Aryl Hydrocarbon Receptor Controls Monocyte Differentiation into Dendritic Cells versus Macrophages

Immunity

Volumn 47, Issue 3, 2017, Pages 582-596.e6

  Goudot, Christel ^a   Coillard, Alice ^a   Villani, Alexandra Chloé ^b,c   Gueguen, Paul ^a   Cros, Adeline ^a   Sarkizova, Siranush ^d   Tang Huau, Tsing Lee ^a,e   Bohec, Mylène ^f   Baulande, Sylvain ^f   Hacohen, Nir ^b,c   Amigorena, Sebastian ^a   Segura, Elodie ^a  

^a PSL RESEARCH UNIVERSITY   (France)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e SANOFI   (France)

^f INSTITUT CURIE   (France)

Author keywords

aryl hydrocarbon receptor; dendritic cell; human; IRF4; macrophage; MAFB; monocyte

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; INTERFERON REGULATORY FACTOR 4; TRANSCRIPTION FACTOR MAFB; CYTOKINE; INTERFERON REGULATORY FACTOR; INTERFERON REGULATORY FACTOR-4; PRDM1 PROTEIN, HUMAN; REPRESSOR PROTEIN; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASCITES TUMOR; CELL CULTURE; CELL DIFFERENTIATION; CELL INFILTRATION; CONTROLLED STUDY; CORRELATION ANALYSIS; DENDRITIC CELL; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LEPROSY; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; ANIMAL; ASCITES; CLUSTER ANALYSIS; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; NEOPLASM;

ANIMALS; ASCITES; CELLS, CULTURED; CLUSTER ANALYSIS; CYTOKINES; DENDRITIC CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; INTERFERON REGULATORY FACTORS; LEPROSY; MACROPHAGES; MAFB TRANSCRIPTION FACTOR; MALE; MICE; MICE, KNOCKOUT; MONOCYTES; NEOPLASMS; RECEPTORS, ARYL HYDROCARBON; REPRESSOR PROTEINS; TRANSCRIPTOME;

EID: 85031751449     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2017.08.016     Document Type: Article

References (66)

