Recovery from overt type 1 diabetes ensues when immune tolerance and β-Cell formation are coupled with regeneration of endothelial cells in the pancreatic islets

Diabetes

Volumn 62, Issue 8, 2013, Pages 2879-2889

  Wan, Xiaoxiao ^a   Guloglu, F Betul ^a   VanMorlan, Amie M ^a   Rowland, Linda M ^a   Zaghouani, Sarah ^a   Cascio, Jason A ^a   Dhakal, Mermagya ^a   Hoeman, Christine M ^a   Zaghouani, Habib ^a  

^a University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE DECARBOXYLASE; IG GAD2 PEPTIDE; IMMUNOMODULATING AGENT; UNCLASSIFIED DRUG; IMMUNOGLOBULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL REGENERATION; CELL TRANSPLANTATION; ENDOTHELIUM CELL; IMMUNOHISTOCHEMISTRY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; ANIMAL; B LYMPHOCYTE; BONE MARROW TRANSPLANTATION; DISEASE COURSE; IMMUNOLOGY; INFLAMMATION; NONOBESE DIABETIC MOUSE; REGENERATION;

ANIMALS; B-LYMPHOCYTES; BONE MARROW TRANSPLANTATION; DIABETES MELLITUS, TYPE 1; DISEASE PROGRESSION; ENDOTHELIAL CELLS; IMMUNE TOLERANCE; IMMUNOGLOBULINS; INFLAMMATION; ISLETS OF LANGERHANS; MICE; MICE, INBRED NOD; REGENERATION;

EID: 84883430960     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db12-1281     Document Type: Article

References (50)

