FcRγ Controls the Fas-Dependent Regulatory Function of Lymphoproliferative Double Negative T Cells

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Juvet, Stephen C ^a,b,c   Thomson, Christopher W ^a,c   Kim, Edward Y ^a,c   Han, Mei ^a,c   Zhang, Li ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FAS ANTIGEN; FC RECEPTOR; FC RECEPTOR GAMMA; UNCLASSIFIED DRUG; CD4 ANTIGEN; CD8 ANTIGEN; FAS PROTEIN, HUMAN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CONTROLLED STUDY; CYTOLYSIS; GRAFT VERSUS HOST REACTION; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; LYMPHOPROLIFERATIVE DISEASE; MALE; MOUSE; NONHUMAN; T LYMPHOCYTE; ANIMAL; AUTOIMMUNE LYMPHOPROLIFERATIVE SYNDROME; CELL PROLIFERATION; DEFICIENCY; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; PATHOLOGY; TRANSPLANTATION;

MUS;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD4; ANTIGENS, CD8; ANTIGENS, CD95; AUTOIMMUNE LYMPHOPROLIFERATIVE SYNDROME; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; MALE; MICE; RECEPTORS, IGG;

EID: 84878775078     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065253     Document Type: Article

References (50)

1. Klinman DM, Eisenberg RA, Steinberg AD, (1990) Development of the autoimmune B cell repertoire in MRL-lpr/lpr mice. J Immunol 144: 506-511.
2. Jevnikar AM, Grusby MJ, Glimcher LH, (1994) Prevention of nephritis in major histocompatibility complex class II-deficient MRL-lpr mice. J Exp Med 179: 1137-1143.
3. Merino R, Fossati L, Iwamoto M, Takahashi S, Lemoine R, et al. (1995) Effect of long-term anti-CD4 or anti-CD8 treatment on the development of lpr CD4- CD8- double negative T cells and of the autoimmune syndrome in MRL-lpr/lpr mice. J Autoimmun 8: 33-45.
4. Ford MS, Young KJ, Zhang Z, Ohashi PS, Zhang L, (2002) The immune regulatory function of lymphoproliferative double negative T cells in vitro and in vivo. J Exp Med 196: 261-267.
5. Hamad AR, Mohamood AS, Trujillo CJ, Huang CT, Yuan E, et al. (2003) B220+ double-negative T cells suppress polyclonal T cell activation by a Fas-independent mechanism that involves inhibition of IL-2 production. J Immunol 171: 2421-2426.
6. Gonzalez-Quintial R, Lawson BR, Scatizzi JC, Craft J, Kono DH, et al. (2011) Systemic autoimmunity and lymphoproliferation are associated with excess IL-7 and inhibited by IL-7Ralpha blockade. PLoS One 6: e27528.
7. Kyttaris VC, Zhang Z, Kuchroo VK, Oukka M, Tsokos GC, (2010) Cutting edge: IL-23 receptor deficiency prevents the development of lupus nephritis in C57BL/6-lpr/lpr mice. J Immunol 184: 4605-4609.
8. Zhang Z, Kyttaris VC, Tsokos GC, (2009) The role of IL-23/IL-17 axis in lupus nephritis. J Immunol 183: 3160-3169.
9. Kakkanaiah VN, Nagarkatti M, Nagarkatti PS, (1990) Evidence for the existence of distinct heterogeneity among the peripheral CD4-CD8- T cells from MRL-lpr/lpr mice based on the expression of the J11d marker, activation requirements, and functional properties. Cell Immunol 127: 442-457.
10. Nimmerjahn F, Ravetch JV, (2007) Fc-receptors as regulators of immunity. Adv Immunol 96: 179-204.
11. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV, (1994) FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 76: 519-529.
12. Orloff DG, Ra CS, Frank SJ, Klausner RD, Kinet JP, (1990) Family of disulphide-linked dimers containing the zeta and eta chains of the T-cell receptor and the gamma chain of Fc receptors. Nature 347: 189-191.
13. Shores E, Flamand V, Tran T, Grinberg A, Kinet JP, et al. (1997) Fc epsilonRI gamma can support T cell development and function in mice lacking endogenous TCR zeta-chain. J Immunol 159: 222-230.
