Role of B cells in tolerance induction

Current Opinion in Organ Transplantation

Volumn 20, Issue 4, 2015, Pages 369-375

  Kim, James I ^a   Rothstein, David M ^b   Markmann, James F ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

IL 10; regulatory B cells; rituximab; transplant tolerance

Indexed keywords

BIOLOGICAL MARKER; INTERLEUKIN 10; KIDNEY INJURY MOLECULE 1;

ADOPTIVE TRANSFER; B LYMPHOCYTE; CELL EXPANSION; CELL FUNCTION; CYTOKINE PRODUCTION; GRAFT RECIPIENT; GRAFT REJECTION; GRAFT SURVIVAL; HUMAN; HUMORAL IMMUNE DEFICIENCY; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; INFLAMMATION; KIDNEY GRAFT; LYMPHOCYTE DEPLETION; NONHUMAN; ORGAN TRANSPLANTATION; PHENOTYPE; PROTEIN EXPRESSION; REVIEW; ALLOTRANSPLANTATION; ANIMAL; CELLULAR IMMUNITY; HUMORAL IMMUNITY; IMMUNOLOGY;

ANIMALS; B-LYMPHOCYTES; GRAFT REJECTION; HUMANS; IMMUNE TOLERANCE; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; TRANSPLANTATION, HOMOLOGOUS;

EID: 84941365939     PISSN: 10872418     EISSN: 15317013     Source Type: Journal    
DOI: 10.1097/MOT.0000000000000204     Document Type: Review

References (71)

