The microRNA miR-182 is induced by IL-2 and promotes clonal expansion of activated helper T lymphocytes

Nature Immunology

Volumn 11, Issue 11, 2010, Pages 1057-1062

  Stittrich, Anna Barbara ^a   Haftmann, Claudia ^a   Sgouroudis, Evridiki ^a   Kühl, Anja Andrea ^b   Hegazy, Ahmed Nabil ^a,b   Panse, Isabel ^a,b   Riedel, Rene ^a   Flossdorf, Michael ^c   Dong, Jun ^a,b   Fuhrmann, Franziska ^a,d   Heinz, Gitta Anne ^a   Fang, Zhuo ^e   Li, Na ^e   Bissels, Ute ^f   Hatam, Farahnaz ^a   Jahn, Angelina ^a   Hammoud, Ben ^a   Matz, Mareen ^b   Schulze, Felix Michael ^g   Baumgrass, Ria ^a   Bosio, Andreas ^f   Mollenkopf, Hans Joachim ^h   Grün, Joachim ^a   Thiel, Andreas ^b   Chen, Wei ^e   Höfer, Thomas ^c   Loddenkemper, Christoph ^b   Löhning, Max ^a,b   Chang, Hyun Dong ^a   Rajewsky, Nikolaus ^e   Radbruch, Andreas ^a   Mashreghi, Mir Farzin ^a   more..

^a DEUTSCHES RHEUMA FORSCHUNGSZENTRUM   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d ROBERT KOCH INSTITUTE   (Germany)

^e MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^f MILTENYI BIOTEC GMBH   (Germany)

^g UNIVERSITY OF GREIFSWALD   (Germany)

^h MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 2; MICRORNA; TRANSCRIPTION FACTOR FKHR;

ANIMAL CELL; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; HELPER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA ANALYSIS; T LYMPHOCYTE ACTIVATION;

ANIMALS; ARTHRITIS; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; HUMANS; INTERLEUKIN-2; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICRORNAS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 77958149675     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.1945     Document Type: Article

References (41)

