Genetics, pathogenesis and clinical interventions in type 1 diabetes - Nature
- ️Eisenbarth, George
- ️Thu Apr 01 2010
Anderson, M. S. & Bluestone, J. A. The NOD mouse: a model of immune dysregulation. Annu. Rev. Immunol. 23, 447–485 (2005)
Vauzelle-Kervroedan, F. et al. Analysis of mortality in French diabetic patients from death certificates: a comparative study. Diabete Metab. 25, 404–411 (1999)
Maahs, D. M. & Rewers, M. Editorial: mortality and renal disease in type 1 diabetes mellitus—progress made, more to be done. J. Clin. Endocrinol. Metab. 91, 3757–3759 (2006)
Steffes, M. W. et al. (EDIC Research Group). Sustained effect of intensive treatment of type 1 diabetes mellitus on development and progression of diabetic nephropathy: the Epidemiology of Diabetes Interventions and Complications (EDIC) study. J. Am. Med. Assoc. 290, 2159–2167 (2003)
Harjutsalo, V., Sjoberg, L. & Tuomilehto, J. Time trends in the incidence of type 1 diabetes in Finnish children: a cohort study. Lancet 371, 1777–1782 (2008)
Lorenzen, T., Pociot, F., Hougaard, P. & Nerup, J. Long-term risk of IDDM in first-degree relatives of patients with IDDM. Diabetology 37, 321–327 (1994)
Mordes, J. P. et al. The BB/Wor rat and the balance hypothesis of autoimmunity. Diabetes Metab. Rev. 12, 103–109 (1996)
Makino, S. et al. Breeding of a non-obese, diabetic strain of mice. Exp. Anim. 29, 1–13 (1980)
DiLorenzo, T. P. & Serreze, D. V. The good turned ugly: immunopathogenic basis for diabetogenic CD8+ T cells in NOD mice. Immunol. Rev. 204, 250–263 (2005)
Burton, A. R. et al. On the pathogenicity of autoantigen-specific T-cell receptors. Diabetes 57, 1321–1330 (2008)
Han, B. et al. Developmental control of CD8 T cell-avidity maturation in autoimmune diabetes. J. Clin. Invest. 115, 1879–1887 (2005)
Serreze, D. V. et al. B lymphocytes are critical antigen-presenting cells for the initiation of T cell-mediated autoimmune diabetes in nonobese diabetic mice. J. Immunol. 161, 3912–3918 (1998)
Greeley, S. A. et al. Elimination of maternally transmitted autoantibodies prevents diabetes in nonobese diabetic mice. Nature Med. 8, 399–402 (2002)
Hu, C. Y. et al. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J. Clin. Invest. 117, 3857–3867 (2007)
Zipris, D. et al. TLR9-signaling pathways are involved in Kilham rat virus-induced autoimmune diabetes in the biobreeding diabetes-resistant rat. J. Immunol. 178, 693–701 (2007)
Devendra, D. et al. Interferon-α as a mediator of polyinosinic:polycytidylic acid-induced type 1 diabetes. Diabetes 54, 2549–2556 (2005)
Concannon, P., Rich, S. S. & Nepom, G. T. Genetics of type 1A diabetes. N. Engl. J. Med. 360, 1646–1654 (2009)
Wicker, L. S. et al. Type 1 diabetes genes and pathways shared by humans and NOD mice. J. Autoimmun. 25 (Suppl.). 29–33 (2005)
Turley, S. et al. Physiological beta cell death triggers priming of self-reactive T cells by dendritic cells in a type-1 diabetes model. J. Exp. Med. 198, 1527–1537 (2003)
Lieberman, S. M. & DiLorenzo, T. P. A comprehensive guide to antibody and T-cell responses in type 1 diabetes. Tissue Antigens 62, 359–377 (2003)
Medarova, Z. et al. In vivo imaging of a diabetogenic CD8+ T cell response during type 1 diabetes progression. Magn. Reson. Med. 59, 712–720 (2008)
Lennon, G. P. et al. T cell islet accumulation in type 1 diabetes is a tightly regulated, cell-autonomous event. Immunity 31, 643–653 (2009)
Vafiadis, P. et al. Insulin expression in human thymus is modulated by INS VNTR alleles at the IDDM2 locus. Nature Genet. 15, 289–292 (1997)
