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Systematic Review Article

Effects of High Efficacy Multiple Sclerosis Disease Modifying Drugs on the Immune Synapse: A Systematic Review

Author(s): Spyros N. Deftereos, George D. Vavougios, Christos Bakirtzis, George Hadjigeorgiou and Nikolaos Grigoriadis*

Volume 30, Issue 7, 2024

Published on: 09 February, 2024

Page: [536 - 551] Pages: 16

DOI: 10.2174/0113816128288102240131053205

Price: $65

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Abstract

Background: Co-signaling and adhesion molecules are important elements for creating immune synapses between T lymphocytes and antigen-presenting cells; they positively or negatively regulate the interaction between a T cell receptor with its cognate antigen, presented by the major histocompatibility complex.

Objectives: We conducted a systematic review on the effects of High Efficacy Disease Modifying Drugs (HEDMDs) for Multiple Sclerosis (MS) on the co-signaling and adhesion molecules that form the immune synapse.

Methods: We searched EMBASE, MEDLINE, and other sources to identify clinical or preclinical reports on the effects of HEDMDs on co-signaling and adhesion molecules that participate in the formation of immune synapses in patients with MS or other autoimmune disorders. We included reports on cladribine tablets, anti- CD20 monoclonal antibodies, S1P modulators, inhibitors of Bruton’s Tyrosine Kinase, and natalizumab.

Results: In 56 eligible reports among 7340 total publications, limited relevant evidence was uncovered. Not all co-signaling and adhesion molecules have been studied in relation to every HEDMD, with more data being available on the anti-CD20 monoclonal antibodies (that affect CD80, CD86, GITR and TIGIT), cladribine tablets (affecting CD28, CD40, ICAM-1, LFA-1) and the S1P modulators (affecting CD86, ICAM-1 and LFA-1) and less on Natalizumab (affecting CD80, CD86, CD40, LFA-1, VLA-4) and Alemtuzumab (affecting GITR and CTLA-4).

Conclusion: The puzzle of HEDMD effects on the immune synapse is far from complete. The available evidence suggests that distinguishing differences exist between drugs and are worth pursuing further.

Keywords: Multiple sclerosis, autoimmune disorders, disease modifying drugs, immune synapse, co-signaling molecules, adhesion molecules.

