Antisense oligonucleotides down-regulating costimulation confer diabetes-preventive properties to nonobese diabetic mouse dendritic cells

Journal of Immunology

Volumn 173, Issue 7, 2004, Pages 4331-4341

  Machen, Jennifer ^a   Harnaha, Jo ^a   Lakomy, Robert ^a   Styche, Alexis ^a   Trucco, Massimo ^a   Giannoukakis, Nick ^a,b  

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

^b CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; B7 ANTIGEN; CD4 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; INTERLEUKIN 2 RECEPTOR;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL INTERACTION; CONTROLLED STUDY; DENDRITIC CELL; DIABETES MELLITUS; DOWN REGULATION; FLOW CYTOMETRY; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SCID MOUSE; SPLEEN CELL; T LYMPHOCYTE ACTIVATION;

EID: 4644297765     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.7.4331     Document Type: Article

References (86)

1. Bach, J. F. 1994. Insulin-dependent diabetes mellitus as an autoimmune disease. Endocr. Rev. 15:516.
2. Eisenbarth, G. S. 1993. Molecular aspects of the etiology of type I diabetes mellitus. J. Diabetes Complications 7:142.
3. Steinman, R. M., and M. C. Nussenzweig. 2002. Inaugural article: avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc. Natl. Acad. Sci. USA 99:351.
4. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392:245.
5. Steptoe, R. J., and A. W. Thomson. 1996. Dendritic cells and tolerance induction. Clin. Exp. Immunol. 105:397.
6. Morel, P. A., A. C. Vasquez, and M. Feili-Hariri. 1999. Immunobiology of DC in NOD mice. J. Leukocyte Biol. 66:276.
7. Rosmalen, J. G., P. J. Leenen, J. D. Katz, J. S. Voerman, and H. A. Drexhage. 1997. Dendritic cells in the autoimmune insulitis in NOD mouse models of diabetes. Adv. Exp. Med. Biol. 417:291.
8. Clare-Salzler, M. J., J. Brooks, A. Chai, K. Van Herle, and C. Anderson. 1992. Prevention of diabetes in nonobese diabetic mice by dendritic cell transfer. J. Clin. Invest. 90:741.
9. Steinman, R. M., M. Pack, and K. Inaba. 1997. Dendritic cell development and maturation. Adv. Exp. Med. Biol. 417:1.
10. Lanzavecchia, A., and F. Sallusto. 2001. Regulation of T cell immunity by dendritic cells. Cell 106:263.
11. Thomson, A. W., and L. Lu. 1999. Dendritic cells as regulators of immune reactivity: implications for transplantation. Transplantation 68:1.
12. Lu, L., S. Qian, P. A. Hershberger, W. A. Rudert, D. H. Lynch, and A. W. Thomson. 1997. Fas ligand (CD95L) and B7 expression on dendritic cells provide counter-regulatory signals for T cell survival and proliferation. J. Immunol. 158:5676.
13. Lu, L., S. Qian, P. Hershberger, W. A. Rudert, Y. Li, F. G. Chambers, T. E. Starzl, D. H. Lynch, and A. W. Thomson. 1997. Blocking of the B7-CD28 pathway increases apoptosis induced in activated T cells by in vitro-generated CD95L (FasL) positive dendritic cells. Transplant. Proc. 29:1094.
14. +) dendritic cells to kill alloactivated T cells. Adv. Exp. Med. Biol. 417:275.
15. McBride, J. M., and C. G. Fathman. 2002. A complicated relationship: fulfilling the interactive needs of the T lymphocyte and the dendritic cell. Pharmacogenomics J. 2:367.
16. Feili-Hariri, M., X. Dong, S. M. Alber, S. C. Watkins, R. D. Salter, and P. A. Morel. 1999. Immunotherapy of NOD mice with bone marrow-derived dendritic cells. Diabetes 48:2300.
17. Feili-Hariri, M., D. H. Falkner, A. Gambotto, G. D. Papworth, S. C. Watkins, P. D. Robbins, and P. A. Morel. 2003. Dendritic cells transduced to express interleukin-4 prevent diabetes in nonobese diabetic mice with advanced insulitis. Hum. Gene Ther. 14:13.
