Unique B cell responses in B cell-dependent and B cell-independent EAE

References

• Sospedra M, Martin R. Immunology of multiple sclerosis. Ann Rev Immunol. 2005; 23:683–747.
   PubMed Web of Science ®Google Scholar
• Warrington AE, Asakura K, Bieber AJ, Ciric B, Van Keulen V, Kaveri SV, Kyle RA, Pease LR, Rodriguez M. Human monoclonal antibodies reactive to oligodendrocytes promote remyelination in a model of mutiple sclerosis. Proc Natl Acad Sci U S A. 2000; 97:6820–6825.
   PubMed Web of Science ®Google Scholar
• Matsushita T, Yanaba K, Bouaziz JD, Fujimoto M, Tedder TF. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest. 2006; 118:3420–3430.
   Google Scholar
• Fillatreau S, Sweenie C, McGeachy M, Gray D, Anderton S. B cells regulate autoimmunity by provision of IL-10. Nat Immunol. 2002; 3:944–950.
   PubMed Web of Science ®Google Scholar
• Genain CP, Nguyen M-H, Letvin NL, Pearl R, Davis RL, Adelman M, Lees MB, Linington C, Hauser SL. Antibody facilitation of multiple sclerosis-like lesions in a nonhuman primate. J Clin Invest. 1995; 96:2966–2974.
   PubMedGoogle Scholar
• von Budingen HC, Hauser SL, Ouallet JC, Tanuma N, Menge T, Genain CP. Frontline: Epitope recognition on the myelin/oligodendrocyte glycoprotein differentially influences disease phenotype and antibody effector functions in autoimmune demyelination. Eur J Immunol. 2004; 34:2072–2083.
   PubMed Web of Science ®Google Scholar
• von Budingen HC, Hauser SL, Fuhrmann A, Nabavi CB, Lee JI, Genain CP. Molecular characterization of antibody specificities against myelin/oligodendrocyte glycoprotein in autoimmune demyelination. Proc Natl Acad Sci U S A. 2002; 99:8207–8212.
   Google Scholar
• Genain CP, Cannella B, Hauser SL, Raine CS. Identification of autoantibodies associated with myelin damage in multiple sclerosis. Nat Med. 1999; 5:170–175.
   PubMed Web of Science ®Google Scholar
• Raine CS, Cannella B, Hauser SL, Genain CP. Demyelination in primate autoimmune encephalomyelitis and acute multiple sclerosis lesions: A case for antigen-specific antibody mediation. Ann Neurol. 1999; 46:144–160.
   PubMed Web of Science ®Google Scholar
• Brehm U, Piddlesden SJ, Gardinier MV, Linington C. Epitope specificity of demyelinating monoclonal antibodies directed against human myelin oligodendrocyte glycoprotein. J Neuroimmunol. 1999; 97:9–15.
   PubMedGoogle Scholar
• Forsthuber TG, Shive CL, Weinhold W, de Graaf K, Spack EG, Sublett R, Melms A, Kort J, Racke MK, Weissert R. T cell epitopes of human myelin oligodendrocyte glycoprotein indentified in HLA-DR4 (DRB1*0401) transgenic mice are encephalitogenic and are presented by human B cells. J Immunol. 2001; 167:7119–7125.
   PubMed Web of Science ®Google Scholar
• Dai Y, Carayanniotis KA, Eliades P, Lymberi P, Shepherd P, Kong Y, Carayanniotis G. Enhancing or suppressive effects of antibodies on processing of a pathogenic T cell epitope in thyroglobulin. J Immunol. 1999; 62:6987–6992.
   Google Scholar
• Dai YD, Eliades P, Carayanniotis KA, McCormick DJ, Kong YC, Magafa V, Cordopatis P, Lymberi P, Carayanniotis G. Thyroxine-binding antibodies inhibit T cell recognition of a pathogenic thyroglobulin epitope. J Immunol. 2005; 174:3105–3110.
