Langerhans cells are generated by two distinct PU.1-dependent transcriptional networks

Journal of Experimental Medicine

Volumn 210, Issue 13, 2013, Pages 2967-2980

  Chopin, Michaël ^a,b   Seillet, Cyril ^a,b   Chevrier, Stéphane ^a,b   Wu, Li ^a,b,c   Wang, Hongsheng ^d   Morse III, Herbert C ^d   Belz, Gabrielle T ^a,b   Nutt, Stephen L ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c PEKING UNIVERSITY   (China)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INHIBITOR OF DIFFERENTIATION 2; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERFERON REGULATORY FACTOR 4; TRANSCRIPTION FACTOR PU 1; TRANSCRIPTION FACTOR RUNX3; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; CONTROLLED STUDY; EPIDERMIS; GENE EXPRESSION REGULATION; HOMEOSTASIS; INFLAMMATION; LANGERHANS CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY SEQUENCE; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; CELL DIFFERENTIATION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; INFLAMMATION; INHIBITOR OF DIFFERENTIATION PROTEIN 2; INTERFERON REGULATORY FACTORS; LANGERHANS CELLS; MICE; MOLECULAR SEQUENCE DATA; MONOCYTES; PROTO-ONCOGENE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84890809254     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20130930     Document Type: Article

References (60)

1. Bachem, A., E. Hartung, S. Güttler, A. Mora, X. Zhou, A. Hegemann, M. Plantinga, E. Mazzini, P. Stoitzner, S. Gurka, et al. 2012. Expression of XCR1 characterizes the Batf3-dependent lineage of dendritic cells capable of antigen cross-presentation. Front Immunol. 3:214. http://dx.doi.org/10.3389/fimmu.2012.00214
2. Bajaña, 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. http://dx.doi.org/10.4049/jimmunol.1102613
3. Becker, M.R., Y.S. Choi, S.E. Millar, and M.C. Udey. 2011. Wnt signaling influences the development of murine epidermal Langerhans cells. J. Invest. Dermatol. 131:1861-1868. http://dx.doi.org/10.1038/jid.2011.131
4. Belz, G.T., and S.L. Nutt. 2012. Transcriptional programming of the dendritic cell network. Nat. Rev. Immunol. 12:101-113. http://dx.doi.org/10.1038/nri3149
5. Borkowski, T.A., J.J. Letterio, A.G. Farr, and M.C. Udey. 1996. A role for endogenous transforming growth factor beta 1 in Langerhans cell biology: the skin of transforming growth factor beta 1 null mice is devoid of epidermal Langerhans cells. J. Exp. Med. 184:2417-2422. http://dx.doi.org/10.1084/jem.184.6.2417
6. Borkowski, T.A., J.J. Letterio, C.L. Mackall, A. Saitoh, X.J. Wang, D.R. Roop, R.E. Gress, and M.C. Udey. 1997. A role for TGFbeta1 in langerhans cell biology. Further characterization of the epidermal Langerhans cell defect in TGFbeta1 null mice. J. Clin. Invest. 100:575-581. http://dx.doi.org/10.1172/JCI119567
7. Bursch, L.S., L. Wang, B. Igyarto, A. Kissenpfennig, B. Malissen, D.H. Kaplan, and K.A. Hogquist. 2007. Identification of a novel population of Langerin+ dendritic cells. J. Exp. Med. 204:3147-3156. http://dx.doi.org/10.1084/jem.20071966
8. Carotta, S., A. Dakic, A. D'Amico, S.H. Pang, K.T. Greig, S.L. Nutt, and L. Wu. 2010. The transcription factor PU.1 controls dendritic cell development and Flt3 cytokine receptor expression in a dose-dependent manner. Immunity. 32:628-641. http://dx.doi.org/10.1016/j.immuni.2010.05.005
9. Caton, M.L., M.R. Smith-Raska, and B. Reizis. 2007. Notch-RBP-J signaling controls the homeostasis of CD8-dendritic cells in the spleen. J. Exp. Med. 204:1653-1664.
