Adaptive immune regulation in autoimmune diabetes

Autoimmunity Reviews

Volumn 15, Issue 3, 2016, Pages 236-241

  Ferretti, Concetta ^a   La Cava, Antonio ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Regulatory T cell immunotherapy; Type 1 diabetes; Cells

Indexed keywords

ADAPTIVE IMMUNITY; AUTOIMMUNE DISEASE; DISEASE PREDISPOSITION; ENVIRONMENTAL FACTOR; GENETIC SUSCEPTIBILITY; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS DISEASE; PANCREAS ISLET; PATHOGENESIS; PATHOPHYSIOLOGY; REGULATORY T LYMPHOCYTE; REVIEW; ANIMAL; IMMUNOLOGY; INNATE IMMUNITY;

ADAPTIVE IMMUNITY; ANIMALS; DIABETES MELLITUS, TYPE 1; HUMANS; IMMUNITY, INNATE; ISLETS OF LANGERHANS; T-LYMPHOCYTES, REGULATORY;

EID: 84958925577     PISSN: 15689972     EISSN: 18730183     Source Type: Journal    
DOI: 10.1016/j.autrev.2015.11.008     Document Type: Review

References (89)

1. Pociot F., Akolkar B., Concannon P., Erlich H.A., Julier C., Morahan G., et al. Genetics of type 1 diabetes: what's next?. Diabetes 2010, 59:1561-1571.
2. Noble J.A., Valdes A.M., Varney M.D., Carlson J.A., Moonsamy P., Fear A.L., et al. HLA class I and genetic susceptibility to type 1 diabetes: results from the type 1 Diabetes Genetics Consortium. Diabetes 2010, 59:2972-2979.
3. Gianchecchi E., Fierabracci A. Gene/environment interactions in the pathogenesis of autoimmunity: new insights on the role of Toll-like receptors. Autoimmun Rev 2015, 14:971-983.
4. Canivell S., Gomis R. Diagnosis and classification of autoimmune diabetes mellitus. Autoimmun Rev 2014, 13:403-407.
5. Atkinson Mark A., Eisenbarth George S., Michels Aaron W. Type 1 diabetes. Lancet 2014, 383:69-82.
6. Richardson S.J., Morgan N.G., Foulis A.K. Pancreatic pathology in type 1 diabetes mellitus. Endocr Pathol 2014, 25:80-92.
7. Heath W.R., Kurts C., Miller J.F., Carbone F.R. Cross-tolerance: a pathway for inducing tolerance to peripheral tissue antigens. J Exp Med 1998, 187:1549-1553.
8. Bashi T., Bizzaro G., Ben-Ami Shor D., Blank M., Shoenfeld Y. The mechanisms behind Helminth's immunomodulation in autoimmunity. Autoimmun Rev 2015, 14:98-104.
9. Meka R.R., Venkatesha S.H., Dudics S., Acharya B., Moudgil K.D. IL-27-induced modulation of autoimmunity and its therapeutic potential. Autoimmun Rev 2015, 14:1131-1141.
10. Lehuen A., Diana J.Z., Zaccone P., Cooke A. Immune cell crosstalk in type 1 diabetes. Nat Rev Immunol 2010, 10:501-513.
11. Kakleas K., Soldatou A., Karachaliou F., Karavanaki K. Associated autoimmune diseases in children and adolescents with type 1 diabetes mellitus (T1DM). Autoimmun Rev 2015, 14:781-797.
12. Naumov Y.N., Bahjat K.S., Gausling R., Abraham R., Exley M.A., Koezuka Y., et al. Activation of CD1d-restricted T cells protects NOD mice from developing diabetes by regulating dendritic cell subsets. Proc Natl Acad Sci U S A 2001, 98:13838-13843.
13. O'Brien B.A., Huang Y., Geng X., Dutz J.P., Finegood D.T. Phagocytosis of apoptotic cells by macrophages from NOD mice is reduced. Diabetes 2002, 51:2481-2488.
14. Vetere A., Choudhary A., Burns S.M., Wagner B.K. Targeting the pancreatic β-cell to treat diabetes. Nat Rev Drug Discov 2014, 13:278-289.
15. Sarvetnick N., Shizuru J., Liggitt D., Martin L., McIntyre B., Gregory A., et al. Loss of pancreatic islet tolerance induced by β-cell expression of interferon-γ. Nature 1990, 346:844-847.
16. Mathis D., Vence L., Benoist C. β-Cell death during progression to diabetes. Nature 2001, 414:792-798.
17. Zhang Y., O'Brien B., Trudeau J., Tan R., Santamaria P., Dutz J.P. In situ β cell death promotes priming of diabetogenic CD8 T lymphocytes. J Immunol 2002, 168:1466-1472.
