Transcription factor EBF1 is essential for the maintenance of B cell identity and prevention of alternative fates in committed cells
Abstract
The transcription factors EBF1 and Pax5 have been linked to activation of the B cell lineage program and irreversible loss of alternative lineage potential (commitment), respectively. Here we conditionally deleted Ebf1 in committed pro-B cells after transfer into alymphoid mice. We found that those cells converted into innate lymphoid cells (ILCs) and T cells with variable-diversity-joining (VDJ) rearrangements of loci encoding both B cell and T cell antigen receptors. As intermediates in lineage conversion, Ebf1-deficient CD19(+) cells expressing Pax5 and transcriptional regulators of the ILC and T cell fates were detectable. In particular, genes encoding the transcription factors Id2 and TCF-1 were bound and repressed by EBF1. Thus, both EBF1 and Pax5 are required for B lineage commitment by repressing distinct and common determinants of alternative cell fates.
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Loss of master regulators, such as Pax5 in B cells, can cause plasticity and even cancer.
“Their loss, for example, Pax5 in B cells, can cause plasticity and even cancer6,7,55,56.”
From Active repression of cell fate plasticity by PROX1 safeguards hepatocyte identity and prevents liver tumorigenesis (2025) · cites this paper as [56]
Cites
Innate lymphoid cells — a proposal for uniform nomenclature
Spits, H., Artis, D., Colonna, M., Diefenbach, A., Disanto, J. D., Eberl, G., Koyasu, S., Locksley, R., McKenzie, A., Mebius, R., et al. (2013) · Nature reviews. Immunology · doi:10.1038/nri3365 · Cited by 2,380 · see citing works
Self-citationInnate production of TH2 cytokines by adipose tissue-associated c-Kit+Sca-1+ lymphoid cells
Moro, K., Yamada, T., Tanabe, M., Takeuchi, T., Ikawa, T., Kawamoto, H., Furusawa, J.-I., Ohtani, M., Fujii, H., & Koyasu, S. (2009) · Nature · doi:10.1038/nature08636 · Cited by 1,994 · see citing works
The Immunological Genome Project: networks of gene expression in immune cells
The Immunological Genome Project Consortium, Heng, T. S. P., Painter, M. W., Elpek, K., Lukacs-Kornek, V., Mauermann, N., Turley, S. J., Koller, D., Kim, F. S., Wagers, A. J., et al. (2008) · Nature Immunology · doi:10.1038/ni1008-1091 · Cited by 1,864 · see citing works
Identification of Flt3+ Lympho-Myeloid Stem Cells Lacking Erythro-Megakaryocytic Potential
Adolfsson, J., Månsson, R., Buza-Vidas, N., Hultquist, A., Liuba, K., Jensen, C. T., Bryder, D., Yang, L., Borge, O. J., Thorén, L., et al. (2005) · Cell · doi:10.1016/j.cell.2005.02.013 · Cited by 1,229 · see citing works
Commitment to the B-lymphoid lineage depends on the transcription factor Pax5
Nutt, S. L., Heavey, B., Rolink, A. G., & Busslinger, M. (1999) · Nature · doi:10.1038/44076 · Cited by 1,179 · see citing works
The Transcription Factor GATA-3 Controls Cell Fate and Maintenance of Type 2 Innate Lymphoid Cells
Hoyler, T., Klose, C. S. N., Souabni, A., Turqueti‐Neves, A., Pfeifer, D., Rawlins, E. L., Voehringer, D., Busslinger, M., & Diefenbach, A. (2012) · Immunity · doi:10.1016/j.immuni.2012.06.020 · Cited by 855 · see citing works
Self-citationYokota, Y., Mansouri, A., Mori, S., Sugawara, S., Adachi, S., Nishikawa, S., & Gruß, P. (1999) · Nature · doi:10.1038/17812 · Cited by 851 · see citing works
Testing gene function early in the B cell lineage in mb1-cre mice
Hobeika, E., Thiemann, S., Storch, B., Jumaa, H., Nielsen, P. J., Pelanda, R., & Reth, M. G. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605944103 · Cited by 581 · see citing works
Lin, Y. C., Jhunjhunwala, S., Benner, C. W., Heinz, S., Welinder, E., Månsson, R., Sigvardsson, M., Hagman, J. R., Espinoza, C. A., Dutkowski, J., et al. (2010) · Nature Immunology · doi:10.1038/ni.1891 · Cited by 502 · see citing works
Conversion of mature B cells into T cells by dedifferentiation to uncommitted progenitors
Cobaleda, C., Jochum, W., & Busslinger, M. (2007) · Nature · doi:10.1038/nature06159 · Cited by 502 · see citing works
Transcription from the RAG1 Locus Marks the Earliest Lymphocyte Progenitors in Bone Marrow
Igarashi, H., Gregory, S. C., Yokota, T., Sakaguchi, N., & Kincade, P. W. (2002) · Immunity · doi:10.1016/s1074-7613(02)00366-7 · Cited by 452 · see citing works
A critical role for TCF-1 in T-lineage specification and differentiation
Weber, B., Chi, A. W. S., Chavez, A., Yashiro–Ohtani, Y., Yang, Q., Shestova, O. E., & Bhandoola, A. (2011) · Nature · doi:10.1038/nature10279 · Cited by 420 · see citing works
Pax5 induces V -to- DJ rearrangements and locus contraction of the immunoglobulin heavy-chain genePreprint
Fuxa, M., Skok, J. A., Souabni, A., Salvagiotto, G., Roldán, E., & Busslinger, M. (2004) · Genes & Development · doi:10.1101/gad.291504 · Cited by 414 · see citing works
Long-term in vivo reconstitution of T-cell development by Pax5-deficient B-cell progenitors
Rolink, A. G., Nutt, S. L., Melchers, F., & Busslinger, M. (1999) · Nature · doi:10.1038/44164 · Cited by 386 · see citing works
The Transcriptional Regulation of B Cell Lineage Commitment
