Regulation of the tolerogenic function of steady-state DCs

European Journal of Immunology

Volumn 44, Issue 4, 2014, Pages 927-933

  Probst, Hans Christian ^a,b   Muth, Sabine ^a,b   Schild, Hansjörg ^a,b  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

DC maturation; Dendritic cells; Peripheral T cell tolerance; Steady state DCs

Indexed keywords

CYCLIC AMP; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; RETINOIC ACID; TOLL LIKE RECEPTOR 4;

ARTICLE; AUTOIMMUNITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL MATURATION; DENDRITIC CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STEADY STATE; T LYMPHOCYTE ACTIVATION; VIDEO MICROSCOPY;

DC MATURATION; DENDRITIC CELLS; PERIPHERAL T-CELL TOLERANCE; STEADY-STATE DCS;

ANTIGEN PRESENTATION; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; DENDRITIC CELLS; HUMANS; IMMUNE TOLERANCE; MODELS, IMMUNOLOGICAL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY;

EID: 84898012891     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343862     Document Type: Article

References (75)

1. Steinman, R. M. and Cohn, Z. A., Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J. Exp. Med. 1973. 137: 1142-1162.
2. Takeuchi, O. and Akira, S., Pattern recognition receptors and inflammation. Cell 2010. 140: 805-820.
3. Broz, P. and Monack, D. M., Newly described pattern recognition receptors team up against intracellular pathogens. Nat. Rev. Immunol. 2013. 13: 551-565.
4. Zelenay, S. and Reis Sousa, C., Adaptive immunity after cell death. Trends Immunol. 2013. 34: 329-335.
5. Banchereau, J., Briere, F., Caux, C., Davoust, J., Lebecque, S., Liu, Y. J., Pulendran, B. et al., Immunobiology of dendritic cells. Annu. Rev. Immunol. 2000. 18: 767-811.
6. Mattei, F., Schiavoni, G. and Tough, D. F., Regulation of immune cell homeostasis by type I interferons. Cytokine Growth Factor Rev. 2010. 21: 227-236.
7. + T cell expansion with variable dependence on type I IFN. J. Exp. Med. 2004. 199: 775-784.
8. Frenz, T., Waibler, Z., Hofmann, J., Hamdorf, M., Lantermann, M., Reizis, B., Tovey, M. G. et al., Concomitant type I IFN receptor-triggering of T cells and of DC is required to promote maximal modified vaccinia virus Ankara-induced T-cell expansion. Eur. J. Immunol. 2010. 40: 2769-2777.
9. Diamond, M. S., Kinder, M., Matsushita, H., Mashayekhi, M., Dunn, G. P., Archambault, J. M., Lee, H. et al., Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J. Exp. Med. 2011. 208: 1989-2003.
10. Cella, M., Scheidegger, D., Palmer-Lehmann, K., Lane, P., Lanzavecchia, A. and Alber, G., 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. 1996. 184: 747-752.
11. Di Rosa, F., Ramaswamy, S., Ridge, J. P. and Matzinger, P., On the lifespan of virgin T lymphocytes. J. Immunol. 1999. 163: 1253-1257.
12. Inaba, K., Metlay, J. P., Crowley, M. T. and Steinman, R. M., Dendritic cells pulsed with protein antigens in vitro can prime antigen-specific, MHC-restricted T cells in situ. J. Exp. Med. 1990. 172: 631-640.
13. Gallucci, S., Lolkema, M. and Matzinger, P., Natural adjuvants: endogenous activators of dendritic cells. Nat. Med. 1999. 5: 1249-1255.
14. Hawiger, D., Inaba, K., Dorsett, Y., Guo, M., Mahnke, K., Rivera, M., Ravetch, J. V. et al., Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 2001. 194: 769-779.
15. + T cell tolerance. J. Exp. Med. 2002. 196: 1627-1638.
16. + T cell tolerance. Immunity 2003. 18: 713-720.
17. + T cell tolerance through PD-1 and CTLA-4. Nat. Immunol. 2005. 6: 280-286.
18. Yamazaki, T., Akiba, H., Iwai, H., Matsuda, H., Aoki, M., Tanno, Y., Shin, T. et al., Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 2002. 169: 5538-5545.
