IL-2 production by dendritic cells promotes Foxp3⁺ regulatory T-cell expansion in autoimmune-resistant NOD congenic mice

References

• Bach JF, Chatenoud L. Tolerance to islet autoantigens in type 1 diabetes. Annu Rev Immunol. 2001; 19:131–161.
   PubMed Web of Science ®Google Scholar
• Anderson MS, Bluestone JA. The NOD mouse: A model of immune dysregulation. Annu Rev Immunol. 2005; 23:447–485.
   PubMed Web of Science ®Google Scholar
• Bluestone JA, Tang Q. How do CD4+ CD25+ regulatory T cells control autoimmunity?. Curr Opin Immunol. 2005; 17:638–642.
   PubMed Web of Science ®Google Scholar
• Tang Q, Henriksen KJ, Boden EK, Tooley AJ, Ye J, Subudhi SK, Zheng XX, Strom TB, Bluestone JA. Cutting edge: CD28 controls peripheral homeostasis of CD4+ CD25+ regulatory T cells. J Immunol. 2003; 171:3348–3352.
   PubMed Web of Science ®Google Scholar
• Chen Z, Herman AE, Matos M, Mathis D, Benoist C. Where CD4+ CD25+ T reg cells impinge on autoimmune diabetes. J Exp Med. 2005; 202:1387–1397.
   PubMed Web of Science ®Google Scholar
• Salomon B, Lenschow DJ, Rhee L, Ashourian N, Singh B, Sharpe A, Bluestone JA. B7/CD28 costimulation is essential for the homeostasis of the CD4+ CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity. 2000; 12:431–440.
   PubMed Web of Science ®Google Scholar
• Serra P, Amrani A, Yamanouchi J, Han B, Thiessen S, Utsugi T, Verdaguer J, Santamaria P. CD40 ligation releases immature dendritic cells from the control of regulatory CD4+ CD25+ T cells. Immunity. 2003; 19:877–889.
   PubMed Web of Science ®Google Scholar
• 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; 201:723–735.
   PubMed Web of Science ®Google Scholar
• Mellanby RJ, Thomas D, Phillips JM, Cooke A. Diabetes in non-obese diabetic mice is not associated with quantitative changes in CD4+ CD25+ Foxp3+ regulatory T cells. Immunology. 2007; 121:15–28.
   PubMed Web of Science ®Google Scholar
• Brusko T, Wasserfall C, McGrail K, Schatz R, Viener HL, Schatz D, Haller M, Rockell J, Gottlieb P, Clare-Salzler M, Atkinson M. No alterations in the frequency of FOXP3+ regulatory T-cells in type 1 diabetes. Diabetes. 2007; 56:604–612.
   PubMed Web of Science ®Google Scholar
• You S, Belghith M, Cobbold S, Alyanakian MA, Gouarin C, Barriot S, Garcia C, Waldmann H, Bach JF, Chatenoud L. Autoimmune diabetes onset results from qualitative rather than quantitative age-dependent changes in pathogenic T-cells. Diabetes. 2005; 54:1415–1422.
   PubMed Web of Science ®Google Scholar
• Sgouroudis E, Albanese A, Piccirillo CA. Impact of protective IL-2 allelic variants on CD4+ Foxp3+ regulatory T cell function in situ and resistance to autoimmune diabetes in NOD mice. J Immunol. 2008; 181:6283–6292.
   PubMed Web of Science ®Google Scholar
• Tritt M, Sgouroudis E, d'Hennezel E, Albanese A, Piccirillo CA. Functional waning of naturally occurring CD4+ regulatory T-cells contributes to the onset of autoimmune diabetes. Diabetes. 2008; 57:113–123.
   PubMed Web of Science ®Google Scholar
• Pop SM, Wong CP, Culton DA, Clarke SH, Tisch R. Single cell analysis shows decreasing FoxP3 and TGFbeta1 coexpressing CD4+ CD25+ regulatory T cells during autoimmune diabetes. J Exp Med. 2005; 201:1333–1346.
   PubMed Web of Science ®Google Scholar
• Tang Q, Adams JY, Penaranda C, Melli K, Piaggio E, Sgouroudis E, Piccirillo CA, Salomon BL, Bluestone JA. Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity. 2008; 28:687–697.
   PubMed Web of Science ®Google Scholar
• Wicker LS, Todd JA, Prins JB, Podolin PL, Renjilian RJ, Peterson LB. Resistance alleles at two non-major histocompatibility complex-linked insulin-dependent diabetes loci on chromosome 3, Idd3 and Idd10, protect nonobese diabetic mice from diabetes. J Exp Med. 1994; 180:1705–1713.
   PubMed Web of Science ®Google Scholar
• Yamanouchi J, Rainbow D, Serra P, Howlett S, Hunter K, Garner VE, Gonzalez-Munoz A, Clark J, Veijola R, Cubbon R, Chen SL, Rosa R, Cumiskey AM, Serreze DV, Gregory S, Rogers J, Lyons PA, Healy B, Smink LJ, Todd JA, Peterson LB, Wicker LS, Santamaria P. Interleukin-2 gene variation impairs regulatory T cell function and causes autoimmunity. Nat Genet. 2007; 39:329–337.
   PubMed Web of Science ®Google Scholar
• Lyons PA, Armitage N, Argentina F, Denny P, Hill NJ, Lord CJ, Wilusz MB, Peterson LB, Wicker LS, Todd JA. Congenic mapping of the type 1 diabetes locus, Idd3, to a 780-kb region of mouse chromosome 3: Identification of a candidate segment of ancestral DNA by haplotype mapping. Genome Res. 2000; 10:446–453.