« Previous Next »
[1]
Freedman MS, Selchen D, Prat A, Giacomini PS. Managing multiple sclerosis: Treatment initiation, modification, and sequencing. Can J Neurol Sci 2018; 45(5): 489-503.
[http://dx.doi.org/10.1017/cjn.2018.17] [PMID: 29893652]
[2]
Stankiewicz JM, Weiner HL. An argument for broad use of high efficacy treatments in early multiple sclerosis. Neurol Neuroimmunol Neuroinflamm 2020; 7(1): e636.
[http://dx.doi.org/10.1212/NXI.0000000000000636] [PMID: 31757815]
[3]
Pipek LZ, Mahler JV, Nascimento RFV, Apóstolos-Pereira SL, Silva GD, Callegaro D. Cost, efficacy, and safety comparison between early intensive and escalating strategies for multiple sclerosis: A systematic review and meta-analysis. Mult Scler Relat Disord 2023; 71: 104581.
[http://dx.doi.org/10.1016/j.msard.2023.104581] [PMID: 36848839]
[4]
Le Page E, Edan G. Induction or escalation therapy for patients with multiple sclerosis? Rev Neurol 2018; 174(6): 449-57.
[http://dx.doi.org/10.1016/j.neurol.2018.04.004] [PMID: 29799415]
[5]
Bourre B, Casez O, Ciron J, et al. Paradigm shifts in multiple sclerosis management: Implications for daily clinical practice. Rev Neurol 2023; 179(4): 256-64.
[http://dx.doi.org/10.1016/j.neurol.2022.09.006]
[6]
Liu C, Zhu J, Mi Y, Jin T. Impact of disease-modifying therapy on dendritic cells and exploring their immunotherapeutic potential in multiple sclerosis. J Neuroinflammation 2022; 19(1): 298.
[http://dx.doi.org/10.1186/s12974-022-02663-z] [PMID: 36510261]
[7]
Kemmerer CL, Pernpeintner V, Ruschil C, et al. Differential effects of disease modifying drugs on peripheral blood B cell subsets: A cross sectional study in multiple sclerosis patients treated with interferon-β, glatiramer acetate, dimethyl fumarate, fingolimod or natalizumab. PLoS One 2020; 15(7): e0235449.
[http://dx.doi.org/10.1371/journal.pone.0235449] [PMID: 32716916]
[8]
Staun-Ram E, Miller A. Effector and regulatory B cells in multiple sclerosis. Clin Immunol 2017; 184: 11-25.
[http://dx.doi.org/10.1016/j.clim.2017.04.014] [PMID: 28461106]
[9]
Stuve O, Soelberg Soerensen P, Leist T, et al. Effects of cladribine tablets on lymphocyte subsets in patients with multiple sclerosis: An extended analysis of surface markers. Ther Adv Neurol Disord 2019; 12.
[http://dx.doi.org/10.1177/1756286419854986] [PMID: 31244898]
[10]
Sellner J, Rommer PS. Immunological consequences of “immune reconstitution therapy” in multiple sclerosis: A systematic review. Autoimmun Rev 2020; 19(4): 102492.
[http://dx.doi.org/10.1016/j.autrev.2020.102492] [PMID: 32062028]
[11]
Ibañez-Vega J, Vilchez C, Jimenez K, Guevara C, Burgos PI, Naves R. Cellular and molecular regulation of the programmed death-1/programmed death ligand system and its role in multiple sclerosis and other autoimmune diseases. J Autoimmun 2021; 123: 102702.
[http://dx.doi.org/10.1016/j.jaut.2021.102702] [PMID: 34311143]
[12]
Dustin ML. Cell adhesion molecules and actin cytoskeleton at immune synapses and kinapses. Curr Opin Cell Biol 2007; 19(5): 529-33.
[http://dx.doi.org/10.1016/j.ceb.2007.08.003] [PMID: 17923403]
[13]
The Cochrane Collaboration. Cochrane handbook for systematic reviews of interventions. 2011. Available from: https://training.cochrane.org/handbook/archive/v5.1/
[14]
Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. J Clin Epidemiol 2009; 62(10): e1-e34.
[http://dx.doi.org/10.1016/j.jclinepi.2009.06.006] [PMID: 19631507]
[15]
Moher D, Shamseer L, Clarke M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev 2015; 4(1): 1.
[http://dx.doi.org/10.1186/2046-4053-4-1] [PMID: 25554246]
[16]
Schneider R, Oh J. Bruton’s tyrosine kinase inhibition in multiple sclerosis. Curr Neurol Neurosci Rep 2022; 22(11): 721-34.
[http://dx.doi.org/10.1007/s11910-022-01229-z] [PMID: 36301434]
[17]
EMBASE. Available from: https://www.embase.com
[18]
Cochrane Database of Systematic Reviews. Available from: https://www.cochranelibrary.com/cdsr/reviews
[19]
Cochrane Central Register of Controlled Trials (CENTRAL). Available from: https://www.cochranelibrary.com/central