1. Aziz, A., Vanhille, L., Mohideen, P., Kelly, L.M., Otto, C., Bakri, Y., Mossadegh, N., Sarrazin, S., Sieweke, M.H., Development of macrophages with altered actin organization in the absence of MafB. Mol. Cell. Biol. 26 (2006), 6808–6818.
2. Aziz, A., Soucie, E., Sarrazin, S., Sieweke, M.H., MafB/c-Maf deficiency enables self-renewal of differentiated functional macrophages. Science 326 (2009), 867–871.
3. Bain, C.C., Scott, C.L., Uronen-Hansson, H., Gudjonsson, S., Jansson, O., Grip, O., Guilliams, M., Malissen, B., Agace, W.W., Mowat, A.M., Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol. 6 (2013), 498–510.
4. Bain, C.C., Bravo-Blas, A., Scott, C.L., Perdiguero, E.G., Geissmann, F., Henri, S., Malissen, B., Osborne, L.C., Artis, D., Mowat, A.M., Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat. Immunol. 15 (2014), 929–937.
5. Bakri, Y., Sarrazin, S., Mayer, U.P., Tillmanns, S., Nerlov, C., Boned, A., Sieweke, M.H., Balance of MafB and PU.1 specifies alternative macrophage or dendritic cell fate. Blood 105 (2005), 2707–2716.
6. Bjeldanes, L.F., Kim, J.Y., Grose, K.R., Bartholomew, J.C., Bradfield, C.A., Aromatic hydrocarbon responsiveness-receptor agonists generated from indole-3-carbinol in vitro and in vivo: comparisons with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Proc. Natl. Acad. Sci. USA 88 (1991), 9543–9547.
7. Breton, G., Zheng, S., Valieris, R., Tojal da Silva, I., Satija, R., Nussenzweig, M.C., Human dendritic cells (DCs) are derived from distinct circulating precursors that are precommitted to become CD1c+ or CD141+ DCs. J. Exp. Med. 213 (2016), 2861–2870.
8. Briseño, C.G., Haldar, M., Kretzer, N.M., Wu, X., Theisen, D.J., Kc, W., Durai, V., Grajales-Reyes, G.E., Iwata, A., Bagadia, P., et al. Distinct transcriptional programs control cross-priming in classical and monocyte-derived dendritic cells. Cell Rep. 15 (2016), 2462–2474.
9. Buenrostro, J.D., Wu, B., Litzenburger, U.M., Ruff, D., Gonzales, M.L., Snyder, M.P., Chang, H.Y., Greenleaf, W.J., Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523 (2015), 486–490.
10. Carpentier, S., Vu Manh, T.P., Chelbi, R., Henri, S., Malissen, B., Haniffa, M., Ginhoux, F., Dalod, M., Comparative genomics analysis of mononuclear phagocyte subsets confirms homology between lymphoid tissue-resident and dermal XCR1(+) DCs in mouse and human and distinguishes them from Langerhans cells. J. Immunol. Methods 432 (2016), 35–49.
11. Carvalho, B.S., Irizarry, R.A., A framework for oligonucleotide microarray preprocessing. Bioinformatics 26 (2010), 2363–2367.
12. Chessel, D., Dufour, A.B., and Thioulouse, J. (2004). The ade4 package-I: One-table methods. R News http://pbil.univ-lyon1.fr/JTHome/ref/ade4-Rnews.pdf.
13. Croxford, A.L., Lanzinger, M., Hartmann, F.J., Schreiner, B., Mair, F., Pelczar, P., Clausen, B.E., Jung, S., Greter, M., Becher, B., The cytokine GM-CSF drives the inflammatory signature of CCR2+ monocytes and licenses autoimmunity. Immunity 43 (2015), 502–514.
14. Davies, L.C., Rosas, M., Jenkins, S.J., Liao, C.T., Scurr, M.J., Brombacher, F., Fraser, D.J., Allen, J.E., Jones, S.A., Taylor, P.R., Distinct bone marrow-derived and tissue-resident macrophage lineages proliferate at key stages during inflammation. Nat. Commun., 4, 2013, 1886.
15. De Abrew, K.N., Kaminski, N.E., Thomas, R.S., An integrated genomic analysis of aryl hydrocarbon receptor-mediated inhibition of B-cell differentiation. Toxicol. Sci. 118 (2010), 454–469.
16. Di Meglio, P., Duarte, J.H., Ahlfors, H., Owens, N.D., Li, Y., Villanova, F., Tosi, I., Hirota, K., Nestle, F.O., Mrowietz, U., et al. Activation of the aryl hydrocarbon receptor dampens the severity of inflammatory skin conditions. Immunity 40 (2014), 989–1001.