18. Adorini, L., G. Penna, N. Giarratana, and M. Uskokovic. 2003. Tolerogenic dendritic cells induced by vitamin D receptor ligands enhance regulatory T cells inhibiting allograft rejection and autoimmune diseases. J. Cell. Biochem. 88:227.
19. Papaccio, G., F. Nicoletti, F. A. Pisanti, K. Bendtzen, and M. Galdieri. 2000. Prevention of spontaneous autoimmune diabetes in NOD mice by transferring in vitro antigen-pulsed syngeneic dendritic cells. Endocrinology 141:1500.
20. Shinomiya, M., S. M. Fazle Akbar, H. Shinomiya, and M. Onji. 1999. Transfer of dendritic cells (DC) ex vivo stimulated with interferon-γ (IFN-γ) down-modulates autoimmune diabetes in non-obese diabetic (NOD) mice. Clin. Exp. Immunol. 117:38.
21. Weaver, D. J., Jr., B. Poligone, T. Bui, U. M. Abdel-Motal, A. S. Baldwin, Jr., and R. Tisch. 2001. Dendritic cells from nonobese diabetic mice exhibit a defect in NF-κB regulation due to a hyperactive IκB kinase. J. Immunol. 167:1461.
22. Poligone, B., D. J. Weaver, Jr., P. Sen, A. S. Baldwin, Jr., and R. Tisch. 2002. Elevated NF-κB activation in nonobese diabetic mouse dendritic cells results in enhanced APC function. J. Immunol. 168:188.
23. Sen, P., S. Bhattacharyya, M. Wallet, C. P. Wong, B. Poligone, M. Sen, A. S. Baldwin, Jr., and R. Tisch. 2003. NF-κB hyperactivation has differential effects on the APC function of nonobese diabetic mouse macrophages. J. Immunol. 170:1770.
24. Ma, L., S. Qian, X. Liang, L. Wang, J. E. Woodward, N. Giannoukakis, P. D. Robbins, S. Bertera, M. Trucco, J. J. Fung, and L. Lu. 2003. Prevention of diabetes in NOD mice by administration of dendritic cells deficient in nuclear transcription factor-κB activity. Diabetes 52:1976.
25. Lenschow, D. J., Y. Zeng, J. R. Thistlethwaite, A. Montag, W. Brady, M. G. Gibson, P. S. Linsley, and J. A. Bluestone. 1992. Long-term survival of xenogeneic pancreatic islet grafts induced by CTLA4Ig. Science 257:789.
26. Chahine, A. A., M. Yu, M. M. McKeman, C. Stoeckert, and H. T. Lau. 1995. Immunomodulation of pancreatic islet allografts in mice with CTLA4Ig secreting muscle cells. Transplantation 59:1313.
27. Lenschow, D. J., S. C. Ho, H. Sattar, L. Rhee, G. Gray, N. Nabavi, K. C. Herold, and J. A. Bluestone. 1995. Differential effects of anti-B7-I and anti-B7-2 monoclonal antibody treatment on the development of diabetes in the nonobese diabetic mouse. J. Exp. Med. 181:1145.
28. Lew, A. M., J. L. Brady, A. Silva, J. E. Coligan, and H. M. Georgiou. 1996. Secretion of CTLA4Ig by an SV40 T antigen-transformed islet cell line inhibits graft rejection against the neoantigen. Transplantation 62:83.
29. Sayegh, M. H., E. Akalin, W. W. Hancock, M. E. Russell, C. B. Carpenter, P. S. Linsley, and L. A. Turka. 1995. CD28-B7 blockade after alloantigenic challenge in vivo inhibits Th1 cytokines but spares TbZ J. Exp. Med. 181:1869.
30. Steurer, W., P. W. Nickerson, A. W. Steele, J. Steiger, X. X. Zheng, and T. B. Strom. 1995. Ex vivo coating of islet cell allografts with murine CTLA4/Fc promotes graft tolerance. J. Immunol. 155:1165.
31. Woodward, J. E., A. L. Bayer, K. D. Chavin, M. L. Blue, and P. Baliga. 1998. T-cell alterations in cardiac allograft recipients after B7 (CD80 and CD86) blockade. Transplantation 66:14.
32. Chahine, A. A., M. Yu, M. McKernan, C. Stoeckert, P. S. Linsley, and H. T. Lau. 1994. Local CTLA4Ig synergizes with one-dose anti-LFA-1 to achieve long-term acceptance of pancreatic islet allografts. Transplant. Proc. 26:3296.
