Functional regulation of monocyte-derived dendritic cells by microRNAs
Functional regulation of monocyte-derived dendritic cells by microRNAs
Yifan Zhan1,2(), Li Wu3
1. The Walter and Eliza Hall Institute of Medical Research, Parkville 3052, Australia; 2. Department of Medical Biology, University of Melbourne, Parkville 3010, Australia; 3. Tsignhua University and Peking University Joint Center for Life Sciences and Tsinghua University School of Medicine, Beijing 100084, China
Dendritic cells (DCs) as a rare type of leukocytes play an important role in bridging the innate and adaptive immune system. A subset of DCs, monocyte-derived dendritic cells (moDCs), exists in very low numbers at steady state but become abundant in inflammatory states. These inflammation-associated DCs are potent producers of pro-inflammatory cytokines and potent inducers of T helper differentiation. They behave as a “double-edge” sword so that they not only mediate protective immunity but also immuno-pathology. It is still incompletely understood how their function is regulated. Emerging evidence indicates that microRNAs (miRNAs), as a new class of gene regulators, potently regulate the function of moDCs. Here we summarize recent progress in this area.
Aldridge, J.R., Jr., Moseley, C.E., Boltz, D.A., Negovetich, N.J., Reynolds, C., Franks, J., Brown, S.A., Doherty, P.C., Webster, R.G., and Thomas, P.G. (2009). TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc Natl Acad Sci U S A 106, 5306-5311 . doi: 10.1073/pnas.0900655106
2
Aliberti, J., Schulz, O., Pennington, D.J., Tsujimura, H., Reis e Sousa, C., Ozato, K., and Sher, A. (2003). Essential role for ICSBP in the in vivo development of murine CD8alpha+ dendritic cells. Blood 101, 305-310 . doi: 10.1182/blood-2002-04-1088
3
Asselin-Paturel, C., Boonstra, A., Dalod, M., Durand, I., Yessaad, N., Dezutter-Dambuyant, C., Vicari, A., O'Garra, A., Biron, C., Briere, F.,.(2001). Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat Immunol 2, 1144-1150 . doi: 10.1038/ni736
4
Bedoui, S., Whitney, P.G., Waithman, J., Eidsmo, L., Wakim, L., Caminschi, I., Allan, R.S., Wojtasiak, M., Shortman, K., Carbone, F.R.,.(2009). Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol 10, 488-495 . doi: 10.1038/ni.1724
5
Bogunovic, M., Ginhoux, F., Helft, J., Shang, L., Hashimoto, D., Greter, M., Liu, K., Jakubzick, C., Ingersoll, M.A., Leboeuf, M.,.(2009). Origin of the lamina propria dendritic cell network. Immunity 31, 513-525 . doi: 10.1016/j.immuni.2009.08.010
6
Campbell, I.K., van Nieuwenhuijze, A., Segura, E., O'Donnell, K., Coghill, E., Hommel, M., Gerondakis, S., Villadangos, J.A., and Wicks, I.P. (2011). Differentiation of inflammatory dendritic cells is mediated by NF-{kappa}B1-dependent GM-CSF production in CD4 T cells. J Immunol 186, 5468-5477 . doi: 10.4049/jimmunol.1002923
7
Carotta, S., Dakic, A., D'Amico, A., Pang, S.H., Greig, K.T., Nutt, S.L., and Wu, L. (2010). The transcription factor PU.1 controls dendritic cell development and Flt3 cytokine receptor expression in a dose-dependent manner. Immunity 32, 628-641 . doi: 10.1016/j.immuni.2010.05.005
8
Cekaite, L., Clancy, T., and Sioud, M. (2010). Increased miR-21 expression during human monocyte differentiation into DCs. Front Biosci (Elite Ed) 2, 818-828 . doi: 10.2741/E143
9
Ceppi, M., Pereira, P.M., Dunand-Sauthier, I., Barras, E., Reith, W., Santos, M.A., and Pierre, P.. (2009). MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocytederived dendritic cells. Proc Natl Acad Sci U S A 106, 2735-2740 . doi: 10.1073/pnas.0811073106
Chen, T., Li, Z., Jing, T., Zhu, W., Ge, J., Zheng, X., Pan, X., Yan, H., and Zhu, J. (2011a). MicroRNA-146a regulates the maturation process and pro-inflammatory cytokine secretion by targeting CD40L in oxLDL-stimulated dendritic cells. FEBS Lett 585, 567-573 . doi: 10.1016/j.febslet.2011.01.010
12