Nutt, S. L., & Kee, B. L. (2007) · Immunity · doi:10.1016/j.immuni.2007.05.010 · Cited by 384 · see citing works
Delogu, A., Schebesta, A., Sun, Q., Aschenbrenner, K., Perlot, T., & Busslinger, M. (2006) · Immunity · doi:10.1016/j.immuni.2006.01.012 · Cited by 366 · see citing works
Notch signaling controls the generation and differentiation of early T lineage progenitors
Sambandam, A., Maillard, I. P., Zediak, V. P., Xu, L., Gerstein, R. M., Aster, J. C., Pear, W. S., & Bhandoola, A. (2005) · Nature Immunology · doi:10.1038/ni1216 · Cited by 364 · see citing works
Distinct functions for the transcription factor Foxo1 at various stages of B cell differentiation
Dengler, H. S., Baracho, G. V., Omori, S. A., Bruckner, S. R., Arden, K. C., Castrillón, D. H., DePinho, R. A., & Rickert, R. C. (2008) · Nature Immunology · doi:10.1038/ni.1667 · Cited by 354 · see citing works
Inlay, M. A., Bhattacharya, D., Sahoo, D., Serwold, T. F., Seita, J., Karsunky, H., Plevritis, S. K., Dill, D. L., & Weissman, I. L. (2009) · Genes & Development · doi:10.1101/gad.1836009 · Cited by 319 · see citing works
Reversion of B Cell Commitment upon Loss of Pax5 Expression
Mikkola, I., Heavey, B., Horcher, M., & Busslinger, M. (2002) · Science · doi:10.1126/science.1067518 · Cited by 291 · see citing works
Regulation of B cell fate commitment and immunoglobulin heavy-chain gene rearrangements by Ikaros
Reynaud, D., Demarco, I. A., Reddy, K. L., Schjerven, H., Bertolino, E., Chen, Z., Smale, S. T., Winandy, S., & Singh, H. (2008) · Nature Immunology · doi:10.1038/ni.1626 · Cited by 261 · see citing works
Pongubala, J. M. R., Northrup, D. L., Lancki, D. W., Medina, K. L., Treiber, T., Bertolino, E., Thomas, M., Grosschedl, R., Allman, D., & Singh, H. (2008) · Nature Immunology · doi:10.1038/ni1555 · Cited by 250 · see citing works
Self-citationNg, S. Y., Yoshida, T., Zhang, J., & Georgopoulos, K. (2009) · Immunity · doi:10.1016/j.immuni.2009.01.014 · Cited by 245 · see citing works
Assembling a Gene Regulatory Network for Specification of the B Cell Fate
Medina, K. L., Pongubala, J. M. R., Reddy, K. L., Lancki, D. W., DeKoter, R. P., Kieslinger, M., Grosschedl, R., & Singh, H. (2004) · Developmental Cell · doi:10.1016/j.devcel.2004.08.006 · Cited by 240 · see citing works
Self-citationTreiber, T., Mandel, E. M., Pott, S., Győry, I., Firner, S., Liu, E. T., & Grosschedl, R. (2010) · Immunity · doi:10.1016/j.immuni.2010.04.013 · Cited by 235 · see citing works
Self-citationT-cell factor 1 is a gatekeeper for T-cell specification in response to Notch signaling
Germar, K., Dose, M., Konstantinou, T., Zhang, J., Wang, H., Lobry, C., Arnett, K. L., Blacklow, S. C., Aifantis, I., Aster, J. C., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110230108 · Cited by 219 · see citing works
Decker, T., di Magliano, M. P., McManus, S., Sun, Q., Bonifer, C., Tagoh, H., & Busslinger, M. (2009) · Immunity · doi:10.1016/j.immuni.2009.01.012 · Cited by 194 · see citing works
Role of Deltex-1 as a Transcriptional Regulator Downstream of the Notch Receptor
Yamamoto, N., Yamamoto, S.-I., Inagaki, F. F., Kawaichi, M., Fukamizu, A., Kishi, N., Matsuno, K., Nakamura, K., Weinmaster, G., Okano, H., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m105245200 · Cited by 189 · see citing works
Distinct Promoters Mediate the Regulation of Ebf1 Gene Expression by Interleukin-7 and Pax5
Roessler, S. K., Győry, I., Imhof, S., Spivakov, M., Williams, R. R. E., Busslinger, M., Fisher, A. G., & Grosschedl, R. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01192-06 · Cited by 175 · see citing works
Self-citationSeet, C. S., Brumbaugh, R. L., & Kee, B. L. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20032202 · Cited by 168 · see citing works
A Robust and Highly Efficient Immune Cell Reprogramming System
Bussmann, L. H., Schubert, A., Manh, T. V., de Andrés-Aguayo, L., Desbordes, S. C., Parra, M., Zimmermann, T., Rapino, F. A., Rodríguez‐Ubreva, J., Ballestar, E., et al. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.10.004 · Cited by 162 · see citing works
Győry, I., Boller, S., Nechanitzky, R., Mandel, E. M., Pott, S., Liu, E., & Grosschedl, R. (2012) · Genes & Development · doi:10.1101/gad.187328.112 · Cited by 158 · see citing works
Self-citationMcManus, S., Ebert, A., Salvagiotto, G., Medvedovic, J., Sun, Q., Tamir, I., Jaritz, M., Tagoh, H., & Busslinger, M. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.140 · Cited by 151 · see citing works
Mercer, E. M., Lin, Y. C., Benner, C. W., Jhunjhunwala, S., Dutkowski, J., Flores, M., Sigvardsson, M., Ideker, T. E., Glass, C. K., & Murre, C. (2011) · Immunity · doi:10.1016/j.immuni.2011.06.013 · Cited by 139 · see citing works
Essential role of EBF1 in the generation and function of distinct mature B cell types
Vilagos, B., Hoffmann, M., Souabni, A., Sun, Q., Werner, B., Medvedovic, J., Bilić, I., Minnich, M., Axelsson, E., Jaritz, M., et al. (2012) · The Journal of Experimental Medicine · doi:10.1084/jem.20112422 · Cited by 138 · see citing works
Transcription control of early B cell differentiation
