CD20+ B Cell Depletion Alters T Cell Homing

Journal of Immunology

Volumn 192, Issue 9, 2014, Pages 4242-4253

  Kap, Yolanda S ^a,b   Van Driel, Nikki ^a   Laman, Jon D ^b   Tak, Paul P ^c,e   Hart, Bert A ^a,b,d  

^a BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^e GLAXOSMITHKLINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

APRIL PROTEIN; B CELL ACTIVATING FACTOR; B7 ANTIGEN; CD20 ANTIGEN; CD40 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR7; INTERLEUKIN 7 RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD20; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ARTICLE; CALLITHRIX; CELL ISOLATION; CONTROLLED STUDY; DRUG MECHANISM; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FLOW CYTOMETRY; HISTOPATHOLOGY; HUMORAL IMMUNE DEFICIENCY; IMMUNOSTIMULATION; LYMPHOCYTE HOMING; LYMPHOID ORGAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SINGLE DRUG DOSE; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD20; B-LYMPHOCYTES; CALLITHRIX; CHEMOTAXIS, LEUKOCYTE; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE DEPLETION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES;

EID: 84899581695     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303125     Document Type: Article

References (49)

1. Dörner, T., N. Kinnman, and P. P. Tak. 2010. Targeting B cells in immunemediated inflammatory disease: A comprehensive review of mechanisms of action and identification of biomarkers. Pharmacol. Ther. 125: 464-475
2. Edwards, J. C., L. Szczepanski, J. Szechinski, A. Filipowicz-Sosnowska, P. Emery, D. R. Close, R. M. Stevens, and T. Shaw. 2004. Efficacy of B-celltargeted therapy with rituximab in patients with rheumatoid arthritis. N. Engl. J. Med. 350: 2572-2581
3. Tak, P. P., W. F. Rigby, A. Rubbert-Roth, C. G. Peterfy, R. F. Van Vollenhoven, W. Stohl, E. Hessey, A. Chen, H. Tyrrell, and T. M. Shaw; IMAGE Investigators. 2011. Inhibition of joint damage and improved clinical outcomes with rituximab plus methotrexate in early active rheumatoid arthritis: The IMAGE trial. Ann. Rheum. Dis. 70: 39-46
4. Hauser, S. L., E. Waubant, D. L. Arnold, T. Vollmer, J. Antel, R. J. Fox, A. Bar-Or, M. Panzara, N. Sarkar, S. Agarwal, et al; HERMES Trial Group. 2008. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N. Engl. J. Med. 358: 676-688
5. Bar-Or, A., P. A. Calabresi, D. Arnold, C. Markowitz, S. Shafer, L. H. Kasper, E. Waubant, S. Gazda, R. J. Fox, M. Panzara, et al. 2008. Rituximab in relapsingremitting multiple sclerosis: A 72-week, open-label, phase I trial. [Published erratum appears in 2008 Ann. Neurol. 63: 803.] Ann. Neurol. 63: 395-400
6. Barun, B., and A. Bar-Or. 2012. Treatment of multiple sclerosis with anti-CD20 antibodies. Clin. Immunol. 142: 31-37
7. Reddy, V., D. Jayne, D. Close, and D. Isenberg. 2013. B-cell depletion in SLE: Clinical and trial experience with rituximab and ocrelizumab and implications for study design. Arthritis Res. Ther. 15(Suppl. 1): S2
8. Gottenberg, J. E., G. Cinquetti, C. Larroche, B. Combe, E. Hachulla, O. Meyer, E. Pertuiset, G. Kaplanski, L. Chiche, J. M. Berthelot, et al; Club Rhumatismes et Inflammations and the French Society of Rheumatology. 2013. Efficacy of rituximab in systemic manifestations of primary Sjogren?s syndrome: Results in 78 patients of the AutoImmune and Rituximab registry. Ann. Rheum. Dis. 72: 1026-1031
