MicroRNA-146a and microRNA-146b regulate human dendritic cell apoptosis and cytokine production by targeting TRAF6 and IRAK1 proteins

Journal of Biological Chemistry

Volumn 290, Issue 5, 2015, Pages 2831-2841

  Park, Haein ^a   Huang, Xin ^a   Lu, Changming ^b   Cairo, Mitchell S ^a   Zhou, Xianzheng ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CELLS; FEEDBACK;

CYTOKINE PRODUCTION; DENDRITIC CELLS; HUMAN DENDRITIC CELLS; HUMAN MONOCYTES; NATURAL KILLER CELLS; NEGATIVE FEEDBACK MECHANISM; OVER-EXPRESSION; SIRNA SILENCING;

RNA;

B7 ANTIGEN; CD40 ANTIGEN; CD56 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; HLA ANTIGEN CLASS 2; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 6; MICRORNA; MICRORNA 146A; MICRORNA 146B; PROSTAGLANDIN E2; PROTEIN BCL 2; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; CYTOKINE; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; IRAK1 PROTEIN, HUMAN; MIRN146 MICRORNA, HUMAN;

ADAPTIVE IMMUNITY; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CD3+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INNATE IMMUNITY; LENTIVIRINAE; MONOCYTE; NATURAL KILLER CELL; NEGATIVE FEEDBACK; PROTEIN EXPRESSION; PROTEIN TARGETING; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VIRUS EXPRESSION; CELL CULTURE; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETICS; METABOLISM; PHYSIOLOGY; WESTERN BLOTTING;

LENTIVIRUS;

APOPTOSIS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; MICRORNAS; MONOCYTES; REAL-TIME POLYMERASE CHAIN REACTION; TNF RECEPTOR-ASSOCIATED FACTOR 6;

EID: 84921932058     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.591420     Document Type: Article

References (45)