14. Ohno H, Ono S, Hirayama N, Shimada S, Saito T, (1994) Preferential usage of the Fc receptor gamma chain in the T cell antigen receptor complex by gamma/delta T cells localized in epithelia. J Exp Med 179: 365-369.
15. Park SY, Arase H, Wakizaka K, Hirayama N, Masaki S, et al. (1995) Differential contribution of the FcR gamma chain to the surface expression of the T cell receptor among T cells localized in epithelia: analysis of FcR gamma-deficient mice. Eur J Immunol 25: 2107-2110.
16. Enyedy EJ, Nambiar MP, Liossis SN, Dennis G, Kammer GM, et al. (2001) Fc epsilon receptor type I gamma chain replaces the deficient T cell receptor zeta chain in T cells of patients with systemic lupus erythematosus. Arthritis Rheum 44: 1114-1121.
17. Krishnan S, Warke VG, Nambiar MP, Tsokos GC, Farber DL, (2003) The FcR gamma subunit and Syk kinase replace the CD3 zeta-chain and ZAP-70 kinase in the TCR signaling complex of human effector CD4 T cells. J Immunol 170: 4189-4195.
18. Okoye FI, Krishnan S, Chandok MR, Tsokos GC, Farber DL, (2007) Proximal signaling control of human effector CD4 T cell function. Clin Immunol 125: 5-15.
19. Nambiar MP, Fisher CU, Kumar A, Tsokos CG, Warke VG, et al. (2003) Forced expression of the Fc receptor gamma-chain renders human T cells hyperresponsive to TCR/CD3 stimulation. J Immunol 170: 2871-2876.
20. Zhang ZX, Yang L, Young KJ, DuTemple B, Zhang L, (2000) Identification of a previously unknown antigen-specific regulatory T cell and its mechanism of suppression. Nat Med 6: 782-789.
21. Young KJ, Yang L, Phillips MJ, Zhang L, (2002) Donor-lymphocyte infusion induces transplantation tolerance by activating systemic and graft-infiltrating double-negative regulatory T cells. Blood 100: 3408-3414.
22. Chen W, Ford MS, Young KJ, Zhang L, (2003) Infusion of in vitro-generated DN T regulatory cells induces permanent cardiac allograft survival in mice. Transplant Proc 35: 2479-2480.
23. Young KJ, DuTemple B, Phillips MJ, Zhang L, (2003) Inhibition of graft-versus-host disease by double-negative regulatory T cells. J Immunol 171: 134-141.
24. Lee BP, Mansfield E, Hsieh SC, Hernandez-Boussard T, Chen W, et al. (2005) Expression profiling of murine double-negative regulatory T cells suggest mechanisms for prolonged cardiac allograft survival. J Immunol 174: 4535-4544.
25. Thomson CW, Teft WA, Chen W, Lee BP, Madrenas J, et al. (2006) FcR gamma presence in TCR complex of double-negative T cells is critical for their regulatory function. J Immunol 177: 2250-2257.
26. Juvet SC, Thomson CW, Kim EY, Joe B, Adeyi O, et al. (2013) FcRgamma promotes T cell apoptosis in Fas-deficient mice. J Autoimmun in press.
27. Davidson WF, Dumont FJ, Bedigian HG, Fowlkes BJ, Morse HC 3rd (1986) Phenotypic, functional, and molecular genetic comparisons of the abnormal lymphoid cells of C3H-lpr/lpr and C3H-gld/gld mice. J Immunol 136: 4075-4084.
28. Gao JF, McIntyre MS, Juvet SC, Diao J, Li X, et al. (2011) Regulation of Antigen-expressing Dendritic Cells by Double Negative Regulatory T Cells. Eur J Immunol.
29. Juvet SC, Han M, Vanama R, Joe B, Kim EY, et al. (2012) Autocrine IFNgamma Controls the Regulatory Function of Lymphoproliferative Double Negative T Cells. PLoS One 7: e47732.
30. Hillhouse EE, Lesage S (2012) A comprehensive review of the phenotype and function of antigen-specific immunoregulatory double negative T cells. J Autoimmun.
31. Juvet SC, Zhang L, (2012) Double negative regulatory T cells in transplantation and autoimmunity: recent progress and future directions. J Mol Cell Biol 4: 48-58.
