The role of Ets2 transcription factor in the induction of microrna-155 (miR-155) by lipopolysaccharide and its targeting by interleukin-10

Journal of Biological Chemistry

Volumn 289, Issue 7, 2014, Pages 4316-4325

  Quinn, Susan R ^a   Mangan, Niamh E ^b   Caffrey, Brian E ^a   Gantier, Michael P ^b   Williams, Bryan R G ^b   Hertzog, Paul J ^b   McCoy, Claire E ^b   O'Neill, Luke A J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTORS;

INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MICRORNAS;

TRANSCRIPTION;

INTERLEUKIN 10; LIPOPOLYSACCHARIDE; MESSENGER RNA; MICRORNA 155; PRIMARY MICRORNA 155; TRANSCRIPTION FACTOR ETS 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; GENE CONTROL; GENE FUNCTION; GENE INDUCTION; GENETIC CONSERVATION; HUMAN; HUMAN CELL; INFLAMMATION; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; TATA BOX; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; UPREGULATION;

ETS FAMILY TRANSCRIPTION FACTOR; ETS2; INTERLEUKIN; INTERLEUKIN 10; LIPOPOLYSACCHARIDE (LPS); MICRORNA; MIR-155; SHIP1; TLR4; TOLL-LIKE RECEPTORS (TLR);

ANIMALS; CELL LINE; HUMANS; INFLAMMATION; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MICE; MICRORNAS; PROTO-ONCOGENE PROTEIN C-ETS-2; RESPONSE ELEMENTS;

EID: 84894177746     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.522730     Document Type: Article

References (35)

