Exploiting apoptosis for therapeutic tolerance induction

Journal of Immunology

Volumn 191, Issue 11, 2013, Pages 5341-5346

  Getts, Daniel R ^a   McCarthy, Derrick P ^a   Miller, Stephen D ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CYTOKINE; INTERLEUKIN 10; PROTEIN PD L1; SCAVENGER RECEPTOR; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; APOPTOSIS; CLONAL ANERGY; CYTOKINE PRODUCTION; HOST CELL; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INNATE IMMUNITY; LEUKOCYTE; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; UPREGULATION;

EID: 84888348583     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302070     Document Type: Review

References (74)

1. Chatenoud, L., and J. A. Bluestone. 2007. CD3-specific antibodies: a portal to the treatment of autoimmunity. Nat. Rev. Immunol. 7: 622-632.
2. Kohm, A. P., D. M. Turley, and S. D. Miller. 2005. Targeting the TCR: T-cell receptor and peptide-specific tolerance-based strategies for restoring self-tolerance in CNS autoimmune disease. Int. Rev. Immunol. 24: 361-392.
3. Miller, S. D., D. M. Turley, and J. R. Podojil. 2007. Antigen-specific tolerance strategies for the prevention and treatment of autoimmune disease. Nat. Rev. Immunol. 7: 665-677.
4. Miller, S. D., R. P. Wetzig, and H. N. Claman. 1979. The induction of cell-mediated immunity and tolerance with protein antigens coupled to syngeneic lymphoid cells. J. Exp. Med. 149: 758-773.
5. Jenkins, M. K., and R. H. Schwartz. 1987. Antigen presentation by chemically modified splenocytes induces antigen-specific T cell unresponsiveness in vitro and in vivo. J. Exp. Med. 165: 302-319.
6. Luo, X., K. L. Pothoven, D. McCarthy, M. DeGutes, A. Martin, D. R. Getts, G. Xia, J. He, X. Zhang, D. B. Kaufman, and S. D. Miller. 2008. ECDI-fixed allogeneic splenocytes induce donor-specific tolerance for long-term survival of islet transplants via two distinct mechanisms. Proc. Natl. Acad. Sci. USA 105: 14527-14532.
7. Turley, D. M., and S. D. Miller. 2007. Peripheral tolerance induction using ethylenecarbodiimide-fixed APCs uses both direct and indirect mechanisms of antigen presentation for prevention of experimental autoimmune encephalomyelitis. J. Immunol. 178: 2212-2220.
8. Lutterotti, A., S. Yusef, A. Sputtek, K. Sturner, J.-P. Stellmann, P. Breiden, S. Reinhardt, C. Schulze, M. Bester, C. Heesen, et al. 2013. Antigen-specific tolerance by autologous myelin peptide-coupled cells: a phase 1 trial in multiple sclerosis. Sci. Transl. Med. 5: 188ra75.
9. Getts, D. R., D. M. Turley, C. E. Smith, C. T. Harp, D. McCarthy, E. M. Feeney, M. T. Getts, A. J. Martin, X. Luo, R. L. Terry, et al. 2011. Tolerance induced by apoptotic antigen-coupled leukocytes is induced by PD-L1+ and IL-10?producing splenic macrophages and maintained by T regulatory cells. J. Immunol. 187: 2405-2417.
10. Prasad, S., A. P. Kohm, J. S. McMahon, X. Luo, and S. D. Miller. 2012. Pathogenesis of NOD diabetes is initiated by reactivity to the insulin B chain 9-23 epitope and involves functional epitope spreading. J. Autoimmun. 39: 347-353.
11. Smarr, C. B., C. L. Hsu, A. J. Byrne, S. D. Miller, and P. J. Bryce. 2011. Antigen-fixed leukocytes tolerize Th2 responses in mouse models of allergy. J. Immunol. 187: 5090-5098.
12. Elliott, C., K. Wang, S. D. Miller, and R. Melvold. 1994. Ethylcarbodiimide as an agent for induction of specific transplant tolerance. Transplantation 58: 966-968.