   Google Scholar
• Antoniou AN, Watts C. Antibody modulation of antigen presentation: Positive and negative effects on presentation of the tetanus toxin antigen via the murine B cell isoform of FcgammaRII. Eur J Immunol. 2002; 32:530–540.
   Google Scholar
• Simitsek PD, Campbell DG, Lanzavecchia A, Fairweather N, Watts C. Modulation of antigen processing by bound antibodies can boost or suppress class II major histocompatibility complex presentation of different T cell determinants. J Exp Med. 1995; 181:1957–1963.
   PubMedGoogle Scholar
• Watts C, Lanzavecchia A. Suppressive effect of antibody on processing of T cell epitopes. J Exp Med. 1993; 178:1459–1463.
   PubMedGoogle Scholar
• Weber MS, Prod'homme T, Patarroyo JC, Molnarfi N, Karnezis T, Lehmann-Horn K, Danilenko DM, Eastham-Anderson J, Slavin AJ, Linington C, Bernard CCA, Martin F, Zamvil SS. B-cell activation influences T-cell polarization and outcome of anti-CD20 B-cell depletion in central nervous system autoimmunity. Ann Neurol. 2010; 68:369–383.
   PubMed Web of Science ®Google Scholar
• Monson N, Cravens P, Hussain R, Harp C, Cummings M, de Pilar Martin M, Ben L-H, Do J, Lyons J-A, Lovette-Racke A, Cross A, Racke M, Stüve O, Shlomchik M, Eagar T. Rituximab treatment reduces organ-specific T cell responses and ameliorates experimental autoimmune ecephalomyelitis. PLoS ONE. 2011; 6:e17103.
   PubMed Web of Science ®Google Scholar
• Harp C, Ireland S, Davis L, Cassidy B, Cravens P, Stuve O, Lovett-Racke A, Eagar T, Greenberg B, Racke M, Cowell L, Karandikar N, Frohman E, Monson N. Memory B cells from a subset of treatment-naive relapsing remitting multiple sclerosis patients elicit CD4+T cell profliferation and INF-g in response to myelin basic protein and myelin oligodendrocyte glycoprotein. Eur J Immunol. 2010; 40:2942–2956.
   PubMed Web of Science ®Google Scholar
• Duddy M, Niino M, Adatia F, Hebert S, Freedman M, Atkins H, Kim HJ, Bar-Or A. Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J Immunol. 2007; 178:6092–6099.
   PubMed Web of Science ®Google Scholar
• Asakura K, Rodriguez M. A unique population of circulating autoantibodies promotes central nervous system remyelination. Multiple Sclerosis. 1998; 4:212–221.
   Google Scholar
• Rodriguez M, Lennon VA. Immunoglobulins promote remyelination in the CNS. Ann Neurol. 1990; 27:12–17.
   PubMed Web of Science ®Google Scholar
• Avasarala JR, Cross AH, Trotter JL. Oligoclonal band number as a marker for prognosis in multiple sclerosis. Arch Neurol. 2001; 58:2044–2045.
   PubMedGoogle Scholar
• Villar LM, Sadaba MC, Roldan E, Masjuan J, Gonzalez-Porque P, Villarrubia N, Espino M, Garcia-Trujillo JA, Bootello A, Alvarez-Cermeno JC. Intrathecal synthesis of oligoclonal IgM against myelin lipids predicts an aggressive disease course in MS. J Clin Invest. 2005; 1115:187–194.
   Google Scholar
• Zeman AZJ, Kidd D, McLean BN, Kelly MA, Francis DA, Miller DH, Kendall BE, Rudge P, Thompson EJ, McDonald WI. A study of oligoclonal band negative multiple sclerosis. J Neurol Neurosurg Psych. 1996; 60:27–30.
