B cell depletion changes the immune cell profile in multiple sclerosis patients: One-year report

Journal of Neuroimmunology - Tập 359 - Trang 577676 - 2021
Amy E. Lovett-Racke1,2, Yuhong Yang3, Yue Liu1, Matthew Gormley1, Emma Kraus1, Calsey Graham1, Sibyl Wray4, Michael K. Racke3, Enrique Alvarez5, Ann Bass6, Edward Fox7
1Department of Microbial Infection and Immunity, The Ohio State University Wexner Medical Center, Columbus, OH, USA
2Department of Neuroscience, The Ohio State University Wexner Medical Center, Columbus, OH, USA
3Department of Neurology, The Ohio State University Wexner Medical Center, The Ohio State University Wexner Medical Center, Columbus, OH, USA
4Hope Neurology Multiple Sclerosis Center, Knoxville, TN, USA
5Department of Neurology, University of Colorado School of Medicine, Aurora, CO, USA
6Neurology Center of San Antonio, San Antonio, TX, USA
7Central Texas Neurology Consultants, UT Dell Medical School, Austin, TX, USA

Tài liệu tham khảo

Achiron, 2020, Humoral immune response to COVID-19 mRNA vaccine in patients with multiple sclerosis treated with high-efficacy disease-modifying therapies, Ther. Adv. Neurol. Disord., 14 Allegretta, 1990, T cell responsive to myelin basic protein in patients with multiple sclerosis, Science, 247, 718, 10.1126/science.1689076 Aqel, 2019, Novel small molecule IL-6 inhibitor suppresses autoreactive Th17 development and promotes Treg development, Clin. Exp. Immunol., 196, 215, 10.1111/cei.13258 Aqel, 2021, Selective inhibition of STAT3 with a novel small molecule improves Teff:Treg balance and ameliorates CNS autoimmunity, JCI Insight, 142376 Badami, 2019, Activation-induced cell death of self-reactive regulatory T cells drives autoimmunity, Proc. Natl. Acad. Sci. U. S. A., 116, 26788, 10.1073/pnas.1910281116 Baecher-Allan, 2018, Multiple sclerosis: mechanisms and immunotherapy, Neuron, 97, 742, 10.1016/j.neuron.2018.01.021 Bar-Or, 2008, Rituximab in relapsing-remitting multiple sclerosis: a 72-week, open-label, phase I trial, Ann. Neurol., 63, 395, 10.1002/ana.21363 Bigaut, 2021, Impact of disease-modifying treatments on humoral response after COVID-19 vaccination: a mirror of the response after SARS-CoV-2 infection, Rev. Neurol. (Paris), 10.1016/j.neurol.2021.05.001 Burnard, 2017, EBV and MS: major cause, minor contributor or red-herring?, Mult. Scler. Relat. Disord., 16, 24, 10.1016/j.msard.2017.06.002 Burns, 1999, Isolation of myelin basic protein-specific T cells predominantly from the memory T-cell compartment in multiple sclerosis, Ann. Neurol., 45, 33, 10.1002/1531-8249(199901)45:1<33::AID-ART7>3.0.CO;2-G Chen, 2019, CXCR5+PD-1+ follicular helper CD8 T cells control B cell tolerance, Nat. Commun., 10, 4415, 10.1038/s41467-019-12446-5 Chen, 2020, Apremilast regulates the Teff/Treg balance to ameliorate uveitis via PI3K/AKT/FoxO1 signaling pathway, Front. Immunol., 11, 581673, 10.3389/fimmu.2020.581673 Codarri, 2011, RORgammat drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation, Nat Immunol, 12, 560, 10.1038/ni.2027 Cross, 2006, Rituximab reduces B cells and T cells in cerebrospinal fluid of multiple sclerosis patients, J. Neuroimmunol., 180, 63, 10.1016/j.jneuroim.2006.06.029 Deola, 2017, Evidence for CD19B-CD8T cell interactions in blood and tissues from patients with GvHD, Bone Marrow Transplant., 52, 459, 10.1038/bmt.2016.294 Desai, 2020, Lack of B lymphocytes enhances CD8 T cell-mediated resistance against respiratory viral infection but