IL-10 from marginal zone precursor B cells controls the differentiation of Th17, Tfh and Tfr cells in transplantation tolerance

Immunology Letters

Volumn 170, Issue , 2016, Pages 52-63

  Lal, Girdhari ^a   Kulkarni, Neeraja ^a   Nakayama, Yumi ^b   Singh, Amit K ^a   Sethi, Apoorva ^a   Burrell, Bryna E ^b   Brinkman, C Colin ^b   Iwami, Daiki ^b   Zhang, Tianshu ^b   Hehlgans, Thomas ^c   Bromberg, Jonathan S ^b  

^a NATIONAL CENTRE FOR CELL SCIENCE   (India)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

B cells; Breg; Costimulatory blockade; Tfh; Th17; Transplantation tolerance

Indexed keywords

CHEMOKINE RECEPTOR CCR6; INTERLEUKIN 10; INTERLEUKIN 21; INTERLEUKIN 6; BIOLOGICAL MARKER;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HELPER CELL; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T FOLLICULAR HELPER CELL; TH17 CELL; TRANSPLANTATION TOLERANCE; ALLOGRAFT; ANIMAL; CYTOLOGY; DEFICIENCY; GERMINAL CENTER; GRAFT REJECTION; IMMUNOLOGY; IMMUNOPHENOTYPING; KNOCKOUT MOUSE; LYMPHOCYTE DEPLETION; METABOLISM; PHENOTYPE; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ALLOGRAFTS; ANIMALS; BIOMARKERS; CELL DIFFERENTIATION; GERMINAL CENTER; GRAFT REJECTION; IMMUNOPHENOTYPING; INTERLEUKIN-10; LYMPHOCYTE DEPLETION; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PHENOTYPE; PRECURSOR CELLS, B-LYMPHOID; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER; TH17 CELLS; TRANSPLANTATION TOLERANCE;

EID: 84953931661     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2016.01.002     Document Type: Article

References (60)