   PubMed Web of Science ®Google Scholar
• Bar-Or A, Calabresi PA, Arnold D, Markowitz C, Shafer S, Kasper LH, Waubant E, Gazda S, Fox RJ, Panzara M, Sarkar N, Agarwal S, Smith CH. Rituximab in relapsing-remitting multiple sclerosis: A 72-week, open-label, phase I trial. Ann Neurol. 2008; 63:395–400 [erratum appears in Ann Neurol 2008;Jun;63(6):803 Note: Arnlod, Douglas [corrected to Arnold, Douglas].
   PubMed Web of Science ®Google Scholar
• Dalakas MC. B cells as therapeutic targets in autoimmune neurological disorders. Nat Clin Pract Neurol. 2008; 4:557–567.
   PubMedGoogle Scholar
• Hauser SL, Waubant E, Arnold DL, Vollmer T, Antel J, Fox RJ, Bar-Or A, Panzara M, Sarkar N, Agarwal S, Langer-Gould A, Smith CH, Group HT. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. New Engl J Med. 2008; 358:676–688.
   PubMed Web of Science ®Google Scholar
• Leussink VI, Lehmann HC, Meyer zu Horste G, Hartung HP, Stuve O, Kieseier BC. Rituximab induces clinical stabilization in a patient with fulminant multiple sclerosis not responding to natalizumab: Evidence for disease heterogeneity. J Neurol. 2008; 255:1436–1438.
   Google Scholar
• Stuve O, Cepok S, Elias B, Saleh A, Hartung HP, Hemmer B, Kieseier BC. Clinical stabilization and effective B-lymphocyte depletion in the cerebrospinal fluid and peripheral blood of a patient with fulminant relapsing-remitting multiple sclerosis. Arch Neurol. 2005; 62:1620–1623.
   PubMed Web of Science ®Google Scholar
• Stuve O, Leussink VI, Frohlich R, Hemmer B, Hartung HP, Menge T, Kieseier BC. Long-term B-lymphocyte depletion with rituximab in patients with relapsing-remitting multiple sclerosis. Arch Neurol. 2009; 66:259–261.
   PubMedGoogle Scholar
• Naismith RT, Piccio L, Lyons JA, Lauber J, Tutlam NT, Parks BJ, Trinkaus K, Song SK, Cross AH. Rituximab add-on therapy for breakthrough relapsing multiple sclerosis: A 52-week phase II trial. Neurology. 2010; 74:1860–1867.
   PubMed Web of Science ®Google Scholar
• Dittel BN, Urbania TH, Janeway CAJ. Relapsing and remitting experimental autoimmune encephalomyelitis in B cell deficient mice. J Autoimmun. 2000; 14:311–318.
   Google Scholar
• Mann MK, Maresz K, Shriver LP, Tan Y, Dittel BN. B cell regulation of CD4+CD25+T regulatory cells and IL-10 via B7 is essential for recovery from experimental autoimmune encephalomyelitis. J Immunol. 2007; 178:3447–3456.
   PubMed Web of Science ®Google Scholar
• Wolf SD, Dittel BN, Hardarottir F, Janeway CAJr. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J Exp Med. 1996; 184:2271–2278.
   PubMed Web of Science ®Google Scholar
• Lyons J-A, Ramsbottom MJ, Cross AH. Critical role of antigen-specific antibody in experimental autoimmune encephalomyelitis induced by recombinant myelin oligodendrocyte glycoprotein. Eur J Immunol. 2002; 32:1905–1913.
   PubMed Web of Science ®Google Scholar
• Lyons J-A, San M, Happ MP, Cross AH. B cells are critical to induction of experimental allergic encephalomyelitis by protein but not by a short encephalitogenic peptide. Eur J Immunol. 1999; 29:3432–3439.
   PubMed Web of Science ®Google Scholar
• Oliver AR, Lyon GM, Ruddle NH. Rat and human myelin oligodendrocyte glycoproteins induce experimental autoimmune encephalomyelitis by different mechanisms in C57BL/6 mice. J Immunol. 2003; 171:462–468.