[20]
ECTRIMS Online Library. Available from: https://www.ectrims.eu/online-ms-information-resources/online-library-2/
[21]
American Academy of Neurology Annual Meetings. 2023. Available from: https://www.aan.com/events/annual-meeting
[22]
Kiapour N, Wu B, Wang Y, et al. Therapeutic effect of anti-CD52 monoclonal antibody in multiple sclerosis and its animal models is mediated via T regulatory cells. J Immunol Baltim Md 2022; 209(1): 49-56.
[http://dx.doi.org/10.4049/jimmunol.2100176] [PMID: 35750335]
[23]
Kim Y, Kim G, Shin HJ, et al. Restoration of regulatory B cell deficiency following alemtuzumab therapy in patients with relapsing multiple sclerosis. J Neuroinflammation 2018; 15(1): 300.
[http://dx.doi.org/10.1186/s12974-018-1334-y] [PMID: 30373595]
[24]
Ladwig A, Suh J, Roeth P, et al. Alemtuzumab induces changes in the innate immune system in patients with relapsing-remitting multiple sclerosis. Mult Scler J 2020; 26(S3): 259.
[25]
Medeiros-Furquim T, Ayoub S, Johnson LJ, et al. Cladribine treatment for MS preserves the differentiative capacity of subsequently generated monocytes, whereas its administration in vitro acutely influences monocyte differentiation but not microglial activation. Front Immunol 2022; 13: 678817.
[http://dx.doi.org/10.3389/fimmu.2022.678817] [PMID: 35734180]
[26]
Kraus SHP, Luessi F, Trinschek B, et al. Cladribine exerts an immunomodulatory effect on human and murine dendritic cells. Int Immunopharmacol 2014; 18(2): 347-57.
[http://dx.doi.org/10.1016/j.intimp.2013.11.027] [PMID: 24316255]
[27]
Ford RK, Juillard P, Hawke S, Grau GE, Marsh-Wakefield F. Cladribine reduces trans-endothelial migration of memory T cells across an in vitro blood-brain barrier. J Clin Med 2022; 11(20): 6006.
[http://dx.doi.org/10.3390/jcm11206006] [PMID: 36294327]
[28]
Moser T, Hoepner L, Schwenker K, et al. Cladribine alters immune cell surface molecules for adhesion and costimulation: Further insights to the mode of action in multiple sclerosis. Cells 2021; 10(11): 3116.
[http://dx.doi.org/10.3390/cells10113116] [PMID: 34831335]
[29]
Gammoh O, AlQudah A, Rob OAA, et al. Modulation of salivary ICAM-1 and SIRT1 by disease modifying drugs in undepressed relapsing-remitting multiple sclerosis patients. Mult Scler Relat Disord 2022; 68: 104257.
[http://dx.doi.org/10.1016/j.msard.2022.104257] [PMID: 36308972]
[30]
Feng Y, Feng F, Pan S, Zhang J, Li W. Fingolimod ameliorates chronic experimental autoimmune neuritis by modulating inflammatory cytokines and Akt/mTOR/NF-κB signaling. Brain Behav 2023; 13(4): e2965.
[http://dx.doi.org/10.1002/brb3.2965] [PMID: 36917739]
[31]
Li XK, Enosawa S, Kakefuda T, Amemiya H, Suzuki S. FTY720, a novel immunosuppressive agent, enhances upregulation of the cell adhesion molecular ICAM-1 in TNF-a treated human umbilical vein endothelial cells. Transplant Proc 1997; 29(1-2): 1265-6.
[http://dx.doi.org/10.1016/S0041-1345(96)00491-5] [PMID: 9123298]
[32]
Mathias A, Perriot S, Canales M, et al. Impaired T-cell migration to the CNS under fingolimod and dimethyl fumarate. Neurol Neuroimmunol Neuroinflamm 2017; 4(6): e401.
[http://dx.doi.org/10.1212/NXI.0000000000000401] [PMID: 29075657]
[33]
Tuzun E, Ulusoy CA, Turan S, et al. Short term fingolimod treatment decreases soluble VLA 4 levels in MS patients. J Neuroimmunol 2014; 275(1-2): 228.
[http://dx.doi.org/10.1016/j.jneuroim.2014.08.610]
[34]
Derakhshani A, Asadzadeh Z, Safarpour H, et al. Regulation of CTLA-4 and PD-L1 expression in relapsing-remitting multiple sclerosis patients after treatment with fingolimod, IFNβ-1α, glatiramer acetate, and dimethyl fumarate drugs. J Pers Med 2021; 11(8): 721.
[http://dx.doi.org/10.3390/jpm11080721] [PMID: 34442365]
[35]
Thomas K, Sehr T, Proschmann U, Rodriguez-Leal FA, Haase R, Ziemssen T. Fingolimod additionally acts as immunomodulator focused on the innate immune system beyond its prominent effects on lymphocyte recirculation. J Neuroinflammation 2017; 14(1): 41.
[http://dx.doi.org/10.1186/s12974-017-0817-6] [PMID: 28231856]
[36]
