Cytokine-dependent regulation of dendritic cell differentiation in the splenic microenvironment

European Journal of Immunology

Volumn 44, Issue 2, 2014, Pages 500-510

  Globisch, Theresa ^a,b   Steiner, Nancy ^b   Fülle, Lorenz ^b   Lukacs Kornek, Veronika ^b,f   Degrandi, Daniel ^c   Dresing, Philipp ^c   Alferink, Judith ^b,d   Lang, Roland ^e   Pfeffer, Klaus ^c   Beyer, Marc ^b   Weighardt, Heike ^a,b   Kurts, Christian ^b   Ulas, Thomas ^b   Schultze, Joachim L ^b   Förster, Irmgard ^a,b  

^a IUF LEIBNIZ RESEARCH INSTITUTE FOR ENVIRONMENTAL MEDICINE   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d UNIVERSITY OF MÜNSTER   (Germany)

^e UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^f SAARLAND UNIVERSITY   (Germany)

Author keywords

DCs; GM CSF; IFN receptor; IL 4; Spleen

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; CD8 ANTIGEN; CYTOKINE; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR 1; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 4; LIPOPOLYSACCHARIDE; NEUTRALIZING ANTIBODY; THYMUS AND ACTIVATION REGULATED CHEMOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; DENDRITIC CELL; FLOW CYTOMETRY; HISTOLOGY; IMMUNE RESPONSE; INFLAMMATION; LYMPHOCYTE ACTIVATION; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; SPLEEN CELL; TH1 CELL; TH2 CELL;

DCS; GM-CSF; IFN-Γ RECEPTOR; IL-4; SPLEEN;

ANIMALS; ANTIGENS, CD11B; CELL DIFFERENTIATION; CELLULAR MICROENVIRONMENT; CHEMOKINE CCL17; DENDRITIC CELLS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; INTERFERON-GAMMA; INTERLEUKIN-4; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; RECEPTORS, INTERFERON; SPLEEN;

EID: 84893589101     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343820     Document Type: Article

References (47)

