Functional langerinhigh-expressing langerhans-like cells can arise from CD14highCD16- human blood monocytes in serum-free condition

Journal of Immunology

Volumn 196, Issue 9, 2016, Pages 3716-3728

  Picarda, Gaëlle ^a,b,c,d   Chéneau, Coraline ^a,b,c   Humbert, Jean Marc ^b   Bériou, Gaëlle ^a,b,c   Pilet, Paul ^c,e   Martin, Jerome ^a,b,c   Duteille, Franck ^b   Perrot, Pierre ^b   Bellier Waast, Frederique ^b   Heslan, Michèle ^a,b,c   Haspot, Fabienne ^a,b,c   Guillon, Fabien ^f   Josien, Regis ^a,b,c   Halary, Franck Albert ^a,b,c  

^a Centre National de la Recherche Scientifique   (France)

^b NANTES UNIVERSITY HOSPITAL   (France)

^c UNIVERSITÉ DE NANTES   (France)

^d LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^e Universite de Nantes   (France)

^f Sterlab   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD16 ANTIGEN; CELL SURFACE MARKER; CUTANEOUS T CELL ATTRACTING CHEMOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; LANGERIN; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; PROTEIN AXL; PROTEIN TROP 2; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; UVOMORULIN; ALLOANTIGEN; AXL RECEPTOR TYROSINE KINASE; CELL ADHESION MOLECULE; FC RECEPTOR; ONCOPROTEIN; PROTEIN TYROSINE KINASE; TACSTD2 PROTEIN, HUMAN; TUMOR ANTIGEN;

ADULT; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ARTICLE; BIRBECK GRANULE; CELL ACTIVATION; CELL CONTACT; CELL DIFFERENTIATION; CELL GRANULE; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; HUMAN; HUMAN CELL; KERATINOCYTE; LYMPHOCYTE PROLIFERATION; MONOCYTE DERIVED DENDRITIC CELL; MONOCYTE DERIVED LANGERHANS CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SERUM-FREE MEDIUM; T LYMPHOCYTE; ULTRAVIOLET RADIATION; BLOOD CELL; CELL CULTURE; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LANGERHANS CELL; LYMPHOCYTE ACTIVATION; METABOLISM; MONOCYTE; PHYSIOLOGY;

ANTIGENS, CD14; ANTIGENS, NEOPLASM; BLOOD CELLS; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; CELLS, CULTURED; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; ISOANTIGENS; KERATINOCYTES; LANGERHANS CELLS; LYMPHOCYTE ACTIVATION; MONOCYTES; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, IGG; SELF TOLERANCE; T-LYMPHOCYTES; TRANSFORMING GROWTH FACTOR BETA1; ULTRAVIOLET RAYS;

EID: 84974851112     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501304     Document Type: Article

References (69)

