Human blood CD1c+ dendritic cells encompass CD5high and CD5low subsets that differ significantly in phenotype, gene expression, and functions

Journal of Immunology

Volumn 198, Issue 4, 2017, Pages 1553-1564

  Yin, Xiangyun ^a,b   Yu, Haisheng ^a,b   Jin, Xiaoyang ^a,b   Li, Jingyun ^a   Guo, Hao ^a   Shi, Quanxing ^c   Yin, Zhao ^c   Xu, Yong ^d   Wang, Xuefei ^d   Liu, Rong ^d   Wang, Shouli ^c   Zhang, Liguo ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c 306 HOSPITAL OF PLA   (China)

^d CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD1C ANTIGEN; CD5 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 22; INTERLEUKIN 4; SECONDARY LYMPHOID TISSUE CHEMOKINE; TRANSCRIPTOME; CCL21 PROTEIN, HUMAN; CD1 ANTIGEN; CD1C PROTEIN, HUMAN; GLYCOPROTEIN; IL10 PROTEIN, HUMAN; INTERFERON REGULATORY FACTOR; INTERFERON REGULATORY FACTOR-4; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22;

ANTIGEN EXPRESSION; ARTICLE; BLOOD DENDRITIC CELL; CELL FUNCTION; CELL MIGRATION; CELL SUBPOPULATION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IFN REGULATORY FACTOR 4 GENE; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE PROLIFERATION; MAFB GENE; PROTEIN EXPRESSION; T LYMPHOCYTE; TRANSCRIPTOMICS; BIOSYNTHESIS; BLOOD CELL; CELL DIFFERENTIATION; CLASSIFICATION; DENDRITIC CELL; DRUG EFFECTS; GENETICS; HELPER CELL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PHENOTYPE; PHYSIOLOGY; REGULATORY T LYMPHOCYTE; TH1 CELL;

ANTIGENS, CD1; ANTIGENS, CD5; BLOOD CELLS; CELL DIFFERENTIATION; CHEMOKINE CCL21; DENDRITIC CELLS; GLYCOPROTEINS; HUMANS; IMMUNE TOLERANCE; INTERFERON REGULATORY FACTORS; INTERLEUKIN-10; INTERLEUKIN-4; INTERLEUKINS; LYMPHOCYTE ACTIVATION; PHENOTYPE; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY; TH1 CELLS;

EID: 85014662427     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600193     Document Type: Article

References (63)