9. Furie, R., M. Petri, O. Zamani, R. Cervera, D. J. Wallace, D. Tegzová, J. Sanchez-Guerrero, A. Schwarting, J. T. Merrill, W. W. Chatham, et al; BLISS-76 Study Group. 2011. A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum. 63: 3918-3930
10. Navarra, S. V., R. M. Guzmán, A. E. Gallacher, S. Hall, R. A. Levy, R. E. Jimenez, E. K. Li, M. Thomas, H. Y. Kim, M. G. León, et al; BLISS-52 Study Group. 2011. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: A randomised, placebo-controlled, phase 3 trial. Lancet 377: 721-731
11. Hartung, H. P., and B. C. Kieseier. 2010. Atacicept: Targeting B cells in multiple sclerosis. Ther. Adv. Neurol. Disord. 3: 205-216
12. Genovese, M. C., N. Kinnman, G. De La Bourdonnaye, C. Pena Rossi, and P. P. Tak. 2011. Atacicept in patients with rheumatoid arthritis and an inadequate response to tumor necrosis factor antagonist therapy: Results of a phase II, randomized, placebo-controlled, dose-finding trial. Arthritis Rheum. 63: 1793-1803
13. Genovese, M. C., R. M. Fleischmann, M. Greenwald, J. Satterwhite, M. Veenhuizen, L. Xie, P. Y. Berclaz, S. Myers, and O. Benichou. 2013. Tabalumab, an anti-BAFF monoclonal antibody, in patients with active rheumatoid arthritis with an inadequate response to TNF inhibitors. Ann. Rheum. Dis. 72: 1461-1468
14. Genovese, M. C., E. Lee, J. Satterwhite, M. Veenhuizen, D. Disch, P. Y. Berclaz, S. Myers, G. Sides, and O. Benichou. 2013. A phase 2 dose-ranging study of subcutaneous tabalumab for the treatment of patients with active rheumatoid arthritis and an inadequate response to methotrexate. Ann. Rheum. Dis. 72: 1453-1460
15. Kap, Y. S., J. D. Laman, and B. A. ?t Hart. 2010. Experimental autoimmune encephalomyelitis in the common marmoset, a bridge between rodent EAE and multiple sclerosis for immunotherapy development. J. Neuroimmune Pharmacol. 5: 220-230
16. Kap, Y. S., N. Van Driel, E. Blezer, P. W. Parren, W. K. Bleeker, J. D. Laman, J. L. Craigen, and B. A. ?t Hart. 2010. Late B cell depletion with a human antihuman CD20 IgG1k monoclonal antibody halts the development of experimental autoimmune encephalomyelitis in marmosets. J. Immunol. 185: 3990-4003
17. Kap, Y. S., J. Bauer, Nv. Driel, W. K. Bleeker, P. W. Parren, E. J. Kooi, J. J. Geurts, J. D. Laman, J. L. Craigen, E. Blezer, and B. A. ?t Hart. 2011. B-cell depletion attenuates white and gray matter pathology in marmoset experimental autoimmune encephalomyelitis. J. Neuropathol. Exp. Neurol. 70: 992-1005
18. Jagessar, S. A., N. Heijmans, L. Oh, J. Bauer, E. L. Blezer, J. D. Laman, T. S. Migone, M. N. Devalaraja, and B. A. ?t Hart. 2012. Antibodies against human BLyS and APRIL attenuate EAE development in marmoset monkeys. [Published erratum appears in 2013 J. Neuroimmune Pharmacol. 8: 370.] J. Neuroimmune Pharmacol. 7: 557-570
19. Thurlings, R. M., K. Vos, C. A. Wijbrandts, A. H. Zwinderman, D. M. Gerlag, and P. P. Tak. 2008. Synovial tissue response to rituximab: Mechanism of action and identification of biomarkers of response. Ann. Rheum. Dis. 67: 917-925
20. Bar-Or, A., L. Fawaz, B. Fan, P. J. Darlington, A. Rieger, C. Ghorayeb, P. A. Calabresi, E. Waubant, S. L. Hauser, J. Zhang, and C. H. Smith. 2010. Abnormal B-cell cytokine responses a trigger of T-cell-mediated disease in MS? Ann. Neurol. 67: 452-461
21. Matsushita, T., M. Horikawa, Y. Iwata, and T. F. Tedder. 2010. Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J. Immunol. 185: 2240-2252