17. Eguíluz-Gracia, I., Bosco, A., Dollner, R., Melum, G.R., Lexberg, M.H., Jones, A.C., Dheyauldeen, S.A., Holt, P.G., Bækkevold, E.S., Jahnsen, F.L., Rapid recruitment of CD14(+) monocytes in experimentally induced allergic rhinitis in human subjects. J. Allergy Clin. Immunol. 137 (2016), 1872–1881.e12.
18. Fernandez-Salguero, P., Pineau, T., Hilbert, D.M., McPhail, T., Lee, S.S., Kimura, S., Nebert, D.W., Rudikoff, S., Ward, J.M., Gonzalez, F.J., Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268 (1995), 722–726.
19. Fritsche, E., Schäfer, C., Calles, C., Bernsmann, T., Bernshausen, T., Wurm, M., Hübenthal, U., Cline, J.E., Hajimiragha, H., Schroeder, P., et al. Lightening up the UV response by identification of the arylhydrocarbon receptor as a cytoplasmatic target for ultraviolet B radiation. Proc. Natl. Acad. Sci. USA 104 (2007), 8851–8856.
20. Gautier, E.L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K.G., Gordonov, S., et al., Immunological Genome Consortium. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 13 (2012), 1118–1128.
21. Getts, D.R., Terry, R.L., Getts, M.T., Deffrasnes, C., Müller, M., van Vreden, C., Ashhurst, T.M., Chami, B., McCarthy, D., Wu, H., et al. Therapeutic inflammatory monocyte modulation using immune-modifying microparticles. Sci. Transl. Med., 6, 2014, 219ra7.
22. Gomez de Agüero, M., Ganal-Vonarburg, S.C., Fuhrer, T., Rupp, S., Uchimura, Y., Li, H., Steinert, A., Heikenwalder, M., Hapfelmeier, S., Sauer, U., et al. The maternal microbiota drives early postnatal innate immune development. Science 351 (2016), 1296–1302.
23. Gosselin, D., Link, V.M., Romanoski, C.E., Fonseca, G.J., Eichenfield, D.Z., Spann, N.J., Stender, J.D., Chun, H.B., Garner, H., Geissmann, F., Glass, C.K., Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 159 (2014), 1327–1340.
24. Greter, M., Helft, J., Chow, A., Hashimoto, D., Mortha, A., Agudo-Cantero, J., Bogunovic, M., Gautier, E.L., Miller, J., Leboeuf, M., et al. GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity 36 (2012), 1031–1046.
25. Grimm, M.C., Pullman, W.E., Bennett, G.M., Sullivan, P.J., Pavli, P., Doe, W.F., Direct evidence of monocyte recruitment to inflammatory bowel disease mucosa. J. Gastroenterol. Hepatol. 10 (1995), 387–395.
26. Guilliams, M., Ginhoux, F., Jakubzick, C., Naik, S.H., Onai, N., Schraml, B.U., Segura, E., Tussiwand, R., Yona, S., Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat. Rev. Immunol. 14 (2014), 571–578.
27. Haldar, M., Kohyama, M., So, A.Y., Kc, W., Wu, X., Briseño, C.G., Satpathy, A.T., Kretzer, N.M., Arase, H., Rajasekaran, N.S., et al. Heme-mediated SPI-C induction promotes monocyte differentiation into iron-recycling macrophages. Cell 156 (2014), 1223–1234.
28. Ikuta, T., Ohba, M., Zouboulis, C.C., Fujii-Kuriyama, Y., Kawajiri, K., B lymphocyte-induced maturation protein 1 is a novel target gene of aryl hydrocarbon receptor. J. Dermatol. Sci. 58 (2010), 211–216.
29. Jenner, W., Motwani, M., Veighey, K., Newson, J., Audzevich, T., Nicolaou, A., Murphy, S., Macallister, R., Gilroy, D.W., Characterisation of leukocytes in a human skin blister model of acute inflammation and resolution. PLoS ONE, 9, 2014, e89375.
30. Kamada, N., Hisamatsu, T., Okamoto, S., Chinen, H., Kobayashi, T., Sato, T., Sakuraba, A., Kitazume, M.T., Sugita, A., Koganei, K., et al. Unique CD14 intestinal macrophages contribute to the pathogenesis of Crohn disease via IL-23/IFN-gamma axis. J. Clin. Invest. 118 (2008), 2269–2280.
