Immunotherapy for the prevention and treatment of type 1 diabetes

International Reviews of Immunology

Volumn 24, Issue 5-6, 2005, Pages 307-326

  Goudy, Kevin S ^a   Tisch, Roland ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Antigen; Autoimmunity; Diabetes; T cells

Indexed keywords

ADENOVIRUS VECTOR; ALPHA GALACTOSYLCERAMIDE; B LYMPHOCYTE ANTIGEN; CD4 ANTIGEN; CD40 LIGAND MONOCLONAL ANTIBODY; CD8 ANTIGEN; CHOLERA TOXIN B SUBUNIT; EPITOPE; FC RECEPTOR; FREUND ADJUVANT; GAMMA INTERFERON; GLUCOSE 6 PHOSPHATASE; GLUTAMATE DECARBOXYLASE 65; HEAT SHOCK PROTEIN 60; IMMUNOGLOBULIN; INSULIN; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCLONAL ANTIBODY CD3; PEPTIDE; PLASMID DNA; RECOMBINANT ANTIGEN; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

ADOPTIVE IMMUNOTHERAPY; ANTIGEN PRESENTING CELL; ANTIINFLAMMATORY ACTIVITY; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; CHRONIC INFLAMMATION; CONTROL STRATEGY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISEASE COURSE; DISEASE PREDISPOSITION; DRUG EFFICACY; DRUG POTENCY; DRUG SAFETY; DRUG TOLERABILITY; ENVIRONMENTAL FACTOR; EXPERIMENTAL MOUSE; HIGH RISK POPULATION; HUMAN; HUMORAL IMMUNITY; IMMUNOMODULATION; IMMUNOREACTIVITY; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; LONG TERM CARE; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MOUSE STRAIN; NONHUMAN; PREVENTIVE MEDICINE; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; RECEPTOR DOWN REGULATION; REVIEW; RISK ASSESSMENT; RODENT; T CELL DEPLETION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH1 CELL; TREATMENT INDICATION; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD3; DIABETES MELLITUS, TYPE 1; GENE THERAPY; HUMANS; IMMUNOSUPPRESSION; IMMUNOTHERAPY; INSULIN-SECRETING CELLS; INTERLEUKIN-10; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED NOD; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 28744436698     PISSN: 08830185     EISSN: None     Source Type: Journal    
DOI: 10.1080/08830180500379721     Document Type: Review

References (88)

1. M.A. Permutt, J. Wasson, and N. Cox, Genetic epidemiology of diabetes, J. Clin. Invest., 115: 1431-1439, 2005.
2. 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 hOKT3γy1(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.
3. 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, et al., Anti-CD3 monoclonal antibody in new-onset type 1 diabetes mellitus, N. Engl. J. Med., 346: 1692-1698, 2002.
4. 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.
5. The 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.
6. M.S. Anderson and J.A. Bluestone, The NOD mouse: a model of immune dysregulation, Annu. Rev. Immunol., 23: 447-485, 2005.
7. R. Gianani and G.S. Eisenbarth, The stages of type 1A diabetes: 2005, Immunol. Rev., 204: 232-249, 2005.
8. R. Tisch and H. McDevitt, Insulin-dependent diabetes mellitus, Cell, 85: 291-297, 1996.
9. I. Andre, A. Gonzalez, B. Wang, J. Katz, C. Benoist, and D. Mathis, Checkpoints in the progression of autoimmune disease: lessons from diabetes models, Proc. Natl. Acad. Sci. U. S. A., 93: 2260-2263, 1996.
10. T.L. Delovitch and B. Singh, The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD, Immunity, 7: 727-738, 1997.
11. J.A. Todd and L.S. Wicker, Genetic protection from the inflammatory disease type 1 diabetes in humans and animal models, Immunity, 15: 387-395, 2001.
