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Published in: Seminars in Immunopathology 2/2017

01-02-2017 | Review

The origin of DCs and capacity for immunologic tolerance in central and peripheral tissues

Authors: K . Sanjana P. Devi, Niroshana Anandasabapathy

Published in: Seminars in Immunopathology | Issue 2/2017

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Abstract

Dendritic cells (DCs) are specialized immune sentinels that play key role in maintaining immune homeostasis by efficiently regulating the delicate balance between protective immunity and tolerance to self. Although DCs respond to maturation signals present in the surrounding milieu, multiple layers of suppression also co-exist that reduce the infringement of tolerance against self-antigens. These tolerance inducing properties of DCs are governed by their origin and a range of other factors including distribution, cytokines, growth factors, and transcriptional programing, that collectively impart suppressive functions to these cells. DCs directing tolerance secrete anti-inflammatory cytokines and induce naïve T cells or B cells to differentiate into regulatory T cells (Tregs) or B cells. In this review, we provide a detailed outlook on the molecular mechanisms that induce functional specialization to govern central or peripheral tolerance. The tolerance-inducing nature of DCs can be exploited to overcome autoimmunity and rejection in graft transplantation.
Literature
4.
go back to reference Banchereau J, Briere F, Caux C et al (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18:767–811PubMedCrossRef Banchereau J, Briere F, Caux C et al (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18:767–811PubMedCrossRef
6.
go back to reference Forster R, Schubel A, Breitfeld D et al (1999) CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99:23–33PubMedCrossRef Forster R, Schubel A, Breitfeld D et al (1999) CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99:23–33PubMedCrossRef
7.
go back to reference Martín-Fontecha A, Sebastiani S, Höpken UE et al (2003) Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J Exp Med 198:615–621PubMedPubMedCentralCrossRef Martín-Fontecha A, Sebastiani S, Höpken UE et al (2003) Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J Exp Med 198:615–621PubMedPubMedCentralCrossRef
8.
go back to reference Ohl L, Mohaupt M, Czeloth N et al (2004) CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21:279–288PubMedCrossRef Ohl L, Mohaupt M, Czeloth N et al (2004) CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21:279–288PubMedCrossRef
10.
go back to reference Lutz MB, Schuler G (2002) Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol 23:445–449PubMedCrossRef Lutz MB, Schuler G (2002) Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol 23:445–449PubMedCrossRef
11.
go back to reference Baratin M, Foray C, Demaria O et al (2015) Homeostatic NF-κβ signaling in steady-state migratory dendritic cells regulates immune homeostasis and tolerance. Immunity 42:627–639PubMedCrossRef Baratin M, Foray C, Demaria O et al (2015) Homeostatic NF-κβ signaling in steady-state migratory dendritic cells regulates immune homeostasis and tolerance. Immunity 42:627–639PubMedCrossRef
12.
go back to reference Nirschl CJ, Anandasabapathy N (2016) Duality at the gate: skin dendritic cells as mediators of vaccine immunity and tolerance. Hum Vaccines Immunother 12:104–116CrossRef Nirschl CJ, Anandasabapathy N (2016) Duality at the gate: skin dendritic cells as mediators of vaccine immunity and tolerance. Hum Vaccines Immunother 12:104–116CrossRef
13.
go back to reference Dalod M, Chelbi R, Malissen B, Lawrence T (2014) Dendritic cell maturation: functional specialization through signaling specificity and transcriptional programming. EMBO J 33:1104–1116PubMedPubMedCentralCrossRef Dalod M, Chelbi R, Malissen B, Lawrence T (2014) Dendritic cell maturation: functional specialization through signaling specificity and transcriptional programming. EMBO J 33:1104–1116PubMedPubMedCentralCrossRef
14.
15.
go back to reference Cools N, Ponsaerts P, Van Tendeloo VFI, Berneman ZN (2007) Balancing between immunity and tolerance: an interplay between dendritic cells, regulatory T cells, and effector T cells. J Leukoc Biol 82:1365–1374PubMedCrossRef Cools N, Ponsaerts P, Van Tendeloo VFI, Berneman ZN (2007) Balancing between immunity and tolerance: an interplay between dendritic cells, regulatory T cells, and effector T cells. J Leukoc Biol 82:1365–1374PubMedCrossRef
16.
go back to reference Hill M, Cuturi MC (2010) Negative vaccination by tolerogenic dendritic cells in organ transplantation. Curr Opin Organ Transplant 15:738–743PubMedCrossRef Hill M, Cuturi MC (2010) Negative vaccination by tolerogenic dendritic cells in organ transplantation. Curr Opin Organ Transplant 15:738–743PubMedCrossRef
17.
go back to reference Steinman RM, Hawiger D, Nussenzweig MC (2003) Tolerogenic dendritic cells. Annu Rev Immunol 21:685–711PubMedCrossRef Steinman RM, Hawiger D, Nussenzweig MC (2003) Tolerogenic dendritic cells. Annu Rev Immunol 21:685–711PubMedCrossRef
19.
go back to reference Morelli AE, Thomson AW (2007) Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 7:610–621PubMedCrossRef Morelli AE, Thomson AW (2007) Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 7:610–621PubMedCrossRef
20.
go back to reference Mendieta-Zerón H (2011) Developing immunologic tolerance for transplantation at the fetal stage. Immunotherapy 3:1499–1512PubMedCrossRef Mendieta-Zerón H (2011) Developing immunologic tolerance for transplantation at the fetal stage. Immunotherapy 3:1499–1512PubMedCrossRef
22.
go back to reference Chopin M, Nutt SL (2014) Establishing and maintaining the Langerhans cell network. Semin Cell Dev Biol 41:1–7 Chopin M, Nutt SL (2014) Establishing and maintaining the Langerhans cell network. Semin Cell Dev Biol 41:1–7
24.
go back to reference Tamoutounour S, Guilliams M, MontananaSanchis F et al (2013) Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 39:925–938PubMedCrossRef Tamoutounour S, Guilliams M, MontananaSanchis F et al (2013) Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 39:925–938PubMedCrossRef
25.
go back to reference Merad M, Ginhoux F, Collin M (2008) Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat Rev Immunol 8:935–947PubMedCrossRef Merad M, Ginhoux F, Collin M (2008) Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat Rev Immunol 8:935–947PubMedCrossRef
26.
go back to reference Shortman K, Naik SH (2007) Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 7:19–30PubMedCrossRef Shortman K, Naik SH (2007) Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol 7:19–30PubMedCrossRef
27.
go back to reference Cella M, Jarrossay D, Facchetti F et al (1999) Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 5:919–923PubMedCrossRef Cella M, Jarrossay D, Facchetti F et al (1999) Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 5:919–923PubMedCrossRef
28.
go back to reference Naik SH, Metcalf D, van Nieuwenhuijze A et al (2006) Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat Immunol 7:663–671PubMedCrossRef Naik SH, Metcalf D, van Nieuwenhuijze A et al (2006) Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat Immunol 7:663–671PubMedCrossRef
29.
go back to reference Guilliams M, Ginhoux F, Jakubzick C et al (2014) Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat Rev Immunol 14:571–578PubMedPubMedCentralCrossRef Guilliams M, Ginhoux F, Jakubzick C et al (2014) Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat Rev Immunol 14:571–578PubMedPubMedCentralCrossRef
31.
go back to reference MartIn-Fontecha A, Sebastiani S, Höpken UE et al (2003) Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J Exp Med 198:615–621PubMedPubMedCentralCrossRef MartIn-Fontecha A, Sebastiani S, Höpken UE et al (2003) Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J Exp Med 198:615–621PubMedPubMedCentralCrossRef
32.
go back to reference Saeki H, Moore AM, Brown MJ, Hwang ST (1999) Cutting edge: secondary lymphoid-tissue chemokine (SLC) and CC chemokine receptor 7 (CCR7) participate in the emigration pathway of mature dendritic cells from the skin to regional lymph nodes. J Immunol 162:2472–2475PubMed Saeki H, Moore AM, Brown MJ, Hwang ST (1999) Cutting edge: secondary lymphoid-tissue chemokine (SLC) and CC chemokine receptor 7 (CCR7) participate in the emigration pathway of mature dendritic cells from the skin to regional lymph nodes. J Immunol 162:2472–2475PubMed
34.
go back to reference Valladeau J, Ravel O, Dezutter-Dambuyant C et al (2000) Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity 12:71–81PubMedCrossRef Valladeau J, Ravel O, Dezutter-Dambuyant C et al (2000) Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity 12:71–81PubMedCrossRef
35.
go back to reference Kaplan DH, Igyártó BZ, Gaspari AA (2012) Early immune events in the induction of allergic contact dermatitis. Nat Rev Immunol 12:114–124PubMedPubMedCentral Kaplan DH, Igyártó BZ, Gaspari AA (2012) Early immune events in the induction of allergic contact dermatitis. Nat Rev Immunol 12:114–124PubMedPubMedCentral
36.
