Effector and naturally occurring regulatory T cells display no abnormalities in activation induced cell death in NOD mice

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Kaminitz, Ayelet ^a,b   Yolcu, Esma S ^c   Askenasy, Enosh M ^a   Stein, Jerry ^a   Yaniv, Isaac ^a,b   Shirwan, Haval ^c   Askenasy, Nadir ^a  

^a SCHNEIDER CHILDREN S MEDICAL CENTER OF ISRAEL   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD3 ANTIGEN; FAS ANTIGEN; FAS LIGAND; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; CD4+ T LYMPHOCYTE; CELL DEATH; CONTROLLED STUDY; CROSS LINKING; EFFECTOR CELL; HOMEOSTASIS; IN VITRO STUDY; INCIDENCE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; NONHUMAN; NONOBESE DIABETIC MOUSE; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; SCID MOUSE; UPREGULATION; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; DRUG EFFECT; FLOW CYTOMETRY; IMMUNOLOGY; METABOLISM; MOUSE;

ERAGROSTIS TEF; MUS;

ANIMALS; ANTIGENS, CD28; APOPTOSIS; CELL DEATH; CELL PROLIFERATION; CELLS, CULTURED; FAS LIGAND PROTEIN; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN-2; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; T-LYMPHOCYTES, REGULATORY;

EID: 79959609103     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021630     Document Type: Article

References (66)

