The earliest subpopulation of mouse thymocytes contains potent T, significant macrophage, and natural killer cell but no B-lymphocyte potential
Abstract
The B-lymphocyte potential of progenitor thymocytes and whether the thymus is colonized by common lymphocyte progenitor cells have been subjects of considerable debate. Herein, we have used limiting dilution analysis to determine the lineage potential of phenotypically defined subpopulations of CD4–CD8– double-negative thymocytes. Culture systems used showed single-hit kinetics and had a high plating efficiency for B-, myeloid, and natural killer cell development. The T-cell potential of sorted cells was confirmed by transferring cells to fetal thymus organ cultures. Our results indicate that the earliest population of CD117+ double-negative cells, although containing potent T-cell developmental potential and significant myeloid and natural killer potential, does not have any residual B-cell potential. Gene transcription analysis also indicated that these double-negative cells contained abundant T and myeloid, but not B cell–specific transcripts. The implications of these results within the context of current models of thymocyte development are discussed.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
ETP and DN2 cells can generate myeloid cells if removed from the thymus, whereas pro-T cells past PU.1 expression (DN3 or later) do not make myeloid cells under these conditions.
“Whereas ETP and DN2 cells can generate myeloid cells if removed from the thymus, pro-T cells that have differentiated past the stage of PU.1 expression in the thymus (i.e., from the DN2 stage to the DN3 stage or later) do not make myeloid cells under these conditions”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [54]
Cites
Identification of Clonogenic Common Lymphoid Progenitors in Mouse Bone Marrow
Kondo, M., Weissman, I. L., & Akashi, K. (1997) · Cell · doi:10.1016/s0092-8674(00)80453-5 · Cited by 2,253 · see citing works
IMMUNOLOGICAL FUNCTION OF THE THYMUS
MILLER, J. (1961) · The Lancet · doi:10.1016/s0140-6736(61)90693-6 · Cited by 1,396 · see citing works
Deficient T Cell Fate Specification in Mice with an Induced Inactivation of Notch1
Radtke, F., Wilson, A., Stark, G., Bauer, M., van Meerwijk, J. P. M., MacDonald, H. R., & Aguet, M. (1999) · Immunity · doi:10.1016/s1074-7613(00)80054-0 · Cited by 1,393 · see citing works
Induction of T Cell Development from Hematopoietic Progenitor Cells by Delta-like-1 In Vitro
Schmitt, T. M., & Zúñiga-Pflücker, J. C. (2002) · Immunity · doi:10.1016/s1074-7613(02)00474-0 · Cited by 1,120 · see citing works
Karasuyama, H., & Melchers, F. (1988) · European Journal of Immunology · doi:10.1002/eji.1830180115 · Cited by 1,090 · see citing works
The ikaros gene is required for the development of all lymphoid lineages
Georgopoulos, K., Bigby, M., Wang, J.-H., Molnar, A., Wu, P., Winandy, S., & Sharpe, A. (1994) · Cell · doi:10.1016/0092-8674(94)90407-3 · Cited by 985 · see citing works
Notch1 Expression in Early Lymphopoiesis Influences B versus T Lineage Determination
Pui, J. C., Allman, D., Xu, L., DeRocco, S. E., Karnell, F. G., Bakkour, S., Lee, J. Y., Kadesch, T. R., Hardy, R. R., Aster, J. C., et al. (1999) · Immunity · doi:10.1016/s1074-7613(00)80105-3 · Cited by 943 · see citing works
Generation of Lymphohematopoietic Cells from Embryonic Stem Cells in Culture
Nakano, T., Kodama, H., & Honjo, T. (1994) · Science · doi:10.1126/science.8066449 · Cited by 866 · see citing works
Multilineage gene expression precedes commitment in the hemopoietic system.Preprint
Hu, M., Krause, D. S., Greaves, M. F., Sharkis, S. J., Dexter, M., Heyworth, C. M., & Enver, T. (1997) · Genes & Development · doi:10.1101/gad.11.6.774 · Cited by 719 · see citing works
Ardavı́n, C., Wu, L., Li, C., & Shortman, K. (1993) · Nature · doi:10.1038/362761a0 · Cited by 657 · see citing works
Expression of interleukin-2 receptors as a differentiation marker on intrathymic stem cells
Ceredig, R. H., Lowenthal, J. W., Nabholz, M., & MacDonald, H. R. (1985) · Nature · doi:10.1038/314098a0 · Cited by 594 · see citing works
Self-citationThymopoiesis independent of common lymphoid progenitors.
Allman, D., Sambandam, A., Kim, S., Miller, J. P., Pagan, A., Well, D., Meraz, A., & Bhandoola, A. (2003) · Nature Immunology · doi:10.1038/ni878 · Cited by 544 · see citing works
What does it take to make a natural killer?
