Achieving antigen-specific tolerance in diabetes: Regulating specifically

International Reviews of Immunology

Volumn 24, Issue 5-6, 2005, Pages 287-305

  Chen, Wei ^a   Herold, Kevan C ^a,c   Bluestone, Jeffrey A ^b  

^a Columbia University ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Anti CD3 monoclonal antibody; Antigen specific tolerance; Autoimmune diabetes; Regulatory T cells

Indexed keywords

AUTOANTIGEN; C PEPTIDE; CARBOXYLYASE; CD4 ANTIGEN; CD8 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DENDRITIC CELL VACCINE; GAMMA INTERFERON; GLUTAMIC ACID; IMMUNOGLOBULIN G1; INSULIN; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; MESSENGER RNA; MONOCLONAL ANTIBODY CD3; MYELIN BASIC PROTEIN; OKT 3; PANCREAS ISLET CELL ANTIBODY; PLACEBO; PROINSULIN; RETINA S ANTIGEN; T LYMPHOCYTE RECEPTOR; THYROGLOBULIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ADOPTIVE IMMUNOTHERAPY; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CELL ISOLATION; CLINICAL TRIAL; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; DIABETOGENESIS; DISEASE PREDISPOSITION; DRUG DOSE REGIMEN; DRUG MECHANISM; EFFECTOR CELL; EXPERIMENTAL MOUSE; GENETIC TRANSCRIPTION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOGENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOREACTIVITY; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE DEPLETION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PREVENTIVE MEDICINE; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; SIDE EFFECT; SPLEEN CELL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TANDEM REPEAT; THYMOCYTE; THYMUS; TRANSGENIC MOUSE; TREG CELL; VACCINATION; VIRUS MENINGITIS;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD3; DENDRITIC CELLS; DIABETES MELLITUS, TYPE 1; HUMANS; IMMUNOSUPPRESSION; IMMUNOTHERAPY; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTE DEPLETION; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, T-CELL; SELF TOLERANCE; T-LYMPHOCYTES, REGULATORY;

EID: 28744432367     PISSN: 08830185     EISSN: None     Source Type: Journal    
DOI: 10.1080/08830180500379671     Document Type: Review

References (88)

