Human tolerogenic dendritic cells produce IL-35 in the absence of other IL-12 family members

European Journal of Immunology

Volumn 45, Issue 6, 2015, Pages 1736-1747

  Dixon, Karen O ^a   van der Kooij, Sandra W ^a   Vignali, Dario A A ^b   van Kooten, Cees ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

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

Author keywords

Dendritic cells; Human; IL 12 IL 35 axis; Tolerance

Indexed keywords

CD40 LIGAND; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12P35; INTERLEUKIN 12P40; INTERLEUKIN 23P19; INTERLEUKIN 27; INTERLEUKIN 35; B7 ANTIGEN; CD86 ANTIGEN; DEXAMETHASONE; EBI3 PROTEIN, HUMAN; INTERLEUKIN 12; INTERLEUKIN DERIVATIVE; INTERLEUKIN-35, HUMAN; LIPOPOLYSACCHARIDE; PROGRAMMED DEATH 1 LIGAND 1;

ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; GENE SILENCING; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; RNA INTERFERENCE; T LYMPHOCYTE ACTIVATION; UPREGULATION; ANTIGEN PRESENTING CELL; BIOSYNTHESIS; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; PHENOTYPE;

ANTIGEN-PRESENTING CELLS; ANTIGENS, CD274; ANTIGENS, CD86; B7 ANTIGENS; DENDRITIC CELLS; DEXAMETHASONE; GENE EXPRESSION; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-12; INTERLEUKIN-12 SUBUNIT P35; INTERLEUKIN-27; INTERLEUKINS; LIPOPOLYSACCHARIDES; PHENOTYPE;

EID: 84930407196     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201445217     Document Type: Article

References (45)