1. Tedder TF. B10 cells: a functionally defined regulatory B cell subset. J Immunol 2015; 194:1395-1401.
2. Dilillo DJ, Matsushita T, Tedder TF. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann N Y Acad Sci 2010; 1183:38-57.
3. Mauri C, Blair PA. Regulatory B cells in autoimmunity: developments and controversies. Nat Rev Rheumatol 2010; 6:636-643.
4. Yanaba K, Bouaziz JD, Matsushita T, et al. B-lymphocyte contributions to human autoimmune disease. Immunol Rev 2008; 223:284-299.
5. Brummel R, Lenert P. Activation of marginal zone B cells from lupus mice with type A(D) CpG-oligodeoxynucleotides. J Immunol 2005; 174:2429-2434.
6. Lenert P, Brummel R, Field EH, Ashman RF. TLR-9 activation of marginal zone B cells in lupus mice regulates immunity through increased IL-10 production. J Clin Immunol 2005; 25:29-40.
7. Gray M, Miles K, Salter D, et al. Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc Natl Acad Sci USA 2007; 104:14080-14085.
8. Mizoguchi A, Mizoguchi E, Takedatsu H, et al. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 2002; 16:219-230.
9. Evans JG, Chavez-Rueda KA, Eddaoudi A, et al. Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol 2007; 178:7868-7878.
10. Blair PA, Chavez-Rueda KA, Evans JG, et al. 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 2009; 182:3492-3502.
11. Lal G, Nakayama Y, Sethi A, et al. Interleukin-10 from marginal zone precursor B-cell subset is required for costimulatory blockade-induced transplantation tolerance. Transplantation 2015; in press.
12. Miyazaki D, Kuo CH, Tominaga T, et al. Regulatory function of CpG-activated B cells in late-phase experimental allergic conjunctivitis. Invest Ophthalmol Vis Sci 2009; 50:1626-1635.
13. Yanaba K, Bouaziz JD, Haas KM, et al. A regulatory B cell subset with a unique CD1dhiCD5\+ phenotype controls T cell-dependent inflammatory responses. Immunity 2008; 28:639-650.
14. Montandon R, Korniotis S, Layseca-Espinosa E, et al. Innate pro-B-cell progenitors protect against type 1 diabetes by regulating autoimmune effector T cells. Proc Natl Acad Sci USA 2013; 110:E2199-E2208.
15. Fillatreau S, Sweenie CH, McGeachy MJ, et al. B cells regulate autoimmunity by provision of IL-10. Nat Immunol 2002; 3:944-950.
16. Matsumoto M, Baba A, Yokota T, et al. Interleukin-10-producing plasmablasts exert regulatory function in autoimmune inflammation. Immunity 2014; 41: 1040-1051.
17. Ding Q, Yeung M, Camirand G, 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.
18. Mann MK, Maresz K, Shriver LP, et al. 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.
19. Yang M, Sun L, Wang S, et al. Novel function of B cell-activating factor in the induction of IL-10-producing regulatory B cells. J Immunol 2010; 184:3321-3325.
20. Yang M, Deng J, Liu Y, et al. IL-10-producing regulatory B10 cells ameliorate collagen-induced arthritis via suppressing Th17 cell generation. Am J Pathol 2012; 180:2375-2385.
21. Carter NA, Vasconcellos R, Rosser EC, et al. 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 2011; 186:5569-5579.
22. Natarajan P, Singh A, McNamara JT, et al. Regulatory B cells from hilar lymph nodes of tolerant mice in a murine model of allergic airway disease are CD5\+, express TGF-beta, and co-localize with CD4\+Foxp3\+ T cells. Mucosal Immunol 2012; 5:691-701.
23. Blair PA, Norena LY, Flores-Borja F, et al. CD19\+CD24hiCD38hi B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 2010; 32:129-140.
24. Matsushita T, Horikawa M, Iwata Y, Tedder TF. Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J Immunol 2010; 185:2240-2252.
25. Lee KM, Stott RT, Zhao G, et al. TGF-beta-producing regulatory B cells induce regulatory T cells and promote transplantation tolerance. Eur J Immunol 2014; 44:1728-1736.
26. Ding Q, Rothstein DM, Yeung M, Najarian N, Sayegh MH. Anti-TIM-4-induced islet allograft long-term survival is dependent on the presence of B cells. AST, Philadelphia. 2011; Abstract #246.
27. Parekh VV, Prasad DV, Banerjee PP, et al. B cells activated by lipopolysaccharide, but not by anti-Ig and anti-CD40 antibody, induce anergy in CD8\+ T cells: role of TGF-beta 1. J Immunol 2003; 170:5897-5911.
28. Tian J, Zekzer D, Hanssen L, et al. Lipopolysaccharide-activated B cells downregulate Th1 immunity and prevent autoimmune diabetes in nonobese diabetic mice. J Immunol 2001; 167:1081-1089.
29. Wolf SD, Dittel BN, Hardardottir F, Janeway CA Jr. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J Exp Med 1996; 184:2271-2278.
30. Ray A, Basu S, Williams CB, et al. 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.
31. Moreau A, Blair PA, Chai JG, et al. Transitional-2 B cells acquire regulatory function during tolerance induction and contribute to allograft survival. Eur J Immunol 2015; 45:843-853.
32. Shen H, Goldstein DR. IL-6 and TNF-alpha synergistically inhibit allograft acceptance. J Am Soc Nephrol 2009; 20:1032-1040.
33. Wang RX, Yu CR, Dambuza IM, et al. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nat Med 2014; 20:633-641.
34. Collison LW, Workman CJ, Kuo TT, et al. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 2007; 450:566-569.
35. Collison LW, Chaturvedi V, Henderson AL, et al. IL-35-mediated induction of a potent regulatory T cell population. Nat Immunol 2010; 11:1093-1101.
36. Shen P, Roch T, Lampropoulou V, et al. IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 2014; 507:366-370.
37. Woodle ES, Rothstein DM. Clinical implications of basic science discoveries: janus resurrected-two faces of B cell and plasma cell biology. Am J Transplant 2015; 15:39-43.
38. Lee KM, Kim JI, Stott R, et al. Anti-CD45RB/anti-TIM-1-induced tolerance requires regulatory B cells. Am J Transplant 2012; 12:2072-2078.