Yoshida Y, Mikami N, Nakanishi Y, et al. Characterization of an expanded IL-10-producing-suppressive T cell population associated with immune tolerance. Biol Pharm Bull 2021; 44(4): 585-9.
[http://dx.doi.org/10.1248/bpb.b19-01072] [PMID: 33504740]
[37]
Heitmann N, Gude A, Hendek H, Gold R, Faissner S. Siponimod favours expression of less pro-inflammatory, alternatively activated microglia in a microglia repopulation model of progressive multiple sclerosis - implication for neuroprotection. ECTRIMS 2022.
[38]
Harris S, Maddux R, Hoffmueller U, Raschke E. Effect of ozanimod on circulating leukocyte subtypes in patients with relapsing multiple sclerosis and comparison with healthy volunteers. Mult Scler J 2021; 27(2): 2021.
[39]
Husseini L, Seeger I, Rowold C, Brück W, Weber M. Natalizumab treatment promotes activation and differentiation of peripheral B cells in multiple sclerosis. Mult Scler Int 2018; 24(S2): 689-90.
[40]
Traub JW, Pellkofer HL, Grondey K, et al. Natalizumab promotes activation and pro-inflammatory differentiation of peripheral B cells in multiple sclerosis patients. J Neuroinflammation 2019; 16(1): 228.
[http://dx.doi.org/10.1186/s12974-019-1593-2] [PMID: 31733652]
[41]
De Andres C, Tejeiro R, Sánchez-Madrid F, Martinez ML, Fernández-Cruz E, Sanchez-Ramon S. Decreased proportions and down-regulation of VLA-4 and LFA-1 molecules on circulating myeloid and plasmacytoid dendritic cells due to natalizumab for relapsing-remitting multiple sclerosis. A preliminary prospective study. MS 2009; 15(S9): 134-5.
[42]
Mathias A, Pantazou V, Perriot S, et al. Ocrelizumab impairs the phenotype and function of memory CD8 + T cells. Neurol Neuroimmunol Neuroinflamm 2023; 10(2): e200084.
[http://dx.doi.org/10.1212/NXI.0000000000200084] [PMID: 36717268]
[43]
Shinoda K, Li R, Rezk A, et al. Differential effects of anti-CD20 therapy on CD4 and CD8 T cells and implication of CD20-expressing CD8 T cells in MS disease activity. Proc Natl Acad Sci 2023; 120(3): e2207291120.
[http://dx.doi.org/10.1073/pnas.2207291120] [PMID: 36634138]
[44]
Garcia A, Morille J, Shah S, et al. A broad effect of ocrelizumab on the peripheral immune component in patients with early relapsing-remitting multiple sclerosis. Mult Scler Int 2021; 27(S2): 593-4.
[45]
Nissimov N, Hajiyeva Z, Torke S, et al. B cells reappear less mature and more activated after their anti-CD20-mediated depletion in multiple sclerosis. Proc Natl Acad Sci 2020; 117(41): 25690-9.
[http://dx.doi.org/10.1073/pnas.2012249117] [PMID: 32999069]
[46]
Antonopoulos I, Daoussis D, Lalioti ME, et al. B cell depletion treatment decreases CD4+IL4+ and CD4+CD40L+ T cells in patients with systemic sclerosis. Rheumatol Int 2019; 39(11): 1889-98.
[http://dx.doi.org/10.1007/s00296-019-04350-4] [PMID: 31227855]
[47]
Tokunaga M, Fujii K, Saito K, et al. Down-regulation of CD40 and CD80 on B cells in patients with life-threatening systemic lupus erythematosus after successful treatment with rituximab. Rheumatology 2005; 44(2): 176-82.
[http://dx.doi.org/10.1093/rheumatology/keh443] [PMID: 15494350]
[48]
Tokunaga M, Saito K, Kawabata D, et al. Efficacy of rituximab (anti-CD20) for refractory systemic lupus erythematosus involving the central nervous system. Ann Rheum Dis 2006; 66(4): 470-5.
[http://dx.doi.org/10.1136/ard.2006.057885] [PMID: 17107983]
[49]
Sfikakis PP, Boletis JN, Lionaki S, et al. Remission of proliferative lupus nephritis following B cell depletion therapy is preceded by down‐regulation of the T cell costimulatory molecule CD40 ligand: An open‐label trial. Arthritis Rheum 2005; 52(2): 501-13.
[http://dx.doi.org/10.1002/art.20858] [PMID: 15693003]
[50]
Pontarini E, Chowdhury F, Sciacca E. Clinical response to rituximab is associated with prevention of b-cell driven salivary gland inflammation and epithelial restoration as revealed by molecular pathology: Results from the tractiss trial in primary sjogren’s syndrome. Ann Rheum Dis 2022; 81: 299-300.
[http://dx.doi.org/10.1136/annrheumdis-2022-eular.4458]
[51]