1. Steinman, R. M. 2012. Decisions about dendritic cells: past, present, and future. Annu. Rev. Immunol. 30: 1-22.
2. Iwasaki, A., and R. Medzhitov. 2015. Control of adaptive immunity by the innate immune system. Nat. Immunol. 16: 343-353.
3. Lewis, K. L., and B. Reizis. 2012. Dendritic cells: arbiters of immunity and immunological tolerance. Cold Spring Harb. Perspect. Biol. 4: a007401.
4. Guilliams, M., F. Ginhoux, C. Jakubzick, S. H. Naik, N. Onai, B. U. Schraml, E. Segura, R. Tussiwand, and S. Yona. 2014. Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat. Rev. Immunol. 14: 571-578.
5. Merad, M., P. Sathe, J. Helft, J. Miller, and A. Mortha. 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: 563-604.
6. Robbins, S. H., T. Walzer, D. Dembélé, C. Thibault, A. Defays, G. Bessou, H. Xu, E. Vivier, M. Sellars, P. Pierre, et al. 2008. Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol. 9: R17.
7. Poulin, L. F., M. Salio, E. Griessinger, F. Anjos-Afonso, L. Craciun, J. L. Chen, A. M. Keller, O. Joffre, S. Zelenay, E. Nye, et al. 2010. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8a+ dendritic cells. J. Exp. Med. 207: 1261-1271.
8. Jongbloed, S. L., A. J. Kassianos, K. J. McDonald, G. J. Clark, X. Ju, C. E. Angel, C. J. J. Chen, P. R. Dunbar, R. B. Wadley, V. Jeet, et al. 2010. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that crosspresents necrotic cell antigens. J. Exp. Med. 207: 1247-1260.
9. Crozat, K., R. Guiton, V. Contreras, V. Feuillet, C. A. Dutertre, E. Ventre, T. P. Vu Manh, T. Baranek, A. K. Storset, J. Marvel, et al. 2010. The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8a+ dendritic cells. J. Exp. Med. 207: 1283-1292.
10. Bachem, A., S. Guttler, E. Hartung, F. Ebstein, M. Schaefer, A. Tannert, A. Salama, K. Movassaghi, C. Opitz, H. W. Mages, et al. 2010. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as homologues of mouse CD8+ dendritic cells. J. Exp. Med. 207: 1273-1281.
11. Segura, E., M. Durand, and S. Amigorena. 2013. Similar antigen crosspresentation capacity and phagocytic functions in all freshly isolated human lymphoid organ-resident dendritic cells. J. Exp. Med. 210: 1035-1047.
12. Segura, E., J. Valladeau-Guilemond, M. H. Donnadieu, X. Sastre-Garau, V. Soumelis, and S. Amigorena. 2012. Characterization of resident and migratory dendritic cells in human lymph nodes. J. Exp. Med. 209: 653-660.
13. Tussiwand, R., B. Everts, G. E. Grajales-Reyes, N. M. Kretzer, A. Iwata, J. Bagaitkar, X. Wu, R. Wong, D. A. Anderson, T. L. Murphy, et al. 2015. Klf4 expression in conventional dendritic cells is required for T helper 2 cell responses. Immunity 42: 916-928.
14. Satpathy, A. T., C. G. Brisenõ, J. S. Lee, D. Ng, N. A. Manieri, W. Kc, X. Wu, S. R. Thomas, W. L. Lee, M. Turkoz, et al. 2013. Notch2-dependent classical dendritic cells orchestrate intestinal immunity to attaching-and-effacing bacterial pathogens. Nat. Immunol. 14: 937-948.
15. Lewis, K. L., M. L. Caton, M. Bogunovic, M. Greter, L. T. Grajkowska, D. Ng, A. Klinakis, I. F. Charo, S. Jung, J. L. Gommerman, et al. 2011. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 35: 780-791.
16. Platt, A. M., and G. J. Randolph. 2013. Dendritic cell migration through the lymphatic vasculature to lymph nodes. Adv. Immunol. 120: 51-68.
17. Kellermann, S. A., S. Hudak, E. R. Oldham, Y. J. Liu, and L. M. McEvoy. 1999. The CC chemokine receptor-7 ligands 6Ckine and macrophage inflammatory protein-3b are potent chemoattractants for in vitro-and in vivo-derived dendritic cells. J. Immunol. 162: 3859-3864.
