B cells expressing CD11b effectively inhibit CD4+ T-cell responses and ameliorate experimental autoimmune hepatitis in mice

Hepatology

Volumn 62, Issue 5, 2015, Pages 1563-1575

  Liu, Xiaoming ^a   Jiang, Xuechao ^a   Liu, Ronghua ^a   Wang, Luman ^a   Qian, Tingting ^a   Zheng, Yijie ^a   Deng, Yuting ^a   Huang, Enyu ^a   Xu, Fengkai ^b   Wang, Ji Yang ^a   Chu, Yiwei ^a  

^a FUDAN UNIVERSITY   (China)

^b ZHONGSHAN HOSPITAL OF FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD4 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; T LYMPHOCYTE RECEPTOR; CD20 ANTIGEN; IL10 PROTEIN, MOUSE;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNE HEPATITIS; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DOWN REGULATION; EXPERIMENTAL AUTOIMMUNE HEPATITIS; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; HEPATITIS, AUTOIMMUNE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PHYSIOLOGY;

ANIMALS; ANTIGENS, CD11B; ANTIGENS, CD20; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; HEPATITIS, AUTOIMMUNE; INTERFERON-GAMMA; INTERLEUKIN-10; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL;

EID: 84945199443     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.28001     Document Type: Article

References (63)