Colucci, F., Caligiuri, M. A., & Santo, J. P. D. (2003) · Nature reviews. Immunology · doi:10.1038/nri1088 · Cited by 491 · see citing works
Expression and function of the interleukin 7 receptor in murine lymphocytes.
Sudo, T., Nishikawa, S., Ohno, N., Akiyama, N., Tamakoshi, M., Yoshida, H., & Nishikawa, S. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.19.9125 · Cited by 482 · see citing works
Lymphostromal interactions in thymic development and function
Anderson, G., & Jenkinson, E. J. (2001) · Nature reviews. Immunology · doi:10.1038/35095500 · Cited by 461 · see citing works
Early T Lymphocyte Progenitors
Shortman, K., & Wu, L. (1996) · Annual Review of Immunology · doi:10.1146/annurev.immunol.14.1.29 · Cited by 448 · see citing works
Control points in early T-cell development
Godfrey, D. I., & Zlotnik, A. (1993) · Immunology Today · doi:10.1016/0167-5699(93)90186-o · Cited by 416 · see citing works
Lind, E. F., Prockop, S. E., Porritt, H. E., & Petrie, H. T. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.194.2.127 · Cited by 402 · see citing works
T-cell development made simple
Zúñiga‐Pflücker, J. C. (2004) · Nature reviews. Immunology · doi:10.1038/nri1257 · Cited by 325 · see citing works
Rolink, A. G., Kudō, A., Karasuyama, H., Kikuchi, Y., & Melchers, F. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb07953.x · Cited by 318 · see citing works
Self-citationDevelopmental potential of the earliest precursor cells from the adult mouse thymus.
Wu, L., Antica, M., Johnson, G. R., Scollay, R. G., & Shortman, K. (1991) · The Journal of Experimental Medicine · doi:10.1084/jem.174.6.1617 · Cited by 293 · see citing works
Early T lymphocytes. Differentiation in vivo of adult intrathymic precursor cells.
Fowlkes, B. J., Edison, L. J., Mathieson, B. J., & Chused, T. M. (1985) · The Journal of Experimental Medicine · doi:10.1084/jem.162.3.802 · Cited by 288 · see citing works
Wang, B., Biron, C. A., She, J., Higgins, K. M., Sunshine, M. J., Lacy, E., Lönberg, N., & Terhorst, C. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.20.9402 · Cited by 222 · see citing works
The Importation of Hematogenous Precursors by the Thymus Is a Gated Phenomenon in Normal Adult Mice
Foss, D. L., Donskoy, E., & Goldschneider, I. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.3.365 · Cited by 221 · see citing works
A positive look at double-negative thymocytes
Ceredig, R., & Rolink, T. (2002) · Nature reviews. Immunology · doi:10.1038/nri937 · Cited by 203 · see citing works
Self-citationMartin, C. H., Aifantis, I., Scimone, M. L., von Andrian, U. H., Reizis, B., von Boehmer, H., & Gounari, F. (2003) · Nature Immunology · doi:10.1038/ni965 · Cited by 200 · see citing works
Miller, J. P., Izon, D., DeMuth, W., Gerstein, R., Bhandoola, A., & Allman, D. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20020784 · Cited by 198 · see citing works
Redefinition of lymphoid progenitors
Katsura, Y. (2002) · Nature reviews. Immunology · doi:10.1038/nri721 · Cited by 194 · see citing works
Phenotypic and functional characterization of c-kit expression during intrathymic T cell development
Godfrey, D. I., Zlotnik, A., & Suda, T. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.149.7.2281 · Cited by 185 · see citing works
Lymphocyte Development from Stem Cells
Ikuta, K., Uchida, N., Friedman, J. S., & Weissman, I. L. (1992) · Annual Review of Immunology · doi:10.1146/annurev.iy.10.040192.003551 · Cited by 164 · see citing works
T-cell lineage commitment and cytokine responses of thymic progenitors
Moore, T., & Zlotnik, A. (1995) · Blood · doi:10.1182/blood.v86.5.1850.bloodjournal8651850 · Cited by 162 · see citing works
Ikawa, T., Kawamoto, H., Fujimoto, S., & Katsura, Y. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.190.11.1617 · Cited by 161 · see citing works
Kawamoto, H. (1997) · International Immunology · doi:10.1093/intimm/9.7.1011 · Cited by 141 · see citing works
Akashi, K., Ehrlich, L. I. R., Miyamoto, T., Carr, W. H., & Weissman, I. L. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.10.5221 · Cited by 131 · see citing works
Kang, J., Volkmann, A., & Raulet, D. H. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.6.689 · Cited by 122 · see citing works