12. R. Tisch, B. Wang, and D.V. Serreze, Induction of glutamic acid decarboxylase 65-specific Th2 cells and suppression of autoimmune diabetes at late stages of disease is epitope dependent, J. Immunol., 163: 1178-1187, 1999.
13. D.L. Kaufman, M. Clare-Salzler, J. Tian, T. Forsthuber, G. S. Ting, P. Robinson, M.A. Atkinson, E.E. Sercarz, A.J. Tobin, and P.V. Lehmann, Spontaneous loss of T-cell tolerance to glutamic acid decarboxylase in murine insulin-dependent diabetes, Nature, 366: 69-72, 1993.
14. R. Tisch, X.D. Yang, S.M. Singer, R.S. Liblau, L. Fugger, and H.O. McDevitt, Immune response to glutamic acid decarboxylase correlates with insulitis in non-obese diabetic mice, Nature, 366: 72-75, 1993.
15. D.R. Wegmann, M. Norbury-Glaser, and D. Daniel, Insulin-specific T cells are a predominant component of islet infiltrates in pre-diabetic NOD mice, Eur. J. Immunol., 24: 1853-1857, 1994.
16. S.M. Lieberman, T. Takaki, B. Han, P. Santamaria, D.V. Serreze, and T.P. DiLorenzo, Individual nonobese diabetic mice exhibit unique patterns of CD8+ T cell reactivity to three islet antigens, including the newly identified widely expressed dystrophia myotonica kinase, J. Immunol., 173: 6727-6734, 2004.
17. F.S. Wong, J. Karttunen, C. Dumont, L. Wen, I. Visintin, I.M. Pilip, N. Shastri, E.G. Pamer, and C.A. Janeway, Jr., Identification of an MHC class I-restricted autoantigen in type 1 diabetes by screening an organ-specific cDNA library, Nat. Med., 5: 1026-1031, 1999.
18. P. Achenbach, K. Kelemen, D.R. Wegmann, and J.C. Hutton, Spontaneous peripheral T-cell responses to the IA-2beta (phogrin) autoantigen in young nonobese diabetic mice, J. Autoimmun., 19: 111-116, 2002.
19. O.S. Birk, D.C. Douek, D. Elias, K. Takacs, H. Dewchand, S.L. Gur, M.D. Walker, R. van der Zee, I.R. Cohen, and D.M. Altmann, A role of Hsp60 in autoimmune diabetes: analysis in a transgenic model, Proc. Natl. Acad. Sci. U. S. A., 93: 1032-1037, 1996.
20. C. Benoist and D. Mathis, Selection for survival? Science, 276: 2000-2001, 1997.
21. A. Rabinovitch, Immunoregulatory and cytokine imbalances in the pathogenesis of IDDM. Therapeutic intervention by immunostimulation? Diabetes, 43: 613-621, 1994.
22. 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.
23. C.J. Fox and J.S. Danska, IL-4 expression at the onset of islet inflammation predicts nondestructive insulitis in nonobese diabetic mice, J. Immunol., 158: 2414-2424, 1997.
24. + T-cells in type 1 diabetes, Diabetes, 54: 1407-1414, 2005.
25. S. Gregori, N. Giarratana, S. Smiroldo, and L. Adorini, Dynamics of pathogenic and suppressor T cells in autoimmune diabetes development, J. Immunol., 171: 4040-4047, 2003.
26. + T regulatory cells dependent on ICOS promote regulation of effector cells in the prediabetic lesion, J. Exp. Med., 199: 1479-1489, 2004.
27. + regulatory T cells during autoimmune diabetes, J. Exp. Med., 201: 1333-1346, 2005.
28. S. You, M. Belghith, S. Cobbold, M.A. Alyanakian, C. Gouarin, S. Barriot, C. Garcia, H. Waldmann, J.F. Bach, and L. Chatenoud, Autoimmune diabetes onset results from qualitative rather than quantitative age-dependent changes in pathogenic T-cells, Diabetes, 54: 1415-1422, 2005.
