Costimulatory molecules on immunogenic versus tolerogenic human dendritic cells

Frontiers in Immunology

Volumn 4, Issue APR, 2013, Pages

  Hubo, Mario ^a   Trinschek, Bettina ^a   Kryczanowsky, Fanny ^a   Tuettenberg, Andrea ^a   Steinbrink, Kerstin ^a   Jonuleit, Helmut ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

Costimulation; Dendritic cells; IL 10; Immunity; Inhibitory molecules; Regulatory T cell; Tolerance

Indexed keywords

B7 ANTIGEN; BIOLOGIC FACTORS AND AGENTS ACTING ON THE IMMUNE SYSTEM; CD40 ANTIGEN; CD40 LIGAND; CD86 ANTIGEN; COSTIMULATORY MOLECULE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE T CELL COSTIMULATOR LIGAND; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 4; INTERLEUKIN 6; JANUS KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 14; OX40 LIGAND; PHOSPHATIDYLINOSITOL 3 KINASE; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN KINASE B; PROTEIN KINASE TYK2; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; DENDRITIC CELL; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; MONOCYTE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; TOLEROGENIC DENDRITIC CELL;

EID: 84883716144     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00082     Document Type: Article

References (128)

1. Akbari, O., DeKruyff, R. H., and Umetsu, D. T. (2001). Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat. Immunol. 2, 725-731.
2. Anguille, S., Smits, E. L. J. M., Cools, N., Goossens, H., Berneman, Z. N., and Van Tendeloo, V. F. I. (2009). Short-term cultured, interleukin-15 differentiated dendritic cells have potent immunostimulatory properties. J. Transl. Med. 7, 109.
3. Banchereau, J., and Steinman, R. M. (1998). Dendritic cells and the control of immunity. Nature 392, 245-252.
4. Bhattacharyya, S., Sen, P., Wallet, M., Long, B. Jr., Baldwin, A. S., and Tisch, R. (2004). Immunoregulation of dendritic cells by IL-10 is mediated through suppression of the PI3K/Akt pathway and of I B kinase activity. Immunobiology 104, 1100-1109.
5. Boks, M. A., Kager-Groenland, J. R., Haasjes, M. S. P., Zwaginga, J. J., Van Ham, S. M., and Ten Brinke, A. (2012). IL-10-generated tolerogenic dendritic cells are optimal for functional regulatory T cell induction - a comparative study of human clinical-applicable DC. Clin. Immunol. 142, 332-342.
6. Boks, M. A., Zwaginga, J. J., Van Ham, S. M., and Ten Brinke, A. (2010). An optimized CFSE-based T-cell suppression assay to evaluate the suppressive capacity of regulatory T-cells induced by human tolerogenic dendritic cells. Scand. J. Immunol. 72, 158-168.
7. Burgess, J. K., Carlin, S., Pack, R. A., Arndt, G. M., Au, W. W., Johnson, P. R. A., et al. (2004). Detection and characterization of OX40 ligand expression in human airway smooth muscle cells: a possible role in asthma? J. Allergy Clin. Immunol. 113, 683-689.
8. Busse, M., Krech, M., Meyer-Bahlburg, A., Hennig, C., and Hansen, G. (2012). ICOS mediates the generation and function of CD4+CD25+Foxp3+ regulatory T cells conveying respiratory tolerance. J. Immunol. 189, 1975-1982.
9. Byrne, J. A., Butler, J. L., and Cooper, M. D. (1988). Differential activation requirements for virgin and memory T cells. J. Immunol. 141, 3249-3257.
10. Carreno, B. M., Bennett, F., Chau, T. A., Ling, V., Luxenberg, D., Jussif, J., et al. (2000). CTLA-4 (CD152) can inhibit T cell activation by two different mechanisms depending on its level of cell surface expression. J. Immunol. 165, 1352-1356.
11. Caux, C., Massacrier, C., Vanbervliet, B., Dubois, B., Durand, I., Cella, M., et al. (1997). CD34+ hematopoietic progenitors from human cord blood differentiate along two independent dendritic cell pathways in response to granulocyte-macrophage colony-stimulating factor plus tumor necrosis factor alpha: II. Functional analysis. Blood 90, 1458-1470.
