Long-term B cell depletion in murine lupus eliminates autoantibody- secreting cells and is associated with alterations in the kidney plasma cell niche

Journal of Immunology

Volumn 192, Issue 7, 2014, Pages 3011-3020

  Wang, Wensheng ^b   Rangel Moreno, Javier ^a   Owen, Teresa ^a   Barnard, Jennifer ^a   Nevarez, Sarah ^a   Ichikawa, H Travis ^c   Anolik, Jennifer H ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b HENAN NORMAL UNIVERSITY   (China)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APRIL PROTEIN; B CELL ACTIVATING FACTOR; IMMUNOGLOBULIN G; INTERLEUKIN 6; STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; CELL LINE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GERMINAL CENTER; HUMORAL IMMUNE DEFICIENCY; IMMUNOREACTIVITY; KIDNEY; KIDNEY CELL; LYMPHOCYTE COUNT; LYMPHOCYTE MIGRATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANTIBODIES, ANTINUCLEAR; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTIRHEUMATIC AGENTS; AUTOANTIBODIES; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; CELL SURVIVAL; CHEMOKINE CXCL12; FEMALE; FLOW CYTOMETRY; GERMINAL CENTER; INTERLEUKIN-6; KIDNEY; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED NZB; MICE, INBRED STRAINS; MICROSCOPY, FLUORESCENCE; PLASMA CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPLEEN; TIME FACTORS;

EID: 84897535658     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302003     Document Type: Article

References (49)