compromises memory cell formation, J. Virol., 94, 10.1128/JVI.01877-19 El-Behi, 2011, The encephalitogenicity of T(H)17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF, Nat Immunol, 12, 568, 10.1038/ni.2031 Fox, 2021, A phase 2 multicenter study of ublituximab, a novel glycoengineered anti-CD20 monoclonal antibody, in patients with relapsing forms of multiple sclerosis, Mult. Scler., 27, 420, 10.1177/1352458520918375 Gingele, 2018, Ocrelizumab depletes CD20+ T cells in multiple sclerosis patients, Cells, 8, 12, 10.3390/cells8010012 Guerieri, 2021, Serological response to SARS-CoV-2 vaccination in multiple sclerosis patients treated with fingolimod or ocrelizumab: an initial real-life experience, J. Neurol., 1 Haas, 2007, Prevalence of newly generated naive regulatory T cells (Treg) is critical for Treg suppressive function and determines Treg dysfunction in multiple sclerosis, J. Immunol., 179, 1322, 10.4049/jimmunol.179.2.1322 Haas, 2005, Reduced suppressive effect of CD4+CD25high regulatory T cells on the T cell immune response against myelin oligodendrocyte glycoprotein in patients with multiple sclerosis, Eur. J. Immunol., 35, 3343, 10.1002/eji.200526065 Hauser, 2008, B-cell depletion with rituximab in relapsing-remitting multiple sclerosis, New Engl. J. Med., 358, 676, 10.1056/NEJMoa0706383 Hauser, 2017, Ocrelizumab versus interferon Beta-1a in relapsing multiple sclerosis, New Engl. J. Med., 376, 221, 10.1056/NEJMoa1601277 Hawker, 2009, Rituximab in patients with primary progressive multiple sclerosis: results of a randomized double-blind placebo-controlled multicenter trial, Ann. Neurol., 66, 460, 10.1002/ana.21867 Hermann, 1995, CD40 ligand-positive CD8+ T cell clones allow B cell growth and differentiation, Eur. J. Immunol., 25, 2972, 10.1002/eji.1830251039 Hladfkova, 2019, Tumor-infiltrating B cells affect the progression of oropharyngeal squamous cell carcinoma via cell-to-cell interactions with CD8+ T cells, J. Immunother. Cancer, 7, 261, 10.1186/s40425-019-0726-6 Holley, 2014, CD20+ inflammatory T-cells are present in blood and brain of multiple sclerosis patients and can be selectively targeted for apoptotic elimination, Mult. Scler. Relat. Disord., 3, 650, 10.1016/j.msard.2014.06.001 Huan, 2005, Decreased FOXP3 levels in multiple sclerosis patients, J. Neurosci. Res., 81, 45, 10.1002/jnr.20522 Jelcic, 2018, Memory B cells activate brain-homing, autoreactive CD4+ T cells in multiple sclerosis, Cell, 175, 85, 10.1016/j.cell.2018.08.011 Kantengwa, 2007, Inhibition of naïve Th1 CD4+ T cells by glatiramer acetate in multiple sclerosis, J. Neuroimmunol., 185, 123, 10.1016/j.jneuroim.2006.12.014 Kappos, 2011, Ocrelizumab in relapsing-remitting multiple sclerosis: a phase 2, randomised, placebo-controlled, multicentre trial, Lancet, 378, 1779, 10.1016/S0140-6736(11)61649-8 Kitz, 2018, Regulatory T cells: from discovery to autoimmunity, Cold Spring Harb. Perspect. Med., 8, 10.1101/cshperspect.a029041 Kumar, 2006, CD4+CD25+FoxP3+ T lymphocytes fail to suppress myelin basic protein-induced proliferation in patients with multiple sclerosis, J. Neuroimmunol., 180, 178, 10.1016/j.jneuroim.2006.08.003 Laurence, 2017, Epstein-Barr virus and multiple sclerosis: updating Pender’s hypothesis, Mult. Scler. Relat. Disord., 16, 8, 10.1016/j.msard.2017.05.009 Le Garff-Tavernier, 2014, Antibody-dependent cellular cytotoxicity of the optimized anti-CD20 monoclonal antibody ublituximab on chronic lymphocytic leukemia cells