   PubMedGoogle Scholar
• Fontenot JD, Rasmussen JP, Gavin MA, Rudensky AY. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat Immunol. 2005; 6:114–151.
   Google Scholar
• Hawiger D, Inaba K, Dorsett Y, Guo M, Mahnke K, Rivera M, Ravetch JV, Steinman RM, Nussenzweig MC. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J Exp Med. 2001; 194:769–779.
   PubMed Web of Science ®Google Scholar
• Yamazaki S, Iyoda T, Tarbell K, Olson K, Velinzon K, Inaba K, Steinman RM. Direct expansion of functional CD25+ CD4+ regulatory T cells by antigen-processing dendritic cells. J Exp Med. 2003; 198:235–247.
   PubMed Web of Science ®Google Scholar
• Tarbell KV, Petit L, Zuo X, Toy P, Luo X, Mqadmi A, Yang H, Suthanthiran M, Mojsov S, Steinman RM. Dendritic cell-expanded, islet-specific CD4+ CD25+ CD62L+ regulatory T cells restore normoglycemia in diabetic NOD mice. J Exp Med. 2007; 204:191–201.
   PubMed Web of Science ®Google Scholar
• Tarbell KV, Yamazaki S, Olson K, Toy P, Steinman RM. CD25+ CD4+ T cells, expanded with dendritic cells presenting a single autoantigenic peptide, suppress autoimmune diabetes. J Exp Med. 2004; 199:1467–1477.
   PubMed Web of Science ®Google Scholar
• Prasad SJ, Goodnow CC. Cell-intrinsic effects of non-MHC NOD genes on dendritic cell generation in vivo. Int Immunol. 2002; 14:677–684.
   Google Scholar
• Jansen A, van Hagen M, Drexhage HA. Defective maturation and function of antigen-presenting cells in type 1 diabetes. Lancet. 1995; 345:491–492.
   PubMed Web of Science ®Google Scholar
• Boudaly S, Morin J, Berthier R, Marche P, Boitard C. Altered dendritic cells (DC) might be responsible for regulatory T cell imbalance and autoimmunity in nonobese diabetic (NOD) mice. Eur Cytokine Netw. 2002; 13:29–37.
   PubMed Web of Science ®Google Scholar
• Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG, Rudensky AY. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity. 2005; 22:329–341.
   PubMed Web of Science ®Google Scholar
• Inaba K, Swiggard WJ, Steinman RM, Romani N, Schuler G. Isolation of dendritic cells. Curr Protoc Immunol. 2001 Chapter 3, Unit 3.7.
   Google Scholar
• Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, Romani N, Schuler G. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods. 1999; 223:77–92.
   PubMed Web of Science ®Google Scholar
• Thornton AM, Shevach EM. CD4+ CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med. 1998; 188:287–296.
   PubMed Web of Science ®Google Scholar
• Sgouroudis E, Albanese A, Piccirillo CA. Impact of protective IL-2 allelic variants on CD4+ Foxp3+ Regulatory T cell function in situ and resistance to autoimmune diabetes in NOD mice. J Immunol. 2008; 181:6283–6292.
   PubMed Web of Science ®Google Scholar
• Granucci F, Vizzardelli C, Pavelka N, Feau S, Persico M, Virzi E, Rescigno M, Moro G, Ricciardi-Castagnoli P. Inducible IL-2 production by dendritic cells revealed by global gene expression analysis. Nat Immunol. 2001; 2:882–888.
   PubMed Web of Science ®Google Scholar
• Hamilton-Williams E, Martinez EX, Clark J, Howlett S, Hunter KM, Rainbow DB, Wen L, Shlomchik MJ, Katz JD, Beilhack GF, Wicker LS, Sherman LA. Expression of diabetes-associated genes by dendritic cells and CD4 T cells drives the loss of tolerance in nonobese diabetic mice. J Immunol. 2009; 183:1533–1541.
   Google Scholar
• Tang Q, Bluestone JA. Regulatory T-cell physiology and application to treat autoimmunity. Immunol Rev. 2006; 212:217–237.
   PubMed Web of Science ®Google Scholar
• Jaramillo A, Gill BM, Delovitch TL. Insulin dependent diabetes mellitus in the non-obese diabetic mouse: A disease mediated by T cell anergy?. Life Sci. 1994; 55:1163–1177.
   Google Scholar
• Tang Q, Adams JY, Tooley AJ, Bi M, Fife BT, Serra P, Santamaria P, Locksley RM, Krummel MF, Bluestone JA. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat Immunol. 2006; 7:83–92.
   PubMed Web of Science ®Google Scholar
• Poligone B, Weaver DJJr, Sen P, Baldwin ASJr, Tisch R. Elevated NF-kappaB activation in nonobese diabetic mouse dendritic cells results in enhanced APC function. J Immunol. 2002; 168:188–196.
   PubMedGoogle Scholar
• Grohmann U, Fallarino F, Puccetti P. Tolerance, DCs and tryptophan: Much ado about IDO. Trends Immunol. 2003; 24:242–248.
   PubMed Web of Science ®Google Scholar
• Anderson AC, Chandwaskar R, Lee DH, Kuchroo VK. Cutting edge: The Idd3 genetic interval determines regulatory T cell function through CD11b+ CD11c − APC. J Immunol. 2008; 181:7449–7452.
   Google Scholar