19. Mellor, A. L. and Munn, D. H., IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 2004. 4: 762-774.
20. Belladonna, M. L., Grohmann, U., Guidetti, P., Volpi, C., Bianchi, R., Fioretti, M. C., Schwarcz, R. et al., Kynurenine pathway enzymes in dendritic cells initiate tolerogenesis in the absence of functional IDO. J. Immunol. 2006. 177: 130-137.
21. Pallotta, M. T., Orabona, C., Volpi, C., Vacca, C., Belladonna, M. L., Bianchi, R., Servillo, G. et al., Indoleamine 2, 3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells. Nat. Immunol. 2011. 12: 870-878.
22. Birnberg, T., Bar-On, L., Sapoznikov, A., Caton, M. L., Cervantes-Barragan, L., Makia, D., Krauthgamer, R. et al., Lack of conventional dendritic cells is compatible with normal development and T cell homeostasis, but causes myeloid proliferative syndrome. Immunity 2008. 29: 986-997.
23. Darrasse-Jeze, G., Deroubaix, S., Mouquet, H., Victora, G. D., Eisenreich, T., Yao, K. H., Masilamani, R. F. et al., Feedback control of regulatory T cell homeostasis by dendritic cells in vivo. J. Exp. Med. 2009. 206: 1853-1862.
24. Bar-On, L., Birnberg, T., Kim, K. W. and Jung, S., Dendritic cell-restricted CD80/86 deficiency results in peripheral regulatory T-cell reduction but is not associated with lymphocyte hyperactivation. Eur. J. Immunol. 2011. 41: 291-298.
25. + regulatory T cells in Foxp3.LuciDTR mice. J. Immunol. 2010. 184: 1810-1820.
26. Abbas, A. K., Benoist, C., Bluestone, J. A., Campbell, D. J., Ghosh, S., Hori, S., Jiang, S. et al., Regulatory T cells: recommendations to simplify the nomenclature. Nat. Immunol. 2013. 14: 307-308.
27. Josefowicz, S. Z., Niec, R. E., Kim, H. Y., Treuting, P., Chinen, T., Zheng, Y., Umetsu, D. T. et al., Extrathymically generated regulatory T cells control mucosal TH2 inflammation. Nature 2011. 482: 395-399.
28. Kretschmer, K., Apostolou, I., Hawiger, D., Khazaie, K., Nussenzweig, M. C. and von Boehmer, H., Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 2005. 6: 1219-1227.
29. + regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 2007. 204: 1757-1764.
30. Strainic, M. G., Shevach, E. M., An, F., Lin, F. and Medof, M. E., Absence of signaling into CD4(+) cells via C3aR and C5aR enables autoinductive TGF-beta1 signaling and induction of Foxp3(+) regulatory T cells. Nat. Immunol. 2012. 14: 162-171.
31. Guilliams, M., Crozat, K., Henri, S., Tamoutounour, S., Grenot, P., Devilard, E., de Bovis, B. et al., Skin-draining lymph nodes contain dermis-derived CD103(-) dendritic cells that constitutively produce retinoic acid and induce Foxp3(+) regulatory T cells. Blood 2010. 115: 1958-1968.
32. Idoyaga, J., Fiorese, C., Zbytnuik, L., Lubkin, A., Miller, J., Malissen, B., Mucida, D. et al., Specialized role of migratory dendritic cells in peripheral tolerance induction. J. Clin. Invest. 2013. 123: 844-854.
33. Vitali, C., Mingozzi, F., Broggi, A., Barresi, S., Zolezzi, F., Bayry, J., Raimondi, G. et al., Migratory, and not lymphoid-resident, dendritic cells maintain peripheral self-tolerance and prevent autoimmunity via induction of iTreg cells. Blood 2012. 120: 1237-1245.
34. + regulatory T cells. J. Immunol. 2008. 181: 6923-6933.
35. Manicassamy, S., Ravindran, R., Deng, J., Oluoch, H., Denning, T. L., Kasturi, S. P., Rosenthal, K. M. et al., Toll-like receptor 2-dependent induction of vitamin A-metabolizing enzymes in dendritic cells promotes T regulatory responses and inhibits autoimmunity. Nat. Med. 2009. 15: 401-409.
36. Hammer, G. E., Turer, E. E., Taylor, K. E., Fang, C. J., Advincula, R., Oshima, S., Barrera, J. et al., Expression of A20 by dendritic cells preserves immune homeostasis and prevents colitis and spondyloarthritis. Nat. Immunol. 2011. 12: 1184-1193.
