Unsupervised High-Dimensional Analysis Aligns Dendritic Cells across Tissues and Species

Immunity

Volumn 45, Issue 3, 2016, Pages 669-684

  Guilliams, Martin ^a,b,c   Dutertre, Charles Antoine ^d,e   Scott, Charlotte L ^a,b   McGovern, Naomi ^d   Sichien, Dorine ^a,b   Chakarov, Svetoslav ^d   Van Gassen, Sofie ^a,b   Chen, Jinmiao ^d   Poidinger, Michael ^d   De Prijck, Sofie ^a,b   Tavernier, Simon J ^a,b   Low, Ivy ^d   Irac, Sergio Erdal ^e   Mattar, Citra Nurfarah ^f   Sumatoh, Hermi Rizal ^d   Low, Gillian Hui Ling ^d   Chung, Tam John Kit ^f   Chan, Dedrick Kok Hong ^f   Tan, Ker Kan ^f   Hon, Tony Lim Kiat ^g   Fossum, Even ^h   Bogen, Bjarne ^h,i   Choolani, Mahesh ^f   Chan, Jerry Kok Yen ^d,e,f,j   Larbi, Anis ^d   Luche, Hervé ^c,k   Henri, Sandrine ^c   Saeys, Yvan ^a,b   Newell, Evan William ^d   Lambrecht, Bart N ^a,b,l   Malissen, Bernard ^c,k   Ginhoux, Florent ^d   more..

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d AGENCY FOR SCIENCE   (Singapore)

^e DUKE NUS MEDICAL SCHOOL   (Singapore)

^f NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^g NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^h OSLO UNIVERSITY HOSPITAL   (Norway)

ⁱ OSLO UNIVERSITY HOSPITAL   (Norway)

^j KK WOMEN'S AND CHILDREN'S HOSPITAL   (Singapore)

^k Aix Marseille University UMS3367   (France)

^l GENERAL ELECTRIC COMPANY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTIC METHOD; ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL COMPARTMENTALIZATION; CELL SUBPOPULATION; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; HIGH DIMENSIONAL ANALYSIS; HUMAN; HUMAN CELL; INFLAMMATION; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; MACACA; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; DENDRITIC CELLS; FLOW CYTOMETRY; HUMANS; INFLAMMATION; MACACA; MICE; MICE, INBRED C57BL;

EID: 84990961171     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.08.015     Document Type: Article

References (47)