with the 17p deletion, Leukemia, 28, 230, 10.1038/leu.2013.240 Lee, 2017, IL-23R-activated STAT3/STAT4 is essential for Th1/Th17-mediated CNS autoimmunity, JCI Insight, 2, 91663, 10.1172/jci.insight.91663 Lisak, 2012, Secretory products of multiple sclerosis B cells are cytotoxic to oligodendrocytes in vitro, J. Neuroimmunol., 246, 85, 10.1016/j.jneuroim.2012.02.015 Lisak, 2017, B cells from patients with multiple sclerosis induce cell death via apoptosis in neurons in vitro, J. Neuroimmunol., 309, 88, 10.1016/j.jneuroim.2017.05.004 Lovett-Racke, 1998, Decreased dependence of myelin basic protein-reactive T cells on CD28-mediated costimulation in multiple sclerosis patients – a marker of activated/memory T cells, J. Clin. Invest., 101, 725, 10.1172/JCI1528 Lovett-Racke, 2011, Th1 versus Th17: are T cell cytokines relevant in multiple sclerosis?, Biochim. Biophys. Acta, 1812, 246, 10.1016/j.bbadis.2010.05.012 Lovett-Racke, 2019, B cell depletion with ublituximab reshapes the T cell profile in multiple sclerosis patients, J. Neuroimmunol., 332, 187, 10.1016/j.jneuroim.2019.04.017 Lykken, 2014, Acute and chronic B cell depletion disrupts CD4+ and CD8+ T cell homeostasis and expansion during acute viral infection in mice, J. Immunol., 193, 746, 10.4049/jimmunol.1302848 Montalban, 2017, Ocrelizumab versus placebo in primary progressive multiple sclerosis, New Engl. J. Med., 376, 209, 10.1056/NEJMoa1606468 Naismith, 2010, Rituximab add-on therapy for breakthrough relapsing multiple sclerosis: a 52-week phase II trial, Neurology, 74, 1860, 10.1212/WNL.0b013e3181e24373 Nielsen, 2017, Characterization of naïve, memory and effector T cells in progressive multiple sclerosis, J. Neuroimmunol., 310, 17, 10.1016/j.jneuroim.2017.06.001 Palanichamy, 2014, Rituximab efficiently depletes increased CD20-expressing T cells in multiple sclerosis patients, J. Immunol., 193, 580, 10.4049/jimmunol.1400118 Poli, 2009, CD56bright natural killer (NK) cells: an important NK cell subset, Immunology, 126, 458, 10.1111/j.1365-2567.2008.03027.x Quigley, 2007, CXCR5+ CCR7- CD8 T cells are early effector memory cells that infiltrate tonsil B cell follicles, Eur. J. Immunol., 37, 3352, 10.1002/eji.200636746 Sabatino, 2019, Anti-CD20 therapy depletes activated myelin-specific CD8+ T cells in multiple sclerosis, Proc. Natl, Acad. Sci. USA, 116, 25800, 10.1073/pnas.1915309116 Sawas, 2017, A phase 1/2 trial of ublituximab, a novel anti-CD20 monoclonal antibody, in patients with B-cell non-Hodgkin lymphoma or chronic lymphocytic leukaemia previously exposed to rituximab, Br. J. Haematol., 177, 243, 10.1111/bjh.14534 Schuh, 2016, Features of human CD3+CD20+ T cells, J. Immunol., 197, 1111, 10.4049/jimmunol.1600089 Shen, 2003, A specific role for B cells in the generation of CD8 T cell memory by recombinant listeria monocytogenes, J. Immunol., 170, 1443, 10.4049/jimmunol.170.3.1443 Venken, 2008, Compromised CD4+ CD25(high) regulatory T-cell function in patients with relapsing-remitting multiple sclerosis is correlated with a reduced frequency of FOXP3-positive cells and reduced FOXP3 expression at the single-cell level, Immunology, 123, 79, 10.1111/j.1365-2567.2007.02690.x Viglietta, 2004, Loss of functional suppression by CD4+CD25+ regulatory T cells in patients with multiple sclerosis, J. Exp. Med., 199, 971, 10.1084/jem.20031579 Von Essen, 2019, Proinflammatory CD20+ T cells in the pathogenesis of multiple sclerosis, Brain, 142, 120, 10.1093/brain/awy301