1. Reis e Sousa, C., Dendritic cells in a mature age. Nat. Rev. Immunol. 2006. 6: 476-483.
2. Steinman, R. M., Hawiger, D. and Nussenzweig, M. C., Tolerogenic dendritic cells. Annu. Rev. Immunol. 2003. 21: 685-711.
3. Woltman, A. M. and van Kooten, C., Functional modulation of dendritic cells to suppress adaptive immune responses. J. Leukoc. Biol. 2003. 73: 428-441.
4. Torres-Aguilar, H., Aguilar-Ruiz, S. R., Gonzalez-Perez, G., Munguia, R., Bajana, S., Meraz-Rios, M. A. and Sanchez-Torres, C., Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD4+ T cells. J. Immunol. 2010. 184: 1765-1775.
5. Zhao, Y., Zhang, A., Du, H., Guo, S., Ning, B. and Yang, S., Tolerogenic dendritic cells and rheumatoid arthritis: current status and perspectives. Rheumatol. Int. 2012. 32: 837-844.
6. Morelli, A. E. and Thomson, A. W., Tolerogenic dendritic cells and the quest for transplant tolerance. Nat. Rev. Immunol. 2007. 7: 610-621.
7. van Kooten, C., Lombardi, G., Gelderman, K. A., Sagoo, P., Buckland, M., Lechler, R. and Cuturi, M. C., Dendritic cells as a tool to induce transplantation tolerance: obstacles and opportunities. Transplantation 2011. 91: 2-7.
8. Woltman, A. M., de Fijter, J. W., Kamerling, S. W., Paul, L. C., Daha, M. R. and van Kooten, C., The effect of calcineurin inhibitors and corticosteroids on the differentiation of human dendritic cells. Eur. J. Immunol. 2000. 30: 1807-1812.
9. Collison, L. W. and Vignali, D. A., Interleukin-35: odd one out or part of the family? Immunol. Rev. 2008. 226: 248-262.
10. Dixon, K. O., O'Flynn, J., van der Kooij, S. W. and van Kooten, C., Phagocytosis of apoptotic or necrotic cells differentially regulates the transcriptional expression of IL-12 family members in dendritic cells. J. Leukoc. Biol. 2014. 96: 313-324.
11. Brombacher, F., Kastelein, R. A. and Alber, G., Novel IL-12 family members shed light on the orchestration of Th1 responses. Trends Immunol. 2003. 24: 207-212.
12. Morishima, N., Owaki, T., Asakawa, M., Kamiya, S., Mizuguchi, J. and Yoshimoto, T., Augmentation of effector CD8+ T cell generation with enhanced granzyme B expression by IL-27. J. Immunol. 2005. 175: 1686-1693.
13. Schneider, R., Yaneva, T., Beauseigle, D., El-Khoury, L. and Arbour, N., IL-27 increases the proliferation and effector functions of human naive CD8+ T lymphocytes and promotes their development into Tc1 cells. Eur. J. Immunol. 2011. 41: 47-59.
14. Pot, C., Apetoh, L., Awasthi, A. and Kuchroo, V. K., Induction of regulatory Tr1 cells and inhibition of T(H)17 cells by IL-27. Semin. Immunol. 2011. 23: 438-445.
15. Mascanfroni, I. D., Yeste, A., Vieira, S. M., Burns, E. J., Patel, B., Sloma, I., Wu, Y. et al., IL-27 acts on DCs to suppress the T cell response and autoimmunity by inducing expression of the immunoregulatory molecule CD39. Nat. Immunol. 2013. 14: 1054-1063.
16. Collison, L. W., Chaturvedi, V., Henderson, A. L., Giacomin, P. R., Guy, C., Bankoti, J., Finkelstein, D. et al., IL-35-mediated induction of a potent regulatory T cell population. Nat. Immunol. 2010. 11: 1093-1101.
17. Seyerl, M., Kirchberger, S., Majdic, O., Seipelt, J., Jindra, C., Schrauf, C. and Stockl, J., Human rhinoviruses induce IL-35-producing Treg via induction of B7-H1 (CD274) and sialoadhesin (CD169) on DC. Eur. J. Immunol. 2010. 40: 321-329.
18. Whitehead, G. S., Wilson, R. H., Nakano, K., Burch, L. H., Nakano, H. and Cook, D. N., IL-35 production by inducible costimulator (ICOS)-positive regulatory T cells reverses established IL-17-dependent allergic airways disease. J. Allergy Clin. Immunol. 2012. 129: 207-215 e201-205.
19. Garbers, C., Hermanns, H. M., Schaper, F., Muller-Newen, G., Grotzinger, J., Rose-John, S. and Scheller, J., Plasticity and cross-talk of interleukin 6-type cytokines. Cytokine Growth Factor Rev. 2012. 23: 85-97.
20. Vignali, D. A. and Kuchroo, V. K., IL-12 family cytokines: immunological playmakers. Nat. Immunol. 2012. 13: 722-728.
21. Banchereau, J., Pascual, V. and O'Garra, A., From IL-2 to IL-37: the expanding spectrum of anti-inflammatory cytokines. Nat. Immunol. 2012. 13: 925-931.
22. Trinchieri, G., Interleukin-12 and its role in the generation of TH1 cells. Immunol. Today 1993. 14: 335-338.
23. Awasthi, A., Riol-Blanco, L., Jager, A., Korn, T., Pot, C., Galileos, G., Bettelli, E. et al., Cutting edge: IL-23 receptor gfp reporter mice reveal distinct populations of IL-17-producing cells. J. Immunol. 2009. 182: 5904-5908.
24. Apetoh, L., Quintana, F. J., Pot, C., Joller, N., Xiao, S., Kumar, D., Burns, E. J. et al., The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat. Immunol. 2010. 11: 854-861.
25. Collison, L. W., Pillai, M. R., Chaturvedi, V. and Vignali, D. A., Regulatory T cell suppression is potentiated by target T cells in a cell contact, IL-35- and IL-10-dependent manner. J. Immunol. 2009. 182: 6121-6128.
