Downregulation of microRNA-107 in intestinal CD11c+ myeloid cells in response to microbiota and proinflammatory cytokines increases IL-23p19 expression

European Journal of Immunology

Volumn 44, Issue 3, 2014, Pages 673-682

  Xue, Xiaochang ^a,b   Cao, Anthony T ^a   Cao, Xiaocang ^a   Yao, Suxia ^a   Carlsen, Eric D ^a   Soong, Lynn ^a   Liu, Chang Gong ^c   Liu, Xiuping ^c   Liu, Zhanju ^d   Duck, L Wayne ^e   Elson, Charles O ^e   Cong, Yingzi ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d TONGJI UNIVERSITY   (China)

^e and Clinical Center   (United States)

Author keywords

IL 23p19; Inflammatory bowel disease; MicroRNAs; MiR 107; TLR

Indexed keywords

GAMMA INTERFERON; GLYCOPROTEIN P 15095; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 23P19; INTERLEUKIN 6; MICRORNA 107; MYELOID DIFFERENTIATION FACTOR 88; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; COLITIS; COMMENSAL; CONTROLLED STUDY; DENDRITIC CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; INNATE IMMUNITY; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; MACROPHAGE; MICROFLORA; MOUSE; NONHUMAN; PRIORITY JOURNAL;

IL-23P19; INFLAMMATORY BOWEL DISEASE; MICRORNAS; MIR-107; TLR;

ANIMALS; BACTERIA; BASE PAIRING; BASE SEQUENCE; COLITIS; CYTOKINES; DENDRITIC CELLS; GENE EXPRESSION REGULATION; INFLAMMATION MEDIATORS; INTERLEUKIN-23 SUBUNIT P19; INTESTINES; LIGANDS; MACROPHAGES; MICE; MICE, TRANSGENIC; MICROBIOTA; MICRORNAS; MYELOID CELLS; TOLL-LIKE RECEPTORS;

EID: 84896051012     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343717     Document Type: Article

References (44)

