Human dendritic cell subsets: an update

Immunology

Volumn 154, Issue 1, 2018, Pages 3-20

  Collin, Matthew ^a   Bigley, Venetia ^a  

^a NEWCASTLE UPON TYNE HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

antigen presentation processing; dendritic cell; transcriptomics

Indexed keywords

INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERFERON REGULATORY FACTOR 4; NOTCH2 RECEPTOR; SINAPULTIDE; BIOLOGICAL MARKER;

CD16+ NON CLASSICAL MONOCYTE; CELL MATURATION; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CLASSIFICATION; CROSS PRESENTATION; DENDRITIC CELL; FLOW CYTOMETRY; HEMATOPOIESIS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNITY; LANGERHANS CELL; MACROPHAGE; MAMMAL CELL; MONOCYTE; MONOCYTE DERIVED INFLAMMATORY DENDRITIC CELL; PHENOTYPE; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; REVIEW; CELL COMMUNICATION; CELL DIFFERENTIATION; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; SIGNAL TRANSDUCTION;

BIOMARKERS; CELL COMMUNICATION; CELL DIFFERENTIATION; DENDRITIC CELLS; HUMANS; IMMUNITY; IMMUNOPHENOTYPING; PHENOTYPE; SIGNAL TRANSDUCTION;

EID: 85042530066     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12888     Document Type: Review

References (202)

1. Guilliams M, Ginhoux F, Jakubzick C, Naik SH, Donna N, Schraml BU et al. Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat Rev Immunol 2014; 14:571–8.
2. Guilliams M, Dutertre CA, Scott CL, McGovern N, Sichien D, Chakarov S et al. Unsupervised high-dimensional analysis aligns dendritic cells across tissues and species. Immunity 2016; 45:669–84.
3. Heidkamp GF, Sander J, Lehmann CHK, Heger L, Eissing N, Baranska A et al. Human lymphoid organ dendritic cell identity is predominantly dictated by ontogeny, not tissue microenvironment. Sci Immunol 2016; 1:eaai7677.
4. Granot T, Senda T, Carpenter DJ, Matsuoka N, Weiner J, Gordon CL et al. Dendritic cells display subset and tissue-specific maturation dynamics over human life. Immunity 2017; 46:504–15.
5. Dzionek A, Fuchs A, Schmidt P, Cremer S, Zysk M, Miltenyi S et al. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol 2000; 165:6037–46.
6. MacDonald KP, Munster DJ, Clark GJ, Dzionek A, Schmitz J, Hart DN. Characterization of human blood dendritic cell subsets. Blood 2002; 100:4512–20.
7. Ziegler-Heitbrock L, Ancuta P, Crowe S, Dalod M, Grau V, Hart DN et al. Nomenclature of monocytes and dendritic cells in blood. Blood 2010; 116:e74–80.
8. Yin X, Yu H, Jin X, Li J, Guo H, Shi Q et al. Human blood CD1c+ dendritic cells encompass CD5high and CD5low subsets that differ significantly in phenotype, gene expression, and functions. J Immunol 2017; 198:1553–64.
9. Villani AC, Satija R, Reynolds G, Sarkizova S, Shekhar K, Fletcher J et al. Single-cell RNA-seq reveals new types of human blood dendritic cells, monocytes, and progenitors. Science 2017; 356:eaah4573.
10. See P, Dutertre CA, Chen J, Günther P, McGovern N, Irac SE et al. Mapping the human DC lineage through the integration of high-dimensional techniques. Science 2017; 356:eaag3009.
11. Haniffa M, Ginhoux F, Wang XN, Bigley V, Abel M, Dimmick I et al. Differential rates of replacement of human dermal dendritic cells and macrophages during hematopoietic stem cell transplantation. J Exp Med 2009; 206:371–85.
12. Haniffa M, Shin A, Bigley V, McGovern N, Teo P, See P et al. Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103+ nonlymphoid dendritic cells. Immunity 2012; 37:60–73.
13. McGovern N, Schlitzer A, Gunawan M, Jardine L, Shin A, Poyner E et al. Human dermal CD14⁺ cells are a transient population of monocyte-derived macrophages. Immunity 2014; 41:465–77.
14. Desch AN, Gibbings SL, Goyal R, Kolde R, Bednarek J, Bruno T et al. Flow cytometric analysis of mononuclear phagocytes in non-diseased human lung and lung-draining lymph nodes. Am J Respir Crit Care Med 2016; 193:614–26.
15. Baharom F, Thomas S, Rankin G, Lepzien R, Pourazar J, Behndig AF et al. Dendritic cells and monocytes with distinct inflammatory responses reside in lung mucosa of healthy humans. J Immunol 2016; 196:4498–509.
16. Patel VI, Booth JL, Duggan ES, Cate S, White VL, Hutchings D et al. Transcriptional classification and functional characterization of human airway macrophage and dendritic cell subsets. J Immunol 2017; 198:1183–201.
17. Watchmaker PB, Lahl K, Lee M, Baumjohann D, Morton J, Kim SJ et al. Comparative transcriptional and functional profiling defines conserved programs of intestinal DC differentiation in humans and mice. Nat Immunol 2014; 15:98–108.
18. Yoshio S, Kanto T, Kuroda S, Matsubara T, Higashitani K, Kakita N et al. Human blood dendritic cell antigen 3 (BDCA3)(+) dendritic cells are a potent producer of interferon-λ in response to hepatitis C virus. Hepatology 2013; 57:1705–15.
19. Kelly A, Fahey R, Fletcher JM, Keogh C, Carroll AG, Siddachari R et al. CD141⁺ myeloid dendritic cells are enriched in healthy human liver. J Hepatol 2014; 60:135–42.
