Immunotherapy-based strategies for the treatment of autoimmune diabetes: Searching for the cure

Current Pharmaceutical Design

Volumn 17, Issue 29, 2011, Pages 3217-3223

  Phillips, Brett E ^a   Trucco, Massimo ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Autoimmune disease; Immunotherapy; Type 1 diabetes

Indexed keywords

B7 ANTIGEN; CD4 ANTIBODY; CD40 ANTIGEN; CD86 ANTIGEN; IMMUNOSUPPRESSIVE AGENT; LEUKOCYTE ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RITUXIMAB; T LYMPHOCYTE RECEPTOR; AUTOANTIBODY; AUTOANTIGEN;

ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; BLOOD GLUCOSE MONITORING; CD4+ CD25+ T LYMPHOCYTE; CELL POPULATION; DISEASE COURSE; GENE LOCUS; GENETIC SUSCEPTIBILITY; GLUCOSE BLOOD LEVEL; GRAFT SURVIVAL; HELPER CELL; HUMAN; IMMUNE SYSTEM; IMMUNOTHERAPY; INSULIN DEPENDENT DIABETES MELLITUS; LINKAGE ANALYSIS; MEDICAL EDUCATION; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; T CELL DEPLETION; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TH2 CELL; ANIMAL; B LYMPHOCYTE; CLINICAL TRIAL (TOPIC); DENDRITIC CELL; IMMUNOLOGY; METHODOLOGY; PANCREAS ISLET BETA CELL; REVIEW;

ANIMALS; AUTOANTIBODIES; AUTOANTIGENS; B-LYMPHOCYTES; CLINICAL TRIALS AS TOPIC; DENDRITIC CELLS; DIABETES MELLITUS, TYPE 1; HUMANS; IMMUNOTHERAPY; INSULIN-SECRETING CELLS; T-LYMPHOCYTES;

EID: 84858723178     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/138161211798157603     Document Type: Article

References (120)

1. Bresson D, von Herrath M. Moving towards efficient therapies in type 1 diabetes: to combine or not to combine? Autoimmunity reviews 2007; 6(5): 315-22.
2. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med 1993 Sep 30; 329(14): 977-86.
3. Marzorati S, Pileggi A, Ricordi C. Allogeneic islet transplantation. Expert opinion on biological therapy 2007; 7(11): 1627-45.
4. Roelen DL, Huurman VA, Hilbrands R, Gillard P, Duinkerken G, van der Meer-Prins PW, et al. Relevance of cytotoxic alloreactivity under different immunosuppressive regimens in clinical islet cell transplantation. Clinical and experimental immunology 2009; 156(1): 141-8.
5. Huurman VA, Hilbrands R, Pinkse GG, Gillard P, Duinkerken G, van de Linde P, et al. Cellular islet autoimmunity associates with clinical outcome of islet cell transplantation. PLoS One 2008; 3(6): e2435.
6. Van Belle T, von Herrath M. Immunosuppression in islet transplantation. J clinical investigation 2008; 118(5): 1625-8.
7. Sharma A, Zangen DH, Reitz P, Taneja M, Lissauer ME, Miller CP, et al. The homeodomain protein IDX-1 increases after an early burst of proliferation during pancreatic regeneration. Diabetes 1999; 48(3): 507-13.
8. Lampeter EF, Gurniak M, Brocker U, Klemens C, Tubes M, Friemann J, et al. Regeneration of beta-cells in response to islet inflammation. Exp Clin Endocrinol Diabetes 1995; 103 Suppl 2: 74-8.
9. Trudeau JD, Dutz JP, Arany E, Hill DJ, Fieldus WE, Finegood DT. Neonatal beta-cell apoptosis: a trigger for autoimmune diabetes? Diabetes 2000; 49(1): 1-7.
