ETO family protein Mtg16 regulates the balance of dendritic cell subsets by repressing Id2

Journal of Experimental Medicine

Volumn 211, Issue 8, 2014, Pages 1623-1635

  Ghosh, Hiyaa S ^a   Ceribelli, Michele ^d   Matos, Ines ^a   Lazarovici, Allan ^a,c   Bussemaker, Harmen J ^a   Lasorella, Anna ^a,b   Hiebert, Scott W ^e   Liu, Kang ^a   Staudt, Louis M ^d   Reizis, Boris ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NewYork Presbyterian Hospital   (United States)

^c Institute for Cancer Genetics Columbia University ^*  (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD8 ANTIGEN; INHIBITOR OF DIFFERENTIATION 2; INTERFERON; PROTEIN ETO; PROTEIN MTG16; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; CELL SUBPOPULATION; CONTROLLED STUDY; DENDRITIC CELL; EMBRYO; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREGULATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY;

ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; CHROMATIN; DENDRITIC CELLS; E2F2 TRANSCRIPTION FACTOR; GENE DELETION; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 2; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; REPRESSOR PROTEINS; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 84905093427     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20132121     Document Type: Article

References (53)

1. Allman, D., M. Dalod, C. Asselin-Paturel, T. Delale, S.H. Robbins, G. Trinchieri, C.A. Biron, P. Kastner, and S. Chan. 2006. Ikaros is required for plasmacytoid dendritic cell differentiation. Blood. 108:4025-4034. http://dx.doi.org/10.1182/blood-2006-03-007757.
2. Andersson, R., C. Gebhard, I. Miguel-Escalada, I. Hoof, J. Bornholdt, M. Boyd, Y. Chen, X. Zhao, C. Schmidl, T. Suzuki, et al. FANTOM Consortium. 2014. An atlas of active enhancers across human cell types and tissues. Nature. 507:455-461. http://dx.doi.org/10.1038/nature12787.
3. Asselin-Paturel, C., G. Brizard, K. Chemin, A. Boonstra, A. O'Garra, A. Vicari, and G. Trinchieri. 2005. Type I interferon dependence of plasmacytoid dendritic cell activation and migration. J. Exp. Med. 201:1157-1167. http://dx.doi.org/10.1084/jem.20041930.
4. + dendritic cells are a steady-state population related to plasmacytoid dendritic cells. Proc. Natl. Acad. Sci. USA. 107:14745-14750. http://dx.doi.org/10.1073/pnas.1001562107.
5. Belnoue, E., P. Fontannaz, A.F. Rochat, C. Tougne, A. Bergthaler, P.H. Lambert, D.D. Pinschewer, and C.A. Siegrist. 2013. Functional limitations of plasmacytoid dendritic cells limit type I interferon, T cell responses and virus control in early life. PLoS ONE. 8:e85302. http://dx.doi.org/10.1371/journal.pone.0085302.
6. Bhattacharya, A., and N.E. Baker. 2011. A network of broadly expressed HLH genes regulates tissue-specific cell fates. Cell. 147:881-892. http://dx.doi .org/10.1016/j.cell.2011.08.055.
7. Boos, M.D., Y. Yokota, G. Eberl, and B.L. Kee. 2007. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. J. Exp. Med. 204:1119-1130. http://dx.doi.org/10.1084/jem.20061959.
8. Chaperot, L., A. Blum, O. Manches, G. Lui, J. Angel, J.P. Molens, and J. Plumas. 2006. Virus or TLR agonists induce TRAIL-mediated cytotoxic activity of plasmacytoid dendritic cells. J. Immunol. 176:248-255. http://dx.doi.org/10 .4049/jimmunol.176.1.248.