20. Mittag D, Proietto AI, Loudovaris T, Mannering SI, Vremec D, Shortman K et al. Human dendritic cell subsets from spleen and blood are similar in phenotype and function but modified by donor health status. J Immunol 2011; 186:6207–17.
21. Segura E, Durand M, Amigorena S. Similar antigen cross-presentation capacity and phagocytic functions in all freshly isolated human lymphoid organ-resident dendritic cells. J Exp Med 2013; 210:1035–47.
22. De Monte A, Olivieri CV, Vitale S, Bailleux S, Castillo L, Giordanengo V et al. CD1c-related DCs that express CD207/langerin, but are distinguishable from Langerhans cells, are consistently present in human tonsils. Front Immunol 2016; 7:197.
23. McGovern N, Shin A, Low G, Duan K, Yao LJ et al. Human fetal dendritic cells promote prenatal T-cell immune suppression through arginase-2. Nature 2017; 546:662–6.
24. Segura E, Touzot M, Bohineust A, Cappuccio A, Chiocchia G, Hosmalin A et al. Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity 2013; 38:336–48.
25. Autenrieth SE, Grimm S, Rittig SM, Grünebach F, Gouttefangeas C, Bühring HJ. Profiling of primary peripheral blood- and monocyte-derived dendritic cells using monoclonal antibodies from the HLDA10 Workshop in Wollongong, Australia. Clin Transl Immunol 2015; 4:e50.
26. Fromm PD, Kupresanin F, Brooks AE, Dunbar PR, Haniffa M, Hart DN et al. A multi-laboratory comparison of blood dendritic cell populations. Clin Transl Immunol 2016; 5:e68.
27. Saeys Y, Gassen SV, Lambrecht BN. Computational flow cytometry: helping to make sense of high-dimensional immunology data. Nat Rev Immunol 2016; 16:449–62.
28. Stoeckius M, Hafemeister C, Stephenson W, Houck-Loomis B, Chattopadhyay PK, Swerdlow H et al. Simultaneous epitope and transcriptome measurement in single cells. Nat Methods 2017; 14:865–8.
29. Poulin LF, Salio M, Griessinger E, Anjos-Afonso F, Craciun L, Chen JL et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J Exp Med 2010; 207:1261–71.
30. + progenitors closely resemble blood dendritic cells, including their adjuvant responsiveness, contrary to monocyte-derived dendritic cells. J Immunol 2014; 193:1622–35.
31. Helft J, Anjos-Afonso F, van der Veen AG, Chakravarty P, Bonnet D, Reis E et al. Dendritic cell lineage potential in human early hematopoietic progenitors. Cell Rep 2017; 20:529–37.
32. Lee J, Zhou YJ, Ma W, Zhang W, Aljoufi A, Luh T et al. Lineage specification of human dendritic cells is marked by IRF8 expression in hematopoietic stem cells and multipotent progenitors. Nat Immunol 2017; 18:877–88.
33. Paul F, Arkin Y, Giladi A, Jaitin DA, Kenigsberg E, Keren-Shaul H et al. Transcriptional heterogeneity and lineage commitment in myeloid progenitors. Cell 2015; 163:1663–77.
34. Notta F, Zandi S, Takayama N, Dobson S, Gan OI, Wilson G et al. Distinct routes of lineage development reshape the human blood hierarchy across ontogeny. Science 2016; 351:aab2116.
35. Velten L, Haas SF, Raffel S, Blaszkiewicz S, Islam S, Hennig BP et al. Human haematopoietic stem cell lineage commitment is a continuous process. Nat Cell Biol 2017; 19:271–81.
36. Karamitros D, Stoilova B, Aboukhalil Z, Hamey F, Reinisch A, Samitsch M et al. Single-cell analysis reveals the continuum of human lympho-myeloid progenitor cells. Nat Immunol 2017; 19:85–97.
37. Kawamoto H, Ikawa T, Masuda K, Wada H, Katsura Y. A map for lineage restriction of progenitors during hematopoiesis: the essence of the myeloid-based model. Immunol Rev 2010; 238:23–36.
38. Pelayo R, Hirose J, Huang J, Garrett KP, Delogu A, Busslinger M et al. Derivation of 2 categories of plasmacytoid dendritic cells in murine bone marrow. Blood 2005; 105:4407–15.
39. Corcoran L, Ferrero I, Vremec D, Lucas K, Waithman J, O'Keeffe M et al. The lymphoid past of mouse plasmacytoid cells and thymic dendritic cells. J Immunol 2003; 170:4926–32.
40. + DCs. J Exp Med 2016; 213:2861–70.
41. Grouard G, Rissoan MC, Filgueira L, Durand I, Banchereau J, Liu YJ. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J Exp Med 1997; 185:1101–11.
42. Matsui T, Connolly JE, Michnevitz M, Chaussabel D, Yu CI, Glaser C et al. CD2 distinguishes two subsets of human plasmacytoid dendritic cells with distinct phenotype and functions. J Immunol 2009; 182:6815–23.
43. Bryant C, Fromm PD, Kupresanin F, Clark G, Lee K, Clarke C et al. A CD2 high-expressing stress-resistant human plasmacytoid dendritic-cell subset. Immunol Cell Biol 2016; 94:447–57.
44. + dendritic-like cells: a normal counterpart of blastic plasmacytoid dendritic cell neoplasm. PLoS ONE 2013; 8:e81722.
45. + dendritic cells (DCs) related to blastic plasmacytoid dendritic cell neoplasm represent a unique myeloid DC subset. Protein Cell 2015; 6:297–306.
46. Zhang H, Gregorio JD, Iwahori T, Zhang X, Choi O, Tolentino LL et al. A distinct subset of plasmacytoid dendritic cells induces activation and differentiation of B and T lymphocytes. Proc Natl Acad Sci U S A 2017; 114:1988–93.
47. Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H, Lanzavecchia A et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 1999; 5:919–23.
48. Siegal FP, Kadowaki N, Shodell M, Fitzgerald-Bocarsly PA, Shah K, Ho S et al. The nature of the principal type 1 interferon-producing cells in human blood. Science 1999; 284:1835–7.
49. Dzionek A, Sohma Y, Nagafune J, Cella M, Colonna M, Facchetti F et al. BDCA-2, a novel plasmacytoid dendritic cell-specific type II C-type lectin, mediates antigen capture and is a potent inhibitor of interferon α/β induction. J Exp Med 2001; 194:1823–34.
50. Jardine L, Barge D, Ames-Draycott A, Pagan S, Cookson S, Spickett G et al. Rapid detection of dendritic cell and monocyte disorders using CD4 as a lineage marker of the human peripheral blood antigen-presenting cell compartment. Front Immunol 2013; 4:495.
51. Ju X, Zenke M, Hart DN, Clark GJ. CD300a/c regulate type I interferon and TNF-alpha secretion by human plasmacytoid dendritic cells stimulated with TLR7 and TLR9 ligands. Blood 2008; 112:1184–94.
52. Bao M, Liu YJ. Regulation of TLR7/9 signaling in plasmacytoid dendritic cells. Protein Cell 2013; 4:40–52.
53. Collin M, Dickinson R, Bigley V. Haematopoietic and immune defects associated with GATA2 mutation. Br J Haematol 2015; 169:173–87.
54. Onodera K, Fujiwara T, Onishi Y, Itoh-Nakadai A, Okitsu Y, Fukuhara N et al. GATA2 regulates dendritic cell differentiation. Blood 2016; 128:508–18.
55. Carotta S, Dakic A, D'Amico A, Pang SH, Greig KT, Nutt SL et al. The transcription factor PU.1 controls dendritic cell development and Flt3 cytokine receptor expression in a dose-dependent manner. Immunity 2010; 32:628–41.
56. Rathinam C, Geffers R, Yucel R, Buer J, Welte K, Moroy T et al. The transcriptional repressor Gfi1 controls STAT3-dependent dendritic cell development and function. Immunity 2005; 22:717–28.
57. Allman D, Dalod M, Asselin-Paturel C, Delale T, Robbins SH, Trinchieri G et al. Ikaros is required for plasmacytoid dendritic cell differentiation. Blood 2006; 108:4025–34.
58. Tussiwand R, Gautier EL. Transcriptional regulation of mononuclear phagocyte development. Front Immunol 2015; 6:533.
59. Swiecki M, Colonna M. The multifaceted biology of plasmacytoid dendritic cells. Nat Rev Immunol 2015; 15:471–85.
60. Murphy TL, Grajales-Reyes GE, Wu X, Tussiwand R, Briseño CG, Iwata A et al. Transcriptional control of dendritic cell development. Annu Rev Immunol 2016; 34:93–119.
61. Hambleton S, Salem S, Bustamante J, Bigley V, Boisson-Dupuis S, Azevedo J et al. IRF8 mutations and human dendritic-cell immunodeficiency. N Engl J Med 2011; 365:127–38.
62. Bigley V, Maisuria S, Cytlak U, Jardine L, Care MA, Green K et al. Biallelic interferon regulatory factor 8 mutation: a complex immunodeficiency syndrome with dendritic cell deficiency, monocytopenia, and immune dysregulation. J Allergy Clin Immunol 2017; doi: 10.1016/j.jaci.2017.08.044
63. Cytlak U, Resteu AB. D, Kuehn HS, Altmann TG, A. Ikaros family zinc finger 1 regulates dendritic cell development and function in humans. Nature. Communications 2018; In press.
64. Spits H, Couwenberg F, Bakker AQ, Weijer K, Uittenbogaart CH. Id2 and Id3 inhibit development of CD34(+) stem cells into predendritic cell (pre-DC)2 but not into pre-DC1. Evidence for a lymphoid origin of pre-DC2. J Exp Med 2000; 192:1775–84.
65. Ghosh HS, Ceribelli M, Matos I, Lazarovici A, Bussemaker HJ, Lasorella A et al. ETO family protein Mtg16 regulates the balance of dendritic cell subsets by repressing Id2. J Exp Med 2014; 211:1623–35.
66. Scott CL, Soen B, Martens L, Skrypek N, Saelens W, Taminau J et al. The transcription factor Zeb2 regulates development of conventional and plasmacytoid DCs by repressing Id2. J Exp Med 2016; 213:897–911.
67. Wu X, Briseño CG, Grajales-Reyes GE, Haldar M, Iwata A, Kretzer NM et al. Transcription factor Zeb2 regulates commitment to plasmacytoid dendritic cell and monocyte fate. Proc Natl Acad Sci U S A 2016; 113:14775–80.
68. Kashiwada M, Pham NL, Pewe LL, Harty JT, Rothman PB. NFIL3/E4BP4 is a key transcription factor for CD8alpha dendritic cell development. Blood 2011; 117:6193–7.
69. Bode C, Fox M, Tewary P, Steinhagen A, Ellerkmann RK, Klinman D et al. Human plasmacytoid dentritic cells elicit a Type I Interferon response by sensing DNA via the cGAS-STING signaling pathway. Eur J Immunol 2016; 46:1615–21.
70. Bruni D, Chazal M, Sinigaglia L, Chauveau L, Schwartz O, Després P et al. Viral entry route determines how human plasmacytoid dendritic cells produce type I interferons. Sci Signal 2015; 8:ra25.
71. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, Mizutani T et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005; 434:772–7.
