miR-146a controls the resolution of T cell responses in mice

Journal of Experimental Medicine

Volumn 209, Issue 9, 2012, Pages 1655-1670

  Yang, Lili ^a   Boldin, Mark P ^b   Yu, Yang ^a   Liu, Claret Siyuan ^a   Ea, Chee Kwee ^c   Ramakrishnan, Parameswaran ^a   Taganov, Konstantin D ^d   Zhao, Jimmy L ^a   Baltimore, David ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^c UNIVERSITY OF MALAYA   (Malaysia)

^d MILLIPORE CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; MICRORNA 146A; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ARTICLE; AUTOIMMUNITY; CHRONIC INFLAMMATION; CONTROLLED STUDY; FEMALE; IMMUNE RESPONSE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; T LYMPHOCYTE;

ANIMALS; ANTIGENS; AUTOIMMUNE DISEASES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; GENE EXPRESSION REGULATION; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICRORNAS; NF-KAPPA B; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TNF RECEPTOR-ASSOCIATED FACTOR 6;

EID: 84866354593     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20112218     Document Type: Article

References (46)

1. Ambros, V. 2004. The functions of animal microRNAs. Nature. 431: 350-355. http://dx.doi.org/10.1038/nature02871
2. Baltimore, D., M.P. Boldin, R.M. O'Connell, D.S. Rao, and K.D. Taganov. 2008. MicroRNAs: new regulators of immune cell development and function. Nat. Immunol. 9: 839-845. http://dx.doi.org/10.1038/ni.f.209
3. Bartel, D.P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 116: 281-297. http://dx.doi.org/10.1016/S0092-8674(04)00045-5
4. Beg, A.A., W.C. Sha, R.T. Bronson, and D. Baltimore. 1995. Constitutive NF-kappa B activation, enhanced granulopoiesis, and neonatal lethality in I kappa B alpha-deficient mice. Genes Dev. 9:2736-2746. http://dx.doi.org/10.1101/gad.9.22.2736
5. Boldin, M.P., K.D. Taganov, D.S. Rao, L. Yang, J.L. Zhao, M. Kalwani, Y. Garcia-Flores, M. Luong, A. Devrekanli, J. Xu, et al. 2011. miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J. Exp. Med. 208: 1189-1201. http://dx.doi.org/10.1084/jem.20101823
6. Chassin, C., M. Kocur, J. Pott, C.U. Duerr, D. Gütle, M. Lotz, and M.W. Hornef. 2010. miR-146a mediates protective innate immune tolerance in the neonate intestine. Cell Host Microbe. 8: 358-368. http://dx.doi.org/10.1016/j.chom.2010.09.005
7. Curtale, G., F. Citarella, C. Carissimi, M. Goldoni, N. Carucci, V. Fulci, D. Franceschini, F. Meloni, V. Barnaba, and G. Macino. 2010. 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. http://dx.doi.org/10.1182/blood-2009-06-225987
8. Hamalainen, H.K., J.C. Tubman, S. Vikman, T. Kyrölä, E. Ylikoski, J.A. Warrington, and R. Lahesmaa. 2001. Identification and validation of endogenous reference genes for expression profiling of T helper cell differentiation by quantitative real-time RT-PCR. Anal. Biochem. 299:63- 70. http://dx.doi.org/10.1006/abio.2001.5369
9. Ghosh, S., and M.S. Hayden. 2008. New regulators of NF-kappaB in inflammation. Nat. Rev. Immunol. 8: 837-848. http://dx.doi.org/10.1038/nri2423
10. Hannum, C., J.H. Freed, G. Tarr, J. Kappler, and P. Marrack. 1984. Biochemistry and distribution of the T cell receptor. Immunol. Rev. 81:161-176. http://dx.doi.org/10.1111/j.1600-065X.1984.tb01109.x
11. Hao, S., and D. Baltimore. 2009. The stability of mRNA influences the temporal order of the induction of genes encoding inflammatory molecules. Nat. Immunol. 10: 281-288. http://dx.doi.org/10.1038/ni.1699
12. Hoffmann, A., A. Levchenko, M.L. Scott, and D. Baltimore. 2002. The IkappaB-NF-kappaB signaling module: temporal control and selective gene activation. Science. 298: 1241-1245. http://dx.doi.org/10.1126/science.1071914
