RESEARCH ARTICLE

The network of cytokines, receptors and transcription factors governing the development of dendritic cell subsets

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  • 1. Walter and Eliza Hall Institute, 1G Royal Parade, Parkville, Victoria 3050, Australia; 2. Department of Medical Biology, University of Melbourne, Australia; 3. Tsinghua University School of Medicine, Beijing 100084, China

Received date: 03 Aug 2011

Accepted date: 14 Aug 2011

Published date: 01 Aug 2011

Abstract

The pathways leading to the development of different dendritic cell (DC) subsets have long been unclear. In recent years, a number of precursors on the route to DC development, both under steady state and inflammatory conditions, have been described, and the nature of these pathways is becoming clearer. In addition, the development of various knockout mouse models and an in vitro system modelling DC development have revealed the role of numerous cytokines and transcription factors that influence DC development. Here, we review recent findings on the factors important in DC development in the context of the developmental pathways that have been described.

Cite this article

Priyanka Sathe, Li Wu . The network of cytokines, receptors and transcription factors governing the development of dendritic cell subsets[J]. Protein & Cell, 2011 , 2(8) : 620 -630 . DOI: 10.1007/s13238-011-1088-0

References

[1] Agger, R., Witmer-Pack, M., Romani, N., Stossel, H., Swiggard, W.J., Metlay, J.P., Storozynsky, E., Freimuth, P., and Steinman, R.M. (1992). Two populations of splenic dendritic cells detected with M342, a new monoclonal to an intracellular antigen of interdigitating dendritic cells and some B lymphocytes. J Leukoc Biol 52, 34–42 .1379295
[2] Aliberti, J., Schulz, O., Pennington, D.J., Tsujimura, H., Reis e Sousa, C., Ozato, K., and Sher, A. (2003a). Essential role for ICSBP in the in vivo development of murine CD8alpha+ dendritic cells. Blood 101, 305–310 .12393690
[3] Aliberti, J., Schulz, O., Pennington, D.J., Tsujimura, H., Reis e Sousa, C., Ozato, K., and Sher, A. (2003b). Essential role for ICSBP in the in vivo development of murine CD8alpha+ dendritic cells. Blood 101, 305–310 .12393690
[4] Baiocchi, G., Scambia, G., Benedetti, P., Menichella, G., Testa, U., Pierelli, L., Martucci, R., Foddai, M.L., Bizzi, B., Mancuso, S., (1993). Autologous stem cell transplantation: sequential production of hematopoietic cytokines underlying granulocyte recovery. Cancer Res 53, 1297–1303 .7680283
[5] Banchereau, J., and Steinman, R.M. (1998). Dendritic cells and the control of immunity. Nature 392, 245–252 .9521319
[6] 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 .19349986
[7] 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 .19733489
[8] Brasel, K., De Smedt, T., Smith, J.L., and Maliszewski, C.R. (2000). Generation of murine dendritic cells from Flt3-ligand-supplemented bone marrow cultures. Blood 96, 3029–3039 .11049981
[9] Brawand, P., Fitzpatrick, D.R., Greenfield, B.W., Brasel, K., Maliszewski, C.R., and De Smedt, T. (2002). Murine plasmacytoid pre-dendritic cells generated from Flt3 ligand-supplemented bone marrow cultures are immature APCs. J Immunol 169, 6711– 6719 .12471102
[10] Brugmann, W., and Winandy, S. (2010). Ikaros null mice demonstrate defects in dendritic cell development. J Immunol 184, 36.1719949095.