37.
go back to reference Nizza ST, Campbell JJ (2014) CD11b + Migratory dendritic cells mediate CD8 T cell cross-priming and cutaneous imprinting after topical immunization. PLoS One 9:e91054PubMedPubMedCentralCrossRef Nizza ST, Campbell JJ (2014) CD11b + Migratory dendritic cells mediate CD8 T cell cross-priming and cutaneous imprinting after topical immunization. PLoS One 9:e91054PubMedPubMedCentralCrossRef
38.
go back to reference Clausen BE, Stoitzner P (2015) Functional specialization of skin dendritic cell subsets in regulating T cell responses. Front Immunol 6:1–19CrossRef Clausen BE, Stoitzner P (2015) Functional specialization of skin dendritic cell subsets in regulating T cell responses. Front Immunol 6:1–19CrossRef
39.
go back to reference Igyártá BZ, Haley K, Ortner D et al (2011) Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper responses. Immunity 35:260–272PubMedCentralCrossRef Igyártá BZ, Haley K, Ortner D et al (2011) Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper responses. Immunity 35:260–272PubMedCentralCrossRef
40.
go back to reference Hunger RE, Sieling PA, Ochoa MT et al (2004) Langerhans cells utilize CD1a and langerin to efficiently present nonpeptide antigens to T cells. J Clin Invest 113:701–708PubMedPubMedCentralCrossRef Hunger RE, Sieling PA, Ochoa MT et al (2004) Langerhans cells utilize CD1a and langerin to efficiently present nonpeptide antigens to T cells. J Clin Invest 113:701–708PubMedPubMedCentralCrossRef
41.
go back to reference De Jong A, Cheng T, Huang S et al (2014) CD1a-autoreactive T cells recognize natural skin oils that function as headless antigens. Nat Imunol 15:177–185CrossRef De Jong A, Cheng T, Huang S et al (2014) CD1a-autoreactive T cells recognize natural skin oils that function as headless antigens. Nat Imunol 15:177–185CrossRef
42.
go back to reference Anandasabapathy N, Feder R, Mollah S et al (2014) Classical Flt3L-dependent dendritic cells control immunity to protein vaccine. J Exp Med 211:1875–1891PubMedPubMedCentralCrossRef Anandasabapathy N, Feder R, Mollah S et al (2014) Classical Flt3L-dependent dendritic cells control immunity to protein vaccine. J Exp Med 211:1875–1891PubMedPubMedCentralCrossRef
43.
go back to reference Mollah SA, Dobrin JS, Feder RE et al (2014) Flt3L dependence helps define an uncharacterized subset of murine cutaneous dendritic cells. J Invest Dermatol 134:1265–1275PubMedCrossRef Mollah SA, Dobrin JS, Feder RE et al (2014) Flt3L dependence helps define an uncharacterized subset of murine cutaneous dendritic cells. J Invest Dermatol 134:1265–1275PubMedCrossRef
44.
go back to reference Henri S, Poulin LF, Tamoutounour S et al (2010) CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J Exp Med 207:189–206PubMedPubMedCentralCrossRef Henri S, Poulin LF, Tamoutounour S et al (2010) CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J Exp Med 207:189–206PubMedPubMedCentralCrossRef
45.
go back to reference Tussiwand R, Everts B, Grajales-Reyes GE et al (2015) Klf4 expression in conventional dendritic cells is required for T helper 2 cell responses. Immunity 42:916–928PubMedPubMedCentralCrossRef Tussiwand R, Everts B, Grajales-Reyes GE et al (2015) Klf4 expression in conventional dendritic cells is required for T helper 2 cell responses. Immunity 42:916–928PubMedPubMedCentralCrossRef
46.
go back to reference Schlitzer A, McGovern N, Teo P et al (2013) IRF4 transcription factor-dependent CD11b + dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38:970–983PubMedPubMedCentralCrossRef Schlitzer A, McGovern N, Teo P et al (2013) IRF4 transcription factor-dependent CD11b + dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38:970–983PubMedPubMedCentralCrossRef
47.
go back to reference Nakano H, Free ME, Whitehead GS et al (2012) Pulmonary CD103+ dendritic cells prime Th2 responses to inhaled allergens. Mucosal Immunol 5:53–65PubMedCrossRef Nakano H, Free ME, Whitehead GS et al (2012) Pulmonary CD103+ dendritic cells prime Th2 responses to inhaled allergens. Mucosal Immunol 5:53–65PubMedCrossRef
48.
go back to reference Henri S, Vremec D, Kamath A et al (2001) The dendritic cell populations of mouse lymph nodes. J Immunol 167:741–748PubMedCrossRef Henri S, Vremec D, Kamath A et al (2001) The dendritic cell populations of mouse lymph nodes. J Immunol 167:741–748PubMedCrossRef
49.
go back to reference Borkowski TA, Nelson AJ, Farr AG, Udey MC (1996) Expression of gp40, the murine homologue of human epithelial cell adhesion molecule (ep-CAM), by murine dendritic cells. Eur J Immunol 26:110–114PubMedCrossRef Borkowski TA, Nelson AJ, Farr AG, Udey MC (1996) Expression of gp40, the murine homologue of human epithelial cell adhesion molecule (ep-CAM), by murine dendritic cells. Eur J Immunol 26:110–114PubMedCrossRef
50.
go back to reference Nagao K, Ginhoux F, Leitner WW et al (2009) Murine epidermal Langerhans cells and langerin-expressing dermal dendritic cells are unrelated and exhibit distinct functions. Proc Natl Acad Sci U S A 106:3312–3317PubMedPubMedCentralCrossRef Nagao K, Ginhoux F, Leitner WW et al (2009) Murine epidermal Langerhans cells and langerin-expressing dermal dendritic cells are unrelated and exhibit distinct functions. Proc Natl Acad Sci U S A 106:3312–3317PubMedPubMedCentralCrossRef
51.
go back to reference Malissen B, Tamoutounour S, Henri S (2014) The origins and functions of dendritic cells and macrophages in the skin. Nat Rev Immunol 14:417–428PubMedCrossRef Malissen B, Tamoutounour S, Henri S (2014) The origins and functions of dendritic cells and macrophages in the skin. Nat Rev Immunol 14:417–428PubMedCrossRef
52.
go back to reference Haniffa M, Shin A, Bigley V et al (2012) Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103 + Nonlymphoid dendritic cells. Immunity 37:60–73PubMedPubMedCentralCrossRef Haniffa M, Shin A, Bigley V et al (2012) Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103 + Nonlymphoid dendritic cells. Immunity 37:60–73PubMedPubMedCentralCrossRef
53.
go back to reference Nakano H, Lin KL, Yanagita M et al (2009) Blood-derived inflammatory dendritic cells in lymph nodes stimulate acute TH1 immune responses. Nat Immunol 10:394–402PubMedPubMedCentralCrossRef Nakano H, Lin KL, Yanagita M et al (2009) Blood-derived inflammatory dendritic cells in lymph nodes stimulate acute TH1 immune responses. Nat Immunol 10:394–402PubMedPubMedCentralCrossRef
54.
go back to reference Leon B, Martinez del Hoyo G, Parrillas V et al (2004) Dendritic cell differentiation potential of mouse monocytes: monocytes represent immediate precursors of CD8- and CD8+ splenic dendritic cells. Blood 103:2668–2676PubMedCrossRef Leon B, Martinez del Hoyo G, Parrillas V et al (2004) Dendritic cell differentiation potential of mouse monocytes: monocytes represent immediate precursors of CD8- and CD8+ splenic dendritic cells. Blood 103:2668–2676PubMedCrossRef
55.
