Age-dependent divergent effects of OX40L treatment on the development of diabetes in NOD mice

Autoimmunity

Volumn 49, Issue 5, 2016, Pages 298-311

  Haddad, Christine S ^a   Bhattacharya, Palash ^a   Alharshawi, Khaled ^a   Marinelarena, Alejandra ^a   Kumar, Prabhakaran ^a   El Sayed, Osama ^a   Elshabrawy, Hatem A ^a   Epstein, Alan L ^b   Prabhakar, Bellur S ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Foxp3; IL 2; labile Tregs; Regulatory T cells; stable Tregs

Indexed keywords

CD103 ANTIGEN; CD38 ANTIGEN; CD4 ANTIGEN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 6; OX40 LIGAND; TRANSCRIPTION FACTOR FOXP3; AUTACOID; CD40 ANTIGEN; CD40 LIGAND; CYTOKINE; PROTEIN BINDING;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CELL SURVIVAL; CONTROLLED STUDY; DIABETES MELLITUS; DRUG EFFECT; EX VIVO STUDY; GLUCOSE BLOOD LEVEL; GROUPS BY AGE; HYPERGLYCEMIA; LYMPH NODE; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; THYMECTOMY; TREATMENT OUTCOME; AGE; ANIMAL; DENDRITIC CELL; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; NONOBESE DIABETIC MOUSE; SPLEEN; T LYMPHOCYTE SUBPOPULATION;

ADOPTIVE TRANSFER; AGE FACTORS; ANIMALS; BLOOD GLUCOSE; CD40 ANTIGENS; CD40 LIGAND; CYTOKINES; DENDRITIC CELLS; DIABETES MELLITUS; GENE EXPRESSION; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; INFLAMMATION MEDIATORS; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED NOD; PROTEIN BINDING; SPLEEN; T-LYMPHOCYTE SUBSETS;

EID: 84976606571     PISSN: 08916934     EISSN: 1607842X     Source Type: Journal    
DOI: 10.1080/08916934.2016.1183657     Document Type: Article

References (55)

