Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD4+ T cells

Journal of Immunology

Volumn 184, Issue 4, 2010, Pages 1765-1775

  Torres Aguilar, Honorio ^a   Aguilar Ruiz, Sergio R ^a   González Pérez, Gabriela ^a   Munguía, Rosario ^a   Bajaña, Sandra ^a,b   Meraz Ríos, Marco A ^a   Sánchez Torres, Carmen ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIBODY; IMMUNOGLOBULIN G ANTIBODY; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TRANSCRIPTION FACTOR FOXP3; B LYMPHOCYTE ANTIGEN; CYTOKINE; EPITOPE; HLA ANTIGEN CLASS 2; IL10 PROTEIN, HUMAN; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 10; PROSTAGLANDIN E2; THROMBOSPONDIN 1;

ALLORECOGNITION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN SPECIFICITY; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; GRAFT SURVIVAL; IMMUNOLOGICAL PARAMETERS; IMMUNOLOGICAL TOLERANCE; INHIBITION KINETICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SKIN GRAFT; SURVIVAL TIME; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; CD4+ T LYMPHOCYTE; CELL CULTURE; CELL DIFFERENTIATION; CLASSIFICATION; CLONAL ANERGY; COMPARATIVE STUDY; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INVARIANT CHAIN; MACROPHAGE; METABOLISM; PHYSIOLOGY; REGULATORY T LYMPHOCYTE;

ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; CLONAL ANERGY; CYTOKINES; DENDRITIC CELLS; DINOPROSTONE; EPITOPES, T-LYMPHOCYTE; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IMMUNE TOLERANCE; IMMUNOLOGIC MEMORY; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKIN-10; MACROPHAGES; T-LYMPHOCYTES, REGULATORY; THROMBOSPONDIN 1;

EID: 77949893984     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902133     Document Type: Article

References (50)