13. Hou, J., P. Wang, L. Lin, X. Liu, F. Ma, H. An, Z. Wang, and X. Cao. 2009. MicroRNA-146a feedback inhibits RIG-I-dependent Type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2. J. Immunol. 183: 2150-2158. http://dx.doi.org/10.4049/jimmunol.0900707
14. Isakov, N., and A. Altman. 2002. Protein kinase C(theta) in T cell activation. Annu. Rev. Immunol. 20: 761-794. http://dx.doi.org/10.1146/annurev.immunol.20.100301.064807
15. Itoh, M., T. Takahashi, N. Sakaguchi, Y. Kuniyasu, J. Shimizu, F. Otsuka, and S. Sakaguchi. 1999. Thymus and autoimmunity: production of CD25+CD4+ naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J. Immunol. 162:5317-5326.
16. Jost, P.J., and J. Ruland. 2007. Aberrant NF-kappaB signaling in lymphoma: mechanisms, consequences, and therapeutic implications. Blood. 109:2700-2707.
17. Karin, M., and F.R. Greten. 2005. NF-kappaB: linking inflammation and immunity to cancer development and progression. Nat. Rev. Immunol. 5: 749-759. http://dx.doi.org/10.1038/nri1703
18. King, C.G., T. Kobayashi, P.J. Cejas, T. Kim, K. Yoon, G.K. Kim, E. Chiffoleau, S.P. Hickman, P.T. Walsh, L.A. Turka, and Y. Choi. 2006. TRAF6 is a T cell-intrinsic negative regulator required for the maintenance of immune homeostasis. Nat. Med. 12: 1088-1092. http://dx.doi.org/10.1038/nm1449
19. Klement, J.F., N.R. Rice, B.D. Car, S.J. Abbondanzo, G.D. Powers, P.H. Bhatt, C.H. Chen, C.A. Rosen, and C.L. Stewart. 1996. IkappaBalpha deficiency results in a sustained NF-kappaB response and severe widespread dermatitis in mice. Mol. Cell. Biol. 16:2341-2349.
20. Lee, E.G., D.L. Boone, S. Chai, S.L. Libby, M. Chien, J.P. Lodolce, and A. Ma. 2000. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science. 289: 2350-2354. http://dx.doi.org/10.1126/science.289.5488.2350
21. Li, Q., and I.M. Verma. 2002. NF-kappaB regulation in the immune system. Nat. Rev. Immunol. 2: 725-734. http://dx.doi.org/10.1038/nri910
22. Li, Q.J., J. Chau, P.J. Ebert, G. Sylvester, H. Min, G. Liu, R. Braich, M. Manoharan, J. Soutschek, P. Skare, et al. 2007. miR-181a is an intrinsic modulator of T cell sensitivity and selection. Cell. 129: 147-161. http://dx.doi.org/10.1016/j.cell.2007.03.008
23. Lu, L.F., M.P. Boldin, A. Chaudhry, L.L. Lin, K.D. Taganov, T. Hanada, A. Yoshimura, D. Baltimore, and A.Y. Rudensky. 2010. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell. 142: 914-929. http://dx.doi.org/10.1016/j.cell.2010.08.012
24. Maitra, U., S. Davis, C.M. Reilly, and L. Li. 2009. Differential regulation of Foxp3 and IL-17 expression in CD4 T helper cells by IRAK-1. J. Immunol. 182: 5763-5769. http://dx.doi.org/10.4049/jimmunol.0900124
25. Malek, T.R. 2008. The biology of interleukin-2. Annu. Rev. Immunol. 26:453- 479. http://dx.doi.org/10.1146/annurev.immunol.26.021607.090357
26. Monticelli, S., K.M. Ansel, C. Xiao, N.D. Socci, A.M. Krichevsky, T.H. Thai, N. Rajewsky, D.S. Marks, C. Sander, K. Rajewsky, et al. 2005. MicroRNA profiling of the murine hematopoietic system. Genome Biol. 6:R71. http://dx.doi.org/10.1186/gb-2005-6-8-r71
27. Nahid, M.A., K.M. Pauley, M. Satoh, and E.K. Chan. 2009. miR-146a is critical for endotoxin-induced tolerance: Implication in innate immunity. J. Biol. Chem. 284: 34590-34599. http://dx.doi.org/10.1074/jbc.M109.056317
28. Nakasa, T., S. Miyaki, A. Okubo, M. Hashimoto, K. Nishida, M. Ochi, and H. Asahara. 2008. Expression of microRNA-146 in rheumatoid arthritis synovial tissue. Arthritis Rheum. 58: 1284-1292. http://dx.doi.org/10.1002/art.23429
29. O'Connell, R.M., D. Kahn, W.S. Gibson, J.L. Round, R.L. Scholz, A.A. Chaudhuri, M.E. Kahn, D.S. Rao, and D. Baltimore. 2010. MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity. 33: 607-619. http://dx.doi.org/10.1016/j.immuni.2010.09.009
30. Oeckinghaus, A., M.S. Hayden, and S. Ghosh. 2011. Crosstalk in NF-κB signaling pathways. Nat. Immunol. 12: 695-708. http://dx.doi.org/10.1038/ni.2065