Mandel, E. M., & Grosschedl, R. (2010) · Current Opinion in Immunology · doi:10.1016/j.coi.2010.01.010 · Cited by 125 · see citing works
Self-citationMånsson, R., Zandi, S., Welinder, E., Tsapogas, P., Sakaguchi, N., Bryder, D., & Sigvardsson, M. (2009) · Blood · doi:10.1182/blood-2009-08-236398 · Cited by 124 · see citing works
Positive intergenic feedback circuitry, involving EBF1 and FOXO1, orchestrates B-cell fate
Månsson, R., Welinder, E., Åhsberg, J., Lin, Y. C., Benner, C. W., Glass, C. K., Lucas, J., Sigvardsson, M., & Murre, C. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211427109 · Cited by 109 · see citing works
Tullio, A. D., Manh, T. V., Schubert, A., Castellano, G., Månsson, R., & Graf, T. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1112169108 · Cited by 109 · see citing works
GATA-3 promotes T-cell specification by repressing B-cell potential in pro–T cells in mice
García‐Ojeda, M. E., Wolterink, R. G. J. K., Lemaı̂tre, F., Goff, O. R.-L., Hasan, M., Hendriks, R. W., Cumano, A., & Santo, J. P. D. (2013) · Blood · doi:10.1182/blood-2012-06-440065 · Cited by 105 · see citing works
Ebf1-mediated down-regulation of Id2 and Id3 is essential for specification of the B cell lineage
Thal, M. A., Carvalho, T. L., He, T., Kim, H., Gao, H., Hagman, J. R., & Klug, C. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802550106 · Cited by 93 · see citing works
T Cell Lineage Commitment: Identity and Renunciation
Rothenberg, E. V. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003703 · Cited by 90 · see citing works
Transcriptional drivers of the T-cell lineage program
Rothenberg, E. V. (2012) · Current Opinion in Immunology · doi:10.1016/j.coi.2011.12.012 · Cited by 80 · see citing works
Developmental plasticity of lymphocytes
Cobaleda, C., & Busslinger, M. (2008) · Current Opinion in Immunology · doi:10.1016/j.coi.2008.03.017 · Cited by 57 · see citing works
Early B Cell Factor 2 Regulates Hematopoietic Stem Cell Homeostasis in a Cell-Nonautonomous Manner
Kieslinger, M., Hiechinger, S., Dobreva, G. D., Consalez, G. G., & Grosschedl, R. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.07.015 · Cited by 56 · see citing works
Self-citationFunctional diversity of stem and progenitor cells with B‐lymphopoietic potential
Ichii, M., Shimazu, T., Welner, R. S., Garrett, K. P., Zhang, Q., Esplin, B. L., & Kincade, P. W. (2010) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00933.x · Cited by 48 · see citing works
Zandi, S., Åhsberg, J., Tsapogas, P., Stjernberg, J., Qian, H., & Sigvardsson, M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210144109 · Cited by 39 · see citing works
A dose‐dependent role for EBF1 in repressing non‐B‐cell‐specific genes
Lukin, K., Fields, S., Guerrettaz, L., Straign, D. M., Rodriguez, V., Zandi, S., Månsson, R., Cambier, J. C., Sigvardsson, M., & Hagman, J. R. (2011) · European Journal of Immunology · doi:10.1002/eji.201041137 · Cited by 37 · see citing works
B-lymphocyte commitment: Identifying the point of no return
Welinder, E., Åhsberg, J., & Sigvardsson, M. (2011) · Seminars in Immunology · doi:10.1016/j.smim.2011.08.005 · Cited by 30 · see citing works
Transcriptional control of innate lymphocyte fate decisions
Klose, C. S. N., Hoyler, T., Kiss, E. A., Tanriver, Y., & Diefenbach, A. (2012) · Current Opinion in Immunology · doi:10.1016/j.coi.2012.04.004 · Cited by 18 · see citing works
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Klose, C. S. N., Flach, M., Möhle, L., Rogell, L., Hoyler, T., Ebert, K., Fabiunke, C., Pfeifer, D., Sexl, V., Fonseca‐Pereira, D., et al. (2014) · Cell · doi:10.1016/j.cell.2014.03.030 · Cited by 1,081 · see citing works
Self-citationInterleukin-22: Immunobiology and Pathology
Dudakov, J. A., Hanash, A. M., & van den Brink, M. R. M. (2015) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032414-112123 · Cited by 906 · see citing works
Fine-mapping inflammatory bowel disease loci to single-variant resolution
International Inflammatory Bowel Disease Genetics Consortium, Huang, H., Fang, M., Jostins, L., Umićević Mirkov, M., Boucher, G., Anderson, C. A., Andersen, V., Cleynen, I., Cortes, A., et al. (2017) · Nature · doi:10.1038/nature22969 · Cited by 611 · see citing works
Development, Differentiation, and Diversity of Innate Lymphoid Cells
Diefenbach, A., Colonna, M., & Koyasu, S. (2014) · Immunity · doi:10.1016/j.immuni.2014.09.005 · Cited by 560 · see citing works
Self-citationJacoby, E., Nguyen, S. M., Fountaine, T. J., Welp, K. M., Gryder, B. E., Qin, H., Yang, Y., Chien, C. D., Seif, A. E., Lei, H., et al. (2016) · Nature Communications · doi:10.1038/ncomms12320 · Cited by 431 · see citing works
Gomes, A. C., Hara, T., Lim, V., Herndler‐Brandstetter, D., Nevius, E., Sugiyama, T., Tani‐ichi, S., Schlenner, S., Richie, E. R., Rodewald, H.-R., et al. (2016) · Immunity · doi:10.1016/j.immuni.2016.11.004 · Cited by 288 · see citing works
Dissecting Engineered Cell Types and Enhancing Cell Fate Conversion via CellNet
Morris, S. A., Cahan, P., Li, H., Zhao, A., Roman, A. K. S., Shivdasani, R. A., Collins, J. J., & Daley, G. Q. (2014) · Cell · doi:10.1016/j.cell.2014.07.021 · Cited by 267 · see citing works