Bhatia D, Sinha A, Hari P, et al. Rituximab modulates T- and B-lymphocyte subsets and urinary CD80 excretion in patients with steroid-dependent nephrotic syndrome. Pediatr Res 2018; 84(4): 520-6.
[http://dx.doi.org/10.1038/s41390-018-0088-7] [PMID: 29983411]
[52]
de Flon P, Söderström L, Laurell K, et al. Immunological profile in cerebrospinal fluid of patients with multiple sclerosis after treatment switch to rituximab and compared with healthy controls. PLoS One 2018; 13(2): e0192516.
[http://dx.doi.org/10.1371/journal.pone.0192516] [PMID: 29420590]
[53]
Arruda LCM, Lima-Júnior JR, Clave E, et al. Homeostatic proliferation leads to telomere attrition and increased PD-1 expression after autologous hematopoietic SCT for systemic sclerosis. Bone Marrow Transplant 2018; 53(10): 1319-27.
[http://dx.doi.org/10.1038/s41409-018-0162-0] [PMID: 29670207]
[54]
Arruda LCM, Clave E, Lima-Júnior JR, et al. Impact of homeostatic proliferation, telomere attrition, PD-1 expression and CMV-reactivity on TCR diversity and relapse after AHSCT in systemic sclerosis patients. Bone Marrow Transplant 2019; 53(S1): 145-805.
[http://dx.doi.org/10.1038/s41409-018-0354-7]
[55]
Kawashima-Vasconcelos MY, Santana-Gonçalves M, Zanin-Silva DC, Malmegrim KCR, Oliveira MC. Reconstitution of the immune system and clinical correlates after stem cell transplantation for systemic sclerosis. Front Immunol 2022; 13: 941011.
[http://dx.doi.org/10.3389/fimmu.2022.941011] [PMID: 36032076]
[56]
Malmegrim KCR, Lima-Júnior JR, Arruda LCM, de Azevedo JTC, de Oliveira GLV, Oliveira MC. Autologous hematopoietic stem cell transplantation for autoimmune diseases: From mechanistic insights to biomarkers. Front Immunol 2018; 9: 2602.
[http://dx.doi.org/10.3389/fimmu.2018.02602] [PMID: 30505303]
[57]
Arruda LCM, Clave E, Moins-Teisserenc H, Douay C, Farge D, Toubert A. Resetting the immune response after autologous hematopoietic stem cell transplantation for autoimmune diseases. Curr Res Transl Med 2016; 64(2): 107-13.
[http://dx.doi.org/10.1016/j.retram.2016.03.004] [PMID: 27316394]
[58]
Arruda LCM, de Azevedo JTC, de Oliveira GLV, et al. Immunological correlates of favorable long-term clinical outcome in multiple sclerosis patients after autologous hematopoietic stem cell transplantation. Clin Immunol 2016; 169: 47-57.
[http://dx.doi.org/10.1016/j.clim.2016.06.005] [PMID: 27318116]
[59]
Massey JC, Sutton IJ, Ma DDF, Moore JJ. Regenerating immunotolerance in multiple sclerosis with autologous hematopoietic stem cell transplant. Front Immunol 2018; 9: 410.
[http://dx.doi.org/10.3389/fimmu.2018.00410] [PMID: 29593711]
[60]
Arruda LCM, Lorenzi JCC, Sousa APA, et al. Autologous hematopoietic SCT normalizes miR-16, -155 and -142-3p expression in multiple sclerosis patients. Bone Marrow Transplant 2015; 50(3): 380-9.
[http://dx.doi.org/10.1038/bmt.2014.277] [PMID: 25486582]
[61]
Arruda LCM, Oliveira MC, Moraes DA, Covas DT, Malmegrim KCR. Autologous hematopoietic stem cell transplantation increases T-cell PD-1 expression and regulatory mechanisms in systemic sclerosis patients. Ann Rheum Dis 2015; 74(S2): 67.3-8.3.
[http://dx.doi.org/10.1136/annrheumdis-2015-eular.5276]
[62]
Zhang L, Bertucci AM, Ramsey-Goldman R, Burt RK, Datta SK. Regulatory T cell (Treg) subsets return in patients with refractory lupus following stem cell transplantation, and TGF-beta-producing CD8+ Treg cells are associated with immunological remission of lupus. J Immunol Baltim Md 2009; 183(10): 6346-58.
[http://dx.doi.org/10.4049/jimmunol.0901773] [PMID: 19841178]
[63]
Haile Y, Adegoke A, Laribi B, Lin J, Anderson CC. Anti‐CD52 blocks EAE independent of PD‐1 signals and promotes repopulation dominated by double‐negative T cells and newly generated T and B cells. Eur J Immunol 2020; 50(9): 1362-73.
[http://dx.doi.org/10.1002/eji.201948288] [PMID: 32388861]
[64]
Curran CD, Wagner DH, Vollmer TL. CD20 expression is elevated on at helper cell subpopulation in newly diagnosed multiple sclerosis patients. J Investig Med 2020; 68: A198-9.
[65]