King, A. G., Kondo, M., Scherer, D. C., & Weissman, I. L. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.072087899 · Cited by 115 · see citing works
ON THE SPARSE SEEDING OF BONE MARROW AND THYMUS IN RADIATION CHIMAERAS
WALLIS, V. J., LEUCHARS, E., Chwalinski, S., & Davies, A. J. S. (1975) · Transplantation · doi:10.1097/00007890-197501000-00002 · Cited by 104 · see citing works
Cellular identity and lineage choice
Fisher, A. G. (2002) · Nature reviews. Immunology · doi:10.1038/nri958 · Cited by 102 · see citing works
Development and selection of NKT cells
MacDonald, H. R. (2002) · Current Opinion in Immunology · doi:10.1016/s0952-7915(02)00329-1 · Cited by 99 · see citing works
Wiele, C. J. V. D., Marino, J. H., Murray, B. W., Vo, S. S., Whetsell, M., & Teague, T. K. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.7.4235 · Cited by 96 · see citing works
Tracing lymphopoiesis with the aid of a pTα-controlled reporter gene
Gounari, F., Aifantis, I., Martin, C. H., Fehling, H.-J., Hoeflinger, S., Leder, P., von Boehmer, H., & Reizis, B. (2002) · Nature Immunology · doi:10.1038/ni778 · Cited by 91 · see citing works
In vitro generation of T lymphocytes from embryonic stem cell–derived prehematopoietic progenitors
de Pooter, R. F., Cho, S. K., Carlyle, J. R., & Zúñiga‐Pflücker, J. C. (2003) · Blood · doi:10.1182/blood-2003-01-0224 · Cited by 79 · see citing works
Rodewald, H.-R., Brocker, T., & Haller, C. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.26.15068 · Cited by 76 · see citing works
Differential effects of Flk-2/Flt-3 ligand and stem cell factor on murine thymic progenitor cells
Moore, T. A., & Zlotnik, A. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.158.9.4187 · Cited by 60 · see citing works
Presence of B cell progenitors in the thymus
Mori, S., Inaba, M., Sugihara, A., Taketani, S., Doi, H., Fukuba, Y., Yamamoto, Y., Adachi, Y., Inaba, K., Fukuhara, S., et al. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.158.9.4193 · Cited by 60 · see citing works
New insights into the proliferation and differentiation of early mouse thymocytes
Laurent, J. (2004) · International Immunology · doi:10.1093/intimm/dxh108 · Cited by 60 · see citing works
Wilson, A., Capone, M., & MacDonald, H. R. (1999) · International Immunology · doi:10.1093/intimm/11.10.1641 · Cited by 57 · see citing works
Generation of Macrophages from Early T Progenitors In Vitro
Lee, C.-K., Kim, J. K., Kim, Y., Lee, M.-K., Kim, K., Kang, J.-K., Hofmeister, R., Durum, S. K., & Han, S. S. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.10.5964 · Cited by 56 · see citing works
Characterization of thymus-seeding precursor cells from mouse bone marrow
Mori, S., Shortman, K., & Wu, L. (2001) · Blood · doi:10.1182/blood.v98.3.696 · Cited by 55 · see citing works
Stepwise Lineage Restriction of Progenitors in Lympho-Myelopoiesis
Katsura, Y., & Kawamoto, H. (2001) · International Reviews of Immunology · doi:10.3109/08830180109056720 · Cited by 54 · see citing works
Characterization of Thymic Progenitors in Adult Mouse Bone Marrow
Perry, S. S., Pierce, L., Slayton, W. B., & Spangrude, G. J. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.4.1877 · Cited by 45 · see citing works
Petrie, H. T., Tourigny, M. R., Burtrum, D. B., & Livák, F. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.6.3094 · Cited by 42 · see citing works
Thymic stromal cells can support B cell differentiation from intrathymic precursors
Montecino‐Rodriguez, E., Johnson, A., & Dorshkind, K. A. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.156.3.963 · Cited by 33 · see citing works
Ceredig, R. H. (2002) · International Immunology · doi:10.1093/intimm/14.1.87 · Cited by 31 · see citing works
Self-citationRegulation of NK1.1 Expression During Lineage Commitment of Progenitor Thymocytes
Carlyle, J. R., & Zúñiga‐Pflücker, J. C. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.12.6544 · Cited by 16 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Early T-cell precursor leukaemia: a subtype of very high-risk acute lymphoblastic leukaemia