1. Hashimoto, D., Miller, J. and Merad, M., Dendritic cell and macrophage heterogeneity in vivo. Immunity 2011. 35: 323-335.
2. Jaensson, E., Uronen-Hansson, H., Pabst, O., Eksteen, B., Tian, J., Coombes, J. L., Berg, P. L. et al., Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 2008. 205: 2139-2149.
3. Schulz, O., Jaensson, E., Persson, E. K., Liu, X., Worbs, T., Agace, W. W. and Pabst, O., Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J. Exp. Med. 2009. 206: 3101-3114.
4. Sathe, P. and Shortman, K., The steady-state development of splenic dendritic cells. Mucosal Immunol. 2008. 1: 425-431.
5. Min, L., Mohammad Isa, S. A. B., Fam, W. N., Sze, S. K., Beretta, O., Mortellaro, A. and Ruedl, C., Synergism between curdlan and GM-CSF confers a strong inflammatory signature to dendritic cells. J. Immunol. 2012. 188: 1789-1798.
6. Zhan, Y., Vega-Ramos, J., Carrington, E. M., Villadangos, J. A., Lew, A. M. and Xu, Y., The inflammatory cytokine, GM-CSF, alters the developmental outcome of murine dendritic cells. Eur. J. Immunol. 2012. 42: 2889-2900.
7. Shortman, K. and Naik, S. H., Steady-state and inflammatory dendritic-cell development. Nat. Rev. Immunol. 2007. 7: 19-30.
8. Zhan, Y., Carrington, E. M., van Nieuwenhuijze, A., Bedoui, S., Seah, S., Xu, Y., Wang, N. et al., GM-CSF increases cross-presentation and CD103 expression by mouse CD8+ spleen dendritic cells. Eur. J. Immunol. 2011. 41: 2585-2595.
9. Dresch, C., Leverrier, Y., Marvel, J. and Shortman, K., Development of antigen cross-presentation capacity in dendritic cells. Trends Immunol. 2012. 33: 381-388.
10. Sathe, P., Pooley, J., Vremec, D., Mintern, J., Jin, J. O., Wu, L., Kwak, J. Y. et al., The acquisition of antigen cross-presentation function by newly formed dendritic cells. J. Immunol. 2011. 186: 5184-5192.
11. Elpek, K. G., Bellemare-Pelletier, A., Malhotra, D., Reynoso, E. D., Lukacs-Kornek, V., DeKruyff, R. H. and Turley, S. J., Lymphoid organ-resident dendritic cells exhibit unique transcriptional fingerprints based on subset and site. PLoS One 2011. 6: e23921.
12. Alferink, J., Lieberam, I., Reindl, W., Behrens, A., Weiss, S., Huser, N., Gerauer, K. et al., Compartmentalized production of CCL17 in vivo: strong inducibility in peripheral dendritic cells contrasts selective absence from the spleen. J. Exp. Med. 2003. 197: 585-599.
13. Stutte, S., Quast, T., Gerbitzki, N., Savinko, T., Novak, N., Reifenberger, J., Homey, B. et al., Requirement of CCL17 for CCR7- and CXCR4-dependent migration of cutaneous dendritic cells. Proc. Natl. Acad. Sci. USA 2010. 107: 8736-8741.
14. Lieberam, I. and Förster, I., The murine beta-chemokine TARC is expressed by subsets of dendritic cells and attracts primed CD4+ T cells. Eur. J. Immunol. 1999. 29: 2684-2694.
15. Burdin, N., Brossay, L., Koezuka, Y., Smiley, S. T., Grusby, M. J., Gui, M., Taniguchi, M. et al., Selective ability of mouse CD1 to present glycolipids: alpha-galactosylceramide specifically stimulates V alpha 14+ NK T lymphocytes. J. Immunol. 1998. 161: 3271-3281.
16. Semmling, V., Lukacs-Kornek, V., Thaiss, C. A., Quast, T., Hochheiser, K., Panzer, U., Rossjohn, J. et al., Alternative cross-priming through CCL17-CCR4-mediated attraction of CTLs toward NKT cell-licensed DCs. Nat. Immunol. 2010. 11: 313-320.
17. Gros, E., Bussmann, C., Bieber, T., Förster, I. and Novak, N., Expression of chemokines and chemokine receptors in lesional and nonlesional upper skin of patients with atopic dermatitis. J. Allergy Clin. Immunol. 2009. 124: 753-760.e.1.
18. Heiseke, A. F., Faul, A. C., Lehr, H. A., Förster, I., Schmid, R. M., Krug, A. B. and Reindl, W., CCL17 promotes intestinal inflammation in mice and counteracts regulatory T cell-mediated protection from colitis. Gastroenterology 2012. 142: 335-345.
19. Weber, C., Meiler, S., Doring, Y., Koch, M., Drechsler, M., Megens, R. T., Rowinska, Z. et al., CCL17-expressing dendritic cells drive atherosclerosis by restraining regulatory T cell homeostasis in mice. J. Clin. Invest. 2011. 121: 2898-2910.
20. Poppensieker, K., Otte, D. M., Schurmann, B., Limmer, A., Dresing, P., Drews, E., Schumak, B. et al., CC chemokine receptor 4 is required for experimental autoimmune encephalomyelitis by regulating GM-CSF and IL-23 production in dendritic cells. Proc. Natl. Acad. Sci. USA 2012. 109: 3897-3902.
21. Sallusto, F., Lenig, D., Mackay, C. R. and Lanzavecchia, A., Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. J. Exp. Med. 1998. 187: 875-883.
22. Chvatchko, Y., Hoogewerf, A. J., Meyer, A., Alouani, S., Juillard, P., Buser, R., Conquet, F. et al., A key role for CC chemokine receptor 4 in lipopolysaccharide-induced endotoxic shock. J. Exp. Med. 2000. 191: 1755-1764.
23. Rusinova, I., Forster, S., Yu, S., Kannan, A., Masse, M., Cumming, H., Chapman, R. et al., INTERFEROME v2.0: an updated database of annotated interferon-regulated genes. Nucleic Acids Res. 2013. 41: D1040-D1046.
24. Boehm, U., Guethlein, L., Klamp, T., Ozbek, K., Schaub, A., Futterer, A., Pfeffer, K. et al., Two families of GTPases dominate the complex cellular response to IFN-gamma. J. Immunol. 1998. 161: 6715-6723.