1. Valladeau, J., O. Ravel, C. Dezutter-Dambuyant, K. Moore, M. Kleijmeer, Y. Liu, V. Duvert-Frances, C. Vincent, D. Schmitt, J. Davoust, 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: 71-81.
2. Chu, A., M. Eisinger, J. S. Lee, S. Takezaki, P. C. Kung, and R. L. Edelson. 1982. Immunoelectron microscopic identification of Langerhans cells using a new antigenic marker. J. Invest. Dermatol. 78: 177-180.
3. + dermal dendritic cells. Immunity 29: 497-510.
4. Seneschal, J., R. A. Clark, A. Gehad, C. M. Baecher-Allan, and T. S. Kupper. 2012. Human epidermal Langerhans cells maintain immune homeostasis in skin by activating skin resident regulatory T cells. Immunity 36: 873-884.
5. Shklovskaya, E., B. J. O'Sullivan, L. G. Ng, B. Roediger, R. Thomas, W. Weninger, and B. Fazekas de St Groth. 2011. Langerhans cells are precommitted to immune tolerance induction. Proc. Natl. Acad. Sci. USA 108: 18049-18054.
6. Hoeffel, G., Y.Wang, M. Greter, P. See, P. Teo, B. Malleret, M. Leboeuf, D. Low, G. Oller, F. Almeida, et al. 2012. Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sacderived macrophages. J. Exp. Med. 209: 1167-1181.
7. Merad, M., M. G. Manz, H. Karsunky, A. Wagers, W. Peters, I. Charo, I. L. Weissman, J. G. Cyster, and E. G. Engleman. 2002. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat. Immunol. 3: 1135-1141.
8. Ginhoux, F., F. Tacke, V. Angeli, M. Bogunovic, M. Loubeau, X. M. Dai, E. R. Stanley, G. J. Randolph, and M. Merad. 2006. Langerhans cells arise from monocytes in vivo. Nat. Immunol. 7: 265-273.
9. Seré, K., J. H. Baek, J. Ober-Blöbaum, G. Muller-Newen, F. Tacke, Y. Yokota, M. Zenke, and T. Hieronymus. 2012. Two distinct types of Langerhans cells populate the skin during steady state and inflammation. Immunity 37: 905-916.
10. Collin, M. P., D. N. Hart, G. H. Jackson, G. Cook, J. Cavet, S. Mackinnon, P. G. Middleton, and A. M. Dickinson. 2006. The fate of human Langerhans cells in hematopoietic stem cell transplantation. J. Exp. Med. 203: 27-33.
11. Mielcarek, M., A. Y. Kirkorian, R. C. Hackman, J. Price, B. E. Storer, B. L. Wood, M. Leboeuf, M. Bogunovic, R. Storb, Y. Inamoto, et al. 2014. Langerhans cell homeostasis and turnover after nonmyeloablative and myeloablative allogeneic hematopoietic cell transplantation. Transplantation 98: 563-568.
12. Kanitakis, J., E. Morelon, P. Petruzzo, L. Badet, and J. M. Dubernard. 2011. Selfrenewal capacity of human epidermal Langerhans cells: observations made on a composite tissue allograft. Exp. Dermatol. 20: 145-146.
13. Petruzzo, P., A. Gazarian, J. Kanitakis, H. Parmentier, V. Guigal, M. Guillot, C. Vial, J. M. Dubernard, E. Morelon, and L. Badet. 2015. Outcomes after bilateral hand allotransplantation: a risk/benefit ratio analysis. Ann. Surg. 261: 213-220.
14. Cohn, R. G., A. Mirkovich, B. Dunlap, P. Burton, S. H. Chiu, E. Eugui, and J. P. Caulfield. 1999. Mycophenolic acid increases apoptosis, lysosomes and lipid droplets in human lymphoid and monocytic cell lines. Transplantation 68: 411-418.
15. Laurent, A. F., S. Dumont, P. Poindron, and C. D. Muller. 1996. Mycophenolic acid suppresses protein N-linked glycosylation in human monocytes and their adhesion to endothelial cells and to some substrates. Exp. Hematol. 24: 59-67.
16. Rogacev, K. S., A. M. Zawada, J. Hundsdorfer, M. Achenbach, G. Held, D. Fliser, and G. H. Heine. 2015. Immunosuppression and monocyte subsets. Nephrol. Dial. Transplant. 30: 143-153.
17. +CD163+ monocyte subpopulations in kidney allograft transplantation. BMC Immunol. 15: 4.
18. Weber, C., K. U. Belge, P. von Hundelshausen, G. Draude, B. Steppich, M. Mack, M. Frankenberger, K. S. Weber, and H. W. Ziegler-Heitbrock. 2000. Differential chemokine receptor expression and function in human monocyte subpopulations. J. Leukoc. Biol. 67: 699-704.
19. + cells differentiate into Langerhans cells. Nat. Immunol. 2: 1151-1158.