1. 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 Ly6C(hi) monocyte precursors. Mucosal Immunol. 6 (2012), 498–510.
2. Bajaña, S., Roach, K., Turner, S., Paul, J., Kovats, S., IRF4 promotes cutaneous dendritic cell migration to lymph nodes during homeostasis and inflammation. J. Immunol. 189 (2012), 3368–3377.
3. Becher, B., Schlitzer, A., Chen, J., Mair, F., Sumatoh, H.R., Teng, K.W., Low, D., Ruedl, C., Riccardi-Castagnoli, P., Poidinger, M., et al. High-dimensional analysis of the murine myeloid cell system. Nat. Immunol. 15 (2014), 1181–1189.
4. Breton, G., Lee, J., Zhou, Y.J., Schreiber, J.J., Keler, T., Puhr, S., Anandasabapathy, N., Schlesinger, S., Caskey, M., Liu, K., Nussenzweig, M.C., Circulating precursors of human CD1c+ and CD141+ dendritic cells. J. Exp. Med. 212 (2015), 401–413.
5. Caton, M.L., Smith-Raska, M.R., Reizis, B., Notch-RBP-J signaling controls the homeostasis of CD8- dendritic cells in the spleen. J. Exp. Med. 204 (2007), 1653–1664.
6. Cheng, Y., Wong, M.T., van der Maaten, L., Newell, E.W., Categorical analysis of human t cell heterogeneity with one-dimensional soli-expression by nonlinear stochastic embedding. J. Immunol. 196 (2015), 924–932.
7. Collin, M., McGovern, N., Haniffa, M., Human dendritic cell subsets. Immunology 140 (2013), 22–30.
8. Crozat, K., Guiton, R., Contreras, V., Feuillet, V., Dutertre, C.A., Ventre, E., Vu Manh, T.P., Baranek, T., Storset, A.K., Marvel, J., et al. The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8alpha+ dendritic cells. J. Exp. Med. 207 (2010), 1283–1292.
9. Dorner, B.G., Dorner, M.B., Zhou, X., Opitz, C., Mora, A., Güttler, S., Hutloff, A., Mages, H.W., Ranke, K., Schaefer, M., et al. Selective expression of the chemokine receptor XCR1 on cross-presenting dendritic cells determines cooperation with CD8+ T cells. Immunity 31 (2009), 823–833.
10. Dutertre, C.A., Jourdain, J.P., Rancez, M., Amraoui, S., Fossum, E., Bogen, B., Sanchez, C., Couëdel-Courteille, A., Richard, Y., Dalod, M., et al. TLR3-responsive, XCR1+, CD141(BDCA-3)+/CD8α+-equivalent dendritic cells uncovered in healthy and simian immunodeficiency virus-infected rhesus macaques. J. Immunol. 192 (2014), 4697–4708.
11. Fossum, E., Grødeland, G., Terhorst, D., Tveita, A.A., Vikse, E., Mjaaland, S., Henri, S., Malissen, B., Bogen, B., Vaccine molecules targeting Xcr1 on cross-presenting DCs induce protective CD8+ T-cell responses against influenza virus. Eur. J. Immunol. 45 (2015), 624–635.
12. Gatto, D., Wood, K., Caminschi, I., Murphy-Durland, D., Schofield, P., Christ, D., Karupiah, G., Brink, R., The chemotactic receptor EBI2 regulates the homeostasis, localization and immunological function of splenic dendritic cells. Nat. Immunol. 14 (2013), 446–453.
13. 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.
14. Ginhoux, F., Collin, M.P., Bogunovic, M., Abel, M., Leboeuf, M., Helft, J., Ochando, J., Kissenpfennig, A., Malissen, B., Grisotto, M., et al. Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J. Exp. Med. 204 (2007), 3133–3146.
15. Grajales-Reyes, G.E., Iwata, A., Albring, J., Wu, X., Tussiwand, R., Kc, W., Kretzer, N.M., Briseño, C.G., Durai, V., Bagadia, P., et al. Batf3 maintains autoactivation of Irf8 for commitment of a CD8α(+) conventional DC clonogenic progenitor. Nat. Immunol. 16 (2015), 708–717.
16. 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., 6, 2015, 406.
17. 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.
18. Gurka, S., Hartung, E., Becker, M., Kroczek, R.A., Mouse conventional dendritic cells can be universally classified based on the mutually exclusive expression of xcr1 and sirpα. Front. Immunol., 6, 2015, 35.
19. Henri, S., Poulin, L.F., Tamoutounour, S., Ardouin, L., Guilliams, M., de Bovis, B., Devilard, E., Viret, C., Azukizawa, H., Kissenpfennig, A., Malissen, B., CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J. Exp. Med. 207 (2010), 189–206.
20. Langlet, C., Tamoutounour, S., Henri, S., Luche, H., Ardouin, L., Grégoire, C., Malissen, B., Guilliams, M., CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J. Immunol. 188 (2012), 1751–1760.
21. Lee, J., Breton, G., Oliveira, T.Y., Zhou, Y.J., Aljoufi, A., Puhr, S., Cameron, M.J., Sékaly, R.P., Nussenzweig, M.C., Liu, K., Restricted dendritic cell and monocyte progenitors in human cord blood and bone marrow. J. Exp. Med. 212 (2015), 385–399.
22. Lewis, K.L., Caton, M.L., Bogunovic, M., Greter, M., Grajkowska, L.T., Ng, D., Klinakis, A., Charo, I.F., Jung, S., Gommerman, J.L., et al. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 35 (2011), 780–791.
23. Mair, F., Hartmann, F.J., Mrdjen, D., Tosevski, V., Krieg, C., Becher, B., The end of gating? An introduction to automated analysis of high dimensional cytometry data. Eur. J. Immunol. 46 (2015), 34–43.
24. Maisonnasse, P., Bouguyon, E., Piton, G., Ezquerra, A., Urien, C., Deloizy, C., Bourge, M., Leplat, J.J., Simon, G., Chevalier, C., et al. The respiratory DC/macrophage network at steady-state and upon influenza infection in the swine biomedical model. Mucosal Immunol. 9 (2015), 834–849.