12. Chang, J., Kunkel, S. L., and Chang, C.-H. (2009). Negative regulation of MyD88-dependent signaling by IL-10 in dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 106, 18327-18332.
13. Chemnitz, J. M., Parry, R. V., Nichols, K. E., June, H., Riley, J. L., and June, C. H. (2004). SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J. Immunol. 173, 945-954.
14. Cheong, C., Matos, I., Choi, J.-H., Dandamudi, D. B., Shrestha, E., Longhi, M. P., et al. (2010). Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell 143, 416-429.
15. Correll, A., Tuettenberg, A., Becker, C., and Jonuleit, H. (2010). Increased regulatory T-cell frequencies in patients with advanced melanoma correlate with a generally impaired T-cell responsiveness and are restored after dendritic cell-based vaccination. Exp. Dermatol. 19, e213-e221.
16. Corthay, A. (2006). A three-cell model for activation of naïve T helper cells. Scand. J. Immunol. 64, 93-96.
17. Croft, M. (2009). The role of TNF superfamily members in T-cell function and diseases. Nat. Rev. Immunol. 9, 271-285.
18. Croft, M., Bradley, L. M., and Swain, S. L. (1994). Naive versus memory CD4. J. Immunol. 152, 2675-2685.
19. Curtsinger, J. M., Schmidt, C. S., Mondino, A., Lins, D. C., Kedl, R. M., Jenkins, M. K., et al. (1999). Inflammatory cytokines provide a third signal for activation of naive CD4+ and CD8+ T cells. J. Immunol. 162, 3256-3262.
20. De Smedt, T., Smith, J., Baum, P., Fanslow, W., Butz, E., and Maliszewski, C. (2002). Ox40 costimulation enhances the development of T cell responses induced by dendritic cells in vivo. J. Immunol. 168, 661-670.
21. Dhodapkar, M. V., Steinman, R. M., Krasovsky, J., Munz, C., and Bhardwaj, N. (2001). Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J. Exp. Med. 193, 233-238.
22. Dieu, M. C., Vanbervliet, B., Vicari, A., Bridon, J. M., Oldham, E., Aït-Yahia, S., et al. (1998). Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J. Exp. Med. 188, 373-386.
23. Ding, Y., Chen, D., Tarcsafalvi, A., Su, R., Qin, L., and Bromberg, J. S. (2003). Suppressor of cytokine signaling 1 inhibits IL-10-mediated immune responses. J. Immunol. 170, 1383-1391.
24. Driessler, F., Venstrom, K., Sabat, R., Asadullah, K., and Area, B. (2004). Molecular mechanisms of interleukin-10-mediated inhibition of NF-kB activity: a role for p50. Clin. Exp. Immunol. 135, 64-73.
25. Dubsky, P., Saito, H., Leogier, M., Dantin, C., Connolly, J. E., Banchereau, J., et al. (2007). IL-15-induced human DC efficiently prime melanoma-specific naive CD8+ T cells to differentiate into CTL. Eur. J. Immunol. 37, 1678-1690.
26. Dudda, J. C., and Martin, S. F. (2004). Tissue targeting of T cells by DCs and microenvironments. Trends Immunol. 25, 417-421.
27. Engell-Noerregaard, L., Hansen, T. H., Andersen, M. H., Thor Straten, P., and Svane, I. M. (2009). Review of clinical studies on dendritic cell-based vaccination of patients with malignant melanoma: assessment of correlation between clinical response and vaccine parameters. Cancer Immunol. Immunother. 58, 1-14.
28. Ferreiros-Vidal, I., Gomez-Reino, J. J., Barros, F., Carracedo, A., Carreira, P., Gonzalez-Escribano, F., et al. (2004). Association of PDCD1 with susceptibility to systemic lupus erythematosus: evidence of population-specific effects. Arthritis Rheum. 50, 2590-2597.
29. Figdor, C. G., Bont, W. S., Touw, I., De Roos, J., Roosnek, E. E., and De Vries, J. E. (1982). Isolation of functionally different human monocytes by counterflow centrifugation elutriation. Blood 60, 46-53.