1. Janeway, C. A., Jr., and Medzhitov, R. (2002) Innate immune recognition. Annu. Rev. Immunol. 20, 197-216
2. Guo, H., Ingolia, N. T., Weissman, J. S., and Bartel, D. P. (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466, 835-840
3. O'Neill, L. A., Sheedy, F. J., and McCoy, C. E. (2011) MicroRNAs: the fine-tuners of Toll-like receptor signalling. Nat. Rev. Immunol. 11, 163-175
4. Clurman, B. E., and Hayward, W. S. (1989) Multiple proto-oncogene activations in avian leukosis virus-induced lymphomas: evidence for stagespecific events. Mol. Cell. Biol. 9, 2657-2664
5. O'Connell, R. M., Taganov, K. D., Boldin, M. P., Cheng, G., and Baltimore, D. (2007) MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. U.S.A. 104, 1604-1609
6. O'Connell, R. M., Chaudhuri, A. A., Rao, D. S., and Baltimore, D. (2009) Inositol phosphatase SHIP1 is a primary target of miR-155. Proc. Natl. Acad. Sci. U.S.A. 106, 7113-7118
7. An, H., Xu, H., Zhang, M., Zhou, J., Feng, T., Qian, C., Qi, R., and Cao, X. (2005) Src homology 2 domain-containing inositol-5-phosphatase 1 (SHIP1) negatively regulates TLR4-mediated LPS response primarily through a phosphatase activity-and PI-3K-independent mechanism. Blood 105, 4685-4692
8. Wang, P., Hou, J., Lin, L., Wang, C., Liu, X., Li, D., Ma, F., Wang, Z., and Cao, X. (2010) Inducible microRNA-155 feedback promotes type I IFN signaling in antiviral innate immunity by targeting suppressor of cytokine signaling 1. J. Immunol. 185, 6226-6233
9. Quinn, S. R., and O'Neill, L. A. (2011) A trio of microRNAs that control Toll-like receptor signalling. Int. Immunol. 23, 421-425
10. McCoy, C. E., Sheedy, F. J., Qualls, J. E., Doyle, S. L., Quinn, S. R., Murray, P. J., and O'Neill, L. A. (2010) IL-10 inhibits miR-155 induction by toll-like receptors. J. Biol. Chem. 285, 20492-20498
11. Murray, P. J. (2006) Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr. Opin. Pharmacol. 6, 379-386
12. Yin, Q., Wang, X., McBride, J., Fewell, C., and Flemington, E. (2008) B-cell receptor activation induces BIC/miR-155 expression through a conserved AP-1 element. J. Biol. Chem. 283, 2654-2662
13. Kühn, R., Löhler, J., Rennick, D., Rajewsky, K., and Müller, W. (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263-274
14. Bala, S., Marcos, M., Kodys, K., Csak, T., Catalano, D., Mandrekar, P., and Szabo, G. (2011) Up-regulation of microRNA-155 in macrophages contributes to increased tumor necrosis factor (TNFα) production via increased mRNA half-life in alcoholic liver disease. J. Biol. Chem. 286, 1436-1444
15. Murray, P. J. (2006) STAT3-mediated anti-inflammatory signalling. Biochem. Soc. Trans. 34, 1028-1031
16. Rodriguez, A., Vigorito, E., Clare, S., Warren, M. V., Couttet, P., Soond, D. R., van Dongen, S., Grocock, R. J., Das, P. P., Miska, E. A., Vetrie, D., Okkenhaug, K., Enright, A. J., Dougan, G., Turner, M., and Bradley, A. (2007) Requirement of bic/microRNA-155 for normal immune function. Science 316, 608-611
17. O'Connell, R. M., Kahn, D., Gibson, W. S., Round, J. L., Scholz, R. L., Chaudhuri, A. A., Kahn, M. E., Rao, D. S., and Baltimore, D. (2010) MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 33, 607-619
18. Ceppi, M., Pereira, P. M., Dunand-Sauthier, I., Barras, E., Reith, W., Santos, M. A., and Pierre, P. (2009) MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 106, 2735-2740
19. Chen, C. Z., Li, L., Lodish, H. F., and Bartel, D. P. (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science 303, 83-86
20. Lindsay, M. A. (2008) microRNAs and the immune response. Trends Immunol. 29, 343-351
21. Gallant, S., and Gilkeson, G. (2006) ETS transcription factors and regulation of immunity. Archivum Immunologiae et Therapiae Experimentalis 54, 149-163
22. Wang, C. Y., Petryniak, B., Ho, I. C., Thompson, C. B., and Leiden, J. M. (1992) Evolutionarily conserved Ets family members display distinctDNA binding specificities. J. Exp. Med. 175, 1391-1399
23. Blumenthal, S. G., Aichele, G., Wirth, T., Czernilofsky, A. P., Nordheim, A., and Dittmer, J. (1999) Regulation of the human interleukin-5 promoter by Ets transcription factors. Ets1 and Ets2, but not Elf-1, cooperate with GATA3 and HTLV-I Tax1. J. Biol. Chem. 274, 12910-12916
24. Boulukos, K. E., Pognonec, P., Sariban, E., Bailly, M., Lagrou, C., and Ghysdael, J. (1990) Rapid and transient expression of Ets2 in mature macrophages following stimulation with cMGF, LPS, and PKC activators. Genes Dev. 4, 401-409
25. Sweet, M. J., Stacey, K. J., Ross, I. L., Ostrowski, M. C., and Hume, D. A. (1998) Involvement of Ets, rel and Sp1-like proteins in lipopolysaccharidemediated activation of the HIV-1 LTR in macrophages. J. Inflamm. 48, 67-83
26. Dittmer, J., and Nordheim, A. (1998) Ets transcription factors and human disease. Biochim. Biophys. Acta 1377, F1-11
27. Ruggiero, T., Trabucchi, M., De Santa, F., Zupo, S., Harfe, B. D., McManus, M. T., Rosenfeld, M. G., Briata, P., and Gherzi, R. (2009) LPS induces KH-type splicing regulatory protein-dependent processing of microRNA-155 precursors in macrophages. FASEB J. 23, 2898-2908
28. Trabucchi, M., Briata, P., Filipowicz, W., Ramos, A., Gherzi, R., and Rosenfeld, M. G. (2011) KSRP Promotes the Maturation of a Group of miRNA Precuresors. Adv. Exp. Med. Biol. 700, 36-42
29. Cheung, S. T., So, E. Y., Chang, D., Ming-Lum, A., and Mui, A. L. (2013) Interleukin-10 inhibits lipopolysaccharide induced miR-155 precursor stability and maturation. PloS One 8, e71336
30. Chen, Y., Liu, W., Sun, T., Huang, Y., Wang, Y., Deb, D. K., Yoon, D., Kong, J., Thadhani, R., and Li, Y. C. (2013) 1,25-Dihydroxyvitamin D promotes negative feedback regulation of TLR signaling via targeting microRNA-155-SOCS1 in macrophages. J. Immunol. 190, 3687-3695
31. Dai, Y., Diao, Z., Sun, H., Li, R., Qiu, Z., and Hu, Y. (2011) MicroRNA-155 is involved in the remodelling of human-trophoblast-derived HTR-8/ SVneo cells induced by lipopolysaccharides. Hum. Reprod. 26, 1882-1891
32. Escobar, T., Yu, C. R., Muljo, S. A., and Egwuagu, C. E. (2013) STAT3 activates miR-155 in Th17 cells and acts in concert to promote experimental autoimmune uveitis. Invest. Ophthalmol. Vis. Sci. 54, 4017-4025
33. Tili, E., Michaille, J. J., Cimino, A., Costinean, S., Dumitru, C. D., Adair, B., Fabbri, M., Alder, H., Liu, C. G., Calin, G. A., and Croce, C. M. (2007) Modulation of miR-155 and miR-125b levels following lipopolysaccharide/ TNF stimulation and their possible roles in regulating the response to endotoxin shock. J. Immunol. 179, 5082-5089
34. Rennick, D., Davidson, N., and Berg, D. (1995) Interleukin-10 gene knockout mice: a model of chronic inflammation. Clin. Immunol. Immunopathol. 76, S174-178
35. Berg, D. J., Kühn, R., Rajewsky, K., Müller, W., Menon, S., Davidson, N., Grünig, G., and Rennick, D. (1995) Interleukin-10 is a central regulator of the response to LPS in murine models of endotoxic shock and the Shwartzman reaction but not endotoxin tolerance. J. Clin. Invest. 96, 2339-2347