1. Lund F.E. Cytokine-producing B lymphocytes-key regulators of immunity. Curr. Opin. Immunol. 2008, 20:332-338.
2. Zeng Q., Ng Y.H., Singh T., Jiang K., Sheriff K.A., Ippolito R., et al. B cells mediate chronic allograft rejection independently of antibody production. J. Clin. Invest. 2014, 124:1052-1056.
3. Lal G., Nakayama Y., Sethi A., Singh A.K., Burrell B.E., Kulkarni N., et al. Interleukin-10 from marginal zone precursor B-cell subset is required for costimulatory blockade-induced transplantation tolerance. Transplantation 2015, 99:1817-1828.
4. Newell K.A., Asare A., Kirk A.D., Gisler T.D., Bourcier K., Suthanthiran M., et al. Identification of a B cell signature associated with renal transplant tolerance in humans. J. Clin. Invest. 2010, 120:1836-1847.
5. Bennett S.R., Carbone F.R., Toy T., Miller J.F., Heath W.R. B cells directly tolerize CD8(+) T cells. J. Exp. Med. 1998, 188:1977-1983.
6. Hollsberg P., Batra V., Dressel A., Hafler D.A. Induction of energy in CD8T cells by B cell presentation of antigen. J. Immunol. 1996, 157:5269-5276.
7. Mizoguchi E., Mizoguchi A., Preffer F.I., Bhan A.K. Regulatory role of mature B cells in a murine model of inflammatory bowel disease. Int. Immunol. 2000, 12:597-605.
8. Moulin V., Andris F., Thielemans K., Maliszewski C., Urbain J., Moser M. B lymphocytes regulate dendritic cell (DC) function in vivo: increased interleukin 12 production by DCs from B cell-deficient mice results in T helper cell type 1 deviation. J. Exp. Med. 2000, 192:475-482.
9. Yanaba K., Bouaziz J.D., Haas K.M., Poe J.C., Fujimoto M., Tedder T.F. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 2008, 28:639-650.
10. Moreau A., Blair P.A., Chai J.G., Ratnasothy K., Stolarczyk E., Alhabbab R., et al. Transitional-2 B cells acquire regulatory function during tolerance induction and contribute to allograft survival. Eur. J. Immunol. 2014.
11. 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.
12. Shen P., Roch T., Lampropoulou V., O'Connor R.A., Stervbo U., Hilgenberg E., et al. IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 2014, 507:366-370.
13. Blair P.A., Norena L.Y., Flores-Borja F., Rawlings D.J., Isenberg D.A., Ehrenstein M.R., et al. 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.
14. Carter N.A., Vasconcellos R., Rosser E.C., Tulone C., Munoz-Suano A., Kamanaka M., 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.
15. Mann M.K., Maresz K., Shriver L.P., Tan Y., Dittel B.N. 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.
16. Matsushita T., Horikawa M., Iwata Y., Tedder T.F. 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.
17. Luu V.P., Vazquez M.I., Zlotnik A. B cells participate in tolerance and autoimmunity through cytokine production. Autoimmunity 2014, 47:1-12.
18. Hagn M., Sontheimer K., Dahlke K., Brueggemann S., Kaltenmeier C., Beyer T., et al. Human B cells differentiate into granzyme B-secreting cytotoxic B lymphocytes upon incomplete T-cell help. Immunol. Cell Biol. 2012, 90:457-467.
19. Kaku H., Cheng K.F., Al-Abed Y., Rothstein T.L. A novel mechanism of B cell-mediated immune suppression through CD73 expression and adenosine production. J. Immunol. 2014, 193:5904-5913.
20. Ray A., Basu S., Williams C.B., Salzman N.H., Dittel B.N. 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.
21. Pilat N., Sayegh M.H., Wekerle T. Costimulatory pathways in transplantation. Semin. Immunol. 2011, 23:293-303.
22. Kim E.J., Kwun J., Gibby A.C., Hong J.J., Farris A.B., Iwakoshi N.N., et al. Costimulation blockade alters germinal center responses and prevents antibody-mediated rejection. Am. J. Transplant. 2014, 14:59-69.
23. Quezada S.A., Jarvinen L.Z., Lind E.F., Noelle R.J. CD40/CD154 interactions at the interface of tolerance and immunity. Annu. Rev. Immunol. 2004, 22:307-328.
24. Monk N.J., Hargreaves R.E., Marsh J.E., Farrar C.A., Sacks S.H., Millrain M., et al. Fc-dependent depletion of activated T cells occurs through CD40L-specific antibody rather than costimulation blockade. Nat. Med. 2003, 9:1275-1280.
25. Ochando J.C., Homma C., Yang Y., Hidalgo A., Garin A., Tacke F., et al. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat. Immunol. 2006, 7:652-662.
26. van der Touw W., Burrell B., Lal G., Bromberg J.S. NK cells are required for costimulatory blockade induced tolerance to vascularized allografts. Transplantation 2012, 94:575-584.
27. Rohrl J., Yang D., Oppenheim J.J., Hehlgans T. Specific binding and chemotactic activity of mBD4 and its functional orthologue hBD2 to CCR6-expressing cells. J. Biol. Chem. 2010, 285:7028-7034.
28. Yin N., Zhang N., Lal G., Xu J., Yan M., Ding Y., et al. Lymphangiogenesis is required for pancreatic islet inflammation and diabetes. PLoS One 2011, 6:e28023.
29. Nagano H., Mitchell R.N., Taylor M.K., Hasegawa S., Tilney N.L., Libby P. Interferon-gamma deficiency prevents coronary arteriosclerosis but not myocardial rejection in transplanted mouse hearts. J. Clin. Invest. 1997, 100:550-557.
30. Burrell B.E., Bromberg J.S. Fates of CD4+ T cells in a tolerant environment depend on timing and place of antigen exposure. Am. J. Transplant. 2012, 12:576-589.