1. Lanzavecchia, A., and Sallusto, F. (2004) Lead and follow: the dance of the dendritic cell and T cell. Nat. Immunol. 5, 1201-1202
2. Banchereau, J., Briere, F., Caux, C., Davoust, J., Lebecque, S., Liu, Y. J., Pulendran, B., and Palucka, K. (2000) Immunobiology of dendritic cells. Annu. Rev. Immunol. 18, 767-811
3. Steinman, R. M., Hawiger, D., and Nussenzweig, M. C. (2003) Tolerogenic dendritic cells. Annu. Rev. Immunol. 21, 685-711
4. Jiang, H., Van De Ven, C., Satwani, P., Baxi, L. V., and Cairo, M. S. (2004) Differential gene expression patterns by oligonucleotide microarray of basal versus lipopolysaccharide-activated monocytes from cord blood versus adult peripheral blood. J. Immunol. 172, 5870-5879
5. Jiang, H., van de Ven, C., Baxi, L., Satwani, P., and Cairo, M. S. (2009) Differential gene expression signatures of adult peripheral blood vs cord blood monocyte-derived immature and mature dendritic cells. Exp. Hematol. 37, 1201-1215
6. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297
7. Pasquinelli, A. E. (2012) MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat. Rev. Genet. 13, 271-282
8. O'Connell, R. M., Rao, D. S., Chaudhuri, A. A., and Baltimore, D. (2010) Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10, 111-122
9. Hashimi, S. T., Fulcher, J. A., Chang, M. H., Gov, L., Wang, S., and Lee, B. (2009) MicroRNA profiling identifies miR-34a and miR-21 and their target genes JAG1 and WNT1 in the coordinate regulation of dendritic cell differentiation. Blood 114, 404-414
10. kip1, KPC1, and SOCS-1. Blood 117, 4293-4303
11. Sun, Y., Varambally, S., Maher, C. A., Cao, Q., Chockley, P., Toubai, T., Malter, C., Nieves, E., Tawara, I., Wang, Y., Ward, P. A., Chinnaiyan, A., and Reddy, P. (2011) Targeting of microRNA-142-3p in dendritic cells regulates endotoxin-induced mortality. Blood 117, 6172-6183
12. Taganov, K. D., Boldin, M. P., Chang, K. J., and Baltimore, D. (2006) NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. U.S.A. 103, 12481-12486
13. Hou, J., Wang, P., Lin, L., Liu, X., Ma, F., An, H., Wang, Z., and Cao, X. (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
14. Jurkin, J., Schichl, Y. M., Koeffel, R., Bauer, T., Richter, S., Konradi, S., Gesslbauer, B., and Strobl, H. (2010) miR-146a is differentially expressed by myeloid dendritic cell subsets and desensitizes cells to TLR2-dependent activation. J. Immunol. 184, 4955-4965
15. Kawai, T., and Akira, S. (2006) TLR signaling. Cell Death Differ. 13, 816-825
16. Rescigno, M., Martino, M., Sutherland, C. L., Gold, M. R., and Ricciardi-Castagnoli, P. (1998) Dendritic cell survival and maturation are regulated by different signaling pathways. J. Exp. Med. 188, 2175-2180
17. van de Laar, L., van den Bosch, A., van der Kooij, S. W., Janssen, H. L., Coffer, P. J., van Kooten, C., and Woltman, A. M. (2010) A nonredundant role for canonical NF-κB in human myeloid dendritic cell development and function. J. Immunol. 185, 7252-7261
18. Bhaumik, D., Scott, G. K., Schokrpur, S., Patil, C. K., Campisi, J., and Benz, C. C. (2008) Expression of microRNA-146 suppresses NF-κB activity with reduction of metastatic potential in breast cancer cells. Oncogene 27, 5643-5647
19. Nahid, M. A., Pauley, K. M., Satoh, M., and Chan, E. K. (2009) miR-146a is critical for endotoxin-induced tolerance. Implication in innate immunity. J. Biol. Chem. 284, 34590-34599
20. Zhao, J. L., Rao, D. S., Boldin, M. P., Taganov, K. D., O'Connell, R. M., and Baltimore, D. (2011) NF-κB dysregulation in microRNA-146a-deficient mice drives the development of myeloid malignancies. Proc. Natl. Acad. Sci. U.S.A. 108, 9184-9189
21. Boldin, M. P., Taganov, K. D., Rao, D. S., Yang, L., Zhao, J. L., Kalwani, M., Garcia-Flores, Y., Luong, M., Devrekanli, A., Xu, J., Sun, G., Tay, J., Linsley, P. S., and Baltimore, D. (2011) miR-146a is a significant brake on autoimmunity, myeloproliferation, and cancer in mice. J. Exp. Med. 208, 1189-1201
22. Thurner, B., Röder, C., Dieckmann, D., Heuer, M., Kruse, M., Glaser, A., Keikavoussi, P., Kämpgen, E., Bender, A., and Schuler, G. (1999) Generation of large numbers of fully mature and stable dendritic cells from leukapheresis products for clinical application. J. Immunol. Methods 223, 1-15
23. T method. Methods 25, 402-408
