, Estrada EY, Yang Y. Attenuation of acute stroke injury in rat brain by minocycline promotes blood–brain barrier remodeling and alternative microglia/macrophage activation during recovery. J Neuroinflammation [Internet]. 2015;12(1):26. Available from: http://www.jneuroinflammation.com/content/12/1/26.
  • Metz LM, Li DKB, Traboulsee AL, Duquette P, Eliasziw M, Cerchiaro G, et al. Trial of Minocycline in a Clinically Isolated Syndrome of Multiple Sclerosis. N Engl J Med [Internet]. 2017 Jun;376(22):2122–33. Available from: http://www.jneuroinflammation.com/content/12/1/26.
  • Cho Y, Crichlow G V., Vermeire JJ, Leng L, Du X, Hodsdon ME, et al. Allosteric inhibition of macrophage migration inhibitory factor revealed by ibudilast. Proc Natl Acad Sci [Internet]. 2010;107(25):11313–8. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.1002716107.
  • Mizuno T, Kurotani T, Komatsu Y, Kawanokuchi J, Kato H, Mitsuma N, et al. Neuroprotective role of phosphodiesterase inhibitor ibudilast on neuronal cell death induced by activated microglia. Neuropharmacology [Internet]. 2004;46(3):404–11. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0028390803003721.
  • Fox RJ, Coffey CS, Conwit R, Cudkowicz ME, Gleason T, Goodman A, et al. Phase 2 Trial of Ibudilast in Progressive Multiple Sclerosis. N Engl J Med [Internet]. 2018 Aug 30;379(9):846–55. Available from: http://www.nejm.org/doi/10.1056/NEJMoa1803583.
  • Su KG, Banker G, Bourdette D, Forte M. Axonal degeneration in multiple sclerosis: the mitochondrial hypothesis. Curr Neurol Neurosci Rep [Internet]. 2009;9(5):411–7. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19664372.
  • Dutta R, McDonough J, Yin X, Peterson J, Chang A, Torres T, et al. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol [Internet]. 2006;59(3):478–89. Available from: http://doi.wiley.com/10.1002/ana.20736.
  • Campbell GR, Ziabreva I, Reeve AK, Krishnan KJ, Reynolds R, Howell O, et al. Mitochondrial DNA deletions and neurodegeneration in multiple sclerosis. Ann Neurol [Internet]. 2011;69(3):481–92. Available from: http://doi.wiley.com/10.1002/ana.22109.
  • Sedel F, Bernard D, Mock DM, Tourbah A. Targeting demyelination and virtual hypoxia with high-dose biotin as a treatment for progressive multiple sclerosis. Neuropharmacology [Internet]. 2016;110:644–53. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0028390815300733.
  • Tourbah A, Lebrun-Frenay C, Edan G, Clanet M, Papeix C, Vukusic S, et al. MD1003 (high-dose biotin) for the treatment of progressive multiple sclerosis: A randomised, double-blind, placebo-controlled study. Mult Scler J [Internet]. 2016;22(13):1719–31. Available from: http://journals.sagepub.com/doi/10.1177/1352458516667568.
  • Tourbah A, Gout O, Vighetto A, Deburghgraeve V, Pelletier J, Papeix C, et al. MD1003 (High-Dose Pharmaceutical-Grade Biotin) for the Treatment of Chronic Visual Loss Related to Optic Neuritis in Multiple Sclerosis: A Randomized, Double-Blind, Placebo-Controlled Study. CNS Drugs [Internet]. 2018;32(7):661–72. Available from: http://journals.sagepub.com/doi/10.1177/1352458516667568.
  • Yu-Wai-Man P, Soiferman D, Moore DG, Burté F, Saada A. Evaluating the therapeutic potential of idebenone and related quinone analogues in Leber hereditary optic neuropathy. Mitochondrion [Internet]. 2017;36:36–42. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1567724917300120.
  • Kearney M, Orrell RW, Fahey M, Brassington R, Pandolfo M. Pharmacological treatments for Friedreich ataxia [Internet]. Cochrane Database of Systematic Reviews. 2016 [cited 2019 Mar 14]. Available from: http://doi.wiley.com/10.1002/14651858.CD007791.pub4.
  • Parkinson MH, Schulz JB, Giunti P. Co-enzyme Q 10 and idebenone use in Friedreich’s ataxia. J Neurochem [Internet]. 2013;126:125–41. Available from: http://doi.wiley.com/10.1111/jnc.12322.
  • Idebenone for Primary Progressive Multiple Sclerosis. ClinicalTrials.gov Identifier: NCT01854359 [Internet]. [cited 2019 Mar 14]. Available from: https://clinicaltrials.gov/ct2/show/NCT01854359.