   PubMed Web of Science ®Google Scholar
• Baranzini SE, Jeong MC, Butunoi C, Murray RS, Bernard CCA, Oksenberg JR. B cell repertoire diversity and clonal expansion in multiple sclerosis brain lesions. J Immunol. 1999; 163:5133–5144.
   PubMed Web of Science ®Google Scholar
• Owens GP, Winges KM, Ritchie AM, Edwards S, Burgoon MP, Lehnhoff L, Nielsen K, Corboy J, Gilden DH, Bennett JL. Vh4 gene segments dominate the intrathecal humoral immune response in multiple sclerosis. J Immunol. 2007; 179:6343–6351.
   PubMed Web of Science ®Google Scholar
• Qin Y, Duquette P, Zhang Y, Talbot P, Poole R, Antel JP. Clonal expansion and somatic hypermutation of Vh genes of B cells from cerebrospinal fluid in mulitple sclerosis. J Clin Invest. 1998; 102:1045–1050.
   PubMed Web of Science ®Google Scholar
• Colombo M, Dono M, Gazzola P, Roncella S, Valetto A, Chiorazzi N, Mancardi GL, Ferrarini M. Accumulation of clonally related B lymphocytes in the cerebrospinal fluid of mutliple sclerosis patients. J Immunol. 2000; 164:2782–2789.
   PubMed Web of Science ®Google Scholar
• Harp C, Lee J, Lambracht-Washington D, Cameron E, Olsen G, Frohman E, Racke MK, Monson NL. Cerebrospinal fluid B cells from multiple sclerosis patients are subject to normal germinal center selection. J Neuroimmunol. 2007; 183:189–199.
   Google Scholar
• Devaux B, Enderlin F, Wallner B, Smilek DE. Induction of EAE in mice with recombinant human MOG, and treatment of EAE with MOG peptide. J Neuroimmunol. 1997; 75:169–173.
   PubMed Web of Science ®Google Scholar
• Delassus S, Gey A, Darche S, Cumano A, Roth C, Kourilsky P. PCR-based analysis of the murine immunoglobulin heavy-chain repertoire. J Immunol Meth. 1995; 184:219–229.
   Google Scholar
• Yancopoulos G, Malynn B, Alt F. Developmentally regulated and strain-specific expression of murine Vh gene families. J Exp Med. 1988; 168:417–435.
   PubMedGoogle Scholar
• Pfaffl M. A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res. 2001; 29:2002–2007.
   Google Scholar
• Hjelmström P, Juedes AE, Fjell J, Ruddle NH. B cell-deficient mice develop experimental allergic encephalomyelitis with demyelination after myelin oligodendrocyte glycoprotein sensitization. J Immunol. 1998; 161:4480–4483.
   PubMed Web of Science ®Google Scholar
• Mignon-Godefroy K, Ropars ACB, Charreire J. Ig VH gene family usage in spleen cells of CBA/J mice immunized with experimental autoimmune thyroiditis (EAT) inducer antigens. Autoimmunity. 1993; 14:189–195.
   PubMed Web of Science ®Google Scholar
• Qin Y, Duquette P, Zhang Y, Olek M, Da RR, Richardson J, Antel JP, Talbot P, Cashman NR, Tourtellotte WW, Wekerle H, Van Den Noort S. Intrathecal B cell clonal expansion, an early sign of humoral immunity, in the cerebrospinal fluid of patients with clinically isolated syndrome suggestive of multiple sclerosis. Lab Invest. 2003; 83:1081–1088.
   PubMed Web of Science ®Google Scholar
• Magliozzi R, Columba-Cabezas S, Serafini B, Aloisi F. Intracerebral expression of CXCL13 and BAFF is accompanied by formation of lymphoid follicle-like structures in the meninges of mice with relapsing experimental autoimmune encephalomyelitis. J Neuroimmunol. 2004; 148:11–23.
   PubMed Web of Science ®Google Scholar
• Matsushita T, Yanaba K, Bouaziz JD, Fujimoto M, Tedder TF. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest. 2008; 118:3420–3430.
