Regulatory CD4+ T Cells Promote B Cell Anergy in Murine Lupus

Journal of Immunology

Volumn 192, Issue 9, 2014, Pages 4069-4073

  Liu, Yaoyang ^a   Liu, Aijing ^a,b   Iikuni, Noriko ^a   Xu, Huji ^c   Shi, Fu Dong ^d   La Cava, Antonio ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HEBEI MEDICAL UNIVERSITY   (China)

^c SECOND MILITARY MEDICAL UNIVERSITY   (China)

^d BARROW NEUROLOGICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD86 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DOUBLE STRANDED DNA ANTIBODY; IMMUNOGLOBULIN G ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ANTIBODY TITER; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM TRANSPORT; CD4+ T LYMPHOCYTE; CLONAL ANERGY; CONTROLLED STUDY; FEMALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; ANTIBODY FORMATION; AUTOANTIBODIES; AUTOIMMUNITY; B-LYMPHOCYTES; CELL SEPARATION; CLONAL ANERGY; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICE, INBRED BALB C; T-LYMPHOCYTES, REGULATORY;

EID: 84899501967     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302897     Document Type: Article

References (28)

1. Goodnow, C. C., R. Brink, and E. Adams. 1991. Breakdown of self-tolerance in anergic B lymphocytes. Nature 352: 532-536
2. Merrell, K. T., R. J. Benschop, S. B. Gauld, K. Aviszus, D. Decote-Ricardo, L. J. Wysocki, and J. C. Cambier. 2006. Identification of anergic B cells within a wild-type repertoire. Immunity 25: 953-962
3. Wardemann, H., S. Yurasov, A. Schaefer, J. W. Young, E. Meffre, and M. C. Nussenzweig. 2003. Predominant autoantibody production by early human B cell precursors. Science 301: 1374-1377
4. Iikuni, N., E. V. Lourenço, B. H. Hahn, and A. La Cava. 2009. Cutting edge: Regulatory T cells directly suppress B cells in systemic lupus erythematosus. J. Immunol. 183: 1518-1522
5. Lim, H. W., P. Hillsamer, A. H. Banham, and C. H. Kim. 2005. Cutting edge: Direct suppression of B cells by CD4+ CD25+ regulatory T cells. J. Immunol. 175: 4180-4183
6. Yurasov, S., H. Wardemann, J. Hammersen, M. Tsuiji, E. Meffre, V. Pascual, and M. C. Nussenzweig. 2005. Defective B cell tolerance checkpoints in systemic lupus erythematosus. J. Exp. Med. 201: 703-711
7. Quách, T. D., N. Manjarrez-Orduño, D. G. Adlowitz, L. Silver, H. Yang, C. Wei, E. C. Milner, and I. Sanz. 2011. Anergic responses characterize a large fraction of human autoreactive naive B cells expressing low levels of surface IgM. J. Immunol. 186: 4640-4648
8. Duty, J. A., P. Szodoray, N. Y. Zheng, K. A. Koelsch, Q. Zhang, M. Swiatkowski, M. Mathias, L. Garman, C. Helms, B. Nakken, et al. 2009. Functional anergy in a subpopulation of naive B cells from healthy humans that express autoreactive immunoglobulin receptors. J. Exp. Med. 206: 139-151
9. Karpouzas, G. A., A. La Cava, F. M. Ebling, R. R. Singh, and B. H. Hahn. 2004. Differences between CD8+ T cells in lupus-prone (NZB x NZW) F1 mice and healthy (BALB/c x NZW) F1 mice may influence autoimmunity in the lupus model. Eur. J. Immunol. 34: 2489-2499
10. La Cava, A., F. M. Ebling, and B. H. Hahn. 2004. Ig-reactive CD4+CD25+ T cells from tolerized (New Zealand Black x New Zealand White)F1 mice suppress in vitro production of antibodies to DNA. J. Immunol. 173: 3542-3548
11. Chung, J. B., A. D. Wells, S. Adler, A. Jacob, L. A. Turka, and J. G. Monroe. 2003. Incomplete activation of CD4 T cells by antigen-presenting transitional immature B cells: Implications for peripheral B and T cell responsiveness. J. Immunol. 171: 1758-1767