10. Oldstone MB. Molecular mimicry and autoimmune disease. Cell 1987 Sep 11; 50(6): 819-820.
11. Oldstone MB. Virus-induced autoimmunity: molecular mimicry as a route to autoimmune disease. J autoimmunity 1989; 2 Suppl: 187-194.
12. Oldstone MB. Molecular mimicry as a mechanism for the cause and a probe uncovering etiologic agent(s) of autoimmune disease. Current topics in microbiology and immunology 1989; 145: 127-135.
13. Conrad B, Weidmann E, Trucco G, Rudert WA, Behboo R, Ricordi C, et al. Evidence for superantigen involvement in insulin-dependent diabetes mellitus aetiology. Nature 1994 Sep 22; 371(6495): 351-355.
14. Conrad B, Trucco M. Superantigens as etiopathogenetic factors in the development of insulin-dependent diabetes mellitus. Diabetes/metabolism reviews 1994; 10(4): 309-38.
15. Christen U, von Herrath MG. Manipulating the type 1 vs type 2 balance in type 1 diabetes. Immunologic research 2004; 30(3): 309-325.
16. Christen U, von Herrath MG. Induction, acceleration or prevention of autoimmunity by molecular mimicry. Molecular immunology 2004; 40(14-15): 1113-1120.
17. Ehl S, Hombach J, Aichele P, Rulicke T, Odermatt B, Hengartner H, et al. Viral and bacterial infections interfere with peripheral tolerance induction and activate CD8+ T cells to cause immuno-pathology. J experimental medicine 1998 Mar 2; 187(5): 763-774.
18. Ludewig B, Ehl S, Karrer U, Odermatt B, Hengartner H, Zinkernagel RM. Dendritic cells efficiently induce protective antiviral immunity. J virology 1998; 72(5): 3812-3818.
19. Ludewig B, Odermatt B, Landmann S, Hengartner H, Zinkernagel RM. Dendritic cells induce autoimmune diabetes and maintain disease via de novo formation of local lymphoid tissue. J experimental medicine 1998 Oct 19; 188(8): 1493-1501.
20. Bluestone JA. Costimulation and its role in organ transplantation. Clinical transplantation 1996; 10(1 Pt 2): 104-9.
21. Sayegh MH, Turka LA. T cell costimulatory pathways: promising novel targets for immunosuppression and tolerance induction. J Am Soc Nephrol 1995; 6(4): 1143-1150.
22. Kishimoto K, Dong VM, Sayegh MH. The role of costimulatory molecules as targets for new immunosuppressives in transplantation. Current opinion in urology 2000; 10(2): 57-62.
23. Arnush M, Heitmeier MR, Scarim AL, Marino MH, Manning PT, Corbett JA. IL-1 produced and released endogenously within human islets inhibits beta cell function. J clinical investigation 1998 Aug 1; 102(3): 516-26.
24. Isermann B, Ritzel R, Zorn M, Schilling T, Nawroth PP. Autoantibodies in diabetes mellitus: current utility and perspectives. Exp Clin Endocrinol Diabetes 2007; 115(8): 483-90.
25. Corbett JA, Wang JL, Misko TP, Zhao W, Hickey WF, McDaniel ML. Nitric oxide mediates IL-1 beta-induced islet dysfunction and destruction: prevention by dexamethasone. Autoimmunity 1993; 15(2): 145-53.
26. McDaniel ML, Kwon G, Hill JR, Marshall CA, Corbett JA. Cytokines and nitric oxide in islet inflammation and diabetes. Proceedings of the Society for Experimental Biology and Medicine Society for Experimental Biology and Medicine (New York, NY 1996; 211(1): 24-32.
27. Scarim AL, Heitmeier MR, Corbett JA. Irreversible inhibition of metabolic function and islet destruction after a 36-hour exposure to interleukin-1beta. Endocrinology 1997; 138(12): 5301-7.
28. Dahlen E, Dawe K, Ohlsson L, Hedlund G. Dendritic cells and macrophages are the first and major producers of TNF-alpha in pancreatic islets in the nonobese diabetic mouse. J Immunol 1998; 160(7): 3585-93.