31. Kauffmann, A., Gentleman, R., Huber, W., arrayQualityMetrics–a bioconductor package for quality assessment of microarray data. Bioinformatics 25 (2009), 415–416.
32. Kelly, L.M., Englmeier, U., Lafon, I., Sieweke, M.H., Graf, T., MafB is an inducer of monocytic differentiation. EMBO J. 19 (2000), 1987–1997.
33. Kim, K.W., Williams, J.W., Wang, Y.T., Ivanov, S., Gilfillan, S., Colonna, M., Virgin, H.W., Gautier, E.L., Randolph, G.J., MHC II+ resident peritoneal and pleural macrophages rely on IRF4 for development from circulating monocytes. J. Exp. Med. 213 (2016), 1951–1959.
34. Lavin, Y., Winter, D., Blecher-Gonen, R., David, E., Keren-Shaul, H., Merad, M., Jung, S., Amit, I., Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159 (2014), 1312–1326.
35. Lehtonen, A., Veckman, V., Nikula, T., Lahesmaa, R., Kinnunen, L., Matikainen, S., Julkunen, I., Differential expression of IFN regulatory factor 4 gene in human monocyte-derived dendritic cells and macrophages. J. Immunol. 175 (2005), 6570–6579.
36. Leuschner, F., Dutta, P., Gorbatov, R., Novobrantseva, T.I., Donahoe, J.S., Courties, G., Lee, K.M., Kim, J.I., Markmann, J.F., Marinelli, B., et al. Therapeutic siRNA silencing in inflammatory monocytes in mice. Nat. Biotechnol. 29 (2011), 1005–1010.
37. + cells are a transient population of monocyte-derived macrophages. Immunity 41 (2014), 465–477.
38. Menezes, S., Melandri, D., Anselmi, G., Perchet, T., Loschko, J., Dubrot, J., Patel, R., Gautier, E.L., Hugues, S., Longhi, M.P., et al. The heterogeneity of Ly6C(hi) monocytes controls their differentiation into iNOS(+) macrophages or monocyte-derived dendritic cells. Immunity 45 (2016), 1205–1218.
39. Mildner, A., Yona, S., Jung, S., A close encounter of the third kind: monocyte-derived cells. Adv. Immunol. 120 (2013), 69–103.
40. Mildner, A., Schönheit, J., Giladi, A., David, E., Lara-Astiaso, D., Lorenzo-Vivas, E., Paul, F., Chappell-Maor, L., Priller, J., Leutz, A., et al. Genomic characterization of murine monocytes reveals C/EBPβ transcription factor dependence of Ly6C(-) cells. Immunity 46 (2017), 849–862.e7.
41. Montoya, D., Cruz, D., Teles, R.M., Lee, D.J., Ochoa, M.T., Krutzik, S.R., Chun, R., Schenk, M., Zhang, X., Ferguson, B.G., et al. Divergence of macrophage phagocytic and antimicrobial programs in leprosy. Cell Host Microbe 6 (2009), 343–353.
42. Murphy, T.L., Grajales-Reyes, G.E., Wu, X., Tussiwand, R., Briseno, C.G., Iwata, A., Kretzer, N.M., Durai, V., Murphy, K.M., Transcriptional control of dendritic cell development. Annu. Rev. Immunol. 34 (2015), 93–119.
43. Noy, R., Pollard, J.W., Tumor-associated macrophages: from mechanisms to therapy. Immunity 41 (2014), 49–61.
44. Okabe, Y., Medzhitov, R., Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 157 (2014), 832–844.
45. Patel, A.A., Zhang, Y., Fullerton, J.N., Boelen, L., Rongvaux, A., Maini, A.A., Bigley, V., Flavell, R.A., Gilroy, D.W., Asquith, B., et al. The fate and lifespan of human monocyte subsets in steady state and systemic inflammation. J. Exp. Med. 214 (2017), 1913–1923.
46. Russell, D.G., Cardona, P.J., Kim, M.J., Allain, S., Altare, F., Foamy macrophages and the progression of the human tuberculosis granuloma. Nat. Immunol. 10 (2009), 943–948.
47. Satija, R., Farrell, J.A., Gennert, D., Schier, A.F., Regev, A., Spatial reconstruction of single-cell gene expression data. Nat. Biotechnol. 33 (2015), 495–502.
48. Schlitzer, A., Sivakamasundari, V., Chen, J., Sumatoh, H.R., Schreuder, J., Lum, J., Malleret, B., Zhang, S., Larbi, A., Zolezzi, F., et al. Identification of cDC1- and cDC2-committed DC progenitors reveals early lineage priming at the common DC progenitor stage in the bone marrow. Nat. Immunol. 16 (2015), 718–728.
