Immune mechanisms in type 1 diabetes

Trends in Immunology

Volumn 34, Issue 12, 2013, Pages 583-591

  Wållberg, Maja ^a   Cooke, Anne ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Autoimmunity; Environment; Genetics; Type 1 diabetes

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 8; NON RECEPTOR PROTEIN TYROSINE PHOSPHATASE 22; RANTES;

B LYMPHOCYTE; CELL DESTRUCTION; DENDRITIC CELL; ENVIRONMENTAL FACTOR; GENE EXPRESSION; GENETIC SUSCEPTIBILITY; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; INSULIN DEPENDENT DIABETES MELLITUS; MACROPHAGE; NATURAL KILLER CELL; PANCREAS ISLET BETA CELL; PATHOGENESIS; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE; VIRUS INFECTION;

AUTOIMMUNITY; ENVIRONMENT; GENETICS; TYPE 1 DIABETES;

ANIMALS; AUTOIMMUNE DISEASES; DIABETES MELLITUS, TYPE 1; HUMANS; IMMUNE SYSTEM; INSULIN-SECRETING CELLS;

EID: 84888439466     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2013.08.005     Document Type: Review

References (108)

1. Banting F.G., et al. Pancreatic extracts in the treatment of diabetes mellitus. Can. Med. Assoc. J. 1922, 12:141-146.
2. Lassmann H. Recent neuropathological findings in MS - implications for diagnosis and therapy. J. Neurol. 2004, 251(Suppl. 4):IV2-IV5.
3. Steck A.K., Rewers M.J. Genetics of type 1 diabetes. Clin. Chem. 2011, 57:176-185.
4. Barrett J.C., et al. Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes. Nat. Genet. 2009, 41:703-707.
5. Imkampe A.K., Gulliford M.C. Trends in type 1 diabetes incidence in the UK in 0- to 14-year-olds and in 15- to 34-year-olds, 1991-2008. Diabet. Med. 2011, 28:811-814.
6. von Herrath M. Can we learn from viruses how to prevent type 1 diabetes?: the role of viral infections in the pathogenesis of type 1 diabetes and the development of novel combination therapies. Diabetes 2009, 58:2-11.
7. Richardson S.J., et al. The prevalence of enteroviral capsid protein vp1 immunostaining in pancreatic islets in human type 1 diabetes. Diabetologia 2009, 52:1143-1151.
8. Richardson S.J., et al. Expression of the enteroviral capsid protein VP1 in the islet cells of patients with type 1 diabetes is associated with induction of protein kinase R and downregulation of Mcl-1. Diabetologia 2013, 56:185-193.
9. Roivainen M., Klingel K. Virus infections and type 1 diabetes risk. Curr. Diab. Rep. 2010, 10:350-356.
10. Zaccone P., Cooke A. Infectious triggers protect from autoimmunity. Semin. Immunol. 2011, 23:122-129.
11. Weinstock J.V., Elliott D.E. Translatability of helminth therapy in inflammatory bowel diseases. Int. J. Parasitol. 2013, 43:245-251.
12. Fleming J.O., et al. Probiotic helminth administration in relapsing-remitting multiple sclerosis: a phase 1 study. Mult. Scler. 2011, 17:743-754.
13. Kriegel M.A., et al. Naturally transmitted segmented filamentous bacteria segregate with diabetes protection in nonobese diabetic mice. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:11548-11553.
14. Wen L., et al. Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature 2008, 455:1109-1113.
15. Hansen C.H., et al. Early life treatment with vancomycin propagates Akkermansia muciniphila and reduces diabetes incidence in the NOD mouse. Diabetologia 2012, 55:2285-2294.
16. Markle J.G., et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 2013, 339:1084-1088.
17. Murri M., et al. Gut microbiota in children with type 1 diabetes differs from that in healthy children: a case-control study. BMC Med. 2013, 11:46.
18. Giongo A., et al. Toward defining the autoimmune microbiome for type 1 diabetes. ISME J. 2012, 5:82-91.
19. Cooper J.D., et al. Inherited variation in vitamin D genes is associated with predisposition to autoimmune disease type 1 diabetes. Diabetes 2011, 60:1624-1631.
20. Zipitis C.S., Akobeng A.K. Vitamin D supplementation in early childhood and risk of type 1 diabetes: a systematic review and meta-analysis. Arch. Dis. Child 2008, 93:512-517.
21. Vehik K., et al. Methods, quality control and specimen management in an international multi-center investigation of type 1 diabetes: TEDDY. Diabetes Metab. Res. Rev. 2013, 10.1002/dmrr.2427.
22. Campbell-Thompson M., et al. Network for pancreatic organ donors with diabetes (nPOD): developing a tissue biobank for type 1 diabetes. Diabetes Metab. Res. Rev. 2012, 28:608-617.