[11] 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 .20510871
[12] Caux, C., Vanbervliet, B., Massacrier, C., Dezutter-Dambuyant, C., de Saint-Vis, B., Jacquet, C., Yoneda, K., Imamura, S., Schmitt, D., and Banchereau, J. (1996). CD34+ hematopoietic progenitors from human cord blood differentiate along two independent dendritic cell pathways in response to GM-CSF+TNF α. J Exp Med 184, 695–706 .8760823
[13] Cebon, J., Layton, J.E., Maher, D., and Morstyn, G. (1994). Endogenous haemopoietic growth factors in neutropenia and infection. Br J Haematol 86, 265–274 .7515265
[14] Cheers, C., Haigh, A.M., Kelso, A., Metcalf, D., Stanley, E.R., and Young, A.M. (1988). Production of colony-stimulating factors (CSFs)?during?nfection:?separate?determinations?of macrophage-, granulocyte-, granulocyte-macrophage-, and multi-CSFs. Infect Immun 56, 247–251 .3257205
[15] Chomarat, P., Banchereau, J., Davoust, J., and Palucka, A.K. (2000). IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat Immunol 1, 510–514 .11101873
[16] Cisse, B., Caton, M.L., Lehner, M., Maeda, T., Scheu, S., Locksley, R., Holmberg, D., Zweier, C., den Hollander, N.S., Kant, S.G., (2008). Transcription factor E2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell 135, 37–48 .18854153
[17] Coombes, J.L., Siddiqui, K.R., Arancibia-Cárcamo, C.V., Hall, J., Sun, C.M., Belkaid, Y., and Powrie, F. (2007). A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 204, 1757–1764 .17620361
[18] Corcoran, L., Ferrero, I., Vremec, D., Lucas, K., Waithman, J., O’Keeffe, M., Wu, L., Wilson, A., and Shortman, K. (2003). The lymphoid past of mouse plasmacytoid cells and thymic dendritic cells. J Immunol 170, 4926–4932 .12734335
[19] D’Amico, A., and Wu, L. (2003). The early progenitors of mouse dendritic cells and plasmacytoid predendritic cells are within the bone marrow hemopoietic precursors expressing Flt3. J Exp Med 198, 293–303 .12874262
[20] Dai, X.M., Ryan, G.R., Hapel, A.J., Dominguez, M.G., Russell, R.G., Kapp, S., Sylvestre, V., and Stanley, E.R. (2002). Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 99, 111–120 .11756160
[21] Darrasse-Jèze, G., Deroubaix, S., Mouquet, H., Victora, G.D., Eisenreich, T., Yao, K.H., Masilamani, R.F., Dustin, M.L., Rudensky, A., Liu, K., (2009). Feedback control of regulatory T cell homeostasis by dendritic cells in vivo. J Exp Med 206, 1853–1862 .19667061
[22] de Heer, H.J., Hammad, H., Soullié, T., Hijdra, D., Vos, N., Willart, M.A., Hoogsteden, H.C., and Lambrecht, B.N. (2004). Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J Exp Med 200, 89–98 .15238608
[23] De Smedt, T., Pajak, B., Muraille, E., Lespagnard, L., Heinen, E., De Baetselier, P., Urbain, J., Leo, O., and Moser, M. (1996). Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo. J Exp Med 184, 1413–1424 .8879213
[24] del Rio, M.L., Rodriguez-Barbosa, J.I., Kremmer, E., and F?rster, R. (2007). CD103- and CD103+ bronchial lymph node dendritic cells are specialized in presenting and cross-presenting innocuous antigen to CD4+ and CD8+ T cells. J Immunol 178, 6861–6866 .17513734
[25] 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 .11120766