20. + cells are a transient population of monocyte-derived macrophages. Immunity 41: 465-477.
21. Tamoutounour, S., M. Guilliams, F. Montanana Sanchis, H. Liu, D. Terhorst, C. Malosse, E. Pollet, L. Ardouin, H. Luche, C. Sanchez, et al. 2013. Origins and functional specialization of macrophages and of conventional and monocytederived dendritic cells in mouse skin. Immunity 39: 925-938.
22. Yona, S., K. W. Kim, Y. Wolf, A. Mildner, D. Varol, M. Breker, D. Strauss-Ayali, S. Viukov, M. Guilliams, A. Misharin, et al. 2013. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38: 79-91.
23. Caux, C., B. Vanbervliet, C. Massacrier, C. Dezutter-Dambuyant, B. de Saint-Vis, C. Jacquet, K. Yoneda, S. Imamura, D. Schmitt, and J. Banchereau. 1996. CD34+ hematopoietic progenitors from human cord blood differentiate along two independent dendritic cell pathways in response to GM-CSF+TNF alpha. J. Exp. Med. 184: 695-706.
24. Gatti, E., M. A. Velleca, B. C. Biedermann, W. Ma, J. Unternaehrer, M. W. Ebersold, R. Medzhitov, J. S. Pober, and I. Mellman. 2000. Large-scale culture and selective maturation of human Langerhans cells from granulocyte colony-stimulating factor-mobilized CD34+ progenitors. J. Immunol. 164: 3600-3607.
25. Strobl, H., E. Riedl, C. Scheinecker, C. Bello-Fernandez, W. F. Pickl, K. Rappersberger, O. Majdic, and W. Knapp. 1996. TGF-β1 promotes in vitro development of dendritic cells from CD34+ hemopoietic progenitors. J. Immunol. 157: 1499-1507.
26. Geissmann, F., C. Prost, J. P. Monnet, M. Dy, N. Brousse, and O. Hermine. 1998. Transforming growth factor b1, 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: 961-966.
27. Guironnet, G., C. Dezutter-Dambuyant, C. Vincent, N. Bechetoille, D. Schmitt, and J. Péguet-Navarro. 2002. Antagonistic effects of IL-4 and TGF-β1 on Langerhans cell-related antigen expression by human monocytes. J. Leukoc. Biol. 71: 845-853.
28. Hoshino, N., N. Katayama, T. Shibasaki, K. Ohishi, J. Nishioka, M. Masuya, Y. Miyahara, M. Hayashida, D. Shimomura, T. Kato, et al. 2005. A novel role for Notch ligand Delta-1 as a regulator of human Langerhans cell development from blood monocytes. J. Leukoc. Biol. 78: 921-929.
29. Mohamadzadeh, M., F. Berard, G. Essert, C. Chalouni, B. Pulendran, J. Davoust, G. Bridges, A. K. Palucka, and J. Banchereau. 2001. Interleukin 15 skews monocyte differentiation into dendritic cells with features of Langerhans cells. J. Exp. Med. 194: 1013-1020.
30. Sallusto, F., and A. Lanzavecchia. 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 alpha. J. Exp. Med. 179: 1109-1118.
31. Martńez-Cingolani, C., M. Grandclaudon, M. Jeanmougin, M. Jouve, R. Zollinger, and V. Soumelis. 2014. Human blood BDCA-1 dendritic cells differentiate into Langerhans-like cells with thymic stromal lymphopoietin and TGF-β. Blood 124: 2411-2420.
32. Milne, P., V. Bigley, M. Gunawan, M. Haniffa, and M. Collin. 2015. CD1c+ blood dendritic cells have Langerhans cell potential. Blood 125: 470-473.
33. Péguet-Navarro, J., C. Moulon, C. Caux, C. Dalbiez-Gauthier, J. Banchereau, and D. Schmitt. 1994. Interleukin-10 inhibits the primary allogeneic T cell response to human epidermal Langerhans cells. Eur. J. Immunol. 24: 884-891.
34. Valladeau, J., V. Duvert-Frances, J. J. Pin, C. Dezutter-Dambuyant, C. Vincent, C. Massacrier, J. Vincent, K. Yoneda, J. Banchereau, C. Caux, et al. 1999. The monoclonal antibody DCGM4 recognizes Langerin, a protein specific of Langerhans cells, and is rapidly internalized from the cell surface. Eur. J. Immunol. 29: 2695-2704.
35. Haspot, F., A. Lavault, C. Sinzger, K. Laib Sampaio, Y. D. Stierhof, P. Pilet, C. Bressolette-Bodin, and F. Halary. 2012. Human cytomegalovirus entry into dendritic cells occurs via a macropinocytosis-like pathway in a pH-independent and cholesterol-dependent manner. PLoS One 7: e34795.