go back to reference Hohl TM, Rivera A, Lipuma L et al (2009) Inflammatory monocytes facilitate adaptive CD4 T cell responses during respiratory fungal infection. Cell Host Microbe 6:470–481PubMedPubMedCentralCrossRef Hohl TM, Rivera A, Lipuma L et al (2009) Inflammatory monocytes facilitate adaptive CD4 T cell responses during respiratory fungal infection. Cell Host Microbe 6:470–481PubMedPubMedCentralCrossRef
56.
go back to reference Cheong C, Matos I, Choi J et al (2010) Microbial stimulation fully differentiates monocytes to DC-SIGN / CD209+ dendritic cells for immune T cell areas. Cell 143:416–429PubMedPubMedCentralCrossRef Cheong C, Matos I, Choi J et al (2010) Microbial stimulation fully differentiates monocytes to DC-SIGN / CD209+ dendritic cells for immune T cell areas. Cell 143:416–429PubMedPubMedCentralCrossRef
57.
go back to reference Chicha L (2004) Clonal type I interferon-producing and dendritic cell precursors are contained in both human lymphoid and myeloid progenitor populations. J Exp Med 200:1519–1524PubMedPubMedCentralCrossRef Chicha L (2004) Clonal type I interferon-producing and dendritic cell precursors are contained in both human lymphoid and myeloid progenitor populations. J Exp Med 200:1519–1524PubMedPubMedCentralCrossRef
58.
go back to reference Manz MG, Traver D, Miyamoto T et al (2001) Dendritic cell potentials of early lymphoid and myeloid progenitors. Blood 97:3333–3341PubMedCrossRef Manz MG, Traver D, Miyamoto T et al (2001) Dendritic cell potentials of early lymphoid and myeloid progenitors. Blood 97:3333–3341PubMedCrossRef
59.
go back to reference Wu L, D’Amico A, Hochrein H et al (2001) Development of thymic and splenic dendritic cell populations from different hemopoietic precursors. Blood 98:3376–3382PubMedCrossRef Wu L, D’Amico A, Hochrein H et al (2001) Development of thymic and splenic dendritic cell populations from different hemopoietic precursors. Blood 98:3376–3382PubMedCrossRef
60.
go back to reference Traver D, Akashi K, Manz M et al (2000) Development of CD8α-positive dendritic cells from a common myeloid progenitor. Science 290:2152–2154PubMedCrossRef Traver D, Akashi K, Manz M et al (2000) Development of CD8α-positive dendritic cells from a common myeloid progenitor. Science 290:2152–2154PubMedCrossRef
61.
go back to reference Manz MG, Traver D, Akashi K et al (2001) Dendritic cell development from common myeloid progenitors. Ann N Y Acad Sci 938:167–173PubMedCrossRef Manz MG, Traver D, Akashi K et al (2001) Dendritic cell development from common myeloid progenitors. Ann N Y Acad Sci 938:167–173PubMedCrossRef
62.
go back to reference Lyman SD, Jacobsen SE (1998) C-kit ligand and Flt3 ligand: stem/progenitor cell factors with overlapping yet distinct activities. Blood 91:1101–1134PubMed Lyman SD, Jacobsen SE (1998) C-kit ligand and Flt3 ligand: stem/progenitor cell factors with overlapping yet distinct activities. Blood 91:1101–1134PubMed
63.
go back to reference Onai N, Obata-Onai A, Schmid MA et al (2007) Identification of clonogenic common Flt3 + M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat Immunol 8:1207–1216PubMedCrossRef Onai N, Obata-Onai A, Schmid MA et al (2007) Identification of clonogenic common Flt3 + M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat Immunol 8:1207–1216PubMedCrossRef
64.
go back to reference Naik SH, Sathe P, Park H-Y et al (2007) Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol 8:1217–1226PubMedCrossRef Naik SH, Sathe P, Park H-Y et al (2007) Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol 8:1217–1226PubMedCrossRef
65.
go back to reference Karsunky H, Merad M, Cozzio A et al (2003) Flt3 ligand regulates dendritic cell development from Flt3+ lymphoid and myeloid-committed progenitors to Flt3+ dendritic cells in vivo. J Exp Med 198:305–313PubMedPubMedCentralCrossRef Karsunky H, Merad M, Cozzio A et al (2003) Flt3 ligand regulates dendritic cell development from Flt3+ lymphoid and myeloid-committed progenitors to Flt3+ dendritic cells in vivo. J Exp Med 198:305–313PubMedPubMedCentralCrossRef
66.
go back to reference Waskow C, Liu K, Darrasse-jèze G et al (2008) FMS-like tyrosine kinase 3 is required for dendritic cell development in peripheral lymphoid tissues. Nat Immunol 9:676–683PubMedPubMedCentralCrossRef Waskow C, Liu K, Darrasse-jèze G et al (2008) FMS-like tyrosine kinase 3 is required for dendritic cell development in peripheral lymphoid tissues. Nat Immunol 9:676–683PubMedPubMedCentralCrossRef
67.
go back to reference McKenna HJ (2001) Role of hematopoietic growth factors/flt3 ligand in expansion and regulation of dendritic cells. Curr Opin Hematol 8:149–154PubMedCrossRef McKenna HJ (2001) Role of hematopoietic growth factors/flt3 ligand in expansion and regulation of dendritic cells. Curr Opin Hematol 8:149–154PubMedCrossRef
68.
go back to reference Onai N, Obata-Onai A, Tussiwand R et al (2006) Activation of the Flt3 signal transduction cascade rescues and enhances type I interferon-producing and dendritic cell development. J Exp Med 203:227–238PubMedPubMedCentralCrossRef Onai N, Obata-Onai A, Tussiwand R et al (2006) Activation of the Flt3 signal transduction cascade rescues and enhances type I interferon-producing and dendritic cell development. J Exp Med 203:227–238PubMedPubMedCentralCrossRef
69.
go back to reference Fogg DK, Sibon C, Miled C et al (2006) A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311:83–87PubMedCrossRef Fogg DK, Sibon C, Miled C et al (2006) A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311:83–87PubMedCrossRef
70.
go back to reference Merad M, Sathe P, Helft J et al (2013) The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol 31:563–604PubMedCrossRef Merad M, Sathe P, Helft J et al (2013) The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol 31:563–604PubMedCrossRef
71.
go back to reference Bruno L, Seidl T, Lanzavecchia A (2001) Mouse pre-immunocytes as non-proliferating multipotent precursors of macrophages, interferon-producing cells, CD8α + and CD8α- dendritic cells. Eur J Immunol 31:3403–3412PubMedCrossRef Bruno L, Seidl T, Lanzavecchia A (2001) Mouse pre-immunocytes as non-proliferating multipotent precursors of macrophages, interferon-producing cells, CD8α + and CD8α- dendritic cells. Eur J Immunol 31:3403–3412PubMedCrossRef
74.
go back to reference Langlet C, Tamoutounour S, Henri S et al (2012) CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J Immunol 188:1751–1760PubMedCrossRef Langlet C, Tamoutounour S, Henri S et al (2012) CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J Immunol 188:1751–1760PubMedCrossRef
75.
go back to reference Lewis KL, Caton ML, Bogunovic M et al (2011) Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 35:780–791PubMedPubMedCentralCrossRef Lewis KL, Caton ML, Bogunovic M et al (2011) Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 35:780–791PubMedPubMedCentralCrossRef
77.
go back to reference Hoeffel G, Wang Y, Greter M et al (2012) Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac-derived macrophages. J Exp Med 209:1167–1181PubMedPubMedCentralCrossRef Hoeffel G, Wang Y, Greter M et al (2012) Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac-derived macrophages. J Exp Med 209:1167–1181PubMedPubMedCentralCrossRef
79.
go back to reference Ginhoux F, Collin MP, Bogunovic M et al (2007) Blood-derived dermal langerin + dendritic cells survey the skin in the steady state. J Exp Med 204:3133–3146PubMedPubMedCentralCrossRef Ginhoux F, Collin MP, Bogunovic M et al (2007) Blood-derived dermal langerin + dendritic cells survey the skin in the steady state. J Exp Med 204:3133–3146PubMedPubMedCentralCrossRef
80.