24. Baseler, W. A., Thapa, D., Jagannathan, R., Dabkowski, E. R., Croston, T. L., and Hollander, J. M. (2012) miR-141 as a regulator of the mitochondrial phosphate carrier (Slc25a3) in the type 1 diabetic heart. Am. J. Physiol. Cell Physiol. 303, C1244-C1251
25. + lymphoid malignancies. Mol. Ther. 16, 580-589
26. Zhou, X., Cui, Y., Huang, X., Yu, Z., Thomas, A. M., Ye, Z., Pardoll, D. M., Jaffee, E. M., and Cheng, L. (2003) Lentivirus-mediated gene transfer and expression in established human tumor antigen-specific cytotoxic T cells and primary unstimulated T cells. Hum. Gene Ther. 14, 1089-1105
27. Chen, M., and Wang, J. (2010) Programmed cell death of dendritic cells in immune regulation. Immunol. Rev. 236, 11-27
28. Williams, A. E., Perry, M. M., Moschos, S. A., Larner-Svensson, H. M., and Lindsay, M. A. (2008) Role of miRNA-146a in the regulation of the innate immune response and cancer. Biochem. Soc. Trans. 36, 1211-1215
29. Curtale, G., Citarella, F., Carissimi, C., Goldoni, M., Carucci, N., Fulci, V., Franceschini, D., Meloni, F., Barnaba, V., and Macino, G. (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
30. Xiong, H., Zhu, C., Li, F., Hegazi, R., He, K., Babyatsky, M., Bauer, A. J., and Plevy, S. E. (2004) Inhibition of interleukin-12 p40 transcription and NF-κB activation by nitric oxide in murine macrophages and dendritic cells. J. Biol. Chem. 279, 10776-10783
31. Trinchieri, G. (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3, 133-146
32. Kim, H. J., Kim, H. O., Lee, K., Baek, E. J., and Kim, H. S. (2010) Two-step maturation of immature DCs with proinflammatory cytokine cocktail and poly(I:C) enhances migratory and T cell stimulatory capacity. Vaccine 28, 2877-2886
33. Hemmi, H., Kaisho, T., Takeuchi, O., Sato, S., Sanjo, H., Hoshino, K., Horiuchi, T., Tomizawa, H., Takeda, K., and Akira, S. (2002) Small antiviral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 3, 196-200
34. Garzon, R., Calin, G. A., and Croce, C. M. (2009) MicroRNAs in Cancer. Annu. Rev. Med. 60, 167-179
35. Curtale, G., Mirolo, M., Renzi, T. A., Rossato, M., Bazzoni, F., and Locati, M. (2013) Negative regulation of Toll-like receptor 4 signaling by IL-10-dependent microRNA-146b. Proc. Natl. Acad. Sci. U.S.A. 110, 11499-11504
36. Paik, J. H., Jang, J. Y., Jeon, Y. K., Kim, W. Y., Kim, T. M., Heo, D. S., and Kim, C. W. (2011) MicroRNA-146a downregulates NFκB activity via targeting TRAF6 and functions as a tumor suppressor having strong prognostic implications in NK/T cell lymphoma. Clin. Cancer Res. 17, 4761-4771
37. Yang, W. L., Wang, J., Chan, C. H., Lee, S. W., Campos, A. D., Lamothe, B., Hur, L., Grabiner, B. C., Lin, X., Darnay, B. G., and Lin, H. K. (2009) The E3 ligase TRAF6 regulates Akt ubiquitination and activation. Science 325, 1134-1138
38. Karrich, J. J., Jachimowski, L. C., Libouban, M., Iyer, A., Brandwijk, K., Taanman-Kueter, E. W., Nagasawa, M., de Jong, E. C., Uittenbogaart, C. H., and Blom, B. (2013) MicroRNA-146a regulates survival and maturation of human plasmacytoid dendritic cells. Blood 122, 3001-3009
39. Wang, J., Zheng, L., Lobito, A., Chan, F. K., Dale, J., Sneller, M., Yao, X., Puck, J. M., Straus, S. E., and Lenardo, M. J. (1999) Inherited human caspase 10 mutations underlie defective lymphocyte and dendritic cell apoptosis in autoimmune lymphoproliferative syndrome type II. Cell 98, 47-58
40. Lu, L. F., Boldin, M. P., Chaudhry, A., Lin, L. L., Taganov, K. D., Hanada, T., Yoshimura, A., Baltimore, D., and Rudensky, A. Y. (2010) Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell 142, 914-929
41. Yang, L., Boldin, M. P., Yu, Y., Liu, C. S., Ea, C. K., Ramakrishnan, P., Taganov, K. D., Zhao, J. L., and Baltimore, D. (2012) miR-146a controls the resolution of T cell responses in mice. J. Exp. Med. 209, 1655-1670
42. Kobayashi, T., Walsh, P. T., Walsh, M. C., Speirs, K. M., Chiffoleau, E., King, C. G., Hancock, W. W., Caamano, J. H., Hunter, C. A., Scott, P., Turka, L. A., and Choi, Y. (2003) TRAF6 is a critical factor for dendritic cell maturation and development. Immunity 19, 353-363
43. John, B., Enright, A. J., Aravin, A., Tuschl, T., Sander, C., and Marks, D. S. (2004) Human microRNA targets. PLoS Biol. 2, e363
44. Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20
45. van Kooten, C., and Banchereau, J. (1997) Functions of CD40 on B cells, dendritic cells and other cells. Curr. Opin. Immunol. 9, 330-337