[26] Djouad, F., Charbonnier, L.M., Bouffi, C., Louis-Plence, P., Bony, C., Apparailly, F., Cantos, C., Jorgensen, C., and No?l, D. (2007). Mesenchymal stem cells inhibit the differentiation of dendritic cells through an interleukin-6-dependent mechanism. Stem Cells 25, 2025–2032 .17510220
[27] 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 CD8α+ conventional dendritic cells. J Exp Med 207, 823–836 .20351058
[28] Esashi, E., Wang, Y.H., Perng, O., Qin, X.F., Liu, Y.J., and Watowich, S.S. (2008). The signal transducer STAT5 inhibits plasmacytoid dendritic cell development by suppressing transcription factor Irf8. Immunity 28, 509–520 .18342552
[29] Fancke, B., Suter, M., Hochrein, H., and O’Keeffe, M. (2008). M-CSF: a novel plasmacytoid and conventional dendritic cell poietin. Blood 111, 150–159 .17916748
[30] Fogg, D.K., Sibon, C., Miled, C., Jung, S., Aucouturier, P., Littman, D.R., Cumano, A., and Geissmann, F. (2006). A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311, 83–87 .16322423
[31] Ghosh, H.S., Cisse, B., Bunin, A., Lewis, K.L., and Reizis, B. (2010). Continuous expression of the transcription factor e2-2 maintains the cell fate of mature plasmacytoid dendritic cells. Immunity 33, 905–916 .21145760
[32] Ginhoux, F., Collin, M.P., Bogunovic, M., Abel, M., Leboeuf, M., Helft, J., Ochando, J., Kissenpfennig, A., Malissen, B., Grisotto, M., (2007). Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J Exp Med 204, 3133–3146 .18086862
[33] Ginhoux, F., Liu, K., Helft, J., Bogunovic, M., Greter, M., Hashimoto, D., Price, J., Yin, N., Bromberg, J., Lira, S.A., (2009). The origin and development of nonlymphoid tissue CD103+ DCs. J Exp Med 206, 3115–3130 .20008528
[34] Ginhoux, F., Tacke, F., Angeli, V., Bogunovic, M., Loubeau, M., Dai, X.M., Stanley, E.R., Randolph, G.J., and Merad, M. (2006). Langerhans cells arise from monocytes in vivo. Nat Immunol 7, 265–273 .16444257
[35] Goubier, A., Dubois, B., Gheit, H., Joubert, G., Villard-Truc, F., Asselin-Paturel, C., Trinchieri, G., and Kaiserlian, D. (2008). Plasmacytoid dendritic cells mediate oral tolerance. Immunity 29, 464–475 .18789731
[36] Gregorio, J., Meller, S., Conrad, C., Di Nardo, A., Homey, B., Lauerma, A., Arai, N., Gallo, R.L., Digiovanni, J., and Gilliet, M. (2010). Plasmacytoid dendritic cells sense skin injury and promote wound healing through type I interferons. J Exp Med 207, 2921–2930 .21115688
[37] Hacker, C., Kirsch, R.D., Ju, X.S., Hieronymus, T., Gust, T.C., Kuhl, C., Jorgas, T., Kurz, S.M., Rose-John, S., Yokota, Y., (2003). Transcriptional profiling identifies Id2 function in dendritic cell development. Nat Immunol 4, 380–386 .12598895
[38] Henri, S., Poulin, L.F., Tamoutounour, S., Ardouin, L., Guilliams, M., de Bovis, B., Devilard, E., Viret, C., Azukizawa, H., Kissenpfennig, A., (2010). CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J Exp Med 207, 189–206 .20038600
[39] Hikino, H., Miyagi, T., Hua, Y., Hirohisa, S., Gold, D.P., Li, X.K., Fujino, M., Tetsuya, T., Amemiya, H., Suzuki, S., (2000). GM-CSF-independent development of dendritic cells from bone marrow cells in the GM-CSF-receptor-deficient mouse. Transplant Proc 32, 2458–2459 .11120243
[40] Hildner, K., Edelson, B.T., Purtha, W.E., Diamond, M., Matsushita, H., Kohyama, M., Calderon, B., Schraml, B.U., Unanue, E.R., Diamond, M.S., (2008). Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322, 1097–1100 .
