IL-23-mediated mononuclear phagocyte crosstalk protects mice from Citrobacter rodentium-induced colon immunopathology

Nature Communications

Volumn 6, Issue , 2015, Pages

  Aychek, Tegest ^a   Mildner, Alexander ^a   Yona, Simon ^a   Kim, Ki Wook ^a   Lampl, Nardy ^a   Reich Zeliger, Shlomit ^a   Boon, Louis ^b   Yogev, Nir ^c   Waisman, Ari ^c   Cua, Daniel J ^d   Jung, Steffen ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b BIOCEROS   (Netherlands)

^c UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^d MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 22; INTERLEUKIN 23; ALPHA E INTEGRINS; ALPHA INTEGRIN; CD11B ANTIGEN; CHEMOKINE RECEPTOR; CX3CR1 PROTEIN, HUMAN; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; LEUKOCYTE ANTIGEN;

BACTERIAL DISEASE; BACTERIUM; HOMEOSTASIS; IMMUNE RESPONSE; IMMUNITY; PATHOLOGY; RODENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; BACTERIAL LOAD; CITROBACTER RODENTIUM; COLON DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DNA SYNTHESIS; FLOW CYTOMETRY; HISTOLOGY; IMMUNOPATHOLOGY; MONONUCLEAR PHAGOCYTE; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; TH17 CELL; ANIMAL; COLON; ENTEROBACTERIACEAE INFECTION; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE MUCOSA; MACROPHAGE; MICROBIOLOGY; MONOCYTE; MORTALITY; MUCOSAL IMMUNITY; PATHOGENICITY; PATHOLOGY; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TRANSGENIC MOUSE;

ANIMALIA; CITROBACTER RODENTIUM; MUS;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD11B; CITROBACTER RODENTIUM; COLON; DENDRITIC CELLS; ENTEROBACTERIACEAE INFECTIONS; GENE EXPRESSION REGULATION; HOMEOSTASIS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; INTEGRIN ALPHA CHAINS; INTERFERON-GAMMA; INTERLEUKIN-12; INTERLEUKIN-23; INTERLEUKINS; INTESTINAL MUCOSA; MACROPHAGES; MICE; MICE, TRANSGENIC; MONOCYTES; RECEPTORS, CHEMOKINE; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TH17 CELLS;

EID: 84924529911     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7525     Document Type: Article

References (51)