1. Lund FE, Randall TD. Effector and regulatory B cells: modulators of CD4+ T cell immunity. Nat Rev Immunol 2010;10:236-247.
2. Yang M, Rui K, Wang S, Lu L. Regulatory B cells in autoimmune diseases. Cell Mol Immunol 2013;10:122-132.
3. Yanaba K, Bouaziz JD, Haas KM, Poe JC, Fujimoto M, Tedder TF. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 2008;28:639-650.
4. Mauri C, Gray D, Mushtaq N, Londei M. Prevention of arthritis by interleukin 10-producing B cells. J Exp Med 2003;197:489-501.
5. Sattler S, Ling GS, Xu D, Hussaarts L, Romaine A, Zhao H, et al. IL-10-producing regulatory B cells induced by IL-33 (Breg(IL-33)) effectively attenuate mucosal inflammatory responses in the gut. J Autoimmun 2014;50:107-122.
6. Yoshizaki A, Miyagaki T, DiLillo DJ, Matsushita T, Horikawa M, Kountikov EI, et al. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 2012;491:264-268.
7. Zha B, Wang L, Liu X, Liu J, Chen Z, Xu J, et al. Decrease in proportion of CD19+ CD24(hi) CD27+ B cells and impairment of their suppressive function in Graves' disease. PLoS One 2012;7:e49835.
8. Bankoti R, Gupta K, Levchenko A, Stager S. Marginal zone B cells regulate antigen-specific T cell responses during infection. J Immunol 2012;188:3961-3971.
9. Ding Q, Yeung M, Camirand G, Zeng Q, Akiba H, Yagita H, et al. Regulatory B cells are identified by expression of TIM-1 and can be induced through TIM-1 ligation to promote tolerance in mice. J Clin Invest 2011;121:3645-3656.
10. Goode I, Xu H, Ildstad ST. Regulatory B cells: the new "it" cell. Transplant Proc 2014;46:3-8.
11. SK L. Killer B lymphocytes: the evidence and the potential. Inflamm Res 2009;58:345-357.
12. Ray A, Basu S, Williams CB, Salzman NH, Dittel BN. A novel IL-10-independent regulatory role for B cells in suppressing autoimmunity by maintenance of regulatory T cells via GITR ligand. J Immunol 2012;188:3188-3198.
13. 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.
14. Morva A, Lemoine S, Achour A, Pers JO, Youinou P, Jamin C. Maturation and function of human dendritic cells are regulated by B lymphocytes. Blood 2012;119:106-114.
15. Gray D, Gray M. What are regulatory B cells? Eur J Immunol 2010;40:2677-2679.
16. Rosser EC, Blair PA, Mauri C. Cellular targets of regulatory B cell-mediated suppression. Mol Immunol 2014;62:296-304.
17. Han C, Jin J, Xu S, Liu H, Li N, Cao X. Integrin CD11b negatively regulates TLR-triggered inflammatory responses by activating Syk and promoting degradation of MyD88 and TRIF via Cbl-b. Nat Immunol 2010;11:734-742.
18. Ling GS, Bennett J, Woollard KJ, Szajna M, Fossati-Jimack L, Taylor PR, et al. Integrin CD11b positively regulates TLR4-induced signalling pathways in dendritic cells but not in macrophages. Nat Commun 2014;5:3039.
19. Abdelbaqi M, Chidlow JH, Matthews KM, Pavlick KP, Barlow SC, Linscott AJ, et al. Regulation of dextran sodium sulfate induced colitis by leukocyte beta 2 integrins. Lab Invest 2006;86:380-390.
20. Zhang M, Han Y, Han C, Xu S, Bao Y, Chen Z, et al. The beta2 integrin CD11b attenuates polyinosinic:polycytidylic acid-induced hepatitis by negatively regulating natural killer cell functions. Hepatology 2009;50:1606-1616.
21. Ehirchiou D, Xiong Y, Xu G, Chen W, Shi Y, Zhang L. CD11b facilitates the development of peripheral tolerance by suppressing Th17 differentiation. J Exp Med 2007;204:1519-1524.
22. Varga G, Balkow S, Wild MK, Stadtbaeumer A, Krummen M, Rothoeft T, et al. Active MAC-1 (CD11b/CD18) on DCs inhibits full T-cell activation. Blood 2007;109:661-669.
23. Pillay J, Kamp VM, van Hoffen E, Visser T, Tak T, Lammers JW, et al. A subset of neutrophils in human systemic inflammation inhibits T cell responses through Mac-1. J Clin Invest 2012;122:327-336.
24. Vergani D, Longhi MS, Bogdanos DP, Ma Y, Mieli-Vergani G. Autoimmune hepatitis. Semin Immunopathol 2009;31:421-435.
25. Jothimani D, Cramp ME, Mitchell JD, Cross TJ. Treatment of autoimmune hepatitis: a review of current and evolving therapies. J Gastroenterol Hepatol 2011;26:619-627.
26. Mattner J. Natural killer T (NKT) cells in autoimmune hepatitis. Curr Opin Immunol 2013;25:697-703.
27. Longhi MS, Ma Y, Mieli-Vergani G, Vergani D. Adaptive immunity in autoimmune hepatitis. Dig Dis 2010;28:63-69.
28. Longhi MS, Ma Y, Mieli-Vergani G, Vergani D. Aetiopathogenesis of autoimmune hepatitis. J Autoimmun 2010;34:7-14.
29. Hardtke-Wolenski M, Jaeckel E. Mouse models for experimental autoimmune hepatitis: limits and chances. Dig Dis 2010;28:70-79.
30. Christen U, Holdener M, Hintermann E. Animal models for autoimmune hepatitis. Autoimmun Rev 2007;6:306-311.
31. Lohse AW, Manns M, Dienes HP, Meyer zum Buschenfelde KH, Cohen IR. Experimental autoimmune hepatitis: disease induction, time course and T-cell reactivity. Hepatology 1990;11:24-30.
32. Novobrantseva TI, Majeau GR, Amatucci A, Kogan S, Brenner I, Casola S, et al. Attenuated liver fibrosis in the absence of B cells. J Clin Invest 2005;115:3072-3082.