[41] Hochrein, H., Shortman, K., Vremec, D., Scott, B., Hertzog, P., and O’Keeffe, M. (2001). Differential production of IL-12, IFN-α, and IFN-γ by mouse dendritic cell subsets. J Immunol 166, 5448–5455 .11313382
[42] Holmes, M.L., Carotta, S., Corcoran, L.M., and Nutt, S.L. (2006). Repression of Flt3 by Pax5 is crucial for B-cell lineage commitment. Genes Dev 20, 933–938 .16618805
[43] Ichikawa, E., Hida, S., Omatsu, Y., Shimoyama, S., Takahara, K., Miyagawa, S., Inaba, K., and Taki, S. (2004). Defective development of splenic and epidermal CD4+ dendritic cells in mice deficient for IFN regulatory factor-2. Proc Natl Acad Sci U S A 101, 3909–3914 .15004277
[44] Igyarto, B.Z., Jenison, M.C., Dudda, J.C., Roers, A., Müller, W., Koni, P.A., Campbell, D.J., Shlomchik, M.J., and Kaplan, D.H. (2009). Langerhans cells suppress contact hypersensitivity responses via cognate CD4 interaction and langerhans cell-derived IL-10. J Immunol 183, 5085–5093 .19801524
[45] Isaksson, M., Ardesj?, B., R?nnblom, L., K?mpe, O., Lassmann, H., Eloranta, M.L., and Lobell, A. (2009). Plasmacytoid DC promote priming of autoimmune Th17 cells and EAE. Eur J Immunol 39, 2925–2935 .19637225
[46] 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 CD8α(+) and CD103(+) dendritic cell lineages. EMBO J 30, 2690–2704 .21587207
[47] Jakubzick, C., Tacke, F., Ginhoux, F., Wagers, A.J., van Rooijen, N., Mack, M., Merad, M., and Randolph, G.J. (2008). Blood monocyte subsets differentially give rise to CD103+ and CD103- pulmonary dendritic cell populations. J Immunol 180, 3019–3027 .18292524
[48] Kabashima, K., Banks, T.A., Ansel, K.M., Lu, T.T., Ware, C.F., and Cyster, J.G. (2005a). Intrinsic lymphotoxin-beta receptor requirement for homeostasis of lymphoid tissue dendritic cells. Immunity 22, 439–450 .15845449
[49] Kabashima, K., Banks, T.A., Ansel, K.M., Lu, T.T., Ware, C.F., and Cyster, J.G. (2005b). Intrinsic lymphotoxin-β receptor requirement for homeostasis of lymphoid tissue dendritic cells. Immunity 22, 439–450 .15845449
[50] Kaplan, D.H., Jenison, M.C., Saeland, S., Shlomchik, W.D., and Shlomchik, M.J. (2005). Epidermal langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 23, 611– 620 .16356859
[51] Kim, J.M., Rasmussen, J.P., and Rudensky, A.Y. (2007). Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol 8, 191–197 .17136045
[52] King, I.L., Kroenke, M.A., and Segal, B.M. (2010). GM-CSF-dependent, CD103+ dermal dendritic cells play a critical role in Th effector cell differentiation after subcutaneous immunization. J Exp Med 207, 953–961 .20421390
[53] Kingston, D., Schmid, M.A., Onai, N., Obata-Onai, A., Baumjohann, D., and Manz, M.G. (2009). The concerted action of GM-CSF and Flt3-ligand on in vivo dendritic cell homeostasis. Blood 114, 835–843 .19465690
[54] 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., (2003). TRAF6 is a critical factor for dendritic cell maturation and development. Immunity 19, 353–363 .14499111
[55] Laouar, Y., Welte, T., Fu, X.Y., and Flavell, R.A. (2003). STAT3 is required for Flt3L-dependent dendritic cell differentiation. Immunity 19, 903–912 .14670306
[56] Lin, H., Lee, E., Hestir, K., Leo, C., Huang, M., Bosch, E., Halenbeck, R., Wu, G., Zhou, A., Behrens, D., (2008). Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science 320, 807–811 .