39. Ueno T, Habicht A, Clarkson MR, et al. The emerging role of T cell Ig mucin 1 in alloimmune responses in an experimental mouse transplant model. J Clin Invest 2008; 118:742-751.
40. Xiao S, Brooks CR, Zhu C, et al. Defect in regulatory B-cell function and development of systemic autoimmunity in T-cell Ig mucin 1 (Tim-1) mucin domain-mutant mice. Proc Natl Acad Sci USA 2012; 109:12105-12110.
41. Yeung MY, Ding Q, Brooks CR, et al. TIM-1 signaling is required for maintenance and induction of regulatory B cells. Am J Transplant 2015; 15:942-953.
42. Xiao S, Brooks CR, Sobel RA, Kuchroo VK. Tim-1 is essential for induction and maintenance of IL-10 in regulatory B cells and their regulation of tissue inflammation. J Immunol 2015; 194:1602-1608.
43. Nagata S, Hanayama R, Kawane K. Autoimmunity and the clearance of dead cells. Cell 2010; 140:619-630.
44. Martin F, Kearney JF. Marginal-zone B cells [review]. Nat Rev Immunol 2002; 2:323-335.
45. Miles K, Heaney J, Sibinska Z, et al. A tolerogenic role for toll-like receptor 9 is revealed by B-cell interaction with DNA complexes expressed on apoptotic cells. Proc Natl Acad Sci USA 2012; 109:887-892.
46. Yoshizaki A, Miyagaki T, DiLillo DJ, et al. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 2012; 491:264-268.
47. Roussey-Kesler G, Giral M, Moreau A, et al. Clinical operational tolerance after kidney transplantation. Am J Transplant 2006; 6:736-746.
48. Newell KA, Asare A, Kirk AD, et al. Identification of a B cell signature associated with renal transplant tolerance in humans. J Clin Invest 2010; 120:1836-1847.
49. Sagoo P, Perucha E, Sawitzki B, et al. Development of a cross-platform biomarker signature to detect renal transplant tolerance in humans. J Clin Invest 2010; 120:1848-1861.
50. Lozano JJ, Pallier A, Martinez-Llordella M, et al. Comparison of transcriptional and blood cell-phenotypic markers between operationally tolerant liver and kidney recipients. Am J Transplant 2011; 11:1916-1926.
51. Chesneau M, Michel L, Dugast E, et al. Tolerant kidney transplant patients produce B cells with regulatory properties. J Am Soc Nephrol 2015; in press.
52. Pallier A, Hillion S, Danger R, et al. Patients with drug-free long-term graft function display increased numbers of peripheral B cells with a memory and inhibitory phenotype. Kidney Int 2010; 78:503-513.
53. Iwata Y, Matsushita T, Horikawa M, et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 2011; 117:530-541.
54. Khoder A, Sarvaria A, Alsuliman A, et al. Regulatory B cells are enriched within the IgM memory and transitional subsets in healthy donors but are deficient in chronic GVHD. Blood 2014; 124:2034-2045.
55. Cherukuri A, Rothstein DM, Clark B, et al. Immunologic human renal allograft injury associates with an altered IL-10/TNF-alpha expression ratio in regulatory B cells. J Am Soc Nephrol 2014; 25:1575-1585.
56. Bar-Or A, Fawaz L, Fan B, et al. Abnormal B-cell cytokine responses a trigger of T-cell-mediated disease in MS? Ann Neurol 2010; 67:452-461.
57. Wojciechowski W, Harris DP, Sprague F, et al. Cytokine-producing effector B cells regulate type 2 immunity to H. polygyrus. Immunity 2009; 30:421-433.
58. Shabir S, Girdlestone J, Briggs D, et al. Transitional B lymphocytes are associated with protection from kidney allograft rejection: a prospective study. Am J Transplant 2015; 15:1384-1391.
59. Viklicky O, Krystufkova E, Brabcova I, et al. B-cell-related biomarkers of tolerance are up-regulated in rejection-free kidney transplant recipients. Transplantation 2013; 95:148-154.
60. Leibler C, Matignon M, Pilon C, et al. Kidney transplant recipients treated with belatacept exhibit increased naive and transitional B cells. Am J Transplant 2014; 14:1173-1182.
61. Clatworthy MR, Watson CJ, Plotnek G, et al. B-cell-depleting induction therapy and acute cellular rejection. N Engl J Med 2009; 360:2683-2685.
62. Bouaziz JD, Yanaba K, Venturi GM, et al. Therapeutic B cell depletion impairs adaptive and autoreactive CD4\+ T cell activation in mice. Proc Natl Acad Sci USA 2007; 104:20878-20883.
63. Tyden G, Mjornstedt L, Ekberg H. More on B-cell-depleting induction therapy and acute cellular rejection. N Engl J Med 2009; 361:1214-1215.
64. Uchida J, Hamaguchi Y, Oliver JA, et al. The innate mononuclear phagocyte network depletes B lymphocytes through Fc receptor-dependent mechanisms during anti-CD20 antibody immunotherapy. J Exp Med 2004; 199: 1659-1669.
65. Yazawa N, Hamaguchi Y, Poe JC, Tedder TF. Immunotherapy using unconjugated CD19 monoclonal antibodies in animal models for B lymphocyte malignancies and autoimmune disease. Proc Natl Acad Sci USA 2005; 102:15178-15183.
66. Deng S, Moore DJ, Huang X, et al. Cutting edge: transplant tolerance induced by anti-CD45RB requires B lymphocytes. J Immunol 2007; 178:6028-6032.
67. Lal G, Tietjens J, van der Touw W, Yang Y, Ding Y, Ochando JC, et al. B cell depletion prevents costimulatory blockade-induced tolerance. AST, Philadelphia. 2011; Abstract 484.
68. van den Hoogen MW, Kamburova EG, Baas MC, et al. Rituximab as induction therapy after renal transplantation: a randomized, double-blind, placebocontrolled study of efficacy and safety. Am J Transplant 2015; 15:407-416.
69. Anolik JH, Barnard J, Owen T, et al. Delayed memory B cell recovery in peripheral blood and lymphoid tissue in systemic lupus erythematosus after B cell depletion therapy. Arthritis Rheum 2007; 56:3044-3056.
70. Kamburova EG, Koenen HJ, van den Hoogen MW, et al. Longitudinal analysis of T and B cell phenotype and function in renal transplant recipients with or without rituximab induction therapy. PLoS One 2014; 9:e112658.
71. Liu C, Noorchashm H, Sutter JA, et al. B lymphocyte-directed immunotherapy promotes long-term islet allograft survival in nonhuman primates. Nat Med 2007; 13:1295-1298.