13. Kaneko, K., A. E. Morelli, Z. Wang, and A. W. Thomson. 2003. Alloantigen presentation by ethylcarbodiimide-treated dendritic cells induces T cell hyporesponsiveness, and prolongs organ graft survival. Clin. Immunol. 108: 190-198.
14. Martin, A. J., D. McCarthy, C. Waltenbaugh, G. Goings, X. Luo, and S. D. Miller. 2010. Ethylenecarbodiimide-treated splenocytes carrying male CD4 epitopes confer histocompatibility Y chromosome antigen transplant protection by inhibiting CD154 upregulation. J. Immunol. 185: 3326-3336.
15. Wang, S., J. Tasch, T. Kheradmand, J. Ulaszek, S. Ely, X. Zhang, B. J. Hering, S. D. Miller, and X. Luo. 2013. Transient B-cell depletion combined with apoptotic donor splenocytes induces xeno-specific T- and B-cell tolerance to islet xenografts. Diabetes 62: 3143-3150.
16. Getts, M. T., B. S. Kim, and S. D. Miller. 2007. Differential outcome of tolerance induction in naive versus activated Theiler's virus epitope-specific CD8+ cytotoxic T cells. J. Virol. 81: 6584-6593.
17. Medawar, P. B. 1961. Immunological tolerance. Nature 189: 14-17.
18. Billingham, R. E., L. Brent, and P. B. Medawar. 1953. Actively acquired tolerance of foreign cells. Nature 172: 603-606.
19. Sulzberger, M. B. 1929. Hypersensitivities to arsphenamine in guinea pigs: experiments in prevention and in desensitization. Arch. Dermatol. Syphiol. 20: 669-697.
20. Chase, M. W. 1946. Inhibition of experimental drug allergy by prior feeding of the sensitizing agent. Proc. Soc. Exp. Biol. Med. 61: 257-259.
21. Landsteiner, K., and J. Jacobs. 1935. Studies on the sensitization of animals with simple chemical compounds. J. Exp. Med. 61: 643-656.
22. Battisto, J. R., and B. R. Bloom. 1966. Dual immunological unresponsiveness induced by cell membrane coupled hapten or antigen. Nature 212: 156-157.
23. Miller, S. D., and H. N. Claman. 1976. The induction of hapten-specific T cell tolerance by using hapten-modified lymphoid cells. I. Characteristics of tolerance induction. J. Immunol. 117: 1519-1526.
24. Doyle, M. V., E. Parks, and W. O. Weigle. 1976. Specific, transient suppression of the immune response by HGG tolerant spleen cells. II. Effector cells and target cells. J. Immunol. 117: 1152-1158.
25. Viorritto, I. C., N. P. Nikolov, and R. M. Siegel. 2007. Autoimmunity versus tolerance: can dying cells tip the balance? Clin. Immunol. 122: 125-134.
26. Barker, R. N., L. Erwig, W. P. Pearce, A. Devine, and A. J. Rees. 1999. Differential effects of necrotic or apoptotic cell uptake on antigen presentation by macrophages. Pathobiology 67: 302-305.
27. Webb, N. R., P. M. Connell, G. A. Graf, E. J. Smart, W. J. de Villiers, F. C. de Beer, and D. R. van der Westhuyzen. 1998. SR-BII, an isoform of the scavenger receptor BI containing an alternate cytoplasmic tail, mediates lipid transfer between high density lipoprotein and cells. J. Biol. Chem. 273: 15241-15248.
28. Getts, D. R., A. J. Martin, D. P. McCarthy, R. L. Terry, Z. N. Hunter, W. T. Yap, M. T. Getts, M. Pleiss, X. Luo, N. J. King, et al. 2012. Microparticles bearing encephalitogenic peptides induce T-cell tolerance and ameliorate experimental autoimmune encephalomyelitis. Nat. Biotechnol. 30: 1217-1224.
29. Arredouani, M. S., A. Palecanda, H. Koziel, Y. C. Huang, A. Imrich, T. H. Sulahian, Y. Y. Ning, Z. Yang, T. Pikkarainen, M. Sankala, et al. 2005. MARCO is the major binding receptor for unopsonized particles and bacteria on human alveolar macrophages. J. Immunol. 175: 6058-6064.
