Langerin-expressing dendritic cells in human tissues are related to CD1c+ dendritic cells and distinct from Langerhans cells and CD141high XCR1+ dendritic cells
Tóm tắt
Langerin is a C-type lectin expressed at high level by LCs of the epidermis. Langerin is also expressed by CD8+/CD103+ XCR1+ cross-presenting DCs of mice but is not found on the homologous human CD141high XCR1+ myeloid DC. Here, we show that langerin is expressed at a low level on DCs isolated from dermis, lung, liver, and lymphoid tissue and that langerin+ DCs are closely related to CD1c+ myeloid DCs. They are distinguishable from LCs by the level of expression of CD1a, EpCAM, CD11b, CD11c, CD13, and CD33 and are found in tissues and tissue-draining LNs devoid of LCs. They are unrelated to CD141high XCR1+ myeloid DCs, lacking the characteristic expression profile of cross-presenting DCs, conserved between mammalian species. Stem cell transplantation and DC deficiency models confirm that dermal langerin+ DCs have an independent homeostasis to LCs. Langerin is not expressed by freshly isolated CD1c+ blood DCs but is rapidly induced on CD1c+ DCs by serum or TGF-β via an ALK-3-dependent pathway. These results show that langerin is expressed outside of the LC compartment of humans and highlight a species difference: langerin is expressed by the XCR1+ “DC1” population of mice but is restricted to the CD1c+ “DC2” population of humans (homologous to CD11b+ DCs in the mouse).
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Guilliams, 2014, Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny, Nat. Rev. Immunol., 14, 571, 10.1038/nri3712
Haniffa, 2012, Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103+ nonlymphoid dendritic cells, Immunity, 37, 60, 10.1016/j.immuni.2012.04.012
Lenz, 1993, Human and murine dermis contain dendritic cells. Isolation by means of a novel method and phenotypical and functional characterization, J. Clin. Invest., 92, 2587, 10.1172/JCI116873
Nestle, 1993, Characterization of dermal dendritic cells obtained from normal human skin reveals phenotypic and functionally distinctive subsets, J. Immunol., 151, 6535, 10.4049/jimmunol.151.11.6535
McLellan, 1998, Dermal dendritic cells associated with T lymphocytes in normal human skin display an activated phenotype, J. Invest. Dermatol., 111, 841, 10.1046/j.1523-1747.1998.00375.x
Angel, 2007, CD14+ antigen-presenting cells in human dermis are less mature than their CD1a+ counterparts, Int. Immunol., 19, 1271, 10.1093/intimm/dxm096
Klechevsky, 2008, Functional specializations of human epidermal Langerhans cells and CD14+ dermal dendritic cells, Immunity, 29, 497, 10.1016/j.immuni.2008.07.013
Haniffa, 2009, Differential rates of replacement of human dermal dendritic cells and macrophages during hematopoietic stem cell transplantation, J. Exp. Med., 206, 371, 10.1084/jem.20081633
Eisenwort, 2011, Identification of TROP2 (TACSTD2), an EpCAM-like molecule, as a specific marker for TGF-beta1-dependent human epidermal Langerhans cells, J. Invest. Dermatol., 131, 2047, 10.1038/jid.2011.164
Welty, 2013, Intestinal lamina propria dendritic cells maintain T cell homeostasis but do not affect commensalism, J. Exp. Med., 210, 2011, 10.1084/jem.20130728
Valladeau, 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, 10.1016/S1074-7613(00)80160-0
Hunger, 2004, Langerhans cells utilize CD1a and langerin to efficiently present nonpeptide antigens to T cells, J. Clin. Invest., 113, 701, 10.1172/JCI200419655
Kissenpfennig, 2005, Disruption of the langerin/CD207 gene abolishes Birbeck granules without a marked loss of Langerhans cell function, Mol. Cell. Biol., 25, 88, 10.1128/MCB.25.1.88-99.2005
Poulin, 2007, The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells, J. Exp. Med., 204, 3119, 10.1084/jem.20071724