72. Li J, Du Q, Hu R, Wang Y, Yin X, Yu H et al. Death receptor 6 is a novel plasmacytoid dendritic cell-specific receptor and modulates type I interferon production. Protein Cell 2016; 7:291–4.
73. Dillmann C, Ringel C, Ringleb J, Mora J, Olesch C, Fink AF et al. S1PR4 signaling attenuates ILT 7 internalization to limit IFN-α production by human plasmacytoid dendritic cells. J Immunol 2016; 196:1579–90.
74. Teijaro JR, Studer S, Leaf N, Kiosses WB, Nguyen N, Matsuki K et al. S1PR1-mediated IFNAR1 degradation modulates plasmacytoid dendritic cell interferon-α autoamplification. Proc Natl Acad Sci USA 2016; 113:1351–6.
75. Ciancanelli MJ, Huang SX, Luthra P, Garner H, Itan Y, Volpi S et al. Infectious disease. Life-threatening influenza and impaired interferon amplification in human IRF7 deficiency. Science 2015; 348:448–53.
76. Keles S, Jabara HH, Reisli I, McDonald DR, Barlan I, Hanna-Wakim R et al. Plasmacytoid dendritic cell depletion in DOCK8 deficiency: rescue of severe herpetic infections with IFN-α 2b therapy. J Allergy Clin Immunol 2014; 133:1753–5.e3.
77. Li H, Goepfert P, Reeves RK. Short communication: plasmacytoid dendritic cells from HIV-1 elite controllers maintain a gut-homing phenotype associated with immune activation. AIDS Res Hum Retroviruses 2014; 30:1213–5.
78. Yonkers NL, Rodriguez B, Milkovich KA, Asaad R, Lederman MM, Heeger PS et al. TLR ligand-dependent activation of naive CD4 T cells by plasmacytoid dendritic cells is impaired in hepatitis C virus infection. J Immunol 2007; 178:4436–44.
79. Woltman AM, Op den Brouw ML, Biesta PJ, Shi CC, Janssen HL. Hepatitis B virus lacks immune activating capacity, but actively inhibits plasmacytoid dendritic cell function. PLoS ONE 2011; 6:e15324.
80. Lande R, Ganguly D, Facchinetti V, Frasca L, Conrad C, Gregorio J et al. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci Transl Med 2011; 3:73ra19.
81. Ganguly D, Chamilos G, Lande R, Gregorio J, Meller S, Facchinetti V et al. Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J Exp Med 2009; 206:1983–94.
82. Berggren O, Alexsson A, Morris DL, Tandre K, Weber G, Vyse TJ et al. IFN-α production by plasmacytoid dendritic cell associations with polymorphisms in gene loci related to autoimmune and inflammatory diseases. Hum Mol Genet 2015; 24:3571–81.
83. Meyer-Wentrup F, Benitez-Ribas D, Tacken PJ, Punt CJ, Figdor CG, de Vries IJ et al. Targeting DCIR on human plasmacytoid dendritic cells results in antigen presentation and inhibits IFN-α production. Blood 2008; 111:4245–53.
84. + T cells by targeting antigens to human dendritic cells through DCIR. Blood 2010; 116:1685–97.
85. Tel J, Sittig SP, Blom RA, Cruz LJ, Schreibelt G, Figdor CG et al. Targeting uptake receptors on human plasmacytoid dendritic cells triggers antigen cross-presentation and robust type I IFN secretion. J Immunol 2013; 191:5005–12.
86. + T cells despite lower Ag uptake than myeloid dendritic cell subsets. Blood 2013; 121:459–67.
87. Froidure A, Vandenplas O, D'Alpaos V, Evrard G, Pilette C. Defects in plasmacytoid dendritic cell expression of inducible costimulator ligand and IFN-α are associated in asthma with disease persistence. Am J Respir Crit Care Med 2015; 192:392–5.
88. Pritchard AL, Carroll ML, Burel JG, White OJ, Phipps S, Upham JW. Innate IFNs and plasmacytoid dendritic cells constrain Th2 cytokine responses to rhinovirus: a regulatory mechanism with relevance to asthma. J Immunol 2012; 188:5898–905.
89. Ghirelli C, Reyal F, Jeanmougin M, Zollinger R, Sirven P, Michea P et al. Breast cancer cell-derived GM-CSF licenses regulatory Th2 induction by plasmacytoid predendritic cells in aggressive disease subtypes. Cancer Res 2015; 75:2775–87.
90. + dendritic cells in human skin produce IL-10 and induce regulatory T cells that suppress skin inflammation. J Exp Med 2012; 209:935–45.
91. Ahrens S, Zelenay S, Sancho D, Hanc P, Kjaer S, Feest C et al. F-actin is an evolutionarily conserved damage-associated molecular pattern recognized by DNGR-1, a receptor for dead cells. Immunity 2012; 36:635–45.
92. Zhang JG, Czabotar PE, Policheni AN, Caminschi I, Wan SS, Kitsoulis S et al. The dendritic cell receptor Clec9A binds damaged cells via exposed actin filaments. Immunity 2012; 36:646–57.
93. Crozat K, Guiton R, Contreras V, Feuillet V, Dutertre CA, Ventre E et al. The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8alpha+ dendritic cells. J Exp Med 2010; 207:1283–92.
94. + dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 2010; 207:1247–60.
95. Segura E, Valladeau-Guilemond J, Donnadieu MH, Sastre-Garau X, Soumelis V, Amigorena S. Characterization of resident and migratory dendritic cells in human lymph nodes. J Exp Med 2012; 209:653–60.
96. Hacker C, Kirsch RD, Ju XS, Hieronymus T, Gust TC, Kuhl C et al. Transcriptional profiling identifies Id2 function in dendritic cell development. Nat Immunol 2003; 4:380–6.