1. Anolik, J. H. 2007. B cell biology and dysfunction in SLE. Bull. NYU Hosp. Jt. Dis. 65: 182-186.
2. Chan, O., and M. J. Shlomchik. 1998. A new role for B cells in systemic autoimmunity: B cells promote spontaneous T cell activation in MRL-lpr/lpr mice. J. Immunol. 160: 51-59.
3. Shlomchik, M. J., M. P. Madaio, D. Ni, M. Trounstein, and D. Huszar. 1994. The role of B cells in lpr/lpr-induced autoimmunity. J. Exp. Med. 180: 1295-1306.
4. Martin, F., and A. C. Chan. 2004. Pathogenic roles of B cells in human autoimmunity; insights from the clinic. Immunity 20: 517-527.
5. Chan, O. T., L. G. Hannum, A. M. Haberman, M. P. Madaio, and M. J. Shlomchik. 1999. A novel mouse with B cells but lacking serum antibody reveals an antibodyindependent role for B cells in murine lupus. J. Exp. Med. 189: 1639-1648.
6. Harris, D. P., L. Haynes, P. C. Sayles, D. K. Duso, S. M. Eaton, N. M. Lepak, L. L. Johnson, S. L. Swain, and F. E. Lund. 2000. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat. Immunol. 1: 475-482.
7. Anolik, J. H., R. J. Looney, F. E. Lund, T. D. Randall, and I. Sanz. 2009. Insights into the heterogeneity of human B cells: diverse functions, roles in autoimmunity, and use as therapeutic targets. Immunol. Res. 45: 144-158.
8. Bave, U., G. V. Alm, and L. Rönnblom. 2000. The combination of apoptotic U937 cells and lupus IgG is a potent IFN-alpha inducer. J. Immunol. 165: 3519-3526.
9. Leadbetter, E. A., I. R. Rifkin, A. M. Hohlbaum, B. C. Beaudette, M. J. Shlomchik, and A. Marshak-Rothstein. 2002. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416: 603-607.
10. Means, T. K., E. Latz, F. Hayashi, M. R. Murali, D. T. Golenbock, and A. D. Luster. 2005. Human lupus autoantibody-DNA complexes activate DCs through cooperation of CD32 and TLR9. J. Clin. Invest. 115: 407-417.
11. Viglianti, G. A., C. M. Lau, T. M. Hanley, B. A. Miko, M. J. Shlomchik, and A. Marshak-Rothstein. 2003. Activation of autoreactive B cells by CpG dsDNA. Immunity 19: 837-847.
12. Lambert, P. H., and F. J. Dixon. 1968. Pathogenesis of the glomerulonephritis of NZB/W mice. J. Exp. Med. 127: 507-522.
13. Winfield, J. B., I. Faiferman, and D. Koffler. 1977. Avidity of anti-DNA antibodies in serum and IgG glomerular eluates from patients with systemic lupus erythematosus. Association of high avidity antinative DNA antibody with glomerulonephritis. J. Clin. Invest. 59: 90-96.
14. Waldman, M., and M. P. Madaio. 2005. Pathogenic autoantibodies in lupus nephritis. Lupus 14: 19-24.
15. Looney, R. J., J. H. Anolik, D. Campbell, R. E. Felgar, F. Young, L. J. Arend, J. A. Sloand, J. Rosenblatt, and I. Sanz. 2004. B cell depletion as a novel treatment for systemic lupus erythematosus: a phase I/II dose-escalation trial of rituximab. Arthritis Rheum. 50: 2580-2589.
16. Smith, K. G., R. B. Jones, S. M. Burns, and D. R. Jayne. 2006. Long-term comparison of rituximab treatment for refractory systemic lupus erythematosus and vasculitis: remission, relapse, and re-treatment. Arthritis Rheum. 54: 2970-2982.
17. Edwards, J. C., M. J. Leandro, and G. Cambridge. 2002. B-lymphocyte depletion therapy in rheumatoid arthritis and other autoimmune disorders. Biochem. Soc. Trans. 30: 824-828.
18. Anolik, J. H., J. Barnard, T. Owen, B. Zheng, S. Kemshetti, R. J. Looney, and I. Sanz. 2007. Delayed memory B cell recovery in peripheral blood and lymphoid tissue in systemic lupus erythematosus after B cell depletion therapy. Arthritis Rheum. 56: 3044-3056.
19. Sabahi, R., and J. H. Anolik. 2006. B-cell-targeted therapy for systemic lupus erythematosus. Drugs 66: 1933-1948.
20. Merrill, J. T., C. M. Neuwelt, D. J. Wallace, J. C. Shanahan, K. M. Latinis, J. C. Oates, T. O. Utset, C. Gordon, D. A. Isenberg, H. J. Hsieh, et al. 2010. Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: the randomized, double-blind, phase II/III systemic lupus erythematosus evaluation of rituximab trial. Arthritis Rheum. 62: 222-233.
21. Hoyer, B. F., K. Moser, A. E. Hauser, A. Peddinghaus, C. Voigt, D. Eilat, A. Radbruch, F. Hiepe, and R. A. Manz. 2004. Short-lived plasmablasts and long-lived plasma cells contribute to chronic humoral autoimmunity in NZB/W mice. J. Exp. Med. 199: 1577-1584.
22. Winter, O., C. Dame, F. Jundt, and F. Hiepe. 2012. Pathogenic long-lived plasma cells and their survival niches in autoimmunity, malignancy, and allergy. J. Immunol. 189: 5105-5111.
23. Sekine, H., H. Watanabe, and G. S. Gilkeson. 2004. Enrichment of antiglomerular antigen antibody-producing cells in the kidneys of MRL/MpJ-Fas (lpr) mice. J. Immunol. 172: 3913-3921.
24. Lacotte, S., H. Dumortier, M. Décossas, J. P. Briand, and S. Muller. 2010. Identification of new pathogenic players in lupus: autoantibody-secreting cells are present in nephritic kidneys of (NZBxNZW)F1 mice. J. Immunol. 184: 3937-3945.
25. Starke, C., S. Frey, U. Wellmann, V. Urbonaviciute, M. Herrmann, K. Amann, G. Schett, T. Winkler, and R. E. Voll. 2011. High frequency of autoantibodysecreting cells and long-lived plasma cells within inflamed kidneys of NZB/W F1 lupus mice. Eur. J. Immunol. 41: 2107-2112.
26. Espeli, M., S. Bökers, G. Giannico, H. A. Dickinson, V. Bardsley, A. B. Fogo, and K. G. Smith. 2011. Local renal autoantibody production in lupus nephritis. J. Am. Soc. Nephrol. 22: 296-305.
27. DiLillo, D. J., Y. Hamaguchi, Y. Ueda, K. Yang, J. Uchida, K. M. Haas, G. Kelsoe, and T. F. Tedder. 2008. Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J. Immunol. 180: 361-371.