1. Moser, M. 2003. Dendritic cells in immunity and tolerance-do they display opposite functions? Immunity 19: 5-8.
2. Steinman, R. M., D. Hawiger, and M. C. Nussenzweig. 2003. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21: 685-711.
3. Morelli, A. E., and A. W. Thomson. 2007. Tolerogenic dendritic cells and the quest for transplant tolerance. Nat. Rev. Immunol. 7: 610-621.
4. Dhodapkar, M. V., R. M. Steinman, J. Krasovsky, C. Munz, and N. Bhardwaj. 2001. Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J. Exp. Med. 193: 233-238.
5. Hawiger, D., K. Inaba, Y. Dorsett, M. Guo, K. Mahnke, M. Rivera, J. V. Ravetch, R. M. Steinman, and M. C. Nussenzweig. 2001. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 194: 769-779.
6. Roncarolo, M. G., M. K. Levings, and C. Traversari. 2001. Differentiation of T regulatory cells by immature dendritic cells. J. Exp. Med. 193: F5-F9.
7. Menges, M., S. Rössner, C. Voigtländer, H. Schindler, N. A. Kukutsch, C. Bogdan, K. Erb, G. Schuler, and M. B. Lutz. 2002. Repetitive injections of dendritic cells matured with tumor necrosis factor a induce antigen-specific protection of mice from autoimmunity. J. Exp. Med. 195: 15-21.
8. Hadeiba, H., T. Sato, A. Habtezion, C. Oderup, J. Pan, and E. C. Butcher. 2008. CCR9 expression defines tolerogenic plasmacytoid dendritic cells able to suppress acute graft-versus-host disease. Nat. Immunol. 9: 1253-1260.
9. Sato, K., N. Yamashita, and T. Matsuyama. 2002. Human peripheral blood monocyte-derived interleukin-10-induced semi-mature dendritic cells induce anergic CD4(+) and CD8(+) T cells via presentation of the internalized soluble antigen and cross-presentation of the phagocytosed necrotic cellular fragments. Cell. Immunol. 215: 186-194.
10. Steinbrink, K., E. Graulich, S. Kubsch, J. Knop, and A. H. Enk. 2002. CD4(+) and CD8(+) anergic T cells induced by interleukin-10-treated human dendritic cells display antigen-specific suppressor activity. Blood 99: 2468-2476.
11. Akbari, O., R. H. DeKruyff, and D. T. Umetsu. 2001. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat. Immunol. 2: 725-731.
12. Sato, K., N. Yamashita, M. Baba, and T. Matsuyama. 2003. Modified myeloid dendritic cells act as regulatory dendritic cells to induce anergic and regulatory T cells. Blood 101: 3581-3589.
13. Geissmann, F., P. Revy, A. Regnault, Y. Lepelletier, M. Dy, N. Brousse, S. Amigorena, O. Hermine, and A. Durandy. 1999. TGF-b 1 prevents the non-cognate maturation of human dendritic Langerhans cells. J. Immunol. 162: 4567-4575.
14. low/neg accessory cells with dendritic-cell features. Blood 108: 218-227.
15. Gonzalez-Rey, E., A. Chorny, A. Fernandez-Martin, D. Ganea, and M. Delgado. 2006. Vasoactive intestinal peptide generates human tolerogenic dendritic cells that induce CD4 and CD8 regulatory T cells. Blood 107: 3632-3638.
16. Penna, G., S. Amuchastegui, N. Giarratana, K. C. Daniel, M. Vulcano, S. Sozzani, and L. Adorini. 2007. 1,25-Dihydroxyvitamin D3 selectively modulates tolerogenic properties in myeloid but not plasmacytoid dendritic cells. J. Immunol. 178: 145-153.
17. Woltman, A. M., S. W. van der Kooij, J. W. de Fijter, and C. van Kooten. 2006. Maturation-resistant dendritic cells induce hyporesponsiveness in alloreactive CD45RA+ and CD45RO+ T-cell populations. Am. J. Transplant. 6: 2580-2591.
18. Gerner, M. Y., and M. F. Mescher. 2009. Antigen processing and MHC-II presentation by dermal and tumor-infiltrating dendritic cells. J. Immunol. 182: 2726-2737.
19. Zhang, Q., Y. Chen, R. L. Fairchild, P. S. Heeger, and A. Valujskikh. 2006. Lymphoid sequestration of alloreactive memory CD4 T cells promotes cardiac allograft survival. J. Immunol. 176: 770-777. (Pubitemid 43099673)
