Self-antigen presentation by mouse B cells results in regulatory T-cell induction rather than anergy or clonal deletion

Blood

Volumn 118, Issue 4, 2011, Pages 984-991

  Morlacchi, Sara ^a   Soldani, Cristiana ^a   Viola, Antonella ^a,b   Sarukhan, Adelaida ^a  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD4 ANTIGEN; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CLONAL ANERGY; DENDRITIC CELL; IMMUNOLOGICAL TOLERANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE;

EID: 79961017479     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-02-336115     Document Type: Article

References (51)

1. Mathis D, Benoist C. Levees of immunological tolerance. Nat Immunol. 2010;11(1):3-6.
2. Kim JM, Rasmussen JP, Rudensky AY. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol. 2007;8(2):191-197. (Pubitemid 46152650)
3. Watanabe-Fukunaga R, Brannan CI, Copeland NG, Jenkins NA, Nagata S. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature. 1992;356(6367):314-317.
4. Ramsdell F, Seaman MS, Miller RE, Tough TW, Alderson MR, Lynch DH. gld/gld mice are unable to express a functional ligand for Fas. Eur J Immunol. 1994;24(4):928-933. (Pubitemid 24093790)
5. Barron L, Knoechel B, Lohr J, Abbas AK. Cutting edge: contributions of apoptosis and anergy to systemic T-cell tolerance. J Immunol. 2008;180(5):2762-2766.
6. King CG, Buckler JL, Kobayashi T, et al. Cutting edge: requirement for TRAF6 in the induction of T cell anergy. J Immunol. 2008;180(1):34-38.
7. Seroogy CM, Soares L, Ranheim EA, et al. The gene related to anergy in lymphocytes, an E3 ubiquitin ligase, is necessary for anergy induction in CD4 T cells. J Immunol. 2004;173(1):79-85. (Pubitemid 38797328)
8. Bachmaier K, Krawczyk C, Kozieradzki I, et al. Negative regulation of lymphocyte activation and autoimmunity by the molecular adaptor Cbl-b. Nature. 2000;403(6766):211-216. (Pubitemid 30050966)
9. Fang D, Elly C, Gao B, et al. Dysregulation of T lymphocyte function in itchy mice: a role for Itch in TH2 differentiation. Nat Immunol. 2002;3(3):281-287. (Pubitemid 34213430)
10. Chiang YJ, Kole HK, Brown K, et al. Cbl-b regulates the CD28 dependence of T-cell activation. Nature. 2000;403(6766):216-220. (Pubitemid 30050967)
11. Nurieva RI, Zheng S, Jin W, et al. The E3 ubiquitin ligase GRAIL regulates T-cell tolerance and regulatory T cell function by mediating T cell receptor-CD3 degradation. Immunity. 2010;32(5):670-680.
12. Schwartz RH. T cell anergy. Annu Rev Immunol. 2003;21:305-334. (Pubitemid 37174534)
13. Lutz MB, Kurts C. Induction of peripheral CD4+T-cell tolerance and CD8+ T-cell cross-tolerance by dendritic cells. Eur J Immunol. 2009;39(9):2325-2330.
14. Kretschmer K, Apostolou I, Hawiger D, Khazaie K, Nussenzweig MC, von Boehmer H. Inducing and expanding regulatory T cell populations by foreign antigen. Nat Immunol. 2005;6(12):1219-1227. (Pubitemid 43045633)
15. Maldonado RA, von Andrian UH. How tolerogenic dendritic cells induce regulatory T cells. Adv Immunol. 2010;108:111-165.
16. Gilbert KM, Weigle WO. Tolerogenicity of resting and activated B cells. J Exp Med. 1994;179(1):249-258. (Pubitemid 24012990)
17. Lund FE, Randall TD. Effector and regulatory B cells: modulators of CD4(+) T cell immunity. Nat Rev Immunol. 2010;10(4):236-247.
18. Reichardt P, Dornbach B, Rong S, et al. Naive B cells generate regulatory T cells in the presence of a mature immunologic synapse. Blood. 2007;110(5):1519-1529. (Pubitemid 47443968)
19. Chen LC, Delgado JC, Jensen PE, Chen X. Direct expansion of human allospecific FoxP3+CD4+ regulatory T cells with allogeneic B cells for therapeutic application. J Immunol. 2009;183(6):4094-4102.
20. Zheng J, Liu Y, Lau YL, Tu W. CD40-activated B cells are more potent than immature dendritic cells to induce and expand CD4(+) regulatory T cells. Cell Mol Immunol. 2010;7(1):44-50.
21. Frommer F, Heinen TJ, Wunderlich FT, et al. Tolerance without clonal expansion: self-antigen-expressing B cells program self-reactive T cells for future deletion. J Immunol. 2008;181(8):5748-5759.
22. Kirberg J, Baron A, Jakob S, Rolink A, Karjalainen K, von Boehmer H. Thymic selection of CD8+ single positive cells with a class II major histocompatibility complex-restricted receptor. J Exp Med. 1994;180(1):25-34. (Pubitemid 24181052)
23. Buer J, Lanoue A, Franzke A, Garcia C, von Boehmer H, Sarukhan A. Interleukin 10 secretion and impaired effector function of major histocompatibility complex class II-restricted T cells anergized in vivo. J Exp Med. 1998;187(2):177-183. (Pubitemid 28060433)