Pugliese, A. et al. The insulin gene is transcribed in the human thymus and transcription levels correlate with allelic variation at the INS VNTR-IDDM2 susceptibility locus for type I diabetes. Nature Genet. 15, 293–297 (1997)
Gardner, J. M., Fletcher, A. L., Anderson, M. S. & Turley, S. J. AIRE in the thymus and beyond. Curr. Opin. Immunol. 21, 582–589 (2009)
Kobayashi, M. et al. Conserved T cell receptor alpha-chain induces insulin autoantibodies. Proc. Natl Acad. Sci. USA 105, 10090–10094 (2008)
Erlich, H. et al. HLA DR-DQ haplotypes and genotypes and type 1 diabetes risk: analysis of the Type 1 Diabetes Genetics Consortium families. Diabetes 57, 1084–1092 (2008)
Dotta, F. et al. Coxsackie B4 virus infection of beta cells and natural killer cell insulitis in recent-onset type 1 diabetic patients. Proc. Natl Acad. Sci. USA 104, 5115–5120 (2007)
Gianani, R. et al. Dimorphic histopathology of long-standing childhood-onset diabetes. Diabetologia 53 (4). 690–698 (2010)
Itoh, N. et al. Mononuclear cell infiltration and its relation to the expression of major histocompatibility complex antigens and adhesion molecules in pancreas biopsy specimens from newly diagnosed insulin-dependent diabetes mellitus patients. J. Clin. Invest. 92, 2313–2322 (1993)
Willcox, A. et al. Analysis of islet inflammation in human type 1 diabetes. Clin. Exp. Immunol. 155, 173–181 (2009)
Esensten, J. H., Lee, M. R., Glimcher, L. H. & Bluestone, J. A. T-bet-deficient NOD mice are protected from diabetes due to defects in both T cell and innate immune system function. J. Immunol. 183, 75–82 (2009)
Bending, D. et al. Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J. Clin. Invest. 119 (3), 565–572 (2009)
Ogasawara, K. et al. Impairment of NK cell function by NKG2D modulation in NOD mice. Immunity 18, 41–51 (2003)
Feuerer, M. et al. How punctual ablation of regulatory T cells unleashes an autoimmune lesion within the pancreatic islets. Immunity 31, 654–664 (2009)
Wong, F. S. et al. Investigation of the role of B-cells in type 1 diabetes in the NOD mouse. Diabetes 53, 2581–2587 (2004)
Xiu, Y. et al. B lymphocyte depletion by CD20 monoclonal antibody prevents diabetes in nonobese diabetic mice despite isotype-specific differences in Fc gamma R effector functions. J. Immunol. 180, 2863–2875 (2008)
Boni-Schnetzler, M. et al. Increased interleukin (IL)-1beta messenger ribonucleic acid expression in beta -cells of individuals with type 2 diabetes and regulation of IL-1beta in human islets by glucose and autostimulation. J. Clin. Endocrinol. Metab. 93, 4065–4074 (2008)
Koulmanda, M. et al. Modification of adverse inflammation is required to cure new-onset type 1 diabetic hosts. Proc. Natl Acad. Sci. USA 104, 13074–13079 (2007)
Feuerer, M., Hill, J. A., Mathis, D. & Benoist, C. Foxp3+ regulatory T cells: differentiation, specification, subphenotypes. Nature Immunol. 10, 689–695 (2009)
Bacchetta, R. et al. Defective regulatory and effector T cell functions in patients with FOXP3 mutations. J. Clin. Invest. 116, 1713–1722 (2006)
Tang, Q. & Bluestone, J. A. The Foxp3+ regulatory T cell: a jack of all trades, master of regulation. Nature Immunol. 9, 339–344 (2008)
Winer, S. et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nature Med. 15, 921–929 (2009)
Feuerer, M. et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nature Med. 15, 930–939 (2009)