30. Józefowski, S., M. Arredouani, T. Sulahian, and L. Kobzik. 2005. Disparate regulation and function of the class A scavenger receptors SR-AI/II and MARCO. J. Immunol. 175: 8032-8041.
31. Li, D., G. Romain, A. L. Flamar, D. Duluc, M. Dullaers, X. H. Li, S. Zurawski, N. Bosquet, A. K. Palucka, R. Le Grand, et al. 2012. Targeting self- and foreign antigens to dendritic cells via DC-ASGPR generates IL-10?producing suppressive CD4+ T cells. J. Exp. Med. 209: 109-121.
32. Gray, M., K. Miles, D. Salter, D. Gray, and J. Savill. 2007. Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc. Natl. Acad. Sci. USA 104: 14080-14085.
33. Rosenblum, M. D., I. K. Gratz, J. S. Paw, and A. K. Abbas. 2012. Treating human autoimmunity: current practice and future prospects. Sci. Transl. Med. 4: 125sr121.
34. Freeman, G. J., A. J. Long, Y. Iwai, K. Bourque, T. Chernova, H. Nishimura, L. J. Fitz, N. Malenkovich, T. Okazaki, M. C. Byrne, et al. 2000. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192: 1027-1034.
35. Zinselmeyer, B. H., S. Heydari, C. Sacristán, D. Nayak, M. Cammer, J. Herz, X. Cheng, S. J. Davis, M. L. Dustin, and D. B. McGavern. 2013. PD-1 promotes immune exhaustion by inducing antiviral T cell motility paralysis. J. Exp. Med. 210: 757-774.
36. Morelli, A. E., A. T. Larregina, W. J. Shufesky, A. F. Zahorchak, A. J. Logar, G. D. Papworth, Z. Wang, S. C. Watkins, L. D. Falo, Jr., and A. W. Thomson. 2003. Internalization of circulating apoptotic cells by splenic marginal zone dendritic cells: dependence on complement receptors and effect on cytokine production. Blood 101: 611-620.
37. Backer, R., T. Schwandt, M. Greuter, M. Oosting, F. Jüngerkes, T. Tüting, L. Boon, T. O'Toole, G. Kraal, A. Limmer, and J. M. den Haan. 2010. Effective collaboration between marginal metallophilic macrophages and CD8+ dendritic cells in the generation of cytotoxic T cells. Proc. Natl. Acad. Sci. USA 107: 216-221.
38. Bretscher, P., and M. Cohn. 1970. A theory of self-nonself discrimination. Science 169: 1042-1049.
39. Schwartz, R. H. 1990. A cell culture model for T lymphocyte clonal anergy. Science 248: 1349-1356.
40. Harding, F. A., J. G. McArthur, J. A. Gross, D. H. Raulet, and J. P. Allison. 1992. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature 356: 607-609.
41. Vandenbark, A. A., D. Barnes, T. Finn, D. N. Bourdette, R. Whitham, I. Robey, J. Kaleeba, B. F. Bebo, Jr., S. D. Miller, H. Offner, and Y. K. Chou. 2000. Differential susceptibility of human T(h)1 versus T(h) 2 cells to induction of anergy and apoptosis by ECDI/antigen-coupled antigen-presenting cells. Int. Immunol. 12: 57-66.
42. Linsley, P. S., W. Brady, M. Urnes, L. S. Grosmaire, N. K. Damle, and J. A. Ledbetter. 1991. CTLA-4 is a second receptor for the B cell activation antigen B7. J. Exp. Med. 174: 561-569.
43. Linsley, P. S., J. L. Greene, P. Tan, J. Bradshaw, J. A. Ledbetter, C. Anasetti, and N. K. Damle. 1992. Coexpression and functional cooperation of CTLA-4 and CD28 on activated T lymphocytes. J. Exp. Med. 176: 1595-1604.