49. Schreiber, H.A., Sandor, M., The role of dendritic cells in mycobacterium-induced granulomas. Immunol. Lett. 130 (2010), 26–31.
50. Segura, E., Amigorena, S., Inflammatory dendritic cells in mice and humans. Trends Immunol. 34 (2013), 440–445.
51. Segura, E., Touzot, M., Bohineust, A., Cappuccio, A., Chiocchia, G., Hosmalin, A., Dalod, M., Soumelis, V., Amigorena, S., Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity 38 (2013), 336–348.
52. Servant, N., Gravier, E., Gestraud, P., Laurent, C., Paccard, C., Biton, A., Brito, I., Mandel, J., Asselain, B., Barillot, E., Hupé, P., EMA - A R package for easy microarray data analysis. BMC Res. Notes, 3, 2010, 277.
53. Sieling, P.A., Jullien, D., Dahlem, M., Tedder, T.F., Rea, T.H., Modlin, R.L., Porcelli, S.A., CD1 expression by dendritic cells in human leprosy lesions: correlation with effective host immunity. J. Immunol. 162 (1999), 1851–1858.
54. Smyth, G.K., Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol., 3, 2004, e3.
55. Stockinger, B., Di Meglio, P., Gialitakis, M., Duarte, J.H., The aryl hydrocarbon receptor: multitasking in the immune system. Annu. Rev. Immunol. 32 (2014), 403–432.
56. Tamoutounour, S., Guilliams, M., Montanana Sanchis, F., Liu, H., Terhorst, D., Malosse, C., Pollet, E., Ardouin, L., Luche, H., Sanchez, C., et al. Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 39 (2013), 925–938.
57. van der Maaten, L. (2013). Barnes-Hut-SNE. arXiv. arXiv:1301.3342v2.
58. Veldhoen, M., Hirota, K., Christensen, J., O'Garra, A., Stockinger, B., Natural agonists for aryl hydrocarbon receptor in culture medium are essential for optimal differentiation of Th17 T cells. J. Exp. Med. 206 (2009), 43–49.
59. Villani, A.C., Satija, R., Reynolds, G., Sarkizova, S., Shekhar, K., Fletcher, J., Griesbeck, M., Butler, A., Zheng, S., Lazo, S., et al. Single-cell RNA-seq reveals new types of human blood dendritic cells, monocytes, and progenitors. Science, 356, 2017, 356.
60. Watchmaker, P.B., Lahl, K., Lee, M., Baumjohann, D., Morton, J., Kim, S.J., Zeng, R., Dent, A., Ansel, K.M., Diamond, B., et al. Comparative transcriptional and functional profiling defines conserved programs of intestinal DC differentiation in humans and mice. Nat. Immunol. 15 (2014), 98–108.
61. 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. 106 (1996), 446–453.
62. Wong, K.L., Tai, J.J., Wong, W.C., Han, H., Sem, X., Yeap, W.H., Kourilsky, P., Wong, S.C., Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood 118 (2011), e16–e31.
63. Zaba, L.C., Fuentes-Duculan, J., Eungdamrong, N.J., Abello, M.V., Novitskaya, I., Pierson, K.C., Gonzalez, J., Krueger, J.G., Lowes, M.A., Psoriasis is characterized by accumulation of immunostimulatory and Th1/Th17 cell-polarizing myeloid dendritic cells. J. Invest. Dermatol. 129 (2009), 79–88.
64. Zelante, T., Iannitti, R.G., Cunha, C., De Luca, A., Giovannini, G., Pieraccini, G., Zecchi, R., D'Angelo, C., Massi-Benedetti, C., Fallarino, F., et al. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 39 (2013), 372–385.
65. Zheng, G.X., Terry, J.M., Belgrader, P., Ryvkin, P., Bent, Z.W., Wilson, R., Ziraldo, S.B., Wheeler, T.D., McDermott, G.P., Zhu, J., et al. Massively parallel digital transcriptional profiling of single cells. Nat. Commun., 8, 2017, 14049.
66. Zigmond, E., Varol, C., Farache, J., Elmaliah, E., Satpathy, A.T., Friedlander, G., Mack, M., Shpigel, N., Boneca, I.G., Murphy, K.M., et al. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 37 (2012), 1076–1090.