1. P. Ehrlich, Collected Studies on Immunity (trans). New York: Wiley, 1906, p. 388.
2. A.M. Silverstein, Autoimmunity versus horror autotoxicus: The struggle for recognition, Nat. Immunol., 2: 279-281, 2001.
3. D. Mathis and C. Benoist, Back to central tolerance, Immunity, 20: 509-516, 2004.
4. A. Pugliese, M. Zeller, A. Fernandez, Jr., L.J. Zalcberg, R.J. Bartlett, C. Ricordi, M. Pietropaolo, G.S. Eisenbarth, S.T. Bennett, and D.D. Patel, The insulin gene is transcribed in the human thymus and transcription levels correlated with allelic variation at the INS VNTR-IDDM2 susceptibility locus for type 1 diabetes, Nat. Genet., 15: 293-297, 1997.
5. H. Moriyama, N. Abiru, J. Paronen, K. Sikora, E. Liu, D. Miao, D. Devendra, J. Beilke, R. Gianani, R.G. Gill, and G.S. Eisenbarth, Evidence for a primary islet autoantigen (preproinsulin 1) for insulitis and diabetes in the nonobese diabetic mouse, Proc. Natl. Acad. Sci. U. S. A., 100: 10376-10381, 2003.
6. M. Nakayama, N. Abiru, H. Moriyama, M. Babaya, E. Liu, D. Miao, L. Yu, D.R. Wegmann, J.C. Hutton, J.F. Elliott, and G.S. Eisenbarth, Prime role for an insulin epitope in the development of type 1 diabetes in NOD mice, Nature, 435: 220-223, 2005.
7. A.M. Posselt, C.F. Barker, J.E. Tomaszewski, J.F. Markmann, M.A. Choti, and A. Naji, Induction of donor-specific unresponsiveness by intrathymic islet transplantation, Science, 249: 1293-1295, 1990.
8. S.B. Koevary and M. Blomberg, Prevention of diabetes in BB/Wor rats by intrathymic islet injection, J. Clin. Invest., 89: 512-516, 1992.
9. K.C. Herold, A.G. Montag, and F. Buckingham, Induction of tolerance to autoimmune diabetes with islet antigens, J. Exp. Med., 176: 1107-1114, 1992.
10. M.S. Anderson, E.S. Venanzi, Z. Chen, S.P. Berzins, C. Benoist, and D. Mathis, The cellular mechanism of aire control of T cell tolerance, Immunity, 23: 227-239, 2005.
11. M.S. Anderson, E.S. Venanzi, L. Klein, Z. Chen, S.P. Berzins, S.J. Turley, H. von Boehmer, R. Bronson, A. Dierich, C. Benoist, and D. Mathis, Projection of an immunological self shadow within the thymus by the aire protein, Science, 298: 1395-1401, 2002.
12. K. Nagamine, P. Peterson, H.S. Scott, J. Kudoh, S. Minoshima, M. Heino, K.J. Krohn, M.D. Lalioti, P.E. Mullis, S.E. Antonarakis, K. Kawasaki, S. Asakawa, F. Ito, and N. Shimizu, Positional cloning of the APECED gene, Nat. Genet., 17: 393-398, 1997.
13. K. Krohn, V. Ovod, P. Vilja, M. Heino, H. Scott, D.S. Kyriakou, S. Antonarakis, H.T. Jacobs, J. Isola, and P. Peterson, Immunochemical characterization of a novel mitochondrially located protein encoded by a nuclear gene within the DFNB8/10 critical region on 21q22.3, Biochem. Biophys. Res. Commun., 238: 806-810, 1997.
14. J.F. Bach and J. Bach Francois, Regulatory T cells under scrutiny, Nat. Rev. Immunol., 3: 189-198, 2003.
15. L. Chatenoud, B. Salomon, and J.A. Bluestone, Suppressor T cells - they're back and critical for regulation of autoimmunity! Immunol. Rev., 182: 149-163, 2001.
16. S. Qin, S.P. Cobbold, H. Pope, J. Elliott, D. Kioussis, J. Davies, and H. Waldmann, "Infectious" transplantation tolerance, Science, 259: 974-977, 1993.
17. A.A. Rossini, Autoimmune diabetes and the circle of tolerance, Diabetes, 53: 267-275, 2004.
18. Diabetes Prevention Trial-Type 1 Diabetes Study Group, Effects of insulin in relatives of patients with type 1 diabetes mellitus, N. Engl. J. Med., 346: 1685-1691, 2002.
19. J.S. Skyler, J.P. Krischer, J. Wolfsdorf, C. Cowie, J.P. Palmer, C. Greenbaum, D. Cuthbertson, L.E. Rafkin-Mervis, H.P. Chase, and E. Leschek, Effects of oral insulin in relatives of patients with type 1 diabetes: The diabetes prevention trial - type 1, Diabetes Care, 28: 1068-1076, 2005.
20. W.J. Riley, N.K. Maclaren, J. Krischer, R.P. Spillar, J.H. Silverstein, D.A. Schatz, S. Schwartz, J. Malone, S. Shah, C. Vadheim, et al., A prospective study of the development of diabetes in relatives of patients with insulin-dependent diabetes, N. Engl. J. Med., 323: 1167-1172, 1990.
