B cells exposed to enterobacterial components suppress development of experimental colitis

Inflammatory Bowel Diseases

Volumn 18, Issue 2, 2012, Pages 284-293

  Schmidt, Esben Gjerløff Wedebye ^a   Larsen, Hjalte List ^a   Kristensen, Nanna Ny ^a   Poulsen, Steen Seier ^a   Claesson, Mogens Helweg ^a   Pedersen, Anders Elm ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

colitis, IL 10; enterobacteria; Regulatory B cells

Indexed keywords

CD1D ANTIGEN; CD5 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; COLITIS; CYTOKINE PRODUCTION; ENTEROBACTERIACEAE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNOREGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCID MOUSE;

ANIMALS; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; COLITIS; CYTOKINES; ENTEROBACTER; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNE TOLERANCE; INTERLEUKIN-10; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, SCID; SPLEEN;

EID: 84855642249     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.21769     Document Type: Article

References (59)

1. Katz SI, Parker D, Turk JL,. B-cell suppression of delayed hypersensitivity reactions. Nature. 1974; 251: 550-551.
2. Neta R, Salvin SB,. Specific suppression of delayed hypersensitivity: the possible presence of a suppressor B cell in the regulation of delayed hypersensitivity. J Immunol. 1974; 113: 1716-1725.
3. Li X, Braun J, Wei B,. Regulatory B cells in autoimmune diseases and mucosal immune homeostasis. Autoimmunity. 2011; 44: 58-68.
4. Mauri C, Ehrenstein MR,. The 'short' history of regulatory B cells. Trends Immunol. 2008; 29: 34-40.
5. Broglio L, Lauria G,. Worsening after rituximab treatment in anti-mag neuropathy. Muscle Nerve. 2005; 32: 378-379. (Pubitemid 41232625)
6. Dass S, Vital EM, Emery P,. Development of psoriasis after B cell depletion with rituximab. Arthritis Rheum. 2007; 56: 2715-2718. (Pubitemid 47237290)
7. El FD, Nielsen CH, Kjeldsen J, et al. Ulcerative colitis following B lymphocyte depletion with rituximab in a patient with Graves' disease. Gut. 2008; 57: 714-715. (Pubitemid 351579988)
8. Goetz M, Atreya R, Ghalibafian M, et al. Exacerbation of ulcerative colitis after rituximab salvage therapy. Inflamm Bowel Dis. 2007; 13: 1365-1368. (Pubitemid 350206846)
9. Mizoguchi A, Mizoguchi E, Smith RN, et al. Suppressive role of B cells in chronic colitis of T cell receptor alpha mutant mice. J Exp Med. 1997; 186: 1749-1756. (Pubitemid 27506287)
10. 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. (Pubitemid 34211962)
11. McPherson M, Wei B, Turovskaya O, et al. Colitis immunoregulation by CD8+ T cell requires T cell cytotoxicity and B cell peptide antigen presentation. Am J Physiol Gastrointest Liver Physiol. 2008; 295: G485-G492.
12. Wei B, Velazquez P, Turovskaya O, et al. Mesenteric B cells centrally inhibit CD4+ T cell colitis through interaction with regulatory T cell subsets. Proc Natl Acad Sci U S A. 2005; 102: 2010-2015. (Pubitemid 40262003)
13. Gerth AJ, Lin L, Neurath MF, et al. An innate cell-mediated, murine ulcerative colitis-like syndrome in the absence of nuclear factor of activated T cells. Gastroenterology. 2004; 126: 1115-1121. (Pubitemid 38451182)
14. Fillatreau S, Sweenie CH, McGeachy MJ, et al. B cells regulate autoimmunity by provision of IL-10. Nat Immunol. 2002; 3: 944-950. (Pubitemid 35154008)
15. Lampropoulou V, Hoehlig K, Roch T, et al. TLR-activated B cells suppress T cell-mediated autoimmunity. J Immunol. 2008; 180: 4763-4773.
