Reversal of autoimmune diabetes by restoration of antigen-specific tolerance using genetically modified Lactococcus lactis in mice

Journal of Clinical Investigation

Volumn 122, Issue 5, 2012, Pages 1717-1725

  Takiishi, Tatiana ^a   Korf, Hannelie ^a   Van Belle, Tom L ^a   Robert, Sofie ^a   Grieco, Fabio A ^b   Caluwaerts, Silvia ^c   Galleri, Letizia ^b   Spagnuolo, Isabella ^b   Steidler, Lothar ^c   Van Huynegem, Karolien ^c   Demetter, Pieter ^d   Wasserfall, Clive ^e   Atkinson, Mark A ^e   Dotta, Francesco ^b   Rottiers, Pieter ^c   Gysemans, Conny ^a   Mathieu, Chantal ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF SIENA   (Italy)

^c ActoGeniX NV   (Belgium)

^d UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^e UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; CD3 ANTIBODY; INTERLEUKIN 10; PROINSULIN; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; DNA MODIFICATION; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; INSULIN DEPENDENT DIABETES MELLITUS; INSULITIS; LACTOCOCCUS LACTIS; MOUSE; NONHUMAN; PANCREAS ISLET; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TOLERANCE RESTORATION;

ANIMALS; ANTIGENS, CD3; AUTOANTIGENS; CELL COUNT; CELL PROLIFERATION; COMBINED MODALITY THERAPY; DIABETES MELLITUS, TYPE 1; HUMANS; HYPOGLYCEMIC AGENTS; IMMUNE TOLERANCE; IMMUNOLOGIC FACTORS; IMMUNOSUPPRESSION; INSULIN; INSULIN-SECRETING CELLS; INTERLEUKIN-10; INTESTINAL MUCOSA; LACTOCOCCUS LACTIS; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; PROINSULIN; T-LYMPHOCYTES, REGULATORY;

EID: 84860228482     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI60530     Document Type: Article

References (41)