37. Srokowski, C. C., Masri, J., Hovelmeyer, N., Krembel, A. K., Tertilt, C., Strand, D., Mahnke, K. et al., Naturally occurring short splice variant of CYLD positively regulates dendritic cell function. Blood 2009. 113: 5891-5895.
38. Kaneko, T., Saito, Y., Kotani, T., Okazawa, H., Iwamura, H., Sato-Hashimoto, M., Kanazawa, Y. et al., Dendritic cell-specific ablation of the protein tyrosine phosphatase Shp1 promotes Th1 cell differentiation and induces autoimmunity. J. Immunol. 2012. 188: 5397-5407.
39. Ramachandran, I. R., Song, W., Lapteva, N., Seethammagari, M., Slawin, K. M., Spencer, D. M. and Levitt, J. M., The phosphatase SRC homology region 2 domain-containing phosphatase-1 is an intrinsic central regulator of dendritic cell function. J. Immunol. 2011. 186: 3934-3945.
40. Kim, J. M., Rasmussen, J. P. and Rudensky, A. Y., Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat. Immunol. 2007. 8: 191-197.
41. + T-cell tolerance induced by steady-state dendritic cells. Proc. Natl. Acad. Sci. USA 2010. 107: 199-203.
42. Liu, K., Victora, G. D., Schwickert, T. A., Guermonprez, P., Meredith, M. M., Yao, K., Chu, F. F. et al., In vivo analysis of dendritic cell development and homeostasis. Science 2009. 324: 392-397.
43. Miloud, T., Fiegler, N., Suffner, J., Hammerling, G. J. and Garbi, N., Organ-specific cellular requirements for in vivo dendritic cell generation. J. Immunol. 2012. 188: 1125-1135.
44. + T-cell recognition results in impaired peripheral tolerance and fatal cytotoxic T-cell mediated autoimmunity. Proc. Natl. Acad. Sci. USA 2012. 109: 9059-9064.
45. Saito, Y., Boddupalli, C. S., Borsotti, C. and Manz, M. G., Dendritic cell homeostasis is maintained by nonhematopoietic and T-cell-produced Flt3-ligand in steady state and during immune responses. Eur. J. Immunol. 2013. 43: 1651-1658.
46. + T-cell response via inhibition of IL-12 production by DCs. Eur. J. Immunol. 2013. 43: 439-446.
47. Han, W. G., Schuurhuis, D. H., Fu, N., Camps, M., van Duivenvoorde, L. M., Louis-Plence, P., Franken, K. L. et al., DC-induced CD8(+) T-cell response is inhibited by MHC class II-dependent DX5(+)CD4(+) Treg. Eur. J. Immunol. 2009. 39: 1765-1773.
48. + T cell receptors. Immunity 2004. 21: 267-277.
49. Moran, A. E., Holzapfel, K. L., Xing, Y., Cunningham, N. R., Maltzman, J. S., Punt, J. and Hogquist, K. A., T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J. Exp. Med. 2011. 208: 1279-1289.
50. Josefowicz, S. Z., Lu, L. F. and Rudensky, A. Y., Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 2012. 30: 531-564.
51. + regulatory T cell function. Science 2008. 322: 271-275.
52. Qureshi, O. S., Zheng, Y., Nakamura, K., Attridge, K., Manzotti, C., Schmidt, E. M., Baker, J. et al., Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science 2011. 332: 600-603.
53. Fallarino, F., Grohmann, U., Hwang, K. W., Orabona, C., Vacca, C., Bianchi, R., Belladonna, M. L. et al., Modulation of tryptophan catabolism by regulatory T cells. Nat. Immunol. 2003. 4: 1206-1212.
54. Liang, B., Workman, C., Lee, J., Chew, C., Dale, B. M., Colonna, L., Flores, M. et al., Regulatory T cells inhibit dendritic cells by lymphocyte activation gene-3 engagement of MHC class II. J. Immunol. 2008. 180: 5916-5926.
55. + T cells induce perforin-dependent dendritic cell death in tumor-draining lymph nodes. Immunity 2010. 32: 266-278.
56. + natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc. Natl. Acad. Sci. USA 2008. 105: 10113-10118.
57. Li, M. O. and Flavell, R. A., TGF-beta: a master of all T cell trades. Cell 2008. 134: 392-404.