97. Tsujimura H, Tamura T, Ozato K. Cutting edge: IFN consensus sequence binding protein/IFN regulatory factor 8 drives the development of type I IFN-producing plasmacytoid dendritic cells. J Immunol 2003; 170:1131–5.
98. + conventional DC clonogenic progenitor. Nat Immunol 2015; 16:708–17.
99. Tamura T, Kurotaki D, Koizumi SI. Regulation of myelopoiesis by the transcription factor IRF8. Int J Hematol 2015; 101:342–51.
100. Sichien D, Scott CL, Martens L, Vanderkerken M, Van Gassen S, Plantinga M et al. IRF8 transcription factor controls survival and function of terminally differentiated conventional and plasmacytoid dendritic cells, respectively. Immunity 2016; 45:626–40.
101. Tailor P, Tamura T, Morse HC, Ozato K. The BXH2 mutation in IRF8 differentially impairs dendritic cell subset development in the mouse. Blood 2008; 111:1942–5.
102. Mace EM, Bigley V, Gunesch JT, Chinn IK, Angelo LS, Care MA et al. Biallelic mutations in IRF8 impair human NK cell maturation and function. J Clin Invest 2017; 127:306–20.
103. Cohen SB, Smith NL, McDougal C, Pepper M, Shah S, Yap GS et al. β-catenin signaling drives differentiation and proinflammatory function of IRF8-dependent dendritic cells. J Immunol 2015; 194:210–22.
104. Poulin LF, Reyal Y, Uronen-Hansson H, Schraml BU, Sancho D, Murphy KM et al. DNGR-1 is a specific and universal marker of mouse and human Batf3-dependent dendritic cells in lymphoid and nonlymphoid tissues. Blood 2012; 119:6052–62.
105. Tussiwand R, Lee WL, Murphy TL, Mashayekhi M, Wumesh KC, Albring JC et al. Compensatory dendritic cell development mediated by BATF-IRF interactions. Nature 2012; 490:502–7.
106. + dendritic cells. J Exp Med 2010; 207:1273–81.
107. + dendritic cells secrete high levels of IL-12 and potently prime cytotoxic T-cell responses. Blood 2013; 122:932–42.
108. + dendritic cells at cross presentation. J Exp Med 2013; 210:1049–63.
109. Sittig SP, Bakdash G, Weiden J, Sköld AE, Tel J, Figdor CG et al. A comparative study of the T cell stimulatory and polarizing capacity of human primary blood dendritic cell subsets. Mediators Inflamm 2016; 2016:3605643.
110. Dalod M, Chelbi R, Malissen B, Lawrence T. Dendritic cell maturation: functional specialization through signaling specificity and transcriptional programming. EMBO J 2014; 33:1104–16.
111. + DCs in mouse and human and distinguishes them from Langerhans cells. J Immunol Methods 2016; 432:35–49.
112. Geginat J, Nizzoli G, Paroni M, Maglie S, Larghi P, Pascolo S et al. Immunity to pathogens taught by specialized human dendritic cell subsets. Front Immunol 2015; 6:527.
113. + dendritic cells. Sci Immunol 2017; 2:eaai8071.
114. + myeloid dendritic cells. Blood 2012; 119:2284–92.
115. Li J, Ahmet F, Sullivan LC, Brooks AG, Kent SJ, De Rose R et al. Antibodies targeting Clec9A promote strong humoral immunity without adjuvant in mice and non-human primates. Eur J Immunol 2015; 45:854–64.
116. Hemont C, Neel A, Heslan M, Braudeau C, Josien R. Human blood mDC subsets exhibit distinct TLR repertoire and responsiveness. J Leukoc Biol 2013; 93:599–609.
117. Colletti NJ, Liu H, Gower AC, Alekseyev YO, Arendt CW, Shaw MH. TLR3 signaling promotes the induction of unique human BDCA-3 dendritic cell populations. Front Immunol 2016; 7:88.
118. Liu S, Cai X, Wu J, Cong Q, Chen X, Li T et al. Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science 2015; 347:aaa2630.
119. Lafaille FG, Pessach IM, Zhang SY, Ciancanelli MJ, Herman M, Abhyankar A et al. Impaired intrinsic immunity to HSV-1 in human iPSC-derived TLR3-deficient CNS cells. Nature 2012; 491:769–73.
120. + DCs are major producers of IFN-λ in response to poly IC. J Exp Med 2010; 207:2703–17.
121. + dendritic cell spatial and functional cooperativity to optimize priming. Immunity 2017; 46:205–19.
122. Ohta T, Sugiyama M, Hemmi H, Yamazaki C, Okura S, Sasaki I et al. Crucial roles of XCR1-expressing dendritic cells and the XCR1-XCL1 chemokine axis in intestinal immune homeostasis. Sci Rep 2016; 6:23505.
123. + T cell recall upon secondary infections with Listeria monocytogenes or certain viruses. J Exp Med 2016; 213:75–92.
124. + regulatory T cells. Blood 2010; 115:1958–68.
125. Idoyaga J, Fiorese C, Zbytnuik L, Lubkin A, Miller J, Malissen B et al. Specialized role of migratory dendritic cells in peripheral tolerance induction. J Clin Invest 2013; 123:844–54.
126. Jiang S, Li X, Hess NJ, Guan Y, Tapping RI. TLR10 is a negative regulator of both MyD88-dependent and -independent TLR signaling. J Immunol 2016; 196:3834–41.
127. Li YH, Kuo CH, Shi GY, Wu HL. The role of thrombomodulin lectin-like domain in inflammation. J Biomed Sci 2012; 19:34.
128. Lenz A, Heine M, Schuler G, Romani N. Human and murine dermis contain dendritic cells. Isolation by means of a novel method and phenotypical and functional characterization. J Clin Invest 1993; 92:2587–96.