30. Figdor, C. G., De Vries, I. J. M., Lesterhuis, W. J., and Melief, C. J. M. (2004). Dendritic cell immunotherapy: mapping the way. Nat. Med. 10, 475-480.
31. Fillatreau, S., and Gray, D. (2003). T cell accumulation in B cell follicles is regulated by dendritic cells and is independent of B cell activation. J. Exp. Med. 197, 195-206.
32. Finbloom, D. S., and Winestock, K. D. (1995). IL-10 induces the tyrosine phosphorylation of tyk2 and Jak1 and the differential assembly of STAT1a and STAT3 complexes in human T cells and monocytes. J. Immunol. 155, 1079-1090.
33. Flynn, S., Toellner, K.-M., Raykundalia, C., Goodall, M., and Lane, P. (1998). CD4 T cell cytokine differentiation: the B cell activation molecule, OX40 ligand, instructs CD4 T cells to express interleukin 4 and upregulates expression of the chemokine receptor, Blr-1. J. Exp. Med. 188, 297-304.
34. Fong, L., Hou, Y., Rivas, A., Benike, C., Yuen, A., Fisher, G. A., et al. (2001). Altered peptide ligand vaccination with Flt3 ligand expanded dendritic cells for tumor immunotherapy. Proc. Natl. Acad. Sci. U.S.A. 98, 8809-8814.
35. Geng, Y., Gulbins, E., Altman, A., and Lotz, M. (1994). Monocyte deactivation by interleukin 10 via inhibition of tyrosine kinase activity and the Ras signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 91, 8602-8606.
36. Giannoukakis, N., Phillips, B., Finegold, D., Harnaha, J., and Trucco, M. (2011). Phase I (safety) study of autologous tolerogenic dendritic cells in type 1 diabetic patients. Diabetes Care 34, 2026-2032.
37. Gilliet, M., and Liu, Y.-J. (2002). Generation of human CD8 T regulatory cells by CD40 ligand-activated plasmacytoid dendritic cells. J. Exp. Med. 195, 695-704.
38. Greene, J. L., Leytze, G. M., Emswiler, J., Peach, R., Bajorath, J., Cosand, W., et al. (1996). Covalent dimerization of CD28/CTLA-4 and oligomerization of CD80/CD86 regulate T cell costimulatory interactions. J. Biol. Chem. 271, 26762-26771.
39. Gregori, S., Tomasoni, D., Pacciani, V., Scirpoli, M., Battaglia, M., Magnani, C. F., et al. (2010). Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway. Blood 116, 935-944.
40. Grewal, I. S., and Flavell, R. A. (1998). CD40 and CD154 in cell-mediated immunity. Annu. Rev. Immunol. 16, 111-135.
41. Habib, M., Rivas, M. N., Wieckowski, S., Sun, W., Trouche, N., Chaloin, O., et al. (2007). Cutting edge: small molecule CD40 ligand mimetics promote control of parasitemia and enhance T cells producing IFN-g during experimental trypanosoma cruzi infection. J. Immunol. 178, 6700-6704.
42. Haenssle, H., Buhl, T., Knudsen, S., Krueger, U., Rosenberger, A., Reich, K., et al. (2008). CD40 ligation during dendritic cell maturation reduces cell death and prevents interleukin-10-induced regression to macrophage-like monocytes. Exp. Dermatol. 17, 177-187.
43. Hamanishi, J., Mandai, M., Iwasaki, M., Okazaki, T., Tanaka, Y., Yamaguchi, K., et al. (2007). Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc. Natl. Acad. Sci. U.S.A. 104, 3360-3365.
44. Hansen, M., Hjortø, G. M., Donia, M., Met, Ö., Larsen, N. B., Andersen, M. H., et al. (2013). Comparison of clinical grade type 1 polarized and standard matured dendritic cells for cancer immunotherapy. Vaccine 31, 639-646.
45. Herman, A. E., Freeman, G. J., Mathis, D., and Benoist, C. (2004). CD4+CD25+ T regulatory cells dependent on ICOS promote regulation of effector cells in the prediabetic lesion. J. Exp. Med. 199, 1479-1489.