26. Unger, W. W., Laban, S., Kleijwegt, F. S., van der Slik, A. R. and Roep, B. O., Induction of Treg by monocyte-derived DC modulated by vitamin D3 or dexamethasone: differential role for PD-L1. Eur. J. Immunol. 2009. 39: 3147-3159.
27. Woltman, A. M., van der Kooij, S. W., de Fijter, J. W. and van Kooten, C., Maturation-resistant dendritic cells induce hyporesponsiveness in alloreactive CD45RA+ and CD45RO+ T-cell populations. Am. J. Transplant. 2006. 6: 2580-2591.
28. Pfistershammer, K., Klauser, C., Pickl, W. F., Stockl, J., Leitner, J., Zlabinger, G., Majdic, O. et al., No evidence for dualism in function and receptors: PD-L2/B7-DC is an inhibitory regulator of human T cell activation. Eur. J. Immunol. 2006. 36: 1104-1113.
29. Zhang, Y., Chung, Y., Bishop, C., Daugherty, B., Chute, H., Holst, P., Kurahara, C. et al., Regulation of T cell activation and tolerance by PDL2. Proc. Natl. Acad. Sci. USA 2006. 103: 11695-11700.
30. Manavalan, J. S., Rossi, P. C., Vlad, G., Piazza, F., Yarilina, A., Cortesini, R., Mancini, D. et al., High expression of ILT3 and ILT4 is a general feature of tolerogenic dendritic cells. Transpl. Immunol. 2003. 11: 245-258.
31. Schuetze, N., Schoeneberger, S., Mueller, U., Freudenberg, M. A., Alber, G. and Straubinger, R. K., IL-12 family members: differential kinetics of their TLR4-mediated induction by Salmonella enteritidis and the impact of IL-10 in bone marrow-derived macrophages. Int. Immunol. 2005. 17: 649-659.
32. Molle, C., Nguyen, M., Flamand, V., Renneson, J., Trottein, F., De Wit, D., Willems, F. et al., IL-27 synthesis induced by TLR ligation critically depends on IFN regulatory factor 3. J. Immunol. 2007. 178: 7607-7615.
33. Zheng, X. F., Hong, Y. X., Feng, G. J., Zhang, G. F., Rogers, H., Lewis, M. A., Williams, D. W. et al., Lipopolysaccharide-induced M2 to M1 macrophage transformation for IL-12p70 production is blocked by Candida albicans mediated up-regulation of EBI3 expression. PLoS One 2013. 8: e63967.
34. Vogelpoel, L. T., Hansen, I. S., Rispens, T., Muller, F. J., van Capel, T. M., Turina, M. C., Vos, J. B. et al., Fc gamma receptor-TLR cross-talk elicits pro-inflammatory cytokine production by human M2 macrophages. Nat. Commun. 2014. 5: 5444.
35. Schoop, R., Wahl, P., Le Hir, M., Heemann, U., Wang, M. and Wuthrich, R. P., Suppressed T-cell activation by IFN-gamma-induced expression of PD-L1 on renal tubular epithelial cells. Nephrol. Dial. Transplant. 2004. 19: 2713-2720.
36. Jurgens, B., Hainz, U., Fuchs, D., Felzmann, T. and Heitger, A., Interferon-gamma-triggered indoleamine 2, 3-dioxygenase competence in human monocyte-derived dendritic cells induces regulatory activity in allogeneic T cells. Blood 2009. 114: 3235-3243.
37. Rojas-Canales, D., Krishnan, R., Jessup, C. F. and Coates, P. T., Early exposure of interferon-gamma inhibits signal transducer and activator of transcription-6 signalling and nuclear factor kappaB activation in a short-term monocyte-derived dendritic cell culture promoting 'FAST' regulatory dendritic cells. Clin. Exp. Immunol. 2012. 167: 447-458.
38. Hill, M., Thebault, P., Segovia, M., Louvet, C., Beriou, G., Tilly, G., Merieau, E. et al., Cell therapy with autologous tolerogenic dendritic cells induces allograft tolerance through interferon-gamma and epstein-barr virus-induced gene 3. Am. J. Transplant. 2011. 11: 2036-2045.
39. de Groot, R., van Beelen, A. J., Bakdash, G., Taanman-Kueter, E. W., de Jong, E. C. and Kapsenberg, M. L., Viral dsRNA-activated human dendritic cells produce IL-27, which selectively promotes cytotoxicity in naive CD8+ T cells. J. Leukoc. Biol. 2012. 92: 605-610.
40. Liu, J., Guan, X. and Ma, X., Regulation of IL-27 p28 gene expression in macrophages through MyD88- and interferon-gamma-mediated pathways. J. Exp. Med. 2007. 204: 141-152.
41. Collison, L. W., Workman, C. J., Kuo, T. T., Boyd, K., Wang, Y., Vignali, K. M., Cross, R. et al., The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 2007. 450: 566-569.
42. Shen, P., Roch, T., Lampropoulou, V., O'Connor, R. A., Stervbo, U., Hilgenberg, E., Ries, S. et al., IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 2014. 507: 366-370.
43. Olson, B. M., Sullivan, J. A. and Burlingham, W. J., Interleukin 35: a key mediator of suppression and the propagation of infectious tolerance. Front. Immunol. 2013. 4: 315.
44. Trinchieri, G., Pflanz, S. and Kastelein, R. A., The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 2003. 19: 641-644.
45. Dixon, K. O., Rossmann, L., Kamerling, S. W. and van Kooten, C., Human renal fibroblasts generate dendritic cells with a unique regulatory profile. Immunol. Cell Biol. 2014. 92: 688-698.