CD45 ligation expands Tregs by promoting interactions with DCs

Journal of Clinical Investigation

Volumn 124, Issue 10, 2014, Pages 4603-4613

  Camirand, Geofrey ^a   Wang, Ying ^a   Lu, Yuning ^b   Wan, Yisong Y ^c   Lin, Yan ^a   Deng, Songyan ^d   Guz, Galip ^d   Perkins, David L ^e   Finn, Patricia W ^e   Farber, Donna L ^f   Flavell, Richard A ^g   Shlomchik, Warren D ^d   Lakkis, Fadi G ^a   Rudd, Christopher E ^b   Rothstein, David M ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF ILLINOIS   (United States)

^f Department of Medicine   (United States)

^g HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIGEN; CD45 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IMMUNOGLOBULIN G; INTEGRIN; INTERLEUKIN 2; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MONOCLONAL ANTIBODY; PROTEIN TYROSINE PHOSPHATASE; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR NFAT; VERY LATE ACTIVATION ANTIGEN 4; VERY LATE ACTIVATION ANTIGEN 5; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; LIGAND; NFATC2 PROTEIN, MOUSE; PTPRC PROTEIN, MOUSE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INTERACTION; CELL MOTILITY; CELL POPULATION; CONFOCAL MICROSCOPY; CONJUGATION; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; GRAFT SURVIVAL; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL PROLIFERATION; CYTOLOGY; FEMALE; HOMEOSTASIS; IMMUNOLOGICAL TOLERANCE; MALE; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD45; CELL PROLIFERATION; DENDRITIC CELLS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HOMEOSTASIS; IMMUNE TOLERANCE; INTERLEUKIN-2; LIGANDS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; NFATC TRANSCRIPTION FACTORS; T-LYMPHOCYTES, REGULATORY;

EID: 84907487311     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI74087     Document Type: Article

References (65)

1. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell. 2008;133(5):775-787.
2. Josefowicz SZ, Lu LF, Rudensky AY. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol. 2012;30(1):531-564.
3. 2+ regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J Exp Med. 2007;204(8):1757-1764.
4. Sun C-M, et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med. 2007;204(8):1775-1785.
5. Josefowicz SZ, et al. Extrathymically generated regulatory T cells control mucosal TH2 inflammation. Nature. 2012;482(7385):395-399.
6. Hippen KL, Riley JL, June CH, Blazar BR. Clinical perspectives for regulatory T cells in transplantation tolerance. Semin Immunol. 2011;23(6):462-468.
7. Gao W, Lu Y, El Essawy B, Oukka M, Kuchroo VK, Strom TB. Contrasting effects of cyclosporine and rapamycin in de novo generation of alloantigen-specific regulatory T cells. Am J Transplant. 2007;7(7):1722-1732.
8. Ochando JC, et al. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat Immunol. 2006;7(6):652-662.
9. 2+ regulatory T cells in the periphery of T cell receptor transgenic mice tolerized to transplants. J Immunol. 2004;172(10):6003-6010.
10. 2+ regulatory T cells are generated following CD40/CD154 blockade. Proc Natl Acad Sci U S A. 2011;108(51):20701-20706.
11. 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.
12. Fan Z, et al. In vivo tracking of 'color-coded' effector, natural and induced regulatory T cells in the allograft response. Nat Med. 2010;16(6):718-722.
13. Hori S, Haury M, Lafaille JJ, Demengeot J, Coutinho A. Peripheral expansion of thymus-derived regulatory cells in anti-myelin basic protein T cell receptor transgenic mice. Eur J Immunol. 2002;32(12):3729-3735.
14. Setoguchi R, Hori S, Takahashi T, Sakaguchi S. Homeostatic maintenance of natural Foxp3 (+) CD25 (+) CD4 (+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med. 2005;201(5):723-735.
15. Lin W, et al. Regulatory T cell development in the absence of functional Foxp3. Nat Immunol. 2007;8(4):359-368.
16. 2+ T cell homeostasis. J Immunol. 2008;181(3):1806.
17. Darrasse-Jèze G, et al. Feedback control of regulatory T cell homeostasis by dendritic cells in vivo. J Exp Med. 2009;206(9):1853-1862.
18. 2+ regulatory T cells. J Immunol. 2003;171(7):3348-3352.
19. 2+ immunoregulatory T cells that control autoimmune diabetes. Immunity. 2000;12(4):431-440.
20. Zhang R, Huynh A, Whitcher G, Chang J, Maltzman JS, Turka LA. An obligate cellintrinsic function for CD28 in Tregs. J Clin Invest. 2013;123(2):580-593.
21. Fontenot JD, Rasmussen JP, Gavin MA, Rudensky AY. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat Immunol. 2005;6(11):1142-1151.
22. Webster KE, et al. In vivo expansion of T reg cells with IL-2-mAb complexes: induction of resistance to EAE and long-term acceptance of islet allografts without immunosuppression. J Exp Med. 2009;206(4):751-760.
23. Chen CY, et al. IL-2 simultaneously expands Foxp3+ T regulatory and T effector cells and confers resistance to severe tuberculosis (TB): implicative Treg-T effector cooperation in immunity to TB. J Immunol. 2012;188(9):4278-4288.
24. 2+ T cells and NK cells driven by complexes of IL-2 and anti-IL-2 monoclonal antibody as novel approach of cancer immunotherapy. J Immunol. 2009;183(8):4904-4912.
25. Basadonna GP, et al. Antibody-mediated targeting of CD45 isoforms: a novel immunotherapeutic strategy. Proc Natl Acad Sci U S A. 1998;95(7):3821-3826.
26. Sho M, et al. Requirements for induction and maintenance of peripheral tolerance in stringent allograft models. Proc Natl Acad Sci U S A. 2005;102(37):13230-13235.
27. Ariyan C, et al. Cutting edge: transplantation tolerance through enhanced CTLA-4 expression. J Immunol. 2003;171(11):5673-5677.
28. Fecteau S, Basadonna GP, Freitas A, Ariyan C, Sayegh MH, Rothstein DM. CTLA-4 up-regulation plays a role in tolerance mediated by CD45. Nat Immunol. 2001;2(1):58-63.
29. Salvalaggio PR, et al. Antigen exposure during enhanced CTLA-4 expression promotes allograft tolerance in vivo. J Immunol. 2006;176(4):2292-2298.
30. Li MO, Wan YY, Flavell RA. T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity. 2007;26(5):579-591.
31. Wan YY, Flavell RA. 'Yin-Yang' functions of transforming growth factor-beta and T regulatory cells in immune regulation. Immunol Rev. 2007;220:199-213.
32. Chytil A, Magnuson MA, Wright CV, Moses HL. Conditional inactivation of the TGF-β type II receptor using Cre: Lox. Genesis. 2002;32(2):73-75.
33. Irie-Sasaki J, et al. CD45 is a JAK phosphatase and negatively regulates cytokine receptor signalling. Nature. 2001;409(6818):349-354.