21. L. Chatenoud, E. Thervet, J. Primo, and J.F. Bach, Anti-CD3 antibody induces long-term remission of overt autoimmunity in nonobese diabetic mice, Proc Natl Acad Sci U. S. A., 91: 123-127, 1994.
22. L. Chatenoud, J. Primo, and J.F. Bach, CD3 antibody-induced dominant self tolerance in overtly diabetic NOD mice, J. Immunol., 158: 2947-2954, 1997.
23. + T cell unresponsiveness and functional reversal of established experimental autoimmune encephalomyelitis, J. Immunol., 174: 4525-4534, 2005.
24. L. Chatenoud, OKT3-induced cytokine-release syndrome: prevention effect of antitumor necrosis factor monoclonal antibody, Transplant Proc., 25: 47-51, 1993.
25. L. Chatenoud, Humoral immune response against OKT3. Transplant Proc., 25: 68-73, 1993.
26. L. Chatenoud, CD3-specific antibody-induced active tolerance: from bench to bedside, Nat. Rev. Immunol., 3: 123-132, 2003.
27. D. Xu, M.L. Alegre, S.S. Varga, A.L. Rothermel, A.M. Collins, V.L. Pulito, L.S. Hanna, K.P. Dolan, P.W. Parren, J.A. Bluestone, L.K. Jolliffe, and R.A. Zivin, In vitro characterization of five humanized OKT3 effector function variant antibodies. Cell Immunol., 200: 16-26, 2000.
28. K.C. Herold, S.E. Gitelman, U. Masharani, W. Hagopian, B. Bisikirska, D. Donaldson, K. Rother, B. Diamond, D.M. Harlan, and J.A. Bluestone, 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.
29. K.C. Herold, W. Hagopian, J.A. Auger, E. Poumian-Ruiz, L. Taylor, D. Donaldson, S.E. Gitelman, D.M. Harlan, D. Xu, R.A. Zivin, and J.A. Bluestone, Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus, N. Engl. J. Med., 346: 1692-1698, 2002.
30. B. Keymeulen, E. Vandemeulebroucke, A.G. Ziegler, C. Mathieu, L. Kaufman, G. Hale, F. Gorus, M. Goldman, M. Walter, S. Candon, et al., Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes, N. Engl. J. Med., 352: 2598-2608, 2005.
31. M. Belghith, J.A. Bluestone, S. Barriot, J. Megret, J.F. Bach, and L. Chatenoud, TGF-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat. Med., 9: 1202-1208, 2003.
32. B.J. Hering, R. Kandaswamy, J.V. Harmon, J.D. Ansite, S.M. Clemmings, T. Sakai, S. Paraskevas, P.M. Eckman, J. Sageshima, M. Nakano, et al., Transplantation of cultured islets from two-layer preserved pancreases in type 1 diabetes with anti-CD3 antibody, Am. J. Transplant, 4: 390-401, 2004.
33. K.C. Herold, J.B. Burton, F. Francois, E. Poumian-Ruiz, M. Glandt, and J.A. Bluestone, Activation of human T cells by FcR nonbinding anti-CD3 mAb, hOKT3γ1(Ala-Ala), J. Clin. Invest., 111: 409-418, 2003.
34. + regulatory T cells, Nat. Immunol., 4: 330-336, 2003.
35. F. Ramsdell, Foxp3 and natural regulatory T cells: Key to a cell lineage? Immunity, 19: 165-168, 2003.
36. + regulatory T cells: Thymus or periphery, J. Clin. Invest., 112: 1310-1312, 2003.
37. - T cells, J. Clin. Invest., 112: 1437-1443, 2003.
38. + regulatory thymocytes, Blood, 102: 4107-4114, 2003.
39. M.E. Brunkow, E.W. Jeffery, K.A. Hjerrild, B. Paeper, L.B. Clark, S.A. Yasayko, J.E. Wilkinson, D. Galas, S.F. Ziegler, and F. Ramsdell, Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse, Nat. Genet., 27: 68-73, 2001.
40. C.L. Bennett, J. Christie, F. Ramsdell, M.E. Brunkow, P.J. Ferguson, L. Whitesell, T.E. Kelly, F.T. Saulsbury, P.F. Chance, and H.D. Ochs, The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3, Nat. Genet., 27: 20-21, 2001.
41. R.S. Wildin, F. Ramsdell, J. Peake, F. Faravelli, J.L. Casanova, N. Buist, E. Levy-Lahad, M. Mazzella, O. Goulet, L. Perroni, et al., X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy, Nat. Genet., 27: 18-20, 2001.
42. + regulatory T cells, Int. Immunol., 16: 1643-1656, 2004.
43. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production, J. Exp. Med., 188: 287-296, 1998.
44. + regulatory T cells induced by an agonist self-peptide, Nat. Immunol., 2: 301-306, 2001.
45. I. Apostolou, A. Sarukhan, L. Klein, and H. von Boehmer, Origin of regulatory T cells with known specificity for antigen, Nat. Immunol., 3: 756-763, 2002.
