TGF-β conditions intestinal T cells to express increased levels of miR-155, associated with down-regulation of IL-2 and itk mRNA

Mucosal Immunology

Volumn 6, Issue 1, 2013, Pages 167-176

  Das, L M ^a   Torres Castillo, M D L A ^a   Gill, T ^a   Levine, A D ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ENZYME; GAMMA INTERFERON; INDUCIBLE T CELL KINASE; INTERLEUKIN 2; MESSENGER RNA; MICRORNA 155; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; BLOOD SAMPLING; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME ASSAY; GENE; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOMODULATION; INDUCIBLE T CELL KINASE GENE; INTERLEUKIN 2 GENE; INTESTINE CELL; LAMINA PROPRIA; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MOLECULAR DYNAMICS; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; UPREGULATION;

EID: 84874087148     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2012.60     Document Type: Article

References (59)

1. Faria, A. M. & Weiner, H. L. Oral tolerance: therapeutic implications for autoimmune diseases. Clin. Dev. Immunol. 13, 143-157 (2006). (Pubitemid 44950033)
2. Izcue, A., Coombes, J. L. & Powrie, F. Regulatory T cells suppress systemic and mucosal immune activation to control intestinal inflammation. Immunol. Rev. 212, 256-271 (2006). (Pubitemid 44116713)
3. Feagins, L. A. Role of transforming growth factor-beta in inflammatory bowel disease and colitis-associated colon cancer. Inflamm. Bowel Dis. 16, 1963-1968 (2010).
4. Neurath, M. F., Fuss, I., Kelsall, B. L., Presky, D. H., Waegell, W. & Strober, W. Experimental granulomatous colitis in mice is abrogated by induction of TGF-beta-mediated oral tolerance. J. Exp. Med. 183, 2605-2616 (1996). (Pubitemid 26192369)
5. Powrie, F., Carlino, J., Leach, M. W., Mauze, S. & Coffman, R. L. A critical role for transforming growth factor-beta but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J. Exp. Med. 183, 2669-2674 (1996).
6. Fahlen, L. et al. T cells that cannot respond to TGF-beta escape control by CD4(+)CD25(+) regulatory T cells. J. Exp. Med. 201, 737-746 (2005). (Pubitemid 40395119)
7. McKarns, S. C. & Schwartz, R. H. Distinct effects of TGF-beta 1 on CD4+ and CD8+ T cell survival, division, and IL-2 production: a role for T cell intrinsic Smad3. J. Immunol. 174, 2071-2083 (2005). (Pubitemid 40223950)
8. Ebert, E. C. et al. Patients with inflammatory bowel disease may have a transforming growth factor-beta-, interleukin (IL)-2- or IL-10-deficient state induced by intrinsic neutralizing antibodies. Clin. Exp. Immunol. 155, 65-71 (2009).
9. Del Zotto, B., Mumolo, G., Pronio, A. M., Montesani, C., Tersigni, R. & Boirivant, M. TGF-beta1 production in inflammatory bowel disease: differing production patterns in Crohn's disease and ulcerative colitis. Clin. Exp. Immunol. 134, 120-126 (2003). (Pubitemid 37186597)
10. Duchmann, R., Kaiser, I., Hermann, E., Mayet, W., Ewe, K. & Meyer zum Buschenfelde, K. H. Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clin. Exp. Immunol. 102, 448-455 (1995). (Pubitemid 26013210)
11. Monteleone, G., Pallone, F. & MacDonald, T. T. Emerging immunological targets in inflammatory bowel disease. Curr. Opin. Pharmacol. 11, 640-645 (2011).
12. Das, L. & Levine, A. D. TGF-beta inhibits IL-2 production and promotes cell cycle arrest in TCR-activated effector/memory T cells in the presence of sustained TCR signal transduction. J. Immunol. 180, 1490-1498 (2008).
13. Braunstein, J. et al. Up-regulation of the phosphoinositide 3-kinase pathway in human lamina propria T lymphocytes. Clin. Exp. Immunol. 151, 496-504 (2008). (Pubitemid 351160720)
14. Chen, C. H. et al. Transforming growth factor beta blocks Tec kinase phosphorylation, Ca2+ influx, and NFATc translocation causing inhibition of T cell differentiation. J. Exp. Med. 197, 1689-1699 (2003).