31. Yuan X., Paez-Cortez J., Schmitt-Knosalla I., D'Addio F., Mfarrej B., Donnarumma M., et al. A novel role of CD4 Th17 cells in mediating cardiac allograft rejection and vasculopathy. J. Exp. Med. 2008, 205:3133-3144.
32. Grubin C.E., Kovats S., deRoos P., Rudensky A.Y. Deficient positive selection of CD4T cells in mice displaying altered repertoires of MHC class II-bound self-peptides. Immunity 1997, 7:197-208.
33. Nakae S., Iwakura Y., Suto H., Galli S.J. Phenotypic differences between Th1 and Th17 cells and negative regulation of Th1 cell differentiation by IL-17. J. Leukoc. Biol. 2007, 81:1258-1268.
34. Nurieva R.I., Chung Y., Hwang D., Yang X.O., Kang H.S., Ma L., et al. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 2008, 29:138-149.
35. Konforte D., Simard N., Paige C.J. IL-21: an executor of B cell fate. J. Immunol. 2009, 182:1781-1787.
36. Korn T., Bettelli E., Gao W., Awasthi A., Jager A., Strom T.B., et al. IL-21 initiates an alternative pathway to induce proinflammatory T(H) 17 cells. Nature 2007, 448:484-487.
37. Burrell B.E., Ding Y., Nakayama Y., Park K.S., Xu J., Yin N., et al. Tolerance and lymphoid organ structure and function. Front. Immunol. 2011, 2:64.
38. Strober W., Zhang F., Kitani A., Fuss I., Fichtner-Feigl S. Proinflammatory cytokines underlying the inflammation of Crohn's disease. Curr. Opin. Gastroenterol. 2010, 26:310-317.
39. He J., Tsai L.M., Leong Y.A., Hu X., Ma C.S., Chevalier N., et al. Circulating precursor CCR7(lo)PD-1(hi) CXCR5(+) CD4(+) T cells indicate Tfh cell activity and promote antibody responses upon antigen reexposure. Immunity 2013, 39:770-781.
40. Linterman M.A., Pierson W., Lee S.K., Kallies A., Kawamoto S., Rayner T.F., et al. Foxp3+ follicular regulatory T cells control the germinal center response3. Nat. Med. 2011, 17:975-982.
41. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17Cells. Annu. Rev. Immunol. 2009, 27:485-517.
42. Martin-Orozco N., Muranski P., Chung Y., Yang X.O., Yamazaki T., Lu S., et al. T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity 2009, 31:787-798.
43. Fillatreau S., Sweenie C.H., McGeachy M.J., Gray D., Anderton S.M. B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 2002, 3:944-950.
44. Clatworthy M.R., Watson C.J., Plotnek G., Bardsley V., Chaudhry A.N., Bradley J.A., et al. B-cell-depleting induction therapy and acute cellular rejection. N. Engl. J. Med. 2009, 360:2683-2685.
45. Candando K.M., Lykken J.M., Tedder T.F. B10 cell regulation of health and disease. Immunol. Rev. 2014, 259:259-272.
46. Rincon-Arevalo H., Sanchez-Parra C.C., Castano D., Yassin L., Vasquez G. Regulatory B cells and mechanisms. Int. Rev. Immunol. 2015.
47. Victora G.D., Nussenzweig M.C. Germinal centers. Annu. Rev. Immunol. 2012, 30:429-457.
48. Wong E.B., Soni C., Chan A.Y., Domeier P.P., Shwetank Abraham T., et al. B cell-intrinsic CD84 and Ly108 maintain germinal center B cell tolerance. J. Immunol. 2015, 194:4130-4143.
49. Brinkman C.C., Burrell B.E., Iwami D., Nakayama Y., Warren K.J., Xiong Y., et al. Anatomy of tolerance. Curr. Opin. Organ Transplant. 2013, 18:393-401.
50. Nakayama Y., Brinkman C.C., Bromberg J.S. Murine fibroblastic reticular cells from lymph node interact with CD4+ T Cells Through CD40-CD40L. Transplantation 2015.
51. Burrell B.E., Warren K.J., Nakayama Y., Iwami D., Brinkman C.C., Bromberg J.S. Lymph node stromal fiber ER-TR7 modulates CD4+ T cell lymph node trafficking and transplant tolerance. Transplantation 2015.
52. Avery D.T., Deenick E.K., Ma C.S., Suryani S., Simpson N., Chew G.Y., et al. B cell-intrinsic signaling through IL-21 receptor and STAT3 is required for establishing long-lived antibody responses in humans. J. Exp. Med. 2010, 207:155-171.
53. Good K.L., Bryant V.L., Tangye S.G. Kinetics of human B cell behavior and amplification of proliferative responses following stimulation with IL-21. J. Immunol. 2006, 177:5236-5247.
54. Spolski R., Kim H.P., Zhu W., Levy D.E., Leonard W.J. IL-21 mediates suppressive effects via its induction of IL-10. J. Immunol. 2009, 182:2859-2867.
55. Van Belle T.L., Nierkens S., Arens R., von Herrath M.G. Interleukin-21 receptor-mediated signals control autoreactive T cell infiltration in pancreatic islets. Immunity 2012, 36:1060-1072.
56. Spolski R., Leonard W.J. Interleukin-21: basic biology and implications for cancer and autoimmunity. Annu. Rev. Immunol. 2008, 26:57-79.
57. Baan C.C., de Graav G.N., Boer K. T follicular helper cells in transplantation: the target to attenuate antibody-mediated allogeneic responses?. Curr. Transplant. Rep. 2014, 1:166-172.
58. Baan C.C., Balk A.H., Dijke I.E., Korevaar S.S., Peeters A.M., de Kuiper R.P., et al. Interleukin-21: an interleukin-2 dependent player in rejection processes. Transplantation 2007, 83:1485-1492.
59. Chung Y., Tanaka S., Chu F., Nurieva R.I., Martinez G.J., Rawal S., et al. Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat. Med. 2011, 17:983-988.
60. Tyden G., Ekberg H., Tufveson G., Mjornstedt L. A randomized, double-blind, placebo-controlled study of single dose rituximab as induction in renal transplantation: a 3-year follow-up. Transplantation 2012, 94:e21-22.