36. Relloso, M., A. Puig-Kröger, O. M. Pello, J. L. Rodŕguez-Fernández, G. de la Rosa, N. Longo, J. Navarro, M. A. Muñoz-Fernández, P. Sánchez-Mateos, and A. L. Corb. 2002. DC-SIGN (CD209) expression is IL-4 dependent and is negatively regulated by IFN, TGF-β, and anti-inflammatory agents. J. Immunol. 168: 2634-2643.
37. Ziegler-Heitbrock, L., P. Ancuta, S. Crowe, M. Dalod, V. Grau, D. N. Hart, P. J. Leenen, Y. J. Liu, G. MacPherson, G. J. Randolph, et al. 2010. Nomenclature of monocytes and dendritic cells in blood. Blood 116: e74-e80.
38. Bigley, V., N. McGovern, P. Milne, R. Dickinson, S. Pagan, S. Cookson, M. Haniffa, and M. Collin. 2015. Langerin-expressing dendritic cells in human tissues are related to CD1c+ dendritic cells and distinct from Langerhans cells and CD141high XCR1+ dendritic cells. J. Leukoc. Biol. 97: 627-634
39. Nizzoli, G., J. Krietsch, A. Weick, S. Steinfelder, F. Facciotti, P. Gruarin, A. Bianco, B. Steckel, M. Moro, M. Crosti, et al. 2013. Human CD1c+ dendritic cells secrete high levels of IL-12 and potently prime cytotoxic T-cell responses. Blood 122: 932-942.
40. Yasmin, N., T. Bauer, M. Modak, K. Wagner, C. Schuster, R. Köffel, M. Seyerl, J. Stöckl, A. Elbe-Burger, D. Graf, and H. Strobl. 2013. Identification of bone morphogenetic protein 7 (BMP7) as an instructive factor for human epidermal Langerhans cell differentiation. J. Exp. Med. 210: 2597-2610.
41. Bauer, T., A. Zagórska, J. Jurkin, N. Yasmin, R. Köffel, S. Richter, B. Gesslbauer, G. Lemke, and H. Strobl. 2012. Identification of Axl as a downstream effector of TGF-β1 during Langerhans cell differentiation and epidermal homeostasis. J. Exp. Med. 209: 2033-2047.
42. Eisenwort, G., J. Jurkin, N. Yasmin, T. Bauer, B. Gesslbauer, and H. Strobl. 2011. Identification of TROP2 (TACSTD2), an EpCAM-like molecule, as a specific marker for TGF-β1-dependent human epidermal Langerhans cells. J. Invest. Dermatol. 131: 2049-2057.
43. Riedl, E., J. Stöckl, O. Majdic, C. Scheinecker, W. Knapp, and H. Strobl. 2000. Ligation of E-cadherin on in vitro-generated immature Langerhans-type dendritic cells inhibits their maturation. Blood 96: 4276-4284.
44. Tang, A., M. Amagai, L. G. Granger, J. R. Stanley, and M. C. Udey. 1993. Adhesion of epidermal Langerhans cells to keratinocytes mediated by E-cadherin. Nature 361: 82-85.
45. Mayumi, N., E. Watanabe, Y. Norose, E. Watari, S. Kawana, T. B. Geijtenbeek, and H. Takahashi. 2013. E-cadherin interactions are required for Langerhans cell differentiation. Eur. J. Immunol. 43: 270-280.
46. Yasmin, N., S. Konradi, G. Eisenwort, Y. M. Schichl, M. Seyerl, T. Bauer, J. Stöckl, and H. Strobl. 2013. b-Catenin promotes the differentiation of epidermal Langerhans dendritic cells. J. Invest. Dermatol. 133: 1250-1259.
47. Mumm, J. S., and R. Kopan. 2000. Notch signaling: from the outside in. Dev. Biol. 228: 151-165.
48. Igyártó, B. Z., and D. H. Kaplan. 2013. Antigen presentation by Langerhans cells. Curr. Opin. Immunol. 25: 115-119.
49. Ratzinger, G., J. Baggers, M. A. de Cos, J. Yuan, T. Dao, J. L. Reagan, C. Munz, G. Heller, and J. W. Young. 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: 2780-2791.
50. Homey, B., W. Wang, H. Soto, M. E. Buchanan, A. Wiesenborn, D. Catron, A. Muller, T. K. McClanahan, M. C. Dieu-Nosjean, R. Orozco, et al. 2000. Cutting edge: the orphan chemokine receptor G protein-coupled receptor-2 (GPR-2, CCR10) binds the skin-associated chemokine CCL27 (CTACK/ALP/ILC). J. Immunol. 164: 3465-3470.
51. Lichtenberger, B. M., P. A. Gerber, M. Holcmann, B. A. Buhren, N. Amberg, V. Smolle, H. Schrumpf, E. Boelke, P. Ansari, C. Mackenzie, et al. 2013. Epidermal EGFR controls cutaneous host defense and prevents inflammation. Sci. Transl. Med. 5: 199ra111.
52. Czernielewski, J., P. Vaigot, and M. Prunièras. 1985. Epidermal Langerhans cells-a cycling cell population. J. Invest. Dermatol. 84: 424-426.