33. Lenschow, D. J., Y. Zeng, K. S. Hathcock, L. A. Zuckerman, G. Freeman, J. R. Thistlethwaite, G. S. Gray, R. J. Hodes, and J. A. Bluestone. 1995. Inhibition of transplant rejection following treatment with anti-B7-2 and anti-B7-1 antibodies. Transplantation 60:1171.
34. Azuma, H., A. Chandraker, K. Nadeau, W. W. Hancock, C. B. Carpenter, N. L. Tilney, and M. H. Sayegh. 1996. Blockade of T-cell costimulation prevents development of experimental chronic renal allograft rejection. Proc. Natl. Acad. Sci. USA 93:12439.
35. Bluestone, J. A. 1996. Costimulation and its role in organ transplantation. Clin. Transplant. 10:104.
36. Bolling, S. F., H. Lin, R. Q. Wei, and L. A. Turka. 1996. Preventing allograft rejection with CTLA4Ig: effect of donor-specific transfusion route or timing. J. Heart Lung Transplant. 15:928.
37. Cabrian, K. M., K. K. Berry, W. W. Shuford, R. S. Mittler, J. N. Rodgers, and P. S. Linsley. 1996. Suppression of T-cell-dependent immune responses in monkeys by CTLA4Ig. Transplant. Proc. 28:3261.
38. Gribben, J. G., E. C. Guinan, V. A. Boussiotis, X. Y. Ke, L. Linsley, C. Sieff, G. S. Gray, G. J. Freeman, and L. M. Nadler. 1996. Complete blockade of B7 family-mediated costimulation is necessary to induce human alloantigen-specific anergy: a method to ameliorate graft- versus-host disease and extend the donor pool. Blood 87:4887.
39. Judge, T. A., A. Tang, L. M. Spain, J. Deans-Gratiot, M. H. Sayegh, and L. A. Turka. 1996. The in vivo mechanism of action of CTLA4Ig. J. Immunol. 156:2294.
40. Larsen, C. P., E. T. Elwood, D. Z. Alexander, S. C. Ritchie, R. Hendrix, C. Tucker-Burden, H. R. Cho, A. Aruffo, D. Hollenbaugh, P. S. Linsley, K. J. Winn, and T. C. Pearson. 1996. Long-term acceptance of skin and cardiac allografts after blocking CD40 and CD28 pathways. Nature 381:434.
41. Daikh, D., D. Wofsy, and J. B. Imboden. 1997. The CD28-B7 costimulatory pathway and its role in autoimmune disease. J. Leukocyte Biol 62:156.
42. Gainer, A. L., G. S. Korbutt, R. V. Rajotte, G. L. Warnock, and J. F. Elliott. 1997. Expression of CTLA4-Ig by biolistically transfected mouse islets promotes islet allograft survival. Transplantation 63:1017.
43. Hale. D. A., R. Gottschalk, T. Maki, and A. P. Monaco. 1997. Use of CTLA4-Ig in combination with conventional immunosuppressive agents to prolong allograft survival. Transplantation 64:897.
44. Hayashi, S., Y. Namii, T. Kozima, T. Kobayashi, I. Yokoyama, I. Saito, H. Hamada, S. Ohtsuka, K. Uchida, and H. Takagi. 1997. Effect of CTLA4-Ig gene transfer using adenoviral vector in organ and cell transplantation. Transplant. Proc. 29:2212.
45. Levisetti, M. G., P. A. Padrid, G. L. Szot, N. Mittal, S. M. Meehan, C. L. Wardrip, G. S. Gray, D. S. Brace, J. R. Thistlethwaite, Jr., and J. A. Bluestone. 1997. Immunosuppressive effects of human CTLA4Ig in a non-human primate model of allogeneic pancreatic islet transplantation. J. Immunol. 159:5187.
46. Roy-Chaudhury, P., P. W. Nickerson, R. C. Manfro, X. X. Zheng, J. Steiger, Y. S. Li, and T. B. Strom. 1997. CTLA4Ig attenuates accelerated rejection (pre-sensitization) in the mouse islet allograft model. Transplantation 64:172.