10. Chorro, L., A. Sarde, M. Li, K.J. Woollard, P. Chambon, B. Malissen, A. Kissenpfennig, J.B. Barbaroux, R. Groves, and F. Geissmann. 2009. Langerhans cell (LC) proliferation mediates neonatal development, homeostasis, and inflammation-associated expansion of the epidermal LC network. J. Exp. Med. 206:3089-3100. http://dx.doi.org/10.1084/jem.20091586
11. Crozat, K., S. Tamoutounour, T.P. Vu Manh, E. Fossum, H. Luche, L. Ardouin, M. Guilliams, H. Azukizawa, B. Bogen, B. Malissen, et al. 2011. Cutting edge: expression of XCR1 defines mouse lymphoid-tissue resident and migratory dendritic cells of the CD8α+ type. J. Immunol. 187:4411-4415. http://dx.doi.org/10.4049/jimmunol.1101717
12. Cunningham, A.L., F. Carbone, and T.B. Geijtenbeek. 2008. Langerhans cells and viral immunity. Eur. J. Immunol. 38:2377-2385. http://dx.doi.org/10.1002/eji.200838521
13. Dakic, A., D. Metcalf, L. Di Rago, S. Mifsud, L. Wu, and S.L. Nutt. 2005. PU.1 regulates the commitment of adult hematopoietic progenitors and restricts granulopoiesis. J. Exp. Med. 201:1487-1502. http://dx.doi.org/10.1084/jem.20050075
14. Dakic, A., L. Wu, and S.L. Nutt. 2007. Is PU.1 a dosage-sensitive regulator of haemopoietic lineage commitment and leukaemogenesis? Trends Immunol. 28:108-114. http://dx.doi.org/10.1016/j.it.2007.01.006
15. + conventional dendritic cells. J. Exp. Med. 207:823-836. http://dx.doi.org/10.1084/jem.20091627
16. Edelson, B.T., T.R. Bradstreet, W. Kc, K. Hildner, J.W. Herzog, J. Sim, J.H. Russell, T.L. Murphy, E.R. Unanue, and K.M. Murphy. 2011. Batf3-dependent CD11b(low/-) peripheral dendritic cells are GM-CSFindependent and are not required for Th cell priming after subcutaneous immunization. PLoS ONE. 6:e25660. http://dx.doi.org/10.1371/journal.pone.0025660
17. Fainaru, O., E. Woolf, J. Lotem, M. Yarmus, O. Brenner, D. Goldenberg, V. Negreanu, Y. Bernstein, D. Levanon, S. Jung, and Y. Groner. 2004. Runx3 regulates mouse TGF-beta-mediated dendritic cell function and its absence results in airway inflammation. EMBO J. 23:969-979. http://dx.doi.org/10.1038/sj.emboj.7600085
18. Feng, J., H. Wang, D.M. Shin, M. Masiuk, C.F. Qi, and H.C. Morse III. 2011. IFN regulatory factor 8 restricts the size of the marginal zone and follicular B cell pools. J. Immunol. 186:1458-1466. http://dx.doi.org/10.4049/jimmunol.1001950
19. Gaiser, M.R., T. Lämmermann, X. Feng, B.Z. Igyarto, D.H. Kaplan, L. Tessarollo, R.N. Germain, and M.C. Udey. 2012. Cancer-associated epithelial cell adhesion molecule (EpCAM; CD326) enables epidermal Langerhans cell motility and migration in vivo. Proc. Natl. Acad. Sci. USA. 109:E889-E897. http://dx.doi.org/10.1073/pnas.1117674109
20. Geissmann, F., C. Prost, J.P. Monnet, M. Dy, N. Brousse, and O. Hermine. 1998. Transforming growth factor β1, 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. http://dx.doi.org/10.1084/jem.187.6.961
21. Geissmann, F., S. Jung, and D.R. Littman. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity. 19:71-82. http://dx.doi.org/10.1016/S1074-7613(03)00174-2