Marsh-Wakefield F, Juillard P, Ashhurst T, et al. In depth analysis of B cells in multiple sclerosis patients after treatment with Cladribine. Mult Scler Int 2020; 26(3): 2021.
[66]
Hawke S, Julliard P, Grau G. Cladribine modulates the expression of ICAM-1 and VCAM-1 on human brain endothelium; relevance to multiple sclerosis (MS) (P2.2-055). Neurology 2019; 92(S15): P2.2-055.
[http://dx.doi.org/10.1212/WNL.92.15_supplement.P2.2-055]
[67]
Gonçalves MVM, Brandão WN, Longo C, et al. Correlation between IL-31 and sCD40L plasma levels in Fingolimod-treated patients with Relapsing-Remitting Multiple Sclerosis (RRMS). J Neuroimmunol 2021; 350: 577435.
[http://dx.doi.org/10.1016/j.jneuroim.2020.577435] [PMID: 33189062]
[68]
Fraussen J, Claes N, Van Wijmeersch B, et al. B cells of multiple sclerosis patients induce autoreactive proinflammatory T cell responses. Clin Immunol 2016; 173: 124-32.
[http://dx.doi.org/10.1016/j.clim.2016.10.001] [PMID: 27717695]
[69]
Fraussen J, Claes N, Hellings N, et al. B cells from MS patients induce autoreactive Th1 and Th17 responses. MS 2015; 23(11): 787-8.
[70]
Santos LMB, Boldrini V, Quintiliano R, et al. Immunomodulatory molecules on plasmacytoid dendritic cell is associated with decreased neurofilament light in the cerebrospinal fluid of patients with multiple sclerosis treated with natalizumab. Mult Scler Int 2018; 24(S2): 2019.
[71]
de Andrés C, Teijeiro R, Alonso B, et al. Long-term decrease in VLA-4 expression and functional impairment of dendritic cells during natalizumab therapy in patients with multiple sclerosis. PLoS One 2012; 7(4): e34103.
[http://dx.doi.org/10.1371/journal.pone.0034103] [PMID: 22496780]
[72]
Dallari S, Franciotta D, Carluccio S, et al. Upregulation of integrin expression on monocytes in multiple sclerosis patients treated with natalizumab. J Neuroimmunol 2015; 287: 76-9.
[http://dx.doi.org/10.1016/j.jneuroim.2015.08.010] [PMID: 26439965]
[73]
Putzki N, Baranwal MK, Tettenborn B, Limmroth V, Kreuzfelder E. Effects of natalizumab on circulating B cells, T regulatory cells and natural killer cells. Eur Neurol 2010; 63(5): 311-7.
[http://dx.doi.org/10.1159/000302687] [PMID: 20453514]
[74]
Wipfler P, Oppermann K, Pilz G, et al. Adhesion molecules are promising candidates to establish surrogate markers for natalizumab treatment. Mult Scler 2011; 17(1): 16-23.
[http://dx.doi.org/10.1177/1352458510383075] [PMID: 20937631]
[75]
Fernández-Velasco JI, Kuhle J, Monreal E, et al. Effect of ocrelizumab in blood leukocytes of patients with primary progressive MS. Neurol Neuroimmunol Neuroinflamm 2021; 8(2): e940.
[http://dx.doi.org/10.1212/NXI.0000000000000940] [PMID: 33408167]
[76]
Karnell FG, Lin D, Motley S, et al. Reconstitution of immune cell populations in multiple sclerosis patients after autologous stem cell transplantation. Clin Exp Immunol 2017; 189(3): 268-78.
[http://dx.doi.org/10.1111/cei.12985] [PMID: 28498568]
[77]
Van Laar JM, Farge D, Baraut J, et al. Cytokine measurement before and after hematopoietic stem cell transplantation in severe diffuse systemic sclerosis. J Invest Dermatol 2009; 129(10): 2523-33.
[http://dx.doi.org/10.1038/jid.2009.276]
[78]
Dustin ML. The immunological synapse. Cancer Immunol Res 2014; 2(11): 1023-33.
[http://dx.doi.org/10.1158/2326-6066.CIR-14-0161] [PMID: 25367977]
[79]
Schubert DA, Gordo S, Sabatino JJ Jr, et al. Self-reactive human CD4 T cell clones form unusual immunological synapses. J Exp Med 2012; 209(2): 335-52.
[http://dx.doi.org/10.1084/jem.20111485] [PMID: 22312112]
[80]
Dustin ML, Colman DR. Neural and immunological synaptic relations. Science 2002; 298(5594): 785-9.
[http://dx.doi.org/10.1126/science.1076386] [PMID: 12399580]
[81]
Harjunpää H, Asens LM, Guenther C, Fagerholm SC. Cell adhesion molecules and their roles and regulation in the immune and tumor microenvironment. Front Immunol 2019; 10: 1078.
[http://dx.doi.org/10.3389/fimmu.2019.01078] [PMID: 31231358]
[82]
Gerasimova EV, Tabakov DV, Gerasimova DA, Popkova TV. Activation markers on B and T cells and immune checkpoints in autoimmune rheumatic diseases. Int J Mol Sci 2022; 23(15): 8656.