46. Hsu, F. J., Benike, C., Fagnoni, F., Liles, T. M., Czerwinski, D., Taidi, B., et al. (1996). Vaccination of patients with B-cell lymphoma using autologous antigen-pulsed dendritic cells. Nat. Med. 2, 52-58.
47. Hubo, M., and Jonuleit, H. (2012). Plasmacytoid dendritic cells are inefficient in activation of human regulatory T cells. PLoS ONE 7:e44056. doi:10.1371/journal.pone.0044056
48. Hutloff, A., Dittrich, A. M., Beier, K. C., Eljaschewitsch, B., Kraft, R., Anagnostopoulos, I., et al. (1999). ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature 397, 263-266.
49. Imura, B. A., Hori, T., Imada, K., Ishikawa, T., Tanaka, Y., Maeda, M., et al. (1996). The human OX40/gp34 system directly mediates adhesion of activated T cells to vascular endothelial cells. J. Exp. Med. 183, 2185-2195.
50. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., et al. (1992). Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176, 1693-1702.
51. Inaba, K., Witmer-Pack, M., Inaba, M., Hathcock, K., Sakuta, H., Azuma, M., et al. (1994). The tissue distribution of the B7-2 costimulator in mice: abundant expression on dendritic cells in situ and during maturation in vitro. J. Exp. Med. 180, 1849-1860.
52. Ito, T., Wang, Y.-H., Duramad, O., Hanabuchi, S., Perng, O. A., Gilliet, M., et al. (2006). OX40 ligand shuts down IL-10-producing regulatory T cells. Proc. Natl. Acad. Sci. U.S.A. 103, 13138-13143.
53. Ito, T., Wang, Y.-H., Duramad, O., Hori, T., Delespesse, G. J., Watanabe, N., et al. (2005). TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J. Exp. Med. 202, 1213-1223.
54. Ito, T., Yang, M., Wang, Y.-H., Lande, R., Gregorio, J., Perng, O. A., et al. (2007). Plasmacytoid dendritic cells prime IL-10-producing T regulatory cells by inducible costimulator ligand. J. Exp. Med. 204, 105-115.
55. Iwasaki, A., and Kelsall, B. L. (1999). Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells. J. Exp. Med. 190, 229-240.
56. Johansson-Lindbom, B., Svensson, M., Wurbel, M.-A., Malissen, B., Márquez, G., and Agace, W. (2003). Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J. Exp. Med. 198, 963-969.
57. Jonuleit, H., Giesecke, A., Kandemir, A., Paragnik, L., Knop, J., and Enk, A. H. (2000a). Induction of tumor peptide-specific cytotoxic T cells under serum-free conditions by mature human dendritic cells. Arch. Dermatol. Res. 292, 325-332.
58. Jonuleit, H., Schmitt, E., Schuler, G., Knop, J., and Enk, A. H. (2000b). Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J. Exp. Med. 192, 1213-1222.
59. Jonuleit, H., Giesecke-Tuettenberg, A., Tüting, T., Thurner-Schuler, B., Stuge, T. B., Paragnik, L., et al. (2001). A comparison of two types of dendritic cell as adjuvants for the induction of melanoma-specific T-cell responses in humans following intranodal injection. Int. J. Cancer 93, 243-251.
60. Jonuleit, H., Kühn, U., Müller, G., Steinbrink, K., Paragnik, L., Schmitt, E., et al. (1997). Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur. J. Immunol. 27, 3135-3142.
61. Kaur, D., and Brightling, C. (2012). OX40/OX40 ligand interactions in T-cell regulation and asthma. Chest 141, 494-499.
62. Keir, M. E., Butte, M. J., Freeman, G. J., and Sharpe, A. H. (2008). PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26, 677-704.
63. Knödler, A., Schmidt, S. M., Bringmann, A., Weck, M. M., Brauer, K. M., Holderried, T. A. W., et al. (2009). Post-transcriptional regulation of adapter molecules by IL-10 inhibits TLR-mediated activation of antigen-presenting cells. Leukemia 23, 535-544.
64. Kopf, M., Coyle, A. J., Schmitz, N., Barner, M., Oxenius, A., Gallimore, A., et al. (2000). Inducible costimulator protein (ICOS) controls T helper cell subset polarization after virus and parasite infection. J. Exp. Med. 192, 53-61.