Chen, T., Li, Z., Tu, J., Zhu, W., Ge, J., Zheng, X., Yang, L., Pan, X., Yan, H., and Zhu, J. (2011b). MicroRNA-29a regulates pro-inflammatory cytokine secretion and scavenger receptor expression by targeting LPL in oxLDL-stimulated dendritic cells. FEBS Lett 585, 657-663 . doi: 10.1016/j.febslet.2011.01.027
13
Chen, T., Yan, H., Li, Z., Jing, T., Zhu, W., Ge, J., Zheng, X., Pan, X., and Zhu, J. (2011c). MicroRNA-155 regulates lipid uptake, adhesion/chemokine marker secretion and SCG2 expression in oxLDL-stimulated dendritic cells/macrophages. Int J Cardiol 147, 446-447 . doi: 10.1016/j.ijcard.2010.10.133
14
Cheong, C., Matos, I., Choi, J.H., Dandamudi, D.B., Shrestha, E., Longhi, M.P., Jeffrey, K.L., Anthony, R.M., Kluger, C., Nchinda, G.,.(2010). Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell 143, 416-429 . doi: 10.1016/j.cell.2010.09.039
15
Chong, M.M., Rasmussen, J.P., Rudensky, A.Y., and Littman, D.R. (2008). The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J Exp Med 205, 2005-2017 . doi: 10.1084/jem.20081219
16
den Haan, J.M., Lehar, S.M., and Bevan, M.J. (2000). CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med 192, 1685-1696 . doi: 10.1084/jem.192.12.1685
17
Dominguez, P.M., and Ardavin, C. (2010). Differentiation and function of mouse monocyte-derived dendritic cells in steady state and inflammation. Immunol Rev 234, 90-104 . doi: 10.1111/j.0105-2896.2009.00876.x
18
Du, J., Wang, J., Tan, G., Cai, Z., Zhang, L., Tang, B., and Wang, Z. (2012). Aberrant elevated microRNA-146a in dendritic cells (DC) induced by human pancreatic cancer cell line BxPC-3-conditioned medium inhibits DC maturation and activation. Med Oncol . (In press) doi: 10.1007/s12032-012-0175-2
19
Dunand-Sauthier, I., Santiago-Raber, M.L., Capponi, L., Vejnar, C.E., Schaad, O., Irla, M., Seguin-Estevez, Q., Descombes, P., Zdobnov, E.M., Acha-Orbea, H.,.(2011). Silencing of c-Fos expression by microRNA-155 is critical for dendritic cell maturation and function. Blood 117, 4490-4500 . doi: 10.1182/blood-2010-09-308064
20
Edelson, B.T., Bradstreet, T.R., Hildner, K., Carrero, J.A., Frederick, K.E., Kc, W., Belizaire, R., Aoshi, T., Schreiber, R.D., Miller, M.J.,.(2011). CD8alpha(+) dendritic cells are an obligate cellular entry point for productive infection by Listeria monocytogenes. Immunity 35, 236-248 . doi: 10.1016/j.immuni.2011.06.012
21
Edelson, B.T., Kc, W., Juang, R., Kohyama, M., Benoit, L.A., Klekotka, P.A., Moon, C., Albring, J.C., Ise, W., Michael, D.G.,.(2010). Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J Exp Med 207, 823-836 . doi: 10.1084/jem.20091627
22
Edwards, A.D., Diebold, S.S., Slack, E.M., Tomizawa, H., Hemmi, H., Kaisho, T., Akira, S., and Reis e Sousa, C. (2003). Toll-like receptor expression in murine DC subsets: lack of TLR7 expression by CD8 alpha+ DC correlates with unresponsiveness to imidazoquinolines. Eur J Immunol 33, 827-833 . doi: 10.1002/eji.200323797
23
Geijtenbeek, T.B., Kwon, D.S., Torensma, R., van Vliet, S.J., van Duijnhoven, G.C., Middel, J., Cornelissen, I.L., Nottet, H.S., KewalRamani, V.N., Littman, D.R.,.(2000). DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100, 587-597 . doi: 10.1016/S0092-8674(00)80694-7
24
Geissmann, F., Manz, M.G., Jung, S., Sieweke, M.H., Merad, M., and Ley, K. (2010). Development of monocytes, macrophages, and dendritic cells. Science 327, 656-661 . doi: 10.1126/science.1178331
25
Grumont, R., Hochrein, H., O'Keeffe, M., Gugasyan, R., White, C., Caminschi, I., Cook, W., and Gerondakis, S. (2001). c-Rel regulates interleukin 12 p70 expression in CD8(+) dendritic cells by specifically inducing p35 gene transcription. J Exp Med 194, 1021-1032 . doi: 10.1084/jem.194.8.1021
26
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 . doi: 10.1182/blood-2008-09-179150
27
Hochrein, H., Shortman, K., Vremec, D., Scott, B., Hertzog, P., and O'Keeffe, M. (2001). Differential production of IL-12, IFN-alpha, and IFN-gamma by mouse dendritic cell subsets. J Immunol 166, 5448-5455 .