29. + regulatory T cells, Curr. Opin. Immunol., 16: 203-208, 2004.
30. M. Kronenberg and A. Rudensky, Regulation of immunity by self-reactive T cells, Nature, 435: 598-604, 2005.
31. + regulatory T cells in immunological tolerance to self and non-self, Nat. Immunol., 6: 345-352, 2005.
32. + regulatory T cells, Nat. Immunol., 4: 330-336, 2003.
33. S. Hori, T. Nomura, and S. Sakaguchi, Control of regulatory T-cell development by the transcription factor Foxp3, Science, 299: 1057-1061, 2003.
34. 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.
35. + regulatory T cells in vivo requires B7 costimulation, but not the thymus, J. Exp. Med., 201: 127-137, 2005.
36. M. Falcone, F. Facciotti, N. Ghidoli, P. Monti, S. Olivieri, L. Zaccagnino, E. Bonifacio, G. Casorati, F. Sanvito, and N. Sarvetnick, Up-regulation of CD1d expression restores the immunoregulatory function of NKT cells and prevents autoimmune diabetes in nonobese diabetic mice, J. Immunol., 172: 5908-5916, 2004.
37. A. Kukreja, G. Cost, J. Marker, C. Zhang, Z. Sun, K. Lin-Su, S. Ten, M. Sanz, M. Exley, et al., Multiple immuno-regulatory defects in type-1 diabetes, J. Clin. Invest., 109: 131-140, 2002.
38. L.D. Poulton, M.J. Smyth, C.G. Hawke, P. Silveira, D. Shepherd, O.V. Naidenko, D.I. Godfrey, and A.G. Baxter, Cytometric and functional analyses of NK and NKT cell deficiencies in NOD mice, Int. Immunol., 13: 887-896, 2001.
39. M. Kronenberg, Toward an understanding of NKT cell biology: progress and paradoxes, Annu. Rev. Immunol., 23: 877-900, 2005.
40. B. Han, P. Serra, J. Yamanouchi, A. Amrani, J.F. Elliott, P. Dickie, T.P. Dilorenzo, and P. Santamaria, Developmental control of CD8 T cell-avidity maturation in autoimmune diabetes, J. Clin. Invest., 115: 1879-1887, 2005.
41. J. Liu and D. Beller, Aberrant production of IL-12 by macrophages from several autoimmune-prone mouse strains is characterized by intrinsic and unique patterns of NF-κ B expression and binding to the IL-12 p40 promoter, J. Immunol., 169: 581-586, 2002.
42. B. Poligone, D.J. Weaver Jr., P. Sen, A.S. Baldwin Jr., and R. Tisch, Elevated NF-κB activation in nonobese diabetic mouse dendritic cells results in enhanced APC function, J. Immunol., 168: 188-196, 2002.
43. P. Sen, S. Bhattacharyya, M. Wallet, C.P. Wong, B. Poligone, M. Sen, A.S. Baldwin Jr., and R. Tisch, NF-κ B hyperactivation has differential effects on the APC function of nonobese diabetic mouse macrophages, J. Immunol., 170: 1770-1780, 2003.
44. P.F. Bougneres, P. Landais, C. Boisson, J.C. Carel, N. Frament, C. Boitard, J.L. Chaussain, and J.F. Bach, Limited duration of remission of insulin dependency in children with recent overt type I diabetes treated with low-dose cyclosporin, Diabetes, 39: 1264-1272, 1990.
45. L.K. Shoda, D.L. Young, S. Ramanujan, C.C. Whiting, M.A. Atkinson, J.A. Bluestone, G.S. Eisenbarth, D. Mathis, A.A. Rossini, S.E. Campbell, et al., A Comprehensive Review of Interventions in the NOD Mouse and Implications for Translation, Immunity, 23: 115-126, 2005.