1. C.Bossen, K.Ingold, A.Tardivel,. 2006. Interactions of tumor necrosis factor (TNF) and TNF receptor family members in the mouse and human. J. Biol. Chem. 281:13964–13971
2. A.Hoshino, Y.Tanaka, H.Akiba,. 2003. Critical role for OX40 ligand in the development of pathogenic Th2 cells in a murine model of asthma. Eur. J. Immunol. 33:861–869
3. T.Ito, R.Amakawa, M.Inaba,. 2004. Plasmacytoid dendritic cells regulate Th cell responses through OX40 ligand and type I IFNs. J. Immunol. 172:4253–4259
4. H.Akiba, H.Oshima, K.Takeda,. 1999. CD28-independent costimulation of T cells by OX40 ligand and CD70 on activated B cells. J. Immunol.162:7058–7066
5. J.T.Vetto, S.Lum, A.Morris,. 1997. Presence of the T-cell activation marker OX-40 on tumor infiltrating lymphocytes and draining lymph node cells from patients with melanoma and head and neck cancers. Am. J. Surg. 174:258–265
6. A.D.Weinberg, M.M.Rivera, R.Prell,. 2000. Engagement of the OX-40 receptor in vivo enhances antitumor immunity. J. Immunol. 164:2160–2169
7. A.Morris, J.T.Vetto, T.Ramstad,. 2001. Induction of anti-mammary cancer immunity by engaging the OX-40 receptor in vivo. Breast Cancer Res. Treat. 67:71–80
8. R.E.Sadun, W.E.Hsu, N.Zhang,. 2008. Fc-mOX40L fusion protein produces complete remission and enhanced survival in 2 murine tumor models. J. Immunother. 31:235–245
9. W.L.Redmond, C.E.Ruby, and A.D.Weinberg. 2009. The role of OX40-mediated co-stimulation in T-cell activation and survival. Crit. Rev. Immunol. 29:187–201
10. A.D.Weinberg, N.P.Morris, M.Kovacsovics-Bankowski,. 2011. Science gone translational:the OX40 agonist story. Immunol. Rev. 244:218–231
11. S.V.Pakala, P.Bansal-Pakala, B.S.Halteman, and M.Croft. 2004. Prevention of diabetes in NOD mice at a late stage by targeting OX40/OX40 ligand interactions. Eur. J. Immunol. 34:3039–3046
12. C.Nohara, H.Akiba, A.Nakajima,. 2001. Amelioration of experimental autoimmune encephalomyelitis with anti-OX40 ligand monoclonal antibody:a critical role for OX40 ligand in migration, but not development, of pathogenic T cells. J. Immunol. 166:2108–2115
13. A.D.Weinberg, D.N.Bourdette, T.J.Sullivan,. 1996. Selective depletion of myelin-reactive T cells with the anti-OX-40 antibody ameliorates autoimmune encephalomyelitis. Nat. Med. 2:183–189
14. L.M.Higgins, S.A.McDonald, N.Whittle,. 1999. Regulation of T cell activation in vitro and in vivo by targeting the OX40-OX40 ligand interaction:amelioration of ongoing inflammatory bowel disease with an OX40-IgG fusion protein, but not with an OX40 ligand-IgG fusion protein. J. Immunol. 162:486–493
15. M.D.Vu, X.Xiao, W.Gao,. 2007. OX40 costimulation turns off Foxp3+ Tregs. Blood. 110:2501–2510
16. T.Griseri, M.Asquith, C.Thompson, and F.Powrie. 2010. OX40 is required for regulatory T cell-mediated control of colitis. J. Exp. Med. 207:699–709
17. I.Takeda, S.Ine, N.Killeen,. 2004. Distinct roles for the OX40-OX40 ligand interaction in regulatory and nonregulatory T cells. J. Immunol. 172:3580–3589
18. C.E.Ruby, M.A.Yates, D.Hirschhorn-Cymerman,. 2009. Cutting Edge:OX40 agonists can drive regulatory T cell expansion if the cytokine milieu is right. J. Immunol. 183:4853–4857
19. D.Bresson, G.Fousteri, Y.Manenkova,. 2011. Antigen-specific prevention of type 1 diabetes in NOD mice is ameliorated by OX40 agonist treatment. J. Autoimmun. 37:342–351
20. D.Cheatem, B.B.Ganesh, E.Gangi,. 2009. Modulation of dendritic cells using granulocyte-macrophage colony-stimulating factor (GM-CSF) delays type 1 diabetes by enhancing CD4 + CD25+ regulatory T cell function. Clin. Immunol. 131:260–270
21. C.Vasu, R.N.Dogan, M.J.Holterman, and B.S.Prabhakar. 2003. Selective induction of dendritic cells using granulocyte macrophage-colony stimulating factor, but not fms-like tyrosine kinase receptor 3-ligand, activates thyroglobulin-specific CD4+/CD25+ T cells and suppresses experimental autoimmune thyroiditis. J. Immunol. 170:5511–5522
22. E.Gangi, C.Vasu, D.Cheatem, and B.S.Prabhakar. 2005. IL-10-producing CD4 + CD25+ regulatory T cells play a critical role in granulocyte-macrophage colony-stimulating factor-induced suppression of experimental autoimmune thyroiditis. J. Immunol. 174:7006–7013
23. J.R.Sheng, L.Li, B.B.Ganesh,. 2006. Suppression of experimental autoimmune myasthenia gravis by granulocyte-macrophage colony-stimulating factor is associated with an expansion of FoxP3+ regulatory T cells. J. Immunol.177:5296–5306
24. J.R.Sheng, L.C.Li, B.B.Ganesh,. 2008. Regulatory T cells induced by GM-CSF suppress ongoing experimental myasthenia gravis. Clin. Immunol. 128:172–180
25. M.N.Meriggioli, J.R.Sheng, L.Li, and B.S.Prabhakar. 2008. Strategies for treating autoimmunity:novel insights from experimental myasthenia gravis. Ann. N. Y. Acad. Sci. 1132:276–282
26. P.Bhattacharya, A.Gopisetty, B.B.Ganesh,. 2011. GM-CSF-induced, bone-marrow-derived dendritic cells can expand natural Tregs and induce adaptive Tregs by different mechanisms. J. Leukoc. Biol. 89:235–249