15. Ragin, M. J., Hu, J., Henderson, A. J. & August, A. A role for the Tec family kinase ITK in regulating SEB-induced interleukin-2 production in vivo via c-jun phosphorylation. BMC Immunol. 6, 19 (2005).
16. Nana-Sinkam, S. P. & Croce, C. M. MicroRNAs as therapeutic targets in cancer. Transl. Res. 157, 216-225 (2011).
17. O'Connell, R. M., Rao, D. S., Chaudhuri, A. A. & Baltimore, D. Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10, 111-122 (2010).
18. Polikepahad, S. et al. Proinflammatory role for let-7 microRNAS in experimental asthma. J. Biol. Chem. 285, 30139-30149 (2010).
19. Tsitsiou, E. & Lindsay, M. A. microRNAs and the immune response. Curr. Opin. Pharmacol. 9, 514-520 (2009).
20. Lu, L. F. et al. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity 30, 80-91 (2009).
21. Baltimore, D., Boldin, M. P., O'Connell, R. M., Rao, D. S. & Taganov, K. D. MicroRNAs: new regulators of immune cell development and function. Nat. Immunol. 9, 839-845 (2008). (Pubitemid 352038302)
22. Wang, P. et al. 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 (2010).
23. Rodriguez, A. et al. Requirement of bic/microRNA-155 for normal immune function. Science 316, 608-611 (2007). (Pubitemid 46683148)
24. Thai, T. H. et al. Regulation of the germinal center response by microRNA-155. Science 316, 604-608 (2007).
25. Bhattacharyya, S. et al. Elevated miR-155 promotes inflammation in cystic fibrosis by driving hyperexpression of interleukin-8. J. Biol. Chem. 286, 11604-11615 (2011).
26. Divekar, A. A., Dubey, S., Gangalum, P. R. & Singh, R. R. Dicer insufficiency and microRNA-155 overexpression in lupus regulatory T cells: an apparent paradox in the setting of an inflammatory milieu. J. Immunol. 186, 924-930 (2011).
27. Louafi, F., Martinez-Nunez, R. T. & Sanchez-Elsner, T. MicroRNA-155 targets SMAD2 and modulates the response of macrophages to transforming growth factor-{beta}. J. Biol. Chem. 285, 41328-41336 (2010).
28. Rai, D., Kim, S. W., McKeller, M. R., Dahia, P. L. & Aguiar, R. C. Targeting of SMAD5 links microRNA-155 to the TGF-beta pathway and lymphomagenesis. Proc. Natl. Acad. Sci. USA 107, 3111-3116 (2010).
29. Kong, W. et al. MicroRNA-155 is regulated by the transforming growth factor beta/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol. Cell Biol. 28, 6773-6784 (2008).
30. Martin, M. M., Lee, E. J., Buckenberger, J. A., Schmittgen, T. D. & Elton, T. S. MicroRNA-155 regulates human angiotensin II type 1 receptor expression in fibroblasts. J. Biol. Chem. 281, 18277-18284 (2006). (Pubitemid 44035484)
31. Banerjee, A., Schambach, F., DeJong, C. S., Hammond, S. M. & Reiner, S. L. Micro-RNA-155 inhibits IFN-gamma signaling in CD4+ T cells. Eur. J. Immunol. 40, 225-231 (2010).
32. Shull, M. M. et al. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359, 693-699 (1992).
33. Monteleone, G., Boirivant, M., Pallone, F. & MacDonald, T. T. TGF-beta1 and Smad7 in the regulation of IBD. Mucosal. Immunol. 1 (Suppl 1), S50 - S53 (2008).
34. Mantel, P. Y. & Schmidt-Weber, C. B. Transforming growth factor-beta: recent advances on its role in immune tolerance. Methods Mol. Biol. 677, 303-338 (2011).
35. Tiemessen, M. M. et al. Transforming growth factor-beta inhibits human antigen-specific CD4+ T cell proliferation without modulating the cytokine response. Int. Immunol. 15, 1495-1504 (2003). (Pubitemid 37536750)
36. Belver, L., Papavasiliou, F. N. & Ramiro, A. R. MicroRNA control of lymphocyte differentiation and function. Curr. Opin. Immunol. 23, 368-373 (2011).
37. Wu, H. et al. miRNA profiling of naive, effector and memory CD8 T cells. PLoS One 2, e1020 (2007).