Yan, Z., Garg, S. K., Kipnis, J. & Banerjee, R. Extracellular redox modulation by regulatory T cells. Nature Chem. Biol. 5, 721–723 (2009)
Tang, Q. et al. Central role of a defective IL-2 production in triggering islet autoimmune destruction. Immunity 28, 687–697 (2008)
Zhou, X. et al. Foxp3 instability leads to the generation of pathogenic memory T cells in vivo . Nat. Immun. 10, 1000–1007 (2009)
Schneider, A. et al. The effector T cells of diabetic subjects are resistant to regulation via CD4+ FOXP3+ regulatory T cells. J. Immunol. 181, 7350–7355 (2008)
D'Alise, A. M. et al. The defect in T-cell regulation in NOD mice is an effect on the T-cell effectors. Proc. Natl Acad. Sci. USA 105, 19857–19862 (2008)
Qin, H. Y. & Singh, B. BCG vaccination prevents insulin-dependent diabetes mellitus (IDDM) in NOD mice after disease acceleration with cyclophosphamide. J. Autoimmun. 10, 271–278 (1997)
Wen, L. et al. Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 455, 1109–1113 (2008)
Weintrob, N. et al. Type 1 diabetes environmental factors and correspondence analysis of HLA class II genes in the Yemenite Jewish community in Israel. Diabetes Care 24, 650–653 (2001)
Virtanen, S. M. et al. Age at introduction of new foods and advanced beta cell autoimmunity in young children with HLA-conferred susceptibility to type 1 diabetes. Diabetologia 49, 1512–1521 (2006)
Akerblom, H. K. et al. Dietary manipulation of beta cell autoimmunity in infants at increased risk of type 1 diabetes: a pilot study. Diabetologia 48, 829–837 (2005)
Norris, J. M. et al. Omega-3 polyunsaturated fatty acid intake and islet autoimmunity in children at increased risk for type 1 diabetes. J. Am. Med. Assoc. 298, 1420–1428 (2007)
Jun, H. S. & Yoon, J. W. A new look at viruses in type 1 diabetes. ILAR J. 45, 349–374 (2004)
Richardson, S. J. et al. The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes. Diabetologia 52, 1143–1151 (2009)
Nejentsev, S. et al. Rare variants of IFIH1, a gene implicated in antiviral responses, protect against type 1 diabetes. Science 324, 387–389 (2009)
Bougneres, P. F. et al. Factors associated with early remission of type I diabetes in children treated with cyclosporine. N. Engl. J. Med. 318, 663–670 (1988)
Stiller, C. R. et al. Effects of cyclosporine immunosuppression in insulin-dependent diabetes mellitus of recent onset. Science 223, 1362–1367 (1984)
Feutren, G. et al. Cyclosporin increases the rate and length of remissions in insulin dependent diabetes of recent onset. Results of a multicentre double-blind trial. Lancet 2, 119–124 (1986)
Eisenbarth, G. S. et al. Anti-thymocyte globulin and prednisone immunotherapy of recent onset type I diabetes mellitus. Diabetes Res. 2, 271–276 (1985)
Allen, H. F. et al. Effect of BCG vaccination on new-onset insulin-dependent diabetes mellitus: a randomized clinical study. Diabetes Care 22, 1703–1707 (1998)
Herold, K. C. et al. Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus. N. Engl. J. Med. 346, 1692–1698 (2002)
Keymeulen, B. Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes. N. Engl. J. Med. 352, 2598–2608 (2005)
Herold, K. C. et al. Treatment of patients with new onset type 1 diabetes with a single course of anti-CD3 mAb teplizumab preserves insulin production for up to 5 years. Clin. Immunol. 132, 166–173 (2009)
Chatenoud, L. & Bluestone, J. A. CD3-specific antibodies: a portal to the treatment of autoimmunity. Nature Rev. Immunol. 7, 622–632 (2007)
Bisikirska, B. et al. TCR stimulation with modified anti-CD3 mAb expands CD8 T cell population and induces CD8 CD25 Tregs. J. Clin. Invest. 115, 2904–2913 (2005)