18. Wachlin G., Augstein P., Schröder D., Kuttler B., Klöting I., Heinke P., et al. IL-1β, IFN-γ and TNF-α increase vulnerability of pancreatic β cells to autoimmune destruction. J Autoimmun 2003, 20:303-312.
19. Tang Q., Bluestone J.A. Regulatory T-cell physiology and application to treat autoimmunity. Immunol Rev 2006, 212:217-237.
20. Pescovitz M.D., Greenbaum C.J., Krause-Steinrauf H., Becker D.J., Gitelman S.E., Goland R., et al. Rituximab, B-lymphocyte depletion, and preservation of β-cell function. N Engl J Med 2009 Nov 26, 361:2143-2152.
21. Sakaguchi S., Wing K., Onishi Y., Prieto-Martin P., Yamaguchi T. Regulatory T cells: how do they suppress immune responses?. Int Immunol 2009, 21:1105-1111.
22. Shao S., He F., Yang Y., Yuan G., Zhang M., Yu X. Th17 cells in type 1 diabetes. Cell Immunol 2012, 280:16-21.
23. Ferraro A. Expansion of Th17 cells and functional defects in T regulatory cells are key features of the pancreatic lymph nodes in patients with type 1 diabetes. Diabetes 2011, 60:2903-2913.
24. Ryba-Stanisławowska M., Skrzypkowska M., Myśliwska J., Myśliwiec M. The serum IL-6 profile and Treg/Th17 peripheral cell populations in patients with type 1 diabetes. Mediators Inflamm 2013, 2013:205284.
25. Bradshaw E.M., Raddassi K., Elyaman W., Orban T., Gottlieb P.A., Kent S.C., et al. Monocytes from patients with type 1 diabetes spontaneously secrete proinflammatory cytokines inducing Th17 cells. J Immunol 2009, 183:4432-4439.
26. Bettelli E., Oukka M., Kuchroo V.K. T(H)-17 cells in the circle of immunity and autoimmunity. Nat Immunol 2007, 8:345-350.
27. Schneider A., Rieck M., Sanda S., Pihoker C., Greenbaum C., Buckner J.H. The effector T cells of diabetic subjects are resistant to regulation via CD4+ FOXP3+ regulatory T cells. J Immunol 2008, 181:7350-7355.
28. Hori S., Nomura T., Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003, 299:1057-1061.
29. Horwitz D.A., Zheng S.G., Wang J., Gray J.D. Critical role of IL-2 and TGF-β in generation, function and stabilization of Foxp3 + CD4+ Treg. Eur J Immunol 2008, 38:912-915.
30. Li C.R., Baaten B.J., Bradley L.M. Harnessing memory adaptive regulatory T cells to control autoimmunity in type 1 diabetes. J Mol Cell Biol 2012, 4:38-47.
31. Li C.R., Deiro M.F., Godebu E., Bradley L.M. IL-7 uniquely maintains FoxP3+ adaptive Treg cells that reverse diabetes in NOD mice via integrin-β7-dependent localization. J Autoimmun 2011, 37:217-227.
32. Li C.R., Baaten B.J., Bradley L.M. Harnessing memory adaptive regulatory T cells to control autoimmunity in type 1 diabetes. J Mol Cell Biol 2012, 4:38-47.
33. Min W.P., Zhou D., Ichim T.E., Strejan G.H., Xia X., Yang J., et al. Inhibitory feedback loop between tolerogenic dendritic cells and regulatory T cells in transplant tolerance. J Immunol 2003, 170:1304-1312.
34. high T cells in type 1 diabetes may be partially mediated by IL-2 deprivation. PLoS One 2009, 4.
35. Monti P., Scirpoli M., Maffi P., Piemonti L., Secchi A., Bonifacio E., et al. Rapamycin monotherapy in patients with type 1 diabetes modifies CD4 + CD25 + FOXP3+ regulatory T-cells. Diabetes 2008, 57:2341-2347.
36. Tang Q., Adams J.Y., Penaranda C., Melli K., Piaggio E., Sgouroudis E., et al. Central role of defective interleukin-2 production in the triggering of islet autoimmune destruction. Immunity 2008, 28:687-697.
37. Kern T.S. Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. Exp Diabetes Res 2007, 2007:95103.
38. Lee L.F., Logronio K., Tu G.H., Zhai W., Ni I., Mei L., et al. Anti-IL-7 receptor-α reverses established type 1 diabetes in nonobese diabetic mice by modulating effector T-cell function. Proc Natl Acad Sci U S A 2012, 109:12674-12679.