129. Nestle FO, Zheng XG, Thompson CB, Turka LA, Nickoloff BJ. Characterization of dermal dendritic cells obtained from normal human skin reveals phenotypic and functionally distinctive subsets. J Immunol 1993; 151:6535–45.
130. Sallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor α. J Exp Med 1994; 179:1109–18.
131. + dendritic cells. J Leukoc Biol 2015; 97:627–34.
132. Melum GR, Farkas L, Scheel C, Van Dieren B, Gran E, Liu YJ et al. A thymic stromal lymphopoietin-responsive dendritic cell subset mediates allergic responses in the upper airway mucosa. J Allergy Clin Immunol 2014; 134:613–21.e7.
133. Martinez-Cingolani C, Grandclaudon M, Jeanmougin M, Jouve M, Zollinger R, Soumelis V. Human blood BDCA-1 dendritic cells differentiate into Langerhans-like cells with thymic stromal lymphopoietin and TGF-beta. Blood 2014; 124:2411–20.
134. + blood dendritic cells have Langerhans cell potential. Blood 2015; 125:470–3.
135. Takahashi K, Asagoe K, Zaishun J, Yanai H, Yoshino T, Hayashi K et al. Heterogeneity of dendritic cells in human superficial lymph node: in vitro maturation of immature dendritic cells into mature or activated interdigitating reticulum cells. Am J Pathol 1998; 153:745–55.
136. Angel CE, Chen CJ, Horlacher OC, Winkler S, John T, Browning J et al. Distinctive localization of antigen-presenting cells in human lymph nodes. Blood 2009; 113:1257–67.
137. van de Ven R, van den Hout MF, Lindenberg JJ, Sluijter BJ, van Leeuwen PA, Lougheed SM et al. Characterization of four conventional dendritic cell subsets in human skin-draining lymph nodes in relation to T-cell activation. Blood 2011; 118:2502–10.
138. Summers KL, Hock BD, McKenzie JL, Hart DN. Phenotypic characterization of five dendritic cell subsets in human tonsils. Am J Pathol 2001; 159:285–95.
139. + dendritic cell isolation kits. PLoS ONE 2016; 11:e0157387.
140. + myeloid cell population in melanoma patients may attenuate the efficacy of dendritic cell vaccines. Cancer Res 2016; 76:4332–46.
141. + dendritic cells and monocyte-derived dendritic cells differ in their ability to stimulate T lymphocytes. Blood 2002; 100:2858–66.
142. Briseño CG, Gargaro M, Durai V, Davidson JT, Theisen DJ, Anderson DA et al. Deficiency of transcription factor RelB perturbs myeloid and DC development by hematopoietic-extrinsic mechanisms. Proc Natl Acad Sci USA 2017; 114:3957–62.
143. Meredith MM, Liu K, Darrasse-Jeze G, Kamphorst AO, Schreiber HA, Guermonprez P et al. Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J Exp Med 2012; 209:1153–65.
144. Satpathy AT, Wumesh KC, Albring JC, Edelson BT, Kretzer NM, Bhattacharya D et al. Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J Exp Med 2012; 209:1135–52.
145. van der Aar AM, Sylva-Steenland RM, Bos JD, Kapsenberg ML, de Jong EC, Teunissen MB. Loss of TLR2, TLR4, and TLR5 on Langerhans cells abolishes bacterial recognition. J Immunol 2007; 178:1986–90.
146. Van Rhijn I, Ly D, Moody DB. CD1a, CD1b, and CD1c in immunity against mycobacteria. Adv Exp Med Biol 2013; 783:181–97.
147. Lundberg K, Albrekt AS, Nelissen I, Santegoets S, de Gruijl TD, Gibbs S et al. Transcriptional profiling of human dendritic cell populations and models - unique profiles of in vitro dendritic cells and implications on functionality and applicability. PLoS ONE 2013; 8:e52875.
148. Harman AN, Bye CR, Nasr N, Sandgren KJ, Kim M, Mercier SK et al. Identification of lineage relationships and novel markers of blood and skin human dendritic cells. J Immunol 2013; 190:66–79.
149. Nizzoli G, Larghi P, Paroni M, Crosti MC, Moro M, Neddermann P et al. IL-10 promotes homeostatic proliferation of human CD8(+) memory T cells and when produced by CD1c(+) DCs, shapes naive CD8(+) T-cell priming. Eur J Immunol 2016; 46:1622–32.
150. Di Blasio S, Wortel IM, van Bladel DA, de Vries LE, Duiveman-de Boer T, Worah K et al. Human CD1c(+) DCs are critical cellular mediators of immune responses induced by immunogenic cell death. Oncoimmunology 2016; 5:e1192739.
151. Bauer T, Zagorska A, Jurkin J, Yasmin N, Köffel R, Richter S et al. Identification of Axl as a downstream effector of TGF-beta1 during Langerhans cell differentiation and epidermal homeostasis. J Exp Med 2012; 209:2033–47.
152. Hieronymus T, Zenke M, Baek JH, Sere K. The clash of Langerhans cell homeostasis in skin: should I stay or should I go? Semin Cell Dev Biol 2015; 41:30–8.
153. Artyomov MN, Munk A, Gorvel L, Korenfeld D, Cella M, Tung T et al. Modular expression analysis reveals functional conservation between human Langerhans cells and mouse cross-priming dendritic cells. J Exp Med 2015; 212:743–57.
154. Romano E, Cotari JW, Barreira da Silva R, Betts BC, Chung DJ, Avogadri F et al. Human Langerhans cells use an IL-15R-α/IL-15/pSTAT5-dependent mechanism to break T-cell tolerance against the self-differentiation tumor antigen WT1. Blood 2012; 119:5182–90.
