An epigenetic profile of early T-cell development from multipotent progenitors to committed T-cell descendants

European Journal of Immunology

Volumn 44, Issue 4, 2014, Pages 1181-1193

  Vigano, Maria Alessandra ^a   Ivanek, Robert ^a,b   Balwierz, Piotr ^c,d   Berninger, Philipp ^c   van Nimwegen, Erik ^b,c   Karjalainen, Klaus ^e   Rolink, Antonius ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Development; Epigenetics; Genome wide; T cells

Indexed keywords

FLUOROURACIL; INTERLEUKIN 6; INTERLEUKIN 7;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CHROMATIN IMMUNOPRECIPITATION; EPIGENETICS; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE ONTOLOGY; HIGH THROUGHPUT SEQUENCING; HISTONE MODIFICATION; IN VITRO STUDY; LYMPHOID PROGENITOR CELL; MOUSE; NONHUMAN; PRE T LYMPHOCYTE; PRIORITY JOURNAL; PROMOTER REGION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THYMOCYTE;

DEVELOPMENT; EPIGENETICS; GENOME-WIDE; T CELLS;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CLUSTER ANALYSIS; EPIGENESIS, GENETIC; EPIGENOMICS; HEMATOPOIETIC STEM CELLS; HISTONES; LYSINE; METHYLATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPOTENT STEM CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PRECURSOR CELLS, T-LYMPHOID; T-LYMPHOCYTES;

EID: 84897995314     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201344022     Document Type: Article

References (42)