31. Pearce, E.L., M.C. Walsh, P.J. Cejas, G.M. Harms, H. Shen, L.S. Wang, R.G. Jones, and Y. Choi. 2009. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature. 460: 103-107. http://dx.doi.org/10.1038/nature08097
32. Rodriguez, A., E. Vigorito, S. Clare, M.V. Warren, P. Couttet, D.R. Soond, S. van Dongen, R.J. Grocock, P.P. Das, E.A. Miska, et al. 2007. Requirement of bic/microRNA-155 for normal immune function. Science. 316: 608-611. http://dx.doi.org/10.1126/science.1139253
33. Ruland, J. 2011. Return to homeostasis: downregulation of NF-κB responses. Nat. Immunol. 12: 709-714. http://dx.doi.org/10.1038/ni.2055
34. Schulze-Luehrmann, J., and S. Ghosh. 2006. Antigen-receptor signaling to nuclear factor kappa B. Immunity. 25: 701-715. http://dx.doi.org/10.1016/j.immuni.2006.10.010
35. Stanczyk, J., D.M. Pedrioli, F. Brentano, O. Sanchez-Pernaute, C. Kolling, R.E. Gay, M. Detmar, S. Gay, and D. Kyburz. 2008. Altered expression of MicroRNA in synovial fibroblasts and synovial tissue in rheumatoid arthritis. Arthritis Rheum. 58: 1001-1009. http://dx.doi.org/10.1002/art.23386
36. Sun, L., L. Deng, C.K. Ea, Z.P. Xia, and Z.J. Chen. 2004. The TRAF6 ubiquitin ligase and TAK1 kinase mediate IKK activation by BCL10 and MALT1 in T lymphocytes. Mol. Cell. 14: 289-301. http://dx.doi.org/10.1016/S1097-2765(04)00236-9
37. Taganov, K.D., M.P. Boldin, K.J. Chang, and D. Baltimore. 2006. NF-kappaB- dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. USA. 103: 12481-12486. http://dx.doi.org/10.1073/pnas.0605298103
38. Tang, Y., X. Luo, H. Cui, X. Ni, M. Yuan, Y. Guo, X. Huang, H. Zhou, N. de Vries, P.P. Tak, et al. 2009. MicroRNA-146A contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum. 60: 1065-1075. http://dx.doi.org/10.1002/art.24436
39. Thai, T.H., D.P. Calado, S. Casola, K.M. Ansel, C. Xiao, Y. Xue, A. Murphy, D. Frendewey, D. Valenzuela, J.L. Kutok, et al. 2007. Regulation of the germinal center response by microRNA-155. Science. 316: 604-608. http://dx.doi.org/10.1126/science.1141229
40. Tsitsiou, E., and M.A. Lindsay. 2009. microRNAs and the immune response. Curr. Opin. Pharmacol. 9: 514-520. http://dx.doi.org/10.1016/j.coph.2009.05.003
41. Vallabhapurapu, S., and M. Karin. 2009. Regulation and function of NF- kappaB transcription factors in the immune system. Annu. Rev. Immunol. 27: 693-733. http://dx.doi.org/10.1146/annurev.immunol.021908.132641
42. Werner, S.L., J.D. Kearns, V. Zadorozhnaya, C. Lynch, E. O'Dea, M.P. Boldin, A. Ma, D. Baltimore, and A. Hoffmann. 2008. Encoding NF- kappaB temporal control in response to TNF: distinct roles for the negative regulators IkappaBalpha and A20. Genes Dev. 22: 2093-2101. http://dx.doi.org/10.1101/gad.1680708
43. Williams, A.E., M.M. Perry, S.A. Moschos, H.M. Larner-Svensson, and M.A. Lindsay. 2008. Role of miRNA-146a in the regulation of the innate immune response and cancer. Biochem. Soc. Trans. 36: 1211-1215. http://dx.doi.org/10.1042/BST0361211
44. Yang, L., and D. Baltimore. 2005. Long-term in vivo provision of antigen-specific T cell immunity by programming hematopoietic stem cells. Proc. Natl. Acad. Sci. USA. 102: 4518-4523. http://dx.doi.org/10.1073/pnas.0500600102
45. Yang, L., H. Yang, K. Rideout, T. Cho, K.I. Joo, L. Ziegler, A. Elliot, A. Walls, D. Yu, D. Baltimore, and P. Wang. 2008. Engineered lentivector targeting of dendritic cells for in vivo immunization. Nat. Biotechnol. 26: 326-334. http://dx.doi.org/10.1038/nbt1390
46. Zhao, J.L., D.S. Rao, M.P. Boldin, K.D. Taganov, R.M. O'Connell, and D. Baltimore. 2011. NF-kappaB dysregulation in microRNA-146a-deficient mice drives the development of myeloid malignancies. Proc. Natl. Acad. Sci. USA. 108: 9184-9189. http://dx.doi.org/10.1073/pnas.1105398108