32. Paulsen M, Valentin S, Mathew B, Adam-Klages S, Bertsch U, et al. (2011) Modulation of CD4+ T-cell activation by CD95 co-stimulation. Cell Death Differ 18: 619-631.
33. Strauss G, Lindquist JA, Arhel N, Felder E, Karl S, et al. (2009) CD95 co-stimulation blocks activation of naive T cells by inhibiting T cell receptor signaling. J Exp Med 206: 1379-1393.
34. Rodewald HR, Arulanandam AR, Koyasu S, Reinherz EL, (1991) The high affinity Fc epsilon receptor gamma subunit (Fc epsilon RI gamma) facilitates T cell receptor expression and antigen/major histocompatibility complex-driven signaling in the absence of CD3 zeta and CD3 eta. J Biol Chem 266: 15974-15978.
35. Ohno H, Aoe T, Ra C, Yamamoto T, Saito T, (1993) TCR isoform containing the Fc receptor gamma chain exhibits structural and functional differences from isoform containing CD3 zeta. Int Immunol 5: 1403-1411.
36. Chu JL, Ramos P, Rosendorff A, Nikolic-Zugic J, Lacy E, et al. (1995) Massive upregulation of the Fas ligand in lpr and gld mice: implications for Fas regulation and the graft-versus-host disease-like wasting syndrome. J Exp Med 181: 393-398.
37. Watanabe D, Suda T, Hashimoto H, Nagata S, (1995) Constitutive activation of the Fas ligand gene in mouse lymphoproliferative disorders. EMBO J 14: 12-18.
38. Bossi G, Griffiths GM, (1999) Degranulation plays an essential part in regulating cell surface expression of Fas ligand in T cells and natural killer cells. Nat Med 5: 90-96.
39. Lettau M, Qing J, Kabelitz D, Janssen O, (2004) Activation-dependent FasL expression in T lymphocytes and natural killer cells. Signal Transduction 4: 206-211.
40. Fontenot JD, Gavin MA, Rudensky AY, (2003) Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 4: 330-336.
41. Azzoni L, Anegon I, Calabretta B, Perussia B, (1995) Ligand binding to Fc gamma R induces c-myc-dependent apoptosis in IL-2-stimulated NK cells. J Immunol 154: 491-499.
42. Eischen CM, Schilling JD, Lynch DH, Krammer PH, Leibson PJ, (1996) Fc receptor-induced expression of Fas ligand on activated NK cells facilitates cell-mediated cytotoxicity and subsequent autocrine NK cell apoptosis. J Immunol 156: 2693-2699.
43. Ortaldo JR, Mason AT, O'Shea JJ, (1995) Receptor-induced death in human natural killer cells: involvement of CD16. J Exp Med 181: 339-344.
44. Gupta S, Thornley TB, Gao W, Larocca R, Turka LA, et al. (2012) Allograft rejection is restrained by short-lived TIM-3+PD-1+Foxp3+ Tregs. J Clin Invest 122: 2395-2404.
45. Hastings WD, Anderson DE, Kassam N, Koguchi K, Greenfield EA, et al. (2009) TIM-3 is expressed on activated human CD4+ T cells and regulates Th1 and Th17 cytokines. Eur J Immunol 39: 2492-2501.
46. Monney L, Sabatos CA, Gaglia JL, Ryu A, Waldner H, et al. (2002) Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease. Nature 415: 536-541.
47. Sanchez-Fueyo A, Tian J, Picarella D, Domenig C, Zheng XX, et al. (2003) Tim-3 inhibits T helper type 1-mediated auto- and alloimmune responses and promotes immunological tolerance. Nat Immunol 4: 1093-1101.
48. Voelkl S, Gary R, Mackensen A, (2011) Characterization of the immunoregulatory function of human TCR-alphabeta+ CD4- CD8- double-negative T cells. Eur J Immunol 41: 739-748.
49. Fischer K, Voelkl S, Heymann J, Przybylski GK, Mondal K, et al. (2005) Isolation and characterization of human antigen-specific TCR alpha beta+ CD4(-)CD8- double-negative regulatory T cells. Blood 105: 2828-2835.
50. Cooke KR, Kobzik L, Martin TR, Brewer J, Delmonte J Jr, et al. (1996) An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood 88: 3230-3239.