34. Krutzik PO, Nolan GP. Intracellular phospho-protein staining techniques for flow cytometry: monitoring single cell signaling events. Cytometry A. 2003;55(2):61-70.
35. Dustin ML. Modular design of immunological synapses and kinapses. Cold Spring Harb Perspect Biol. 2009;1(1):a002873.
36. Negulescu PA, Krasieva TB, Khan A, Kerschbaum HH, Cahalan MD. Polarity of T cell shape, motility, and sensitivity to antigen. Immunity. 1996;4(5):421-430.
37. Dustin ML, Bromley SK, Kan Z, Peterson DA, Unanue ER. Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proc Natl Acad Sci U S A. 1997;94(8):3909-3913.
38. Mempel TR, Henrickson SE, Von Andrian UH. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature. 2004;427(6970):154-159.
39. Lu Y, Schneider H, Rudd CE. Murine regulatory T cells differ from conventional T cells in resisting the CTLA-4 reversal of TCR stop-signal. Blood. 2012;120(23):4560-4570.
40. Schneider H, et al. Reversal of the TCR stop signal by CTLA-4. Science. 2006;313(5795):1972-1975.
41. Grakoui A, et al. The immunological synapse: a molecular machine controlling T cell activation. Science. 1999;285(5425):221-227.
42. Waite JC, et al. Dynamic imaging of the effector immune response to listeria infection in vivo. PLoS Pathog. 2011;7(3):e1001326.
43. Tang Q, Bluestone JA, Kang SM. CD4 (+) Foxp3 (+) regulatory T cell therapy in transplantation. J Mol Cell Biol. 2012;4(1):11-21.
44. Brennan TV, et al. Requirements for prolongation of allograft survival with regulatory T cell infusion in lymphosufficient hosts. J Surg Res. 2011;169(1):e69-e75.
45. 2+ Tregs by TCR gene transfer favors transplantation tolerance in mice. J Clin Invest. 2008;118(11):3619-3628.
46. 2+ regulatory T cells promote experimental transplantation tolerance. Blood. 2007;109(2):827-835.
47. Schreiber TH, et al. Therapeutic Treg expansion in mice by TNFRSF25 prevents allergic lung inflammation. J Clin Invest. 2010;120(10):3629-3640.
48. Wang Y, et al. Regulatory T cells require mammalian target of rapamycin signaling to maintain both homeostasis and alloantigen-driven proliferation in lymphocyte-replete mice. J Immunol. 2011;186(5):2809-2818.
49. Leguern C. Regulatory T cells for tolerance therapy: revisiting the concept. Crit Rev Immunol. 2011;31(3):189-207.
50. Huehn J, Polansky JK, Hamann A. Epigenetic control of FOXP3 expression: the key to a stable regulatory T-cell lineage? Nat Rev Immunol. 2009;9(2):83-89.
51. Rubtsov YP, et al. Stability of the regulatory T cell lineage in vivo. Science. 2010;329(5999):1667-1671.
52. Polansky JK, et al. DNA methylation controls Foxp3 gene expression. Eur J Immunol. 2008;38(6):1654-1663.
53. Hill JA, et al. Foxp3 transcription-factor-dependent and -independent regulation of the regulatory T cell transcriptional signature. Immunity. 2007;27(5):786-800.
54. Gao Z, et al. Adoptively transferable tolerance induced by CD45RB monoclonal antibody. J Am Soc Nephrol. 1999;10(2):374-381.
55. 2+ T cell receptors. Immunity. 2004;21(2):267-277.
56. Sarris M, Andersen KG, Randow F, Mayr L, Betz AG. Neuropilin-1 expression on regulatory T cells enhances their interactions with dendritic cells during antigen recognition. Immunity. 2008;28(3):402-413.
57. Wu Y, et al. FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell. 2006;126(2):375-387.
58. 2+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro actively inhibit their maturation. Proc Natl Acad Sci U S A. 2008;105(29):10113-10118.
59. Edmonds SD, Ostergaard HL. Dynamic association of CD45 with detergent-insoluble microdomains in T lymphocytes. J Immunol. 2002;169(9):5036-5042.
60. Saunders AE, Johnson P. Modulation of immune cell signalling by the leukocyte common tyrosine phosphatase, CD45. Cell Signal. 2010;22(3):339-348.
61. Wong NK, Lai JC, Birkenhead D, Shaw AS, Johnson P. CD45 down-regulates Lck-mediated CD44 signaling and modulates actin rearrangement in T cells. J Immunol. 2008;181(10):7033-7043.
62. Hermiston ML, Xu Z, Weiss A. CD45: a critical regulator of signaling thresholds in immune cells. Annu Re v Immunol. 2003;21:107-137.
63. Birkeland ML, Johnson P, Trowbridge IS, Pure E. Changes in CD45 isoform expression accompany antigen-induced murine T-cell activation. Proc Natl Acad Sci U S A. 1989;86(17):6734-6738.
64. Wan YY, Flavell RA. Identifying Foxp3-expressing suppressor T cells with a bicistronic reporter. Proc Natl Acad Sci U S A. 2005;102(14):5126-5131.
65. Salvalaggio PR, et al. Islet filtration: a simple and rapid new purification procedure that avoids ficoll and improves islet mass and function. Transplantation. 2002;74(6):877-879.