go back to reference Laouar Y, Welte T, Fu XY, Flavell RA (2003) STAT3 is required for Flt3L-dependent dendritic cell differentiation. Immunity 19:903–912PubMedCrossRef Laouar Y, Welte T, Fu XY, Flavell RA (2003) STAT3 is required for Flt3L-dependent dendritic cell differentiation. Immunity 19:903–912PubMedCrossRef
81.
go back to reference Lutz MB, Suri RM, Niimi M et al (2000) Immature dendritic cells generated with low doses of GM-CSF in the absence of IL-4 are maturation resistant and prolong allograft survival in vivo. Eur J Immunol 30:1813–1822PubMedCrossRef Lutz MB, Suri RM, Niimi M et al (2000) Immature dendritic cells generated with low doses of GM-CSF in the absence of IL-4 are maturation resistant and prolong allograft survival in vivo. Eur J Immunol 30:1813–1822PubMedCrossRef
82.
go back to reference Vremec D, J. Lieschke G, R. Dunn A, et al. (1997) The influence of granulocyte/macrophage colony-stimulating factor on dendritic cell levels in mouse lymphoid organs. Eur J Immunol 27:40–44. Vremec D, J. Lieschke G, R. Dunn A, et al. (1997) The influence of granulocyte/macrophage colony-stimulating factor on dendritic cell levels in mouse lymphoid organs. Eur J Immunol 27:40–44.
83.
go back to reference Hamilton JA (2008) Colony-stimulating factors in inflammation and autoimmunity. Nat Rev Immunol 8:533–544PubMedCrossRef Hamilton JA (2008) Colony-stimulating factors in inflammation and autoimmunity. Nat Rev Immunol 8:533–544PubMedCrossRef
84.
go back to reference Lyman SD, Jacobsen SEW (1998) C-kit ligand and Flt3 ligand: stem/progenitor cell factors with overlapping yet distinct activities. Blood 91:1101–1134PubMed Lyman SD, Jacobsen SEW (1998) C-kit ligand and Flt3 ligand: stem/progenitor cell factors with overlapping yet distinct activities. Blood 91:1101–1134PubMed
85.
go back to reference Bozzacco L, Trumpfheller C, Huang Y et al (2010) HIV gag protein is efficiently cross-presented when targeted with an antibody towards the DEC-205 receptor in Flt3 ligand-mobilized murine DC. Eur J Immunol 40:36–46PubMedPubMedCentralCrossRef Bozzacco L, Trumpfheller C, Huang Y et al (2010) HIV gag protein is efficiently cross-presented when targeted with an antibody towards the DEC-205 receptor in Flt3 ligand-mobilized murine DC. Eur J Immunol 40:36–46PubMedPubMedCentralCrossRef
86.
go back to reference Dudziak D, Kampfhorst AO, Heidkamp G et al (2007) Differential antigen processing by dendritic cell subsets in vivo. Science 315:107–111PubMedCrossRef Dudziak D, Kampfhorst AO, Heidkamp G et al (2007) Differential antigen processing by dendritic cell subsets in vivo. Science 315:107–111PubMedCrossRef
87.
go back to reference Tarbell KV, Petit L, Zuo X et al (2007) Dendritic cell-expanded, islet-specific CD4+ CD25+ CD62L+ regulatory T cells restore normoglycemia in diabetic NOD mice. J Exp Med 204:191–201PubMedPubMedCentralCrossRef Tarbell KV, Petit L, Zuo X et al (2007) Dendritic cell-expanded, islet-specific CD4+ CD25+ CD62L+ regulatory T cells restore normoglycemia in diabetic NOD mice. J Exp Med 204:191–201PubMedPubMedCentralCrossRef
88.
89.
go back to reference Dhodapkar MV, Sznol M, Zhao B et al (2014) Induction of antigen-specific immunity with a vaccine targeting NY-ESO-1 to the dendritic cell receptor DEC-205. Sci Transl Med 6:232ra51PubMedCrossRef Dhodapkar MV, Sznol M, Zhao B et al (2014) Induction of antigen-specific immunity with a vaccine targeting NY-ESO-1 to the dendritic cell receptor DEC-205. Sci Transl Med 6:232ra51PubMedCrossRef
90.
go back to reference Spranger S, Bao R, Gajewski TF (2015) Melanoma-intrinsic β-catenin signalling prevents anti-tumour immunity. Nature 523:231–235PubMedCrossRef Spranger S, Bao R, Gajewski TF (2015) Melanoma-intrinsic β-catenin signalling prevents anti-tumour immunity. Nature 523:231–235PubMedCrossRef
91.
go back to reference Salmon H, Idoyaga J, Rahman A et al (2016) Expansion and activation of CD103+ dendritic cell progenitors at the tumor site enhances tumor responses to therapeutic PD-L1 and BRAF inhibition. Immunity 44:924–938PubMedCrossRef Salmon H, Idoyaga J, Rahman A et al (2016) Expansion and activation of CD103+ dendritic cell progenitors at the tumor site enhances tumor responses to therapeutic PD-L1 and BRAF inhibition. Immunity 44:924–938PubMedCrossRef
92.
go back to reference Cisse B, Caton ML, Lehner M et al (2008) Transcription factor E2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell 135:37–48PubMedPubMedCentralCrossRef Cisse B, Caton ML, Lehner M et al (2008) Transcription factor E2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell 135:37–48PubMedPubMedCentralCrossRef
93.
go back to reference Wu L, D’Amico A, Winkel KD et al (1998) RelB is essential for the development of myeloid-related CD8α- dendritic cells but not of lymphoid-related CD8α + dendritic cells. Immunity 9:839–847PubMedCrossRef Wu L, D’Amico A, Winkel KD et al (1998) RelB is essential for the development of myeloid-related CD8α- dendritic cells but not of lymphoid-related CD8α + dendritic cells. Immunity 9:839–847PubMedCrossRef
94.
go back to reference Hildner K, Edelson BT, Purtha WE et al (2008) Batf3 deficiency reveals a critical role for CD8α + dendritic cells in cytotoxic T cell immunity. Science 322:1097–1100PubMedPubMedCentralCrossRef Hildner K, Edelson BT, Purtha WE et al (2008) Batf3 deficiency reveals a critical role for CD8α + dendritic cells in cytotoxic T cell immunity. Science 322:1097–1100PubMedPubMedCentralCrossRef
95.
go back to reference Anderson KL, Perkin H, Surh CD et al (2000) Transcription factor PU.1 is necessary for development of thymic and myeloid progenitor-derived dendritic cells. J Immunol 164:1855–1861PubMedCrossRef Anderson KL, Perkin H, Surh CD et al (2000) Transcription factor PU.1 is necessary for development of thymic and myeloid progenitor-derived dendritic cells. J Immunol 164:1855–1861PubMedCrossRef
96.
go back to reference Spooner CJ, Cheng JX, Pujadas E et al (2009) A recurrent network involving the transcription factors PU.1 and Gfi1 orchestrates innate and adaptive immune cell fates. Immunity 31:576–586PubMedPubMedCentralCrossRef Spooner CJ, Cheng JX, Pujadas E et al (2009) A recurrent network involving the transcription factors PU.1 and Gfi1 orchestrates innate and adaptive immune cell fates. Immunity 31:576–586PubMedPubMedCentralCrossRef
97.
go back to reference Rathinam C, Geffers R, Yucel R et al (2005) The transcriptional repressor Gfi1 controls STAT3-dependent dendritic cell development and function. Immunity 22:717–728PubMedCrossRef Rathinam C, Geffers R, Yucel R et al (2005) The transcriptional repressor Gfi1 controls STAT3-dependent dendritic cell development and function. Immunity 22:717–728PubMedCrossRef
98.
go back to reference Satpathy AT, Kc W, Albring JC et al (2012) Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J Exp Med 209:1135–1152PubMedPubMedCentralCrossRef Satpathy AT, Kc W, Albring JC et al (2012) Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J Exp Med 209:1135–1152PubMedPubMedCentralCrossRef
99.
go back to reference Meredith MM, Liu K, Darrasse-Jeze G et al (2012) Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J Exp Med 209:1153–1165PubMedPubMedCentralCrossRef Meredith MM, Liu K, Darrasse-Jeze G et al (2012) Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J Exp Med 209:1153–1165PubMedPubMedCentralCrossRef
100.