9. Chyla, B.J., I. Moreno-Miralles, M.A. Steapleton, M.A. Thompson, S. Bhaskara, M. Engel, and S.W. Hiebert. 2008. Deletion of Mtg16, a target of t(16;21), alters hematopoietic progenitor cell proliferation and lineage allocation. Mol. Cell. Biol. 28:6234-6247. http://dx.doi.org/10.1128/MCB.00404-08.
10. Cisse, B., M.L. Caton, M. Lehner, T. Maeda, S. Scheu, R. Locksley, D. Holmberg, C. Zweier, N.S. den Hollander, S.G. Kant, et al. 2008. Transcription factor E2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell. 135:37-48. http://dx.doi.org/10.1016/j.cell.2008.09.016.
11. Dakic, A., Q.X. Shao, A. D'Amico, M. O'Keeffe, W.F. Chen, K. Shortman, and L. Wu. 2004. Development of the dendritic cell system during mouse ontogeny. J. Immunol. 172:1018-1027. http://dx.doi.org/10.4049/jimmunol.172.2.1018.
12. Fischer, M.A., I. Moreno-Miralles, A. Hunt, B.J. Chyla, and S.W. Hiebert. 2012. Myeloid translocation gene 16 is required for maintenance of haematopoietic stem cell quiescence. EMBO J. 31:1494-1505. http://dx.doi.org/10.1038/emboj.2011.500.
13. Foat, B.C., A.V. Morozov, and H.J. Bussemaker. 2006. Statistical mechanical modeling of genome-wide transcription factor occupancy data by MatrixREDUCE. Bioinformatics. 22:e141-e149. http://dx.doi.org/10.1093/bioinformatics/btl223.
14. Geissmann, F., M.G. Manz, S. Jung, M.H. Sieweke, M. Merad, and K. Ley. 2010. Development of monocytes, macrophages, and dendritic cells. Science. 327:656-661. http://dx.doi.org/10.1126/science.1178331.
15. Ghosh, H.S., B. Cisse, A. Bunin, K.L. Lewis, and B. Reizis. 2010. Continuous expression of the transcription factor e2-2 maintains the cell fate of mature plasmacytoid dendritic cells. Immunity. 33:905-916. http://dx.doi .org/10.1016/j.immuni.2010.11.023.
16. + DCs. J. Exp. Med. 206:3115-3130. http://dx.doi.org/10.1084/jem.20091756.
17. Guo, C., Q. Hu, C. Yan, and J. Zhang. 2009. Multivalent binding of the ETO corepressor to E proteins facilitates dual repression controls targeting chromatin and the basal transcription machinery. Mol. Cell. Biol. 29:2644-2657. http://dx.doi.org/10.1128/MCB.00073-09.
18. 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.
19. Haniffa, M., M. Collin, and F. Ginhoux. 2013. Ontogeny and functional specialization of dendritic cells in human and mouse. Adv. Immunol. 120:1-49. http://dx.doi.org/10.1016/B978-0-12-417028-5.00001-6.
20. Hunt, A., M. Fischer, M.E. Engel, and S.W. Hiebert. 2011. Mtg16/Eto2 contributes to murine T-cell development. Mol. Cell. Biol. 31:2544-2551. http://dx.doi.org/10.1128/MCB.01458-10.
21. + dendritic cell lineages. EMBO J. 30:2690-2704. http://dx.doi .org/10.1038/emboj.2011.163.
22. Jones-Mason, M.E., X. Zhao, D. Kappes, A. Lasorella, A. Iavarone, and Y. Zhuang. 2012. E protein transcription factors are required for the development of CD4+ lineage T cells. Immunity. 36:348-361. http://dx.doi .org/10.1016/j.immuni.2012.02.010.
23. Jung, S., J. Aliberti, P. Graemmel, M.J. Sunshine, G.W. Kreutzberg, A. Sher, and D.R. Littman. 2000. Analysis of fractalkine receptor CX3CR1 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.