18. Campbell, J. J., E. P. Bowman, K. Murphy, K. R. Youngman, M. A. Siani, D. A. Thompson, L. Wu, A. Zlotnik, and E. C. Butcher. 1998. 6-C-kine (SLC), a lymphocyte adhesion-triggering chemokine expressed by high endothelium, is an agonist for the MIP-3b receptor CCR7. J. Cell Biol. 141: 1053-1059.
19. Idoyaga, J., C. Fiorese, L. Zbytnuik, A. Lubkin, J. Miller, B. Malissen, D. Mucida, M. Merad, and R. M. Steinman. 2013. Specialized role of migratory dendritic cells in peripheral tolerance induction. J. Clin. Invest. 123: 844-854.
20. Azukizawa, H., A. Döhler, N. Kanazawa, A. Nayak, M. Lipp, B. Malissen, I. Autenrieth, I. Katayama, M. Riemann, F. Weih, et al. 2011. Steady state migratory RelB+ langerin+ dermal dendritic cells mediate peripheral induction of antigenspecific CD4+CD25+Foxp3+ regulatory T cells. Eur. J. Immunol. 41: 1420-1434.
21. Guilliams, M., K. Crozat, S. Henri, S. Tamoutounour, P. Grenot, E. Devilard, B. de Bovis, L. Alexopoulou, M. Dalod, and B. Malissen. 2010. Skin-draining lymph nodes contain dermis-derived CD1032 dendritic cells that constitutively produce retinoic acid and induce Foxp3+ regulatory T cells. Blood 115: 1958-1968.
22. Baratin, M., C. Foray, O. Demaria, M. Habbeddine, E. Pollet, J. Maurizio, C. Verthuy, S. Davanture, H. Azukizawa, A. Flores-Langarica, et al. 2015. Homeostatic NF-kB signaling in steady-state migratory dendritic cells regulates immune homeostasis and tolerance. Immunity 42: 627-639.
23. Bajanã, S., K. Roach, S. Turner, J. Paul, and S. Kovats. 2012. IRF4 promotes cutaneous dendritic cell migration to lymph nodes during homeostasis and inflammation. J. Immunol. 189: 3368-3377.
24. Suzuki, S., K. Honma, T. Matsuyama, K. Suzuki, K. Toriyama, I. Akitoyo, K. Yamamoto, T. Suematsu, M. Nakamura, K. Yui, and A. Kumatori. 2004. Critical roles of interferon regulatory factor 4 in CD11bhighCD8a2 dendritic cell development. Proc. Natl. Acad. Sci. USA 101: 8981-8986.
25. Vander Lugt, B., A. A. Khan, J. A. Hackney, S. Agrawal, J. Lesch, M. Zhou, W. P. Lee, S. Park, M. Xu, J. DeVoss, et al. 2014. Transcriptional programming of dendritic cells for enhanced MHC class II antigen presentation. Nat. Immunol. 15: 161-167.
26. Schlitzer, A., N. McGovern, P. Teo, T. Zelante, K. Atarashi, D. Low, A. W. S. Ho, P. See, A. Shin, P. S. Wasan, et al. 2013. IRF4 transcription factordependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38: 970-983.
27. Haniffa, M., A. Shin, V. Bigley, N. McGovern, P. Teo, P. See, P. S. Wasan, X. N. Wang, F. Malinarich, B. Malleret, et al. 2012. Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103+ nonlymphoid dendritic cells. Immunity 37: 60-73.
28. Kim, D., G. Pertea, C. Trapnell, H. Pimentel, R. Kelley, and S. L. Salzberg. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14: R36.
29. Anders, S., P. T. Pyl, and W. Huber. 2015. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31: 166-169.
30. Harrow, J., A. Frankish, J. M. Gonzalez, E. Tapanari, M. Diekhans, F. Kokocinski, B. L. Aken, D. Barrell, A. Zadissa, S. Searle, et al. 2012. GENCODE: the reference human genome annotation for the ENCODE Project. Genome Res. 22: 1760-1774.
31. Robinson, M. D., D. J. McCarthy, and G. K. Smyth. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
32. Wu, D., E. Lim, F. Vaillant, M. L. Asselin-Labat, J. E. Visvader, and G. K. Smyth. 2010. ROAST: rotation gene set tests for complex microarray experiments. Bioinformatics 26: 2176-2182.