58. Ramalingam, R., Larmonier, C. B., Thurston, R. D., Midura-Kiela, M. T., Zheng, S. G., Ghishan, F. K. and Kiela, P. R., Dendritic cell-specific disruption of TGF-beta receptor II leads to altered regulatory T cell phenotype and spontaneous multiorgan autoimmunity. J. Immunol. 2012. 189: 3878-3893.
59. Laouar, Y., Town, T., Jeng, D., Tran, E., Wan, Y., Kuchroo, V. K. and Flavell, R. A., TGF-beta signaling in dendritic cells is a prerequisite for the control of autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 2008. 105: 10865-10870.
60. Li, M. O., Wan, Y. Y. and Flavell, R. A., T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity 2007. 26: 579-591.
61. Nakamura, K., Kitani, A. and Strober, W., Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J. Exp. Med. 2001. 194: 629-644.
62. Gutcher, I., Donkor, M. K., Ma, Q., Rudensky, A. Y., Flavell, R. A. and Li, M. O., Autocrine transforming growth factor-beta1 promotes in vivo Th17 cell differentiation. Immunity 2011. 34: 396-408.
63. Kambayashi, T., Wallin, R. P. and Ljunggren, H. G., cAMP-elevating agents suppress dendritic cell function. J. Leukoc. Biol. 2001. 70: 903-910.
64. Deaglio, S., Dwyer, K. M., Gao, W., Friedman, D., Usheva, A., Erat, A., Chen, J. F. et al., Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 2007. 204: 1257-1265.
65. Challier, J., Bruniquel, D., Sewell, A. K. and Laugel, B., Adenosine and cAMP signalling skew human dendritic cell differentiation towards a tolerogenic phenotype with defective CD8(+) T-cell priming capacity. Immunology 2013. 138: 402-410.
66. Bopp, T., Becker, C., Klein, M., Klein-Hessling, S., Palmetshofer, A., Serfling, E., Heib, V. et al., Cyclic adenosine monophosphate is a key component of regulatory T cell-mediated suppression. J. Exp. Med. 2007. 204: 1303-1310.
67. Fassbender, M., Gerlitzki, B., Ullrich, N., Lupp, C., Klein, M., Radsak, M. P., Schmitt, E. et al., Cyclic adenosine monophosphate and IL-10 coordinately contribute to nTreg cell-mediated suppression of dendritic cell activation. Cell. Immunol. 2010. 265: 91-96.
68. Bodor, J., Bopp, T., Vaeth, M., Klein, M., Serfling, E., Hunig, T., Becker, C. et al., Cyclic AMP underpins suppression by regulatory T cells. Eur. J. Immunol. 2012. 42: 1375-1384.
69. + T cell tolerance and permits effective immunity. Immunity 2008. 29: 934-946.
70. Muth, S., Schutze, K., Hain, T., Yagita, H., Schild, H. and Probst, H. C., A CD40/CD40L feedback loop drives the breakdown of CD8 T-cell tolerance following depletion of suppressive CD4 T cells. Eur. J. Immunol. 2014. 44:1099-1107.
71. Kool, M., van Loo, G., Waelput, W., de Prijck, S., Muskens, F., Sze, M., van Praet, J. et al., The ubiquitin-editing protein A20 prevents dendritic cell activation, recognition of apoptotic cells, and systemic autoimmunity. Immunity 2011. 35: 82-96.
72. Chinen, T., Volchkov, P. Y., Chervonsky, A. V. and Rudensky, A. Y., A critical role for regulatory T cell-mediated control of inflammation in the absence of commensal microbiota. J. Exp. Med. 2010. 207: 2323-2330.
73. Yu, P., Lubben, W., Slomka, H., Gebler, J., Konert, M., Cai, C., Neubrandt, L. et al., Nucleic acid-sensing Toll-like receptors are essential for the control of endogenous retrovirus viremia and ERV-induced tumors. Immunity 2012. 37: 867-879.
74. Shi, Y., Evans, J. E. and Rock, K. L., Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 2003. 425: 516-521.
75. Sancho, D., Joffre, O. P., Keller, A. M., Rogers, N. C., Martinez, D., Hernanz-Falcon, P., Rosewell, I. et al., Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 2009. 458: 899-903.