GATA-3 Function in Innate and Adaptive Immunity
Tindemans, I., Serafini, N., Santo, J. P. D., & Hendriks, R. W. (2014) · Immunity · doi:10.1016/j.immuni.2014.06.006 · Cited by 258 · see citing works
Transcriptional Control of Early T and B Cell Developmental Choices
Rothenberg, E. V. (2014) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-100024 · Cited by 232 · see citing works
Deep Feature Selection: Theory and Application to Identify Enhancers and Promoters
Li, Y., Chen, C., & Wasserman, W. W. (2016) · Journal of Computational Biology · doi:10.1089/cmb.2015.0189 · Cited by 207 · see citing works
A single-cell time-lapse of mouse prenatal development from gastrula to birth
Qiu, C., Martin, B., Welsh, I. C., Daza, R. M., Le, T.-M., Huang, X., Nichols, E. K., Taylor, M. L., Fulton, O., O’Day, D. R., et al. (2024) · Nature · doi:10.1038/s41586-024-07069-w · Cited by 199 · see citing works
NFIL3 Orchestrates the Emergence of Common Helper Innate Lymphoid Cell Precursors
Xu, W., Domingues, R. G., Fonseca‐Pereira, D., Ferreira, M. M., Ribeiro, H., Lopez‐Lastra, S., Motomura, Y., Moreira-Santos, L., Bihl, F., Braud, V. M., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.02.057 · Cited by 184 · see citing works
Innate Lymphoid Cell Development: A T Cell Perspective
Cherrier, D. E., Serafini, N., & Di Santo, J. P. (2018) · Immunity · doi:10.1016/j.immuni.2018.05.010 · Cited by 181 · see citing works
Transcriptional Regulation of Innate and Adaptive Lymphocyte Lineages
Obaldia, M. E. D., & Bhandoola, A. (2015) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032414-112032 · Cited by 163 · see citing works
An Id2RFP-Reporter Mouse Redefines Innate Lymphoid Cell Precursor Potentials
Xu, W., Cherrier, D. E., Chea, S., Vosshenrich, C. A. J., Serafini, N., Petit, M., Liu, P., Golub, R., & Santo, J. P. D. (2019) · Immunity · doi:10.1016/j.immuni.2019.02.022 · Cited by 157 · see citing works
Transcription factor networks in B-cell differentiation link development to acute lymphoid leukemia
Somasundaram, R., Prasad, M. A. J., Ungerbäck, J., & Sigvardsson, M. (2015) · Blood · doi:10.1182/blood-2014-12-575688 · Cited by 135 · see citing works
In Situ Maturation and Tissue Adaptation of Type 2 Innate Lymphoid Cell Progenitors
Zeis, P., Lian, M., Fan, X., Herman, J. S., Hernandez, D., Gentek, R., Elias, S., Symowski, C., Knöpper, K., Peltokangas, N., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.09.002 · Cited by 145 · see citing works
Boller, S., Ramamoorthy, S., Akbas, D., Nechanitzky, R., Burger, L., Murr, R., Schübeler, D., & Grosschedl, R. (2016) · Immunity · doi:10.1016/j.immuni.2016.02.021 · Cited by 133 · see citing works
Self-citationThe regulatory network of B‐cell differentiation: a focused view of early B‐cell factor 1 function
Boller, S., & Grosschedl, R. (2014) · Immunological Reviews · doi:10.1111/imr.12206 · Cited by 127 · see citing works
Self-citationDistinct Epigenetic Effects of Tobacco Smoking in Whole Blood and among Leukocyte Subtypes
Su, D., Wang, X., Campbell, M. R., Porter, D. K., Pittman, G. S., Bennett, B. D., Wan, M., Englert, N. A., Crowl, C. L., Gimple, R. C., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0166486 · Cited by 124 · see citing works
Hosokawa, H., Ungerbäck, J., Wang, X., Matsumoto, M., Nakayama, K. I., Cohen, S. M., Tanaka, T., & Rothenberg, E. V. (2018) · Immunity · doi:10.1016/j.immuni.2018.04.024 · Cited by 116 · see citing works
van Schouwenburg, P. A., Davenport, E. E., Kienzler, A., Marwah, I., Wright, B., Lucas, M., Malinauskas, T., Martin, H. C., Lockstone, H. E., Cazier, J., et al. (2015) · Clinical Immunology · doi:10.1016/j.clim.2015.05.020 · Cited by 110 · see citing works
Razy‐Krajka, F., Lam, K., Wang, W., Stolfi, A., Joly, M., Bonneau, R., & Christiaen, L. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.04.001 · Cited by 95 · see citing works
Eibel, H., Kraus, H., Sic, H., Kienzler, A., & Rizzi, M. (2014) · Current Allergy and Asthma Reports · doi:10.1007/s11882-014-0434-8 · Cited by 101 · see citing works
Crickx, É., Chappert, P., Sokal, A., Weller, S., Azzaoui, I., Vandenberghe, A., Bonnard, G., Rossi, G., Fadeev, T., Storck, S., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abc3961 · Cited by 97 · see citing works
Li, R., Cauchy, P., Ramamoorthy, S., Boller, S., Chavez, L., & Grosschedl, R. (2018) · Genes & Development · doi:10.1101/gad.309583.117 · Cited by 86 · see citing works
Self-citationLópez‐Isac, E., Smith, S. L., Marion, M. C., Wood, A., Sudman, M., Yarwood, A., Shi, C., Gaddi, V. P., Martin, P., Prahalad, S., et al. (2020) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2020-218481 · Cited by 87 · see citing works
Bcl11b and combinatorial resolution of cell fate in the T-cell gene regulatory network
Longabaugh, W. J. R., Zeng, W., Zhang, J. A., Hosokawa, H., Jansen, C. S., Li, L., Romero-Wolf, M., Liu, P., Kueh, H. Y., Mortazavi, A., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610617114 · Cited by 89 · see citing works
Reduced Lymphoid Lineage Priming Promotes Human Hematopoietic Stem Cell Expansion