go back to reference Ichikawa E, Hida S, Omatsu Y et al (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 101:3909–3914PubMedPubMedCentralCrossRef Ichikawa E, Hida S, Omatsu Y et al (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 101:3909–3914PubMedPubMedCentralCrossRef
101.
go back to reference Suzuki S, Honma K, Matsuyama T et al (2004) Critical roles of interferon regulatory factor 4 in CD11bhighCD8alpha- dendritic cell development. Proc Natl Acad Sci U S A 101:8981–8986PubMedPubMedCentralCrossRef Suzuki S, Honma K, Matsuyama T et al (2004) Critical roles of interferon regulatory factor 4 in CD11bhighCD8alpha- dendritic cell development. Proc Natl Acad Sci U S A 101:8981–8986PubMedPubMedCentralCrossRef
102.
go back to reference Tamura T, Tailor P, Yamaoka K et al (2005) IFN regulatory factor-4 and -8 govern dendritic cell subset development and their functional diversity. J Immunol 174:2573–2581PubMedCrossRef Tamura T, Tailor P, Yamaoka K et al (2005) IFN regulatory factor-4 and -8 govern dendritic cell subset development and their functional diversity. J Immunol 174:2573–2581PubMedCrossRef
103.
go back to reference Schiavoni G, Mattei F, Borghi P et al (2004) ICSBP is critically involved in the normal development and trafficking of Langerhans cells and dermal dendritic cells. Blood 103:2221–2228PubMedCrossRef Schiavoni G, Mattei F, Borghi P et al (2004) ICSBP is critically involved in the normal development and trafficking of Langerhans cells and dermal dendritic cells. Blood 103:2221–2228PubMedCrossRef
104.
go back to reference Aliberti J, Schulz O, Pennington DJ et al (2003) Essential role for ICSBP in the in vivo development of murine CD8α + dendritic cells. Blood 101:305–310PubMedCrossRef Aliberti J, Schulz O, Pennington DJ et al (2003) Essential role for ICSBP in the in vivo development of murine CD8α + dendritic cells. Blood 101:305–310PubMedCrossRef
106.
go back to reference Hacker C, Kirsch RD, Ju X-S et al (2003) Transcriptional profiling identifies Id2 function in dendritic cell development. Nat Immunol 4:380–386PubMedCrossRef Hacker C, Kirsch RD, Ju X-S et al (2003) Transcriptional profiling identifies Id2 function in dendritic cell development. Nat Immunol 4:380–386PubMedCrossRef
107.
go back to reference Nagasawa M, Schmidlin H, Hazekamp MG et al (2008) Development of human plasmacytoid dendritic cells depends on the combined action of the basic helix-loop-helix factor E2-2 and the Ets factor Spi-B. Eur J Immunol 38:2389–2400PubMedCrossRef Nagasawa M, Schmidlin H, Hazekamp MG et al (2008) Development of human plasmacytoid dendritic cells depends on the combined action of the basic helix-loop-helix factor E2-2 and the Ets factor Spi-B. Eur J Immunol 38:2389–2400PubMedCrossRef
108.
go back to reference Edelson BT, Kc W, Juang R et al (2010) Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha + conventional dendritic cells. J Exp Med 207:823–836PubMedPubMedCentralCrossRef Edelson BT, Kc W, Juang R et al (2010) Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha + conventional dendritic cells. J Exp Med 207:823–836PubMedPubMedCentralCrossRef
109.
go back to reference Fainaru O, Woolf E, Lotem J et al (2004) Runx3 regulates mouse TGF-beta-mediated dendritic cell function and its absence results in airway inflammation. EMBO J 23:969–979PubMedPubMedCentralCrossRef Fainaru O, Woolf E, Lotem J et al (2004) Runx3 regulates mouse TGF-beta-mediated dendritic cell function and its absence results in airway inflammation. EMBO J 23:969–979PubMedPubMedCentralCrossRef
110.
go back to reference Esashi E, Wang YH, Perng O et al (2008) The signal transducer STAT5 inhibits plasmacytoid dendritic cell development by suppressing transcription factor IRF8. Immunity 28:509–520PubMedPubMedCentralCrossRef Esashi E, Wang YH, Perng O et al (2008) The signal transducer STAT5 inhibits plasmacytoid dendritic cell development by suppressing transcription factor IRF8. Immunity 28:509–520PubMedPubMedCentralCrossRef
111.
112.
go back to reference Wu L, Nichogiannopoulou A, Shortman K, Georgopoulos K (1997) Cell-autonomous defects in dendritic cell populations of Ikaros mutant mice point to a developmental relationship with the lymphoid lineage. Immunity 7:483–492PubMedCrossRef Wu L, Nichogiannopoulou A, Shortman K, Georgopoulos K (1997) Cell-autonomous defects in dendritic cell populations of Ikaros mutant mice point to a developmental relationship with the lymphoid lineage. Immunity 7:483–492PubMedCrossRef
113.
114.
go back to reference Jackson JT, Hu Y, Liu R et al (2011) Id2 expression delineates differential checkpoints in the genetic program of CD8alpha + and CD103+ dendritic cell lineages. EMBO J 30:2690–2704PubMedPubMedCentralCrossRef Jackson JT, Hu Y, Liu R et al (2011) Id2 expression delineates differential checkpoints in the genetic program of CD8alpha + and CD103+ dendritic cell lineages. EMBO J 30:2690–2704PubMedPubMedCentralCrossRef
115.
go back to reference Platzer B, Jörgl A, Taschner S et al (2004) RelB regulates human dendritic cell subset development by promoting monocyte intermediates. Blood 104:3655–3663PubMedCrossRef Platzer B, Jörgl A, Taschner S et al (2004) RelB regulates human dendritic cell subset development by promoting monocyte intermediates. Blood 104:3655–3663PubMedCrossRef
116.
go back to reference Kingston D, Schmid MA, Onai N et al (2009) The concerted action of GM-CSF and Flt3-ligand on in vivo dendritic cell homeostasis. Blood 114:835–843PubMedCrossRef Kingston D, Schmid MA, Onai N et al (2009) The concerted action of GM-CSF and Flt3-ligand on in vivo dendritic cell homeostasis. Blood 114:835–843PubMedCrossRef
117.
go back to reference Greter M, Helft J, Chow A et al (2012) GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity 36:1031–1046PubMedPubMedCentralCrossRef Greter M, Helft J, Chow A et al (2012) GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity 36:1031–1046PubMedPubMedCentralCrossRef
118.
go back to reference Kel JM, Girard-Madoux MJH, Reizis B, Clausen BE (2010) TGF-β is required to maintain the pool of immature langerhans cells in the epidermis. J Immunol 185:3248–3255PubMedCrossRef Kel JM, Girard-Madoux MJH, Reizis B, Clausen BE (2010) TGF-β is required to maintain the pool of immature langerhans cells in the epidermis. J Immunol 185:3248–3255PubMedCrossRef
119.
go back to reference Wang Y-G, Kim KD, Wang J et al (2005) Stimulating lymphotoxin beta receptor on the dendritic cells is critical for their homeostasis and expansion. J Immunol 175:6997–7002PubMedCrossRef Wang Y-G, Kim KD, Wang J et al (2005) Stimulating lymphotoxin beta receptor on the dendritic cells is critical for their homeostasis and expansion. J Immunol 175:6997–7002PubMedCrossRef
120.
go back to reference Wu Q, Wang Y, Wang J et al (1999) The requirement of membrane lymphotoxin for the presence of dendritic cells in lymphoid tissues. J Exp Med 190:629–638PubMedPubMedCentralCrossRef Wu Q, Wang Y, Wang J et al (1999) The requirement of membrane lymphotoxin for the presence of dendritic cells in lymphoid tissues. J Exp Med 190:629–638PubMedPubMedCentralCrossRef
121.
go back to reference Qian C, Qian L, Yu Y et al (2013) Fas signal promotes the immunosuppressive function of regulatory dendritic cells via the ERK/β-catenin pathway. J Biol Chem 288:27825–27835PubMedPubMedCentralCrossRef Qian C, Qian L, Yu Y et al (2013) Fas signal promotes the immunosuppressive function of regulatory dendritic cells via the ERK/β-catenin pathway. J Biol Chem 288:27825–27835PubMedPubMedCentralCrossRef
122.