25. Xiao, T., Fujita, H., Saeki, H., Mitsui, H., Sugaya, M., Tada, Y., Kakinuma, T. et al., Thymus and activation-regulated chemokine (TARC/CCL17) produced by mouse epidermal Langerhans cells is upregulated by TNF-alpha and IL-4 and downregulated by IFN-gamma. Cytokine 2003. 23: 126-132.
26. Fujita, H., Asahina, A., Sugaya, M., Nakamura, K., Gao, P., Fujiwara, H. and Tamaki, K., Differential production of Th1- and Th2-type chemokines by mouse Langerhans cells and splenic dendritic cells. J. Invest. Dermatol. 2005. 124: 343-350.
27. Vestergaard, C., Kirstejn, N., Gesser, B., Mortensen, J. T., Matsushima, K. and Larsen, C. G., IL-10 augments the IFN-gamma and TNF-alpha induced TARC production in HaCaT cells: a possible mechanism in the inflammatory reaction of atopic dermatitis. J. Dermatol. Sci. 2001. 26: 46-54.
28. Qi, X.-F., Teng, Y.-C., Yoon, Y.-S., Kim, D.-H., Cai, D.-Q. and Lee, K.-J., Reactive oxygen species are involved in the IFN-γ-stimulated production of Th2 chemokines in HaCaT keratinocytes. J. Cell Physiol. 2011. 226: 58-65.
29. Inoue, H., Iga, M., Xin, M., Asahi, S., Nakamura, T., Kurita, R., Nakayama, M. et al., TARC and RANTES enhance antitumor immunity induced by the GM-CSF-transduced tumor vaccine in a mouse tumor model. Cancer Immunol. Immunother. 2008. 57: 1399-1411.
30. Godfrey, D. I. and Kronenberg, M., Going both ways: immune regulation via CD1d-dependent NKT cells. J. Clin. Invest. 2004. 114: 1379-1388.
31. Coquet, J. M., Chakravarti, S., Kyparissoudis, K., McNab, F. W., Pitt, L. A., McKenzie, B. S., Berzins, S. P. et al., Diverse cytokine production by NKT cell subsets and identification of an IL-17-producing CD4-NK1.1- NKT cell population. Proc. Natl. Acad. Sci. USA 2008. 105: 11287-11292.
32. Wingender, G., Rogers, P., Batzer, G., Lee, M. S., Bai, D., Pei, B., Khurana, A. et al., Invariant NKT cells are required for airway inflammation induced by environmental antigens. J. Exp. Med. 2011. 208: 1151-1162.
33. Dranoff, G., Crawford, A. D., Sadelain, M., Ream, B., Rashid, A., Bronson, R. T., Dickersin, G. R. et al., Involvement of granulocyte-macrophage colony-stimulating factor in pulmonary homeostasis. Science 1994. 264: 713-716.
34. Bezbradica, J. S., Gordy, L. E., Stanic, A. K., Dragovic, S., Hill, T., Hawiger, J., Unutmaz, D. et al., Granulocyte-macrophage colony-stimulating factor regulates effector differentiation of invariant natural killer T cells during thymic ontogeny. Immunity 2006. 25: 487-497.
35. Mebius, R. E. and Kraal, G., Structure and function of the spleen. Nat. Rev. Immunol. 2005. 5: 606-616.
36. Bousso, P. and Albert, M. L., Signal 0 for guided priming of CTLs: NKT cells do it too. Nat. Immunol. 2010. 11: 284-286.
37. Gros, E., Petzold, S., Maintz, L., Bieber, T. and Novak, N., Reduced IFN-gamma receptor expression and attenuated IFN-gamma response by dendritic cells in patients with atopic dermatitis. J. Allergy Clin. Immunol. 2011. 128: 1015-1021.
38. Imai, T., Nagira, M., Takagi, S., Kakizaki, M., Nishimura, M., Wang, J. B., Gray, P. W. et al., Selective recruitment of CCR4-bearing T(h)2 cells toward antigen-presenting cells by the CC chemokines thymus and activation-regulated chemokine and macrophage-derived chemokine. Int. Immunol. 1999. 11: 81-88.
39. Bell, B. D., Kitajima, M., Larson, R. P., Stoklasek, T. A., Dang, K., Sakamoto, K., Wagner, K. U. et al., The transcription factor STAT5 is critical in dendritic cells for the development of TH2 but not TH1 responses. Nat. Immunol. 2013. 14: 364-371.
40. Liddiard, K., Welch, J. S., Lozach, J., Heinz, S., Glass, C. K. and Greaves, D. R., Interleukin-4 induction of the CC chemokine TARC (CCL17) in murine macrophages is mediated by multiple STAT6 sites in the TARC gene promoter. BMC Mol. Biol. 2006. 7: 45.
41. Stevenson, N. J., Addley, M. R., Ryan, E. J., Boyd, C. R., Carroll, H. P., Paunovic, V., Bursill, C. A. et al., CCL11 blocks IL-4 and GM-CSF signaling in hematopoietic cells and hinders dendritic cell differentiation via suppressor of cytokine signaling expression. J. Leukoc. Biol. 2009. 85: 289-297.
42. Dickensheets, H. L., Venkataraman, C., Schindler, U. and Donnelly, R. P., Interferons inhibit activation of STAT6 by interleukin 4 in human monocytes by inducing SOCS-1 gene expression. Proc. Natl. Acad. Sci. USA 1999. 96: 10800-10805.
43. Zhan, Y., Xu, Y. and Lew, A. M., The regulation of the development and function of dendritic cell subsets by GM-CSF: more than a hematopoietic growth factor. Mol. Immunol. 2012. 52: 30-37.
44. van de Laar, L., Coffer, P. J. and Woltman, A. M., Regulation of dendritic cell development by GM-CSF: molecular control and implications for immune homeostasis and therapy. Blood 2012. 119: 3383-3393.
45. Edelson, B. T., Bradstreet, T. R., Kc, W., Hildner, K., Herzog, J. W., Sim, J., Russell, J. H. et al., Batf3-dependent CD11b(low/-) peripheral dendritic cells are GM-CSF-independent and are not required for Th cell priming after subcutaneous immunization. PLoS One 2011. 6: e25660.
46. Huang, S., Hendriks, W., Althage, A., Hemmi, S., Bluethmann, H., Kamijo, R., Vilcek, J. et al., Immune response in mice that lack the interferon-gamma receptor. Science 1993. 259: 1742-1745.
47. Müller, U., Steinhoff, U., Reis, L. F., Hemmi, S., Pavlovic, J., Zinkernagel, R. M. and Aguet, M., Functional role of type I and type II interferons in antiviral defense. Science 1994. 264: 1918-1921.