1. Iezzi, G., Karjalainen, K. & Lanzavecchia, A. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 8, 89-95 (1998).
2. Van Stipdonk, M.J., Lemmens, E.E. & Schoenberger, S.P. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol. 2, 423-429 (2001).
3. Jelley-Gibbs, D.M., Lepak, N.M., Yen, M. & Swain, S.L. Two distinct stages in the transition from naive CD4 T cells to effectors, early antigen-dependent and late cytokine-driven expansion and differentiation. J. Immunol. 165, 5017-5026 (2000).
4. Peng, S.L. Foxo in the immune system. Oncogene 27, 2337-2344 (2008).
5. Pellegrini, M. et al. Loss of Bim increases T cell production and function in interleukin 7 receptor-defcient mice. J. Exp. Med. 200, 1189-1195 (2004).
6. Fabre, S. et al. Stable activation of phosphatidylinositol 3-kinase in the T cell immunological synapse stimulates Akt signaling to FoxO1 nuclear exclusion and cell growth control. J. Immunol. 174, 4161-4171 (2005).
7. Xu, S., Witmer, P.D., Lumayag, S., Kovacs, B. & Valle, D. MicroRNA (miRNA) transcriptome of mouse retina and identifcation of a sensory organ-specifc miRNA cluster. J. Biol. Chem. 282, 25053-25066 (2007).
8. Krek, A. et al. Combinatorial microRNA target predictions. Nat. Genet. 37, 495-500 (2005).
9. Lewis, B.P., Shih, I.H., Jones-Rhoades, M.W., Bartel, D.P. & Burge, C.B. Prediction of mammalian microRNA targets. Cell 115, 787-798 (2003).
10. Orom, U.A., Kauppinen, S. & Lund, A.H. LNA-modifed oligonucleotides mediate specifc inhibition of microRNA function. Gene 372, 137-141 (2006).
11. c family cytokines. Nat. Rev. Immunol. 9, 480-490 (2009).
12. Muller, J., Sperl, B., Reindl, W., Kiessling, A. & Berg, T. Discovery of chromone-based inhibitors of the transcription factor STAT5. ChemBioChem 9, 723-727 (2008).
13. Paust, S. & Cantor, H. Regulatory T cells and autoimmune disease. Immunol. Rev. 204, 195-207 (2005).
14. Oxenius, A. et al. Functional in vivo MHC class II loading by endogenously synthesized glycoprotein during viral infection. J. Immunol. 158, 5717-5726 (1997).
15. Stahl, M. et al. The forkhead transcription factor FoxO regulates transcription of p27Kip1 and Bim in response to IL-2. J. Immunol. 168, 5024-5031 (2002).
16. KIP1. Mol. Cell. Biol. 20, 9138-9148 (2000).
17. Dijkers, P.F., Medema, R.H., Lammers, J.W., Koenderman, L. & Coffer, P.J. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr. Biol. 10, 1201-1204 (2000).
18. Brunet, A. et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868 (1999).
19. Ouyang, W., Beckett, O., Flavell, R.A. & Li, M.O. An essential role of the Forkhead-box transcription factor Foxo1 in control of T cell homeostasis and tolerance. Immunity 30, 358-371 (2009).
20. Kerdiles, Y.M. et al. Foxo1 links homing and survival of naive T cells by regulating L-selectin, CCR7 and interleukin 7 receptor. Nat. Immunol. 10, 176-184 (2009).
21. Essaghir, A., Dif, N., Marbehant, C.Y., Coffer, P.J. & Demoulin, J.B. The transcription of FOXO genes is stimulated by FOXO3 and repressed by growth factors. J. Biol. Chem. 284, 10334-10342 (2009).
22. Al-Mubarak, B., Soriano, F.X. & Hardingham, G.E. Synaptic NMDAR activity suppresses FOXO1 expression via a cis-acting FOXO binding site: FOXO1 is a FOXO target gene. Channels (Austin) 3, 233-238 (2009).
23. + T cell proliferation and effector function. J. Immunol. 174, 3359-3368 (2005).
24. Wells, A.D., Walsh, M.C., Sankaran, D. & Turka, L.A. T cell effector function and anergy avoidance are quantitatively linked to cell division. J. Immunol. 165, 2432-2443 (2000).
25. Naramura, M. et al. c-Cbl and Cbl-b regulate T cell responsiveness by promoting ligand-induced TCR down-modulation. Nat. Immunol. 3, 1192-1199 (2002).
26. Valitutti, S., Muller, S., Cella, M., Padovan, E. & Lanzavecchia, A. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature 375, 148-151 (1995).
27. Salio, M., Valitutti, S. & Lanzavecchia, A. Agonist-induced T cell receptor down-regulation: molecular requirements and dissociation from T cell activation. Eur. J. Immunol. 27, 1769-1773 (1997).
28. Muljo, S.A. et al. Aberrant T cell differentiation in the absence of Dicer. J. Exp. Med. 202, 261-269 (2005).
29. Szabo, S.J. et al. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100, 655-669 (2000).
30. + T cell memory by promoting the generation of IL-7Rα-expressing cells. J. Exp. Med. 204, 547-557 (2007).
31. Long, D. et al. Potent effect of target structure on microRNA function. Nat. Struct. Mol. Biol. 14, 287-294 (2007).
32. Guttilla, I.K. & White, B.A. Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J. Biol. Chem. 284, 23204-23216 (2009).
33. Krutzfeldt, J. et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 438, 685-689 (2005).
34. Wang, V. & Wu, W. MicroRNA-based therapeutics for cancer. BioDrugs 23, 15-23 (2009).
35. Richter, A., Lohning, M. & Radbruch, A. Instruction for cytokine expression in T helper lymphocytes in relation to proliferation and cell cycle progression. J. Exp. Med. 190, 1439-1450 (1999).
36. Chang, H.D. et al. Expression of IL-10 in Th memory lymphocytes is conditional on IL-12 or IL-4, unless the IL-10 gene is imprinted by GATA-3. Eur. J. Immunol. 37, 807-817 (2007).
37. Lexberg, M.H. et al. Th memory for interleukin-17 expression is stable in vivo. Eur. J. Immunol. 38, 2654-2664 (2008).
38. + memory T lymphocytes. J. Immunol. 179, 2389-2396 (2007).
39. Niesner, U. et al. Autoregulation of Th1-mediated infammation by twist1. J. Exp. Med. 205, 1889-1901 (2008).
40. Quah, B.J., Warren, H.S. & Parish, C.R. Monitoring lymphocyte proliferation in vitro and in vivo with the intracellular fuorescent dye carboxyfuorescein diacetate succinimidyl ester. Nat. Protocols 2, 2049-2056 (2007).
41. Mashreghi, M.F. et al. Inhibition of dendritic cell maturation and function is independent of heme oxygenase 1 but requires the activation of STAT3. J. Immunol. 180, 7919-7930 (2008).