Constitutive p40 promoter activation and IL-23 production in the terminal ileum mediated by dendritic cells

Journal of Clinical Investigation

Volumn 112, Issue 5, 2003, Pages 693-706

  Becker, Christoph ^a   Wirtz, Stefan ^a   Blessing, Manfred ^a   Pirhonen, Jaana ^b   Strand, Dennis ^a   Bechthold, Oliver ^c   Frick, Julia ^c   Galle, Peter R ^a   Autenrieth, Ingo ^c   Neurath, Markus F ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 23; MESSENGER RNA; PROTEIN P40; BACTERIAL ANTIGEN; GLYCOPROTEIN P 15095; IL23A PROTEIN, MOUSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 23P19; INTERLEUKIN DERIVATIVE; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CROHN DISEASE; CYTOKINE PRODUCTION; DENDRITIC CELL; FLUORESCENCE IN SITU HYBRIDIZATION; GENE ACTIVATION; GENE EXPRESSION; ILEUM; LAMINA PROPRIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION REGULATION; TRANSGENIC MOUSE; ANIMAL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PROMOTER REGION;

ANIMALS; ANTIGENS, BACTERIAL; ANTIGENS, CD11C; CROHN DISEASE; DENDRITIC CELLS; GENE EXPRESSION REGULATION; ILEUM; INTERLEUKIN-12; INTERLEUKIN-12 SUBUNIT P40; INTERLEUKIN-23; INTERLEUKIN-23 SUBUNIT P19; INTERLEUKINS; MICE; MICE, TRANSGENIC; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; PROMOTER REGIONS (GENETICS); PROTEIN SUBUNITS;

EID: 0141835046     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200317464     Document Type: Article

References (56)