1. Atkinson MA, Eisenbarth GS. Type 1 diabetes: new perspectives on disease pathogenesis and treatment. Lancet 2001;358:221-229
2. Bluestone JA, Herold K, Eisenbarth G. Genetics, pathogenesis and clinical interventions in type 1 diabetes. Nature 2010;464:1293-1300
3. Belghith M, Bluestone JA, Barriot S, Mégret J, Bach JF, Chatenoud L. TGFbeta- dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat Med 2003;9:1202-1208
4. Herold KC, Hagopian W, Auger JA, et al. Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus. N Engl J Med 2002;346:1692-1698
5. Herold KC, Gitelman SE, Masharani U, et al. A single course of anti-CD3 monoclonal antibody hOKT3gamma1(Ala-Ala) results in improvement in C-peptide responses and clinical parameters for at least 2 years after onset of type 1 diabetes. Diabetes 2005;54:1763-1769
6. Kim SK, Tarbell KV, Sanna M, et al. Prevention of type 1 diabetes transfer by glutamic acid decarboxylase 65 peptide 206-220-specific T cells. Proc Natl Acad Sci USA 2004;101:14204-14209
7. Jain R, Tartar DM, Gregg RK, et al. Innocuous IFNgamma induced by adjuvant-free antigen restores normoglycemia in NOD mice through inhibition of IL-17 production. J Exp Med 2008;205:207-218
8. Hess D, Li L, Martin M, et al. Bone marrow-derived stem cells initiate pancreatic regeneration. Nat Biotechnol 2003;21:763-770
9. Mathews V, Hanson PT, Ford E, Fujita J, Polonsky KS, Graubert TA. Recruitment of bone marrow-derived endothelial cells to sites of pancreatic beta-cell injury. Diabetes 2004;53:91-98
10. Wallet MA, Flores RR, Wang Y, et al. MerTK regulates thymic selection of autoreactive T cells. Proc Natl Acad Sci USA 2009;106:4810-4815
11. Heit JJ, Apelqvist AA, Gu X, et al. Calcineurin/NFAT signalling regulates pancreatic beta-cell growth and function. Nature 2006;443:345-349
12. Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 2004;429:41-46
13. Koulmanda M, Budo E, Bonner-Weir S, et al. Modification of adverse inflammation is required to cure new-onset type 1 diabetic hosts. Proc Natl Acad Sci USA 2007;104:13074-13079
14. Koulmanda M, Bhasin M, Hoffman L, et al. Curative and beta cell regenerative effects of alpha1-Antitrypsin treatment in autoimmune diabetic NOD mice. Proc Natl Acad Sci USA 2008;105:16242-16247
15. Ablamunits V, Sherry NA, Kushner JA, Herold KC. Autoimmunity and beta cell regeneration in mouse and human type 1 diabetes: the peace is not enough. Ann N Y Acad Sci 2007;1103:19-32
16. Choi JB, Uchino H, Azuma K, et al. Little evidence of transdifferentiation of bone marrow-derived cells into pancreatic beta cells. Diabetologia 2003; 46:1366-1374
17. Lechner A, Yang YG, Blacken RA, Wang L, Nolan AL, Habener JF. No evidence for significant transdifferentiation of bone marrow into pancreatic beta-cells in vivo. Diabetes 2004;53:616-623
18. Lammert E, Cleaver O, Melton D. Induction of pancreatic differentiation by signals from blood vessels. Science 2001;294:564-567
19. Cleaver O, Melton DA. Endothelial signaling during development. Nat Med 2003;9:661-668
20. Nikolova G, Jabs N, Konstantinova I, et al. The vascular basement membrane: A niche for insulin gene expression and Beta cell proliferation. Dev Cell 2006;10:397-405
21. Johansson M, Mattsson G, Andersson A, Jansson L, Carlsson PO. Islet endothelial cells and pancreatic beta-cell proliferation: studies in vitro and during pregnancy in adult rats. Endocrinology 2006;147:2315-2324
22. Kaido T, Yebra M, Cirulli V, Montgomery AM. Regulation of human betacell adhesion, motility, and insulin secretion by collagen 4 and its receptor alpha1beta1. J Biol Chem 2004;279:53762-53769
23. Guney MA, Petersen CP, Boustani A, et al. Connective tissue growth factor acts within both endothelial cells and beta cells to promote proliferation of developing beta cells. Proc Natl Acad Sci USA 2011;108: 15242-15247
24. Loomans CJ, de Koning EJ, Staal FJ, et al. Endothelial progenitor cell dysfunction: A novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 2004;53:195-199
25. Schatteman GC, Hanlon HD, Jiao C, Dodds SG, Christy BA. Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice. J Clin Invest 2000;106:571-578
26. Caballero S, Sengupta N, Afzal A, et al. Ischemic vascular damage can be repaired by healthy, but not diabetic, endothelial progenitor cells. Diabetes 2007;56:960-967
27. Thum T, Fraccarollo D, Schultheiss M, et al. Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes. Diabetes 2007;56:666-674
28. Khoo CP, Valorani MG, Brittan M, et al. Characterization of endothelial progenitor cells in the NOD mouse as a source for cell therapies. Diabetes Metab Res Rev 2009;25:89-93
29. Brissova M, Shostak A, Shiota M, et al. Pancreatic islet production of vascular endothelial growth factor-A is essential for islet vascularization, revascularization, and function. Diabetes 2006;55:2974-2985
30. Lammert E, Gu G, McLaughlin M, et al. Role of VEGF-A in vascularization of pancreatic islets. Curr Biol 2003;13:1070-1074
31. Dentelli P, Rosso A, Balsamo A, et al. C-KIT, by interacting with the membrane-bound ligand, recruits endothelial progenitor cells to inflamed endothelium. Blood 2007;109:4264-4271
32. Peichev M, Naiyer AJ, Pereira D, et al. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000;95:952-958
33. Reyes M, Dudek A, Jahagirdar B, Koodie L, Marker PH, Verfaillie CM. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 2002;109:337-346
34. Chatenoud L, Bluestone JA. CD3-specific antibodies: A portal to the treatment of autoimmunity. Nat Rev Immunol 2007;7:622-632
35. Waldron-Lynch F, Herold KC. Immunomodulatory therapy to preserve pancreatic β-cell function in type 1 diabetes. Nat Rev Drug Discov 2011;10:439-452
36. Luo X, Herold KC, Miller SD. Immunotherapy of type 1 diabetes: where are we and where should we be going? Immunity 2010;32:488-499
37. Tian J, Clare-Salzler M, Herschenfeld A, et al. Modulating autoimmune responses to GAD inhibits disease progression and prolongs islet graft survival in diabetes-prone mice. Nat Med 1996;2:1348-1353
38. Tisch R, Liblau RS, Yang XD, Liblau P, McDevitt HO. Induction of GAD65- specific regulatory T-cells inhibits ongoing autoimmune diabetes in nonobese diabetic mice. Diabetes 1998;47:894-899
39. Gregg RK, Jain R, Schoenleber SJ, et al. A sudden decline in active membrane-bound TGF-beta impairs both T regulatory cell function and protection against autoimmune diabetes. J Immunol 2004;173:7308-7316
40. Gregg RK, Bell JJ, Lee HH, et al. IL-10 diminishes CTLA-4 expression on islet-resident T cells and sustains their activation rather than tolerance. J Immunol 2005;174:662-670
41. Agardh CD, Cilio CM, Lethagen A, et al. Clinical evidence for the safety of GAD65 immunomodulation in adult-onset autoimmune diabetes. J Diabetes Complications 2005;19:238-246
42. Michels AW, von Herrath M. 2011 update: Antigen-specific therapy in type 1 diabetes. Curr Opin Endocrinol Diabetes Obes 2011;18:235-240
43. Li L, Yi Z, Wang B, Tisch R. Suppression of ongoing T cell-mediated autoimmunity by peptide-MHC class II dimer vaccination. J Immunol 2009; 183:4809-4816
44. Tang Q, Henriksen KJ, Bi M, et al. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J Exp Med 2004;199:1455- 1465
45. Ianus A, Holz GG, Theise ND, Hussain MA. In vivo derivation of glucosecompetent pancreatic endocrine cells from bone marrow without evidence of cell fusion. J Clin Invest 2003;111:843-850
46. Phillips JM, O'Reilly L, Bland C, Foulis AK, Cooke A. Patients with chronic pancreatitis have islet progenitor cells in their ducts, but reversal of overt diabetes in NOD mice by anti-CD3 shows no evidence for islet regeneration. Diabetes 2007;56:634-640
47. Takiishi T, Korf H, Van Belle TL, et al. Reversal of autoimmune diabetes by restoration of antigen-specific tolerance using genetically modified Lactococcus lactis in mice. J Clin Invest 2012;122:1717-1725
48. Wang M, Racine JJ, Song X, et al. Mixed chimerism and growth factors augment beta cell regeneration and reverse late-stage type 1 diabetes. Sci Transl Med 2012;4:133ra59
49. Tartar DM, VanMorlan AM, Wan X, et al. FoxP3+RORgammat+ T helper intermediates display suppressive function against autoimmune diabetes. J Immunol 2010;184:3377-3385
50. Wan X, Guloglu FB, VanMorlan AM, et al. Mechanisms underlying antigenspecific tolerance of stable and convertible Th17 cells during suppression of autoimmune diabetes. Diabetes 2012;61:2054-2065