44. Walunas, T. L., D. J. Lenschow, C. Y. Bakker, P. S. Linsley, G. J. Freeman, J. M. Green, C. B. Thompson, and J. A. Bluestone. 1994. CTLA-4 can function as a negative regulator of T cell activation. Immunity 1: 405-413.
45. Lühder, F., P. Höglund, J. P. Allison, C. Benoist, and D. Mathis. 1998. Cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) regulates the unfolding of autoimmune diabetes. J. Exp. Med. 187: 427-432.
46. Karandikar, N. J., T. N. Eagar, C. L. Vanderlugt, J. A. Bluestone, and S. D. Miller. 2000. CTLA-4 downregulates epitope spreading and mediates remission in relapsing experimental autoimmune encephalomyelitis. J. Neuroimmunol. 109: 173-180.
47. Fife, B. T., I. Guleria, M. Gubbels Bupp, T. N. Eagar, Q. Tang, H. Bour-Jordan, H. Yagita, M. Azuma, M. H. Sayegh, and J. A. Bluestone. 2006. Insulin-induced remission in new-onset NOD mice is maintained by the PD-1 ?PD-L1 pathway. J. Exp. Med. 203: 2737-2747.
48. Eagar, T. N., N. J. Karandikar, J. A. Bluestone, and S. D. Miller. 2002. The role of CTLA-4 in induction and maintenance of peripheral T cell tolerance. Eur. J. Immunol. 32: 972-981.
49. Walunas, T. L., A. I. Sperling, R. Khattri, C. B. Thompson, and J. A. Bluestone. 1996. CD28 expression is not essential for positive and negative selection of thymocytes or peripheral T cell tolerance. J. Immunol. 156: 1006-1013.
50. Keir, M. E., S. C. Liang, I. Guleria, Y. E. Latchman, A. Qipo, L. A. Albacker, M. Koulmanda, G. J. Freeman, M. H. Sayegh, and A. H. Sharpe. 2006. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J. Exp. Med. 203: 883-895.
51. Fife, B. T., K. E. Pauken, T. N. Eagar, T. Obu, J. Wu, Q. Tang, M. Azuma, M. F. Krummel, and J. A. Bluestone. 2009. Interactions between PD-1 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat. Immunol. 10: 1185-1192.
52. Friedl, P., A. T. den Boer, and M. Gunzer. 2005. Tuning immune responses: diversity and adaptation of the immunological synapse. Nat. Rev. Immunol. 5: 32-545.
53. Cemerski, S., J. Das, E. Giurisato, M. A. Markiewicz, P. M. Allen, A. K. Chakraborty, and A. S. Shaw. 2008. The balance between T cell receptor signaling and degradation at the center of the immunological synapse is determined by antigen quality. Immunity 29: 414-422.
54. Cemerski, S., J. Das, J. Locasale, P. Arnold, E. Giurisato, M. A. Markiewicz, D. Fremont, P. M. Allen, A. K. Chakraborty, and A. S. Shaw. 2007. The stimulatory potency of T cell antigens is influenced by the formation of the immunological synapse. Immunity 26: 345-355.
55. Mossman, K. D., G. Campi, J. T. Groves, and M. L. Dustin. 2005. Altered TCR signaling from geometrically repatterned immunological synapses. Science 310: 1191-1193.
56. Bromley, S. K., A. Iaboni, S. J. Davis, A. Whitty, J. M. Green, A. S. Shaw, A. Weiss, and M. L. Dustin. 2001. The immunological synapse and CD28?CD80 interactions. Nat. Immunol. 2: 1159-1166.
57. Acuto, O., and F. Michel. 2003. CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat. Rev. Immunol. 3: 939-951.
58. Yokosuka, T., W. Kobayashi, K. Sakata-Sogawa, M. Takamatsu, A. Hashimoto-Tane, M. L. Dustin, M. Tokunaga, and T. Saito. 2008. Spatiotemporal regulation of T cell costimulation by TCR-CD28 microclusters and protein kinase C theta translocation. Immunity 29: 589-601.
59. Schneider, H., J. Downey, A. Smith, B. H. Zinselmeyer, C. Rush, J. M. Brewer, B. Wei, N. Hogg, P. Garside, and C. E. Rudd. 2006. Reversal of the TCR stop signal by CTLA-4. Science 313: 1972-1975.