155. Banchereau J, Thompson-Snipes L, Zurawski S, Blanck JP, Cao Y, Clayton S et al. The differential production of cytokines by human Langerhans cells and dermal CD14(+) DCs controls CTL priming. Blood 2012; 119:5742–9.
156. Geissmann F, Dieu-Nosjean MC, Dezutter C, Valladeau J, Kayal S, Leborgne M et al. Accumulation of immature Langerhans cells in human lymph nodes draining chronically inflamed skin. J Exp Med 2002; 196:417–30.
157. Mueller CG, Voisin B. Of skin and bone: did Langerhans cells and osteoclasts evolve from a common ancestor. J Anat 2016 doi: 10.1111/joa.12543
158. Romani N, Brunner PM, Stingl G. Changing views of the role of Langerhans cells. J Invest Dermatol 2012; 132:872–81.
159. Wu X, Briseño CG, Durai V, Albring JC, Haldar M, Bagadia P et al. Mafb lineage tracing to distinguish macrophages from other immune lineages reveals dual identity of Langerhans cells. J Exp Med 2016; 213:2553–65.
160. Price JG, Idoyaga J, Salmon H, Hogstad B, Bigarella CL, Ghaffari S et al. CDKN1A regulates Langerhans cell survival and promotes Treg cell generation upon exposure to ionizing irradiation. Nat Immunol 2015; 16:1060–8.
161. Czernielewski JM, Demarchez M. Further evidence for the self-reproducing capacity of Langerhans cells in human skin. J Invest Dermatol 1987; 88:17–20.
162. Bigley V, Haniffa M, Doulatov S, Wang XN, Dickinson R, McGovern N et al. The human syndrome of dendritic cell, monocyte, B and NK lymphoid deficiency. J Exp Med 2011; 208:227–34.
163. Kanitakis J, Morelon E, Petruzzo P, Badet L, Dubernard JM. Self-renewal capacity of human epidermal Langerhans cells: observations made on a composite tissue allograft. Exp Dermatol 2011; 20:145–6.
164. Capucha T, Mizraji G, Segev H, Blecher-Gonen R, Winter D, Khalaileh A et al. Distinct Murine Mucosal Langerhans Cell Subsets Develop from Pre-dendritic Cells and Monocytes. Immunity 2015; 43:369–81.
165. Collin M, Milne P. Langerhans cell origin and regulation. Curr Opin Hematol 2016; 23:28–35.
166. Schuster C, Mildner M, Mairhofer M, Bauer W, Fiala C, Prior M et al. Human embryonic epidermis contains a diverse Langerhans cell precursor pool. Development 2014; 141:807–15.
167. Riedl E, Stockl J, Majdic O, Scheinecker C, Knapp W, Strobl H. Ligation of E-cadherin on in vitro-generated immature Langerhans-type dendritic cells inhibits their maturation. Blood 2000; 96:4276–84.
168. Yasmin N, Konradi S, Eisenwort G, Schichl YM, Seyerl M, Bauer T et al. β-Catenin promotes the differentiation of epidermal langerhans dendritic cells. J Invest Dermatol 2013; 133:1250–9.
169. Chorro L, Sarde A, Li M, Woollard KJ, Chambon P, Malissen B et al. Langerhans cell (LC) proliferation mediates neonatal development, homeostasis, and inflammation-associated expansion of the epidermal LC network. J Exp Med 2009; 206:3089–100.
170. Seré K, Baek JH, Ober-Blöbaum J, Müller-Newen G, Tacke F, Yokota Y et al. Two distinct types of Langerhans cells populate the skin during steady state and inflammation. Immunity 2012; 37:905–16.
171. Nagao K, Kobayashi T, Moro K, Ohyama M, Adachi T, Kitashima DY et al. Stress-induced production of chemokines by hair follicles regulates the trafficking of dendritic cells in skin. Nat Immunol 2012; 13:744–52.
172. Collin MP, Hart DN, Jackson GH, Cook G, Cavet J, Mackinnon S et al. The fate of human Langerhans cells in hematopoietic stem cell transplantation. J Exp Med 2006; 203:27–33.
173. Mielcarek M, Kirkorian AY, Hackman RC, Price J, Storer BE, Wood BL et al. Langerhans cell homeostasis and turnover after nonmyeloablative and myeloablative allogeneic hematopoietic cell transplantation. Transplantation 2014; 98:563–8.
174. Strobl H, Bello-Fernandez C, Riedl E, Pickl WF, Majdic O, Lyman SD et al. flt3 ligand in cooperation with transforming growth factor-beta1 potentiates in vitro development of Langerhans-type dendritic cells and allows single-cell dendritic cell cluster formation under serum-free conditions. Blood 1997; 90:1425–34.
175. Geissmann F, Prost C, Monnet JP, Dy M, Brousse N, Hermine O. 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 1998; 187:961–6.
176. Hoshino N, Katayama N, Shibasaki T, Ohishi K, Nishioka J, Masuya M et al. A novel role for Notch ligand Delta-1 as a regulator of human Langerhans cell development from blood monocytes. J Leukoc Biol 2005; 78:921–9.
177. Hutter C, Kauer M, Simonitsch-Klupp I, Jug G, Schwentner R, Leitner J et al. Notch is active in Langerhans cell histiocytosis and confers pathognomonic features on dendritic cells. Blood 2012; 120:5199–208.
178. Jurkin J, Krump C, Köffel R, Fieber C, Schuster C, Brunner PM et al. Human skin dendritic cell fate is differentially regulated by the monocyte identity factor KLF4 during steady state and inflammation. J Allergy Clin Immunol 2016; 139:1873–84.