53. Czernielewski, J. M., and M. Demarchez. 1987. Further evidence for the selfreproducing capacity of Langerhans cells in human skin. J. Invest. Dermatol. 88: 17-20.
54. Gogolak, P., B. Rethi, I. Szatmari, A. Lanyi, B. Dezso, L. Nagy, and E. Rajnavolgyi. 2007. Differentiation of CD1a2 and CD1a+ monocyte-derived dendritic cells is biased by lipid environment and PPARg. Blood 109: 643-652.
55. Merlot, A. M., D. S. Kalinowski, and D. R. Richardson. 2014. Unraveling the mysteries of serum albumin-more than just a serum protein. Front. Physiol. 5: 299.
56. Peters, T., Jr. 1996. All about Albumin: Biochemistry, Genetics, and Medical Applications. Academic, San Diego, CA.
57. Dzionek, A., A. Fuchs, P. Schmidt, S. Cremer, M. Zysk, S. Miltenyi, D.W. Buck, and J. Schmitz. 2000. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J. Immunol. 165: 6037-6046.
58. Hutter, C., M. Kauer, I. Simonitsch-Klupp, G. Jug, R. Schwentner, J. Leitner, P. Bock, P. Steinberger, W. Bauer, N. Carlesso, et al. 2012. Notch is active in Langerhans cell histiocytosis and confers pathognomonic features on dendritic cells. Blood 120: 5199-5208.
59. Igyártó, B. Z., K. Haley, D. Ortner, A. Bobr, M. Gerami-Nejad, B. T. Edelson, S. M. Zurawski, B. Malissen, G. Zurawski, J. Berman, and D. H. Kaplan. 2011. Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper cell responses. Immunity 35: 260-272.
60. Ingersoll, M. A., R. Spanbroek, C. Lottaz, E. L. Gautier, M. Frankenberger, R. Hoffmann, R. Lang, M. Haniffa, M. Collin, F. Tacke, et al. 2010. Comparison of gene expression profiles between human and mouse monocyte subsets. Blood 115: e10-e19.
61. Ancuta, P., K. Y. Liu, V. Misra, V. S. Wacleche, A. Gosselin, X. Zhou, and D. Gabuzda. 2009. Transcriptional profiling reveals developmental relationship and distinct biological functions of CD16+ and CD162 monocyte subsets. BMC Genomics 10: 403.
62. Zhao, C., H. Zhang, W. C. Wong, X. Sem, H. Han, S. M. Ong, Y. C. Tan, W. H. Yeap, C. S. Gan, K. Q. Ng, et al. 2009. Identification of novel functional differences in monocyte subsets using proteomic and transcriptomic methods. J. Proteome Res. 8: 4028-4038.
63. Jakubzick, C., E. L. Gautier, S. L. Gibbings, D. K. Sojka, A. Schlitzer, T. E. Johnson, S. Ivanov, Q. Duan, S. Bala, T. Condon, et al. 2013. Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 39: 599-610.
64. Miller, J. C., B. D. Brown, T. Shay, E. L. Gautier, V. Jojic, A. Cohain, G. Pandey, M. Leboeuf, K. G. Elpek, J. Helft, et al. 2012. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13: 888-899.
65. Nagao, K., T. Kobayashi, K. Moro, M. Ohyama, T. Adachi, D. Y. Kitashima, S. Ueha, K. Horiuchi, H. Tanizaki, K. Kabashima, et al. 2012. Stress-induced production of chemokines by hair follicles regulates the trafficking of dendritic cells in skin. Nat. Immunol. 13: 744-752.
66. Egea, L., C. S. McAllister, O. Lakhdari, I. Minev, S. Shenouda, and M. F. Kagnoff. 2013. GM-CSF produced by nonhematopoietic cells is required for early epithelial cell proliferation and repair of injured colonic mucosa. J. Immunol. 190: 1702-1713.
67. Hirata, Y., L. Egea, S. M. Dann, L. Eckmann, and M. F. Kagnoff. 2010. GMCSF-facilitated dendritic cell recruitment and survival govern the intestinal mucosal response to a mouse enteric bacterial pathogen. Cell Host Microbe 7: 151-163.
68. Trutmann, M., L. Terracciano, C. Noppen, J. Kloth, M. Kaspar, R. Peterli, P. Tondelli, C. Schaeffer, P. Zajac, M. Heberer, and G. C. Spagnoli. 1998. GMCSF gene expression and protein production in human colorectal cancer cell lines and clinical tumor specimens. Int. J. Cancer 77: 378-385.
69. Schuster, C., C. Vaculik, C. Fiala, S. Meindl, O. Brandt, M. Imhof, G. Stingl, W. Eppel, and A. Elbe-Burger. 2009. HLA-DR+ leukocytes acquire CD1 antigens in embryonic and fetal human skin and contain functional antigenpresenting cells. J. Exp. Med. 206: 169-181.