  • Mao P, Manczak M, Shirendeb UP, Reddy PH. MitoQ, a mitochondria-targeted antioxidant, delays disease progression and alleviates pathogenesis in an experimental autoimmune encephalomyelitis mouse model of multiple sclerosis. Biochim Biophys Acta – Mol Basis Dis [Internet]. 2013;1832(12):2322–31. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0925443913002846.
  • Biewenga GP, Haenen GRMM, Bast A. The pharmacology of the antioxidant lipoic acid. Gen Pharmacol Vasc Syst [Internet]. 1997;29(3):315–31. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0306362396004740.
  • Yadav V, Marracci G, Lovera J, Woodward W, Bogardus K, Marquardt W, et al. Lipoic acid in multiple sclerosis: a pilot study. Mult Scler J [Internet]. 2005 Apr 2;11(2):159–65. Available from: http://journals.sagepub.com/doi/10.1191/1352458505ms1143oa.
  • Spain R, Powers K, Murchison C, Heriza E, Winges K, Yadav V, et al. Lipoic acid in secondary progressive MS. Neurol - Neuroimmunol Neuroinflammation [Internet]. 2017;4(5):e374. Available from: http://nn.neurology.org/lookup/doi/10.1212/NXI.0000000000000374.
  • Danesh FR, Anel RL, Zeng L, Lomasney J, Sahai A, Kanwar YS. Immunomodulatory effects of HMG-CoA reductase inhibitors. Arch Immunol Ther Exp (Warsz) [Internet]. 2003;51(3):139–48. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12894868.
  • Chan D, Binks S, Nicholas JM, Frost C, Cardoso MJ, Ourselin S, et al. Effect of high-dose simvastatin on cognitive, neuropsychiatric, and health-related quality-of-life measures in secondary progressive multiple sclerosis: secondary analyses from the MS-STAT randomised, placebo-controlled trial. Lancet Neurol [Internet]. 2017;16(8):591–600. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1474442217301138.
  • Chataway J, Schuerer N, Alsanousi A, Chan D, MacManus D, Hunter K, et al. Effect of high-dose simvastatin on brain atrophy and disability in secondary progressive multiple sclerosis (MS-STAT): a randomised, placebo-controlled, phase 2 trial. Lancet [Internet]. 2014;383(9936):2213–21. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0140673613622424.
  • Sohn H-M, Hwang J-Y, Ryu J-H, Kim J, Park S, Park J, et al. Simvastatin protects ischemic spinal cord injury from cell death and cytotoxicity through decreasing oxidative stress: in vitro primary cultured rat spinal cord model under oxygen and glucose deprivation-reoxygenation conditions. J Orthop Surg Res [Internet]. 2017;12(1):36. Available from: http://josr-online.biomedcentral.com/articles/10.1186/s13018-017-0536-9.
  • van der Most PJ, Dolga AM, Nijholt IM, Luiten PGM, Eisel ULM. Statins: Mechanisms of neuroprotection. Prog Neurobiol [Internet]. 2009;88(1):64–75. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0301008209000318.
  • Kappos L, Bar-Or A, Cree BAC, Fox RJ, Giovannoni G, Gold R, et al. Siponimod versus placebo in secondary progressive multiple sclerosis (EXPAND): a double-blind, randomised, phase 3 study. Lancet [Internet]. 2018;391(10127):1263–73. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0140673618304756.
  • Gajofatto A. Spotlight on siponimod and its potential in the treatment of secondary progressive multiple sclerosis: the evidence to date. Drug Des Devel Ther [Internet]. 2017;Volume 11:3153–7. Available from: https://www.dovepress.com/spotlight-on-siponimod-and-its-potential-in-the-treatment-of-secondary-peer-reviewed-article-DDDT.
  • Jope RS, Yuskaitis CJ, Beurel E. Glycogen Synthase Kinase-3 (GSK3): Inflammation, Diseases, and Therapeutics. Neurochem Res [Internet]. 2007;32(4–5):577–95. Available from: http://link.springer.com/10.1007/s11064-006-9128-5.
  • De Sarno P, Axtell RC, Raman C, Roth KA, Alessi DR, Jope RS. Lithium Prevents and Ameliorates Experimental Autoimmune Encephalomyelitis. J Immunol [Internet]. 2008;181(1):338–45. Available from: http://www.jimmunol.org/cgi/doi/10.4049/jimmunol.181.1.338.