1. Van Belle TL, Coppieters KT, Von Herrath MG. Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol Rev. 2011;91(1):79-118.
2. Bluestone JA, Herold K, Eisenbarth G. Genetics, pathogenesis and clinical interventions in type 1 diabetes. Nature. 2010;464(7293):1293-1300.
3. Chatenoud L, Thervet E, Primo J, Bach JF. Anti-CD3 antibody induces long-term remission of overt autoimmunity in nonobese diabetic mice. Proc Natl Acad Sci U S A. 1994;91(1):123-127. (Pubitemid 24018655)
4. von Herrath MG, Coon B, Wolfe T, Chatenoud L. Nonmitogenic CD3 antibody reverses virally induced (rat insulin promoter-lymphocytic choriomeningitis virus) autoimmune diabetes without impeding viral clearance. J Immunol. 2002; 168(2):933-941. (Pubitemid 34049598)
5. Herold KC, et al. Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus. N Engl J Med. 2002;346(22):1692-1698. (Pubitemid 34547482)
6. Keymeulen B, et al. Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes. N Engl J Med. 2005;352(25):2598-2608. (Pubitemid 41007846)
7. Herold KC, 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(6):1763-1769. (Pubitemid 40770766)
8. Keymeulen B, et al. Transient Epstein-Barr virus reactivation in CD3 monoclonal antibody-treated patients. Blood. 2010;115(6):1145-1155.
9. GlaxoSmithKline and Tolerx announce phase III DEFEND-1 study of otelixizumab in type 1 diabetes did not meet its primary endpoint [press release]. Cambridge, Massachusetts, USA: Associated Press; March 11, 2011.
10. 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(9790):487-497.
11. Daniel D, Wegmann DR. Protection of nonobese diabetic mice from diabetes by intranasal or subcutaneous administration of insulin peptide B-(9-23). Proc Natl Acad Sci U S A. 1996;93(2):956-960. (Pubitemid 26041202)
12. Zhang ZJ, Davidson L, Eisenbarth G, Weiner HL. Suppression of diabetes in nonobese diabetic mice by oral administration of porcine insulin. Proc Natl Acad Sci U S A. 1991;88(22):10252-10256. (Pubitemid 21915813)
13. Wherrett DK, et al. Antigen-based therapy with glutamic acid decarboxylase (GAD) vaccine in patients with recent-onset type 1 diabetes: a randomised double-blind trial. Lancet. 2011;378(9788):319-327.
14. Matthews JB, et al. Developing combination immunotherapies for type 1 diabetes: recommendations from the ITN-JDRF Type 1 Diabetes Combination Therapy Assessment Group. Clin Exp Immunol. 2010; 160(2):176-184.
15. Steidler L, et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science. 2000;289(5483):1352-1355. (Pubitemid 30656052)
16. Huibregtse IL, et al. Induction of antigen-specific tolerance by oral administration of Lactococcus lactis delivered immunodominant DQ8-restricted gliadin peptide in sensitized nonobese diabetic Abo Dq8 transgenic mice. J Immunol. 2009;183(4):2390-2396.
17. Rottiers P, De Smedt T, Steidler L. Modulation of gut-associated lymphoid tissue functions with genetically modified Lactococcus lactis. Int Rev Immunol. 2009;28(6):465-486.
18. Steidler L, et al. Biological containment of genetically modified Lactococcus lactis for intestinal delivery of human interleukin 10. Nat Biotechnol. 2003; 21(7):785-789. (Pubitemid 36791397)
19. Steidler L, Rottiers P. Therapeutic drug delivery by genetically modified Lactococcus lactis. Ann N Y Acad Sci. 2006;1072:176-186. (Pubitemid 44448451)
20. Steidler L, Rottiers P, Coulie B. Actobiotics as a novel method for cytokine delivery. Ann N Y Acad Sci. 2009;1182:135-145.
21. Mehta DS, Christmas RA, Waldmann H, Rosenzweig M. Partial and transient modulation of the CD3-T-cell receptor complex, elicited by low-dose regimens of monoclonal anti-CD3, is sufficient to induce disease remission in non-obese diabetic mice. Immunology. 2010;130(1):103-113.
22. Chatenoud L, Bluestone JA. CD3-specific antibodies: a portal to the treatment of autoimmunity. Nat Rev Immunol. 2007;7(8):622-632. (Pubitemid 47123550)
23. Yamaguchi T, et al. Control of immune responses by antigen-specific regulatory T cells expressing the folate receptor. Immunity. 2007;27(1):145-159. (Pubitemid 47089022)
24. Ludvigsson J, et al. Extended evaluation of the safety and efficacy of GAD treatment of children and adolescents with recent-onset type 1 diabetes: a randomised controlled trial. Diabetologia. 2011;54(3):634-640.
25. Boettler T, von Herrath M. Immunotherapy of type 1 diabetes - how to rationally prioritize combination therapies in T1D. Int Immunopharmacol. 2010;10(12):1491-1495.
26. Luo X, Herold KC, Miller SD. Immunotherapy of type 1 diabetes: where are we and where should we be going? Immunity. 2010;32(4):488-499.
27. Seifarth C, Pop S, Liu B, Wong CP, Tisch R. More stringent conditions of plasmid DNA vaccination are required to protect grafted versus endogenous islets in nonobese diabetic mice. J Immunol. 2003;171(1):469-476. (Pubitemid 36745322)
28. Murai M, et al. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol. 2009;10(11):1178-1184.
29. 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(10):3390-3402.
30. Waldron-Lynch F, et al. Teplizumab treatment induces migration of human t regulatory lymphocytes to the small intestine in vivo. Diabetes. 2011;60(suppl 1):A90.
31. Narendran P, Mannering SI, Harrison LC. Proinsulin- a pathogenic autoantigen in type 1 diabetes. Autoimmun Rev. 2003;2(4):204-210. (Pubitemid 36793944)
32. Peakman M, von Herrath M. Antigen-specific immunotherapy for type 1 diabetes: maximizing the potential. Diabetes. 2010;59(9):2087-2093.
33. Thrower SL, et al. Proinsulin peptide immunotherapy in type 1 diabetes: report of a firstin- man Phase I safety study. Clin Exp Immunol. 2009;155(2):156-165.
34. Bach JF. Anti-CD3 antibodies for type 1 diabetes: beyond expectations. Lancet. 2011; 378(9790):459-460.
35. Bresson D, et al. Anti-CD3 and nasal proinsulin combination therapy enhances remission from recent-onset autoimmune diabetes by inducing Tregs. J Clin Invest. 2006;116(5):1371-1381.
36. Huibregtse IL, et al. Induction of ovalbumin-specific tolerance by oral administration of Lactococcus lactis secreting ovalbumin. Gastroenterology. 2007;133(2):517-528. (Pubitemid 47187339)
37. Vandenbroucke K, et al. Active delivery of trefoil factors by genetically modified Lactococcus lactis prevents and heals acute colitis in mice. Gastroenterology. 2004;127(2):502-513. (Pubitemid 39091899)
38. Wen L, et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature. 2008;455(7216):1109-1113.
39. Braat H, et al. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin Gastroenterol Hepatol. 2006;4(6):754-759. (Pubitemid 43841860)
40. Wasserfall CH, Atkinson MA. Autoantibody markers for the diagnosis and prediction of type 1 diabetes. Autoimmun Rev. 2006;5(6):424-428. (Pubitemid 44150627)
41. Overbergh L, Giulietti A, Valckx D, Decallonne R, Bouillon R, Mathieu C. The use of real-time reverse transcriptase PCR for the quantification of cytokine gene expression. J Biomol Tech. 2003;14(1):33-43.