Hu, C. Y. et al. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J. Clin. Invest. 117, 3857–3867 (2007)
Bouaziz, J. D., Yanaba, K. & Tedder, T. F. Regulatory B cells as inhibitors of immune responses and inflammation. Immunol. Rev. 224, 201–214 (2008)
Pescovitz, M. D. et al. Rituxan, B-lymphocyte depletion, and preservation of beta-cell function. N. Engl. J. Med. 361, 2143–2152 (2009)
Wise, M. et al. CD4 T cells can reject major histocompatibility complex class I-incompatible skin grafts. Eur. J. Immunol. 29, 156–167 (1999)
Homann, D. et al. Autoreactive CD4+ T cells protect from autoimmune diabetes via bystander suppression using the IL-4/Stat6 pathway. Immunity 11, 463–472 (1999)
Masteller, E. L. et al. Expansion of functional endogenous antigen-specific CD4+CD25+ regulatory T cells from nonobese diabetic mice. J. Immunol. 175, 3053–3059 (2005)
Qin, S. et al. ‘Infectious’ transplantation tolerance. Science 259, 974–977 (1993)
Waldmann, H. & Cobbold, S. How do monoclonal antibodies induce tolerance? A role for infectious tolerance? Annu. Rev. Immunol. 16, 619–644 (1998)
Tang, Q. et al. In vitro expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J. Exp. Med. 199, 1455–1465 (2004)
Skyler, J. S. et al. Effects of oral insulin in relatives of patients with type 1 diabetes: the Diabetes Prevention Trial—Type 1. Diabetes Care 28, 1068–1076 (2005)
Ludvigsson, J. et al. GAD treatment and insulin secretion in recent-onset type 1 diabetes. N. Engl. J. Med. 359, 1909–1920 (2008)
Levings, M. K., Sangregorio, R. & Roncarolo, M. G. Human CD25(+)CD4(+) T regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function. J. Exp. Med. 193, 1295–1302 (2001)
Strom, T. B. & Koulmanda, M. Cytokine related therapies for autoimmune disease. Curr. Opin. Immunol. 20, 676–681 (2008)
Koulmanda, M. et al. Curative and beta cell regenerative effects of α1-antitrypsin treatment in autoimmune diabetic NOD mice. Proc. Natl Acad. Sci. USA 105, 16242–16247 (2008)
Louvet, C. et al. Tyrosine kinase inhibitors reverse type 1 diabetes in nonobese diabetic mice. Proc. Natl Acad. Sci. USA 105, 18895–18900 (2008)
Couri, C. E. & Voltarelli, J. C. Stem cell therapy for type 1 diabetes mellitus: a review of recent clinical trials. Diabetol. Metabol. Syndr. 1, 1–19 (2009)
Bresson, D. et al. Anti-CD3 and nasal proinsulin combination therapy enhances remission from recent-onset autoimmune diabetes by inducing Tregs. J. Clin. Invest. 116, 1371–1381 (2006)
Suarez-Pinzon, W. L. et al. Combination therapy with epidermal growth factor and gastrin increases beta-cell mass and reverses hyperglycemia in diabetic NOD mice. Diabetes 54, 2596–2601 (2005)
Matthews, J. B. et al. Developing combination immunotherapies for type 1 diabetes: recommendations from the ITN-JDRF Type 1 Diabetes Combination Therapy Assessment Group. Clin. Exp. Immunol. 10.1111/j.1365–2249.2010.04153.x (in the press)
Skyler, J. S. et al. Effects of oral insulin in relatives of patients with type 1 diabetes: The Diabetes Prevention Trial--Type 1. Diabetes Care 28, 1068–1075 (2005)
Herold, K. C. et al. A single course of anti-CD3 monoclonal antibody hOKT3γ1(Ala-Ala) results in improvement in C-peptide responses and clinical parameters for at least 2 years after onset of Type 1 diabetes. Diabetes 54, 1763–1769 (2005)
Wong, F. S. et al. Investigation of the role of β-cells in type 1 diabetes in the NOD mouse. Diabetes 53, 2581–2587 (2004)