20. Heeger, P. S., N. S. Greenspan, S. Kuhlenschmidt, C. Dejelo, D. E. Hricik, J. A. Schulak, and M. Tary-Lehmann. 1999. Pretransplant frequency of donorspecific, IFN-γ-producing lymphocytes is a manifestation of immunologic memory and correlates with the risk of posttransplant rejection episodes. J. Immunol. 163: 2267-2275.
21. Vu, M. D., M. R. Clarkson, H. Yagita, L. A. Turka, M. H. Sayegh, and X. C. Li. 2006. Critical, but conditional, role of OX40 in memory T cell-mediated rejection. J. Immunol. 176: 1394-1401.
22. Elyaman, W., P. Kivisäkk, J. Reddy, T. Chitnis, K. Raddassi, J. Imitola, E. Bradshaw, V. K. Kuchroo, H. Yagita, M. H. Sayegh, and S. J. Khoury. 2008. Distinct functions of autoreactive memory and effector CD4+ T cells in experimental autoimmune encephalomyelitis. Am. J. Pathol. 173: 411-422.
23. Mirshahidi, S., C. T. Huang, and S. Sadegh-Nasseri. 2001. Anergy in peripheral memory CD4(+) T cells induced by low avidity engagement of T cell receptor. J. Exp. Med. 194: 719-731.
24. den Boer, A. T., G. J. van Mierlo, M. F. Fransen, C. J. Melief, R. Offringa, and R. E. Toes. 2004. The tumoricidal activity of memory CD8+ T cells is hampered by persistent systemic antigen, but full functional capacity is regained in an antigen-free environment. J. Immunol. 172: 6074-6079.
25. high cells suppress proliferative memory lymphocyte responses to herpes simplex virus type 2. J. Virol. 80: 8271-8273.
26. Anderson, A. E., B. L. Sayers, M. A. Haniffa, D. J. Swan, J. Diboll, X. N. Wang, J. D. Isaacs, and C. M. Hilkens. 2008. Differential regulation of naïve and memory CD4+ T cells by alternatively activated dendritic cells. J. Leukoc. Biol. 84: 124-133.
27. Gavin, M. A., J. P. Rasmussen, J. D. Fontenot, V. Vasta, V. C. Manganiello, J. A. Beavo, and A. Y. Rudensky. 2007. Foxp3-dependent programme of regulatory T-cell differentiation. Nature 445: 771-775.
28. Grimbert, P., S. Bouguermouh, N. Baba, T. Nakajima, Z. Allakhverdi, D. Braun, H. Saito, M. Rubio, G. Delespesse, and M. Sarfati. 2006. Thrombospondin/CD47 interaction: a pathway to generate regulatory T cells from human CD4+ CD25- T cells in response to inflammation. J. Immunol. 177: 3534-3541.
29. Deaglio, S., K. M. Dwyer, W. Gao, D. Friedman, A. Usheva, A. Erat, J. F. Chen, K. Enjyoji, J. Linden, M. Oukka, et al. 2007. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204: 1257-1265.
30. Zarek, P. E., C. T. Huang, E. R. Lutz, J. Kowalski, M. R. Horton, J. Linden, C. G. Drake, and J. D. Powell. 2008. A2A receptor signaling promotes peripheral tolerance by inducing T-cell anergy and the generation of adaptive regulatory T cells. Blood 111: 251-259.
31. Mazzoni, A., V. Bronte, A. Visintin, J. H. Spitzer, E. Apolloni, P. Serafini, P. Zanovello, and D. M. Segal. 2002. Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism. J. Immunol. 168: 689-695.
32. Chomarat, P., J. Banchereau, J. Davoust, and A. K. Palucka. 2000. IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat. Immunol. 1: 510-514.
33. Allavena, P., L. Piemonti, D. Longoni, S. Bernasconi, A. Stoppacciaro, L. Ruco, and A. Mantovani. 1998. IL-10 prevents the differentiation of monocytes to dendritic cells but promotes their maturation to macrophages. Eur. J. Immunol. 28: 359-369.
34. Kitani, A., I. Fuss, K. Nakamura, F. Kumaki, T. Usui, and W. Strober. 2003. Transforming growth factor (TGF)-β1-producing regulatory T cells induce Smad-mediated interleukin 10 secretion that facilitates coordinated immunoregulatory activity and amelioration of TGF-β1-mediated fibrosis. J. Exp. Med. 198: 1179-1188.
