CD19+CD24hiCD38hi B cells maintain regulatory T cells while limiting TH1 and TH17 differentiation

Science Translational Medicine

Volumn 5, Issue 173, 2013, Pages

  Flores Borja, Fabian ^a,b   Bosma, Anneleen ^a   Ng, Dorothy ^a   Reddy, Venkat ^a   Ehrenstein, Michael R ^a   Isenberg, David A ^a   Mauri, Claudia ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD19 ANTIGEN; CD24 ANTIGEN; CD38 ANTIGEN; CD4 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA; INTERLEUKIN 6; INTERLEUKIN 8;

ADULT; AGED; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ACTIVITY; FEMALE; HUMAN; HUMAN CELL; IMMUNOREGULATION; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; T LYMPHOCYTE; TH1 CELL; TH17 CELL; BIOSYNTHESIS; CELL DIFFERENTIATION; CYTOLOGY; IMMUNOLOGY; MIDDLE AGED; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD19; ANTIGENS, CD24; ANTIGENS, CD38; ARTHRITIS, RHEUMATOID; B-LYMPHOCYTES; CELL DIFFERENTIATION; FEMALE; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-6; INTERLEUKIN-8; MALE; MIDDLE AGED; T-LYMPHOCYTES, REGULATORY; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

MLCS; MLOWN;

EID: 84874720574     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3005407     Document Type: Article

References (49)