29. Baquerizo H, Rabinovitch A. Interferon-gamma sensitizes rat pancreatic islet cells to lysis by cytokines and cytotoxic cells. J autoimmunity 1990; 3 Suppl 1: 123-130.
30. Rabinovitch A, Sumoski W, Rajotte RV, Warnock GL. Cytotoxic effects of cytokines on human pancreatic islet cells in monolayer culture. J clinical endocrinology and metabolism 1990; 71(1): 152-6.
31. Jones EY, Fugger L, Strominger JL, Siebold C. MHC class II proteins and disease: a structural perspective. Nature reviews 2006; 6(4): 271-82.
32. Kantarova D, Buc M. Genetic susceptibility to type 1 diabetes mellitus in humans. Physiological research/Academia Scientiarum Bohemoslovaca 2007; 56(3): 255-66.
33. Maier LM, Wicker LS. Genetic susceptibility to type 1 diabetes. Current opinion in immunology 2005; 17(6): 601-8.
34. Cai CQ, Zhang T, Breslin MB, Giraud M, Lan MS. Both polymorphic variable number of tandem repeats and autoimmune regulator modulate differential expression of insulin in human thymic epithelial cells. Diabetes 2011; 60(1): 336-44.
35. Anderson MS, Venanzi ES, Chen Z, Berzins SP, Benoist C, Mathis D. The cellular mechanism of Aire control of T cell tolerance. Immunity 2005; 23(2): 227-39.
36. Fan Y, Rudert WA, Grupillo M, He J, Sisino G, Trucco M. Thymus-specific deletion of insulin induces autoimmune diabetes. EMBO J 2009; 28(18): 2812-24.
37. Vaziri-Sani F, Oak S, Radtke J, et al. ZnT8 autoantibody titers in type 1 diabetes patients decline rapidly after clinical onset. Autoimmunity 2010; 43(8): 598-606.
38. Verge CF, Gianani R, Kawasaki E, et al. Prediction of type I diabetes in first-degree relatives using a combination of insulin, GAD, and ICA512bdc/IA-2 autoantibodies. Diabetes 1996; 45(7): 926-33.
39. Verge CF, Howard NJ, Rowley MJ, et al. Anti-glutamate decarboxylase and other antibodies at the onset of childhood IDDM: a population-based study. Diabetologia 1994; 37(11): 1113-20.
40. Bingley PJ, Bonifacio E, Williams AJ, Genovese S, Bottazzo GF, Gale EA. Prediction of IDDM in the general population: strategies based on combinations of autoantibody markers. Diabetes 1997; 46(11): 1701-10.
41. Schlosser M, Mueller PW, Torn C, Bonifacio E, Bingley PJ. Diabetes Antibody Standardization Program: evaluation of assays for insulin autoantibodies. Diabetologia 2010; 53(12): 2611-20.
42. Chaillous L, Lefevre H, Thivolet C, et al. Oral insulin administration and residual beta-cell function in recent-onset type 1 diabetes: a multicentre randomised controlled trial. Diabete Insuline Orale group. Lancet 2000; 356(9229): 545-9.
43. Skyler JS, Krischer JP, Wolfsdorf J, et al. Effects of oral insulin in relatives of patients with type 1 diabetes: The Diabetes Prevention Trial--Type 1. Diabetes care 2005; 28(5): 1068-76.
44. Oral Insulin for Prevention of Diabetes in Relatives at Risk for Type 1 Diabetes Mellitus. ClincalTrials.gov; 2009 [updated October 5, 2009]; Available from: http://clinicaltrials.gov/ct2/show/NCT00419562.
45. Harrison LC, Honeyman MC, Steele CE, et al. Pancreatic beta-cell function and immune responses to insulin after administration of intranasal insulin to humans at risk for type 1 diabetes. Diabetes care 2004; 27(10): 2348-55.