46. J.D. Fontenot and A.Y. Rudensky, A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3, Nat. Immunol., 6: 331-337, 2005.
47. + T cells, expanded with dendritic cells presenting a single autoantigenic peptide, suppress autoimmune diabetes, J. Exp. Med., 199: 1467-1477, 2004.
48. + regulatory T cells by antigen-processing dendritic cells, J. Exp. Med., 198: 235-247, 2003.
49. M.V. Dhodapkar and R.M. Steinman, Antigen-bearing immature dendritic cells induce peptide-specific CD8(+) regulatory T cells in vivo in humans, Blood, 100: 174-177, 2002.
50. + regulatory T cells that prevent allograft rejection does not compromise immunity to a viral pathogen, J. Immunol., 174: 3290-3297, 2005.
51. R. Cabrera, Z. Tu, Y. Xu, R.J. Firpi, H.R. Rosen, C. Liu, and D.R. Nelson, An immunomodulatory role for CD4(+)CD25(+) regulatory T lymphocytes in hepatitis C virus infection, Hepatology, 40: 1062-1071, 2004.
52. T. Boettler, H.C. Spangenberg, C. Neumann-Haefelin, E. Panther, S. Urbani, C. Ferrari, H.E. Blum, F. von Weizsacker, and R. Thimme, T cells with a CD4+ CD25+ regulatory phenotype suppress in vitro proliferation of virus-specific CD8+ T cells during chronic hepatitis C virus infection, J. Virol., 79: 7860-7867, 2005.
53. M.G. von Herrath, B. Coon, T. Wolfe, and L. Chatenoud, Nonmitogenic CD3 antibody reverses virally induced (rat insulin promoter-lymphocytic choriomeningitis virus) autoimmune diabetes without impeding viral clearance, J. Immunol., 168: 933-941, 2002.
54. J.A. Smith and J.A. Bluestone, T cell inactivation and cytokine deviation promoted by anti-CD3 mAbs, Curr. Opin. Immunol., 9: 648-654, 1997.
55. J.A. Smith, Q. Tang, and J.A. Bluestone, Partial TCR signals delivered by FcR-non-binding anti-CD3 monoclonal antibodies differentially regulate individual Th subsets, J. Immunol., 160: 4841-4849, 1998.
56. I.R. Cohen, F.J. Quintana, and A. Mimran, Tregs in T cell vaccination: Exploring the regulation of regulation, J. Clin. Invest., 114: 1227-1232, 2004.
57. H. Jiang and L. Chess, The specific regulation of immune responses by CD8+ T cells restricted by the MHC class Ib molecule, Qa-1, Annu. Rev. Immunol., 18: 185-216, 2000.
58. H. Nishikawa, T. Kato, I. Tawara, K. Saito, H. Ikeda, K. Kuribayashi, P.M. Allen, R.D. Schreiber, S. Sakaguchi, L. J. Old, et al., Definition of target antigens for naturally occurring CD4(+)CD25(+) regulatory T cells, J. Exp. Med., 201: 681-686, 2005.
59. Q. Tang, K.J. Henriksen, M. Bi, E.B. Finger, G. Szot, J. Ye, E.L. Masteller, H. McDevitt, M. Bonyhadi, and J.A. Bluestone, In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes, J Exp Med., 199: 1455-1465, 2004.
60. I. Apostolou and H. von Boehmer, In vivo instruction of suppressor commitment in naive T cells, J. Exp. Med., 199: 1401-1408, 2004.
61. J.A. Bluestone and A.K. Abbas, Natural versus adaptive regulatory T cells, Nat. Rev. Immunol., 3: 253-257, 2003.
62. R. Setoguchi, S. Hori, T. Takahashi, and S. Sakaguchi, Homeostatic maintenance of natural Foxp3(+)CD25(+)CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization, J. Exp. Med., 201: 723-735, 2005.
63. M.G. Roncarolo, R. Bacchetta, C. Bordignon, S. Narula, and M.K. Levings, Type 1 T regulatory cells, Immunol. Rev., 182: 68-79, 2001.
64. + T regulatory cells, Novartis Found. Symp., 252: 115-127; discussion 127-131, 203-110, 2003.
65. + regulatory T cells prevent graft rejection: CTLA-4- and IL-10-dependent immunoregulation of alloresponses, J. Immunol., 168: 1080-1086, 2002.
66. + regulatory T cell function, Eur. J. Immunol., 34: 2996-3005, 2004.
67. C.T. Huang, C.J. Workman, D. Flies, X. Pan, A.L. Marson, G. Zhou, E.L. Hipkiss, S. Ravi, J. Kowalski, H.I. Levitsky, et al., Role of LAG-3 in regulatory T cells, Immunity, 21: 503-513, 2004.
68. C.C. Chang, R. Ciubotariu, J.S. Manavalan, J. Yuan, A.I. Colovai, F. Piazza, S. Lederman, M. Colonna, R. Cortesini, R. Dalla-Favera, et al., Tolerization of dendritic cells by TS cells: the crucial role of inhibitory receptors ILT3 and ILT4, Nat. Immunol., 3: 237-243, 2002.