27. M.D.Sharma, L.Huang, J.H.Choi,. 2013. An inherently bifunctional subset of Foxp3+ T helper cells is controlled by the transcription factor eos. Immunity. 38:998–1012
28. F.Waldron-Lynch, M.von Herrath, and K.C.Herold. 2008. Towards a curative therapy n type 1 diabetes:remission of autoimmunity, maintenance and augmentation of beta cell mass. Novartis. Found. Symp. 292:146–155
29. D.M.Waid, G.M.Vaitaitis, N.D.Pennock, and D.H.WagnerJr.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
30. E.M.Akirav, J.Lebastchi, E.M.Galvan,. 2011. Detection of beta cell death in diabetes using differentially methylated circulating DNA. Proc. Natl. Acad. Sci. U. S. A. 108:19018–19023
31. A.Gopisetty, P.Bhattacharya, C.Haddad,. 2013. OX40L/Jagged1 cosignaling by GM-CSF-induced bone marrow-derived dendritic cells is required for the expansion of functional regulatory T cells. J. Immunol. 190:5516–5525
32. W.Chen, W.Jin, N.Hardegen,. 2003. Conversion of peripheral CD4 + CD25- naive T cells to CD4 + CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198:1875–1886
33. M.C.Fantini, C.Becker, G.Monteleone,. 2004. Cutting edge:TGF-beta induces a regulatory phenotype in CD4 + CD25- T cells through Foxp3 induction and down-regulation of Smad7. J. Immunol. 172:5149–5153
34. P.Hoffmann, T.J.Boeld, R.Eder,. 2009. Loss of FOXP3 expression in natural human CD4 + CD25+ regulatory T cells upon repetitive in vitro stimulation. Eur. J. Immunol. 39:1088–1097
35. D.Q.Tran, J.Andersson, D.Hardwick,. 2009. Selective expression of latency-associated peptide (LAP) and IL-1 receptor type I/II (CD121a/CD121b) on activated human FOXP3+ regulatory T cells allows for their purification from expansion cultures. Blood. 113:5125–5133
36. H.Kishimoto, and J.Sprent. 1997. Negative selection in the thymus includes semimature T cells. J. Exp. Med. 185:263–271
37. J.Sprent, and H.Kishimoto. 2001. The thymus and central tolerance. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356:609–616
38. G.T.Nepom, 2012. MHC class II tetramers. J. Immunol. 188:2477–2482
39. L.Zhang, M.Nakayama, and G.S.Eisenbarth. 2008. Insulin as an autoantigen in NOD/human diabetes. Curr. Opin. Immunol. 20:111–118
40. R.J.Chaparro, and T.P.Dilorenzo. 2010. An update on the use of NOD mice to study autoimmune (Type 1) diabetes. Expert. Rev. Clin. Immunol. 6:939–955
41. D.Daniel, R.G.Gill, N.Schloot, and D.Wegmann. 1995. Epitope specificity, cytokine production profile and diabetogenic activity of insulin-specific T cell clones isolated from NOD mice. Eur. J. Immunol. 25:1056–1062
42. M.Nakayama, N.Abiru, H.Moriyama,. 2005. Prime role for an insulin epitope in the development of type 1 diabetes in NOD mice. Nature. 435:220–223
43. Q.Tang, J.Y.Adams, C.Penaranda,. 2008. Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity. 28:687–697
44. M.A.Hulme, C.H.Wasserfall, M.A.Atkinson, and T.M.Brusko. 2012. Central role for interleukin-2 in type 1 diabetes. Diabetes. 61:14–22
45. L.A.Turka, and P.T.Walsh. 2008. IL-2 signaling and CD4+ CD25+ Foxp3+ regulatory T cells. Front. Biosci. 13:1440–1446
46. N.Komatsu, K.Okamoto, S.Sawa,. 2014. Pathogenic conversion of Foxp3+ T cells into TH17 cells in autoimmune arthritis. Nat. Med. 20:62–68
47. X.Zhou, S.L.Bailey-Bucktrout, L.T.Jeker,. 2009. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat. Immunol. 10:1000–1007
48. J.A.Todd, N.M.Walker, J.D.Cooper,. 2007. Robust associations of four new chromosome regions from genome-wide analyses of type 1 diabetes. Nat. Genet. 39:857–864
49. C.E.Lowe, J.D.Cooper, T.Brusko,. 2007. Large-scale genetic fine mapping and genotype-phenotype associations implicate polymorphism in the IL2RA region in type 1 diabetes. Nat. Genet. 39:1074–1082
50. H.Q.Qu, A.Montpetit, B.Ge,. 2007. Toward further mapping of the association between the IL2RA locus and type 1 diabetes. Diabetes. 56:1174–1176
51. A.Kaminitz, K.Mizrahi, and N.Askenasy. 2014. Surge in regulatory T cells does not prevent onset of hyperglycemia in NOD mice:immune profiles do not correlate with disease severity. Autoimmunity. 47:105–112
52. A.Zoka, G.Barna, A.Somogyi,. 2015. Extension of the CD4(+)Foxp3(+)CD25(-/low) regulatory T-cell subpopulation in type 1 diabetes mellitus. Autoimmunity. 48:289–297
53. Y.Grinberg-Bleyer, A.Baeyens, S.You,. 2010. IL-2 reverses established type 1 diabetes in NOD mice by a local effect on pancreatic regulatory T cells. J. Exp. Med. 207:1871–1878
54. M.Rosenzwajg, G.Churlaud, R.Mallone,. 2015. Low-dose interleukin-2 fosters a dose-dependent regulatory T cell tuned milieu in T1D patients. J. Autoimmun. 58:48–58
55. A.Yu, I.Snowhite, F.Vendrame,. 2015. Selective IL-2 responsiveness of regulatory T cells through multiple intrinsic mechanisms supports the use of low-dose IL-2 therapy in type 1 diabetes. Diabetes. 64:2172–2183