go back to reference Bonasio R, Scimone ML, Schaerli P et al (2006) Clonal deletion of thymocytes by circulating dendritic cells homing to the thymus. Nat Immunol 7:1092–1100PubMedCrossRef Bonasio R, Scimone ML, Schaerli P et al (2006) Clonal deletion of thymocytes by circulating dendritic cells homing to the thymus. Nat Immunol 7:1092–1100PubMedCrossRef
123.
go back to reference Proietto AI, van Dommelen S, Zhou P et al (2008) Dendritic cells in the thymus contribute to T-regulatory cell induction. Proc Natl Acad Sci U S A 105:19869–19874PubMedPubMedCentralCrossRef Proietto AI, van Dommelen S, Zhou P et al (2008) Dendritic cells in the thymus contribute to T-regulatory cell induction. Proc Natl Acad Sci U S A 105:19869–19874PubMedPubMedCentralCrossRef
124.
go back to reference Watanabe N, Wang Y-H, Lee HK et al (2005) Hassall’s corpuscles instruct dendritic cells to induce CD4 + CD25+ regulatory T cells in human thymus. Nature 436:1181–1185PubMedCrossRef Watanabe N, Wang Y-H, Lee HK et al (2005) Hassall’s corpuscles instruct dendritic cells to induce CD4 + CD25+ regulatory T cells in human thymus. Nature 436:1181–1185PubMedCrossRef
125.
go back to reference Besin G, Gaudreau S, Menard M et al (2008) Thymic stromal lymphopoietin and thymic stromal lymphopoietin-conditioned dendritic cells induce regulatory T-cell differentiation and protection of NOD mice against diabetes. Diabetes 57:2107–2117PubMedPubMedCentralCrossRef Besin G, Gaudreau S, Menard M et al (2008) Thymic stromal lymphopoietin and thymic stromal lymphopoietin-conditioned dendritic cells induce regulatory T-cell differentiation and protection of NOD mice against diabetes. Diabetes 57:2107–2117PubMedPubMedCentralCrossRef
126.
go back to reference Martin-Gayo E, Sierra-Filardi E, Corbi AL, Toribio ML (2010) Plasmacytoid dendritic cells resident in human thymus drive natural Treg cell development. Blood 115:5366–5375PubMedCrossRef Martin-Gayo E, Sierra-Filardi E, Corbi AL, Toribio ML (2010) Plasmacytoid dendritic cells resident in human thymus drive natural Treg cell development. Blood 115:5366–5375PubMedCrossRef
128.
go back to reference Ardouin L, Luche H, Chelbi R et al (2016) Broad and largely concordant molecular changes characterize tolerogenic and immunogenic dendritic cell maturation in thymus and periphery. Immunity 45:305–318PubMedCrossRef Ardouin L, Luche H, Chelbi R et al (2016) Broad and largely concordant molecular changes characterize tolerogenic and immunogenic dendritic cell maturation in thymus and periphery. Immunity 45:305–318PubMedCrossRef
129.
go back to reference McGrath MM, Najafian N (2012) The role of coinhibitory signaling pathways in transplantation and tolerance. Front Immunol 3:1–17CrossRef McGrath MM, Najafian N (2012) The role of coinhibitory signaling pathways in transplantation and tolerance. Front Immunol 3:1–17CrossRef
130.
go back to reference Yang J, Riella LV, Chock S et al (2011) The novel costimulatory programmed death ligand 1/B7.1 pathway is functional in inhibiting alloimmune responses in vivo. J Immunol 187:1113–1119PubMedPubMedCentralCrossRef Yang J, Riella LV, Chock S et al (2011) The novel costimulatory programmed death ligand 1/B7.1 pathway is functional in inhibiting alloimmune responses in vivo. J Immunol 187:1113–1119PubMedPubMedCentralCrossRef
131.
go back to reference Li H, Shi B (2015) Tolerogenic dendritic cells and their applications in transplantation. Cell Mol Immunol 12:24–30PubMedCrossRef Li H, Shi B (2015) Tolerogenic dendritic cells and their applications in transplantation. Cell Mol Immunol 12:24–30PubMedCrossRef
132.
go back to reference Morelli AE, Thomson AW (2003) Dendritic cells: regulators of alloimmunity and opportunities for tolerance induction. Immunol Rev 196:125–146PubMedCrossRef Morelli AE, Thomson AW (2003) Dendritic cells: regulators of alloimmunity and opportunities for tolerance induction. Immunol Rev 196:125–146PubMedCrossRef
133.
go back to reference Munn DH, Sharma MD, Mellor AL (2004) Ligation of B7-1/B7-2 by human CD4+ T cells triggers indoleamine 2,3-dioxygenase activity in dendritic cells. J Immunol 172:4100–4110PubMedCrossRef Munn DH, Sharma MD, Mellor AL (2004) Ligation of B7-1/B7-2 by human CD4+ T cells triggers indoleamine 2,3-dioxygenase activity in dendritic cells. J Immunol 172:4100–4110PubMedCrossRef
134.
go back to reference Grohmann U, Orabona C, Fallarino F et al (2002) CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat Immunol 3:1097–1101PubMedCrossRef Grohmann U, Orabona C, Fallarino F et al (2002) CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat Immunol 3:1097–1101PubMedCrossRef
135.
go back to reference Mellor AL, Munn DH (2004) IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol 4:762–774PubMedCrossRef Mellor AL, Munn DH (2004) IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol 4:762–774PubMedCrossRef
136.
go back to reference Jürgens B, Hainz U, Fuchs D et al (2009) Interferon-γ-triggered indoleamine2,3-dioxygenase competence in human monocyte-derived dendritic cells induces regulatory activity in allogeneic T cells. Blood 114:3235–3243PubMedCrossRef Jürgens B, Hainz U, Fuchs D et al (2009) Interferon-γ-triggered indoleamine2,3-dioxygenase competence in human monocyte-derived dendritic cells induces regulatory activity in allogeneic T cells. Blood 114:3235–3243PubMedCrossRef
137.
go back to reference Grohmann U, Puccetti P (2002) The immunosuppressive activity of proinflammatory cytokines in experimental models : potential for therapeutic intervention in autoimmunity. Curr Drug Targets Inflamm Allergy 1:77–87PubMedCrossRef Grohmann U, Puccetti P (2002) The immunosuppressive activity of proinflammatory cytokines in experimental models : potential for therapeutic intervention in autoimmunity. Curr Drug Targets Inflamm Allergy 1:77–87PubMedCrossRef
138.
go back to reference Brenk M, Scheler M, Koch S et al (2009) Tryptophan deprivation induces inhibitory receptors ILT3 and ILT4 on dendritic cells favoring the induction of human CD4 + CD25+ Foxp3+ T regulatory cells. J Immunol 183:145–154PubMedCrossRef Brenk M, Scheler M, Koch S et al (2009) Tryptophan deprivation induces inhibitory receptors ILT3 and ILT4 on dendritic cells favoring the induction of human CD4 + CD25+ Foxp3+ T regulatory cells. J Immunol 183:145–154PubMedCrossRef
139.
go back to reference Chauveau C, Rémy S, Royer PJ et al (2005) Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 106:1694–1702PubMedCrossRef Chauveau C, Rémy S, Royer PJ et al (2005) Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood 106:1694–1702PubMedCrossRef
140.
go back to reference Yamashita K, Ollinger R, McDaid J et al (2006) Heme oxygenase-1 is essential for and promotes tolerance to transplanted organs. FASEB J 20:776–778PubMed Yamashita K, Ollinger R, McDaid J et al (2006) Heme oxygenase-1 is essential for and promotes tolerance to transplanted organs. FASEB J 20:776–778PubMed
141.
go back to reference Luckashenak N, Schroeder S, Endt K et al (2008) Constitutive crosspresentation of tissue antigens by dendritic cells controls CD8+ T cell tolerance in vivo. Immunity 28:521–532PubMedCrossRef Luckashenak N, Schroeder S, Endt K et al (2008) Constitutive crosspresentation of tissue antigens by dendritic cells controls CD8+ T cell tolerance in vivo. Immunity 28:521–532PubMedCrossRef
142.