33. Lau, C. M., S. A. Nish, N. Yogev, A.Waisman, S. L. Reiner, and B. Reizis. 2016. Leukemia-associated activating mutation of Flt3 expands dendritic cells and alters T cell responses. J. Exp. Med. 213: 415-431.
34. Huang da, W., B. T. Sherman, and R. A. Lempicki. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4: 44-57.
35. Huang da, W., B. T. Sherman, and R. A. Lempicki. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37: 1-13.
36. O'Doherty, U., M. Peng, S. Gezelter, W. J. Swiggard, M. Betjes, N. Bhardwaj, and R. M. Steinman. 1994. Human blood contains two subsets of dendritic cells, one immunologically mature and the other immature. Immunology 82: 487-493.
37. Wood, G. S., and P. S. Freudenthal. 1992. CD5 monoclonal antibodies react with human peripheral blood dendritic cells. Am. J. Pathol. 141: 789-795.
38. Liu, Y. J. 2005. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 23: 275-306.
39. Kadowaki, N., S. Ho, S. Antonenko, R. W. Malefyt, R. A. Kastelein, F. Bazan, and Y. J. Liu. 2001. Subsets of human dendritic cell precursors express different Toll-like receptors and respond to different microbial antigens. J. Exp. Med. 194: 863-869.
40. Persson, E. K., H. Uronen-Hansson, M. Semmrich, A. Rivollier, K. Hägerbrand, J. Marsal, S. Gudjonsson, U. Håkansson, B. Reizis, K. Kotarsky, and W. W. Agace. 2013. IRF4 transcription-factor-dependent CD103+CD11b+ dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 38: 958-969.
41. Sarrazin, S., N. Mossadegh-Keller, T. Fukao, A. Aziz, F. Mourcin, L. Vanhille, L. Kelly Modis, P. Kastner, S. Chan, E. Duprez, et al. 2009. MafB restricts M-CSF-dependent myeloid commitment divisions of hematopoietic stem cells. Cell 138: 300-313.
42. Kelly, L. M., U. Englmeier, I. Lafon, M. H. Sieweke, and T. Graf. 2000. MafB is an inducer of monocytic differentiation. EMBO J. 19: 1987-1997.
43. Bakri, Y., S. Sarrazin, U. P. Mayer, S. Tillmanns, C. Nerlov, A. Boned, and M. H. Sieweke. 2005. Balance of MafB and PU.1 specifies alternative macrophage or dendritic cell fate. Blood 105: 2707-2716.
44. Buechler, C., M. Ritter, E. Orsó, T. Langmann, J. Klucken, and G. Schmitz. 2000. Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro-and antiinflammatory stimuli. J. Leukoc. Biol. 67: 97-103.
45. Frederiksen, P. D., S. Thiel, C. B. Larsen, and J. C. Jensenius. 2005. M-ficolin, an innate immune defence molecule, binds patterns of acetyl groups and activates complement. Scand. J. Immunol. 62: 462-473.
46. Vogl, T., K. Tenbrock, S. Ludwig, N. Leukert, C. Ehrhardt, M. A. D. van Zoelen, W. Nacken, D. Foell, T. van der Poll, C. Sorg, and J. Roth. 2007. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat. Med. 13: 1042-1049.
47. Vu Manh, T. P., J. Elhmouzi-Younes, C. Urien, S. Ruscanu, L. Jouneau, M. Bourge, M. Moroldo, G. Foucras, H. Salmon, H. Marty, et al. 2015. Defining mononuclear phagocyte subset homology across several distant warm-blooded vertebrates through comparative transcriptomics. [Published erratum appears in 2016 Front. Immunol. 7: 143.] Front. Immunol. 6: 299.
48. Balan, S., V. Ollion, N. Colletti, R. Chelbi, F. Montanana-Sanchis, H. Liu, T. P. Vu Manh, C. Sanchez, J. Savoret, I. Perrot, et al. 2014. Human XCR1+ dendritic cells derived in vitro from CD34+ progenitors closely resemble blood dendritic cells, including their adjuvant responsiveness, contrary to monocytederived dendritic cells. J. Immunol. 193: 1622-1635.