16. 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. (Pubitemid 46417609)
17. Wolf SD, Dittel BN, Hardardottir F, et al. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J Exp Med. 1996; 184: 2271-2278. (Pubitemid 27023727)
18. Mauri C, Gray D, Mushtaq N, et al. Prevention of arthritis by interleukin 10-producing B cells. J Exp Med. 2003; 197: 489-501. (Pubitemid 36278604)
19. Tian J, Zekzer D, Hanssen L, et al. Lipopolysaccharide-activated B cells down-regulate Th1 immunity and prevent autoimmune diabetes in nonobese diabetic mice. J Immunol. 2001; 167: 1081-1089. (Pubitemid 32660868)
20. Hussain S, Delovitch TL,. Intravenous transfusion of BCR-activated B cells protects NOD mice from type 1 diabetes in an IL-10-dependent manner. J Immunol. 2007; 179: 7225-7232.
21. 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.
22. 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. (Pubitemid 36682569)
23. Moulin V, Andris F, Thielemans K, et al. 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. (Pubitemid 30666248)
24. 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. (Pubitemid 351636247)
25. Matsushita T, Yanaba K, Bouaziz JD, et al. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest. 2008; 118: 3420-3430.
26. Watanabe R, Ishiura N, Nakashima H, et al. Regulatory B cells (B10 cells) have a suppressive role in murine lupus: CD19 and B10 cell deficiency exacerbates systemic autoimmunity. J Immunol. 2010; 184: 4801-4809.
27. Yanaba K, Yoshizaki A, Asano Y, et al. IL-10-Producing Regulatory B10 Cells Inhibit Intestinal Injury in a Mouse Model. Am J Pathol. 2011; 178: 735-743.
28. Burke F, Stagg AJ, Bedford PA, et al. IL-10-producing B220+CD11c- APC in mouse spleen. J Immunol. 2004; 173: 2362-2372. (Pubitemid 39063092)
29. Dalwadi H, Wei B, Schrage M, et al. B cell developmental requirement for the G alpha i2 gene. J Immunol. 2003; 170: 1707-1715. (Pubitemid 36197385)
30. Watanabe R, Fujimoto M, Ishiura N, et al. CD19 expression in B cells is important for suppression of contact hypersensitivity. Am J Pathol. 2007; 171: 560-570. (Pubitemid 47344688)
31. 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. (Pubitemid 46898059)
32. Barr TA, Brown S, Ryan G, et al. TLR-mediated stimulation of APC: Distinct cytokine responses of B cells and dendritic cells. Eur J Immunol. 2007; 37: 3040-3053. (Pubitemid 350131284)
33. Caradonna L, Amati L, Magrone T, et al. Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. J Endotoxin Res. 2000; 6: 205-214.
34. Gutierrez A, Frances R, Amoros A, et al. Cytokine association with bacterial DNA in serum of patients with inflammatory bowel disease. Inflamm Bowel Dis. 2009; 15: 508-514.
35. Schmidt EG, Kristensen NN, Claesson MH, et al. Enteroantigen-presenting B cells efficiently stimulate CD4(+) T cells in vitro. Inflamm Bowel Dis. 2011; 17: 308-318.
36. Brimnes J, Reimann J, Nissen M, et al. Enteric bacterial antigens activate CD4(+) T cells from scid mice with inflammatory bowel disease. Eur J Immunol. 2001; 31: 23-31.
37. Gad M, Pedersen AE, Kristensen NN, et al. Demonstration of strong enterobacterial reactivity of CD4+CD25- T cells from conventional and germ-free mice which is counter-regulated by CD4+CD25+ T cells. Eur J Immunol. 2004; 34: 695-704. (Pubitemid 39255917)
38. Ostanin DV, Bao J, Koboziev I, et al. T cell transfer model of chronic colitis: concepts, considerations, and tricks of the trade. Am J Physiol Gastrointest Liver Physiol. 2009; 296: G135-G146.