28
Hsieh, C.S., Macatonia, S.E., Tripp, C.S., Wolf, S.F., O'Garra, A., and Murphy, K.M. (1993). Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science 260, 547-549 . doi: 10.1126/science.8097338
29
Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., Muramatsu, S., and Steinman, R.M. (1992). Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 176, 1693-1702 . doi: 10.1084/jem.176.6.1693
30
Iyoda, T., Shimoyama, S., Liu, K., Omatsu, Y., Akiyama, Y., Maeda, Y., Takahara, K., Steinman, R.M., and Inaba, K. (2002). The CD8+ dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J Exp Med 195, 1289-1302 . doi: 10.1084/jem.20020161
31
Jackson, J.T., Hu, Y., Liu, R., Masson, F., D'Amico, A., Carotta, S., Xin, A., Camilleri, M.J., Mount, A.M., Kallies, A., . (2011). Id2 expression delineates differential checkpoints in the genetic program of CD8alpha(+) and CD103(+) dendritic cell lineages. EMBO J 30, 2690-2704 . doi: 10.1038/emboj.2011.163
King, I.L., Kroenke, M.A., and Segal, B.M. (2010). GM-CSFdependent, CD103+ dermal dendritic cells play a critical role in Theffector cell differentiation after subcutaneous immunization. J Exp Med 207, 953-961 . doi: 10.1084/jem.20091844
36
Kuipers, H., Schnorfeil, F.M., and Brocker, T. (2010a). Differentially expressed microRNAs regulate plasmacytoid vs. conventional dendritic cell development. Mol Immunol 48, 333-340 . doi: 10.1016/j.molimm.2010.07.007
37
Kuipers, H., Schnorfeil, F.M., Fehling, H.J., Bartels, H., and Brocker, T. (2010b). Dicer-dependent microRNAs control maturation, function, and maintenance of Langerhans cells in vivo. J Immunol 185, 400-409 . doi: 10.4049/jimmunol.0903912
38
Lanoue, A., Clatworthy, M.R., Smith, P., Green, S., Townsend, M.J., Jolin, H.E., Smith, K.G., Fallon, P.G., and McKenzie, A.N. (2004). SIGN-R1 contributes to protection against lethal pneumococcal infection in mice. J Exp Med 200, 1383-1393 . doi: 10.1084/jem.20040795
39
Leon, B., Lopez-Bravo, M., and Ardavin, C. (2007). Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26, 519-531 . doi: 10.1016/j.immuni.2007.01.017
40
Lewis, K.L., Caton, M.L., Bogunovic, M., Greter, M., Grajkowska, L.T., Ng, D., Klinakis, A., Charo, I.F., Jung, S., Gommerman, J.L.,.(2011). Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 35, 780-791 . doi: 10.1016/j.immuni.2011.08.013
41
Liu, X., Zhan, Z., Xu, L., Ma, F., Li, D., Guo, Z., Li, N., and Cao, X. (2010). MicroRNA-148/152 impair innate response and antigen presentation of TLR-triggered dendritic cells by targeting CaMKIIalpha. J Immunol 185, 7244-7251 . doi: 10.4049/jimmunol.1001573
42
Liu, Y., Chen, Q., Song, Y., Lai, L., Wang, J., Yu, H., Cao, X., and Wang, Q. (2011). MicroRNA-98 negatively regulates IL-10 production and endotoxin tolerance in macrophages after LPS stimulation. FEBS Lett 585, 1963-1968 . doi: 10.1016/j.febslet.2011.05.029
43
Lu, C., Huang, X., Zhang, X., Roensch, K., Cao, Q., Nakayama, K.I., Blazar, B.R., Zeng, Y., and Zhou, X. (2011a). miR-221 and miR-155 regulate human dendritic cell development, apoptosis, and IL-12 production through targeting of p27kip1, KPC1, and SOCS-1. Blood 117, 4293-4303 . doi: 10.1182/blood-2010-12-322503
44
Lu, L.F., Thai, T.H., Calado, D.P., Chaudhry, A., Kubo, M., Tanaka, K., Loeb, G.B., Lee, H., Yoshimura, A., Rajewsky, K., . (2009a). Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity 30, 80-91 . doi: 10.1016/j.immuni.2008.11.010