22. Matsushita, T., K. Yanaba, J. D. Bouaziz, M. Fujimoto, and T. F. Tedder. 2008. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J. Clin. Invest. 118: 3420-3430
23. Duddy, M., M. Niino, F. Adatia, S. Hebert, M. Freedman, H. Atkins, H. J. Kim, and A. Bar-Or. 2007. Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. J. Immunol. 178: 6092-6099
24. Wood, K. J., A. Bushell, and J. Hester. 2012. Regulatory immune cells in transplantation. Nat. Rev. Immunol. 12: 417-430
25. Harp, C. T., S. Ireland, L. S. Davis, G. Remington, B. Cassidy, P. D. Cravens, O. Stuve, A. E. Lovett-Racke, T. N. Eagar, B. M. Greenberg, et al. 2010. Memory B cells from a subset of treatment-näve relapsing-remitting multiple sclerosis patients elicit CD4(+) T-cell proliferation and IFN-g production in response to myelin basic protein and myelin oligodendrocyte glycoprotein. Eur. J. Immunol. 40: 2942-2956
26. Jagessar, S. A., M. Vierboom, E. L. Blezer, J. Bauer, B. A. Hart, and Y. S. Kap. 2013. Overview of models, methods, and reagents developed for translational autoimmunity research in the common marmoset (Callithrix jacchus). Exp. Anim. 62: 159-171
27. Beillard, E., N. Pallisgaard, V. H.Van Der Velden, W. Bi, R. Dee, E.Van Der Schoot, E. Delabesse, E. Macintyre, E. Gottardi, G. Saglio, et al. 2003. Evaluation of candidate control genes for diagnosis and residual disease detection in leukemic patients using real-time quantitative reverse- transcriptase polymerase chain reaction (RQ-PCR) -a Europe against cancer program. Leukemia 17: 2474-2486
28. De Vos, A. F., D. A. Van Riel, M. Van Meurs, H. P. Brok, L. Boon, R. Q. Hintzen, E. Claassen, B. A. ?t Hart, and J. D. Laman. 2005. Severe T-cell depletion from the PALS leads to altered spleen composition in common marmosets with experimental autoimmune encephalomyelitis (EAE). J. Neuroimmunol. 161: 29-39
29. Förster, R., A. C. Davalos-Misslitz, and A. Rot. 2008. CCR7 and its ligands: Balancing immunity and tolerance. Nat. Rev. Immunol. 8: 362-371
30. Jagessar, S. A., N. Heijmans, E. L. Blezer, J. Bauer, J. H. Blokhuis, J. A. Wubben, J. W. Drijfhout, P. J.Van Den Elsen, J. D. Laman, and B. A. Hart. 2012. Unravelling the T-cell-mediated autoimmune attack on CNS myelin in a new primate EAE model induced with MOG34-56 peptide in incomplete adjuVant. Eur. J. Immunol. 42: 217-227
31. Lechmann, M., E. Zinser, A. Golka, and A. Steinkasserer. 2002. Role of CD83 in the immunomodulation of dendritic cells. Int. Arch. Allergy Immunol. 129: 113-118
32. Teeling, J. L., R. R. French, M. S. Cragg, J.Van Den Brakel, M. Pluyter, H. Huang, C. Chan, P. W. Parren, C. E. Hack, M. Dechant, et al. 2004. Characterization of new human CD20 monoclonal antibodies with potent cytolytic activity against non-Hodgkin lymphomas. Blood 104: 1793-1800
33. Bleeker, W. K., M. E. Munk, W. J. Mackus, J. H.Van Den Brakel, M. Pluyter, M. J. Glennie, J. G.Van De Winkel, and P. W. Parren. 2008. Estimation of dose requirements for sustained in vivo activity of a therapeutic human anti-CD20 antibody. Br. J. Haematol. 140: 303-312
34. Unsoeld, H., D. Voehringer, S. Krautwald, and H. Pircher. 2004. Constitutive expression of CCR7 directs effector CD8 T cells into the splenic white pulp and impairs functional activity. J. Immunol. 173: 3013-3019