46. C. Seifarth, S. Pop, B. Liu, C.P. Wong, and R. Tisch, More stringent conditions of plasmid DNA vaccination are required to protect grafted versus endogenous islets in nonobese diabetic mice, J. Immunol., 171: 469-476, 2003.
47. R. Tisch, B. Wang, D.J. Weaver, B. Liu, T. Bui, J. Arthos, and D.V. Serreze, Antigen-specific mediated suppression of beta cell autoimmunity by plasmid DNA vaccination, J. Immunol., 166: 2122-2132, 2001.
48. I. Raz, D. Elias, A. Avron, M. Tamir, M. Metzger, and I.R. Cohen, Beta-cell function in new-onset type 1 diabetes and immunomodulation with a heat-shock protein peptide (DiaPep277): a randomised, double-blind, phase II trial, Lancet, 358: 1749-1753, 2001.
49. 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.
50. A.P. Olcott, J. Tian, V. Walker, H. Dang, B. Middleton, L. Adorini, L. Washburn, and D.L. Kaufman, Antigen-based therapies using ignored determinants of β cell antigens can more effectively inhibit late-stage autoimmune disease in diabetes-prone mice, J. Immunol., 175: 1991-1999, 2005.
51. K.D. Moudgil and E.E. Sercarz, Understanding crypticity is the key to revealing the pathogenesis of autoimmunity, Trends Immunol., 26: 355-359, 2005.
52. A.M. Faria and H.L. Weiner, Oral tolerance, Immunol. Rev., 206: 232-259, 2005.
53. R. Maron, M. Guerau-de-Arellano, X. Zhang, and H.L. Weiner, Oral administration of insulin to neonates suppresses spontaneous and cyclophosphamide induced diabetes in the NOD mouse, J. Autoimmun., 16: 21-28, 2001.
54. + regulatory T-cells, Diabetes, 48: 2150-2156, 1999.
55. 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.
56. E. Blanas, F.R. Carbone, J. Allison, J.F. Miller, and W.R. Heath, Induction of autoimmune diabetes by oral administration of autoantigen, Science, 274: 1707-1709, 1996.
57. L.C. Harrison, M.C. Honeyman, C.E. Steele, N.L. Stone, E. Sarugeri, E. Bonifacio, J.J. Couper, and P.G. Colman, Pancreatic beta-cell function and immune responses to insulin after administration of intranasal insulin to humans at risk for type 1 diabetes, Diabetes Care, 27: 2348-2355, 2004.
58. L.B. Nicholson, A. Murtaza, B.P. Hafler, A. Sette, and V.K. Kuchroo, A T-cell receptor antagonist peptide induces T cells that mediate bystander suppression and prevent autoimmune encephalomyelitis induced with multiple myelin antigens, Proc. Natl. Acad. Sci. U. S. A., 94: 9279-9284, 1997.
59. J. Sloan-Lancaster and P.M. Allen, Altered peptide ligand-induced partial T-cell activation: Molecular mechanisms and role in T-cell biology, Annu. Rev. Immunol., 14: 1-27, 1996.
60. D.G. Alleva, A. Gaur, L. Jin, D. Wegmann, P.A. Gottlieb, A. Pahuja, E.B. Johnson, T. Motheral, A. Putnam, P.D. Crowe, et al., Immunological characterization and therapeutic activity of an altered-peptide ligand, NBI-6024, based on the immunodominant type 1 diabetes autoantigen insulin B-chain (9-23) peptide, Diabetes, 51: 2126-2134, 2002.
61. B. Bielekova, B. Goodwin, N. Richert, I. Cortese, T. Kondo, G. Afshar, B. Gran, J. Eaton, J. Antel, J.A. Frank, et al., Encephalitogenic potential of the myelin basic protein peptide (amino acids 83-99) in multiple sclerosis: results of a phase II clinical trial with an altered peptide ligand, Nat. Med., 6: 1167-1175, 2000.