45
Lu, T.X., Hartner, J., Lim, E.J., Fabry, V., Mingler, M.K., Cole, E.T., Orkin, S.H., Aronow, B.J., and Rothenberg, M.E. (2011b). MicroRNA-21 limits in vivo immune response-mediated activation of the IL-12/IFN-gamma pathway, Th1 polarization, and the severity of delayed-type hypersensitivity. J Immunol 187, 3362-3373 . doi: 10.4049/jimmunol.1101235
46
Lu, T.X., Munitz, A., and Rothenberg, M.E. (2009b). MicroRNA-21 is up-regulated in allergic airway inflammation and regulates IL-12p35 expression. J Immunol 182, 4994-5002 . doi: 10.4049/jimmunol.0803560
47
Ma, F., Liu, X., Li, D., Wang, P., Li, N., Lu, L., and Cao, X. (2010). MicroRNA-466l upregulates IL-10 expression in TLR-triggered macrophages by antagonizing RNA-binding protein tristetraprolinmediated IL-10 mRNA degradation. J Immunol 184, 6053-6059 . doi: 10.4049/jimmunol.0902308
48
Martinez-Nunez, R.T., Louafi, F., Friedmann, P.S., and Sanchez-Elsner, T. (2009). MicroRNA-155 modulates the pathogen binding ability of dendritic cells (DCs) by down-regulation of DC-specific intercellular adhesion molecule-3 grabbing non-integrin (DC-SIGN). J Biol Chem 284, 16334-16342 . doi: 10.1074/jbc.M109.011601
49
Merad, M., Ginhoux, F., and Collin, M. (2008). Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat Rev Immunol 8, 935-947 . doi: 10.1038/nri2455
50
Montecalvo, A., Larregina, A.T., Shufesky, W.J., Stolz, D.B., Sullivan, M.L., Karlsson, J.M., Baty, C.J., Gibson, G.A., Erdos, G., Wang, Z., . (2012). Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119, 756-766 . doi: 10.1182/blood-2011-02-338004
51
Naik, S.H., Metcalf, D., van Nieuwenhuijze, A., Wicks, I., Wu, L., O'Keeffe, M., and Shortman, K. (2006). Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. NatImmunol 7, 663-671 . doi: 10.1038/ni1340
52
Nakano, H., Yanagita, M., and Gunn, M.D. (2001). CD11c(+)B220(+)Gr-1(+) cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J Exp Med 194, 1171-1178 . doi: 10.1084/jem.194.8.1171
53
Neuenhahn, M., Kerksiek, K.M., Nauerth, M., Suhre, M.H., Schiemann, M., Gebhardt, F.E., Stemberger, C., Panthel, K., Schroder, S., Chakraborty, T., . (2006). CD8alpha+ dendritic cells are required for efficient entry of Listeria monocytogenes into the spleen. Immunity 25, 619-630 . doi: 10.1016/j.immuni.2006.07.017
54
O'Connell, R.M., Chaudhuri, A.A., Rao, D.S., and Baltimore, D. (2009). Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci U S A 106, 7113-7118 . doi: 10.1073/pnas.0902636106
55
O'Connell, R.M., Kahn, D., Gibson, W.S., Round, J.L., Scholz, R.L., Chaudhuri, A.A., Kahn, M.E., Rao, D.S., and Baltimore, D. (2010). MicroRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity 33, 607-619 . doi: 10.1016/j.immuni.2010.09.009
56
O'Keeffe, M., Hochrein, H., Vremec, D., Caminschi, I., Miller, J.L., Anders, E.M., Wu, L., Lahoud, M.H., Henri, S., Scott, B., . (2002). Mouse plasmacytoid cells: long-lived cells, heterogeneous in surface phenotype and function, that differentiate into CD8(+) dendritic cells only after microbial stimulus. J Exp Med 196, 1307-1319 . doi: 10.1084/jem.20021031
57
Pauley, K.M., Stewart, C.M., Gauna, A.E., Dupre, L.C., Kuklani, R., Chan, A.L., Pauley, B.A., Reeves, W.H., Chan, E.K., and Cha, S. (2011). Altered miR-146a expression in Sjogren's syndrome and its functional role in innate immunity. Eur J Immunol 41, 2029-2039 . doi: 10.1002/eji.201040757