van Galen, P., Kreso, A., Wienholds, E., Laurenti, E., Eppert, K., Lechman, E. R., Mbong, N., Hermans, K. G., Dobson, S. M., April, C., et al. (2014) · Cell stem cell · doi:10.1016/j.stem.2013.11.021 · Cited by 78 · see citing works
Wang, Y., Zolotarev, N., Yang, C., Rambold, A. S., Mittler, G., & Grosschedl, R. (2020) · Immunity · doi:10.1016/j.immuni.2020.10.009 · Cited by 75 · see citing works
Self-citationLescale, C., Schenten, V., Djeghloul, D., Bennabi, M., Gaignier, F., Vandamme, K., Strazielle, C., Kuzniak, I., Petite, H., Dosquet, C., et al. (2014) · The FASEB Journal · doi:10.1096/fj.14-259770 · Cited by 73 · see citing works
Doghish, A. S., Abulsoud, A. I., Elshaer, S. S., Abdelmaksoud, N. M., Zaki, M. B., El‐Mahdy, H. A., Ismail, A., Fathi, D., & Elsakka, E. G. E. (2023) · Pathology - Research and Practice · doi:10.1016/j.prp.2023.154363 · Cited by 64 · see citing works
The Innate Lymphoid Cell Precursor
Ishizuka, I. E., Constantinides, M. G., Gudjonson, H., & Bendelac, A. S. (2016) · Annual Review of Immunology · doi:10.1146/annurev-immunol-041015-055549 · Cited by 63 · see citing works
Leca, J., Lemonnier, F., Meydan, C., Foox, J., Ghamrasni, S. E., Mboumba, D.-L., Duncan, G. S., Fortin, J., Sakamoto, T., Tobin, C., et al. (2023) · Cancer Cell · doi:10.1016/j.ccell.2023.01.003 · Cited by 60 · see citing works
scATAC-pro: a comprehensive workbench for single-cell chromatin accessibility sequencing data
Yu, W., Uzun, Y., Zhu, Q., Chen, C., & Tan, K. (2020) · Genome biology · doi:10.1186/s13059-020-02008-0 · Cited by 60 · see citing works
The making of a lymphocyte: the choice among disparate cell fates and the IKAROS enigmaPreprint
Georgopoulos, K. (2017) · Genes & Development · doi:10.1101/gad.297002.117 · Cited by 62 · see citing works
Deep Feature Selection: Theory and Application to Identify Enhancers and Promoters
Li, Y., Chen, C., & Wasserman, W. W. (2015) · Lecture notes in computer science · doi:10.1007/978-3-319-16706-0_20 · Cited by 64 · see citing works
Beyond NK Cells: The Expanding Universe of Innate Lymphoid Cells
Cella, M., Miller, H. L., & Song, C. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00282 · Cited by 59 · see citing works
Denoising genome-wide histone ChIP-seq with convolutional neural networks
Koh, P. W., Pierson, E., & Kundaje, A. B. (2017) · Bioinformatics · doi:10.1093/bioinformatics/btx243 · Cited by 59 · see citing works
Lin, Y., Zhang, Q., Zhang, H., Liu, W., Liu, C., Li, Q., & Guo, A. (2015) · Scientific Reports · doi:10.1038/srep15215 · Cited by 57 · see citing works
Innate lymphoid cells, precursors and plasticity
Gronke, K., Kofoed-Nielsen, M., & Diefenbach, A. (2016) · Immunology Letters · doi:10.1016/j.imlet.2016.07.004 · Cited by 55 · see citing works
Self-citationExplaiNN: interpretable and transparent neural networks for genomics
Novakovsky, G., Fornés, O., Saraswat, M., Mostafavi, S., & Wasserman, W. W. (2023) · Genome biology · doi:10.1186/s13059-023-02985-y · Cited by 55 · see citing works
Azagra, A., Román-González, L., Collazo, O., Rodríguez‐Ubreva, J., de Yébenes, V. G., Barneda‐Zahonero, B., Rodríguez, J., de Moura, M. C., Grego‐Bessa, J., Fernández-Duran, I., et al. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20150821 · Cited by 55 · see citing works
An Erg-driven transcriptional program controls B cell lymphopoiesis
Ng, A. P., Coughlan, H. D., Hediyeh-zadeh, S., Behrens, K., Johanson, T. M., Low, M. S. Y., Bell, C. C., Gilan, O., Chan, Y.-C., Kueh, A. J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16828-y · Cited by 51 · see citing works
Single-cell sequencing reveals the evolution of immune molecules across multiple vertebrate species
Jiao, A., Zhang, C., Wang, X., Sun, L., Liu, H., Su, Y., Lei, L., Li, W., Ding, R., Ding, C., et al. (2023) · Journal of Advanced Research · doi:10.1016/j.jare.2023.02.017 · Cited by 53 · see citing works
Hematopoietic Stem Cells and the Immune System in Development and Aging
Shevyrev, D., Tereshchenko, V., Berezina, T. N., & Александрович, Р. С. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065862 · Cited by 54 · see citing works
Transcription factor Hoxb5 reprograms B cells into functional T lymphocytes
Zhang, M., Dong, Y., Hu, F., Yang, D., Zhao, Q., Lv, C., Wang, Y., Xia, C., Weng, Q., Liu, X., et al. (2018) · Nature Immunology · doi:10.1038/s41590-018-0046-x · Cited by 53 · see citing works
PHF6 regulates phenotypic plasticity through chromatin organization within lineage-specific genesPreprint
Soto‐Feliciano, Y. M., Bartlebaugh, J. M. E., Liu, Y., Rivera, F. J. S., Bhutkar, A. J., Weintraub, A. S., Buenrostro, J. D., Cheng, C. S., Regev, A., Jacks, T., et al. (2017) · Genes & Development · doi:10.1101/gad.295857.117 · Cited by 53 · see citing works
Yang, X., Shao, X., Gao, L., & Zhang, S. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv172 · Cited by 48 · see citing works
Aryl Hydrocarbon Receptor Activation Suppresses EBF1 and PAX5 and Impairs Human B Lymphopoiesis
Li, J., Bhattacharya, S., Zhou, J., Phadnis-Moghe, A. S., Crawford, R. B., & Kaminski, N. E. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1700289 · Cited by 49 · see citing works
Defining B Cell Chromatin: Lessons from EBF1.