38. Weitzel, R. P. et al. microRNA 184 regulates expression of NFAT1 in umbilical cord blood CD4+ T cells. Blood 113, 6648-6657 (2009).
39. Li, Q. J. et al. miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell 129, 147-161 (2007).
40. Curtale, G. et al. An emerging player in the adaptive immune response: microRNA-146a is a modulator of IL-2 expression and activation-induced cell death in T lymphocytes. Blood 115, 265-273 (2010).
41. Pekow, J. R. et al. miR-143 and miR-145 are downregulated in ulcerative colitis: putative regulators of inflammation and protooncogenes. Inflamm. Bowel. Dis. 18, 94-100 (2012).
42. Biton, M. et al. Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat. Immunol. 12, 239-246 (2011).
43. Faraoni, I., Antonetti, F. R., Cardone, J. & Bonmassar, E. miR-155 gene: a typical multifunctional microRNA. Biochim. Biophys. Acta 1792, 497-505 (2009).
44. O'Connell, R. M., Chaudhuri, A. A., Rao, D. S. & Baltimore, D. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc. Natl. Acad. Sci. USA 106, 7113-7118 (2009).
45. Haasch, D. et al. T cell activation induces a noncoding RNA transcript sensitive to inhibition by immunosuppressant drugs and encoded by the proto-oncogene, BIC. Cell Immunol. 217, 78-86 (2002). (Pubitemid 35352162)
46. Vigorito, E. et al. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 27, 847-859 (2007). (Pubitemid 350258623)
47. Lu, T. X., Munitz, A. & Rothenberg, M. E. MicroRNA-21 is up-regulated in allergic airway inflammation and regulates IL-12p35 expression. J. Immunol. 182, 4994-5002 (2009).
48. Trotta, R. et al. miR-155 regulates IFN-gamma production in natural killer cells. Blood 119, 3478-3485 (2012).
49. Oertli, M., Engler, D. B., Kohler, E., Koch, M., Meyer, T. F. & Muller, A. MicroRNA-155 is essential for the T cell-mediated control of Helicobacter pylori infection and for the induction of chronic Gastritis and Colitis. J. Immunol. 187, 3578-3586 (2011).
50. Kurowska-Stolarska, M. et al. MicroRNA-155 as a proinflammatory regulator in clinical and experimental arthritis. Proc. Natl. Acad. Sci. USA 108, 11193-11198 (2011).
51. Ranganathan, P. et al. Regulation of acute graft-versus-host disease by microRNA-155. Blood 119, 4786-4797 (2012).
52. Ceppi, M. et al. MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc. Natl. Acad. Sci. USA 106, 2735-2740 (2009).
53. Bazzoni, F. et al. Induction and regulatory function of miR-9 in human monocytes and neutrophils exposed to proinflammatory signals. Proc. Natl. Acad. Sci. USA 106, 5282-5287 (2009).
54. Schaeffer, E. M., Broussard, C., Debnath, J., Anderson, S., McVicar, D. W. & Schwartzberg, P. L. Tec family kinases modulate thresholds for thymocyte development and selection. J. Exp. Med. 192, 987-1000 (2000).
55. Yamamoto, M. et al. miR-155, a modulator of FOXO3a protein expression, is underexpressed and cannot be upregulated by stimulation of HOZOT, a line of multifunctional Treg. PLoS One 6, e16841 (2011).
56. Xiao, B. et al. Induction of microRNA-155 during Helicobacter pylori infection and its negative regulatory role in the inflammatory response. J. Infect. Dis. 200, 916-925 (2009).
57. Sturm, A., Itoh, J., Jacobberger, J. W. & Fiocchi, C. p53 negatively regulates intestinal immunity by delaying mucosal T cell cycling. J. Clin. Invest. 109, 1481-1492 (2002). (Pubitemid 34596174)
58. Gruber, A. R., Lorenz, R., Bernhart, S. H., Neubock, R. & Hofacker, I. L. The Vienna RNA websuite. Nucleic Acids Res. 36 (Web Server issue), W70 - W74 (2008).
59. Peltier, H. J. & Latham, G. J. Normalization of microRNA expression levels in quantitative RT-PCR assays: identification of suitable reference RNA targets in normal and cancerous human solid tissues. RNA 14, 844-852 (2008). (Pubitemid 351574906)