23. Ridgway W.M., et al. Gene-gene interactions in the NOD mouse model of type 1 diabetes. Adv. Immunol. 2008, 100:151-175.
24. Eizirik D.L., et al. The human pancreatic islet transcriptome: expression of candidate genes for type 1 diabetes and the impact of pro-inflammatory cytokines. PLoS Genet. 2012, 8:e1002552.
25. Arif S., et al. Peripheral and islet interleukin-17 pathway activation characterizes human autoimmune diabetes and promotes cytokine-mediated beta-cell death. Diabetes 2011, 60:2112-2119.
26. Singh B., et al. Immunomodulation and regeneration of islet beta cells by cytokines in autoimmune type 1 diabetes. J. Interferon Cytokine Res. 2011, 31:711-719.
27. Bachmann M., et al. IFNalpha converts IL-22 into a cytokine efficiently activating STAT1 and its downstream targets. Biochem. Pharmacol. 2013, 85:396-403.
28. Li Q., McDevitt H.O. The role of interferon alpha in initiation of type I diabetes in the NOD mouse. Clin. Immunol. 2011, 140:3-7.
29. Kassem S.A., et al. Beta-cell proliferation and apoptosis in the developing normal human pancreas and in hyperinsulinism of infancy. Diabetes 2000, 49:1325-1333.
30. 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. 2003, 198:1527-1537.
31. Calderon B., Unanue E.R. Antigen presentation events in autoimmune diabetes. Curr. Opin. Immunol. 2012, 24:119-128.
32. Marrack P., Kappler J.W. Do MHCII-presented neoantigens drive type 1 diabetes and other autoimmune diseases?. Cold Spring Harb. Perspect. Med. 2012, 2:a007765.
33. Willcox A., et al. Analysis of islet inflammation in human type 1 diabetes. Clin. Exp. Immunol. 2009, 155:173-181.
34. Skowera A., et al. CTLs are targeted to kill beta cells in patients with type 1 diabetes through recognition of a glucose-regulated preproinsulin epitope. J. Clin. Invest. 2008, 118:3390-3402.
35. Knight R.R., et al. Human beta-cell killing by autoreactive preproinsulin-specific CD8 T cells is predominantly granule-mediated with the potency dependent upon T-cell receptor avidity. Diabetes 2013, 62:205-213.
36. Wong F.S., et al. Identification of an MHC class I-restricted autoantigen in type 1 diabetes by screening an organ-specific cDNA library. Nat. Med. 1999, 5:1026-1031.
37. Katz J., et al. Major histocompatibility complex class I molecules are required for the development of insulitis in non-obese diabetic mice. Eur. J. Immunol. 1993, 23:3358-3360.
38. Hamilton-Williams E.E., et al. Beta cell MHC class I is a late requirement for diabetes. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:6688-6693.
39. Kagi D., et al. Reduced incidence and delayed onset of diabetes in perforin-deficient nonobese diabetic mice. J. Exp. Med. 1997, 186:989-997.
40. Phillips J.M., et al. Type 1 diabetes development requires both CD4+ and CD8+ T cells and can be reversed by non-depleting antibodies targeting both T cell populations. Rev. Diabet. Stud. 2009, 6:97-103.
41. Joffre O.P., et al. Cross-presentation by dendritic cells. Nat. Rev. Immunol. 2012, 12:557-569.
42. Smith C.M., et al. Cognate CD4(+) T cell licensing of dendritic cells in CD8(+) T cell immunity. Nat. Immunol. 2004, 5:1143-1148.
43. Makhlouf L., et al. Depleting anti-CD4 monoclonal antibody cures new-onset diabetes, prevents recurrent autoimmune diabetes, and delays allograft rejection in nonobese diabetic mice. Transplantation 2004, 77:990-997.
44. Calderon B., et al. In CD4+ T-cell-induced diabetes, macrophages are the final effector cells that mediate islet beta-cell killing: studies from an acute model. Am. J. Pathol. 2006, 169:2137-2147.
45. Arif S., et al. Autoreactive T cell responses show proinflammatory polarization in diabetes but a regulatory phenotype in health. J. Clin. Invest. 2004, 113:451-463.
46. 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. 2009, 119:565-572.
47. Serreze D.V., et al. B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new "speed congenic" stock of NOD.Ig mu null mice. J. Exp. Med. 1996, 184:2049-2053.
48. Noorchashm H., et al. B-cells are required for the initiation of insulitis and sialitis in nonobese diabetic mice. Diabetes 1997, 46:941-946.
49. 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. 1998, 161:3912-3918.
50. Wong F.S., et al. Investigation of the role of B-cells in type 1 diabetes in the NOD mouse. Diabetes 2004, 53:2581-2587.