1. F. E. Lund, T. D. Randall, Effector and regulatory B cells: Modulators of CD4+ T cell immunity. Nat. Rev. Immunol. 10, 236-247 (2010).
2. K. Yanaba, J. D. Bouaziz, K. M. Haas, J. C. Poe, M. Fujimoto, T. F. Tedder, A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 28, 639-650 (2008).
3. P. A. Blair, K. A. Chavez-Rueda, J. G. Evans, M. J. Shlomchik, A. Eddaoudi, D. A. Isenberg, M. R. Ehrenstein, C. Mauri, Selective targeting of B cells with agonistic anti-CD40 is an efficacious strategy for the generation of induced regulatory T2-like B cells and for the suppression of lupus in MRL/lpr mice. J. Immunol. 182, 3492-3502 (2009).
4. P. Neves, V. Lampropoulou, E. Calderon-Gomez, T. Roch, U. Stervbo, P. Shen, A. A. Kühl, C. Loddenkemper, M. Haury, S. A. Nedospasov, S. H. Kaufmann, U. Steinhoff, D. P. Calado, S. Fillatreau, Signaling via the MyD88 adaptor protein in B cells suppresses protective immunity during Salmonella typhimurium infection. Immunity 33, 777-790 (2010).
5. T. Schioppa, R. Moore, R. G. Thompson, E. C. Rosser, H. Kulbe, S. Nedospasov, C. Mauri, L. M. Coussens, F. R. Balkwill, B regulatory cells and the tumor-promoting actions of TNF-a during squamous carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 108, 10662-10667 (2011).
6. C. Mauri, A. Bosma, Immune regulatory function of B cells. Annu. Rev. Immunol. 30, 221-241 (2012).
7. hi B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity 32, 129-140 (2010).
8. S. Lemoine, A. Morva, P. Youinou, C. Jamin, Human T cells induce their own regulation through activation of B cells. J. Autoimmun. 36, 228-238 (2011).
9. J. D. Bouaziz, S. Calbo, M. Maho-Vaillant, A. Saussine, M. Bagot, A. Bensussan, P. Musette, IL-10 produced by activated human B cells regulates CD4+ T-cell activation in vitro. Eur. J. Immunol. 40, 2686-2691 (2010).
10. K. A. Newell, A. Asare, A. D. Kirk, T. D. Gisler, K. Bourcier, M. Suthanthiran, W. J. Burlingham, W. H. Marks, I. Sanz, R. I. Lechler, M. P. Hernandez-Fuentes, L. A. Turka, V. L. Seyfert-Margolis; Immune Tolerance Network ST507 Study Group, Identification of a B cell signature associated with renal transplant tolerance in humans. J. Clin. Invest. 120, 1836-1847 (2010).
11. A. Bosma, A. Abdel-Gadir, D. A. Isenberg, E. C. Jury, C. Mauri, Lipid-antigen presentation by CD1d+ B cells is essential for the maintenance of invariant natural killer T cells. Immunity 36, 477-490 (2012).
12. D. L. Scott, F. Wolfe, T. W. J. Huizinga, Rheumatoid arthritis. Lancet 376, 1094-1108 (2010).
13. J. S. Smolen, K. Redlich, J. Zwerina, D. Aletaha, G. Steiner, G. Schett, Pro-inflammatory cytokines in rheumatoid arthritis: Pathogenetic and therapeutic aspects. Clin. Rev. Allergy Immunol. 28, 239-248 (2005).
14. M. R. Ehrenstein, J. G. Evans, A. Singh, S. Moore, G. Warnes, D. A. Isenberg, C. Mauri, Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFa therapy. J. Exp. Med. 200, 277-285 (2004).
15. R. Singh, A. Aggarwal, R. Misra, Th1/Th17 cytokine profiles in patients with reactive arthritis/undifferentiated spondyloarthropathy. J. Rheumatol. 34, 2285-2290 (2007).
16. X. Valencia, C. Yarboro, G. Illei, P. E. Lipsky, Deficient CD4+CD25high T regulatory cell function in patients with active systemic lupus erythematosus. J. Immunol. 178, 2579-2588 (2007).
17. K. Nistala, L. R. Wedderburn, Th17 and regulatory T cells: Rebalancing pro- and antiinflammatory forces in autoimmune arthritis. Rheumatology 48, 602-606 (2009).
18. E. Bettelli, Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, V. K. Kuchroo, Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441, 235-238 (2006).
19. L. Yang, D. E. Anderson, C. Baecher-Allan, W. D. Hastings, E. Bettelli, M. Oukka, V. K. Kuchroo, D. A. Hafler, L-21 and TGF-b are required for differentiation of human TH17 cells. Nature 454, 350-352 (2008).
20. E. V. Acosta-Rodriguez, L. Rivino, J. Geginat, D. Jarrossay, M. Gattorno, A. Lanzavecchia, F. Sallusto, G. Napolitani, Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 8, 639-646 (2007).
21. S. J. Szabo, S. T. Kim, G. L. Costa, X. Zhang, C. G. Fathman, L. H. Glimcher, A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100, 655-669 (2000).
22. N. A. Carter, R. Vasconcellos, E. C. Rosser, C. Tulone, A. Muñoz-Suano, M. Kamanaka, M. R. Ehrenstein, R. A. Flavell, C. Mauri, Mice lacking endogenous IL-10-producing regulatory B cells develop exacerbated disease and present with an increased frequency of Th1/Th17 but a decrease in regulatory T cells. J. Immunol. 186, 5569-5579 (2011).
23. M. R.Walker, D. J. Kasprowicz, V. H. Gersuk, A. Benard,M. Van Landeghen, J. H. Buckner, S. F. Ziegler, Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25- T cells. J. Clin. Invest. 112, 1437-1443 (2003).
24. V. Pillai, S. B. Ortega, C. K. Wang, N. J. Karandikar, Transient regulatory T-cells: A state attained by all activated human T-cells. Clin. Immunol. 123, 18-29 (2007).
25. D. Q. Tran, H. Ramsey, E. M. Shevach, Induction of FOXP3 expression in naive human CD4+FOXP3- T cells by T-cell receptor stimulation is transforming growth factorb- dependent but does not confer a regulatory phenotype. Blood 110, 2983-2990 (2007).
26. W. Liu, A. L. Putnam, Z. Xu-Yu, G. L. Szot, M. R. Lee, S. Zhu, P. A. Gottlieb, P. Kapranov, T. R. Gingeras, B. Fazekas de St Groth, C. Clayberger, D. M. Soper, S. F. Ziegler, J. A. Bluestone, CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J. Exp. Med. 203, 1701-1711 (2006).