25. Malissen, B., Tamoutounour, S., Henri, S., The origins and functions of dendritic cells and macrophages in the skin. Nat. Rev. Immunol. 14 (2014), 417–428.
26. + cells are a transient population of monocyte-derived macrophages. Immunity 41 (2014), 465–477.
27. McGovern, N., Chan, J.K., Ginhoux, F., Dendritic cells in humans–from fetus to adult. Int. Immunol. 27 (2015), 65–72.
28. 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.
29. Naik, S.H., Metcalf, D., van Nieuwenhuijze, A., Wicks, I., Wu, L., O'Keeffe, M., Shortman, K., Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat. Immunol. 7 (2006), 663–671.
30. Nakano, H., Lin, K.L., Yanagita, M., Charbonneau, C., Cook, D.N., Kakiuchi, T., Gunn, M.D., Blood-derived inflammatory dendritic cells in lymph nodes stimulate acute T helper type 1 immune responses. Nat. Immunol. 10 (2009), 394–402.
31. Onai, N., Kurabayashi, K., Hosoi-Amaike, M., Toyama-Sorimachi, N., Matsushima, K., Inaba, K., Ohteki, T., A clonogenic progenitor with prominent plasmacytoid dendritic cell developmental potential. Immunity 38 (2013), 943–957.
32. Osorio, F., Tavernier, S.J., Hoffmann, E., Saeys, Y., Martens, L., Vetters, J., Delrue, I., De Rycke, R., Parthoens, E., Pouliot, P., et al. The unfolded-protein-response sensor IRE-1α regulates the function of CD8α+ dendritic cells. Nat. Immunol. 15 (2014), 248–257.
33. Persson, E.K., Uronen-Hansson, H., Semmrich, M., Rivollier, A., Hägerbrand, K., Marsal, J., Gudjonsson, S., Håkansson, U., Reizis, B., Kotarsky, K., Agace, W.W., IRF4 transcription-factor-dependent CD103(+)CD11b(+) dendritic cells drive mucosal T helper 17 cell differentiation. Immunity 38 (2013), 958–969.
34. Plantinga, M., Guilliams, M., Vanheerswynghels, M., Deswarte, K., Branco-Madeira, F., Toussaint, W., Vanhoutte, L., Neyt, K., Killeen, N., Malissen, B., et al. Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 38 (2013), 322–335.
35. Saeys, Y., Gassen, S.V., Lambrecht, B.N., Computational flow cytometry: helping to make sense of high-dimensional immunology data. Nat. Rev. Immunol. 16 (2016), 449–462.
36. Schlitzer, A., McGovern, N., Teo, P., Zelante, T., Atarashi, K., Low, D., Ho, A.W., See, P., Shin, A., Wasan, P.S., et al. IRF4 transcription factor-dependent CD11b+ dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38 (2013), 970–983.
37. 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.
38. Schraml, B.U., van Blijswijk, J., Zelenay, S., Whitney, P.G., Filby, A., Acton, S.E., Rogers, N.C., Moncaut, N., Carvajal, J.J., Reis e Sousa, C., Genetic tracing via DNGR-1 expression history defines dendritic cells as a hematopoietic lineage. Cell 154 (2013), 843–858.
39. Scott, C.L., Bain, C.C., Wright, P.B., Sichien, D., Kotarsky, K., Persson, E.K., Luda, K., Guilliams, M., Lambrecht, B.N., Agace, W.W., et al. CCR2(+)CD103(-) intestinal dendritic cells develop from DC-committed precursors and induce interleukin-17 production by T cells. Mucosal Immunol. 8 (2015), 327–339.
40. Scott, C.L., Soen, B., Martens, L., Skrypek, N., Saelens, W., Taminau, J., Blancke, G., Van Isterdael, G., Huylebroeck, D., Haigh, J., et al. The transcription factor Zeb2 regulates development of conventional and plasmacytoid DCs by repressing Id2. J. Exp. Med. 213 (2016), 897–911.
41. Sichien, D., Scott, C.L., Martens, L., Vanderkerken, M., Van Gassen, S., Plantinga, M., Joeris, T., De Prijck, S., Vanhoutte, L., Vanheerswynghels, M., et al. IRF8 controls survival and function in terminally differentiated conventional and plasmacytoid dendritic cells respectively. Immunity 45 (2016), 626–640 this issue.
42. Tamoutounour, S., Henri, S., Lelouard, H., de Bovis, B., de Haar, C., van der Woude, C.J., Woltman, A.M., Reyal, Y., Bonnet, D., Sichien, D., et al. CD64 distinguishes macrophages from dendritic cells in the gut and reveals the Th1-inducing role of mesenteric lymph node macrophages during colitis. Eur. J. Immunol. 42 (2012), 3150–3166.
43. 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.
44. Tussiwand, R., Everts, B., Grajales-Reyes, G.E., Kretzer, N.M., Iwata, A., Bagaitkar, J., Wu, X., Wong, R., Anderson, D.A., Murphy, T.L., et al. Klf4 expression in conventional dendritic cells is required for T helper 2 cell responses. Immunity 42 (2015), 916–928.
45. Van Gassen, S., Callebaut, B., Van Helden, M.J., Lambrecht, B.N., Demeester, P., Dhaene, T., Saeys, Y., FlowSOM: Using self-organizing maps for visualization and interpretation of cytometry data. Cytometry A 87 (2015), 636–645.
46. 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.
47. Wong, M.T., Chen, J., Narayanan, S., Lin, W., Anicete, R., Kiaang, H.T., De Lafaille, M.A., Poidinger, M., Newell, E.W., Mapping the Diversity of Follicular Helper T Cells in Human Blood and Tonsils Using High-Dimensional Mass Cytometry Analysis. Cell Rep. 11 (2015), 1822–1833.