58
Pegtel, D.M., Cosmopoulos, K., Thorley-Lawson, D.A., van Eijndhoven, M.A., Hopmans, E.S., Lindenberg, J.L., de Gruijl, T.D., Wurdinger, T., and Middeldorp, J.M. (2010). Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci U S A 107, 6328-6333 . doi: 10.1073/pnas.0914843107
59
Poulin, L.F., Henri, S., de Bovis, B., Devilard, E., Kissenpfennig, A., and Malissen, B. (2007). The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells. J Exp Med 204, 3119-3131 . doi: 10.1084/jem.20071724
60
Reid, C.D., Stackpoole, A., Meager, A., and Tikerpae, J. (1992). Interactions of tumor necrosis factor with granulocyte-macrophage colony-stimulating factor and other cytokines in the regulation of dendritic cell growth in vitro from early bipotent CD34+ progenitors in human bone marrow. J Immunol 149, 2681-2688 .
61
Rodriguez, A., Vigorito, E., Clare, S., Warren, M.V., Couttet, P., Soond, D.R., van Dongen, S., Grocock, R.J., Das, P.P., Miska, E.A.,.(2007). Requirement of bic/microRNA-155 for normal immune function. Science 316, 608-611 . doi: 10.1126/science.1139253
Sathe, P., and Wu, L. (2011). The network of cytokines, receptors and transcription factors governing the development of dendritic cell subsets. Protein Cell 2, 620-630 . doi: 10.1007/s13238-011-1088-0
64
Serbina, N.V., and Pamer, E.G. (2006). Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 7, 311-317 . doi: 10.1038/ni1309
65
Serbina, N.V., Salazar-Mather, T.P., Biron, C.A., Kuziel, W.A., and Pamer, E.G. (2003). TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19, 59-70 . doi: 10.1016/S1074-7613(03)00171-7
66
Sharma, A., Kumar, M., Aich, J., Hariharan, M., Brahmachari, S.K., Agrawal, A., and Ghosh, B. (2009). Posttranscriptional regulation of interleukin-10 expression by hsa-miR-106a. Proc Natl Acad Sci U S A 106, 5761-5766 . doi: 10.1073/pnas.0808743106
67
Shklovskaya, E., O'Sullivan, B.J., Ng, L.G., Roediger, B., Thomas, R., Weninger, W., and Fazekas de St Groth, B. (2011). Langerhans cells are precommitted to immune tolerance induction. Proc Natl Acad Sci U S A 108, 18049-18054 . doi: 10.1073/pnas.1110076108
68
Shortman, K., and Naik, S.H. (2007). Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 7, 19-30 . doi: 10.1038/nri1996
69
Steinman, R.M., and Cohn, Z.A. (1973). Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med 137, 1142-1162 . doi: 10.1084/jem.137.5.1142
70
Stockinger, B., and Veldhoen, M. (2007). Differentiation and function of Th17 T cells. Curr Opin Immunol 19, 281-286 . doi: 10.1016/j.coi.2007.04.005
71
Sun, Y., Varambally, S., Maher, C.A., Cao, Q., Chockley, P., Toubai, T., Malter, C., Nieves, E., Tawara, I., Wang, Y.,.(2011). Targeting of microRNA-142-3p in dendritic cells regulates endotoxin-induced mortality. Blood 117, 6172-6183 . doi: 10.1182/blood-2010-12-325647
72
Tserel, L., Runnel, T., Kisand, K., Pihlap, M., Bakhoff, L., Kolde, R., Peterson, H., Vilo, J., Peterson, P., and Rebane, A. (2011). MicroRNA expression profiles of human blood monocyte-derived dendritic cells and macrophages reveal miR-511 as putative positive regulator of Toll-like receptor 4. J Biol Chem 286, 26487-26495 . doi: 10.1074/jbc.M110.213561
73