27. M. Gray, K. Miles, D. Salter, D. Gray, J. Savill, Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc. Natl. Acad. Sci. U.S.A. 104, 14080-14085 (2007).
28. J. S. Smolen, F. C. Breedveld, M. H. Schiff, J. R. Kalden, P. Emery, G. Eberl, P. L. van Riel, P. Tugwell, A simplified disease activity index for rheumatoid arthritis for use in clinical practice. Rheumatology 42, 244-257 (2003).
29. R. K. Mallya, F. C. de Beer, H. Berry, E. D. Hamilton, B. E. Mace, M. B. Pepys, Correlation of clinical parameters of disease activity in rheumatoid arthritis with serum concentration of C-reactive protein and erythrocyte sedimentation rate. J. Rheumatol. 9, 224-228 (1982).
30. Y. Iwata, T. Matsushita, M. Horikawa, D. J. Dilillo, K. Yanaba, G. M. Venturi, P. M. Szabolcs, S. H. Bernstein, C. M. Magro, A. D. Williams, R. P. Hall, E. W. St Clair, T. F. Tedder, Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 117, 530-541 (2011).
31. M. Kallikourdis, K. G. Andersen, K. A. Welch, A. G. Betz, Alloantigen-enhanced accumulation of CCR5+ 'effector' regulatory T cells in the gravid uterus. Proc. Natl. Acad. Sci. U.S.A. 104, 594-599 (2007).
32. K. Wing, S. Sakaguchi, Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat. Immunol. 11, 7-13 (2010).
33. X. Valencia, G. Stephens, R. Goldbach-Mansky, M. Wilson, E. M. Shevach, P. E. Lipsky, TNF downmodulates the function of human CD4+CD25hi T-regulatory cells. Blood 108, 253-261 (2006).
34. M. Murai, O. Turovskaya, G. Kim, R. Madan, C. L. Karp, H. Cheroutre, M. Kronenberg, Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat. Immunol. 10, 1178-1184 (2009).
35. S. Akira, T. Hirano, T. Taga, T. Kishimoto, Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF). FASEB J. 4, 2860-2867 (1990).
36. Y. Chung, S. H. Chang, G. J. Martinez, X. O. Yang, R. Nurieva, H. S. Kang, L. Ma, S. S. Watowich, A. M. Jetten, Q. Tian, C. Dong, Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 30, 576-587 (2009).
37. T. Korn, M. Mitsdoerffer, A. L. Croxford, A. Awasthi, V. A. Dardalhon, G. Galileos, P. Vollmar, G. L. Stritesky, M. H. Kaplan, A. Waisman, V. K. Kuchroo, M. Oukka, IL-6 controls Th17 immunity in vivo by inhibiting the conversion of conventional T cells into Foxp3+ regulatory T cells. Proc. Natl. Acad. Sci. U.S.A. 105, 18460-18465 (2008).
38. E. Murphy, K. Shibuya, N. Hosken, P. Openshaw, V. Maino, K. Davis, K. Murphy, A. O'Garra, Reversibility of T helper 1 and 2 populations is lost after long-term stimulation. J. Exp. Med. 183, 901-913 (1996).
39. L. S. Miller, J. S. Cho, Immunity against Staphylococcus aureus cutaneous infections. Nat. Rev. Immunol. 11, 505-518 (2011).
40. A. Yoshizaki, T. Miyagaki, D. J. DiLillo, T. Matsushita, M. Horikawa, E. I. Kountikov, R. Spolski, J. C. Poe, W. J. Leonard, T. F. Tedder, Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 491, 264-268 (2012).
41. R. Carsetti, M. M. Rosado, H. Wardmann, Peripheral development of B cells in mouse and man. Immunol. Rev. 197, 179-191 (2004).
42. C. R. Wang, M. F. Liu, Regulation of CCR5 expression and MIP-1a production in CD4+ T cells from patients with rheumatoid arthritis. Clin. Exp. Immunol. 132, 371-378 (2003).
43. D. D. Patel, J. P. Zachariah, L. P. Whichard, CXCR3 and CCR5 ligands in rheumatoid arthritis synovium. Clin. Immunol. 98, 39-45 (2001).
44. M. Henneken, T. Dörner, G. R. Burmester, C. Berek, Differential expression of chemokine receptors on peripheral blood B cells from patients with rheumatoid arthritis and systemic lupus erythematosus. Arthritis Res. Ther. 7, R1001-R1013 (2005).
45. T. Nanki, K. Takada, Y. Komano, T. Morio, H. Kanegane, A. Nakajima, P. E. Lipsky, N. Miyasaka, Chemokine receptor expression and functional effects of chemokines on B cells: Implication in the pathogenesis of rheumatoid arthritis. Arthritis Res. Ther. 11, R149 (2009).
46. K. E. Balashov, J. B. Rottman, H. L. Weiner, W. W. Hancock, CCR5+ and CXCR3+ T cells are increased in multiple sclerosis and their ligands MIP-1a and IP-10 are expressed in demyelinating brain lesions. Proc. Natl. Acad. Sci. U.S.A. 96, 6873-6878 (1999).
47. C. A. Wysocki, Q. Jiang, A. Panoskaltsis-Mortari, P. A. Taylor, K. P. McKinnon, L. Su, B. R. Blazar, J. S. Serody, Critical role for CCR5 in the function of donor CD4+CD25+ regulatory T cells during acute graft-versus-host disease. Blood 106, 3300-3307 (2005).
48. D. Aletaha, T. Neogi, A. J. Silman, J. Funovits, D. T. Felson, C. O. Bingham III, N. S. Birnbaum, G. R. Burmester, V. P. Bykerk, M. D. Cohen, B. Combe, K. H. Costenbader, M. Dougados, P. Emery, G. Ferraccioli, J. M. Hazes, K. Hobbs, T. W. Huizinga, A. Kavanaugh, J. Kay, T. K. Kvien, T. Laing, P. Mease, H. A. Ménard, L. W. Moreland, R. L. Naden, T. Pincus, J. S. Smolen, E. Stanislawska-Biernat, D. Symmons, P. P. Tak, K. S. Upchurch, J. Vencovský, F. Wolfe, G. Hawker, 2010 Rheumatoid arthritis classification criteria: An American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum. 62, 2569-2581 (2010).
49. J. Zhu, B. Min, J. Hu-Li, C. J. Watson, A. Grinberg, Q. Wang, N. Killeen, J. F. Urban Jr., L. Guo, W. E. Paul, Conditional deletion of Gata3 shows its essential function in TH1-TH2 responses. Nat. Immunol. 5, 1157-1165 (2004).