Bursch, 2007, Identification of anovel population of Langerin+ dendritic cells, J. Exp. Med., 204, 3147, 10.1084/jem.20071966
Ginhoux, 2007, Blood-derived dermal langerin+dendritic cells survey the skin in the steady state, J. Exp. Med., 204, 3133, 10.1084/jem.20071733
Ginhoux, 2009, The origin and development of nonlymphoid tissue CD103+ DCs, J. Exp. Med., 206, 3115, 10.1084/jem.20091756
Nagao, 2009, Murine epidermal Langerhans cells and langerin-expressing dermal dendritic cells are unrelated and exhibit distinct functions, Proc. Natl. Acad. Sci. USA, 106, 3312, 10.1073/pnas.0807126106
Henri, 2010, CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells, J. Exp. Med., 207, 189, 10.1084/jem.20091964
Caux, 1992, GM-CSF and TNF-alpha cooperate in the generation of dendritic Langerhans cells, Nature, 360, 258, 10.1038/360258a0
Strobl, 1996, TGF-beta 1 promotes in vitro development of dendritic cells from CD34+ hemopoietic progenitors, J. Immunol., 157, 1499, 10.4049/jimmunol.157.4.1499
Ratzinger, 2004, Mature human Langerhans cells derived from CD34+ hematopoietic progenitors stimulate greater cytolytic T lymphocyte activity in the absence of bioactive IL-12p70, by either single peptide presentation or cross-priming, than do dermal-interstitial or monocyte-derived dendritic cells, J. Immunol., 173, 2780, 10.4049/jimmunol.173.4.2780
Yasmin, 2013, Identification of bone morphogenetic protein 7 (BMP7) as an instructive factor for human epidermal Langerhans cell differentiation, J. Exp. Med., 210, 2597, 10.1084/jem.20130275
Collin, 2006, The fate of human Langerhans cells in hematopoietic stem cell transplantation, J. Exp. Med., 203, 27, 10.1084/jem.20051787
Bigley, 2011, The human syndrome of dendritic cell, monocyte, B and NK lymphoid deficiency, J. Exp. Med., 208, 227, 10.1084/jem.20101459
Dickinson, 2011, Exome sequencing identifies GATA-2 mutation as the cause of dendritic cell, monocyte, B and NK lymphoid deficiency, Blood, 118, 2656, 10.1182/blood-2011-06-360313
MacDonald, 2002, Characterization of human blood dendritic cell subsets, Blood, 100, 4512, 10.1182/blood-2001-11-0097
Harman, 2013, Identification of lineage relationships and novel markers of blood and skin human dendritic cells, J. Immunol., 190, 66, 10.4049/jimmunol.1200779
Hoshino, 2005, A novel role for Notch ligand Delta-1 as a regulator of human Langerhans cell development from blood monocytes, J. Leukoc. Biol., 78, 921, 10.1189/jlb.1204746
Bauer, 2012, Identification of Axl as a downstream effector of TGF-β1 during Langerhans cell differentiation and epidermal homeostasis, J. Exp. Med., 209, 2033, 10.1084/jem.20120493
Hutter, 2012, Notch is active in Langerhans cell histiocytosis and confers pathognomonic features on dendritic cells, Blood, 120, 5199, 10.1182/blood-2012-02-410241
Geissmann, 1998, Transforming growth factor beta1, in the presence of granulocyte/macrophage colony-stimulating factor and interleukin 4, induces differentiation of human peripheral blood monocytes into dendritic Langerhans cells, J. Exp. Med., 187, 961, 10.1084/jem.187.6.961
Geissmann, 2001, Differentiation of Langerhans cells in Langerhans cell histiocytosis, Blood, 97, 1241, 10.1182/blood.V97.5.1241
Fleming, 2003, Coincident expression of the chemokine receptors CCR6 and CCR7 by pathologic Langerhans cells in Langerhans cell histiocytosis, Blood, 101, 2473, 10.1182/blood.V101.7.2473
Rust, 2006, Gene expression analysis of dendritic/Langerhans cells and Langerhans cell histiocytosis, J. Pathol., 209, 474, 10.1002/path.2003
Allen, 2010, Cell-specific gene expression in Langerhans cell histiocytosis lesions reveals a distinct profile compared with epidermal Langerhans cells, J. Immunol., 184, 4557, 10.4049/jimmunol.0902336
Chu, 1994, The normal Langerhans cell and the LCH cell, Br. J. Cancer Suppl., 23