1. Ley, R. E., Peterson, D. A. and Gordon, J. I., Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 2006. 124: 837-848.
2. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S. and Medzhitov, R., Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004. 118: 229-241.
3. Backhed, F., Ding, H., Wang, T., Hooper, L. V., Koh, G. Y., Nagy, A., Semenkovich, C. F. et al., The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci. USA 2004. 101: 15718-15723.
4. Mazmanian, S. K., Liu, C. H., Tzianabos, A. O. and Kasper, D. L., An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005. 122: 107-118.
5. Backhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A. and Gordon, J. I., Host-bacterial mutualism in the human intestine. Science 2005. 307: 1915-1920.
6. Zhao, J., Schloss, P. D., Kalikin, L. M., Carmody, L. A., Foster, B. K., Petrosino, J. F., Cavalcoli, J. D. et al., Decade-long bacterial community dynamics in cystic fibrosis airways. Proc. Natl. Acad. Sci. USA 2012. 109: 5809-5814.
7. Sartor, R. B., Microbial influences in inflammatory bowel diseases. Gastroenterology 2008. 134: 577-594.
8. Elson, C. O., Cong, Y., McCracken, V. J., Dimmitt, R. A., Lorenz, R. G. and Weaver, C. T., Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol. Rev. 2005. 206: 260-276.
9. O'Connell, R. M., Rao, D. S. and Baltimore, D., microRNA regulation of inflammatory responses. Annu. Rev. Immunol. 2012. 30: 295-312.
10. Biton, M., Levin, A., Slyper, M., Alkalay, I., Horwitz, E., Mor, H., Kredo-Russo, S. et al., Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat. Immunol. 2011. 12: 239-246.
11. Paraskevi, A., Theodoropoulos, G., Papaconstantinou, I., Mantzaris, G., Nikiteas, N. and Gazouli, M., Circulating microRNA in inflammatory bowel disease. J. Crohns Colitis 2012. 6: 900-904.
12. Pekow, J. R., Dougherty, U., Mustafi, R., Zhu, H., Kocherginsky, M., Rubin, D. T., Hanauer et al., miR-143 and miR-145 are downregulated in ulcerative colitis: putative regulators of inflammation and protooncogenes. Inflamm. Bowel Dis. 2011. 18: 94-100.
13. Wu, F., Zhang, S., Dassopoulos, T., Harris, M. L., Bayless, T. M., Meltzer, S. J., Brant, S. R. et al., Identification of microRNAs associated with ileal and colonic Crohn's disease. Inflamm. Bowel Dis. 2010. 16: 1729-1738.
14. Wu, F., Zikusoka, M., Trindade, A., Dassopoulos, T., Harris, M. L., Bayless, T. M., Brant et al., MicroRNAs are differentially expressed in ulcerative colitis and alter expression of macrophage inflammatory peptide-2 alpha. Gastroenterology 2008. 135: 1624-1635 e1624.
15. Dalmasso, G., Nguyen, H. T., Yan, Y., Laroui, H., Charania, M. A., Ayyadurai, S., Sitaraman, S. V. et al., Microbiota modulate host gene expression via microRNAs. PLoS One 2011. 6: e19293.
16. Xue, X., Feng, T., Yao, S., Wolf, K. J., Liu, C. G., Liu, X., Elson, C. O. et al., Microbiota downregulates dendritic cell expression of miR-10a, which targets IL-12/IL-23p40. J. Immunol. 2011. 187: 5879-5886.
17. Hennessy, E. J., Sheedy, F. J., Santamaria, D., Barbacid, M. and O'Neill, L. A., Toll-like receptor-4 (TLR4) downregulates microRNA-107, increasing macrophage adhesion via cyclin-dependent kinase 6. J. Biol. Chem. 2011. 286: 25531-25539.
18. Dolt, K. S., Mishra, M. K., Karar, J., Baig, M. A., Ahmed, Z. and Pasha, M. A., cDNA cloning, gene organization and variant specific expression of HIF-1 alpha in high altitude yak (Bos grunniens). Gene 2007. 386: 73-80.
19. Li, X., Zhang, Y., Shi, Y., Dong, G., Liang, J., Han, Y., Wang, X. et al., MicroRNA-107, an oncogene microRNA that regulates tumour invasion and metastasis by targeting DICER1 in gastric cancer. J. Cell. Mol. Med. 2011. 15: 1887-1895.
20. Feng, T., Wang, L., Schoeb, T. R., Elson, C. O. and Cong, Y., Microbiota innate stimulation is a prerequisite for T cell spontaneous proliferation and induction of experimental colitis. J. Exp. Med. 2010. 207: 1321-1332.
21. Lodes, M. J., Cong, Y., Elson, C. O., Mohamath, R., Landers, C. J., Targan, S. R., Fort, M. et al., Bacterial flagellin is a dominant antigen in Crohn disease. J. Clin. Invest. 2004. 113: 1296-1306.