49. Bouchon, A., J. Dietrich, and M. Colonna. 2000. Cutting edge: inflammatory responses can be triggered by TREM-1, a novel receptor expressed on neutrophils and monocytes. J. Immunol. 164: 4991-4995.
50. Dieu, M. C., B. Vanbervliet, A. Vicari, J. M. Bridon, E. Oldham, S. A?t-Yahia, F. Brière, A. Zlotnik, S. Lebecque, and C. Caux. 1998. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J. Exp. Med. 188: 373-386.
51. Yanagihara, S., E. Komura, J. Nagafune, H. Watarai, and Y. Yamaguchi. 1998. EBI1/CCR7 is a new member of dendritic cell chemokine receptor that is upregulated upon maturation. J. Immunol. 161: 3096-3102.
52. Teijeira, A., E. Russo, and C. Halin. 2014. Taking the lymphatic route: dendritic cell migration to draining lymph nodes. Semin. Immunopathol. 36: 261-274.
53. de Saint-Vis, B., J. Vincent, S. Vandenabeele, B. Vanbervliet, J. J. Pin, S. A?t-Yahia, S. Patel, M. G. Mattei, J. Banchereau, S. Zurawski, et al. 1998. A novel lysosome-associated membrane glycoprotein, DC-LAMP, induced upon DC maturation, is transiently expressed in MHC class II compartment. Immunity 9: 325-336.
54. Vremec, D., M. O'Keeffe, A. Wilson, I. Ferrero, U. Koch, F. Radtke, B. Scott, P. Hertzog, J. Villadangos, and K. Shortman. 2011. Factors determining the spontaneous activation of splenic dendritic cells in culture. Innate Immun. 17: 338-352.
55. Ochiai, K., M. Maienschein-Cline, G. Simonetti, J. Chen, R. Rosenthal, R. Brink, A. S. Chong, U. Klein, A. R. Dinner, H. Singh, and R. Sciammas. 2013. Transcriptional regulation of germinal center B and plasma cell fates by dynamical control of IRF4. Immunity 38: 918-929.
56. Sciammas, R., A. L. Shaffer, J. H. Schatz, H. Zhao, L. M. Staudt, and H. Singh. 2006. Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity 25: 225-236.
57. Negishi, H., Y. Ohba, H. Yanai, A. Takaoka, K. Honma, K. Yui, T. Matsuyama, T. Taniguchi, and K. Honda. 2005. Negative regulation of Toll-like-receptor signaling by IRF-4. Proc. Natl. Acad. Sci. USA 102: 15989-15994.
58. Schoenemeyer, A., B. J. Barnes, M. E. Mancl, E. Latz, N. Goutagny, P. M. Pitha, K. A. Fitzgerald, and D. T. Golenbock. 2005. The interferon regulatory factor, IRF5, is a central mediator of Toll-like receptor 7 signaling. J. Biol. Chem. 280: 17005-17012.
59. Akbari, M., K. Honma, D. Kimura, M. Miyakoda, K. Kimura, T. Matsuyama, and K. Yui. 2014. IRF4 in dendritic cells inhibits IL-12 production and controls Th1 immune responses against Leishmania major. J. Immunol. 192: 2271-2279.
60. Lutz, M. B., and G. Schuler. 2002. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol. 23: 445-449.
61. Kassianos, A. J.,M. Y.Hardy, X. Ju, D. Vijayan, Y. Ding, A. J. Vulink, K. J.McDonald, S. L. Jongbloed, R. B.Wadley, C.Wells, et al. 2012. Human CD1c (BDCA-1)+ myeloid dendritic cells secrete IL-10 and display an immuno-regulatory phenotype and function in response to Escherichia coli. Eur. J. Immunol. 42: 1512-1522.
62. Prue, R. L., F. Vari, K. J. Radford, H. Tong, M. Y. Hardy, R. D'Rozario, N. J. Waterhouse, T. Rossetti, R. Coleman, C. Tracey, et al. 2015. A phase I clinical trial of CD1c (BDCA-1)+ dendritic cells pulsed with HLA-A0201 peptides for immunotherapy of metastatic hormone refractory prostate cancer. J. Immunother. 38: 71-76.
63. Schreibelt, G., K. F. Bol, H.Westdorp, F.Wimmers, E. H. Aarntzen, T. Duiveman-de Boer, M. W. van de Rakt, N. M. Scharenborg, A. J. de Boer, J. M. Pots, et al. 2016. Effective clinical responses in metastatic melanoma patients after vaccination with primary myeloid dendritic cells. Clin. Cancer Res. 22: 2155-2166.