33. Dhirapong A, Lleo A, Yang GX, Tsuneyama K, Dunn R, Kehry M, et al. B cell depletion therapy exacerbates murine primary biliary cirrhosis. Hepatology 2011;53:527-535.
34. Xia S, Guo Z, Xu X, Yi H, Wang Q, Cao X. Hepatic microenvironment programs hematopoietic progenitor differentiation into regulatory dendritic cells, maintaining liver tolerance. Blood 2008;112:3175-3185.
35. Lohse AW, Dienes HP, Meyer zum Buschenfelde KH. Suppression of murine experimental autoimmune hepatitis by T-cell vaccination or immunosuppression. Hepatology 1998;27:1536-1543.
36. Liu R, Liu X, Zheng Y, Gu J, Xiong S, Jiang P, et al. MicroRNA-7 sensitizes non-small cell lung cancer cells to paclitaxel. Oncol Lett 2014;8:2193-2200.
37. Gu J, Ding JY, Lu CL, Lin ZW, Chu YW, Zhao GY, et al. Overexpression of CD88 predicts poor prognosis in non-small-cell lung cancer. Lung Cancer 2013;81:259-265.
38. Rauch PJ, Chudnovskiy A, Robbins CS, Weber GF, Etzrodt M, Hilgendorf I, et al. Innate response activator B cells protect against microbial sepsis. Science 2012;335:597-601.
39. Allman D, Pillai S. Peripheral B cell subsets. Curr Opin Immunol 2008;20:149-157.
40. Tian J, Zekzer D, Hanssen L, Lu Y, Olcott A, Kaufman DL. Lipopolysaccharide-activated B cells down-regulate Th1 immunity and prevent autoimmune diabetes in nonobese diabetic mice. J Immunol 2001;167:1081-1089.
41. Lampropoulou V, Hoehlig K, Roch T, Neves P, Calderón Gómez E, Sweenie CH, et al. TLR-activated B cells suppress T cell-mediated autoimmunity. J Immunol 2008;180:180-187.
42. Yanaba K, Bouaziz JD, Matsushita T, Tsubata T, Tedder TF. The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J Immunol 2009;182:7459-7472.
43. Heymann F, Hamesch K, Weiskirchen R, Tacke F. The concanavalin A model of acute hepatitis in mice. Lab Anim 2015;49(1 Suppl):12-20.
44. Ouchida R, Yamasaki S, Hikida M, Masuda K, Kawamura K, Wada A, et al. A lysosomal protein negatively regulates surface T cell antigen receptor expression by promoting CD3zeta-chain degradation. Immunity 2008;29:33-43.
45. Zhang H, Stolz DB, Chalasani G, Thomson AW. Hepatic B cells are readily activated by Toll-like receptor-4 ligation and secrete less interleukin-10 than lymphoid tissue B cells. Clin Exp Immunol 2013;173:473-479.
46. Heneghan MA, Yeoman AD, Verma S, Smith AD, Longhi MS. Autoimmune hepatitis. Lancet 2013;382:1433-1444.
47. Burak KW, Swain MG, Santodomingo-Garzon T, Lee SS, Urbanski SJ, Aspinall AI, et al. Rituximab for the treatment of patients with autoimmune hepatitis who are refractory or intolerant to standard therapy. Can J Gastroenterol 2013;27:273-280.
48. Del Prete CJ, Cohen NS. A case of rituximab-induced hepatitis. Cancer Biother Radiopharm 2010;25:747-748.
49. Al-Busafi SA, Michel RP, Deschenes M. Rituximab for refractory autoimmune hepatitis: a case report. Arab J Gastroenterol 2013;14:135-138.
50. Lohse AW, Brunner S, Kyriatsoulis A, Manns M, Meyer zum Buschenfelde KH. Autoantibodies in experimental autoimmune hepatitis. J Hepatol 1992;14:48-53.
51. Christen U. The role of autoantibodies in autoimmune hepatitis type 2. Immunotherapy 2013;5:247-256.
52. Blair PA, Noreña LY, Flores-Borja F, Rawlings DJ, Isenberg DA, Ehrenstein MR, Mauri C. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 2010;32:129-140.
53. Bosma A, Abdel-Gadir A, Isenberg DA, Jury EC, Mauri C. Lipid-antigen presentation by CD1d(+) B cells is essential for the maintenance of invariant natural killer T cells. Immunity 2012;36:477-490.
54. Griffin DO, Rothstein TL. Human "orchestrator" CD11b(+) B1 cells spontaneously secrete interleukin-10 and regulate T-cell activity. Mol Med 2012;18:1003-1008.
55. Kawai K, Tsuno NH, Matsuhashi M, Kitayama J, Osada T, Yamada J, et al. CD11b-mediated migratory property of peripheral blood B cells. J Allergy Clin Immunol 2005;116:192-197.
56. Ding C, Ma Y, Chen X, Liu M, Cai Y, Hu X, et al. Integrin CD11b negatively regulates BCR signalling to maintain autoreactive B cell tolerance. Nat Commun 2013;4:2813.
57. Lim J, Hotchin NA. Signalling mechanisms of the leukocyte integrin alphaMbeta2: current and future perspectives. Biol Cell 2012;104:631-640.
58. Zhang X. Regulatory functions of innate-like B cells. Cell Mol Immunol 2013;10:113-121.
59. O'Garra A, Chang R, Go N, Hastings R, Haughton G, Howard M. Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur J Immunol 1992;22:711-717.
60. Sun CM, Deriaud E, Leclerc C, Lo-Man R. Upon TLR9 signaling, CD5+ B cells control the IL-12-dependent Th1-priming capacity of neonatal DCs. Immunity 2005;22:467-477.
61. Griffin DO, Rothstein TL. A small CD11b(+) human B1 cell subpopulation stimulates T cells and is expanded in lupus. J Exp Med 2011;208:2591-2598.
62. Barr TA, Brown S, Ryan G, Zhao J, Gray D. TLR-mediated stimulation of APC: distinct cytokine responses of B cells and dendritic cells. Eur J Immunol 2007;37:3040-3053.
63. Bouaziz JD, Calbo S, Maho-Vaillant M, Saussine A, Bagot M, Bensussan A, Musette P. IL-10 produced by activated human B cells regulates CD4(+) T-cell activation in vitro. Eur J Immunol 2010;40:2686-2691.