62. L. Kappos, G. Comi, H. Panitch, J. Oger, J. Antel, P. Conlon, and L. Steinman, Induction of a non-encephalitogenic type 2 T helper-cell autoimmune response in multiple sclerosis after administration of an altered peptide ligand in a placebo-controlled, randomized phase II trial. The Altered Peptide Ligand in Relapsing MS Study Group, Nat. Med., 6: 1176-1182, 2000.
63. R.K. Gregg, J.J. Bell, H.H. Lee, R. Jain, S.J. Schoenleber, R. Divekar, and H. Zaghouani, IL-10 diminishes CTLA-4 expression on islet-resident T cells and sustains their activation rather than tolerance, J. Immunol., 174: 662-670, 2005.
64. + T cells by a soluble dimeric peptide-MHC class II chimera, Nat. Immunol., 3: 383-391, 2002.
65. A. Hanninen, N.R. Martinez, G.M. Davey, W.R. Heath, and L.C. Harrison, Transient blockade of CD40 ligand dissociates pathogenic from protective mucosal immunity, J. Clin. Invest., 109: 261-267, 2002.
66. V.K. Ramiya, X.Z. Shang, P.G. Pharis, C.H. Wasserfall, T.V. Stabler, A.B. Muir, D.A. Schatz, and N.K. Maclaren, Antigen based therapies to prevent diabetes in NOD mice, J. Autoimmun., 9: 349-356, 1996.
67. L. Adorini, G. Penna, N. Giarratana, and M. Uskokovic, Tolerogenic dendritic cells induced by vitamin D receptor ligands enhance regulatory T cells inhibiting allograft rejection and autoimmune diseases, J. Cell. Biochem., 88: 227-233, 2003.
68. A.E. Pedersen, M. Gad, M.R. Walter, and M.H. Claesson, Induction of regulatory dendritic cells by dexamethasone and 1alpha, 25-Dihydroxyvitamin D(3), Immunol. Lett., 91: 63-69, 2004.
69. + regulatory T cells by 1,25-dihydroxyvitamin D, Blood, 2005.
70. S. Hong, M.T. Wilson, I. Serizawa, L. Wu, N. Singh, O.V. Naidenko, T. Miura, T. Haba, D.C. Scherer, J. Wei, et al., The natural killer T-cell ligand alpha-galactosylceramide prevents autoimmune diabetes in non-obese diabetic mice, Nat. Med., 7: 1052-1056, 2001.
71. S. Sharif, G.A. Arreaza, P. Zucker, Q.S. Mi, J. Sondhi, O.V. Naidenko, M. Kronenberg, Y. Koezuka, T.L. Delovitch, J.M. Gombert, et al., Activation of natural killer T cells by alpha-galactosylceramide treatment prevents the onset and recurrence of autoimmune Type 1 diabetes, Nat. Med., 7: 1057-1062, 2001.
72. K.O. Yu, J.S. Im, A. Molano, Y. Dutronc, P.A. Illarionov, C. Forestier, N. Fujiwara, I. Arias, S. Miyake, T. Yamamura, et al., Modulation of CD1d-restricted NKT cell responses by using N-acyl variants of alpha-galactosylceramides, Proc. Natl. Acad. Sci. U. S. A.., 102: 3383-3388, 2005.
73. Y.G. Chen, C.M. Choisy-Rossi, T.M. Holl, H.D. Chapman, G.S. Besra, S.A. Porcelli, D.J. Shaffer, D. Roopenian, S.B. Wilson, and D.V. Serreze, Activated NKT cells inhibit autoimmune diabetes through tolerogenic recruitment of dendritic cells to pancreatic lymph nodes, J. Immunol., 174: 1196-1204, 2005.