60. Yokosuka, T., W. Kobayashi, M. Takamatsu, K. Sakata-Sogawa, H. Zeng, A. Hashimoto-Tane, H. Yagita, M. Tokunaga, and T. Saito. 2010. Spatiotemporal basis of CTLA-4 costimulatory molecule-mediated negative regulation of T cell activation. Immunity 33: 326-339.
61. Yokosuka, T., M. Takamatsu, W. Kobayashi-Imanishi, A. Hashimoto-Tane, M. Azuma, and T. Saito. 2012. Programmed cell death 1 forms negative costimulatory microclusters that directly inhibit T cell receptor signaling by recruiting phosphatase SHP2. J. Exp. Med. 209: 1201-1217.
62. Bowen, F., J. Haluskey, and H. Quill. 1995. Altered CD40 ligand induction in tolerant T lymphocytes. Eur. J. Immunol. 25: 2830-2834.
63. Cella, M., D. Scheidegger, K. Palmer-Lehmann, P. Lane, A. Lanzavecchia, and G. Alber. 1996. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 184: 747-752.
64. Guy, C. S., K. M. Vignali, J. Temirov, M. L. Bettini, A. E. Overacre, M. Smeltzer, H. Zhang, J. B. Huppa, Y. H. Tsai, C. Lobry, et al. 2013. Distinct TCR signaling pathways drive proliferation and cytokine production in T cells. Nat. Immunol. 14: 262-270.
65. Schwartz, R. H. 2003. T cell anergy. Annu. Rev. Immunol. 21: 305-334.
66. Fontenot, J. D., J. P. Rasmussen, M. A. Gavin, and A. Y. Rudensky. 2005. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6: 1142-1151.
67. Meagher, C., Q. Tang, B. T. Fife, H. Bour-Jordan, J. Wu, C. Pardoux, M. Bi, K. Melli, and J. A. Bluestone. 2008. Spontaneous development of a pancreatic exocrine disease in CD28-deficient NOD mice. J. Immunol. 180: 7793-7803.
68. Zhang, H., J. R. Podojil, X. Luo, and S. D. Miller. 2008. Intrinsic and induced regulation of the age-associated onset of spontaneous experimental autoimmune encephalomyelitis. J. Immunol. 181: 4638-4647.
69. Eagar, T. N., D. M. Turley, J. Padilla, N. J. Karandikar, L. J. Tan, J. A. Bluestone, and S. D. Miller. 2004. CTLA-4 regulates expansion and differentiation of Th1 cells following induction of peripheral T cell tolerance. J. Immunol. 172: 7442-7450.
70. Meuer, S. C., R. E. Hussey, D. A. Cantrell, J. C. Hodgdon, S. F. Schlossman, K. A. Smith, and E. L. Reinherz. 1984. Triggering of the T3-Ti antigen-receptor complex results in clonal T-cell proliferation through an interleukin 2-dependent autocrine pathway. Proc. Natl. Acad. Sci. USA 81: 1509-1513.
71. Lindstein, T., C. H. June, J. A. Ledbetter, G. Stella, and C. B. Thompson. 1989. Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science 244: 339-343.
72. Jenkins, M. K., D. M. Pardoll, J. Mizuguchi, T. M. Chused, and R. H. Schwartz. 1987. Molecular events in the induction of a nonresponsive state in interleukin 2-producing helper T-lymphocyte clones. Proc. Natl. Acad. Sci. USA 84: 5409-5413.
73. Qureshi, O. S., Y. Zheng, K. Nakamura, K. Attridge, C. Manzotti, E. M. Schmidt, J. Baker, L. E. Jeffery, S. Kaur, Z. Briggs, et al. 2011. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science 332: 600-603.
74. Rosenblum, M. D., I. K. Gratz, J. S. Paw, K. Lee, A. Marshak-Rothstein, and A. K. Abbas. 2011. Response to self antigen imprints regulatory memory in tissues. Nature 480: 538-542.