24. EEC Council Directive 86/609, OJ L 358,1,12-12-1287; NIH Guide for the Care and Use of Laboratory Animals, Unites States National Research Council 1996.
25. Jordan MS, Boesteanu A, Reed AJ, et al. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat Immunol. 2001;2(4):301-306. (Pubitemid 33706340)
26. Apostolou I, Sarukhan A, Klein L, von Boehmer H. Origin of regulatory T cells with known specificity for antigen. Nat Immunol. 2002;3(8):756-763.
27. Apostolou I, Verginis P, Kretschmer K, Polansky J, Huhn J, von Boehmer H. Peripherally induced Treg: mode, stability, and role in specific tolerance. J Clin Immunol. 2008;28(6):619-624.
28. Kalberer CP, Reininger L, Melchers F, Rolink AG. Priming of helper T cell-dependent antibody responses by hemagglutinin-transgenic B cells. Eur J Immunol. 1997;27(9):2400-2407. (Pubitemid 27404327)
29. Lambolez F, Jooss K, Vasseur F, Sarukhan A. Tolerance induction to self antigens by peripheral dendritic cells. Eur J Immunol. 2002;32(9):2588-2597.
30. Jooss K, Gjata B, Danos O, von Boehmer H, Sarukhan A. Regulatory function of in vivo anergized CD4(+) T cells. Proc Natl Acad Sci U S A. 2001;98(15):8738-8743. (Pubitemid 32678097)
31. Thomson AW, Knolle PA. Antigen-presenting cell function in the tolerogenic liver environment. Nat Rev Immunol. 2010;10(11):753-766.
32. Wan YY, Flavell RA. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature. 2007;445(7129):766-770. (Pubitemid 46279706)
33. Kleindienst P, Chretien I, Winkler T, Brocker T. Functional comparison of thymic B cells and dendritic cells in vivo. Blood. 2000;95(8):2610-2616. (Pubitemid 30210540)
34. Crivellato E, Vacca A, Ribatti D. Setting the stage: an anatomist's view of the immune system. Trends Immunol. 2004;25(4):210-217. (Pubitemid 38368168)
35. Soares A, Govender L, Hughes J, et al. Novel application of Ki67 to quantify antigen-specific in vitro lymphoproliferation. J Immunol Methods. 2010;362(1):43-50.
36. Wirnsberger G, Mair F, Klein L. Regulatory T cell differentiation of thymocytes does not require a dedicated antigen-presenting cell but is under T cell-intrinsic developmental control. Proc Natl Acad Sci U S A. 2009;106(25):10278-10283.
37. Marks BR, Nowyhed HN, Choi JY, et al. Thymic self-reactivity selects natural interleukin 17-producing T cells that can regulate peripheral inflammation. Nat Immunol. 2009;10(10):1125-1132.
38. Suto A, Nakajima H, Ikeda K, et al. CD4(+)CD25(+) T-cell development is regulated by at least 2 distinct mechanisms. Blood. 2002;99(2):555-560. (Pubitemid 34533092)
39. Rankin AL, Reed AJ, Oh S, et al. CD4+ T cells recognizing a single self-peptide expressed by APCs induce spontaneous autoimmune arthritis. J Immunol. 2008;180(2):833-841.
40. Tanchot C, Barber DL, Chiodetti L, Schwartz RH. Adaptive tolerance of CD4+ T cells in vivo: multiple thresholds in response to a constant level of antigen presentation. J Immunol. 2001;167(4):2030-2039. (Pubitemid 32747510)
41. Sun JB, Flach CF, Czerkinsky C, Holmgren J. B lymphocytes promote expansion of regulatory T cells in oral tolerance: powerful induction by antigen coupled to cholera toxin B subunit. J Immunol. 2008;181(12):8278-8287.
42. Wolf SD, Dittel BN, Hardardottir F, Janeway CA Jr. Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J Exp Med. 1996;184(6):2271-2278. (Pubitemid 27023727)
43. Chen X, Jensen PE. Cutting edge: primary B lymphocytes preferentially expand allogeneic FoxP3+ CD4 T cells. J Immunol. 2007;179(4):2046-2050.
44. Hu CY, Rodriguez-Pinto D, Du W, et al. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J Clin Invest. 2007;117(12):3857-3867. (Pubitemid 350224095)
45. Moritoki Y, Zhang W, Tsuneyama K, et al. B cells suppress the inflammatory response in a mouse model of primary biliary cirrhosis. Gastroenterology. 2009;136(3):1037-1047.
46. 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(6):2554-2562.
47. Shah S, Qiao L. Resting B cells expand a CD4+CD25+Foxp3+ Treg population via TGF-beta3. Eur J Immunol. 2008;38(9):2488-2498.
48. Gros MJ, Naquet P, Guinamard RR. Cell intrinsic TGF-beta 1 regulation of B cells. J Immunol. 2008;180(12):8153-8158.
49. 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(6):2010-2015. (Pubitemid 40262003)
50. Phillips WJ, Smith DJ, Bona CA, Bot A, Zaghouani H. Recombinant immunoglobulin-based epitope delivery: a novel class of autoimmune regulators. Int Rev Immunol. 2005;24(5):501-517. (Pubitemid 41755158)
51. Scott DW. Gene therapy for immunological tolerance: using 'transgenic' B cells to treat inhibitor formation. Haemophilia. 2010;16(102):89-94.