Boller, S., Li, R., & Grosschedl, R. (2018) · Trends in Genetics · doi:10.1016/j.tig.2017.12.014 · Cited by 44 · see citing works
Self-citationThe establishment of B versus T cell identity
Miyazaki, K., Miyazaki, M., & Murre, C. (2014) · Trends in Immunology · doi:10.1016/j.it.2014.02.009 · Cited by 48 · see citing works
Prasad, M. A. J., Ungerbäck, J., Åhsberg, J., Somasundaram, R., Strid, T., Larsson, M., Månsson, R., Paepe, A. D., Lilljebjörn, H., Fioretos, T., et al. (2015) · Blood · doi:10.1182/blood-2014-12-617282 · Cited by 46 · see citing works
Combined heterozygous loss of Ebf1 and Pax5 allows for T-lineage conversion of B cell progenitors
Ungerbäck, J., Åhsberg, J., Strid, T., Somasundaram, R., & Sigvardsson, M. (2015) · The Journal of Experimental Medicine · doi:10.1084/jem.20132100 · Cited by 45 · see citing works
EBF1 and PAX5 control pro-B cell expansion via opposing regulation of the Myc gene.
Somasundaram, R., Jensen, C. T., Tingvall-Gustafsson, J., Åhsberg, J., Okuyama, K., Prasad, M., Hagman, J., Wang, X., Soneji, S., Strid, T., et al. (2021) · Blood · doi:10.1182/blood.2020009564 · Cited by 38 · see citing works
Molecular Regulation of Differentiation in Early B-Lymphocyte Development
Sigvardsson, M. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19071928 · Cited by 43 · see citing works
Cell Fate Decisions: The Role of Transcription Factors in Early B-cell Development and Leukemia
Fischer, U., Yang, J. J. J., Ikawa, T., Hein, D., Vicente‐Dueñas, C., Borkhardt, A., & Sánchez-Garcı́a, I. (2020) · Blood Cancer Discovery · doi:10.1158/2643-3230.bcd-20-0011 · Cited by 44 · see citing works
ACE2-lentiviral transduction enables mouse SARS-CoV-2 infection and mapping of receptor interactions
Rawle, D. J., Le, T. T., Dumenil, T. D., Yan, K., Tang, B., Nguyen, W., Watterson, D., Modhiran, N., Hobson‐Peters, J., Bishop, C., et al. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009723 · Cited by 40 · see citing works
Appiah‐Kubi, K., Lan, T., Wang, Y., Qian, H., Wu, M. C., Yao, X., Wu, Y. R., & Chen, Y. (2016) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2016.11.008 · Cited by 42 · see citing works
Katsaraki, K., Karousi, P., Artemaki, P. I., Scorilas, A., Pappa, V., Kontos, C. K., & Papageorgiou, S. G. (2021) · Cancers · doi:10.3390/cancers13040593 · Cited by 42 · see citing works
Moore, B. L., Aitken, S., & Semple, C. A. M. (2015) · Genome biology · doi:10.1186/s13059-015-0661-x · Cited by 40 · see citing works
Reilly, A., Creamer, J. P., Stewart, S., Stolla, M. C., Wang, Y., Du, J., Wellington, R., Busch, S., Estey, E. H., Becker, P. S., et al. (2022) · Cell stem cell · doi:10.1016/j.stem.2022.02.010 · Cited by 40 · see citing works
A Chemoattractant-Guided Walk Through Lymphopoiesis
Lim, V., Zehentmeier, S., Fistonich, C., & Pereira, J. P. (2017) · Advances in immunology · doi:10.1016/bs.ai.2017.02.001 · Cited by 38 · see citing works
Yang, C.-Y., Ramamoorthy, S., Boller, S., Rosenbaum, M., Gil, A. R., Mittler, G., Imai, Y., Kuba, K., & Grosschedl, R. (2016) · Genes & Development · doi:10.1101/gad.285452.116 · Cited by 36 · see citing works
Self-citationSystematic identification of protein combinations mediating chromatin looping
Zhang, K., Li, N., Ainsworth, R. I., & Wang, W. (2016) · Nature Communications · doi:10.1038/ncomms12249 · Cited by 34 · see citing works
Ikawa, T., Masuda, K., Endo, T. A., Mitsuhiro, E. N. D. O., Isono, K., Koseki, Y., Nakagawa, R., Kometani, K., Takano, J., Agata, Y., et al. (2016) · Genes & Development · doi:10.1101/gad.290593.116 · Cited by 35 · see citing works
Transcription Factors Controlling Innate Lymphoid Cell Fate Decisions
Klose, C. S. N., & Diefenbach, A. (2014) · Current topics in microbiology and immunology · doi:10.1007/82_2014_381 · Cited by 33 · see citing works
Self-citationDynamic Control of Long-Range Genomic Interactions at the Immunoglobulin κ Light-Chain Locus
de Almeida, C. R., Hendriks, R. W., & Stadhouders, R. (2015) · Advances in immunology · doi:10.1016/bs.ai.2015.07.004 · Cited by 33 · see citing works
Musa, Y., Boller, S., Puchalska, M., Grosschedl, R., & Mittler, G. (2017) · Journal of Proteome Research · doi:10.1021/acs.jproteome.7b00369 · Cited by 32 · see citing works
Self-citationTumor suppressors BTG1 and BTG2 regulate early mouse B-cell development
