IL-10 inhibits transcription elongation of the human TNF gene in primary macrophages

Journal of Experimental Medicine

Volumn 207, Issue 10, 2010, Pages 2081-2088

  Smallie, Tim ^a,b   Ricchetti, Giuseppe ^a   Horwood, Nicole J ^a   Feldmann, Marc ^a   Clark, Andrew R ^a   Williams, Lynn M ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 9; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; RNA POLYMERASE II; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INHIBITION KINETICS; MACROPHAGE; PRIORITY JOURNAL; TRANSCRIPTION INITIATION;

3' UNTRANSLATED REGIONS; BINDING SITES; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 9; HUMANS; I-KAPPA B PROTEINS; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MACROPHAGES; NF-KAPPA B; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77957726025     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20100414     Document Type: Article

References (35)

1. Adelman, K., M.A. Kennedy, S. Nechaev, D.A. Gilchrist, G.W. Muse, Y. Chinenov, and I. Rogatsky. 2009. Immediate mediators of the inflammatory response are poised for gene activation through RNA polymerase II stalling. Proc. Natl. Acad. Sci. USA. 106:18207-18212. doi:10.1073/pnas.0910177106
2. Barboric, M., R.M. Nissen, S. Kanazawa, N. Jabrane-Ferrat, and B.M. Peterlin. 2001. NF-kappaB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol. Cell. 8:327-337. doi:10.1016/S1097-2765(01)00314-8 (Pubitemid 32831550)
3. Behmoaras, J., G. Bhangal, J. Smith, K. McDonald, B. Mutch, P.C. Lai, J. Domin, L. Game, A. Salama, B.M. Foxwell, et al. 2008. Jund is a determinant of macrophage activation and is associated with glomerulonephritis susceptibility. Nat. Genet. 40:553-559. doi:10.1038/ng.137
4. Buelens, C., F. Willems, A. Delvaux, G. Piérard, J.P. Delville, T. Velu, and M. Goldman. 1995. Interleukin-10 differentially regulates B7-1 (CD80) and B7-2 (CD86) expression on human peripheral blood dendritic cells. Eur. J. Immunol. 25:2668-2672. doi:10.1002/eji.1830250940
5. Chao, S.-H., and D.H. Price. 2001. Flavopiridol inactivates P-TEFb and blocks most RNA polymerase II transcription in vivo. J. Biol. Chem. 276:31793-31799. doi:10.1074/jbc.M102306200 (Pubitemid 33657539)
6. Denys, A., I.A. Udalova, C. Smith, L.M. Williams, C.J. Ciesielski, J. Campbell, C. Andrews, D. Kwaitkowski, and B.M. Foxwell. 2002. Evidence for a dual mechanism for IL-10 suppression of TNF-alpha production that does not involve inhibition of p38 mitogen-activated protein kinase or NF-kappa B in primary human macrophages. J. Immunol. 168:4837-4845.
7. Feldmann, M., and R.N. Maini. 2003. Lasker Clinical Medical Research Award. TNF defined as a therapeutic target for rheumatoid arthritis and other autoimmune diseases. Nat. Med. 9:1245-1250. doi:10.1038/nm939
8. Foxwell, B., K. Browne, J. Bondeson, C. Clarke, R. de Martin, F. Brennan, and M. Feldmann. 1998. Efficient adenoviral infection with IkappaB alpha reveals that macrophage tumor necrosis factor alpha production in rheumatoid arthritis is NF-kappaB dependent. Proc. Natl. Acad. Sci. USA. 95:8211-8215. doi:10.1073/pnas.95.14.8211 (Pubitemid 28326092)
9. Glocker, E.-O., D. Kotlarz, K. Boztug, E.M. Gertz, A.A. Schäffer, F. Noyan, M. Perro, J. Diestelhorst, A. Allroth, D. Murugan, et al. 2009. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N. Engl. J. Med. 361:2033-2045. doi:10.1056/NEJMoa0907206
10. Grütz, G. 2005. New insights into the molecular mechanism of interleukin-10- mediated immunosuppression. J. Leukoc. Biol. 77:3-15.
11. Hargreaves, D.C., T. Horng, and R. Medzhitov. 2009. Control of inducible gene expression by signal-dependent transcriptional elongation. Cell. 138:129-145. doi:10.1016/j.cell.2009.05.047
12. He, T.C., A.B. Sparks, C. Rago, H. Hermeking, L. Zawel, L.T. da Costa, P.J. Morin, B. Vogelstein, and K.W. Kinzler. 1998. Identification of c-MYC as a target of the APC pathway. Science. 281:1509-1512. doi:10.1126/science.281.5382. 1509
13. Huang, B., X.-D. Yang, M.-M. Zhou, K. Ozato, and L.-F. Chen. 2009. Brd4 coactivates transcriptional activation of NF-kappaB via specific binding to acetylated RelA. Mol. Cell. Biol. 29:1375-1387. doi:10.1128/MCB.01365-08
14. Kontoyiannis, D., A. Kotlyarov, E. Carballo, L. Alexopoulou, P.J. Blackshear, M. Gaestel, R. Davis, R. Flavell, and G. Kollias. 2001. Interleukin-10 targets p38 MAPK to modulate ARE-dependent TNF mRNA translation and limit intestinal pathology. EMBO J. 20:3760-3770. doi:10.1093/emboj/20.14. 3760