65. Krupnick, A. S., Gelman, A. E., Richardson, S., Kreisel, F. H., Turka, A., Colonna, M., et al. (2005). Cutting edge: murine vascular endothelium activates and induces the generation of allogeneic CD4+25+Foxp3+ regulatory T cells. J. Immunol. 175, 6265-6270.
66. Kubsch, S., Graulich, E., Knop, J., and Steinbrink, K. (2003). Suppressor activity of anergic T cells induced by IL-10-treated human dendritic cells: association with IL-2- and CTLA-4-dependent G1 arrest of the cell cycle regulated by p27Kip1. Eur. J. Immunol. 33, 1988-1997.
67. Lapteva, N., Seethammagari, M. R., Hanks, B. A., Jiang, J., Levitt, J. M., Slawin, K. M., et al. (2007). Enhanced activation of human dendritic cells by inducible CD40 and Toll-like receptor-4 ligation. Cancer Res. 67, 10528-10537.
68. Lenschow, D. J., Walunas, T. L., and Jeffrey, A. (1996). CD28/B7 System of T cell costimulation. Annu. Rev. Immunol. 14, 233-258.
69. Linsley, P. S., Brady, W., Grosmaire, L., Aruffo, A., Damle, N. K., and Ledbetter, J. A. (1991). Binding of the B cell activation antigen B7 to CD28 costimulates T cell proliferation and interleukin 2 mRNA accumulation. J. Exp. Med. 173, 721-730.
70. Loke, P., and Allison, J. P. (2003). PD-L1 and PD-L2 are differentially regulated by Th1 and Th2 cells. Proc. Natl. Acad. Sci. U.S.A. 100, 5336-5341.
71. Lyman, S. D., and Jacobsen, S. E. (1998). c-kit Ligand and Flt3 ligand: stem/progenitor cell factors with overlapping yet distinct activities. Blood 91, 1101-1134.
72. MacDonald, A. S., Patton, E. A., La Flamme, A. C., Araujo, M. I., Huxtable, C. R., Bauman, B., et al. (2002). Impaired Th2 development and increased mortality during Schistosoma mansoni infection in the absence of CD40/CD154 interaction. J. Immunol. 168, 4643-4649.
73. Macdonald, K. P. A., Munster, D. J., Clark, G. J., Dzionek, A., Schmitz, J., and Hart, D. N. J. (2002). Characterization of human blood dendritic cell subsets. Blood 100, 4512-4520.
74. Medzhitov, R. (2001). Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1, 135-145.
75. Migone, T. S., Zhang, J., Luo, X., Zhuang, L., Chen, C., Hu, B., et al. (2002). TL1A is a TNF-like ligand for DR3 and TR6/DcR3 and functions as a T cell costimulator. Immunity 16, 479-492.
76. Mohamadzadeh, M., Berard, F., Essert, G., Chalouni, C., Pulendran, B., Davoust, J., et al. (2001). Interleukin 15 skews monocyte differentiation into dendritic cells with features of Langerhans cells. J. Exp. Med. 194, 1013-1020.
77. Murugaiyan, G., Agrawal, R., Mishra, G. C., Mitra, D., and Saha, B. (2007). Differential CD40/CD40L expression results in counteracting antitumor immune responses. J. Immunol. 178, 2047-2055.
78. Naik, S., Bouladoux, N., Wilhelm, C., Molloy, M. J., Salcedo, R., Kastenmuller, W., et al. (2012). Compartmentalized control of skin immunity by resident commensals. Science 337, 1115-1119.
79. Nakanishi, J., Wada, Y., Matsumoto, K., Azuma, M., Kikuchi, K., and Ueda, S. (2007). Overexpression of B7-H1 (PD-L1) significantly associates with tumor grade and postoperative prognosis in human urothelial cancers. Cancer Immunol. Immunother. 56, 1173-1182.
80. Niiro, H., Otsuka, T., Ogami, E., Yamaoka, K., Nagano, S., Akahoshi, M., et al. (1998). MAP kinase pathways as a route for regulatory mechanisms of IL-10 and IL-4 which inhibit COX-2 expression in human monocytes. Biochem. Biophys. Res. Commun. 250, 200-205.