Tijchon, E. J. H., van Emst, L., Yuniati, L., Schenau, D. V. I., Havinga, J., Rouault, J.-P., Hoogerbrugge, P. M., van Leeuwen, F. N., & Scheijen, B. (2016) · Haematologica · doi:10.3324/haematol.2015.139675 · Cited by 31 · see citing works
Ramamoorthy, S., Kometani, K., Herman, J. S., Bayer, M., Boller, S., Edwards-Hicks, J., Ramachandran, H., Li, R., Geltink, R. I. K., Pearce, E. L., et al. (2020) · Genes & Development · doi:10.1101/gad.340216.120 · Cited by 31 · see citing works
Self-citationDissection of progenitor compartments resolves developmental trajectories in B-lymphopoiesis
Jensen, C. T., Åhsberg, J., Sommarin, M. N. E., Strid, T., Somasundaram, R., Okuyama, K., Ungerbäck, J., Kupari, J., Airaksinen, M. S., Lang, S., et al. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20171384 · Cited by 30 · see citing works
Kuciński, I., Wilson, N. K., Hannah, R., Kinston, S., Cauchy, P., Lenaerts, A., Grosschedl, R., & Göttgens, B. (2020) · The EMBO Journal · doi:10.15252/embj.2020104983 · Cited by 28 · see citing works
Self-citationZNF423 and ZNF521: EBF1 Antagonists of Potential Relevance in B-Lymphoid Malignancies
Mesuraca, M., Chiarella, E., Scicchitano, S., Codispoti, B., Giordano, M., Nappo, G., Bond, H. M., & Morrone, G. (2015) · BioMed Research International · doi:10.1155/2015/165238 · Cited by 30 · see citing works
Miyazaki, K., & Miyazaki, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.659761 · Cited by 29 · see citing works
Zhou, Y., Petrovic, J., Zhao, J.-R., Zhang, W., Bigdeli, A., Zhang, Z., Berger, S., Pear, W., & Faryabi, R. (2022) · Molecules and Cells · doi:10.1016/j.molcel.2022.01.015 · Cited by 29 · see citing works
Functional interplay of Epstein-Barr virus oncoproteins in a mouse model of B cell lymphomagenesis
Sommermann, T. G., Yasuda, T., Ronen, J., Wirtz, T., Weber, T., Sack, U., Caeser, R., Zhang, J., Li, X., Chu, V. T., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1921139117 · Cited by 28 · see citing works
Salerno, L., Cosentino, C., Morrone, G., & Amato, F. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132208 · Cited by 28 · see citing works
Hernandez‐Davies, J. E., Dollinger, E., Pone, E. J., Felgner, J. H., Liang, L., Strohmeier, S., Jan, S., Albin, T. J., Jain, A., Nakajima, R., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-12727-y · Cited by 27 · see citing works
CEBPA Phase Separation Links Transcriptional Activity and 3D Chromatin Hubs
Christou‐Kent, M., Cuartero, S., Garcia‐Cabau, C., Rühle, J., Naderi, J., Erber, J., Neguembor, M. V., Plana-Carmona, M., Alcoverro-Bertran, M., de Andrés-Aguayo, L., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2023.112897 · Cited by 26 · see citing works
Genome-Wide Identification of Target Genes for the Key B Cell Transcription Factor Ets1
Saelee, P., Kearly, A., Nutt, S. L., & Garrett‐Sinha, L. A. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00383 · Cited by 26 · see citing works
Understanding and Modulating Immunity With Cell Reprogramming
Pires, C. F., Rosa, F. A., Kurochkin, I., & Pereira, C. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02809 · Cited by 25 · see citing works
Transcriptional Control of Pre-B Cell Development and Leukemia Prevention
Pang, S. H. M., Carotta, S., & Nutt, S. L. (2014) · Current topics in microbiology and immunology · doi:10.1007/82_2014_377 · Cited by 26 · see citing works
Patton, D. T., Plumb, A. W., & Abraham, N. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302925 · Cited by 25 · see citing works
Clonal conversion of B lymphoid leukemia reveals cross-lineage transfer of malignant statesPreprint
Somasundaram, R., Åhsberg, J., Okuyama, K., Ungerbäck, J., Lilljebjörn, H., Fioretos, T., Strid, T., & Sigvardsson, M. (2016) · Genes & Development · doi:10.1101/gad.285536.116 · Cited by 24 · see citing works
EBF1 primes B-lymphoid enhancers and limits the myeloid bias in murine multipotent progenitors
Lenaerts, A., Kuciński, I., Deboutte, W., Derecka, M., Cauchy, P., Manke, T., Göttgens, B., & Grosschedl, R. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20212437 · Cited by 22 · see citing works
Self-citationGaurav, R., Mikuls, T. R., Thiele, G. M., Nelson, A. J., Niu, M., Guda, C., Eudy, J. D., Barry, A., Wyatt, T. A., Romberger, D. J., et al. (2021) · PLoS ONE · doi:10.1371/journal.pone.0240707 · Cited by 23 · see citing works