51. Silveira P.A., et al. The preferential ability of B lymphocytes to act as diabetogenic APC in NOD mice depends on expression of self-antigen-specific immunoglobulin receptors. Eur. J. Immunol. 2002, 32:3657-3666.
52. Hulbert C., et al. B cell specificity contributes to the outcome of diabetes in nonobese diabetic mice. J. Immunol. 2001, 167:5535-5538.
53. Hu C.Y., et al. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J. Clin. Invest. 2007, 117:3857-3867.
54. Saxena V., et al. The countervailing actions of myeloid and plasmacytoid dendritic cells control autoimmune diabetes in the nonobese diabetic mouse. J. Immunol. 2007, 179:5041-5053.
55. Lund T., et al. Prevention of insulin-dependent diabetes mellitus in non-obese diabetic mice by transgenes encoding modified I-A beta-chain or normal I-E alpha-chain. Nature 1990, 345:727-729.
56. Poligone B., et al. Elevated NF-kappaB activation in nonobese diabetic mouse dendritic cells results in enhanced APC function. J. Immunol. 2002, 168:188-196.
57. Liu J., Beller D.I. Distinct pathways for NF-kappa B regulation are associated with aberrant macrophage IL-12 production in lupus- and diabetes-prone mouse strains. J. Immunol. 2003, 170:4489-4496.
58. Katz J.D., et al. Cutting edge: merocytic dendritic cells break T cell tolerance to beta cell antigens in nonobese diabetic mouse diabetes. J. Immunol. 2010, 185:1999-2003.
59. Hutchings P., et al. Transfer of diabetes in mice prevented by blockade of adhesion-promoting receptor on macrophages. Nature 1990, 348:639-642.
60. Uno S., et al. Macrophages and dendritic cells infiltrating islets with or without beta cells produce tumour necrosis factor-alpha in patients with recent-onset type 1 diabetes. Diabetologia 2007, 50:596-601.
61. O'Brien B.A., et al. A deficiency in the in vivo clearance of apoptotic cells is a feature of the NOD mouse. J. Autoimmun. 2006, 26:104-115.
62. 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. U.S.A. 2007, 104:5115-5120.
63. Flodstrom M., et al. Target cell defense prevents the development of diabetes after viral infection. Nat. Immunol. 2002, 3:373-382.
64. Sitrin J., et al. Regulatory T cells control NK cells in an insulitic lesion by depriving them of IL-2. J. Exp. Med. 2013, 210:1153-1165.
65. Beilke J.N., et al. NK cells are not required for spontaneous autoimmune diabetes in NOD mice. PLoS ONE 2012, 7:e36011.
66. Bluestone J.A. Mechanisms of tolerance. Immunol. Rev. 2011, 241:5-19.
67. Dilts S.M., Lafferty K.J. Autoimmune diabetes: the involvement of benign and malignant autoimmunity. J. Autoimmun. 1999, 12:229-232.
68. Sakaguchi S., et al. The plasticity and stability of regulatory T cells. Nat. Rev. Immunol. 2013, 13:461-467.
69. Katz J.D., et al. Following a diabetogenic T cell from genesis through pathogenesis. Cell 1993, 74:1089-1100.
70. Feuerer M., et al. How punctual ablation of regulatory T cells unleashes an autoimmune lesion within the pancreatic islets. Immunity 2009, 31:654-664.
71. Shull M.M., et al. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 1992, 359:693-699.
72. Lindley S., et al. Defective suppressor function in CD4(+)CD25(+) T-cells from patients with type 1 diabetes. Diabetes 2005, 54:92-99.
73. 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. U.S.A. 2008, 105:19857-19862.
74. Attridge K., et al. IL-21 inhibits T cell IL-2 production and impairs Treg homeostasis. Blood 2013, 119:4656-4664.
75. Lehuen A., et al. Immune cell crosstalk in type 1 diabetes. Nat. Rev. Immunol. 2010, 10:501-513.
76. Lee P.T., et al. Testing the NKT cell hypothesis of human IDDM pathogenesis. J. Clin. Invest. 2002, 110:793-800.
77. Unger W.W., et al. Induction of Treg by monocyte-derived DC modulated by vitamin D3 or dexamethasone: differential role for PD-L1. Eur. J. Immunol. 2009, 39:3147-3159.
78. Steinbrink K., et al. Induction of tolerance by IL-10-treated dendritic cells. J. Immunol. 1997, 159:4772-4780.
79. Turnquist H.R., et al. Rapamycin-conditioned dendritic cells are poor stimulators of allogeneic CD4+ T cells, but enrich for antigen-specific Foxp3+ T regulatory cells and promote organ transplant tolerance. J. Immunol. 2007, 178:7018-7031.
80. Hackstein H., Thomson A.W. Dendritic cells: emerging pharmacological targets of immunosuppressive drugs. Nat. Rev. Immunol. 2004, 4:24-34.