39. Ahern PP, Schiering C, Buonocore S, et al. Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity. 2010; 33: 279-288.
40. Kristensen NN, Brudzewsky D, Gad M, et al. Chemokines involved in protection from colitis by CD4+CD25+ regulatory T cells. Inflamm Bowel Dis. 2006; 12: 612-618. (Pubitemid 43977743)
41. Groux H, O'Garra A, Bigler M, et al. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature. 1997; 389: 737-742. (Pubitemid 27458961)
42. Vieira PL, Christensen JR, Minaee S, et al. IL-10-secreting regulatory T cells do not express Foxp3 but have comparable regulatory function to naturally occurring CD4+CD25+ regulatory T cells. J Immunol. 2004; 172: 5986-5993. (Pubitemid 38621199)
43. 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 U S A. 2007; 104: 14080-14085. (Pubitemid 350003338)
44. Lenert P, Brummel R, Field EH, et al. 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. (Pubitemid 40386176)
45. Nakashima H, Hamaguchi Y, Watanabe R, et al. CD22 expression mediates the regulatory functions of peritoneal B-1a cells during the remission phase of contact hypersensitivity reactions. J Immunol. 2010; 184: 4637-4645.
46. Ronet C, Hauyon-La TY, Revaz-Breton M, et al. Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production. J Immunol. 2010; 184: 886-894.
47. Mishima Y, Ishihara S, Amano Y, et al. Alterations of peripheral blood CD5+ B cells in inflammatory bowel disease. Scand J Gastroenterol. 2009; 44: 172-179.
48. Neil GA, Summers RW, Cheyne BA, et al. CD5+ B cells are decreased in peripheral blood of patients with Crohn's disease. Dig Dis Sci. 1992; 37: 1390-1395.
49. Polese L, De FG, Scarpa M, et al. B1a lymphocytes in ulcerative colitis. Int J Colorectal Dis. 2007; 22: 1005-1011. (Pubitemid 47500240)
50. Mizoguchi A, Mizoguchi E, Chiba C, et al. Cytokine imbalance and autoantibody production in T cell receptor-alpha mutant mice with inflammatory bowel disease. J Exp Med. 1996; 183: 847-856. (Pubitemid 26113957)
51. Sugimoto K, Ogawa A, Shimomura Y, et al. Inducible IL-12-producing B cells regulate Th2-mediated intestinal inflammation. Gastroenterology. 2007; 133: 124-136. (Pubitemid 47031122)
52. Day MJ, Tse AG, Puklavec M, et al. Targeting autoantigen to B cells prevents the induction of a cell-mediated autoimmune disease in rats. J Exp Med. 1992; 175: 655-659.
53. Harrington LE, Hatton RD, Mangan PR, et al. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol. 2005; 6: 1123-1132. (Pubitemid 41541790)
54. Park H, Li Z, Yang XO, et al. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol. 2005; 6: 1133-1141. (Pubitemid 41541791)
55. Ashour HM, Niederkorn JY,. Peripheral tolerance via the anterior chamber of the eye: role of B cells in MHC class I and II antigen presentation. J Immunol. 2006; 176: 5950-5957.
56. Tu W, Lau YL, Zheng J, et al. Efficient generation of human alloantigen-specific CD4+ regulatory T cells from naive precursors by CD40-activated B cells. Blood. 2008; 112: 2554-2562.
57. Chen LC, Delgado JC, Jensen PE, et al. Direct expansion of human allospecific FoxP3+CD4+ regulatory T cells with allogeneic B cells for therapeutic application. J Immunol. 2009; 183: 4094-4102.
58. Uhlig HH, Coombes J, Mottet C, et al. Characterization of Foxp3+CD4+CD25+ and IL-10-secreting CD4+CD25+ T cells during cure of colitis. J Immunol. 2006; 177: 5852-5860.
59. Murai M, Turovskaya O, Kim G, et al. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol. 2009; 10: 1178-1184.