1. Gubler, U., et al. 1991. Coexpression of two distinct genes is required to generate secreted bioactive cytotoxic lymphocyte maturation factor. Proc. Natl. Acad. Sci. U. S. A. 88:4143-4147.
2. Kobayashi, M., et al. 1989. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J. Exp. Med. 170:827-845.
3. Stern, A.S., et al. 1990. Purification to homogeneity and partial characterization of cytotoxic lymphocyte maturation factor from human B-lymphoblastoid cells. Proc. Natl. Acad. Sci. U. S. A. 87:6808-6812.
4. Wolf, S.F., et al. 1991. Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells. J. Immunol. 146:3074-3081.
5. D'Andrea, A., et al. 1992. Production of natural killer cell stimulatory factor (interleukin 12) by peripheral blood mononuclear cells. J. Exp. Med. 176:1387-1398.
6. Barbulescu, K., et al. 1998. IL-12 and IL-18 differentially regulate the transcriptional activity of the human IFN-gamma promoter in primary CD4+ T lymphocytes. J. Immunol. 160:3642-3647.
7. Jacobson, N.G., et al. 1995. Interleukin 12 signaling in T helper type 1 (Th1) cells involves tyrosine phosphorylation of signal transducer and activator of transcription (Stat)3 and Stat4. J. Exp. Med. 181:1755-1762.
8. Oppmann, B., et al. 2000. 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.
9. Belladonna, M.L., et al. 2002. IL-23 and IL-12 have overlapping, but distinct, effects on murine dendritic cells. J. Immunol. 168:5448-5454.
10. Parham, C., et al. 2002. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rbeta1 and a novel cytokine receptor subunit, IL-23R. J. Immunol. 168:5699-5708.
11. Wiekowski, M.T., et al. 2001. Ubiquitous transgenic expression of the IL-23 subunit p19 induces multiorgan inflammation, runting, infertility, and premature death. J. Immunol. 166:7563-7570.
12. Ma, X., et al. 1996. The interleukin 12 p40 gene promoter is primed by interferon gamma in monocytic cells. J. Exp. Med. 183:147-157.
13. Murphy, T.L., Cleveland, M.G., Kulesza, P., Magram, J., and Murphy, K.M. 1995. Regulation of interleukin 12 p40 expression through an NF-kappa B half-site. Mol. Cell Biol. 15:5258-5267.
14. Weinmann, A.S., Plevy, S.E., and Smale, S.T. 1999. Rapid and selective remodeling of a positioned nucleosome during the induction of IL-12 p40 transcription. Immunity. 11:665-675.
15. Weinmann, A.S., et al. 2001. Nucleosome remodeling at the IL-12 p40 promoter is a TLR-dependent, Rel-independent event. Nat. Immunol. 2:51-57.
16. Becker, C., et al. 2001. Regulation of IL-12 p40 promoter activity in primary human monocytes: roles of NF-kappaB, CCAAT/enhancer-binding protein beta, and PU.1 and identification of a novel repressor element (GA-12) that responds to IL-4 and prostaglandin E(2). J. Immunol. 167:2608-2618.
17. Ma, X., Gri, G., and Trinchieri, G. 1996. A novel Ets-2-related nuclear factor is involved in transcriptional activation of the human interleukin-12 p40 gene promoter in response to interferon-gamma and LPS stimulation of monocytic cells. Ann. N. Y. Acad. Sci. 795:357-360.
18. Ma, X., Neurath, M., Gri, G., and Trinchieri, G. 1997. Identification and characterization of a novel Ets-2-related nuclear complex implicated in the activation of the human interleukin-12 p40 gene promoter. J. Biol. Chem. 272:10389-10395.
19. Plevy, S.E., Gemberling, J.H., Hsu, S., Dorner, A.J., and Smale, S.T. 1997. Multiple control elements mediate activation of the murine and human interleukin 12 p40 promoters: evidence of functional synergy between C/EBP and Rel proteins. Mol. Cell Biol. 17:4572-4588.
20. Nordeen, S.K. 1988. Luciferase reporter gene vectors for analysis of promoters and enhancers. Biotechniques. 6:454-458.
21. Waidmann, M., et al. 2002. Microflora reactive IL-10 producing regulatory T cells are present in the colon of IL-2 deficient mice but lack efficacious inhibition of IFN-gamma and TNF-alpha production. Gut. 50:170-179.
22. Neurath, M.F., Fuss, I., Kelsall, B.L., Stuber, E., and Strober, W. 1995. Antibodies to interleukin 12 abrogate established experimental colitis in mice. J. Exp. Med. 182:1281-1290.
23. Schreiber, E., Matthias, P., Muller, M.M., and Schaffner, W. 1989. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 17:6419.
24. Pirhonen, J., Matikainen, S., and Julkunen, I. 2002. Regulation of virus-induced IL-12 and IL-23 expression in human macrophages. J. Immunol. 169:5673-5678.
25. Amann, R.I., Krumholz, L., and Stahl, D.A. 1990. Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J. Bacteriol. 172:762-770.
26. Kempf, V.A., Trebesius, K., and Autenrieth, I.B. 2000. Fluorescent in situ hybridization allows rapid identification of microorganisms in blood cultures. J. Clin. Microbiol. 38:830-838.
27. D'Andrea, A., Ma, X., Aste-Amezaga, M., Paganin, C., and Trinchieri, G. 1995. Stimulatory and inhibitory effects of interleukin (IL)-4 and IL-13 on the production of cytokines by human peripheral blood mononuclear cells: priming for IL-12 and tumor necrosis factor alpha production. J. Exp. Med. 181:537-546.