1. Cerovic, V., Bain, C. C., Mowat, A. M. & Milling, S. W. F. Intestinal macrophages and dendritic cells: what's the difference? Trends. Immunol. 35, 270-277 (2014).
2. Farache, J., Zigmond, E., Shakhar, G. & Jung, S. Contributions of dendritic cells and macrophages to intestinal homeostasis and immune defense. Immunol. Cell. Biol. 91, 232-239 (2013).
3. Mildner, A. & Jung, S. Development and function of dendritic cell subsets. Immunity 40, 642-656 (2014).
4. Cerovic, V. et al. Lymph-borne CD8α(+) dendritic cells are uniquely able to cross-prime CD8(+) T cells with antigen acquired from intestinal epithelial cells. Mucosal Immunol. 4, 104-113 (2014).
5. Lewis, K. L. et al. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 35, 780-791 (2011).
6. Schlitzer, A. et al. IRF4 transcription factor-dependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38, 970-983 (2013).
7. Persson, E. K. et al. IRF4 transcription-factor-dependent CD103(+)CD11b(+) dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 38, 958-969 (2013).
8. Welty, N. E. et al. Intestinal lamina propria dendritic cells maintain T cell homeostasis but do not affect commensalism. J. Exp. Med. 210, 2011-2024 (2013).
9. Cerovic, V. et al. Intestinal CD103- dendritic cells migrate in lymph and prime effector T cells. Mucosal Immunol. 6, 104-113 (2012).
10. Schreiber, H. A. et al. Intestinal monocytes and macrophages are required for T cell polarization in response to Citrobacter rodentium. J. Exp. Med. 210, 2025-2039 (2013).
11. Rivollier, A., He, J., Kole, A., Valatas, V. & Kelsall, B. L. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J. Exp. Med. 209, 139-155 (2012).
12. Zigmond, E. et al. Ly6Chi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 37, 1076-1090 (2012).
13. Mortha, A. et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 343, 1249288-1249288 (2014).
14. Lai, Y., Rosenshine, I., Leong, J. M. & Frankel, G. Intimate host attachment: enteropathogenic and enterohaemorrhagic Escherichia coli. Cell. Microbiol. 15, 1796-1808 (2013).
15. Mundy, R., Macdonald, T. T., Dougan, G., Frankel, G. & Wiles, S. Citrobacter rodentium of mice and man. Cell. Microbiol. 7, 1697-1706 (2005).
16. Maaser, C. et al. Clearance of citrobacter rodentium requires B Cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect. Immun. 72, 3315-3324 (2004).
17. Oppmann, B. et al. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13, 715-725 (2000).
18. Mangan, P. R. et al. Transforming growth factor-β induces development of the TH17 lineage. Nature 441, 231-234 (2006).
19. Sonnenberg, G. F., Fouser, L. A. & Artis, D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat. Immunol. 12, 383-390 (2011).
20. Zheng, Y. et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14, 282-289 (2008).
21. Basu, R. et al. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity 37, 1061-1075 (2012).
22. Ivanov, I. I. et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485-498 (2009).
23. Wiles, S., Pickard, K. M., Peng, K., Macdonald, T. T. & Frankel, G. In vivo bioluminescence imaging of the murine pathogen Citrobacter rodentium. Infect. Immun. 74, 5391-5396 (2006).
24. Jung, S. et al. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity 17, 211-220 (2002).
25. Varol, C. et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31, 502-512 (2009).
26. Sapoznikov, A. et al. Organ-dependent in vivo priming of naive CD4+, but not CD8+, T cells by plasmacytoid dendritic cells. J. Exp. Med. 204, 1923-1933 (2007).
27. Yona, S. et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79-91 (2012).
28. Buch, T. et al. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat. Methods 2, 419-426 (2005).
29. Kinnebrew, M. A. et al. Bacterial flagellin stimulates Toll-like receptor 5-dependent defense against vancomycin-resistant Enterococcus infection. J. Infect. Dis. 201, 534-543 (2010).
30. Satpathy, A. T. et al. Notch2-dependent classical dendritic cells orchestrate intestinal immunity to attaching- and-effacing bacterial pathogens. Nat. Immunol. 14, 937-948 (2013).
31. Longman, R. S. et al. CX3CR1+ mononuclear phagocytes support colitis-associated innate lymphoid cell production of IL-22. J. Exp. Med. 9, 143 (2014).
32. Awasthi, A. et al. Cutting Edge: IL-23 receptor GFP reporter mice reveal distinct populations of IL-17-producing cells. J. Immunol. 182, 5904-5908 (2009).
33. Vignali, D. A. A. & Kuchroo, V. K. IL-12 family cytokines: immunological playmakers. Nat. Immunol. 13, 722-728 (2012).
34. Kurschus, F. C. et al. Genetic proof for the transient nature of the Th17 phenotype. Eur. J. Immunol. 40, 3336-3346 (2010).
35. Hirota, K. et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 12, 255-263 (2011).
36. Morrison, P. J. et al. Th17-cell plasticity in Helicobacter hepaticus-induced intestinal inflammation. Mucosal Immunol. 6, 1143-1156 (2013).
37. Ouyang, W., Kolls, J. K. & Zheng, Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28, 454-467 (2008).
38. Maynard, C. L. et al. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3- precursor cells in the absence of interleukin 10. Nat. Immunol. 8, 931-941 (2007).
39. Becker, C. et al. Cutting edge: IL-23 cross-regulates IL-12 production in T cell-dependent experimental colitis. J. Immunol. 177, 2760-2764 (2006).
40. Sieve, A. N., Meeks, K. D., Lee, S. & Berg, R. E. A novel immunoregulatory function for IL-23: Inhibition of IL-12-dependent IFN-γ production. Eur. J. Immunol. 40, 2236-2247 (2010).
41. Kortylewski, M. et al. Regulation of the IL-23 and IL-12 balanceby Stat3 signaling in the tumor microenvironment. Cancer Cell 15, 114-123 (2009).
42. O'garra, A. Cytokines induce the development review of functionally heterogeneousT helper cell subsets. Immunity 8, 275-283 (1998).
43. Fuchs, A. et al. Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-g-producing cells. Immunity 38, 769-781 (2013).
44. Buonocore, S. et al. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 464, 1371-1375 (2010).
45. Aychek, T. & Jung, S. The axis of tolerance. Science 343, 1439-1440 (2014).
46. Duerr, R. H. et al. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 314, 1461-1463 (2006).
47. Cho, J. H. The genetics and immunopathogenesis of inflammatory bowel disease. Nat. Rev. Immunol. 8, 458-466 (2008).
48. Magram, J. et al. IL-12-deficient mice are defective in IFN gamma production and type 1 cytokine responses. Immunity 4, 471-481 (1996).
49. Cua, D. J. et al. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421, 744-748 (2003).
50. Luche, H., Weber, O., Nageswara Rao, T., Blum, C. & Fehling, H. J. Faithful activation of an extra-bright red fluorescent protein in 'knock-in' Cre-reporter mice ideally suited for lineage tracing studies. Eur. J. Immunol. 37, 43-53 (2007).
51. Aychek, T., Vandoorne, K., Brenner, O., Jung, S. & Neeman, M. Quantitative analysis of intravenously administered contrast media reveals changes in vascular barrier functions in a murine colitis model. Magn. Reson. Med. 66, 235-243 (2011).