39. Kornete M., Piccirillo C.A. Critical co-stimulatory pathways in the stability of Foxp3+ Treg cell homeostasis in Type I diabetes. Autoimmun Rev 2011, 11:104-111.
40. Penaranda C., Kuswanto W., Hofmann J., Kenefeck R., Narendran P., Walker L.S., et al. IL-7 receptor blockade reverses autoimmune diabetes by promoting inhibition of effector/memory T cells. Proc Natl Acad Sci U S A 2012, 109:12668-12673.
41. Lan Q., Fan H., Quesniaux V., Ryffel B., Liu Z., Zheng S.G. Induced Foxp3+ regulatory T cells: a potential new weapon to treat autoimmune and inflammatory diseases?. J Mol Cell Biol 2012, 4:22-28.
42. Singer B.D., King L.S., D'Alessio F.R. Regulatory T cells as immunotherapy. Front Immunol 2014, 5:46.
43. Gaudreau S., Guindi C., Ménard M., Besin G., Dupuis G., Amrani A. Granulocyte-macrophage colony-stimulating factor prevents diabetes development in NOD mice by inducing tolerogenic dendritic cells that sustain the suppressive function of CD4 + CD25+ regulatory T cells. J Immunol 2007, 179:3638-3647.
44. Kared H., Masson A., Adle-Biassette H., Bach J.F., Chatenoud L., Zavala F. Treatment with granulocyte colony-stimulating factor prevents diabetes in NOD mice by recruiting plasmacytoid dendritic cells and functional CD4 + CD25+ regulatory T-cells. Diabetes 2005, 54:78-84.
45. Bischoff L., Alvarez S., Dai D.L., Soukhatcheva G., Orban P.C., Verchere C.B. Cellular mechanisms of CCL22-mediated attenuation of autoimmune diabetes. J Immunol 2015, 194:3054-3064.
46. Tarbell K.V., Petit L., Zuo X., Toy P., Luo X., Mqadmi A., et al. Dendritic cell-expanded, islet-specific CD4 + CD25 + CD62L+ regulatory T cells restore normoglycemia in diabetic NOD mice. J Exp Med 2007, 204:191-201.
47. Petzold C., Riewaldt J., Koenig T., Schallenberg S., Kretschmer K. Dendritic cell-targeted pancreatic beta-cell antigen leads to conversion of self-reactive CD4+ T cells into regulatory T cells and promotes immunotolerance in NOD mice. Rev Diabet Stud 2010, 7:47-61.
48. Gaudreau S., Guindi C., Ménard M., Besin G., Dupuis G., Amrani A. Granulocyte-macrophage colony-stimulating factor prevents diabetes development in NOD mice by inducing tolerogenic dendritic cells that sustain the suppressive function of CD4 + CD25+ regulatory T cells. J Immunol 2007, 179:3638-3647.
49. Kared H., Masson A., Adle-Biassette H., Bach J.F., Chatenoud L., Zavala F. Treatment with granulocyte colony-stimulating factor prevents diabetes in NOD mice by recruiting plasmacytoid dendritic cells and functional CD4 + CD25+ regulatory T-cells. Diabetes 2005, 54:78-84.
50. Brusko T., Bluestone J. Clinical application of regulatory T cells for treatment of type 1 diabetes and transplantation. Eur J. Immunol. 2008, 38:931-934.
51. Weaver T.A., Charafeddine A.H., Agarwal A., Turner A.P., Russell M., Leopardi F.V., et al. Alefacept promotes co-stimulation blockade based allograft survival in nonhuman primates. Nat Med 2009, 15:746-749.
52. Rigby M.R., Di Meglio L.A., Rendell M.S., Felner E.I., Dostou J.M., Gitelman S.E., et al. Targeting of memory T cells with alefacept in new-onset type 1 diabetes (T1DAL study): 12 month results of a randomised, double-blind, placebo-controlled phase 2 trial. Lancet Diabetes Endocrinol 2013, 1:284-294.
53. Grewal I.S., Grewal K.D., Wong F.S., Wang H., Picarella D.E., Janeway C.A., et al. Expression of transgene encoded TGF-beta in islets prevents autoimmune diabetes in NOD mice by a local mechanism. J Autoimmun 2002, 19:9-22.
54. Gao X., Liu H., Ding G., Wang Z., Fu H., Ni Z., et al. Complement C3 deficiency prevent against the onset of streptozotocin-induced autoimmune diabetes involving expansion of regulatory T cells. Clin Immunol 2011, 140:236-243.