46. Harrison LC, Dempsey-Collier M, Kramer DR, Takahashi K. Aerosol insulin induces regulatory CD8 gamma delta T cells that prevent murine insulin-dependent diabetes. J experimental medicine 1996; 184(6): 2167-74.
47. Agardh CD, Cilio CM, Lethagen A, et al. Clinical evidence for the safety of GAD65 immunomodulation in adult-onset autoimmune diabetes. J diabetes and its complications 2005; 19(4): 238-46.
48. Hinke SA. Diamyd, an alum-formulated recombinant human GAD65 for the prevention of autoimmune diabetes. Curr Opin Mol Ther 2008; 10(5): 516-25.
49. Ludvigsson J. GAD-alum (Diamyd)--a new concept for preservation of residual insulin secretion. Expert opinion on biological therapy 2010; 10(5): 787-99.
50. Kotani R, Nagata M, Moriyama H, et al. Detection of GAD65-reactive T-Cells in type 1 diabetes by immunoglobulin-free ELISPOT assays. Diabetes care 2002; 25(8): 1390-7.
51. Atkinson MA, Maclaren NK. The pathogenesis of insulin-dependent diabetes mellitus. N Engl J Med 1994 Nov 24; 331(21): 1428-36.
52. Delovitch TL, Singh B. The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity 1997; 7(6): 727-38.
53. Wicker LS, Todd JA, Peterson LB. Genetic control of autoimmune diabetes in the NOD mouse. Annual review of immunology 1995; 13: 179-200.
54. Durinovic-Bello I. Autoimmune diabetes: the role of T cells, MHC molecules and autoantigens. Autoimmunity 1998; 27(3): 159-77.
55. Abulafia-Lapid R, Elias D, Raz I, Keren-Zur Y, Atlan H, Cohen IR. T cell proliferative responses of type 1 diabetes patients and healthy individuals to human hsp60 and its peptides. J autoimmunity 1999; 12(2): 121-9.
56. Raz I, Avron A, Tamir M, et al. Treatment of new-onset type 1 diabetes with peptide DiaPep277 is safe and associated with preserved beta-cell function: extension of a randomized, double-blind, phase II trial. Diabetes/metabolism research and reviews 2007; 23(4): 292-8.
57. Raz I, Elias D, Avron A, Tamir M, Metzger M, Cohen IR. 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 2001 Nov 24; 358(9295): 1749-53.
58. Schloot NC, Meierhoff G, Lengyel C, et al. Effect of heat shock protein peptide DiaPep277 on beta-cell function in paediatric and adult patients with recent-onset diabetes mellitus type 1: two prospective, randomized, double-blind phase II trials. Diabetes/metabolism research and reviews 2007; 23(4): 276-85.
59. Huurman VA, van der Meide PE, Duinkerken G, et al. Immunological efficacy of heat shock protein 60 peptide DiaPep277 therapy in clinical type I diabetes. Clinical and experimental immunology 2008; 152(3): 488-97.
60. Di Lorenzo TP, Peakman M, Roep BO. Translational mini-review series on type 1 diabetes: Systematic analysis of T cell epitopes in autoimmune diabetes. Clinical and experimental immunology 2007; 148(1): 1-16.
61. Sloan-Lancaster J, Allen PM. Altered peptide ligand-induced partial T cell activation: molecular mechanisms and role in T cell biology. Annual review of immunology 1996; 14: 1-27.
62. Alleva DG, Crowe PD, Jin L, et al. A disease-associated cellular immune response in type 1 diabetics to an immunodominant epitope of insulin. J clinical investigation 2001; 107(2): 173-80.
63. Nicholson LB, Kuchroo VK. T cell recognition of self and altered self antigens. Critical reviews in immunology 1997; 17(5-6): 449-62.
64. Alleva DG, Gaur A, Jin L, 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 2002; 51(7): 2126-34.
65. Wong FS, Karttunen J, Dumont C, et al. Identification of an MHC class I-restricted autoantigen in type 1 diabetes by screening an organ-specific cDNA library. Nature medicine 1999; 5(9): 1026-31.