[57] Liu, K., Victora, G.D., Schwickert, T.A., Guermonprez, P., Meredith, M.M., Yao, K., Chu, F.F., Randolph, G.J., Rudensky, A.Y., and Nussenzweig, M. (2009). In vivo analysis of dendritic cell development and homeostasis. Science 324, 392–397 .19286519
[58] Liu, Y.-J. (2005). IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol 23, 275–306 .15771572
[59] Manz, M.G., Traver, D., Miyamoto, T., Weissman, I.L., and Akashi, K. (2001). Dendritic cell potentials of early lymphoid and myeloid progenitors. Blood 97, 3333–3341 .11369621
[60] McKenna, H.J., Stocking, K.L., Miller, R.E., Brasel, K., De Smedt, T., Maraskovsky, E., Maliszewski, C.R., Lynch, D.H., Smith, J., Pulendran, B., (2000). Mice lacking Flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood 95, 3489–3497 .10828034
[61] Metlay, J.P., Witmer-Pack, M.D., Agger, R., Crowley, M.T., Lawless, D., and Steinman, R.M. (1990). The distinct leukocyte integrins of mouse spleen dendritic cells as identified with new hamster monoclonal antibodies. J Exp Med 171, 1753–1771 .2185332
[62] 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. Nat Immunol 7, 663–671 .16680143
[63] Naik, S.H., Proietto, A.I., Wilson, N.S., Dakic, A., Schnorrer, P., Fuchsberger, M., Lahoud, M.H., O’Keeffe, M., Shao, Q.X., Chen, W.F., (2005). Cutting edge: generation of splenic CD8+ and CD8- dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J Immunol 174, 6592–6597 .15905497
[64] Nutt, S.L., Heavey, B., Rolink, A.G., and Busslinger, M. (1999). Commitment to the B-lymphoid lineage depends on the transcription factor Pax5. Nature 401, 556–562 .10524622
[65] O’Keeffe, M., Brodnicki, T.C., Fancke, B., Vremec, D., Morahan, G., Maraskovsky, E., Steptoe, R., Harrison, L.C., and Shortman, K. (2005). Fms-like tyrosine kinase 3 ligand administration overcomes a genetically determined dendritic cell deficiency in NOD mice and protects against diabetes development. Int Immunol 17, 307–314 .15684037
[66] Onai, N., Obata-Onai, A., Tussiwand, R., Lanzavecchia, A., and Manz, M.G. (2006). Activation of the Flt3 signal transduction cascade rescues and enhances type I interferon-producing and dendritic cell development. J Exp Med 203, 227–238 .16418395
[67] Park, S.J., Nakagawa, T., Kitamura, H., Atsumi, T., Kamon, H., Sawa, S., Kamimura, D., Ueda, N., Iwakura, Y., Ishihara, K., (2004). IL-6 regulates in vivo dendritic cell differentiation through STAT3 activation. J Immunol 173, 3844–3854 .15356132
[68] Pelayo, R., Hirose, J., Huang, J., Garrett, K.P., Delogu, A., Busslinger, M., and Kincade, P.W. (2005). Derivation of 2 categories of plasmacytoid dendritic cells in murine bone marrow. Blood 105, 4407–4415 .15728131
[69] Pooley, J.L., Heath, W.R., and Shortman, K. (2001). Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8- dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J Immunol 166, 5327–5330 .11313367
[70] 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 .18086861
[71] Proietto, A.I., O’Keeffe, M., Gartlan, K., Wright, M.D., Shortman, K., Wu, L., and Lahoud, M.H. (2004). Differential production of inflammatory chemokines by murine dendritic cell subsets. Immunobiology 209, 163–172 .15481150
[72] Qiu, C.H., Miyake, Y., Kaise, H., Kitamura, H., Ohara, O., and Tanaka, M. (2009). Novel subset of CD8α+ dendritic cells localized in the marginal zone is responsible for tolerance to cell-associated antigens. J immunol 182, 4127–4136 .