15. Krausgruber, T., D. Saliba, G. Ryzhakov, A. Lanfrancotti, K. Blazek, and I.A. Udalova. 2010. IRF5 is required for late-phase TNF secretion by human dendritic cells. Blood. 115:4421-4430. doi:10.1182/blood-2010-01-263020
16. Kühn, R., J. Löhler, D. Rennick, K. Rajewsky, and W. Müller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 75:263-274. doi:10.1016/0092-8674(93)80068-P (Pubitemid 23320290)
17. Lang, R., D. Patel, J.J. Morris, R.L. Rutschman, and P.J. Murray. 2002. Shaping gene expression in activated and resting primary macrophages by IL-10. J. Immunol. 169:2253-2263.
18. Luecke, H.F., and K.R. Yamamoto. 2005. The glucocorticoid receptor blocks P-TEFb recruitment by NFkappaB to effect promoter-specific transcriptional repression. Genes Dev. 19:1116-1127. doi:10.1101/gad.1297105
19. Moore, K.W., R. de Waal Malefyt, R.L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19:683-765. doi:10.1146/annurev.immunol.19.1.683
20. Murray, P.J. 2005. The primary mechanism of the IL-10-regulated antiinflammatory response is to selectively inhibit transcription. Proc. Natl. Acad. Sci. USA. 102:8686-8691. doi:10.1073/pnas.0500419102
21. Natoli, G. 2009. Control of NF-kappaB-dependent transcriptional responses by chromatin organization. Cold Spring Harb Perspect Biol. 1:a000224. doi:10.1101/cshperspect.a000224
22. Price, D.H. 2000. P-TEFb, a cyclin-dependent kinase controlling elongation by RNA polymerase II. Mol. Cell. Biol. 20:2629-2634. doi:10.1128/MCB.20.8.2629-2634.2000
23. Ramirez-Carrozzi, V.R., D. Braas, D.M. Bhatt, C.S. Cheng, C. Hong, K.R. Doty, J.C. Black, A. Hoffmann, M. Carey, and S.T. Smale. 2009. A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Cell. 138:114-128. doi:10.1016/j.cell.2009.04.020
24. Sandoval, J., J.L. Rodríguez, G. Tur, G. Serviddio, J. Pereda, A. Boukaba, J. Sastre, L. Torres, L. Franco, and G. López-Rodas. 2004. RNAPol-ChIP: a novel application of chromatin immunoprecipitation to the analysis of real-time gene transcription. Nucleic Acids Res. 32:e88. doi:10.1093/nar/gnh091
25. Saraiva, M., and A. O'Garra. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10:170-181. doi:10.1038/nri2711
26. Schaljo, B., F. Kratochvill, N. Gratz, I. Sadzak, I. Sauer, M. Hammer, C. Vogl, B. Strobl, M. Müller, P.J. Blackshear, et al. 2009. Tristetraprolin is required for full anti-inflammatory response of murine macrophages to IL-10. J. Immunol. 183:1197-1206. doi:10.4049/jimmunol.0803883
27. Schottelius, A.J., M.W. Mayo, R.B. Sartor, and A.S. Baldwin Jr. 1999. Interleukin-10 signaling blocks inhibitor of kappaB kinase activity and nuclear factor kappaB DNA binding. J. Biol. Chem. 274:31868-31874. doi:10.1074/jbc.274. 45.31868 (Pubitemid 129503773)
28. Takeda, K., B.E. Clausen, T. Kaisho, T. Tsujimura, N. Terada, I. Förster, and S. Akira. 1999. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity. 10:39-49. doi:10.1016/S1074-7613(00)80005-9
29. Tsytsykova, A.V., R. Rajsbaum, J.V. Falvo, F. Ligeiro, S.R. Neely, and A.E. Goldfeld. 2007. Activation-dependent intrachromosomal interactions formed by the TNF gene promoter and two distal enhancers. Proc. Natl. Acad. Sci. USA. 104:16850-16855. doi:10.1073/pnas.0708210104
30. Udalova, I.A., J.C. Knight, V. Vidal, S.A. Nedospasov, and D. Kwiatkowski. 1998. Complex NF-kappaB interactions at the distal tumor necrosis factor promoter region in human monocytes. J. Biol. Chem. 273:21178-21186. doi:10.1074/jbc.273.33.21178
31. Udalova, I.A., V. Vidal, I.G. Scragg, and D. Kwiatkowski. 2000. Direct evidence for involvement of NF-kappaB in transcriptional activation of tumor necrosis factor by a spirochetal lipoprotein. Infect. Immun. 68:5447-5449. doi:10.1128/IAI.68.9.5447-5449.2000
32. Wang, P., P. Wu, M.I. Siegel, R.W. Egan, and M.M. Billah. 1995. Interleukin (IL)-10 inhibits nuclear factor kappa B (NF kappa B) activation in human monocytes. IL-10 and IL-4 suppress cytokine synthesis by different mechanisms. J. Biol. Chem. 270:9558-9563. doi:10.1074/jbc.270.16.9558
33. Williams, L., L. Bradley, A. Smith, and B. Foxwell. 2004a. Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages. J. Immunol. 172:567-576.
34. Williams, L.M., G. Ricchetti, U. Sarma, T. Smallie, and B.M. Foxwell. 2004b. Interleukin-10 suppression of myeloid cell activation - a continuing puzzle. Immunology. 113:281-292. doi:10.1111/j.1365-2567.2004.01988.x
35. Yasukawa, H., M. Ohishi, H. Mori, M. Murakami, T. Chinen, D. Aki, T. Hanada, K. Takeda, S. Akira, M. Hoshijima, et al. 2003. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat. Immunol. 4:551-556. doi:10.1038/ni938