66. Alleva DG, Maki RA, Putnam AL, et al. Immunomodulation in type 1 diabetes by NBI-6024, an altered peptide ligand of the insulin B epitope. Scand J Immunol 2006; 63(1): 59-69.
67. Walter M, Philotheou A, Bonnici F, Ziegler AG, Jimenez R. No effect of the altered peptide ligand NBI-6024 on beta-cell residual function and insulin needs in new-onset type 1 diabetes. Diabetes care 2009; 32(11): 2036-40.
68. McLaughlin P, White CA, Grillo-Lopez AJ, Maloney DG. Clinical status and optimal use of rituximab for B-cell lymphomas. Oncology (Williston Park) 1998; 12(12): 1763-1769; discussion 9-70, 75-7.
69. Scott SD. Rituximab: a new therapeutic monoclonal antibody for non-Hodgkin's lymphoma. Cancer Pract 1998 May-Jun; 6(3): 195-197.
70. Edwards JC, Szczepanski L, Szechinski J, et al. Efficacy of B-cell-targeted therapy with rituximab in patients with rheumatoid arthritis. N Engl J Med 2004 Jun 17; 350(25): 2572-81.
71. Reis EA, Athanazio DA, Lima I, et al. NK and NKT cell dynamics after rituximab therapy for systemic lupus erythematosus and rheumatoid arthritis. Rheumatol Int 2009; 29(4): 469-75.
72. Suzuki K, Nagasawa H, Kameda H, et al. Severe acute thrombotic exacerbation in two cases with anti-phospholipid syndrome after retreatment with rituximab in phase I/II clinical trial for refractory systemic lupus erythematosus. Rheumatology (Oxford) 2009; 48(2): 198-9.
73. Xiu Y, Wong CP, Bouaziz JD, et al. B lymphocyte depletion by CD20 monoclonal antibody prevents diabetes in nonobese diabetic mice despite isotype-specific differences in Fc gamma R effector functions. J Immunol 2008 Mar 1; 180(5): 2863-75.
74. Hu CY, Rodriguez-Pinto D, Du W, et al. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J clinical investigation 2007; 117(12): 3857-67.
75. Pescovitz MD, Greenbaum CJ, Krause-Steinrauf H, et al. Rituximab, B-lymphocyte depletion, and preservation of beta-cell function. N Engl J Med 2009 Nov 26; 361(22): 2143-52.
76. Makhlouf L, Grey ST, Dong V, et al. Depleting anti-CD4 monoclonal antibody cures new-onset diabetes, prevents recurrent autoimmune diabetes, and delays allograft rejection in nonobese diabetic mice. Transplantation 2004 Apr 15; 77(7): 990-7.
77. Chatenoud L. Immune therapy for type 1 diabetes mellitus-what is unique about anti-CD3 antibodies? Nat Rev Endocrinol 2010; 6(3): 149-57.
78. Chatenoud L, Primo J, Bach JF. CD3 antibody-induced dominant self tolerance in overtly diabetic NOD mice. J Immunol 1997 Mar 15; 158(6): 2947-54.
79. Chatenoud L, Thervet E, Primo J, Bach JF. Anti-CD3 antibody induces long-term remission of overt autoimmunity in nonobese diabetic mice. Proceedings of the National Academy of Sciences of the United States of America 1994 Jan 4; 91(1): 123-7.
80. Belghith M, Bluestone JA, Barriot S, Megret J, Bach JF, Chatenoud L. TGF-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nature medicine 2003; 9(9): 1202-8.
81. Bisikirska B, Colgan J, Luban J, Bluestone JA, Herold KC. TCR stimulation with modified anti-CD3 mAb expands CD8+ T cell population and induces CD8+CD25+ Tregs. J clinical investigation 2005; 115(10): 2904-13.