22. Ghisletti, S., I. Barozzi, F. Mietton, S. Polletti, F. De Santa, E. Venturini, L. Gregory, L. Lonie, A. Chew, C.L. Wei, et al. 2010. Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity. 32:317-328. http://dx.doi.org/10.1016/j.immuni.2010.02.008
23. 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. http://dx.doi.org/10.1038/ni1307
24. + DCs. J. Exp. Med. 206:3115-3130. http://dx.doi.org/10.1084/jem.20091756
25. Greter, M., I. Lelios, P. Pelczar, G. Hoeffel, J. Price, M. Leboeuf, T.M. Kündig, K. Frei, F. Ginhoux, M. Merad, and B. Becher. 2012. Stromaderived interleukin-34 controls the development and maintenance of langerhans cells and the maintenance of microglia. Immunity. 37:1050-1060. http://dx.doi.org/10.1016/j.immuni.2012.11.001
26. Hacker, C., R.D. Kirsch, X.S. Ju, T. Hieronymus, T.C. Gust, C. Kuhl, T. Jorgas, S.M. Kurz, S. Rose-John, Y. Yokota, and M. Zenke. 2003. Transcriptional profiling identifies Id2 function in dendritic cell development. Nat. Immunol. 4:380-386. http://dx.doi.org/10.1038/ni903
27. Hambleton, S., S. Salem, J. Bustamante, V. Bigley, S. Boisson-Dupuis, J. Azevedo, A. Fortin, M. Haniffa, L. Ceron-Gutierrez, C.M. Bacon, et al. 2011. IRF8 mutations and human dendritic-cell immunodeficiency. N. Engl. J. Med. 365:127-138. http://dx.doi.org/10.1056/NEJMoa1100066
28. Hashimoto, D., J. Miller, and M. Merad. 2011. Dendritic cell and macrophage heterogeneity in vivo. Immunity. 35:323-335. http://dx.doi.org/10.1016/j.immuni.2011.09.007
29. Heinz, L.X., B. Platzer, P.M. Reisner, A. Jörgl, S. Taschner, F. Göbel, and H. Strobl. 2006. Differential involvement of PU.1 and Id2 downstream of TGF-beta1 during Langerhans-cell commitment. Blood. 107:1445-1453. http://dx.doi.org/10.1182/blood-2005-04-1721
30. Hildner, K., B.T. Edelson, W.E. Purtha, M. Diamond, H. Matsushita, M. Kohyama, B. Calderon, B.U. Schraml, E.R. Unanue, M.S. Diamond, et al. 2008. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science. 322:1097-1100. http://dx.doi.org/10.1126/science.1164206
31. 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 sac-derived macrophages. J. Exp. Med. 209:1167-1181. http://dx.doi.org/10.1084/jem.20120340
32. Holtschke, T., J. Löhler, Y. Kanno, T. Fehr, N. Giese, F. Rosenbauer, J. Lou, K.P. Knobeloch, L. Gabriele, J.F. Waring, et al. 1996. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell. 87:307-317. http://dx.doi.org/10.1016/S0092-8674(00)81348-3
33. Ito, Y. 2004. Oncogenic potential of the RUNX gene family: 'overview'. Oncogene. 23:4198-4208. http://dx.doi.org/10.1038/sj.onc.1207755
34. Iwama, A., M. Osawa, R. Hirasawa, N. Uchiyama, S. Kaneko, M. Onodera, K. Shibuya, A. Shibuya, C. Vinson, D.G. Tenen, and H. Nakauchi. 2002. Reciprocal roles for CCAAT/enhancer binding protein (C/EBP) and PU.1 transcription factors in Langerhans cell commitment. J. Exp. Med. 195:547-558. http://dx.doi.org/10.1084/jem.20011465