81. Nishimura, H., Okazaki, T., Tanaka, Y., Nakatani, K., Hara, M., Matsumori, A., et al. (2001). Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 291, 319-322.
82. Ohshima, Y., Tanaka, Y., Tozawa, H., Takahashi, Y., Maliszewski, C., and Delespesse, G. (1997). Expression and function of OX40 ligand on human dendritic cells. J. Immunol. 159, 3838-3848.
83. Prokunina, L., Castillejo-López, C., Oberg, F., Gunnarsson, I., Berg, L., Magnusson, V., et al. (2002). A regulatory polymorphism in PDCD1 is associated with susceptibility to systemic lupus erythematosus in humans. Nat. Genet. 32, 666-669.
84. Reichmann, G., Walker, W., Villegas, E. N., Cai, G., Alexander, J., Christopher, A., et al. (2000). The CD40/CD40 ligand interaction is required for resistance to toxoplasmic encephalitis. Infect. Immun. 68, 1312-1318.
85. Romani, N., Gruner, S., Brang, D., Eckhart, K., Lenz, A., Trockenbacher, B., et al. (1994). Proliferating dendritic cell progenitors in human blood. J. Exp. Med. 180, 83-93.
86. Romani, N., Reider, D., Heuer, M., Ebner, S., Kämpgen, E., Eibl, B., et al. (1996). Generation of mature dendritic cells from human blood an improved method with special regard to clinical applicability. J. Immunol. Methods 196, 137-151.
87. Romano, E., Rossi, M., Ratzinger, G., De Cos, M.-A., Chung, D. J., Panageas, K. S., et al. (2011). Peptide-loaded Langerhans cells, despite increased IL15 secretion and T-cell activation in vitro, elicit antitumor T-cell responses comparable to peptide-loaded monocyte-derived dendritic cells in vivo. Clin. Cancer Res. 17, 1984-1997.
88. Rottman, J. B., Smith, T., Tonra, J. R., Ganley, K., Bloom, T., Silva, R., et al. (2001). The costimulatory molecule ICOS plays an important role in the immunopathogenesis of EAE. Nat. Immunol. 2, 605-611.
89. Royer, P., Ebstein, F., Sapede, C., Simon, T., Barbieux, I., Oger, R., et al. (2006). Culture medium and protein supplementation in the generation and maturation of dendritic cells. Scand. J. Immunol. 63, 401-409.
90. Saito, M., Nagasawa, M., Takada, H., Hara, T., Tsuchiya, S., Agematsu, K., et al. (2011). Defective IL-10 signaling in hyper-IgE syndrome results in impaired generation of tolerogenic dendritic cells and induced regulatory T cells. J. Exp. Med. 208, 235-249.
91. Sallusto, B. F., and Lanzavecchia, A. (1994). Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor c. J. Exp. Med. 179, 1109-1118.
92. Sallusto, F., and Lanzavecchia, A. (2000). Understanding dendritic cell and T-lymphocyte traffic through the analysis of chemokine receptor expression. Immunol. Rev. 177, 134-140.
93. Sato, K., Nagayama, H., Tadokoro, K., Juji, T., and Takahashi, T. A. (1999). Extracellular signal-regulated kinase, stress-activated protein kinase/c-Jun N-terminal kinase, and p38mapk are involved in IL-10-mediated selective repression of TNF-a-induced activation and maturation of human peripheral blood monocyte-derived dendritic. J. Immunol. 162, 3865-3872.
94. Savary, C. A., Grazziutti, M. L., Melichar, B., Przepiorka, D., Freedman, R. S., Cowart, R. E., et al. (1998). Multidimensional flow-cytometric analysis of dendritic cells in peripheral blood of normal donors and cancer patients. Cancer Immunol. Immunother. 45, 234-240.
95. Schadendorf, D., Ugurel, S., Schuler-Thurner, B., Nestle, F. O., Enk, A., Bröcker, E.-B., et al. (2006). Dacarbazine (DTIC) versus vaccination with autologous peptide-pulsed dendritic cells (DC) in first-line treatment of patients with metastatic melanoma: a randomized phase III trial of the DC study group of the DeCOG. Ann. Oncol. 17, 563-570.