24. Karrich, J.J., M. Balzarolo, H. Schmidlin, M. Libouban, M. Nagasawa, R. Gentek, S. Kamihira, T. Maeda, D. Amsen, M.C. Wolkers, and B. Blom. 2012. The transcription factor Spi-B regulates human plasmacytoid dendritic cell survival through direct induction of the antiapoptotic gene BCL2-A1. Blood. 119:5191-5200. http://dx.doi.org/10.1182/blood-2011-07-370239.
25. Kee, B.L. 2009. E and ID proteins branch out. Nat. Rev. Immunol. 9:175-184. http://dx.doi.org/10.1038/nri2507.
26. 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. http://dx.doi.org/10 .1016/j.immuni.2011.08.013.
27. Liu, K., G.D. Victora, T.A. Schwickert, P. Guermonprez, M.M. Meredith, K. Yao, F.F. Chu, G.J. Randolph, A.Y. Rudensky, and M. Nussenzweig. 2009. In vivo analysis of dendritic cell development and homeostasis. Science. 324:392-397.
28. Liu, Y.J. 2005. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 23:275-306. http://dx.doi.org/10.1146/annurev.immunol.23.021704.115633.
29. Maeda, T., K. Murata, T. Fukushima, K. Sugahara, K. Tsuruda, M. Anami, Y. Onimaru, K. Tsukasaki, M. Tomonaga, R. Moriuchi, et al. 2005. A novel plasmacytoid dendritic cell line, CAL-1, established from a patient with blastic natural killer cell lymphoma. Int. J. Hematol. 81:148-154. http://dx.doi.org/10.1532/IJH97.04116.
30. 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. http://dx.doi.org/10.1146/annurev-immunol-020711-074950.
31. Miller, J.C., B.D. Brown, T. Shay, E.L. Gautier, V. Jojic, A. Cohain, G. Pandey, M. Leboeuf, K.G. Elpek, J. Helft, et al. Immunological Genome Consortium. 2012. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13:888-899. http://dx.doi.org/10.1038/ni.2370.
32. Murre, C. 2005. Helix-loop-helix proteins and lymphocyte development. Nat. Immunol. 6:1079-1086. http://dx.doi.org/10.1038/ni1260.
33. Nagasawa, M., H. Schmidlin, M.G. Hazekamp, R. Schotte, and B. Blom. 2008. Development of human plasmacytoid dendritic cells depends on the combined action of the basic helix-loop-helix factor E2-2 and the Ets factor Spi-B. Eur. J. Immunol. 38:2389-2400. http://dx.doi.org/10 .1002/eji.200838470.
34. - dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J. Immunol. 174:6592-6597. http://dx.doi.org/10.4049/jimmunol.174.11.6592.
35. Naik, S.H., D. Metcalf, A. van Nieuwenhuijze, I. Wicks, L. Wu, M. O'Keeffe, and K. Shortman. 2006. Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat. Immunol. 7:663-671. http://dx.doi.org/10.1038/ni1340.
36. 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.
37. Naik, S.H., L. Perié, E. Swart, C. Gerlach, N. van Rooij, R.J. de Boer, and T.N. Schumacher. 2013. Diverse and heritable lineage imprinting of early haematopoietic progenitors. Nature. 496:229-232. http://dx.doi .org/10.1038/nature12013.
38. + plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat. Immunol. 8:1207-1216. http://dx.doi.org/10.1038/ni1518.
39. Onai, N., K. Kurabayashi, M. Hosoi-Amaike, N. Toyama-Sorimachi, K. Matsushima, K. Inaba, and T. Ohteki. 2013. A clonogenic progenitor with prominent plasmacytoid dendritic cell developmental potential. Immunity. 38:943-957. http://dx.doi.org/10.1016/j.immuni.2013.04.006.