35. Jackson, J.T., Y. Hu, R. Liu, F. Masson, A. D'Amico, S. Carotta, A. Xin, M.J. Camilleri, A.M. Mount, A. Kallies, et al. 2011. Id2 expression delineates differential checkpoints in the genetic program of CD8α+ and CD103+ dendritic cell lineages. EMBO J. 30:2690-2704. http://dx.doi.org/10.1038/emboj.2011.163
36. Jung, S., J. Aliberti, P. Graemmel, M.J. Sunshine, G.W. Kreutzberg, A. Sher, and D.R. Littman. 2000. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 20:4106-4114. http://dx.doi.org/10.1128/MCB.20.11.4106-4114.2000
37. Klein, U., S. Casola, G. Cattoretti, Q. Shen, M. Lia, T. Mo, T. Ludwig, K. Rajewsky, and R. Dalla-Favera. 2006. Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat. Immunol. 7:773-782. http://dx.doi.org/10.1038/ni1357
38. Li, Z., J. Yan, C.J. Matheny, T. Corpora, J. Bravo, A.J. Warren, J.H. Bushweller, and N.A. Speck. 2003. Energetic contribution of residues in the Runx1 Runt domain to DNA binding. J. Biol. Chem. 278:33088-33096. http://dx.doi.org/10.1074/jbc.M303973200
39. Liao, X., N. Sharma, F. Kapadia, G. Zhou, Y. Lu, H. Hong, K. Paruchuri, G.H. Mahabeleshwar, E. Dalmas, N. Venteclef, et al. 2011. Krüppellike factor 4 regulates macrophage polarization. J. Clin. Invest. 121:2736-2749. http://dx.doi.org/10.1172/JCI45444
40. McKenna, H.J., K.L. Stocking, R.E. Miller, K. Brasel, T. De Smedt, E. Maraskovsky, C.R. Maliszewski, D.H. Lynch, J. Smith, B. Pulendran, et al. 2000. Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood. 95:3489-3497.
41. 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. http://dx.doi.org/10.1038/ni852
42. Merad, M., F. Ginhoux, and M. Collin. 2008. Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells. Nat. Rev. Immunol. 8:935-947. http://dx.doi.org/10.1038/nri2455
43. Michaud, J., F. Wu, M. Osato, G.M. Cottles, M. Yanagida, N. Asou, K. Shigesada, Y. Ito, K.F. Benson, W.H. Raskind, et al. 2002. In vitro analyses of known and novel RUNX1/AML1 mutations in dominant familial platelet disorder with predisposition to acute myelogenous leukemia: implications for mechanisms of pathogenesis. Blood. 99:1364-1372. http://dx.doi.org/10.1182/blood.V99.4.1364
44. Mittrücker, H.W., T. Matsuyama, A. Grossman, T.M. Kündig, J. Potter, A. Shahinian, A. Wakeham, B. Patterson, P.S. Ohashi, and T.W. Mak. 1997. Requirement for the transcription factor LSIRF/IRF4 for mature B and T lymphocyte function. Science. 275:540-543. http://dx.doi.org/10.1126/science.275.5299.540
45. Mullen, A.C., D.A. Orlando, J.J. Newman, J. Lovén, R.M. Kumar, S. Bilodeau, J. Reddy, M.G. Guenther, R.P. DeKoter, and R.A. Young. 2011. Master transcription factors determine cell-type-specific responses to TGF-β signaling. Cell. 147:565-576. http://dx.doi.org/10.1016/j.cell.2011.08.050
46. 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. http://dx.doi.org/10.1038/ni.2353
47. Naik, S.H., P. Sathe, H.Y. Park, D. Metcalf, A.I. Proietto, A. Dakic, S. Carotta, M. O'Keeffe, M. Bahlo, A. Papenfuss, et al. 2007. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat. Immunol. 8:1217-1226. http://dx.doi.org/10.1038/ni1522