179. Milne P, Bigley V, Bacon CM, Néel A, McGovern N, Bomken S et al. Hematopoietic origin of Langerhans cell histiocytosis and Erdheim-Chester disease in adults. Blood 2017; 130:167–75.
180. Kim JH, Hu Y, Yongqing T, Kim J, Hughes VA, Le Nours J et al. CD1a on Langerhans cells controls inflammatory skin disease. Nat Immunol 2016; 17:1159–66.
181. Seneschal J, Clark RA, Gehad A, Baecher-Allan CM, Kupper TS. Human epidermal Langerhans cells maintain immune homeostasis in skin by activating skin resident regulatory T cells. Immunity 2012; 36:873–84.
182. Kashem SW, Igyarto BZ, Gerami-Nejad M, Kumamoto Y, Mohammed JA, Jarrett E et al. Candida albicans morphology and dendritic cell subsets determine T helper cell differentiation. Immunity 2015; 42:356–66.
183. Langlet C, Tamoutounour S, Henri S, Luche H, Ardouin L, Grégoire C et al. CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J Immunol 2012; 188:1751–60.
184. Segura E, Amigorena S. Inflammatory dendritic cells in mice and humans. Trends Immunol 2013; 34:440–5.
185. Schlitzer A, McGovern N, Ginhoux F. Dendritic cells and monocyte-derived cells: Two complementary and integrated functional systems. Semin Cell Dev Biol 2015; 41:9–22.
186. Wollenberg A, Kraft S, Hanau D, Bieber T. Immunomorphological and ultrastructural characterization of Langerhans cells and a novel, inflammatory dendritic epidermal cell (IDEC) population in lesional skin of atopic eczema. J Invest Dermatol 1996; 106:446–53.
187. Wollenberg A, Mommaas M, Oppel T, Schottdorf EM, Gunther S, Moderer M. Expression and function of the mannose receptor CD206 on epidermal dendritic cells in inflammatory skin diseases. J Invest Dermatol 2002; 118:327–34.
188. Zaba LC, Fuentes-Duculan J, Eungdamrong NJ, Abello MV, Novitskaya I, Pierson KC et al. Psoriasis is characterized by accumulation of immunostimulatory and Th1/Th17 cell-polarizing myeloid dendritic cells. J Invest Dermatol 2009; 129:79–88.
189. Jenner W, Motwani M, Veighey K, Newson J, Audzevich T, Nicolaou A et al. Characterisation of leukocytes in a human skin blister model of acute inflammation and resolution. PLoS ONE 2014; 9:e89375.
190. Eguíluz-Gracia I, Bosco A, Dollner R, Melum GR, Lexberg MH, Jones AC et al. Rapid recruitment of CD14(+) monocytes in experimentally induced allergic rhinitis in human subjects. J Allergy Clin Immunol 2016; 137:1872–81.e12.
191. Beitnes AC, Raki M, Brottveit M, Lundin KE, Jahnsen FL, Sollid LM. Rapid accumulation of CD14+CD11c+ dendritic cells in gut mucosa of celiac disease after in vivo gluten challenge. PLoS ONE 2012; 7:e33556.
192. Grimm MC, Pullman WE, Bennett GM, Sullivan PJ, Pavli P, Doe WF. Direct evidence of monocyte recruitment to inflammatory bowel disease mucosa. J Gastroenterol Hepatol 1995; 10:387–95.
193. Bain CC, Scott CL, Uronen-Hansson H, Gudjonsson S, Jansson O, Grip O et al. Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol 2013; 6:498–510.
194. Liao CT, Andrews R, Wallace LE, Khan MW, Kift-Morgan A, Topley N et al. Peritoneal macrophage heterogeneity is associated with different peritoneal dialysis outcomes. Kidney Int 2017; 91:1088–103.
195. Guilliams M, van de Laar L. A Hitchhiker's guide to myeloid cell subsets: practical implementation of a novel mononuclear phagocyte classification system. Front Immunol 2015; 6:406.
196. Wimmers F, Schreibelt G, Skold AE, Figdor CG, De Vries IJ. Paradigm shift in dendritic cell-based immunotherapy: from generated monocyte-derived DCs to naturally circulating DC subsets. Front Immunol 2014; 5:165.
197. Schakel K, von Kietzell M, Hansel A, Ebling A, Schulze L, Haase M et al. Human 6-sulfo LacNAc-expressing dendritic cells are principal producers of early interleukin-12 and are controlled by erythrocytes. Immunity 2006; 24:767–77.
198. Hofer TP, Zawada AM, Frankenberger M, Skokann K, Satzl AA, Gesierich W et al. slan-defined subsets of CD16-positive monocytes: impact of granulomatous inflammation and M-CSF receptor mutation. Blood 2015; 126:2601–10.
199. Cros J, Cagnard N, Woollard K, Patey N, Zhang SY, Senechal B et al. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 2010; 33:375–86.
200. van Leeuwen-Kerkhoff N, Lundberg K, Westers TM, Kordasti S, Bontkes HJ, de Gruijl TD et al. Transcriptional profiling reveals functional dichotomy between human slan(+) non-classical monocytes and myeloid dendritic cells. J Leukoc Biol 2017; 102:1055–68.
201. Patel AA, Zhang Y, Fullerton JN, Boelen L, Rongvaux A, Maini AA et al. The fate and lifespan of human monocyte subsets in steady state and systemic inflammation. J Exp Med 2017; 214:1913–23.
202. Calzetti F, Tamassia N, Micheletti A, Finotti G, Bianchetto-Aguilera F, Cassatella MA. Human dendritic cell subset 4 (DC4) correlate to a subset of CD14dim/- CD16++ monocytes. J Allergy Clin Immunol 2018 doi: 10.1016/j.jaci.2017.12.988