82. Herold KC, Burton JB, Francois F, Poumian-Ruiz E, Glandt M, Bluestone JA. Activation of human T cells by FcR nonbinding anti-CD3 mAb, hOKT3gamma1(Ala-Ala). J clinical investigation 2003; 111(3): 409-18.
83. Keymeulen B, Vandemeulebroucke E, Ziegler AG, et al. Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes. N Engl J Med 2005; 352(25): 2598-608.
84. MacroGenics and Lilly Announce Pivotal Clinical Trial of Teplizumab Did Not Meet Primary Efficacy Endpoint. 2010; Available from: http://www.fiercepharma.com/press_releases/ macrogenics-and-lilly-announce-pivotal-clinical-trial-teplizumab-did-not-meet-primary.
85. Clarkson MR, Sayegh MH. T-cell costimulatory pathways in allograft rejection and tolerance. Transplantation 2005; 80(5): 555-563.
86. Lenschow DJ, Herold KC, Rhee L, et al. CD28/B7 regulation of Th1 and Th2 subsets in the development of autoimmune diabetes. Immunity 1996; 5(3): 285-93.
87. Steinman RM, Inaba K, Turley S, Pierre P, Mellman I. Antigen capture, processing, and presentation by dendritic cells: recent cell biological studies. Hum Immunol 1999; 60(7): 562-7.
88. Steinman RM. The control of immunity and tolerance by dendritic cell. Pathol Biol (Paris) 2003; 51(2): 59-60.
89. Hackstein H, Morelli AE, Thomson AW. Designer dendritic cells for tolerance induction: guided not misguided missiles. Trends Immunol 2001; 22(8): 437-42.
90. Morelli AE, Thomson AW. Dendritic cells: regulators of alloim-munity and opportunities for tolerance induction. Immunological reviews 2003; 196: 125-46.
91. Coates PT, Barratt-Boyes SM, Donnenberg AD, Morelli AE, Murphey-Corb M, Thomson AW. Strategies for preclinical evaluation of dendritic cell subsets for promotion of transplant tolerance in the nonhuman primate. Hum Immunol 2002; 63(10): 955-65.
92. Nouri-Shirazi M, Thomson AW. Dendritic cells as promoters of transplant tolerance. Expert opinion on biological therapy 2006; 6(4): 325-39.
93. Chen D, Sung R, Bromberg JS. Gene therapy in transplantation. Transpl Immunol 2002; 9(2-4): 301-14.
94. Giannoukakis N, Thomson A, Robbins P. Gene therapy in transplantation. Gene Ther 1999; 6(9): 1499-511.
95. Bottino R, Lemarchand P, Trucco M, Giannoukakis N. Gene- and cell-based therapeutics for type I diabetes mellitus. Gene Ther 2003; 10(10): 875-89.
96. Giannoukakis N, Trucco M. Gene therapy for type 1 diabetes. Am J Ther 2005; 12(6): 512-28.
97. Tarner IH, Fathman CG. The potential for gene therapy in the treatment of autoimmune disease. Clinical immunology (Orlando, Fla 2002; 104(3): 204-16.
98. Tarner IH, Slavin AJ, McBride J, et al. Treatment of autoimmune disease by adoptive cellular gene therapy. Annals of the New York Academy of Sciences 2003; 998: 512-9.
99. Trucco M, Robbins PD, Thomson AW, Giannoukakis N. Gene therapy strategies to prevent autoimmune disorders. Curr Gene Ther 2002; 2(3): 341-54.
100. Ma L, Qian S, Liang X, et al. Prevention of diabetes in NOD mice by administration of dendritic cells deficient in nuclear transcription factor-kappaB activity. Diabetes 2003; 52(8): 1976-85.
101. Machen J, Harnaha J, Lakomy R, Styche A, Trucco M, Giannoukakis N. Antisense oligonucleotides down-regulating costimulation confer diabetes-preventive properties to nonobese diabetic mouse dendritic cells. J Immunol 2004; 173(7): 4331-41.