40. Reizis, B., A. Bunin, H.S. Ghosh, K.L. Lewis, and V. Sisirak. 2011a. Plasmacytoid dendritic cells: recent progress and open questions. Annu. Rev. Immunol. 29:163-183. http://dx.doi.org/10.1146/annurev-immunol-031210-101345.
41. Reizis, B., M. Colonna, G. Trinchieri, F. Barrat, and M. Gilliet. 2011b. Plasmacytoid dendritic cells: one-trick ponies or workhorses of the immune system? Nat. Rev. Immunol. 11:558-565. http://dx.doi.org/10.1038/nri3027.
42. Sathaliyawala, T., W.E. O'Gorman, M. Greter, M. Bogunovic, V. Konjufca, Z.E. Hou, G.P. Nolan, M.J. Miller, M. Merad, and B. Reizis. 2010. Mammalian target of rapamycin controls dendritic cell development downstream of Flt3 ligand signaling. Immunity. 33:597-606. http://dx.doi.org/10.1016/j.immuni.2010.09.012.
43. Sathe, P., D. Vremec, L. Wu, L. Corcoran, and K. Shortman. 2013. Convergent differentiation: myeloid and lymphoid pathways to murine plasmacytoid dendritic cells. Blood. 121:11-19. http://dx.doi.org/10.1182/blood-2012-02-413336.
44. Satpathy, A.T., W. Kc, J.C. Albring, B.T. Edelson, N.M. Kretzer, D. Bhattacharya, T.L. Murphy, and K.M. Murphy. 2012a. Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 209:1135-1152. http://dx.doi.org/10.1084/jem.20120030.
45. Satpathy, A.T., X. Wu, J.C. Albring, and K.M. Murphy. 2012b. Re(de)fining the dendritic cell lineage. Nat. Immunol. 13:1145-1154. http://dx.doi .org/10.1038/ni.2467.
46. Sawai, C.M., V. Sisirak, H.S. Ghosh, E.Z. Hou, M. Ceribelli, L.M. Staudt, and B. Reizis. 2013. Transcription factor Runx2 controls the development and migration of plasmacytoid dendritic cells. J. Exp. Med. 210:2151-2159. http://dx.doi.org/10.1084/jem.20130443.
47. Sepp, M., K. Kannike, A. Eesmaa, M. Urb, and T. Timmusk. 2011. Functional diversity of human basic helix-loop-helix transcription factor TCF4 isoforms generated by alternative 5' exon usage and splicing. PLoS ONE. 6:e22138. http://dx.doi.org/10.1371/journal.pone.0022138.
48. Soler, E., C. Andrieu-Soler, E. de Boer, J.C. Bryne, S. Thongjuea, R. Stadhouders, R.J. Palstra, M. Stevens, C. Kockx, W. van Ijcken, et al. 2010. The genome-wide dynamics of the binding of Ldb1 complexes during erythroid differentiation. Genes Dev. 24:277-289. http://dx.doi.org/10.1101/gad.551810.
49. + stem cells into predendritic cell (pre-DC)2 but not into pre-DC1. Evidence for a lymphoid origin of pre-DC2. J. Exp. Med. 192:1775-1784. http://dx.doi.org/10 .1084/jem.192.12.1775.
50. Spyrou, C., R. Stark, A.G. Lynch, and S. Tavaré. 2009. BayesPeak: Bayesian analysis of ChIP-seq data. BMC Bioinformatics. 10:299. http://dx.doi.org/10.1186/1471-2105-10-299.
51. Steinman, R.M. 2012. Decisions about dendritic cells: past, present, and future. Annu. Rev. Immunol. 30:1-22. http://dx.doi.org/10.1146/annurevimmunol-100311-102839.
52. Weirauch, M.T., A. Cote, R. Norel, M. Annala, Y. Zhao, T.R. Riley, J. Saez-Rodriguez, T. Cokelaer, A. Vedenko, S. Talukder, et al. DREAM5 Consortium. 2013. Evaluation of methods for modeling transcription factor sequence specificity. Nat. Biotechnol. 31:126-134. http://dx.doi .org/10.1038/nbt.2486.
53. Zhang, J., M. Kalkum, S. Yamamura, B.T. Chait, and R.G. Roeder. 2004. E protein silencing by the leukemogenic AML1-ETO fusion protein. Science. 305:1286-1289. http://dx.doi.org/10.1126/science.1097937.