22. Cao, A. T., Yao, S., Gong, B., Elson, C. O. and Cong, Y., Th17 cells upregulate polymeric Ig receptor and intestinal IgA and contribute to intestinal homeostasis. J. Immunol. 2012. 189: 4666-4673.
23. Duck, L. W., Walter, M. R., Novak, J., Kelly, D., Tomasi, M., Cong, Y. and Elson, C. O., Isolation of flagellated bacteria implicated in Crohn's disease. Inflamm. Bowel Dis. 2007. 13: 1191-1201.
24. Akira, S., Uematsu, S. and Takeuchi, O., Pathogen recognition and innate immunity. Cell 2006. 124: 783-801.
25. Medzhitov, R., TLR-mediated innate immune recognition. Semin. Immunol. 2007. 19: 1-2.
26. Medzhitov, R., Preston-Hurlburt, P., Kopp, E., Stadlen, A., Chen, C., Ghosh, S. and Janeway, C. A., Jr., MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 1998. 2: 253-258.
27. Lewis, B. P., Burge, C. B. and Bartel, D. P., Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005. 120: 15-20.
28. Wu, H. J., Ivanov, II, Darce, J., Hattori, K., Shima, T., Umesaki, Y., Littman, D. R. et al., Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010. 32: 815-827.
29. Wu, S., Rhee, K. J., Albesiano, E., Rabizadeh, S., Wu, X., Yen, H. R., Huso, D. L. et al., A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat. Med. 2009. 15: 1016-1022.
30. Comelli, E. M., Simmering, R., Faure, M., Donnicola, D., Mansourian, R., Rochat, F., Corthesy-Theulaz, I. et al., Multifaceted transcriptional regulation of the murine intestinal mucus layer by endogenous microbiota. Genomics 2008. 91: 70-77.
31. Chowdhury, S. R., King, D. E., Willing, B. P., Band, M. R., Beever, J. E., Lane, A. B., Loor, J. J. et al., Transcriptome profiling of the small intestinal epithelium in germfree versus conventional piglets. BMC Genomics 2007. 8: 215.
32. Chen, H. Y., Lin, Y. M., Chung, H. C., Lang, Y. D., Lin, C. J., Huang, J., Wang, W. C. et al., miR-103/107 promote metastasis of colorectal cancer by targeting the metastasis suppressors DAPK and KLF4. Cancer Res. 2012. 72: 3631-3641.
33. Inoue, T., Iinuma, H., Ogawa, E., Inaba, T. and Fukushima, R., Clinicopathological and prognostic significance of microRNA-107 and its relationship to DICER1 mRNA expression in gastric cancer. Oncol. Rep. 2012. 27: 1759-1764.
34. Martello, G., Rosato, A., Ferrari, F., Manfrin, A., Cordenonsi, M., Dupont, S., Enzo, E. et al., A microRNA targeting dicer for metastasis control. Cell 2010. 141: 1195-1207.
35. Trinchieri, G., Pflanz, S. and Kastelein, R. A., The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 2003. 19: 641-644.
36. Ahern, P. P., Schiering, C., Buonocore, S., McGeachy, M. J., Cua, D. J., Maloy, K. J. and Powrie, F., Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity 2010. 33: 279-288.
37. Elson, C. O., Cong, Y., Weaver, C. T., Schoeb, T. R., McClanahan, T. K., Fick, R. B. and Kastelein, R. A., Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice. Gastroenterology 2007. 132: 2359-2370.
38. Geremia, A., Arancibia-Carcamo, C. V., Fleming, M. P., Rust, N., Singh, B., Mortensen, N. J., Travis, S. P. et al., IL-23-responsive innate lymphoid cells are increased in inflammatory bowel disease. J. Exp. Med. 2011. 208: 1127-1133.
39. Qiu, J., Heller, J. J., Guo, X., Chen, Z. M., Fish, K., Fu, Y. X. and Zhou, L., The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 2012. 36: 92-104.
40. Yen, D., Cheung, J., Scheerens, H., Poulet, F., McClanahan, T., McKenzie, B., Kleinschek, M. A. et al., IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J. Clin. Invest. 2006. 116: 1310-1316.
41. Cong, Y., Feng, T., Fujihashi, K., Schoeb, T. R. and Elson, C. O., A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc. Natl. Acad. Sci. USA 2009. 106: 19256-19261.
42. Wang, Q., Garrity, G. M., Tiedje, J. M. and Cole, J. R., Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007. 73: 5261-5267.
43. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J., Basic local alignment search tool. J. Mol. Biol. 1990. 215: 403-410.
44. Kolli, D., Bao, X., Liu, T., Hong, C., Wang, T., Garofalo, R. P. and Casola, A., Human metapneumovirus glycoprotein G inhibits TLR4-dependent signaling in monocyte-derived dendritic cells. J. Immunol. 2011. 187: 47-54.