1. Ceredig, R., Rolink, A. G. and Brown, G., Models of haematopoiesis: seeing the wood for the trees. Nat. Rev. Immunol. 2009. 9: 293-300.
2. Seita, J. and Weissman, I. L., Hematopoietic stem cell: self-renewal versus differentiation. Wiley Interdiscip. Rev. Syst. Biol. Med. 2010. 2: 640-653.
3. Kawamoto, H., Ikawa, T., Masuda, K., Wada, H. and Katsura, Y., A map for lineage restriction of progenitors during hematopoiesis: the essence of the myeloid-based model. Immunol. Rev. 2010. 238: 23-36.
4. Bhandoola, A. and Sambandam, A., From stem cell to T cell: one route or many? Nat. Rev. Immunol. 2006. 6: 117-126.
5. Bhandoola, A., von Boehmer, H., Petrie, H. T. and Zuniga-Pflucker, J. C., Commitment and developmental potential of extrathymic and intrathymic T cell precursors: plenty to choose from. Immunity 2007. 26: 678-689.
6. Balciunaite, G., Ceredig, R. and Rolink, A. G., The earliest subpopulation of mouse thymocytes contains potent T, significant macrophage, and natural killer cell but no B-lymphocyte potential. Blood 2005. 105: 1930-1936.
7. Balciunaite, G., Ceredig, R., Fehling, H. J., Zuniga-Pflucker, J. C. and Rolink, A. G., The role of Notch and IL-7 signaling in early thymocyte proliferation and differentiation. Eur. J. Immunol. 2005. 35: 1292-1300.
8. Ceredig, R. and Rolink, A. G., The key role of IL-7 in lymphopoiesis. Semin. Immunol. 2012. 24: 159-164.
9. Radtke, F., Fasnacht, N. and Macdonald, H. R., Notch signaling in the immune system. Immunity 2010. 32: 14-27.
10. Radtke, F., Ferrero, I., Wilson, A., Lees, R., Aguet, M. and MacDonald, H. R., Notch1 deficiency dissociates the intrathymic development of dendritic cells and T cells. J. Exp. Med. 2000. 191: 1085-1094.
11. Mohn, F. and Schubeler, D., Genetics and epigenetics: stability and plasticity during cellular differentiation. Trends Genet. 2009. 25: 129-136.
12. Barrero, M. J., Boue, S. and Izpisua Belmonte, J. C., Epigenetic mechanisms that regulate cell identity. Cell Stem Cell 2010. 7: 565-570.
13. Zhou, V. W., Goren, A. and Bernstein, B. E., Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 2011. 12: 7-18.
14. Pekowska, A., Benoukraf, T., Zacarias-Cabeza, J., Belhocine, M., Koch, F., Holota, H., Imbert, J. et al., H3K4 tri-methylation provides an epigenetic signature of active enhancers. EMBO J. 2011. 30: 4198-4210.
15. de Gobbi, M., Garrick, D., Lynch, M., Vernimmen, D., Hughes, J. R., Goardon, N., Luc, S. et al., Generation of bivalent chromatin domains during cell fate decisions. Epigenetics Chromatin 2011. 4: 9. DOI: 10.1186/1756-8935-4-9.
16. Adli, M., Zhu, J. and Bernstein, B. E., Genome-wide chromatin maps derived from limited numbers of hematopoietic progenitors. Nat. Methods 2010. 7: 615-618.
17. Wong, P., Hattangadi, S. M., Cheng, A. W., Frampton, G. M., Young, R. A. and Lodish, H. F., Gene induction and repression during terminal erythropoiesis are mediated by distinct epigenetic changes. Blood 2011. 118: e128-e138.
18. Wei, G., Wei, L., Zhu, J., Zang, C., Hu-Li, J., Yao, Z., Cui, K. et al., Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4 +T cells. Immunity 2009. 30: 155-167.
19. Cedar, H. and Bergman, Y., Epigenetics of haematopoietic cell development. Nat. Rev. Immunol. 2011. 11: 478-488.
20. Zhang, J. A., Mortazavi, A., Williams, B. A., Wold, B. J. and Rothenberg, E. V., Dynamic transformations of genome-wide epigenetic marking and transcriptional control establish T cell identity. Cell 2012. 149: 467-482.
21. Ruedl, C., Khameneh, H. J. and Karjalainen, K., Manipulation of immune system via immortal bone marrow stem cells. Int. Immunol. 2008. 20: 1211-1218.
22. Ikawa, T., Hirose, S., Masuda, K., Kakugawa, K., Satoh, R., Shibano-Satoh, A., Kominami, R. et al., An essential developmental checkpoint for production of the T cell lineage. Science 2010. 329: 93-96.
23. Tussiwand, R., Engdahl, C., Gehre, N., Bosco, N., Ceredig, R. and Rolink, A. G., The preTCR-dependent DN3 to DP transition requires Notch signaling, is improved by CXCL12 signaling and is inhibited by IL-7 signaling. Eur. J. Immunol. 2011. 41: 3371-3380.
24. Mingueneau, M., Kreslavsky, T., Gray, D., Heng, T., Cruse, R., Ericson, J., Bendall, S. et al., The transcriptional landscape of alphabeta T cell differentiation. Nat. Immunol. 2013. 14: 619-632.
25. Chambers, S. M., Boles, N. C., Lin, K. Y., Tierney, M. P., Bowman, T. V., Bradfute, S. B., Chen, A. J. et al., Hematopoietic fingerprints: an expression database of stem cells and their progeny. Cell Stem Cell 2007. 1: 578-591.
26. Miranda-Saavedra, D. and Gottgens, B., Transcriptional regulatory networks in haematopoiesis. Curr. Opin. Genet. Dev. 2008. 18: 530-535.
27. Porritt, H. E., Rumfelt, L. L., Tabrizifard, S., Schmitt, T. M., Zuniga-Pflucker, J. C. and Petrie, H. T., Heterogeneity among DN1 prothymocytes reveals multiple progenitors with different capacities to generate T cell and non-T cell lineages. Immunity 2004. 20: 735-745.
28. Rothenberg, E. V., Moore, J. E. and Yui, M. A., Launching the T-cell-lineage developmental programme. Nat. Rev. Immunol. 2008. 8: 9-21.
29. Jojic, V., Shay, T., Sylvia, K., Zuk, O., Sun, X., Kang, J., Regev, A. et al., Identification of transcriptional regulators in the mouse immune system. Nat. Immunol. 2013. 14: 633-643.
30. Balwierz, P. J., Carninci, P., Daub, C. O., Kawai, J., Hayashizaki, Y., van Belle, W., Beisel, C. et al., Methods for analyzing deep sequencing expression data: constructing the human and mouse promoterome with deepCAGE data. Genome. Biol. 2009. 10: R79. DOI: 10.1186/gb-2009-10-7-r79.
31. Mohn, F., Weber, M., Rebhan, M., Roloff, T. C., Richter, J., Stadler, M. B., Bibel, M. et al., Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell 2008. 30: 755-766.
32. Weishaupt, H., Sigvardsson, M. and Attema, J. L., Epigenetic chromatin states uniquely define the developmental plasticity of murine hematopoietic stem cells. Blood 2010. 115: 247-256.
33. Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P. et al., Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007. 448: 553-560.
34. Cui, K., Zang, C., Roh, T. Y., Schones, D. E., Childs, R. W., Peng, W. and Zhao, K., Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 2009. 4: 80-93.
35. Naito, T., Tanaka, H., Naoe, Y. and Taniuchi, I., Transcriptional control of T-cell development. Int. Immunol. 2011. 23: 661-668.
36. Arnold, P., Scholer, A., Pachkov, M., Balwierz, P. J., Jorgensen, H., Stadler, M. B., van Nimwegen, E. et al., Modeling of epigenome dynamics identifies transcription factors that mediate Polycomb targeting. Genome Res. 2013. 23: 60-73.
37. Jhunjhunwala, S., van Zelm, M. C., Peak, M. M. and Murre, C., Chromatin architecture and the generation of antigen receptor diversity. Cell 2009. 138: 435-448.
38. Krangel, M. S., T cell development: better living through chromatin. Nat. Immunol. 2007. 8: 687-694.
39. Schlenner, S. M., Madan, V., Busch, K., Tietz, A., Laufle, C., Costa, C., Blum, C. et al., Fate mapping reveals separate origins of T cells and myeloid lineages in the thymus. Immunity 2010. 32: 426-436.
40. Lenhard, B., Sandelin, A. and Carninci, P., Metazoan promoters: emerging characteristics and insights into transcriptional regulation. Nat. Rev. Genet. 2012. 13: 233-245.
41. Hawkins, R. D., Hon, G. C., Lee, L. K., Ngo, Q., Lister, R., Pelizzola, M., Edsall, L. E. et al., Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 2010. 6: 479-491.
42. Vigano, M. A., Lamartine, J., Testoni, B., Merico, D., Alotto, D., Castagnoli, C., Robert, A. et al., New p63 targets in keratinocytes identified by a genome-wide approach. EMBO J. 2006. 25: 5105-5116.