Organism-wide cellular dynamics and epigenomic remodeling in mammalian aging
Lu, Z., Zhang, Z., Xu, Z., Abdulraouf, A., Zhou, W. Y., & Cao, J. (2026) · Science · doi:10.1126/science.adw6273 · Cited by 27 · see citing works
Hematopoietic Reprogramming Entangles with Hematopoiesis
Wei, C., Yu, P., & Cheng, L. (2020) · Trends in Cell Biology · doi:10.1016/j.tcb.2020.07.006 · Cited by 22 · see citing works
Cholinergic control of Th17 cell pathogenicity in experimental autoimmune encephalomyelitis
Nechanitzky, R., Nechanitzky, D., Ramachandran, P., Duncan, G. S., Zheng, C., Göbl, C., Gill, K. T., Haight, J., Wakeham, A. C., Snow, B. E., et al. (2022) · Cell Death and Differentiation · doi:10.1038/s41418-022-01092-y · Cited by 21 · see citing works
Self-citationThe transcription factor Gli3 promotes B cell development in fetal liver through repression of Shh
Solanki, A., Lau, C., Saldaña, J. I., Ross, S. E., & Crompton, T. (2017) · The Journal of Experimental Medicine · doi:10.1084/jem.20160852 · Cited by 22 · see citing works
Signalling circuits that direct early B-cell development
Petkau, G., & Turner, M. (2019) · Biochemical Journal · doi:10.1042/bcj20180565 · Cited by 22 · see citing works
The Multifaceted Role and Utility of MicroRNAs in Indolent B-Cell Non-Hodgkin Lymphomas
Artemaki, P. I., Letsos, P. A., Zoupa, I. C., Katsaraki, K., Karousi, P., Papageorgiou, S. G., Pappa, V., Scorilas, A., & Kontos, C. K. (2021) · Biomedicines · doi:10.3390/biomedicines9040333 · Cited by 22 · see citing works
Wang, O., McAllister, T. A., Plastow, G. S., Stanford, K., Selinger, L. B., & Guan, L. L. (2017) · Scientific Reports · doi:10.1038/s41598-017-06737-4 · Cited by 21 · see citing works
Transcription factor networks link B-lymphocyte development and malignant transformation in leukemiaPreprint
Sigvardsson, M. (2023) · Genes & Development · doi:10.1101/gad.349879.122 · Cited by 22 · see citing works
Lim, B., Kamal, A., Gomez Ramos, B., Adrian Segarra, J. M., Ibarra, I. L., Dignas, L., Kindinger, T., Volz, K., Rahbari, M., Rahbari, N., et al. (2025) · Nature Genetics · doi:10.1038/s41588-025-02081-w · Cited by 17 · see citing works
Can autoimmune disease be cured by deep CD19+ cell depletion?
Suan, D., Moore, J., & Goodnow, C. C. (2025) · The Journal of Immunology · doi:10.1093/jimmun/vkaf008 · Cited by 18 · see citing works
Impaired bone marrow B-cell development in mice with a bronchiolitis obliterans model of cGVHD
Kolupaev, O., Dant, T. A., Bommiasamy, H., Bruce, D., Fowler, K. A., Tilley, S. L., McKinnon, K. P., Sarantopoulos, S., Blazar, B. R., Coghill, J. M., et al. (2018) · Blood Advances · doi:10.1182/bloodadvances.2017014977 · Cited by 17 · see citing works
Noncoding RNA‐guided recruitment of transcription factors: A prevalent but undocumented mechanism?
Lee, N., & STEITZ, J. A. (2015) · BioEssays · doi:10.1002/bies.201500060 · Cited by 17 · see citing works
- Authors
- Nechanitzky, R., Akbas, D., Scherer, S., Györy, I., Hoyler, T., Ramamoorthy, S., Diefenbach, A., & Grosschedl, R.
- Affiliations
- Max Planck Institute of Immunobiology and Epigenetics (DE)
- Max Planck Society (DE)
- University of Freiburg (DE)
- Corresponding author
- Grosschedl, Rudolf
- ORCID
- Venue
- Nature Immunology
- Published
- 2013-06-30
- Volume
- 14
- Issue
- 8
- Pages
- 867-875
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- OpenAlex
- W2064993419
- Cited by
- 218
- References
- 50
- Citations by year
- 2026: 13 · 2025: 22 · 2024: 19 · 2023: 12 · 2022: 19 · 2021: 14 · 2020: 19 · 2019: 10 · 2018: 14 · 2017: 17 · 2016: 20 · 2015: 17 · 2014: 18 · 2013: 1
- FWCI
- 10.30
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Immunology (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Digital Library (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- EBF1, B cell identity, lineage commitment, pro-B cells, innate lymphoid cells, T cell fate, PAX5, Id2, TCF1, VDJ rearrangement, conditional gene deletion, transcriptional repression
- MeSH terms
- Animals, B-Lymphocytes, Cell Differentiation, DNA, Gene Expression Regulation, Receptors, Antigen, T-Cell, T-Lymphocytes, Trans-Activators, Polymerase Chain Reaction, Mice, Knockout, Cell Lineage, Adoptive Transfer, Oligonucleotide Array Sequence Analysis, Lymphopoiesis, Mice, V(D)J Recombination
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