28. Koch, F., et al. 1996. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J. Exp Med. 184:741-746.
29. Naz, R.K., and Evans, L. 1998. Presence and modulation of interleukin-12 in seminal plasma of fertile and infertile men. J. Androl. 19:302-307.
30. Yamamoto, K., et al. 1997. cDNA cloning, expression and chromosome mapping of the human STAT4 gene: both STAT4 and STAT1 genes are mapped to 2q32.2? q32.3. Cytogenet. Cell Genet. 77:207-210.
31. Iwasaki, A., and Kelsall, B.L. 2001. Unique functions of CD11b+, CD8 alpha+, and double-negative Peyer's patch dendritic cells. J. Immunol. 166:4884-4890.
32. Iwasaki, A., and Kelsall, B.L. 2000. Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3alpha, MIP-3beta, and secondary lymphoid organ chemokine. J. Exp. Med. 191:1381-1394.
33. Chow, J.C., Young, D.W., Golenbock, D.T., Christ, W.J., and Gusovsky, F. 1999. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem. 274:10689-10692.
34. Zhang, F.X., et al. 1999. Bacterial lipopolysaccharide activates nuclear factor-kappaB through interleukin-1 signaling mediators in cultured human dermal endothelial cells and mononuclear phagocytes. J. Biol. Chem. 274:7611-7614.
35. Bucht, A., et al. 1996. Expression of interferon-gamma (IFN-gamma), IL-10, IL-12 and transforming growth factor-beta (TGF-beta) mRNA in synovial fluid cells from patients in the early and late phases of rheumatoid arthritis (RA). Clin. Exp. Immunol. 103:357-367.
36. Fuss, I.J., et al. 1996. Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J. Immunol. 157:1261-1270.
37. Gately, M.K., et al. 1996. Interleukin-12 antagonist activity of mouse interleukin-12 p40 homodimer in vitro and in vivo. Ann. N. Y. Acad. Sci. 795:1-12.
38. McIntyre, K.W., et al. 1996. Reduced incidence and severity of collagen-induced arthritis in interleukin-12-deficient mice. Eur. J. Immunol. 26:2933-2938.
39. Ozmen, L., et al. 1994. Interleukin 12, interferon gamma, and tumor necrosis factor alpha are the key cytokines of the generalized Shwartzman reaction. J. Exp. Med. 180:907-915.
40. Trembleau, S., Penna, G., Gregori, S., Gately, M.K., and Adorini, L. 1997. Deviation of pancreas-infiltrating cells to Th2 by interleukin-12 antagonist administration inhibits autoimmune diabetes. Eur. J. Immunol. 27:2330-2339.
41. Wysocka, M., et al. 1995. Interleukin-12 is required for interferon-gamma production and lethality in lipopolysaccharide-induced shock in mice. Eur. J. Immunol. 25:672-676.
42. Zipris, D., et al. 1996. Cytokine gene expression in islets and thyroids of BB rats. IFN-gamma and IL-12p40 mRNA increase with age in both diabetic and insulin-treated nondiabetic BB rats. J. Immunol. 156:1315-1321.
43. Strober, W., Fuss, I.J., and Blumberg, R.S. 2002. The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 20:495-549.
44. Cowdery, J.S., Boerth, N.J., Norian, L.A., Myung, P.S., and Koretzky, G.A. 1999. Differential regulation of the IL-12 p40 promoter and of p40 secretion by CpG DNA and lipopolysaccharide. J. Immunol. 162:6770-6775.
45. Cua, D.J., et al. 2003. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature. 421:744-748.
46. Huang, F.P., et al. 2000. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J. Exp. Med. 191:435-444.
47. Iwasaki, A., and Kelsall, B.L. 1999. Mucosal immunity and inflammation. I. Mucosal dendritic cells: their specialized role in initiating T cell responses. Am. J. Physiol. 276:G1074-G1078.
48. Iwasaki, A., and Kelsall, B.L. 1999. Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differenriation of T helper type 2 cells. J. Exp. Med. 190:229-239.
49. Steinman, R.M., Turley, S., Mellman, I., and Inaba, K. 2000. The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med. 191:411-416.
50. Liu, K., et al. 2002. Immune tolerance after delivery of dying cells to dendritic cells in situ. J. Exp Med. 196:1091-1097.
51. Rescigno, M., Rotta, G., Valzasina, B., and Ricciardi-Castagnoli, P. 2001. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology. 204:572-581.
52. Rescigno, M., et al. 2001. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2:361-367.
53. Kuckelkorn, U., et al. 2002. Link between organ-specific antigen processing by 20S proteasomes and CD8(+) T cell-mediated autoimmunity. J. Exp. Med. 195:983-990.
54. Atreya, R., et al. 2000. Blockade of IL-6 trans-signaling suppresses T cell resistance against apoptosis in chronic intestinal inflammation: Evidence in Crohn's disease and experimental colitis in vivo. Nat. Med. 6:583-588.
55. Friedman, S., and Blumberg, R.S. 1999. Inflammatory bowel disease. In Harrison's principles of internal medicine. 15th edition. McGraw-Hill. New York, New York, USA. 1679-1691.
56. Aggarwal, S., Ghilardi, N., Xie, M.H., de Sauvage, F.J., and Gurney, A.L. 2003. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278:1910-1914.