Turner, M.L., Schnorfeil, F.M., and Brocker, T. (2011). MicroRNAs regulate dendritic cell differentiation and function. J Immunol 187, 3911-3917 . doi: 10.4049/jimmunol.1101137
74
Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J.J., and Lotvall, J.O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9, 654-659 . doi: 10.1038/ncb1596
75
Varol, C., Vallon-Eberhard, A., Elinav, E., Aychek, T., Shapira, Y., Luche, H., Fehling, H.J., Hardt, W.D., Shakhar, G., and Jung, S. (2009). Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31, 502-512 . doi: 10.1016/j.immuni.2009.06.025
76
Wakim, L.M., Waithman, J., van Rooijen, N., Heath, W.R., and Carbone, F.R. (2008). Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science 319, 198-202 . doi: 10.1126/science.1151869
77
Wen, H., Dou, Y., Hogaboam, C.M., and Kunkel, S.L. (2008). Epigenetic regulation of dendritic cell-derived interleukin-12 facilitates immunosuppression after a severe innate immune response. Blood 111, 1797-1804 . doi: 10.1182/blood-2007-08-106443
78
Xiao, C., Calado, D.P., Galler, G., Thai, T.H., Patterson, H.C., Wang, J., Rajewsky, N., Bender, T.P., and Rajewsky, K. (2007). MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 131, 146-159 . doi: 10.1016/j.cell.2007.07.021
79
Xiao, C., and Rajewsky, K. (2009). MicroRNA control in the immune system: basic principles. Cell 136, 26-36 . doi: 10.1016/j.cell.2008.12.027
80
Xu, Y., Zhan, Y., Lew, A.M., Naik, S.H., and Kershaw, M.H. (2007). Differential development of murine dendritic cells by GM-CSF versus Flt3 ligand has implications for inflammation and trafficking. J Immunol 179, 7577-7584 .
81
Xue, X., Feng, T., Yao, S., Wolf, K.J., Liu, C.G., Liu, X., Elson, C.O., and Cong, Y. (2011). Microbiota downregulates dendritic cell expression of miR-10a, which targets IL-12/IL-23p40. J Immunol 187, 5879-5886 . doi: 10.4049/jimmunol.1100535
Zhan, Y., Xu, Y., and Lew, A.M. (2012). The regulation of the development and function of dendritic cell subsets by GM-CSF: More than a hematopoietic growth factor. Mol Immunol 52, 30-37 . doi: 10.1016/j.molimm.2012.04.009
84
Zhan, Y., Xu, Y., Seah, S., Brady, J.L., Carrington, E.M., Cheers, C., Croker, B.A., Wu, L., Villadangos, J.A., and Lew, A.M. (2010). Resident and monocyte-derived dendritic cells become dominant IL-12 producers under different conditions and signaling pathways. J Immunol 185, 2125-2133 . doi: 10.4049/jimmunol.0903793
85
Zhang, M., Liu, F., Jia, H., Zhang, Q., Yin, L., Liu, W., Li, H., Yu, B., and Wu, J. (2011). Inhibition of microRNA let-7i depresses maturation and functional state of dendritic cells in response to lipopolysaccharide stimulation via targeting suppressor of cytokine signaling 1. J Immunol 187, 1674-1683 . doi: 10.4049/jimmunol.1001937
Zheng, J., Jiang, H.Y., Li, J., Tang, H.C., Zhang, X.M., Wang, X.R., Du, J.T., Li, H.B., and Xu, G. (2012). MicroRNA-23b promotes tolerogenic properties of dendritic cells in vitro through inhibiting Notch1/NF-kappaB signalling pathways. Allergy 67, 362-370 . doi: 10.1111/j.1398-9995.2011.02776.x
88
Zhou, H., Huang, X., Cui, H., Luo, X., Tang, Y., Chen, S., Wu, L., and Shen, N. (2010). miR-155 and its star-form partner miR-155* cooperatively regulate type I interferon production by human plasmacytoid dendritic cells. Blood 116, 5885-5894 . doi: 10.1182/blood-2010-04-280156