28. Ahuja, A., S. M. Anderson, A. Khalil, and M. J. Shlomchik. 2008. Maintenance of the plasma cell pool is independent of memory B cells. Proc. Natl. Acad. Sci. USA 105: 4802-4807.
29. Bekar, K. W., T. Owen, R. Dunn, T. Ichikawa, W. Wang, R. Wang, J. Barnard, S. Brady, S. Nevarez, B. I. Goldman, et al. 2010. Prolonged effects of short-term anti-CD20 B cell depletion therapy in murine systemic lupus erythematosus. Arthritis Rheum. 62: 2443-2457.
30. Ichikawa, H. T., T. Conley, T. Muchamuel, J. Jiang, S. Lee, T. Owen, J. Barnard, S. Nevarez, B. I. Goldman, C. J. Kirk, et al. 2012. Beneficial effect of novel proteasome inhibitors in murine lupus via dual inhibition of type I interferon and autoantibody-secreting cells. Arthritis Rheum. 64: 493-503.
31. Cassese, G., S. Lindenau, B. de Boer, S. Arce, A. Hauser, G. Riemekasten, C. Berek, F. Hiepe, V. Krenn, A. Radbruch, and R. A. Manz. 2001. Inflamed kidneys of NZB / W mice are a major site for the homeostasis of plasma cells. Eur. J. Immunol. 31: 2726-2732.
32. Cassese, G., S. Arce, A. E. Hauser, K. Lehnert, B. Moewes, M. Mostarac, G. Muehlinghaus, M. Szyska, A. Radbruch, and R. A. Manz. 2003. Plasma cell survival is mediated by synergistic effects of cytokines and adhesion-dependent signals. J. Immunol. 171: 1684-1690.
33. Basso, K., and R. Dalla-Favera. 2010. BCL6: master regulator of the germinal center reaction and key oncogene in B cell lymphomagenesis. Adv. Immunol. 105: 193-210.
34. Ahuja, A., J. Shupe, R. Dunn, M. Kashgarian, M. R. Kehry, and M. J. Shlomchik. 2007. Depletion of B cells in murine lupus: efficacy and resistance. J. Immunol. 179: 3351-3361.
35. Gong, Q., Q. Ou, S. Ye, W. P. Lee, J. Cornelius, L. Diehl, W. Y. Lin, Z. Hu, Y. Lu, Y. Chen, et al. 2005. Importance of cellular microenvironment and circulatory dynamics in B cell immunotherapy. J. Immunol. 174: 817-826.
36. Fairfax, K. A., A. Kallies, S. L. Nutt, and D. M. Tarlinton. 2008. Plasma cell development: from B-cell subsets to long-term survival niches. Semin. Immunol. 20: 49-58.
37. Schiffer, L., R. Bethunaickan, M. Ramanujam, W. Huang, M. Schiffer, H. Tao, M. P. Madaio, E. P. Bottinger, and A. Davidson. 2008. Activated renal macrophages are markers of disease onset and disease remission in lupus nephritis. [Published erratum appears in 2008 J. Immunol. 180: 3613.] J. Immunol. 180: 1938-1947.
38. Hirano, T., T. Taga, N. Nakano, K. Yasukawa, S. Kashiwamura, K. Shimizu, K. Nakajima, K. H. Pyun, and T. Kishimoto. 1985. Purification to homogeneity and characterization of human B-cell differentiation factor (BCDF or BSFp-2). Proc. Natl. Acad. Sci. USA 82: 5490-5494.
39. Chang, A., S. G. Henderson, D. Brandt, N. Liu, R. Guttikonda, C. Hsieh, N. Kaverina, T. O. Utset, S. M. Meehan, R. J. Quigg, et al. 2011. In situ B cellmediated immune responses and tubulointerstitial inflammation in human lupus nephritis. J. Immunol. 186: 1849-1860.
40. Anolik, J. H., J. Barnard, A. Cappione, A. E. Pugh-Bernard, R. E. Felgar, R. J. Looney, and I. Sanz. 2004. Rituximab improves peripheral B cell abnormalities in human systemic lupus erythematosus. Arthritis Rheum. 50: 3580-3590.
41. Mumtaz, I. M., B. F. Hoyer, D. Panne, K. Moser, O. Winter, Q. Y. Cheng, T. Yoshida, G. R. Burmester, A. Radbruch, R. A. Manz, and F. Hiepe. 2012. Bone marrow of NZB/W mice is the major site for plasma cells resistant to dexamethasone and cyclophosphamide: implications for the treatment of autoimmunity. J. Autoimmun. 39: 180-188.
42. Huang, H., C. Benoist, and D. Mathis. 2010. Rituximab specifically depletes short-lived autoreactive plasma cells in a mouse model of inflammatory arthritis. Proc. Natl. Acad. Sci. USA 107: 4658-4663.
43. O'Connor, B. P., V. S. Raman, L. D. Erickson, W. J. Cook, L. K. Weaver, C. Ahonen, L. L. Lin, G. T. Mantchev, R. J. Bram, and R. J. Noelle. 2004. BCMA is essential for the survival of long-lived bone marrow plasma cells. J. Exp. Med. 199: 91-98.
44. Liu, Z., and A. Davidson. 2011. BAFF and selection of autoreactive B cells. Trends Immunol. 32: 388-394.
45. Jacob, C. O., S. Guo, N. Jacob, R. D. Pawar, C. Putterman, W. J. Quinn, III, M. P. Cancro, T. S. Migone, and W. Stohl. 2012. Dispensability of APRIL to the development of systemic lupus erythematosus in NZM 2328 mice. Arthritis Rheum. 64: 1610-1619.
46. Ramanujam, M., R. Bethunaickan, W. Huang, H. Tao, M. P. Madaio, and A. Davidson. 2010. Selective blockade of BAFF for the prevention and treatment of systemic lupus erythematosus nephritis in NZM2410 mice. Arthritis Rheum. 62: 1457-1468.
47. Ramanujam, M., X. Wang, W. Huang, Z. Liu, L. Schiffer, H. Tao, D. Frank, J. Rice, B. Diamond, K. O. Yu, et al. 2006. Similarities and differences between selective and nonselective BAFF blockade in murine SLE. J. Clin. Invest. 116: 724-734.
48. Bethunaickan, R., C. C. Berthier, M. Ramanujam, R. Sahu, W. Zhang, Y. Sun, E. P. Bottinger, L. Ivashkiv, M. Kretzler, and A. Davidson. 2011. A unique hybrid renal mononuclear phagocyte activation phenotype in murine systemic lupus erythematosus nephritis. J. Immunol. 186: 4994-5003.
49. Mahévas, M., P. Patin, F. Huetz, M. Descatoire, N. Cagnard, C. Bole-Feysot, S. Le Gallou, M. Khellaf, O. Fain, D. Boutboul, et al. 2013. B cell depletion in immune thrombocytopenia reveals splenic long-lived plasma cells. J. Clin. Invest. 123: 432-442.