96. Schottelius, A. J., Mayo, M. W., Sartor, R. B., and Baldwin, A. S. (1999). Interleukin-10 signaling blocks inhibitor of kappaB kinase activity and nuclear factor kappaB DNA binding. J. Biol. Chem. 274, 31868-31874.
97. Schuler, G. (2011). Dendritic cells. Cancer J. 17, 337-342.
98. Schuler-Thurner, B., Dieckmann, D., Keikavoussi, P., Bender, A., Maczek, C., Jonuleit, H., et al. (2000). Mage-3 and influenza-matrix peptide-specific cytotoxic T cells are inducible in terminal stage HLA-A2.1+ melanoma patients by mature monocyte-derived dendritic cells. J. Immunol. 165, 3492-3496.
99. Schwarz, A., Navid, F., Sparwasser, T., Clausen, B. E., and Schwarz, T. (2011). In vivo reprogramming of UV radiation-induced regulatory T-cell migration to inhibit the elicitation of contact hypersensitivity. J. Allergy Clin. Immunol. 128, 826-833.
100. Shames, B. D., Selzman, C. H., Meldrum, D. R., Pulido, E. J., Barton, H. A., Meng, X., et al. (1998). Interleukin-10 stabilizes inhibitory kappaB-alpha in human monocytes. Shock. 10, 389-394.
101. Shortman, K., and Naik, S. H. (2007). Steady-state and inflammatory dendritic-cell development. Nat. Rev. Immunol. 7, 19-30.
102. Sigmundsdottir, H., and Butcher, E. C. (2008). Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat. Immunol. 9, 981-987.
103. Snijders, A., Kalinski, P., Hilkens, C. M., and Kapsenberg, M. L. (1998). High-level IL-12 production by human dendritic cells requires two signals. Int. Immunol. 10, 1593-1598.
104. Steinbrink, K. (2002). CD4+ and CD8+ anergic T cells induced by interleukin-10-treated human dendritic cells display antigen-specific suppressor activity. Blood 99, 2468-2476.
105. Steinbrink, K., Jonuleit, H., Müller, G., Schuler, G., Knop, J., and Enk, A. H. (1999). Interleukin-10-treated human dendritic cells induce a melanoma-antigen-specific anergy in CD8(+) T cells resulting in a failure to lyse tumor cells. Blood 93, 1634-1642.
106. Steinbrink, K., Paragnik, L., Jonuleit, H., Tüting, T., Knop, J., and Enk, A. H. (2000). Induction of dendritic cell maturation and modulation of dendritic cell-induced immune responses by prostaglandins. Arch. Dermatol. Res. 292, 437-445.
107. Steinbrink, K., Wolfl, M., Jonuleit, H., Knop, J., and Enk, A. H. (1997). Induction of tolerance by IL-10-treated dendritic cells. J. Immunol. 159, 4772-4780.
108. Steinman, R. M. (2012). Decisions about dendritic cells: past, present, and future. Annu. Rev. Immunol. 30, 1-22.
109. Tel, J., Aarntzen, E. H. J. G., Baba, T., Schreibelt, G., Schulte, B. M., Benitez-Ribas, D., et al. (2013). Natural human plasmacytoid dendritic cells induce antigen-specific T-cell responses in melanoma patients. Cancer Res. 73, 1063-1075.
110. Thurner, B., Röder, C., Dieckmann, D., Heuer, M., Kruse, M., Glaser, A., et al. (1999). Generation of large numbers of fully mature and stable dendritic cells from leukapheresis products for clinical application. J. Immunol. Methods 223, 1-15.
111. Torres-Aguilar, H., Aguilar-Ruiz, S. R., González-Pérez, G., Munguía, R., Bajaña, S., Meraz-Ríos, M. A., et al. (2010). Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD4+ T cells. J. Immunol. 184, 1765-1775.