[73] Reis e Sousa, C., Hieny, S., Scharton-Kersten, T., Jankovic, D., Charest, H., Germain, R.N., and Sher, A. (1997). In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J Exp Med 186, 1819–1829 .9382881
[74] Reizis, B. (2010). Regulation of plasmacytoid dendritic cell development. Curr Opin Immunol 22, 206–211 .20144853
[75] Romani, N., Holzmann, S., Tripp, C.H., Koch, F., and Stoitzner, P. (2003). Langerhans cells- dendritic cells of the epidermis. APMIS 111, 725–740 .12974775
[76] Sallusto, F., and Lanzavecchia, A. (1994). Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor α. J Exp Med 179, 1109–1118 .8145033
[77] Sathe, P., Pooley, J., Vremec, D., Mintern, J., Jin, J.O., Wu, L., Kwak, J.Y., Villadangos, J.A., and Shortman, K. (2011). The Acquisition of Antigen Cross-Presentation Function by Newly Formed Dendritic Cells. J Immunol 186, 5184–5192 .
[78] Schiavoni, G., Mattei, F., Borghi, P., Sestili, P., Venditti, M., Morse, H.C. 3rd, Belardelli, F., and Gabriele, L. (2004). ICSBP is critically involved in the normal development and trafficking of Langerhans cells and dermal dendritic cells. Blood 103, 2221–2228 .14615368
[79] Schiavoni, G., Mattei, F., Sestili, P., Borghi, P., Venditti, M., Morse, H.C. 3rd, Belardelli, F., and Gabriele, L. (2002). ICSBP is essential for the development of mouse type I interferon-producing cells and for the generation and activation of CD8alpha(+) dendritic cells. J Exp Med 196, 1415–1425 .12461077
[80] Schotte, R., Nagasawa, M., Weijer, K., Spits, H., and Blom, B. (2004). The ETS transcription factor Spi-B is required for human plasmacytoid dendritic cell development. J Exp Med 200, 1503–1509 .15583020
[81] Schulz, O., Jaensson, E., Persson, E.K., Liu, X., Worbs, T., Agace, W.W., and Pabst, O. (2009). Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med 206, 3101–3114 .20008524
[82] 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 .12871639
[83] Shigematsu, H., Reizis, B., Iwasaki, H., Mizuno, S., Hu, D., Traver, D., Leder, P., Sakaguchi, N., and Akashi, K. (2004). Plasmacytoid dendritic cells activate lymphoid-specific genetic programs irrespective of their cellular origin. Immunity 21, 43–53 .15345219
[84] Spits, H., Couwenberg, F., Bakker, A.Q., Weijer, K., and Uittenbogaart, C.H. (2000). Id2 and Id3 inhibit development of CD34(+) stem cells into predendritic cell (pre-DC)2 but not into pre-DC1. Evidence for a lymphoid origin of pre-DC2. J Exp Med 192, 1775–1784 .11120774
[85] Steinman, R.M., Pack, M., and Inaba, K. (1997). Dendritic cells in the T-cell areas of lymphoid organs. Immunol Rev 156, 25–37 .9176697
[86] Sung, S.S., Fu, S.M., Rose, C.E. Jr, Gaskin, F., Ju, S.T., and Beaty, S.R. (2006). A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J Immunol 176, 2161–2172 .16455972
[87] Suzuki, S., Honma, K., Matsuyama, T., Suzuki, K., Toriyama, K., Akitoyo, I., Yamamoto, K., Suematsu, T., Nakamura, M., Yui, K., (2004). Critical roles of interferon regulatory factor 4 in CD11bhighCD8alpha- dendritic cell development. Proc Natl Acad Sci U S A 101, 8981–8986 .15184678
[88] Swee, L.K., Bosco, N., Malissen, B., Ceredig, R., and Rolink, A. (2009). Expansion of peripheral naturally occurring T regulatory cells by Fms-like tyrosine kinase 3 ligand treatment. Blood 113, 6277–6287 .19211508
[89] Tsujimura, H., Tamura, T., Gongora, C., Aliberti, J., Reis e Sousa, C., Sher, A., and Ozato, K. (2003). ICSBP/Irf-8 retrovirus transduction rescues dendritic cell development in vitro. Blood 101, 961–969 .12393459