[http://dx.doi.org/10.3390/ijms23158656] [PMID: 35955790]
[83]
Huppa JB, Davis MM. T-cell-antigen recognition and the immunological synapse. Nat Rev Immunol 2003; 3(12): 973-83.
[http://dx.doi.org/10.1038/nri1245] [PMID: 14647479]
[84]
Buchbinder EI, Desai A. CTLA-4 and PD-1 pathways. Am J Clin Oncol 2016; 39(1): 98-106.
[http://dx.doi.org/10.1097/COC.0000000000000239] [PMID: 26558876]
[85]
Nagai S, Azuma M. The CD28-B7 family of co-signaling molecules. Adv Exp Med Biol 2019; 1189: 25-51.
[http://dx.doi.org/10.1007/978-981-32-9717-3_2] [PMID: 31758530]
[86]
Tian J, Zhang B, Rui K, Wang S. The role of GITR/GITRL interaction in autoimmune diseases. Front Immunol 2020; 11: 588682.
[http://dx.doi.org/10.3389/fimmu.2020.588682] [PMID: 33163004]
[87]
Wang F, Chau B, West SM, et al. Structures of mouse and human GITR-GITRL complexes reveal unique TNF superfamily interactions. Nat Commun 2021; 12(1): 1378.
[http://dx.doi.org/10.1038/s41467-021-21563-z] [PMID: 33654081]
[88]
Manian M, Motallebnezhad M, Nedaeinia R, et al. Comparison of OX40 expression in patients with multiple sclerosis and neuromyelitis optica as an approach to diagnosis. Allergy Asthma Clin Immunol 2023; 19(1): 19.
[http://dx.doi.org/10.1186/s13223-023-00772-9] [PMID: 36899405]
[89]
Machcińska M, Kierasińska M, Michniowska M, et al. Reduced expression of PD-1 in circulating CD4+ and CD8+ tregs is an early feature of RRMS. Int J Mol Sci 2022; 23(6): 3185.
[http://dx.doi.org/10.3390/ijms23063185] [PMID: 35328606]
[90]
Mohammadzadeh A, Rad IA, Ahmadi-Salmasi B. CTLA-4, PD-1 and TIM-3 expression predominantly downregulated in MS patients. J Neuroimmunol 2018; 323: 105-8.
[http://dx.doi.org/10.1016/j.jneuroim.2018.08.004] [PMID: 30196822]
[91]
Mena E, Rohowsky-Kochan C. Expression of costimulatory molecules on peripheral blood mononuclear cells in multiple sclerosis. Acta Neurol Scand 1999; 100(2): 92-6.
[http://dx.doi.org/10.1111/j.1600-0404.1999.tb01044.x] [PMID: 10442449]
[92]
Oliveira MCB, de Brito MH, Simabukuro MM. Central nervous system demyelination associated with immune checkpoint inhibitors: Review of the literature. Front Neurol 2020; 11: 538695.
[http://dx.doi.org/10.3389/fneur.2020.538695] [PMID: 33362680]
[93]
Deftereos SN, Georgonikou D. Effectiveness of rituximab in treating immune-checkpoint-inhibitor-induced immune-related adverse events: Results of a systematic review. Ann Oncol 2021; 32(2): 282-3.
[http://dx.doi.org/10.1016/j.annonc.2020.12.001] [PMID: 33309745]
[94]
Valencia-Sanchez C, Sechi E, Dubey D, et al. Immune checkpoint inhibitor‐associated central nervous system autoimmunity. Eur J Neurol 2023; 30(8): 2418-29.
[http://dx.doi.org/10.1111/ene.15835] [PMID: 37151179]
[95]
Vermersch P, Granziera C, Mao-Draayer Y. Frexalimab, a CD40L inhibitor, in relapsing multiple sclerosis: Results from a randomized controlled phase 2 trial. 2023. Available from: https://cmsc.confex.com/cmsc/2023/meetingapp.cgi/Paper/9072
[96]
Giovannoni G, Comi G, Cook S, et al. A placebo-controlled trial of oral cladribine for relapsing multiple sclerosis. N Engl J Med 2010; 362(5): 416-26.
[http://dx.doi.org/10.1056/NEJMoa0902533] [PMID: 20089960]
[97]
Giovannoni G, Soelberg Sorensen P, Cook S, et al. Safety and efficacy of cladribine tablets in patients with relapsing-remitting multiple sclerosis: Results from the randomized extension trial of the CLARITY study. Mult Scler 2018; 24(12): 1594-604.
[http://dx.doi.org/10.1177/1352458517727603] [PMID: 28870107]
[98]
Vogel DYS, Vereyken EJF, Glim JE, et al. Macrophages in inflammatory multiple sclerosis lesions have an intermediate activation status. J Neuroinflammation 2013; 10(1): 809.
[http://dx.doi.org/10.1186/1742-2094-10-35] [PMID: 23452918]
[99]
Kappos L, Radue EW, O’Connor P, et al. A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N Engl J Med 2010; 362(5): 387-401.
[http://dx.doi.org/10.1056/NEJMoa0909494] [PMID: 20089952]
[100]