47. Sun, H., V. Subbotin, C. Chen, A. Aitouche, L. A. Valdivia, M. H. Sayegh, P. S. Linsley, J. J. Fung, T. E. Starzl, and A. S. Rao. 1997. Prevention of chronic rejection in mouse aortic allografts by combined treatment with CTLA4-Ig and anti-CD40 ligand monoclonal antibody. Transplantation 64:1838.
48. Tu, Y., A. Rehman, and M. W. Flye. 1997. CTLA4-Ig treatment prolongs rat orthotopic liver graft survival. Transplant. Proc. 29:1036.
49. Weber, C. J., M. K. Hagler, J. T. Chryssochoos, J. A. Kapp, G. S. Korbutt, R. V. Rajotte, and P. S. Linsley. 1997. CTLA4-Ig-prolongs survival of microencapsulated neonatal porcine islet xenografts in diabetic NOD mice. Cell Transplant. 6:505.
50. Yi-qun, Z., K. Lorre, M. de Boer, and J. L. Ceuppens. 1997. B7-blocking agents, alone or in combination with cyclosporin A, induce antigen-specific anergy of human memory T cells. J. Immunol 158:4734.
51. Gainer, A. L., W. L. Suarez-Pinzon, W. P. Min, C. Hancock-Friesen, G. S. Korbutt, R. V. Rajotte, A. Rabinovitch, G. L. Warnock, and J. F. Elliott. 1998. Prolongation of allograft survival of transfected islets expressing human CTLA4-Ig, human soluble Fas ligand or a combination of the two. Transplant. Proc. 30:534.
52. Guo, Z., D. Mital, Y. Y. Mo, Y. Tian, J. Shen, A. S. Chong, P. Foster, H. Sankary, L. McChesney, S. C. Jensik, and J. W. Williams. 1998. Effect of gene gun-mediated CTLA4IG and Fas ligand gene transfection on concordant xenogeneic islet graft rejection. Transplant. Proc. 30:589.
53. Hong, J. C., and B. D. Kahan. 2000. Immunosuppressive agents in organ transplantation: past, present, and future. Semin. Nephrol. 20:108.
54. Wekerle, T., P. Blaha, F. Langer, M. Schmid, and F. Muehlbacher. 2002. Tolerance through bone marrow transplantation with costimulation blockade. Transplant Immunol. 9:125.
55. Fu, F., Y. Li, S. Qian, L. Lu, F. D. Chambers, T. E. Starzl, J. J. Fung, and A. W. Thomson. 1997. Costimulatory molecule-deficient dendritic cell progenitors induce T cell hyporesponsiveness in vitro and prolong the survival of vascularized cardiac allografts. Transplant. Proc. 29:1310.
56. -) prolong cardiac allograft survival in nonimmunosuppressed recipients. Transplantation 62:659.
57. -) induce alloantigen-specific hyporesponsiveness in murine T lymphocytes. Transplantation 60:1539.
58. Hamaguchi, K., H. R. Gaskins, and E. H. Leiter. 1991. NIT-1, a pancreatic β-cell line established from a transgenic NOD/Lt mouse. Diabetes 40:842.
59. Reid, B. D., H. Y. Qin, S. Prange, E. Lee-Chan, Q. Yu, J. F. Elliott, and B. Singh. 1997. Modulation and detection of IDDM by membrane associated antigens from the islet β cell line NIT. J. Autoimmun. 10:27.
60. + T cells of non-obese diabetic mice. J. Immunol. 151:1723.
61. Giannoukakis, N., C. A. Bonham, S. Qian, Z. Chen, L. Peng, J. Harnaha, W. Li, A. W. Thomson, J. J. Fung, P. D. Robbins, and L. Lu. 2000. Prolongation of cardiac allograft survival using dendritic cells treated with NF-κB decoy oligodeoxyribonucleotides. Mol. Ther. 1:430.
62. Cameron, M. J., G. A. Arreaza, and T. L. Delovitch. 1997. Cytokine- and co-stimulation-mediated therapy of IDDM. Crit. Rev. Immunol. 17:537.
63. Cameron, M. J., G. A. Arreaza, P. Zucker, S. W. Chensue, R. M. Strieter, S. Chakrabarti, and T. L. Delovitch. 1997. IL-4 prevents insulins and insulin-dependent diabetes mellitus in nonobese diabetic mice by potentiation of regulatory T helper-2 cell function. J. Immunol. 159:4686.