1. Delovitch TL, Singh B, (1997) The non-obese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity 7: 727-738.
2. Kukreja A, Cost G, Marker J, Zhang C, Sun Z, et al. (2002) Multiple immuno-regulatory defects in type-1 diabetes. J Clin Invest 109: 131-140.
3. Waid DM, Vaitaitis GM, Pennock ND, Wagner DH Jr, (2008) Disruption of the homeostatic balance between autoaggressive (CD4+CD40+) and regulatory (CD4+CD25+FoxP3+) T cells promotes diabetes. J Leukoc Biol 84: 431-439.
4. D'Alise AM, Auyeung V, Feuerer M, Nishio J, Fontenot J, et al. (2008) The defect in T-cell regulation in NOD mice is an effect on the T-cell effectors. Proc Natl Acad Sci USA 105: 19857-1962.
5. Yarkoni S, Kaminitz A, Sagiv Y, Yaniv I, Askenasy N, (2010) Targeted depletion of cells expressing the IL-2 receptor disrupts autoimmunity in prediabetic NOD mice. Diabetologia 53: 356-368.
6. Belghith M, Bluestone JA, Barriot S, Megret J, Bach JF, et al. (2003) TGF-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat Med 9: 1202-1208.
7. Berzins SP, Venanzi ES, Benoist C, Mathis D, (2003) T-cell compartments of prediabetic NOD mice. Diabetes 52: 327-334.
8. Gregg RK, Jain R, Schoenleber SJ, Divekar R, Bell JJ, et al. (2004) A sudden decline in active membranebound TGF-beta impairs both T regulatory cell function and protection against autoimmune diabetes. J Immunol 173: 7308-7316.
9. Lindley S, Dayan CM, Bishop A, Roep BO, Peakman M, et al. (2005) Defective suppressor function in CD4(+)CD25(+) T-cells from patients with type 1 diabetes. Diabetes 2005;54: 92-9.
10. Tritt M, Sgouroudis E, d'Hennezel E, Albanese A, Piccirillo CA, (2008) Functional waning of naturally occurring CD4+ regulatory T-cells contributes to the onset of autoimmune diabetes. Diabetes 57: 113-123.
11. Gregori S, Giarratana N, Smiroldo S, Adorini L, (2003) Dynamics of pathogenic and suppressor T cells in autoimmune diabetes development. J Immunol 171: 4040-4047.
12. Pop SM, Wong CP, Culton DA, Clarke SH, Tisch R, (2005) Single cell analysis shows decreasing FoxP3 and TGFbeta1 coexpressing CD4+CD25+ regulatory T cells during autoimmune diabetes. J Exp Med 201: 1333-1346.
13. You S, Belghith M, Cobbold S, Alyanakian MA, Gouarin C, et al. (2005) Autoimmune diabetes onset results from qualitative rather than quantitative age-dependent changes in pathogenic T-cells. Diabetes 54: 1415-1422.
14. Askenasy N, Yolcu ES, Yaniv I, Shirwan H, (2005) Induction of tolerance using Fas ligand: a double-edged immunomodulator. Blood 105: 1396-1404.
15. Decallonne B, van Etten E, Giulietti A, Casteels K, Overbergh L, et al. (2003) Defect in activation induced cell death in non-obese diabetic (NOD) T lymphocytes. J Autoimmun 20: 219-226.
16. Yang W, Hussain S, Mi QS, Santamaria P, Delovitch TL, (2004) Perturbed homeostasis of peripheral T cells elicits decreased susceptibility to anti-CD3-induced apoptosis in prediabetic nonobese diabetic mice. J Immunol 173: 4407-4416.
17. Arreaza G, Salojin K, Yang W, Zhang J, Gill B, et al. (2003) Deficient activation and resistance to activation-induced apoptosis of CD8+ T cells is associated with defective peripheral tolerance in nonobese diabetic mice. Clin Immunol 107: 103-15.
18. Kishimoto H, Sprent J, (2001) A defect in central tolerance in NOD mice. Nat Immunol 2: 1025-1031.
19. Banz A, Pontoux C, Papiernik M, (2002) Modulation of Fas-dependent apoptosis: a dynamic process controlling both the persistence and death of CD4 regulatory T cells and effector T cells. J Immunol 169: 750-757.
20. Fritzsching B, Oberle N, Pauly E, Geffers R, Buer J, et al. (2006) Naive regulatory T cells: a novel subpopulation defined by resistance toward CD95L-mediated cell death. Blood 108: 3371-3378.
21. Weber SE, Harbertson J, Godebu E, Mros GA, Padrick RC, et al. (2006) Adaptive islet-specific regulatory CD4 T cells control autoimmune diabetes and mediate the disappearance of pathogenic Th1 cells in vivo. J Immunol 176: 4730-4739.