go back to reference Bonifaz L, Bonnyay D, Mahnke K et al (2002) Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J Exp Med 196:1627–1638PubMedPubMedCentralCrossRef Bonifaz L, Bonnyay D, Mahnke K et al (2002) Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J Exp Med 196:1627–1638PubMedPubMedCentralCrossRef
143.
go back to reference Belz GT, Behrens GMN, Smith CM et al (2002) The CD8 + dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J Exp Med 196:1099–1104PubMedPubMedCentralCrossRef Belz GT, Behrens GMN, Smith CM et al (2002) The CD8 + dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J Exp Med 196:1099–1104PubMedPubMedCentralCrossRef
144.
go back to reference Segura E, Amigorena S (2015) Cross-Presentation in Mouse and Human Dendritic Cells, 1st ed. Adv Immunol Segura E, Amigorena S (2015) Cross-Presentation in Mouse and Human Dendritic Cells, 1st ed. Adv Immunol
145.
go back to reference Bedoui S, Whitney PG, Waithman J et al (2009) Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol 10:488–495PubMedCrossRef Bedoui S, Whitney PG, Waithman J et al (2009) Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol 10:488–495PubMedCrossRef
146.
go back to reference del Rio M-L, Rodriguez-Barbosa J-I, Kremmer E, Förster 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 178:6861–6866PubMedCrossRef del Rio M-L, Rodriguez-Barbosa J-I, Kremmer E, Förster 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 178:6861–6866PubMedCrossRef
147.
go back to reference Amigorena S, Savina A (2010) Intracellular mechanisms of antigen cross presentation in dendritic cells. Curr Opin Immunol 22:109–117PubMedCrossRef Amigorena S, Savina A (2010) Intracellular mechanisms of antigen cross presentation in dendritic cells. Curr Opin Immunol 22:109–117PubMedCrossRef
148.
go back to reference Lennon-Duménil A-M, Bakker AH, Maehr R et al (2002) Analysis of protease activity in live antigen-presenting cells shows regulation of the phagosomal proteolytic contents during dendritic cell activation. J Exp Med 196:529–540PubMedPubMedCentralCrossRef Lennon-Duménil A-M, Bakker AH, Maehr R et al (2002) Analysis of protease activity in live antigen-presenting cells shows regulation of the phagosomal proteolytic contents during dendritic cell activation. J Exp Med 196:529–540PubMedPubMedCentralCrossRef
149.
go back to reference Trombetta ES, Ebersold M, Garrett MP, Mellman I (2003) Activation of lysosomal function during dendritic cell maturation. Science 299:1400–1403PubMedCrossRef Trombetta ES, Ebersold M, Garrett MP, Mellman I (2003) Activation of lysosomal function during dendritic cell maturation. Science 299:1400–1403PubMedCrossRef
150.
go back to reference Savina A, Jancic C, Hugues S et al (2006) NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126:205–218PubMedCrossRef Savina A, Jancic C, Hugues S et al (2006) NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126:205–218PubMedCrossRef
152.
go back to reference Kim JM, Kim JM, Rudensky A, Rudensky A (2006) The role of the transcription factor Foxp3 in the development of regulatory T cells. Immunol Rev 212:86–98PubMedCrossRef Kim JM, Kim JM, Rudensky A, Rudensky A (2006) The role of the transcription factor Foxp3 in the development of regulatory T cells. Immunol Rev 212:86–98PubMedCrossRef
153.
go back to reference Vigouroux S, Yvon E, Biagi E, Brenner MK (2004) Antigen-induced regulatory T cells. Blood 104:26–33PubMedCrossRef Vigouroux S, Yvon E, Biagi E, Brenner MK (2004) Antigen-induced regulatory T cells. Blood 104:26–33PubMedCrossRef
156.
go back to reference Ostroukhova M, Seguin-devaux C, Oriss TB et al (2004) Tolerance induced by inhaled antigen involves CD4 + T cells expressing membrane-bound TGF-β and FOXP3. J Clin Invest 114:28–38PubMedPubMedCentralCrossRef Ostroukhova M, Seguin-devaux C, Oriss TB et al (2004) Tolerance induced by inhaled antigen involves CD4 + T cells expressing membrane-bound TGF-β and FOXP3. J Clin Invest 114:28–38PubMedPubMedCentralCrossRef
157.
go back to reference Tsuji NM, Kosaka A (2008) Oral tolerance: intestinal homeostasis and antigen-specific regulatory T cells. Trends Immunol 29:532–540PubMedCrossRef Tsuji NM, Kosaka A (2008) Oral tolerance: intestinal homeostasis and antigen-specific regulatory T cells. Trends Immunol 29:532–540PubMedCrossRef
158.
go back to reference Cronin SJF, Penninger JM (2007) From T-cell activation signals to signaling control of anti-cancer immunity. Immunol Rev 220:151–168PubMedCrossRef Cronin SJF, Penninger JM (2007) From T-cell activation signals to signaling control of anti-cancer immunity. Immunol Rev 220:151–168PubMedCrossRef
159.
go back to reference Tisch R (2010) Immunogenic versus tolerogenic dendritic cells: a matter of maturation. Int Rev Immunol 29:111–118PubMedCrossRef Tisch R (2010) Immunogenic versus tolerogenic dendritic cells: a matter of maturation. Int Rev Immunol 29:111–118PubMedCrossRef
160.
go back to reference Hintzen G, Ohl L, del Rio M-L et al (2006) Induction of tolerance to innocuous inhaled antigen relies on a CCR7-dependent dendritic cell-mediated antigen transport to the bronchial lymph node. J Immunol 177:7346–7354PubMedCrossRef Hintzen G, Ohl L, del Rio M-L et al (2006) Induction of tolerance to innocuous inhaled antigen relies on a CCR7-dependent dendritic cell-mediated antigen transport to the bronchial lymph node. J Immunol 177:7346–7354PubMedCrossRef
161.
go back to reference Worbs T, Bode U, Yan S et al (2006) Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J Exp Med 203:519–527PubMedPubMedCentralCrossRef Worbs T, Bode U, Yan S et al (2006) Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J Exp Med 203:519–527PubMedPubMedCentralCrossRef
162.
go back to reference Förster R, Davalos-Misslitz AC, Rot A (2008) CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol 8:362–371PubMedCrossRef Förster R, Davalos-Misslitz AC, Rot A (2008) CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol 8:362–371PubMedCrossRef
163.
go back to reference Langenkamp A, Messi M, Lanzavecchia A, Sallusto F (2000) Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat Immunol 1:311–316PubMedCrossRef Langenkamp A, Messi M, Lanzavecchia A, Sallusto F (2000) Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat Immunol 1:311–316PubMedCrossRef
164.
go back to reference Langenkamp A, Casorati G, Garavaglia C et al (2002) T cell priming by dendritic cells: thresholds for proliferation, differentiation and death and intraclonal functional diversification. Eur J Immunol 32:2046–2054PubMedCrossRef Langenkamp A, Casorati G, Garavaglia C et al (2002) T cell priming by dendritic cells: thresholds for proliferation, differentiation and death and intraclonal functional diversification. Eur J Immunol 32:2046–2054PubMedCrossRef
165.
go back to reference Croker BA, Krebs DL, Zhang J-G et al (2003) SOCS3 negatively regulates IL-6 signaling in vivo. Nat Immunol 4:540–545PubMedCrossRef Croker BA, Krebs DL, Zhang J-G et al (2003) SOCS3 negatively regulates IL-6 signaling in vivo. Nat Immunol 4:540–545PubMedCrossRef
166.
go back to reference Pasare C, Medzhitov R (2003) Toll pathway-dependent blockade of CD4 + CD25+ T cell-mediated suppression by dendritic cells. Science 299:1033–1036PubMedCrossRef Pasare C, Medzhitov R (2003) Toll pathway-dependent blockade of CD4 + CD25+ T cell-mediated suppression by dendritic cells. Science 299:1033–1036PubMedCrossRef
167.
go back to reference Veillette A, Latour S (2003) The SLAM family of immune-cell receptors. Curr Opin Immunol 15:277–285PubMedCrossRef Veillette A, Latour S (2003) The SLAM family of immune-cell receptors. Curr Opin Immunol 15:277–285PubMedCrossRef
168.