81. Li M., et al. Tolerogenic dendritic cells transferring hyporesponsiveness and synergizing T regulatory cells in transplant tolerance. Int. Immunol. 2008, 20:285-293.
82. Fallarino F., et al. Indoleamine 2,3-dioxygenase: from catalyst to signaling function. Eur. J. Immunol. 2012, 42:1932-1937.
83. Thomas, T.D.C.Z., P; Wong, F.S.; Green, E.A. and Wallberg, M. (2013) Islet-specific TGF beta expression promotes islet graft survival through induction of tolerogenic DC. In manuscript under second review.
84. Parsa R., et al. Adoptive transfer of immunomodulatory M2 macrophages prevents type 1 diabetes in NOD mice. Diabetes 2012, 61:2881-2892.
85. Kleijwegt F.S., et al. Tolerogenic dendritic cells impede priming of naive CD8(+) T cells and deplete memory CD8(+) T cells. Eur. J. Immunol. 2012, 43:85-92.
86. Thomas T.D.C., et al. Protection of islet grafts through TGF beta induced tolerogenic DC. Diabetes 2013, 62:3132-3142.
87. Adorini L. Tolerogenic dendritic cells induced by vitamin D receptor ligands enhance regulatory T cells inhibiting autoimmune diabetes. Ann. N. Y. Acad. Sci. 2003, 987:258-261.
88. Herold K.C., et al. Teplizumab treatment may improve C-peptide responses in participants with type 1 diabetes after the new-onset period: a randomised controlled trial. Diabetologia 2013, 56:391-400.
89. Herold K.C., et al. Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus. N. Engl. J. Med. 2002, 346:1692-1698.
90. Pescovitz M.D., et al. Rituximab, B-lymphocyte depletion, and preservation of beta-cell function. N. Engl. J. Med. 2009, 361:2143-2152.
91. Gu W., et al. Diabetic ketoacidosis at diagnosis influences complete remission after treatment with hematopoietic stem cell transplantation in adolescents with type 1 diabetes. Diabetes Care 2012, 35:1413-1419.
92. Keymeulen B., et al. Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes. N. Engl. J. Med. 2005, 352:2598-2608.
93. Mastrandrea L., et al. Etanercept treatment in children with new-onset type 1 diabetes: pilot randomized, placebo-controlled, double-blind study. Diabetes Care 2009, 32:1244-1249.
94. Sumpter K.M., et al. Preliminary studies related to anti-interleukin-1beta therapy in children with newly diagnosed type 1 diabetes. Pediatr. Diabetes 2011, 12:656-667.
95. Moran A., et al. Interleukin-1 antagonism in type 1 diabetes of recent onset: two multicentre, randomised, double-blind, placebo-controlled trials. Lancet 2013, 381:1905-1915.
96. Ludvigsson J., et al. GAD treatment and insulin secretion in recent-onset type 1 diabetes. N. Engl. J. Med. 2008, 359:1909-1920.
97. Ludvigsson J., et al. GAD65 antigen therapy in recently diagnosed type 1 diabetes mellitus. N. Engl. J. Med. 2012, 366:433-442.
98. 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 2005, 28:1068-1076.
99. Buzzetti R., et al. C-peptide response and HLA genotypes in subjects with recent-onset type 1 diabetes after immunotherapy with DiaPep277: an exploratory study. Diabetes 2011, 60:3067-3072.
100. Long S.A., et al. Rapamycin/IL-2 combination therapy in patients with type 1 diabetes augments Tregs yet transiently impairs beta-cell function. Diabetes 2012, 61:2340-2348.
101. von Herrath M., et al. Progress in immune-based therapies for type 1 diabetes. Clin. Exp. Immunol. 2013, 172:186-202.
102. Yi P., et al. Betatrophin: a hormone that controls pancreatic beta cell proliferation. Cell 2013, 153:747-758.
103. Cechin S.R., et al. Anti-inflammatory properties of exenatide in human pancreatic islets. Cell Transplant. 2012, 21:633-648.
104. Sysi-Aho M., et al. Metabolic regulation in progression to autoimmune diabetes. PLoS Comput. Biol. 2011, 7:e1002257.
105. Oresic M., et al. Dysregulation of lipid and amino acid metabolism precedes islet autoimmunity in children who later progress to type 1 diabetes. J. Exp. Med. 2008, 205:2975-2984.
106. Sherry N., et al. Teplizumab for treatment of type 1 diabetes (Protege study): 1-year results from a randomised, placebo-controlled trial. Lancet 2011, 378:487-497.
107. Daifotis A.G., et al. Anti-CD3 clinical trials in type 1 diabetes mellitus. Clin. Immunol. 2013, 10.1016/j.clim.2013.05.001.
108. Saudek F., et al. Polyclonal anti-T-cell therapy for type 1 diabetes mellitus of recent onset. Rev. Diabet. Stud. 2004, 1:80-88.