  • Rinker J., Meador W, Sung V, Nicholas A, Cutter G. Results of a pilot trial of lithium in progressive multiple sclerosis [Internet]. ECTRIMS Online Library. [cited 2019 Mar 14]. Available from: https://onlinelibrary.ectrims-congress.eu/ectrims/2016/32nd/145965/john.rinker.ii.results.of.a.pilot.trial.of.lithium.in.progressive.multiple.html.
  • Chu F, Shi M, Lang Y, Shen D, Jin T, Zhu J, et al. Gut Microbiota in Multiple Sclerosis and Experimental Autoimmune Encephalomyelitis: Current Applications and Future Perspectives. Mediators Inflamm [Internet]. 2018;2018:1–17. Available from: https://www.hindawi.com/journals/mi/2018/8168717/.
  • Islas Weinstein L, Revuelta A, Pando RH. Catecholamines and acetylcholine are key regulators of the interaction between microbes and the immune system. Ann N Y Acad Sci [Internet]. 2015;1351(1):39–51. Available from: http://doi.wiley.com/10.1111/nyas.12792.
  • Kim Y-K, Shin C. The Microbiota-Gut-Brain Axis in Neuropsychiatric Disorders: Pathophysiological Mechanisms and Novel Treatments. Curr Neuropharmacol [Internet]. 2018;16(5):559–73. Available from: http://www.eurekaselect.com/155613/article.
  • Ochoa-Repáraz J, Mielcarz DW, Haque-Begum S, Kasper LH. Induction of a regulatory B cell population in experimental allergic encephalomyelitis by alteration of the gut commensal microflora. Gut Microbes [Internet]. 2010 Mar 4;1(2):103–8. Available from: http://www.tandfonline.com/doi/abs/10.4161/gmic.1.2.11515.
  • Wang Y, Begum-Haque S, Telesford KM, Ochoa-Repáraz J, Christy M, Kasper EJ, et al. A commensal bacterial product elicits and modulates migratory capacity of CD39 + CD4 T regulatory subsets in the suppression of neuroinflammation. Gut Microbes [Internet]. 2014;5(4):552–61. Available from: http://www.tandfonline.com/doi/abs/10.4161/gmic.29797.
  • Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci [Internet]. 2011;108(Supplement 1):4615–22. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.1000082107.
  • Berer K, Gerdes LA, Cekanaviciute E, Jia X, Xiao L, Xia Z, et al. Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice. Proc Natl Acad Sci [Internet]. 2017;114(40):10719–24. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas.1711233114.
  • Chen J, Chia N, Kalari KR, Yao JZ, Novotna M, Paz Soldan MM, et al. Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls. Sci Rep [Internet]. 2016;6(1):28484. Available from: http://www.nature.com/articles/srep28484.
  • Kwon H-K, Kim G-C, Kim Y, Hwang W, Jash A, Sahoo A, et al. Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response. Clin Immunol [Internet]. 2013;146(3):217–27. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1521661613000028.
  • Kouchaki E, Tamtaji OR, Salami M, Bahmani F, Daneshvar Kakhaki R, Akbari E, et al. Clinical and metabolic response to probiotic supplementation in patients with multiple sclerosis: A randomized, double-blind, placebo-controlled trial. Clin Nutr [Internet]. 2017;36(5):1245–9. Available from: https://linkinghub.elsevier.com/retrieve/pii/S026156141630214X.
  • Makkawi S, Camara-Lemarroy C, Metz L. Fecal microbiota transplantation associated with 10 years of stability in a patient with SPMS. Neurol - Neuroimmunol Neuroinflammation [Internet]. 2018;5(4):e459. Available from: http://nn.neurology.org/lookup/doi/10.1212/NXI.0000000000000459.
  • Fecal Microbial Transplantation in Relapsing Multiple Sclerosis Patients. ClinicalTrials.gov Identifier: NCT03183869 [Internet]. [cited 2019 Mar 14]. Available from: https://clinicaltrials.gov/ct2/show/NCT03183869.
  • Correale J, Farez MF. The impact of parasite infections on the course of multiple sclerosis. J Neuroimmunol [Internet]. 2011;233(1–2):6–11. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0165572811000051.
  • Dixit A, Tanaka A, Greer JM, Donnelly S. Novel Therapeutics for Multiple Sclerosis Designed by Parasitic Worms. Int J Mol Sci [Internet]. 2017;18(10):2141. Available from: http://www.mdpi.com/1422-0067/18/10/2141.
  • Terrazas C, de Dios Ruiz-Rosado J, Amici SA, Jablonski KA, Martinez-Saucedo D, Webb LM, et al. Helminth-induced Ly6Chi monocyte-derived alternatively activated macrophages suppress experimental autoimmune encephalomyelitis. Sci Rep [Internet]. 2017;7(1):40814. Available from: http://www.nature.com/articles/srep40814.
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