74. Y.N. Naumov, K.S. Bahjat, R. Gausling, R. Abraham, M.A. Exley, Y. Koezuka, S.B. Balk, J.L. Strominger, M. Clare-Salzer, and S.B. Wilson, Activation of CD1d-restricted T cells protects NOD mice from developing diabetes by regulating dendritic cell subsets, Proc. Natl. Acad. Sci. U. S. A., 98: 13838-13843, 2001.
75. G. Giaccone, C.J. Punt, Y. Ando, R. Ruijter, N. Nishi, M. Peters, B.M. von Blomberg, R.J. Scheper, H.J. van der Vliet, A.J. van den Eertwegh, et al., A phase I study of the natural killer T-cell ligand alpha-galactosylceramide (KRN7000) in patients with solid tumors, Clin. Cancer Res., 8: 3702-3709, 2002.
76. L. Bilenki, J. Yang, Y. Fan, S. Wang, and X. Yang, Natural killer T cells contribute to airway eosinophilic inflammation induced by ragweed through enhanced IL-4 and eotaxin production, Eur. J. Immunol., 34: 345-354, 2004.
77. E. Tupin, A. Nicoletti, R. Elhage, M. Rudling, H.G. Ljunggren, G.K. Hansson, and G.P. Berne, CD1d-dependent activation of NKT cells aggravates atherosclerosis, J. Exp. Med., 199: 417-422, 2004.
78. L. Chatenoud, CD3-specific antibody-induced active tolerance: from bench to bedside, Nat. Rev. Immunol., 3: 123-132, 2003.
79. 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.
80. + T-cell unresponsiveness and functional reversal of established experimental autoimmune encephalomyelitis, J. Immunol., 174: 4525-4534, 2005.
81. L.M. Williams, G. Ricchetti, U. Sarma, T. Smallie, and B.M. Foxwell, Interleukin-10 suppression of myeloid cell activation - a continuing puzzle, Immunology, 113: 281-292, 2004.
82. M.V. Dhodapkar, R.M. Steinman, J. Krasovsky, C. Munz, and N. Bhardwaj, Antigen-specific inhibition of effector T-cell function in humans after injection of immature dendritic cells, J. Exp. Med., 193: 233-238, 2001.
83. K. Asadullah, W. Sterry, K. Stephanek, D. Jasulaitis, M. Leupold, H. Audring, H.D. Volk, and W.D. Docke, IL-10 is a key cytokine in psoriasis. Proof of principle by IL-10 therapy: a new therapeutic approach, J. Clin. Invest., 101: 783-794, 1998.
84. K. Goudy, S. Song, C. Wasserfall, Y.C. Zhang, M. Kapturczak, A. Muir, M. Powers, M. Scott-Jorgensen, M. Campbell-Thompson, J.M. Crawford, et al., Adeno-associated virus vector-mediated IL-10 gene delivery prevents type 1 diabetes in NOD mice, Proc. Natl. Acad. Sci. U. S. A., 98: 13913-13918, 2001.
85. + cell populations in vivo and ameliorates type 1 diabetes in nonobese diabetic mice in a dose-dependent fashion, J. Immunol., 171: 2270-2278, 2003.
86. Y.C. Zhang, A. Pileggi, A. Agarwal, R.D. Molano, M. Powers, T. Brusko, C. Wasserfall, K. Goudy, E. Zahr, R. Poggioli, et al., Adeno-associated virus-mediated IL-10 gene therapy inhibits diabetes recurrence in syngeneic islet cell transplantation of NOD mice, Diabetes, 52: 708-716, 2003.
87. R.P. Haberman, T.J. McCown, and R.J. Samulski, Inducible long-term gene expression in brain with adeno-associated virus gene transfer, Gene. Ther., 5: 1604-1611, 1998.
88. X.X. Zheng, A. Sanchez-Fueyo, M. Sho, C. Domenig, M.H. Sayegh, and T.B. Strom, Favorably tipping the balance between cytopathic and regulatory T cells to create transplantation tolerance, Immunity, 19: 503-514, 2003.