[90] Valladeau, J., Clair-Moninot, V., Dezutter-Dambuyant, C., Pin, J.J., Kissenpfennig, A., Mattéi, M.G., Ait-Yahia, S., Bates, E.E., Malissen, B., Koch, F., (2002). Identification of mouse langerin/CD207 in Langerhans cells and some dendritic cells of lymphoid tissues. J Immunol 168, 782–792 .11777972
[91] Valladeau, J., Ravel, O., Dezutter-Dambuyant, C., Moore, K., Kleijmeer, M., Liu, Y., Duvert-Frances, V., Vincent, C., Schmitt, D., Davoust, J., (2000). Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity 12, 71–81 .10661407
[92] Varol, C., Landsman, L., Fogg, D.K., Greenshtein, L., Gildor, B., Margalit, R., Kalchenko, V., Geissmann, F., and Jung, S. (2007). Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med 204, 171–180 .17190836
[93] 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 .19733097
[94] Vremec, D., Lieschke, G.J., Dunn, A.R., Robb, L., Metcalf, D., and Shortman, K. (1997). The influence of granulocyte/macrophage colony-stimulating factor on dendritic cell levels in mouse lymphoid organs. Eur J Immunol 27, 40–44 .9021996
[95] Vremec, D., Pooley, J., Hochrein, H., Wu, L., and Shortman, K. (2000). CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J Immunol 164, 2978–2986 .10706685
[96] Vremec, D., Zorbas, M., Scollay, R., Saunders, D.J., Ardavin, C.F., Wu, L., and Shortman, K. (1992). The surface phenotype of dendritic cells purified from mouse thymus and spleen: investigation of the CD8 expression by a subpopulation of dendritic cells. J Exp Med 176, 47–58 .1613465
[97] Wang, L., Bursch, L.S., Kissenpfennig, A., Malissen, B., Jameson, S.C., and Hogquist, K.A. (2008). Langerin expressing cells promote skin immune responses under defined conditions. J Immunol 180, 4722–4727 .18354196
[98] Wang, Y.D., Gu, Z.J., Huang, J.A., Zhu, Y.B., Zhou, Z.H., Xie, W., Xu, Y., Qiu, Y.H., and Zhang, X.G. (2002). gp130-linked signal transduction promotes the differentiation and maturation of dendritic cells. Int Immunol 14, 599–603 .12039911
[99] Wilson, N.S., El-Sukkari, D., Belz, G.T., Smith, C.M., Steptoe, R.J., Heath, W.R., Shortman, K., and Villadangos, J.A. (2003). Most lymphoid organ dendritic cell types are phenotypically and functionally immature. Blood 102, 2187–2194 .12791652
[100] Worbs, T., Bode, U., Yan, S., Hoffmann, M.W., Hintzen, G., Bernhardt, G., F?rster, R., and Pabst, O. (2006). Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J Exp Med 203, 519–527 .16533884
[101] Wu, L., D’Amico, A., Winkel, K.D., Suter, M., Lo, D., and Shortman, K. (1998). RelB is essential for the development of myeloid-related CD8alpha- dendritic cells but not of lymphoid-related CD8alpha+ dendritic cells. Immunity 9, 839–847 .9881974
[102] Wu, L., Nichogiannopoulou, A., Shortman, K., and Georgopoulos, K. (1997). Cell-autonomous defects in dendritic cell populations of Ikaros mutant mice point to a developmental relationship with the lymphoid lineage. Immunity 7, 483–492 .9354469
[103] 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 .18025203
[104] Zhan, Y., Carrington, E.M., van Nieuwenhuijze, A., Bedoui, S., Seah, S., Xu, Y., Wang, N., Mintern, J.D., Villadangos, J.A., Wicks, I.P., (2011). GM-CSF increases cross presentation and CD103 expression by mouse CD8+ spleen dendritic cells. Eur J Immunol 4 AUG . DOI: 10.1002/eji.201141540
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