22. Taams LS, Smith J, Rustin MH, Salmon M, Poulter LW, et al. (2001) Human anergic/suppressive CD4(+)CD25(+) T cells: a highly differentiated and apoptosis-prone population. Eur J Immunol 31: 1122-1131.
23. Fritzsching B, Oberle N, Eberhardt N, Quick S, Haas J, et al. (2005) In contrast to effector T cells, CD4+CD25+FoxP3+ regulatory T cells are highly susceptible to CD95 ligand- but not to TCR-mediated cell death. J Immunol 175: 32-36.
24. Mohamood AS, Trujillo CJ, Zheng D, Jie C, Murillo FM, et al. (2006) Gld mutation of Fas ligand increases the frequency and up-regulates cell survival genes in CD25+CD4+ TR cells. Int Immunol 18: 1265-1277.
25. Klein L, Khazaie K, von Boehmer H, (2003) In vivo dynamics of antigen-specific regulatory T cells not predicted from behavior in vitro. Proc Natl Acad Sci USA 100: 8886-8891.
26. Yarkoni S, Kaminitz A, Sagiv Y, Yaniv I, Askenasy N, (2008) Involvement of IL-2 in homeostasis of regulatory T cells: the IL-2 cycle. Bio Essays 30: 875-88.
27. Kaminitz A, Askenasy EM, Yaniv I, Stein J, Askenasy N, (2010) Apoptosis of purified CD4+ T cell subsets is dominated by cytokine deprivation and absence of other cells in new onset diabetic NOD mice. PLoS One 5: e15684.
28. Yolcu ES, Kaminitz A, Ash S, Sagiv Y, Askenasy N, et al. (2008) Apoptosis as a mechanism of T regulatory cell homeostasis and suppression. Immunol Cell Biol 86: 650-658.
29. Setoguchi R, Hori S, Takahashi T, Sakaguchi S, (2005) 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 201: 723-735.
30. Tang Q, Adams JY, Penaranda C, Melli K, Piaggio E, et al. (2008) Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity 28: 687-697.
31. Lenardo MJ, (1991) Interleukin-2 programs mouse alpha beta T lymphocytes for apoptosis. Nature 353: 858-861.
32. Kneitz B, Herrmann T, Yonehara S, Schimpl A, (1995) Normal clonal expansion but impaired Fas-mediated cell death and anergy induction in interleukin-2-deficient mice. Eur J Immunol 25: 2672-2677.
33. Parijs LV, Biuckians A, Ibragimov A, Alt FW, Willerford DM, et al. (1997) Functional responses and apoptosis of CD25 (IL-2Rα)-deficient T cells expressing a transgenic antigen receptor. J Immunol 158: 3738-3745.
34. Kaminitz A, Yolcu ES, Stein J, Yaniv I, Shirwan H, et al. (2011) Killer Treg restore immune homeostasis and suppress autoimmune diabetes in prediabetic NOD mice. J Autoimmun in press.
35. Franke DD, Yolcu ES, Alard P, Kosiewicz MM, Shirwan H, (2007) A novel multimeric form of FasL modulates the ability of diabetogenic T cells to mediate type 1 diabetes in an adoptive transfer model. Mol Immunol 44: 2884-2892.
36. Pearl-Yafe M, Kaminitz A, Yolcu ES, Yaniv I, Stein J, et al. (2007) Pancreatic islets under attack: cellular and molecular effectors. Curr Pharm Des 13: 749-60.
37. Giordano C, De Maria R, Stassi G, Todaro M, Richiusa P, et al. (1995) Defective expression of the apoptosis-inducing CD95 (Fas/APO-1) molecule on T and B cells in IDDM. Diabetologia 38: 1449-1454.
38. Colucci F, Cilio CM, Lejon K, Gonçalves CP, Bergman ML, et al. (1996) Programmed cell death in the pathogenesis of murine IDDM: resistance to apoptosis induced in lymphocytes by cyclophosphamide. J Autoimmun 9: 271-276.
39. Radosevic K, Casteels KM, Mathieu C, van Ewijk W, Drexhage H, et al. (1999) Splenic dendritic cells from the nonobese diabetic mouse induce a prolonged proliferation of syngeneic T cells. A role for an impaired apoptosis of NOD T cells? J Autoimmun 13: 373-382.
40. Putnam AL, Vendrame F, Dotta F, Gottlieb PA, (2005) CD4+CD25high regulatory T cells in human autoimmune diabetes. J Autoimmun 24: 55-62.
41. von Boehmer H, (2005) Mechanisms of suppression by suppressor T cells. Nat Immunol 6: 338-344.
42. Miyara M, Sakaguchi S, (2007) Natural regulatory T cells: mechanisms of suppression. Trends Mol Med 13: 108-116.
43. Askenasy N, Kaminitz A, Yarkoni S, (2008) Mechanisms of T regulatory cell function. Autoimmun Rev 7: 370-375.
44. Shevach EM, (2009) Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity 30: 636-645.
45. Pandiyan P, Zheng L, Ishihara S, Reed J, Lenardo MJ, (2007) CD4+CD25+Foxp3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells. Nat Immunol 8: 1353-1362.