Comi G, Kappos L, Selmaj KW, et al. Safety and efficacy of ozanimod versus interferon beta-1a in relapsing multiple sclerosis (SUNBEAM): A multicentre, randomised, minimum 12-month, phase 3 trial. Lancet Neurol 2019; 18(11): 1009-20.
[http://dx.doi.org/10.1016/S1474-4422(19)30239-X] [PMID: 31492651]
[101]
Barry B, Erwin AA, Stevens J, Tornatore C. Fingolimod rebound: A review of the clinical experience and management considerations. Neurol Ther 2019; 8(2): 241-50.
[http://dx.doi.org/10.1007/s40120-019-00160-9] [PMID: 31677060]
[102]
Schiess N, Calabresi PA. Natalizumab. Neurology 2009; 72(5): 392-3.
[http://dx.doi.org/10.1212/01.wnl.0000341783.33962.5b] [PMID: 19188569]
[103]
Lee JD, Chen T. Natalizumab rebound in multiple sclerosis. Neurohospitalist 2022; 12(1): 197-8.
[http://dx.doi.org/10.1177/19418744211031360] [PMID: 34950414]
[104]
Adorisio S, Cannarile L, Delfino DV, Ayroldi E. Glucocorticoid and PD-1 cross-talk: Does the immune system become confused? Cells 2021; 10(9): 2333.
[http://dx.doi.org/10.3390/cells10092333] [PMID: 34571982]
[105]
Cronstein BN, Kimmel SC, Levin RI, Martiniuk F, Weissmann G. A mechanism for the antiinflammatory effects of corticosteroids: The glucocorticoid receptor regulates leukocyte adhesion to endothelial cells and expression of endothelial-leukocyte adhesion molecule 1 and intercellular adhesion molecule 1. Proc Natl Acad Sci 1992; 89(21): 9991-5.
[http://dx.doi.org/10.1073/pnas.89.21.9991] [PMID: 1279685]
[106]
Theien BE, Vanderlugt CL, Eagar TN, et al. Discordant effects of anti-VLA-4 treatment before and after onset of relapsing experimental autoimmune encephalomyelitis. J Clin Invest 2001; 107(8): 995-1006.
[http://dx.doi.org/10.1172/JCI11717] [PMID: 11306603]
[107]
Theien BE, Vanderlugt CL, Nickerson-Nutter C, et al. Differential effects of treatment with a small-molecule VLA-4 antagonist before and after onset of relapsing EAE. Blood 2003; 102(13): 4464-71.
[http://dx.doi.org/10.1182/blood-2003-03-0974] [PMID: 12933585]
[108]
Ramanujam M, Steffgen J, Visvanathan S, Mohan C, Fine JS, Putterman C. Phoenix from the flames: Rediscovering the role of the CD40-CD40L pathway in systemic lupus erythematosus and lupus nephritis. Autoimmun Rev 2020; 19(11): 102668.
[http://dx.doi.org/10.1016/j.autrev.2020.102668] [PMID: 32942031]
[109]
McHale JF, Harari OA, Marshall D, Haskard DO. TNF-alpha and IL-1 sequentially induce endothelial ICAM-1 and VCAM-1 expression in MRL/lpr lupus-prone mice. J Immunol Baltim Md 1999; 163(7): 3993-4000.
[PMID: 10491002]
[110]
Robertson NP, Scolding NJ. Immune reconstitution and treatment response in multiple sclerosis following alemtuzumab. Neurology 2014; 82(24): 2150-1.
[http://dx.doi.org/10.1212/WNL.0000000000000530] [PMID: 24838787]
[111]
Oreja-Guevara C, Brownlee W, Celius EG, et al. Expert opinion on the long-term use of cladribine tablets for multiple sclerosis: Systematic literature review of real-world evidence. Mult Scler Relat Disord 2023; 69: 104459.
[http://dx.doi.org/10.1016/j.msard.2022.104459] [PMID: 36565573]
[112]
Dumitrescu L, Papathanasiou A, Coclitu C, et al. An update on the use of sphingosine 1-phosphate receptor modulators for the treatment of relapsing multiple sclerosis. Expert Opin Pharmacother 2023; 24(4): 495-509.
[http://dx.doi.org/10.1080/14656566.2023.2178898] [PMID: 36946625]
[113]
Khoy K, Mariotte D, Defer G, Petit G, Toutirais O, Le Mauff B. Natalizumab in multiple sclerosis treatment: From biological effects to immune monitoring. Front Immunol 2020; 11: 549842.
[http://dx.doi.org/10.3389/fimmu.2020.549842] [PMID: 33072089]
[114]
de Sèze J, Maillart E, Gueguen A, et al. Anti-CD20 therapies in multiple sclerosis: From pathology to the clinic. Front Immunol 2023; 14: 1004795.
[http://dx.doi.org/10.3389/fimmu.2023.1004795] [PMID: 37033984]
[115]
AlSharoqi IA, Aljumah M, Bohlega S, et al. Immune reconstitution therapy or continuous immunosuppression for the management of active relapsing-remitting multiple sclerosis patients? A narrative review. Neurol Ther 2020; 9(1): 55-66.
[http://dx.doi.org/10.1007/s40120-020-00187-3] [PMID: 32297127]

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