55. Morimoto C., Schlossman S.F. The structure and function of CD26 in the T-cell immune response. Immunol Rev 1998, 161:55-70.
56. Reinhold D., Bank U., Buhling F., Lendeckel U., Faust J., Neubert K., et al. Inhibitors of dipeptidyl peptidase IV induce secretion of transforming growth factor-β 1 in PWM-stimulated PBMC and T cells. Immunology 1997, 91:354-356.
57. Tian L., Gao J., Hao J., Zhang Y., Yi H., O'Brien T.D., et al. Reversal of new-onset diabetes through modulating inflammation and stimulating beta-cell replication in nonobese diabetic mice by a dipeptidyl peptidase IV inhibitor. Endocrinology 2010, 151:3049-3060.
58. Griffin K.J., Thompson P.A., Gottschalk M., Kyllo J.H., Rabinovitch A. Combination therapy with sitagliptin and lansoprazole in patients with recent-onset type 1 diabetes (REPAIR-T1D): 12-month results of a multicentre, randomised, placebo-controlled, phase 2 trial. Lancet Diabetes Endocrinol 2014, 2:710-718.
59. Schambach F., Schupp M., Lazar M.A., Reiner S.L. Activation of retinoic acid receptor-alpha favours regulatory T cell induction at the expense of IL-17-secreting T helper cell differentiation. Eur J Immunol 2007, 37:2396-2399.
60. Van Y.H., Lee W.H., Ortiz S., Lee M.H., Qin H.J., Liu C.P. All-trans retinoic acid inhibits type 1 diabetes by T regulatory (Treg)-dependent suppression of interferon-gamma-producing T-cells without affecting Th17 cells. Diabetes 2009, 58:146-155.
61. Stosić-Grujicić S., Cvjetićanin T., Stojanović I. Retinoids differentially regulate the progression of autoimmune diabetes in three preclinical models in mice. Mol Immunol 2009, 47:79-86.
62. Bresson D., Fousteri G., Manenkova Y., Croft M., von Herrath M. Antigen-specific prevention of type 1 diabetes in NOD mice is ameliorated by OX40 agonist treatment. J Autoimmun 2011, 37:342-351.
63. Zhang J., Gao W., Yang X., Kang J., Zhang Y., Guo Q., et al. Tolerogenic vaccination reduced effector memory CD4 T cells and induced effector memory Treg cells for type I diabetes treatment. PLoS One 2013, 8:e70056.
64. Franchimont D. Overview of the actions of glucocorticoids on the immune response: a good model to characterize new pathways of immunosuppression for new treatment strategies. Ann N Y Acad Sci 2004, 1024:124-137.
65. Pihl M., Akerman L., Axelsson S., Chéramy M., Hjorth M., Mallone R., et al. Regulatory T cell phenotype and function 4 years after GAD-alum treatment in children with type 1 diabetes. Clin Exp Immunol 2013, 172:394-402.
66. Lazar L., Ofan R., Weintrob N., Avron A., Tamir M., Elias D., et al. Heat-shock protein peptide DiaPep277 treatment in children with newly diagnosed type 1 diabetes: a randomised, double-blind phase II study. Diabetes Metab Res Rev 2007, 23:286-291.
67. Marek-Trzonkowska N., Myśliwec M., Siebert J., Trzonkowski P. Clinical application of regulatory T cells in type 1 diabetes. Pediatr Diabetes 2013, 14:322-332.
68. Hering B.J., Kandaswamy R., Harmon J.V., Ansite J.D., Clemmings S.M., Sakai T., et al. Transplantation of cultured islets from two-layer preserved pancreases in type 1 diabetes with antiCD3 antibody. Am J Transplant 2004, 4:390-401.
69. Cabrera S.M., Rigby M.R., Mirmira R.G. Targeting regulatory T cells in the treatment of type 1 diabetes mellitus. Curr Mol Med 2012, 12:1261-1272.
70. Boussiotis V.A., Tsai E.Y., Yunis E.J., Thim S., Delgado J.C., Dascher C.C., et al. IL-10-producing T cells suppress immune responses in anergic tuberculosis patients. J Clin Invest 2000, 105:1317-1325.
71. Parsa R., Andresen P., Gillett A., Mia S., Zhang X.M., Mayans S., et al. Adoptive transfer of immunomodulatory M2 macrophages prevents type 1 diabetes in NOD mice. Diabetes 2012, 61:2881-2892.