169.
go back to reference Ohnmacht C, Pullner A, King SBS et al (2009) Constitutive ablation of dendritic cells breaks self-tolerance of CD4 T cells and results in spontaneous fatal autoimmunity. J Exp Med 206:549–559PubMedPubMedCentralCrossRef Ohnmacht C, Pullner A, King SBS et al (2009) Constitutive ablation of dendritic cells breaks self-tolerance of CD4 T cells and results in spontaneous fatal autoimmunity. J Exp Med 206:549–559PubMedPubMedCentralCrossRef
170.
go back to reference Laouar Y, Town T, Jeng D et al (2008) TGF-beta signaling in dendritic cells is a prerequisite for the control of autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 105:10865–10870PubMedPubMedCentralCrossRef Laouar Y, Town T, Jeng D et al (2008) TGF-beta signaling in dendritic cells is a prerequisite for the control of autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 105:10865–10870PubMedPubMedCentralCrossRef
171.
172.
go back to reference Darrasse-Jeze G, Deroubaix S, Mouquet H et al (2009) Feedback control of regulatory T cell homeostasis by dendritic cells in vivo. J Exp Med 206:1853–1862PubMedPubMedCentralCrossRef Darrasse-Jeze G, Deroubaix S, Mouquet H et al (2009) Feedback control of regulatory T cell homeostasis by dendritic cells in vivo. J Exp Med 206:1853–1862PubMedPubMedCentralCrossRef
173.
go back to reference Volchenkov R, Karlsen M, Jonsson R, Appel S (2013) Type 1 regulatory T cells and regulatory B cells induced by tolerogenic dendritic cells. Scand J Immunol 77:246–254PubMedCrossRef Volchenkov R, Karlsen M, Jonsson R, Appel S (2013) Type 1 regulatory T cells and regulatory B cells induced by tolerogenic dendritic cells. Scand J Immunol 77:246–254PubMedCrossRef
175.
go back to reference Qian L, Qian C, Chen Y et al (2012) Regulatory dendritic cells program B cells to differentiate into CD19hiFcγIIbhi regulatory B cells through IFN-β and CD40L. Blood 120:581–591PubMedCrossRef Qian L, Qian C, Chen Y et al (2012) Regulatory dendritic cells program B cells to differentiate into CD19hiFcγIIbhi regulatory B cells through IFN-β and CD40L. Blood 120:581–591PubMedCrossRef
176.
go back to reference Obayashi K, Doi T, Koyasu S (2007) Dendritic cells suppress IgE production in B cells. Int Immunol 19:217–226PubMedCrossRef Obayashi K, Doi T, Koyasu S (2007) Dendritic cells suppress IgE production in B cells. Int Immunol 19:217–226PubMedCrossRef
177.
go back to reference Caielli S, Conforti-Andreoni C, Di Pietro C et al (2010) On/off TLR signaling decides proinflammatory or tolerogenic dendritic cell maturation upon CD1d-mediated interaction with invariant NKT cells. J Immunol 185:7317–7329PubMedCrossRef Caielli S, Conforti-Andreoni C, Di Pietro C et al (2010) On/off TLR signaling decides proinflammatory or tolerogenic dendritic cell maturation upon CD1d-mediated interaction with invariant NKT cells. J Immunol 185:7317–7329PubMedCrossRef
178.
179.
go back to reference Leveson-Gower DB, Sega EI, Kalesnikoff J et al (2013) Mast cells suppress murine GVHD in a mechanism independent of CD4 + CD25+ regulatory T cells. Blood 122:3659–3665PubMedPubMedCentralCrossRef Leveson-Gower DB, Sega EI, Kalesnikoff J et al (2013) Mast cells suppress murine GVHD in a mechanism independent of CD4 + CD25+ regulatory T cells. Blood 122:3659–3665PubMedPubMedCentralCrossRef
180.
go back to reference Lu L-F, Lind EF, Gondek DC et al (2006) Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 442:997–1002PubMedCrossRef Lu L-F, Lind EF, Gondek DC et al (2006) Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 442:997–1002PubMedCrossRef
181.
182.
go back to reference Ito K, Chung KF, Adcock IM (2006) Update on glucocorticoid action and resistance. J Allergy Clin Immunol 117:522–543PubMedCrossRef Ito K, Chung KF, Adcock IM (2006) Update on glucocorticoid action and resistance. J Allergy Clin Immunol 117:522–543PubMedCrossRef
183.
go back to reference Puccetti P, Grohmann U (2007) IDO and regulatory T cells: a role for reverse signalling and non-canonical NF-kappaB activation. Nat Rev Immunol 7:817–823PubMedCrossRef Puccetti P, Grohmann U (2007) IDO and regulatory T cells: a role for reverse signalling and non-canonical NF-kappaB activation. Nat Rev Immunol 7:817–823PubMedCrossRef
184.
go back to reference Bonizzi G, Karin M (2004) The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25:280–288PubMedCrossRef Bonizzi G, Karin M (2004) The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25:280–288PubMedCrossRef
185.
go back to reference Zhang X, Li M, Lian D et al (2008) Generation of therapeutic dendritic cells and regulatory T cells for preventing allogeneic cardiac graft rejection. Clin Immunol 127:313–321PubMedCrossRef Zhang X, Li M, Lian D et al (2008) Generation of therapeutic dendritic cells and regulatory T cells for preventing allogeneic cardiac graft rejection. Clin Immunol 127:313–321PubMedCrossRef
186.
go back to reference Iruretagoyena MI, Lezana JP, Hermoso M et al (2006) Inhibition of nuclear factor-kappa B enhances the capacity of immature dendritic cells to induce antigen-specific tolerance in experimental autoimmune encephalomyelitis. J Pharmacol Exp Ther 318:59–67PubMedCrossRef Iruretagoyena MI, Lezana JP, Hermoso M et al (2006) Inhibition of nuclear factor-kappa B enhances the capacity of immature dendritic cells to induce antigen-specific tolerance in experimental autoimmune encephalomyelitis. J Pharmacol Exp Ther 318:59–67PubMedCrossRef
187.
go back to reference Bahri R, Naji A, Menier C et al (2009) Dendritic cells secrete the immunosuppressive HLA-G molecule upon CTLA4-Ig treatment: implication in human renal transplant acceptance. J Immunol 183:7054–7062PubMedCrossRef Bahri R, Naji A, Menier C et al (2009) Dendritic cells secrete the immunosuppressive HLA-G molecule upon CTLA4-Ig treatment: implication in human renal transplant acceptance. J Immunol 183:7054–7062PubMedCrossRef
188.
go back to reference Hu J, Wan Y (2010) Tolerogenic dendritic cells and their potential applications. Immunology 132:307–314CrossRef Hu J, Wan Y (2010) Tolerogenic dendritic cells and their potential applications. Immunology 132:307–314CrossRef
189.
go back to reference Anandasabapathy N, Breton G, Hurley A et al (2015) Efficacy and safety of CDX-301, recombinant human Flt3L, at expanding dendritic cells and hematopoietic stem cells in healthy human volunteers. Bone Marrow Transplant 50:924–930PubMedPubMedCentralCrossRef Anandasabapathy N, Breton G, Hurley A et al (2015) Efficacy and safety of CDX-301, recombinant human Flt3L, at expanding dendritic cells and hematopoietic stem cells in healthy human volunteers. Bone Marrow Transplant 50:924–930PubMedPubMedCentralCrossRef
190.
go back to reference He S, Chu J, Vasu S et al (2014) FLT3L and plerixafor combination increases hematopoietic stem cell mobilization and leads to improved transplantation outcome. Biol Blood Marrow Transplant 20:309–313PubMedCrossRef He S, Chu J, Vasu S et al (2014) FLT3L and plerixafor combination increases hematopoietic stem cell mobilization and leads to improved transplantation outcome. Biol Blood Marrow Transplant 20:309–313PubMedCrossRef
Metadata
Title
The origin of DCs and capacity for immunologic tolerance in central and peripheral tissues
Authors
K . Sanjana P. Devi
Niroshana Anandasabapathy
Publication date
01-02-2017
Publisher
Springer Berlin Heidelberg
Published in
Seminars in Immunopathology / Issue 2/2017
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-016-0602-0

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