64. Sharif, S., G. A. Arreaza, P. Zucker, and T. L. Delovitch. 2002. Regulatory natural killer T cells protect against spontaneous and recurrent type 1 diabetes. Ann. NY Acad. Sci. 958:77.
65. + T cells regulate the expansion of peripheral CD4 T cells through the production of IL-10. J. Immunol. 166:3008.
66. Kara, M., C. I. Kingsley, M. Niimi, S. Read, S. E. Turvey, A. R. Bushell, P. J. Morris, F. Powrie, and K. J. Wood. 2001. IL-10 is required for regulatory T cells to mediate tolerance to alloantigens in vivo. J. Immunol. 166:3789.
67. + T cells with regulatory properties isolated from peripheral blood. J. Exp. Med. 193:1285.
68. Chatenoud, L., B. Salomon, and J. A. Bluestone. 2001. Suppressor T cells-they're back and critical for regulation of autoimmunity! Immunol. Rev. 182:149.
69. Bach, J. F., and L. Chatenoud. 2001. Tolerance to islet autoantigens in type 1 diabetes. Annu. Rev. Immunol. 19:131.
70. Shevach, E. M., R. S. McHugh, A. M. Thomton, C. Piccirillo, K. Natarajan, and D. H. Margulies. 2001. Control of autoimmunity by regulatory T cells. Adv. Exp. Med. Biol 490:21.
71. + suppressor T cells. Immunol. Rev. 182:58.
72. + T cells. Microbes Infect. 3:919.
73. + immunoregulatory T cells is antigen nonspecific. J. Immunol. 164:183.
74. Feili-Hariri, M., and P. A. Morel. 2001. Phenotypic and functional characteristics of BM-derived DC from NOD and non-diabetes-prone strains. Clin. Immunol. 98:133.
75. + T cells, expanded with dendritic cells presenting a single autoantigenic peptide, suppress autoimmune diabetes. J. Exp. Med. 199:1467.
76. + regulatory T cells by antigen-processing dendritic cells. J. Exp. Med. 198:235.
77. Ruedl, C., P. Koebel, M. Bachmann, M. Hess, and K. Karjalainen. 2000. Anatomical origin of dendritic cells determines their life span in peripheral lymph nodes. J. Immunol. 165:4910.
78. Lee, W. C., C. Zhong, S. Qian, Y. Wan, J. Gauldie, Z. Mi, P. D. Robbins, A. W. Thomson, and L. Lu. 1998. Phenotype, function, and in vivo migration and survival of allogeneic dendritic cell progenitors genetically engineered to express TGF-β. Transplantation 66:1810.
79. Wang, B., Y. B. Geng, and C. R. Wang. 2001. CDI-restricted NK T cells protect nonobese diabetic mice from developing diabetes. J. Exp. Med. 194:313.
80. Laloux, V., L. Beaudoin, D. Jeske, C. Carnaud, and A. Lehuen. 2001. NK T cell-induced protection against diabetes in Vα14-Jα281 transgenic nonobese diabetic mice is associated with a Th2 shift circumscribed regionally to the islets and functionally to islet autoantigen. J. Immunol. 166:3749.
81. + T regulatory cells dependent on ICOS promote regulation of effector cells in the prediabetic lesion. J. Exp. Med. 199:1479.
82. Tang, Q., K. J. Henriksen, M. Bi, E. B. Finger, G. Szot, J. Ye, E. L. Masteller, H. McDevitt, M. Bonyhadi, and J. A. Bluestone. 2004. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J. Exp. Med. 199:1455.
83. + regulatory T cells. J. Immunol. 171:3348.
84. Adorini, L. 2003. Tolerogenic dendritic cells induced by vitamin D receptor ligands enhance regulatory T cells inhibiting autoimmune diabetes. Ann. NY Acad. Sci. 987:258.
85. Bottino, R., P. Lemarchand, M. Trucco, and N. Giannoukakis. 2003. Gene- and cell-based therapeutics for type I diabetes mellitus. Gene Ther. 10:875.
86. Trucco, M., P. D. Robbins, A. W. Thomson, and N. Giannoukakis. 2002. Gene therapy strategies to prevent autoimmune disorders. Curr. Gene Ther. 2:341.