112. Tuettenberg, A., Becker, C., Huter, E., Knop, J., Enk, A. H., and Jonuleit, H. (2006). Induction of strong and persistent MelanA/MART-1-specific immune responses by adjuvant dendritic cell-based vaccination of stage II melanoma patients. Int. J. Cancer 118, 2617-2627.
113. Tuettenberg, A., Fondel, S., Steinbrink, K., Enk, A. H., and Jonuleit, H. (2010). CD40 signalling induces IL-10-producing, tolerogenic dendritic cells. Exp. Dermatol. 19, 44-53.
114. Tuettenberg, A., Huter, E., Hubo, M., Horn, J., Knop, J., Grimbacher, B., et al. (2009). The role of ICOS in directing T cell responses: ICOS-dependent induction of T cell anergy by tolerogenic dendritic cells. J. Immunol. 182, 3349-3356.
115. Ueno, H., Schmitt, N., Klechevsky, E., Pedroza-Gonzalez, A., Matsui, T., Zurawski, G., et al. (2010). Harnessing human dendritic cell subsets for medicine. Immunol. Rev. 234, 199-212.
116. Velten, F. W., Duperrier, K., Bohlender, J., Metharom, P., and Goerdt, S. (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.
117. Vries, I. J. M., De Eggert, A. A. O., Scharenborg, N. M., Vissers, J. L. M., Lesterhuis, W. J., Boerman, O. C., et al. (2002). Phenotypical and functional characterization of clinical grade dendritic cells. J. Immunother. 25, 429-438.
118. Vu, M. D., Xiao, X., Gao, W., Degauque, N., Chen, M., Kroemer, A., et al. (2007). OX40 costimulation turns off Foxp3+ Tregs. Blood 110, 2501-2510.
119. Weiner, H. L. (2001). The mucosal milieu creates tolerogenic dendritic cells and T(R)1 and T(H)3 regulatory cells. Nat. Immunol. 2, 671-672.
120. Wieckowski, E., Chatta, G. S., Mailliard, R. M., Gooding, W., Palucka, K., Banchereau, J., et al. (2011). Type-1 polarized dendritic cells loaded with apoptotic prostate cancer cells are potent inducers of CD8(+) T cells against prostate cancer cells and defined prostate cancer-specific epitopes. Prostate 71, 125-133.
121. Wiethe, C., Dittmar, K., Doan, T., and Tindle, R. (2003). Enhanced effector and memory CTL responses generated by incorporation of receptor activator of NF-kB (RANK)/RANK ligand costimulatory molecules into dendritic cell immunogens expressing a human tumor-specific antigen. J. Immunol. 171, 4121-4130.
122. Wilson, N. S., El-Sukkari, D., Belz, G. T., Smith, C. M., Steptoe, R. J., Heath, W. R., et al. (2003). Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood 102, 2187-2194.
123. Witsch, E. J., Peiser, M., Hutloff, A., Büchner, K., Dorner, B. G., Jonuleit, H., et al. (2002). ICOS and CD28 reversely regulate IL-10 on re-activation of human effector T cells with mature dendritic cells. Eur. J. Immunol. 32, 2680-2686.
124. Wu, L., and Liu, Y.-J. (2007). Development of dendritic-cell lineages. Immunity 26, 741-750.
125. Xiuling, L., Aimei, Y., Hui, H., Xiabobei, Z., Town, J., Davis, B., et al. (2010). Induction of type 2 T helper cell allergen tolerance by IL-10-differentiated regulatory dendritic cells. Am. J. Respir. Cell Mol. Biol. 42, 190-199.
126. Yamazaki, T., Akiba, H., Iwai, H., Matsuda, H., Aoki, M., Tanno, Y., et al. (2002). Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 169, 5538-5545.
127. Yoshinaga, S. K., Whoriskey, J. S., Khare, S. D., Sarmiento, U., Guo, J., Horan, T., et al. (1999). T-cell co-stimulation through B7RP-1 and ICOS. Nature 402, 827-832.
128. Zhong, X., Tumang, J. R., Gao, W., Bai, C., and Rothstein, T. L. (2007). PD-L2 expression extends beyond dendritic cells/macrophages to B1 cells enriched for V(H)11/V(H)12 and phosphatidylcholine binding. Eur. J. Immunol. 37, 2405-2410.