102. Harnaha J, Machen J, Wright M, et al. Interleukin-7 is a survival factor for CD4+ CD25+ T-cells and is expressed by diabetes-suppressive dendritic cells. Diabetes 2006; 55(1): 158-70.
103. Phillips B, Nylander K, Harnaha J, et al. A microsphere-based vaccine prevents and reverses new-onset autoimmune diabetes. Diabetes 2008; 57(6): 1544-55.
104. Chen W. Dendritic cells and (CD4+)CD25+ T regulatory cells: crosstalk between two professionals in immunity versus tolerance. Front Biosci 2006; 11: 1360-70.
105. Hugues S, Boissonnas A, Amigorena S, Fetler L. The dynamics of dendritic cell-T cell interactions in priming and tolerance. Current opinion in immunology 2006; 18(4): 491-5.
106. Beissert S, Schwarz A, Schwarz T. Regulatory T cells. J Invest Dermatol 2006; 126(1): 15-24.
107. AH. DCs and cytokines cooperate for the induction of tregs. Ernst Schering Res Found Workshop 2006(56): 97-106.
108. Huber S, Schramm C. TGF-beta and CD4+CD25+ regulatory T cells. Front Biosci 2006; 11: 1014-23.
109. Lohr J, Knoechel B, Abbas AK. Regulatory T cells in the periphery. Immunological reviews 2006; 212: 149-62.
110. Roncarolo MG, Gregori S, Battaglia M, Bacchetta R, Fleischhauer K, Levings MK. Interleukin-10-secreting type 1 regulatory T cells in rodents and humans. Immunological reviews 2006; 212: 28-50.
111. Shevach EM, DiPaolo RA, Andersson J, Zhao DM, Stephens GL, Thornton AM. The lifestyle of naturally occurring CD4+ CD25+ Foxp3+ regulatory T cells. Immunological reviews 2006; 212: 60-73.
112. Tang Q, Bluestone JA. Regulatory T-cell physiology and application to treat autoimmunity. Immunological reviews 2006; 212: 217-37.
113. Verhagen J, Blaser K, Akdis CA, Akdis M. Mechanisms of allergen-specific immunotherapy: T-regulatory cells and more. Immunol Allergy Clin North Am 2006; 26(2): 207-231, vi.
114. Zhang L, Yi H, Xia XP, Zhao Y. Transforming growth factor-beta: an important role in CD4+CD25+ regulatory T cells and immune tolerance. Autoimmunity 2006; 39(4): 269-76.
115. Marguti I, Yamamoto GL, da Costa TB, Rizzo LV, de Moraes LV. Expansion of CD4+ CD25+ Foxp3+ T cells by bone marrow-derived dendritic cells. Immunology 2009; 127(1): 50-61.
116. Tarbell KV, Yamazaki S, Olson K, Toy P, Steinman RM. CD25+ CD4+ T cells, expanded with dendritic cells presenting a single autoantigenic peptide, suppress autoimmune diabetes. J experimental medicine 2004 Jun 7; 199(11): 1467-77.
117. Yamazaki S, Iyoda T, Tarbell K, et al. Direct expansion of functional CD25+ CD4+ regulatory T cells by antigen-processing dendritic cells. J experimental medicine 2003 Jul 21; 198(2): 235-47.
118. Giannoukakis N, Phillips, B.E., Finegold, D., Harnaha, J., Trucco, M. A phase I (safety) study of autologous tolerogenic dendritic cells in type 1 diabetes patients. Diabetes care 2011.
119. TIDM Immunotherapy Using CD4+CD127lo/-CD25+ Polyclonal Tregs. San Francisco: Clinicaltrials.gov; 2010 [updated Nov. 12, 2010; cited 2011 June 01, 2011]; Available from: http://clinicaltrials.gov/ct2/show/NCT01210664.
120. Phillips BE, Giannoukakis N. Autoimmune Diseases: Symptoms, Diagnosis and Treatment. Hauppauge: Nove Publishers 2010.