46. Pandiyan P, Lenardo MJ, (2008) The control of CD4+CD25+Foxp3+ regulatory T cell survival. Biol Direct 3: 6.
47. Wang R, Rogers AM, Rush BJ, Russell JH, (1996) Induction of sensitivity to activation-induced death in primary CD4+ cells: a role for interleukin-2 in the negative regulation of responses by mature CD4+ T cells. Eur J Immunol 26: 2263-2270.
48. Refaeli Y, Van Parijs L, London CA, Tschopp J, Abbas AK, (1998) Biochemical mechanisms of IL-2-regulated Fas-mediated T cell apoptosis. Immunity 8: 615-623.
49. de la Rosa M, Rutz S, Dorninger H, Scheffold A, (2004) Interleukin-2 is essential for CD4+CD25+ regulatory T cell function. Eur J Immunol 34: 2480-2488.
50. Feinerman O, Jentsch G, Tkach KE, Coward JW, Hathorn MM, et al. (2010) Single-cell quantification of IL-2 response by effector and regulatory T cells reveals critical plasticity in immune response. Mol Syst Biol 6: 437.
51. Lan RY, Selmi C, Gershwin ME, (2008) The regulatory, inflammatory, and T cell programming roles of interleukin-2 (IL-2). J Autoimmun 31: 7-12.
52. Salomon B, Lenschow DJ, Rhee L, Ashourian N, Singh B, et al. (2000) B7/CD28 co-stimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 12: 431-440.
53. Arreaza GA, Cameron MJ, Jaramillo A, Gill BM, Hardy D, et al. (1997) Neonatal activation of CD28 signaling overcomes T cell anergy and prevents autoimmune diabetes by an IL-4-dependent mechanism. J Clin Invest 100: 2243-2253.
54. Tang Q, Henriksen KJ, Boden EK, Tooley AJ, Ye J, et al. (2003) Cutting edge: CD28 controls peripheral homeostasis of CD4+ CD25+ regulatory T cells. J Immunol 171: 3348-3352.
55. Schneider A, Rieck M, Sanda S, Pihoker C, Greenbaum C, et al. (2008) The effector T cells of diabetic subjects are resistant to regulation via CD4+ FOXP3+ regulatory T cells. J Immunol 181: 7350-3755.
56. Yolcu ES, Askenasy N, Singh NP, Cherradi SE, Shirwan H, (2002) Cell membrane modification for rapid display of proteins as a novel means of immunomodulation: FasL-decorated cells prevent islet graft rejection. Immunity 17: 795-808.
57. Christen U, Darwiche R, Thomas HE, Wolfe T, Rodrigo E, et al. (2004) Virally induced inflammation triggers fratricide of Fas-ligand-expressing beta-cells. Diabetes 53: 591-596.
58. Pearl-Yafe M, Yolcu ES, Yaniv I, Stein J, Shirwan H, et al. (2006) The dual role of Fas-ligand as an injury effector and defense strategy in diabetes and islet transplantation. Bioessays 28: 211-222.
59. Kaminitz A, Mizrahi K, Yaniv I, Farkas DL, Stein J, et al. (2009) Low levels of allogeneic but not syngeneic hematopoietic chimerism reverse autoimmune insulitis in prediabetic NOD mice. J Autoimmun 33: 83-91.
60. Kaminitz A, Mizrahi K, Yaniv I, Stein J, Askenasy N, (2010) Immunosuppressive therapy exacerbates autoimmunity in NOD mice and diminishes the protective activity of regulatory T cells. J Autoimmun 35: 145-152.
61. Li H, Kaufman CL, Boggs SS, Johnson PC, Patrene KD, et al. (1996) Mixed allogeneic chimerism induced by a sublethal approach prevents autoimmune diabetes and reverses insulitis in non-obese diabetic (NOD) mice. J Immunol 156: 380-388.
62. Beilhack GF, Scheffold YC, Weissman IL, Taylor C, Jerabek L, et al. (2003) Purified allogeneic hematopoietic stem cell transplantation blocks diabetes pathogenesis in NOD mice. Diabetes 52: 59-68.
63. Askenasy EM, Askenasy N, Askenasy JJ, (2010) Does lymphopenia preclude restoration of immune homeostasis? The particular case of type 1 diabetes. Autoimmun Rev 9: 687-690.
64. Yaniv I, Ash S, Farkas DL, Askenasy N, Stein J, (2009) Consideration of strategies for hematopoietic cell transplantation. J Autoimmun 33: 255-259.
65. Serreze DV, Hamaguchi K, Leiter EH, (1989) Immunostimulation circumvents diabetes in NOD/Lt mice. J Autoimmun 2: 759-776.
66. Pearl-Yafe M, Yolcu ES, Stein J, Kaplan O, Yaniv I, et al. (2007) Fas ligand enhances hematopoietic cell engraftment through abrogation of alloimmune responses and nonimmunogenic interactions. Stem Cells 25: 1448-1455.