69. N. Suciu-Foca, J.S. Manavalan, and R. Cortesini, Generation and function of antigen-specific suppressor and regulatory T cells, Transpl. Immunol., 11: 235-244, 2003.
70. + regulatory T cells generated by exposure to a model protein antigen prevent allograft rejection: Antigen-specific reactivation in vivo is critical for bystander regulation, Blood, 105: 4871-4877, 2005.
71. S. Arif, T.I. Tree, T.P. Astill, J.M. Tremble, A.J. Bishop, C.M. Dayan, B.O. Roep, and M. Peakman, Autoreactive T cell responses show proinflammatory polarization in diabetes but a regulatory phenotype in health, J. Clin. Invest., 113: 451-463, 2004.
72. K.C. Herold, Achieving antigen-specific immune regulation, J. Clin. Invest., 113: 346-349, 2004.
73. J. Tian, M.A. Atkinson, M. Clare-Salzler, A. Herschenfeld, T. Forsthuber, P.V. Lehmann, and D.L. Kaufman, Nasal administration of glutamate decarboxylase (GAD65) peptides induces Th2 responses and prevents murine insulin-dependent diabetes, J. Exp. Med., 183: 1561-1567, 1996.
74. S.H. Im, D. Barchan, S. Fuchs, and M.C. Souroujon, Mechanism of nasal tolerance induced by a recombinant fragment of acetylcholine receptor for treatment of experimental myasthenia gravis, J. Neuroimmunol., 111: 161-168, 2000.
75. E.J. Massey, A. Sundstedt, M.J. Day, G. Corfield, S. Anderton, and D.C. Wraith, Intranasal peptide-induced peripheral tolerance: The role of IL-10 in regulatory T cell function within the context of experimental autoimmune encephalomyelitis, Vet. Immunol. Immunopathol., 87: 357-372, 2002.
76. L.C. Harrison, M. Dempsey-Collier, D.R. Kramer, and K. Takahashi, Aerosol insulin induces regulatory CD8 gamma delta T cells that prevent murine insulin-dependent diabetes, J. Exp. Med., 184: 2167-2174, 1996.
77. N.R. Martinez, P. Augstein, A.K. Moustakas, G.K. Papadopoulos, S. Gregori, L. Adorini, D.C. Jackson, and L.C. Harrison, Disabling an integral CTL epitope allows suppression of autoimmune diabetes by intranasal proinsulin peptide, J. Clin. Invest., 111: 1365-1371, 2003.
78. Z.J. Zhang, L. Davidson, G. Eisenbarth, and H.L. Weiner, Suppression of diabetes in nonobese diabetic mice by oral administration of porcine insulin, Proc. Natl. Acad. Sci. U. S. A., 88: 10252-10256, 1991.
79. X. Zhang, L. Izikson, L. Liu, and H.L. Weiner, Activation of CD25(+)CD4(+) regulatory T cells by oral antigen administration, J. Immunol., 167: 4245-4253, 2001.
80. K.L. Legge, B. Min, J.J. Bell, J.C. Caprio, L. Li, R.K. Gregg, and H. Zaghouani, Coupling of peripheral tolerance to endogenous interleukin 10 promotes effective modulation of myelin-activated T cells and ameliorates experimental allergic encephalomyelitis, J. Exp. Med., 191: 2039-2052, 2000.
81. S. Rutella and R.M. Lemoli, Regulatory T cells and tolerogenic dendritic cells: From basic biology to clinical applicationsm, Immunol. Lett., 94: 11-26, 2004.
82. K. Mahnke and A.H. Enk, Dendritic cells: key cells for the induction of regulatory T cells? Curr. Top. Microbiol. Immunol., 293: 133-150, 2005.
83. + Tr cells, Blood, 105: 1162-1169, 2005.
84. D.H. Munn and A.L. Mellor, Macrophages and the regulation of self-reactive T cells, Curr. Pharm. Des., 9:257-264, 2003.
85. D.H. Munn, M.D. Sharma, J.R. Lee, K.G. Jhaver, T.S. Johnson, D.B. Keskin, B. Marshall, P. Chandler, S.J. Antonia, R. Burgess, et al., Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase, Science, 297: 1867-1870, 2002.
86. + Regulatory T Cells from Nonobese Diabetic Mice, J. Immunol., 175: 3053-3059, 2005.
87. W.R. Godfrey, Y.G. Ge, D.J. Spoden, B.L. Levine, C.H. June, B.R. Blazar, and S.B. Porter, In vitro-expanded human CD4(+)CD25(+) T-regulatory cells can markedly inhibit allogeneic dendritic cell-stimulated MLR cultures, Blood., 104:453-461, 2004.
88. B. Bisikirska, J. Colgan, J. Luban, J. A. Bluestone, and K. C. Herold, TCR stimulation with modified anti-CD3 mAb expands CD8 T cell population and induces CD8 + CD25 + Tregs, J. Clin. Invest., 115: 2904-2913, 2005.