48. Nutt, S.L., D. Metcalf, A. D'Amico, M. Polli, and L. Wu. 2005. Dynamic regulation of PU.1 expression in multipotent hematopoietic progenitors. J. Exp. Med. 201:221-231. http://dx.doi.org/10.1084/jem.20041535
49. Onai, N., A. Obata-Onai, M.A. Schmid, and M.G. Manz. 2007a. Flt3 in regulation of type I interferon-producing cell and dendritic cell development. Ann. N. Y. Acad. Sci. 1106:253-261. http://dx.doi.org/10.1196/annals.1392.015
50. Onai, N., A. Obata-Onai, M.A. Schmid, T. Ohteki, D. Jarrossay, and M.G. Manz. 2007b. Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat. Immunol. 8:1207-1216. http://dx.doi.org/10.1038/ni1518
51. Sathe, P., J. Pooley, D. Vremec, J. Mintern, J.O. Jin, L. Wu, J.Y. Kwak, J.A. Villadangos, and K. Shortman. 2011. The acquisition of antigen cross-presentation function by newly formed dendritic cells. J. Immunol. 186:5184-5192. http://dx.doi.org/10.4049/jimmunol.1002683
52. Schiavoni, G., F. Mattei, P. Borghi, P. Sestili, M. Venditti, H.C. Morse III, F. Belardelli, and L. Gabriele. 2004. ICSBP is critically involved in the normal development and trafficking of Langerhans cells and dermal dendritic cells. Blood. 103:2221-2228. http://dx.doi.org/10.1182/blood-2003-09-3007
53. Seillet, C., J.T. Jackson, K.A. Markey, H.J. Brady, G.R. Hill, K.P. Macdonald, S.L. Nutt, and G.T. Belz. 2013. CD8α+ DCs can be induced in the absence of transcription factors Id2, Nfil3, and Batf3. Blood. 121:1574-1583. http://dx.doi.org/10.1182/blood-2012-07-445650
54. Seré, K., J.H. Baek, J. Ober-Blöbaum, G. Müller-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. http://dx.doi.org/10.1016/j.immuni.2012.07.019
55. Strobl, H., and W. Knapp. 1999. TGF-beta1 regulation of dendritic cells. Microbes Infect. 1:1283-1290. http://dx.doi.org/10.1016/S1286-4579(99) 00256-7
56. Tripp, C.H., S. Chang-Rodriguez, P. Stoitzner, S. Holzmann, H. Stössel, P. Douillard, S. Saeland, F. Koch, A. Elbe-Bürger, and N. Romani. 2004. Ontogeny of Langerin/CD207 expression in the epidermis of mice. J. Invest. Dermatol. 122:670-672. http://dx.doi.org/10.1111/j.0022-202X.2004.22337.x
57. Tussiwand, R., N. Onai, L. Mazzucchelli, and M.G. Manz. 2005. Inhibition of natural type I IFN-producing and dendritic cell development by a small molecule receptor tyrosine kinase inhibitor with Flt3 affinity. J. Immunol. 175:3674-3680.
58. Wang, Y., K.J. Szretter, W. Vermi, S. Gilfillan, C. Rossini, M. Cella, A.D. Barrow, M.S. Diamond, and M. Colonna. 2012. IL-34 is a tissuerestricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat. Immunol. 13:753-760. http://dx.doi.org/10.1038/ni.2360
59. Waskow, C., K. Liu, G. Darrasse-Jèze, P. Guermonprez, F. Ginhoux, M. Merad, T. Shengelia, K. Yao, and M. Nussenzweig. 2008. The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat. Immunol. 9:676-683. http://dx.doi.org/10.1038/ni.1615
60. Witmer-Pack, M.D., D.A. Hughes, G. Schuler, L. Lawson, A. McWilliam, K. Inaba, R.M. Steinman, and S. Gordon. 1993. Identification of macrophages and dendritic cells in the osteopetrotic (op/op) mouse. J. Cell Sci. 104:1021-1029.