   PubMed Web of Science ®Google Scholar
• Freitas A, Andrade L, Lembezat M, Coutinho A. Selection of Vh gene repertoires: Differentiating B cells of adult bone marrow mimic fetal development. Inter Immunol. 1990; 2:15–23.
   Google Scholar
• Serafini B, Rosicarelli B, Magliozzi R, Stigliano E, Aloisi F. Detection of ectopic B cell follicles with germinal centers in the meninges of patients with secondary progressive multiple sclerosis. Brain Pathol. 2004; 14:164–174.
   PubMed Web of Science ®Google Scholar
• Male D, Pryce G, Hughes C, Lantos PL. Lymphocyte migration into Brain modelled in vitro: Control by lymphocyte activation, cytokines, and antigen. Cell Immunol. 1990; 127:1–11.
   PubMed Web of Science ®Google Scholar
• Hickey WF, Hsu BL, Kimura J. T-lymphocyte entry into the central nervous system. J Neurosci Res. 1991; 28:254–260.
   PubMed Web of Science ®Google Scholar
• Hickey WF. Basic principles of immunological surveillance of the normal central nervous system. Glia. 2001; 36:118–124.
   PubMed Web of Science ®Google Scholar
• Alter A, Duddy M, Hebert S, Biernacki K, Prat A, Antel JP, Yong VW, Nuttall RK, Pennington CJ, Edwards DR, Bar-Or A. Determinants of human B cell migration across brain endothelial cells. J Immunol. 2003; 170:4497–4505.
   PubMed Web of Science ®Google Scholar
• Cross AH, Stark JL, Lauber J, Ramsbottom MJ, Lyons JA. Rituximab reduces B cells and T cells in cerebrospinal fluid of multiple sclerosis patients. J Neuroimmunol. 2006; 180:63–70.
   PubMed Web of Science ®Google Scholar
• Piccio L, Naismith RT, Trinkaus K, Klein RS, Parks BJ, Lyons JA, Cross AH. Changes in B- and T-lymphocyte and chemokine levels with rituximab treatment in multiple sclerosis. Arch Neurol. 2010; 67:707–714.
   PubMed Web of Science ®Google Scholar
• Watts C, Antoniou A, Manoury B, Hewitt EW, McKay LM, Grayson L, Fairweather NF, Emsley P, Isaacs N, Simitsek PD. Modulation by epitope-specific antibodies of class II MHC-restricted presentation of the tetanus toxin antigen. Immunol Rev. 1998; 164:11–16.
   PubMed Web of Science ®Google Scholar
• Sekiguchi Y, Ichikawa M, Takamoto M, Ota H, Koh CS, Muramatsu M, Honjo T, Agematsu K. Antibodies to myelin oligodendrocyte glycoprotein are not involved in the serverity of chronic non-remitting experiemental autoimmune encephalomyelitis. Immunol Lett. 2009; 122:145–149.
   PubMedGoogle Scholar
• Ichikawa M, Koh CS, Inaba Y, Seki C, Inoue A, Itoh M, Ishihara Y, Bernard CA, Komiyama A. IgG subclass switching is associated with the severity of experimental autoimmune encephalomyelitis induced with myelin oligodendrocyte glycoprotein peptide in NOD mice. Cell Immunol. 1999; 191:97–104.
   PubMedGoogle Scholar
• Schluesener HJ, Sobel RA, Linington C, Weiner HL. A monoclonal antibody against a myelin oligodendrocyte glycoprotein induces relapses and demyelination in central nervous system autoimmune disease. J Immunol. 1987; 139:4016–4021.
   PubMedGoogle Scholar
• Lyons JA, Ramsbottom MJ, Mikesell RJ, Cross AH. B cells limit epitope spreading and reduce severity of EAE induced with PLP peptide in BALB/c mice. J Autoimmun. 2008; 31:149–155.
   Google Scholar