12. Yarkoni, Y., A. Getahun, and J. C. Cambier. 2010. Molecular unDerpinning of Bcell anergy. Immunol. Rev. 237: 249-263
13. Rathmell, J. C., S. Fournier, B. C. Weintraub, J. P. Allison, and C. C. Goodnow. 1998. Repression of B7.2 on self-reactive B cells is essential to prevent proliferation and allow Fas-mediated deletion by CD4+ T cells. J. Exp. Med. 188: 651-659
14. Melchers, F. 2006. Anergic B cells caught in the act. Immunity 25: 864-867
15. Wallace, D. J. 2007. Serum and plasma protein abnormalities and other clinical laboratory determinations in systemic lupus erythematosus. In Dubois? Lupus Erythematosus, 7th Ed., D. J. Wallace, and B. H. Hahn, eds. Lippincott Williams & Wilkins, Philadelphia, PA, p. 911-919
16. Levy, J., E. V. Barnett, N. S. MacDonald, and J. R. Klinenberg. 1970. Altered immunoglobulin metabolism in systemic lupus erythematosus and rheumatoid arthritis. J. Clin. Invest. 49: 708-715
17. Lenschow, D. J., T. L. Walunas, and J. A. Bluestone. 1996. CD28/B7 system of T cell costimulation. Annu. Rev. Immunol. 14: 233-258
18. Jeannin, P., Y. Delneste, S. Lecoanet-Henchoz, J. F. Gauchat, J. Ellis, and J. Y. Bonnefoy. 1997. CD86 (B7-2) on human B cells. A functional role in proliferation and selective differentiation into IgE- and IgG4-producing cells. J. Biol. Chem. 272: 15613-15619
19. Parker, D. C. 1993. T cell-dependent B cell activation. Annu. Rev. Immunol. 11: 331-360
20. Stuber, E., M. Neurath, D. CalDerhead, H. P. Fell, and W. Strober. 1995. Crosslinking of OX40 ligand, a member of the TNF/NGF cytokine family, induces proliferation and differentiation in murine splenic B cells. Immunity 2: 507-521
21. Cambier, J. C., S. B. Gauld, K. T. Merrell, and B. J. Vilen. 2007. B-cell anergy: From transgenic models to naturally occurring anergic B cells? Nat. Rev. Immunol. 7: 633-643
22. Oliver, P. M., T. Vass, J. Kappler, and P. Marrack. 2006. Loss of the proapoptotic protein, Bim, breaks B cell anergy. J. Exp. Med. 203: 731-741
23. Nickerson, K. M., S. R. Christensen, J. L. Cullen, W. Meng, E. T. Luning Prak, and M. J. Shlomchik. 2013. TLR9 promotes tolerance by restricting survival of anergic anti-DNA B cells, yet is also required for their activation. J. Immunol. 190: 1447-1456
24. Liubchenko, G. A., H. C. Appleberry, V. M. Holers, N. K. Banda, V. C. Willis, and T. Lyubchenko. 2012. Potentially autoreactive naturally occurring transitional T3 B lymphocytes exhibit a unique signaling profile. J. Autoimmun. 38: 293-303
25. Seo, S. J., M. L. Fields, J. L. Buckler, A. J. Reed, L. Mandik-Nayak, S. A. Nish, R. J. Noelle, L. A. Turka, F. D. Finkelman, A. J. Caton, and J. Erikson. 2002. The impact of T helper and T regulatory cells on the regulation of anti-doublestranded DNA B cells. Immunity 16: 535-546
26. Liubchenko, G. A., H. C. Appleberry, C. C. Striebich, K. E. Franklin, L. A. Derber, V. M. Holers, and T. Lyubchenko. 2013. Rheumatoid arthritis is associated with signaling alterations in naturally occurring autoreactive B-lymphocytes. J. Autoimmun. 40: 111-121
27. Leonardo, S.M., J. A. Josephson, N. L. Hartog, and S. B. Gauld. 2010. Altered B cell development and anergy in the absence of Foxp3. J. Immunol. 185: 2147-2156
28. La Cava, A. 2008. T-regulatory cells in systemic lupus erythematosus. Lupus 17: 421-425