35. Anderson, A. E., D. J. Swan, B. L. Sayers, R. A. Harry, A. M. Patterson, A. von Delwig, J. H. Robinson, J. D. Isaacs, and C. M. U. Hilkens. 2009. LPS activation is required for migratory activity and antigen presentation by tolerogenic dendritic cells. J. Leukoc. Biol. 85: 243-250.
36. Suberville, S., A. Bellocq, I. Peguillet, O. Lantz, P. Stordeur, B. Fouqueray, and L. Baud. 2001. Transforming growth factor-β inhibits interleukin-10 synthesis by human monocytic cells. Eur. Cytokine Netw. 12: 141-146.
37. Wang, J., A. Ioan-Facsinay, E. I. van der Voort, T. W. Huizinga, and R. E. Toes. 2007. Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur. J. Immunol. 37: 129-138.
38. Liu, W., A. L. Putnam, Z. Xu-Yu, G. L. Szot, M. R. Lee, S. Zhu, P. A. Gottlieb, P. Kapranov, T. R. Gingeras, B. Fazekas de St Groth, et al. 2006. CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J. Exp. Med. 203: 1701-1711.
39. Battaglia, M., S. Gregori, R. Bacchetta, and M. G. Roncarolo. 2006. Tr1 cells: from discovery to their clinical application. Semin. Immunol. 18: 120-127.
40. Velten, F. W., K. Duperrier, J. Bohlender, P. Metharom, and S. Goerdt. 2004. A gene signature of inhibitory MHC receptors identifies a BDCA3(+) subset of IL-10-induced dendritic cells with reduced allostimulatory capacity in vitro. Eur. J. Immunol. 34: 2800-2811.
41. Gray, C. P., P. Arosio, and P. Hersey. 2002. Heavy chain ferritin activates regulatory T cells by induction of changes in dendritic cells. Blood 99: 3326-3334.
42. Novitskiy, S. V., S. Ryzhov, R. Zaynagetdinov, A. E. Goldstein, Y. Huang, O. Y. Tikhomirov, M. R. Blackburn, I. Biaggioni, D. P. Carbone, I. Feoktistov, and M. M. Dikov. 2008. Adenosine receptors in regulation of dendritic cell differentiation and function. Blood 112: 1822-1831.
43. Pouliot, M., M. E. Fiset, M. Massé, P. H. Naccache, and P. Borgeat. 2002. Adenosine up-regulates cyclooxygenase-2 in human granulocytes: impact on the balance of eicosanoid generation. J. Immunol. 169: 5279-5286. (Pubitemid 35217200)
44. Harizi, H., and N. Gualde. 2006. Pivotal role of PGE2 and IL-10 in the crossregulation of dendritic cell-derived inflammatory mediators. Cell. Mol. Immunol. 3: 271-277.
45. Beppu, R., K. Nakamura, H. Miyajima-Uchida, M. Kuroki, P. D. Khare, Y. Yamauchi, Y. Yamashita, T. Shirakusa, and M. Kuroki. 2001. Soluble thrombospondin-1 suppresses T cell proliferation and enhances IL-10 secretion by antigen presenting cells stimulated with phytohemagglutinin. Immunol. Invest. 30: 143-156.
46. Doyen, V., M. Rubio, D. Braun, T. Nakajima, J. Abe, H. Saito, G. Delespesse, and M. Sarfati. 2003. Thrombospondin 1 is an autocrine negative regulator of human dendritic cell activation. J. Exp. Med. 198: 1277-1283.
47. Chamuleau, M. E. D., Y. Souwer, S. M. Van Ham, A. Zevenbergen, T. M. Westers, J. Berkhof, C. J. L. M. Meijer, A. A. van de Loosdrecht, and G. J. Ossenkoppele. 2004. Class II-associated invariant chain peptide expression on myeloid leukemic blasts predicts poor clinical outcome. Cancer Res. 64: 5546-5550.
48. Glazier, K. S., S. B. Hake, H. M. Tobin, A. Chadburn, E. J. Schattner, and L. K. Denzin. 2002. Germinal center B cells regulate their capability to present antigen by modulation of HLA-DO. J. Exp. Med. 195: 1063-1069.
49. Röhn, T. A., M. Boes, D. Wolters, S. Spindeldreher, B. Müller, H. Langen, H. Ploegh, A. B. Vogt, and H. Kropshofer. 2004. Upregulation of the CLIP self peptide on mature dendritic cells antagonizes T helper type 1 polarization. Nat. Immunol. 5: 909-918.
50. Hornell, T. M., T. Burster, F. L. Jahnsen, A. Pashine, M. T. Ochoa, J. J. Harding, C. Macaubas, A. W. Lee, R. L. Modlin, and E. D. Mellins. 2006. Human dendritic cell expression of HLA-DO is subset specific and regulated by maturation. J. Immunol. 176: 3536-3547.