35. Tan, J. T., E. Dudl, E. LeRoy, R. Murray, J. Sprent, K. I. Weinberg, and C. D. Surh. 2001. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc. Natl. Acad. Sci. USA 98: 8732-8737
36. Ashbaugh, J. J., R. Brambilla, S. A. Karmally, C. Cabello, T. R. Malek, and J. R. Bethea. 2013. IL7Ra contributes to experimental autoimmune encephalomyelitis through altered T cell responses and nonhematopoietic cell lineages. J. Immunol. 190: 4525-4534
37. Lund, F. E., and T. D. Randall. 2010. Effector and regulatory B cells: Modulators of CD4+ T cell immunity. Nat. Rev. Immunol. 10: 236-247
38. Sfikakis, P. P., V. L. Souliotis, K. G. Fragiadaki, H. M. Moutsopoulos, J. N. Boletis, and A. N. Theofilopoulos. 2007. Increased expression of the FoxP3 functional marker of regulatory T cells following B cell depletion with rituximab in patients with lupus nephritis. Clin. Immunol. 123: 66-73
39. Vallerskog, T., I. Gunnarsson, M. Widhe, A. Risselada, L. Klareskog, R. Van Vollenhoven, V. Malmström, and C. Trollmo. 2007. Treatment with rituximab affects both the cellular and the humoral arm of the immune system in patients with SLE. Clin. Immunol. 122: 62-74
40. Hu, C. Y., D. Rodriguez-Pinto, W. Du, A. Ahuja, O. Henegariu, F. S. Wong, M. J. Shlomchik, and L. Wen. 2007. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J. Clin. Invest. 117: 3857-3867
41. Weber, M. S., T. Prod?homme, J. C. Patarroyo, N. Molnarfi, T. Karnezis, K. Lehmann-Horn, D. M. Danilenko, J. Eastham-Anderson, A. J. Slavin, C. Linington, et al. 2010. B-cell activation influences T-cell polarization and outcome of anti-CD20 B-cell depletion in central nervous system autoimmunity. Ann. Neurol. 68: 369-383
42. Anwar Jagessar, S., Z. Fagrouch, N. Heijmans, J. Bauer, J. D. Laman, L. Oh, T. Migone, E. J. Verschoor, and B. A. ?t Hart. 2013. The different clinical effects of anti-BLyS, anti-APRIL and anti-CD20 antibodies point at a critical pathogenic role of g-herpesvirus infected B cells in the marmoset EAE model. J. Neuroimmune Pharmacol. 8: 727-738
43. Lunemann, J D., and C. Munz. 2009. EBV in MS: Guilty by association? Trends Immunol. 30: 243-248
44. t Hart, B. A., S. A. Jagessar, K. Haanstra, E. Verschoor, J. D. Laman, and Y. S. Kap. 2013. The primate EAE model points at EBV-infected B cells as a preferential therapy target in multiple sclerosis. Front. Immunol. 4: 145
45. Chijioke, O., T. Azzi, D. Nadal, and C. Munz. 2013. Innate immune responses against Epstein Barr virus infection. J. Leukoc. Biol. 94: 1185-1190
46. Haanstra, K. G., J. A. Wubben, M. Jonker, and B. A. ?t Hart. 2013. Induction of encephalitis in rhesus monkeys infused with lymphocryptovirus- infected B-cells presenting MOG(34-56) peptide. PLoS ONE 8: E71549
47. Ariza, M. E., R. Glaser, P. T. Kaumaya, C. Jones, and M. V. Williams. 2009. The EBV-encoded dUTPase activates NF-kappa B through the TLR2 and MyD88-dependent signaling pathway. J. Immunol. 182: 851-859
48. Ariza, M. E., P. Rivailler, R. Glaser, M. Chen, and M. V. Williams. 2013. Epstein-Barr virus encoded dUTPase containing exosomes modulate innate and adaptive immune responses in human dendritic cells and peripheral blood mononuclear cells. PLoS ONE 8: E69827
49. Dudziak, D., A. Kieser, U. Dirmeier, F. Nimmerjahn, S. Berchtold, A. Steinkasserer, G. Marschall, W. Hammerschmidt, G. Laux, and G. W. Bornkamm. 2003. Latent membrane protein 1 of Epstein-Barr virus induces CD83 by the NF-kappaB signaling pathway. J. Virol. 77: 8290-8298