72. Xu A., Zhu W., Li T., Li X., Cheng J., Li C., et al. Interleukin-10 gene transfer into insulin-producing β cells protects against diabetes in non-obese diabetic mice. Mol Med Rep 2015, 12:3881-3889.
73. Fousteri G., Jofra T., Di Fonte R., Battaglia M. Combination of an antigen-specific therapy and an immunomodulatory treatment to simultaneous block recurrent autoimmunity and alloreactivity in non-obese diabetic mice. PLoS One 2015, 10:e0127631.
74. Dendrou C.A., Wicker L.S. The IL-2/CD25 pathway determines susceptibility to T1D in humans and NOD mice. J Clin Immunol 2008, 28:685-696.
75. Long S.A., Rieck M., Sanda S., Bollyky J.B., Samuels P.L., Goland R., et al. Rapamycin/IL-2 combination therapy in patients with type 1 diabetes augments Tregs yet transiently impairs β-cell function. Diabetes 2012, 61:2340-2348.
76. Gruden G., Olivetti C., Cavallo-Perin Bazzan M., Stella S., Tamponi G., et al. Activated protein C resistance in type I diabetes. Diabetes Care 1997, 20:424-425.
77. Xue M., Dervish S., Harrison L.C., Fulcher G., Jackson C.J. Activated protein C inhibits pancreatic islet inflammation, stimulates T regulatory cells, and prevents diabetes in non-obese diabetic (NOD) mice. J Biol Chem 2012, 287:16356-16364.
78. Xue M., Jackson C.J. Activated protein C and its potential applications in prevention of islet β-cell damage and diabetes. Vitam Horm 2014, 95:323-363.
79. Bollyky P.L., Lord J.D., Masewicz S.A., Evanko S.P., Buckner J.H., Wight T.N., et al. Cutting edge: high molecular weight hyaluronan promotes the suppressive effects of CD4 + CD25+ regulatory T cells. J Immunol 2007, 179:744-747.
80. Bollyky P.L., Falk B.A., Long S.A., Preisinger A., Braun K.R., Wu R.P., et al. CD44 costimulation promotes FoxP3+ regulatory T cell persistence and function via production of IL-2, IL-10, and TGF-beta. J Immunol 2009, 183:2232-2241.
81. Bollyky P.L., Bogdani M., Bollyky J.B., Hull R.L., Wight T.N. The role of hyaluronan and the extracellular matrix in islet inflammation and immune regulation. Curr Diab Rep 2012, 12:471-480.
82. Bogdani M., Johnson P.Y., Potter-Perigo S., Nagy N., Day A.J., Bollyky P.L., et al. Hyaluronan and hyaluronan-binding proteins accumulate in both human type 1 diabetic islets and lymphoid tissues and associate with inflammatory cells in insulitis. Diabetes 2014, 63:2727-2743.
83. Chilton P.M., Rezzoug F., Fugier-Vivier I., Weeter L.A., Xu H., Huang Y., et al. Flt3-ligand treatment prevents diabetes in NOD mice. Diabetes 2004, 53:1995-2002.
84. Van Belle T.M., Juntti T., Liao J., von Herrath M. Pre-existing autoimmunity determines type 1 diabetes outcome after Flt3-ligand treatment. J Autoimmun 2010, 34:445-452.
85. Diana J., Griseri T., Lagaye S., Beaudoin L., Autrusseau E., Gautron A.S., et al. NKT cell-plasmacytoid dendritic cell cooperation via OX40 controls viral infection in a tissue-specific manner. Immunity 2009, 30:289-299.
86. Beaudoin L., Laloux V., Novak J., Lucas B., Lehuen A. NKT cells inhibit the onset of diabetes by impairing the development of pathogenic T cells specific for pancreatic β cells. Immunity 2002, 17:725-736.
87. Chen Y.G., Choisy-Rossi C.M., Holl T.M., Chapman H.D., Besra G.S., Porcelli S.A., et al. Activated NKT cells inhibit autoimmune diabetes through tolerogenic recruitment of dendritic cells to pancreatic lymph nodes. J Immunol 2005, 174:1196-1204.
88. Beaudoin L., et al. Plasmacytoid dendritic cells license regulatory T cells, upon iNKT-cell stimulation, to prevent autoimmune diabetes. Eur J Immunol 2014, 4:1454-1466.
89. Smith S.H., Tedder T.F. Targeting B-cells mitigates autoimmune diabetes in NOD mice: what is plan B?. Diabetes 2009, 58:1479-1481.