Coustan‐Smith, E., Mullighan, C. G., Onciu, M. M., Behm, F. G., Raimondi, S. C., Pei, D., Cheng, C., Su, X., Rubnitz, J. E., Basso, G., et al. (2009) · The Lancet Oncology · doi:10.1016/s1470-2045(08)70314-0 · Cited by 1,012 · see citing works
Launching the T-cell-lineage developmental programme
Rothenberg, E. V., Moore, J. E., & Yui, M. A. (2007) · Nature reviews. Immunology · doi:10.1038/nri2232 · Cited by 475 · see citing works
The earliest thymic progenitors for T cells possess myeloid lineage potential
Bell, J. J., & Bhandoola, A. (2008) · Nature · doi:10.1038/nature06840 · Cited by 460 · see citing works
Adult T-cell progenitors retain myeloid potential
Wada, H., Masuda, K., Satoh, R., Kakugawa, K., Ikawa, T., Katsura, Y., & Kawamoto, H. (2008) · Nature · doi:10.1038/nature06839 · Cited by 368 · 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
Laiosa, C. V., Stadtfeld, M., Xie, H., de Andres-Aguayo, L., & Graf, T. (2006) · Immunity · doi:10.1016/j.immuni.2006.09.011 · Cited by 351 · see citing works
Fate Mapping Reveals Separate Origins of T Cells and Myeloid Lineages in the Thymus
Schlenner, S., Madan, V., Busch, K., Tietz, A., Läufle, C., Costa, C., Blum, C., Fehling, H. J., & Rodewald, H.-R. (2010) · Immunity · doi:10.1016/j.immuni.2010.03.005 · Cited by 322 · see citing works
Mechanisms of T Cell Development and Transformation
Koch, U., & Radtke, F. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154008 · Cited by 282 · see citing works
Bhandoola, A., von Boehmer, H., Petrie, H. T., & Zúñiga‐Pflücker, J. C. (2007) · Immunity · doi:10.1016/j.immuni.2007.05.009 · Cited by 272 · see citing works
DETERMINANTS OF LYMPHOID-MYELOID LINEAGE DIVERSIFICATION
Laiosa, C. V., Stadtfeld, M., & Graf, T. (2006) · Annual Review of Immunology · doi:10.1146/annurev.immunol.24.021605.090742 · Cited by 260 · see citing works
Rosenbauer, F., Owens, B. M., Yu, L., Tumang, J. R., Steidl, U., Kutok, J. L., Clayton, L. K., Wagner, K., Scheller, M., Iwasaki, H., et al. (2006) · Nature Genetics · doi:10.1038/ng1679 · Cited by 237 · 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
Taghon, T., Yui, M. A., & Rothenberg, E. V. (2007) · Nature Immunology · doi:10.1038/ni1486 · Cited by 195 · see citing works
Requirement for Notch1 signals at sequential early stages of intrathymic T cell development
Tan, J. B. L., Visan, I., Yuan, J. S., & Guidos, C. J. (2005) · Nature Immunology · doi:10.1038/ni1217 · Cited by 191 · see citing works
Bocelli‐Tyndall, C., Bracci, L., Spagnoli, G. C., Braccini, A., Bouchenaki, M., Ceredig, R. H., Pistoia, V., Martín, I., & Tyndall, A. (2006) · Rheumatology · doi:10.1093/rheumatology/kel267 · Cited by 190 · see citing works
Self-citationFeyerabend, T. B., Terszowski, G., Tietz, A., Blum, C., Luche, H., Gossler, A., Gale, N. W., Radtke, F., Fehling, H. J., & Rodewald, H.-R. (2008) · Immunity · doi:10.1016/j.immuni.2008.10.016 · Cited by 177 · see citing works
Vadillo, E., Dorantes-Acosta, E. M., Pelayo, R., & Michael Schnoor, A. (2017) · Blood Reviews · doi:10.1016/j.blre.2017.08.006 · Cited by 169 · see citing works
A multipotent precursor in the thymus maps to the branching point of the T versus B lineage decision
Benz, C., & Bleul, C. C. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050146 · Cited by 161 · see citing works
From the cradle to the grave: activities of GATA‐3 throughout T‐cell development and differentiation
Hosoya, T., Maillard, I. P., & Engel, J. D. (2010) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00954.x · Cited by 157 · see citing works
GATA-3 is required for early T lineage progenitor development
Hosoya, T., Kuroha, T., Moriguchi, T., Cummings, D. R., Maillard, I. P., Lim, K.-C., & Engel, J. D. (2009) · The Journal of Experimental Medicine · doi:10.1084/jem.20090934 · Cited by 154 · see citing works
Fine-Scale Staging of T Cell Lineage Commitment in Adult Mouse Thymus
Yui, M. A., Feng, N., & Rothenberg, E. V. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1000679 · Cited by 152 · see citing works
From stem cell to T cell: one route or many?
Bhandoola, A., & Sambandam, A. (2006) · Nature reviews. Immunology · doi:10.1038/nri1778 · Cited by 145 · see citing works
Key factors in the organized chaos of early T cell development
Hayday, A., & Pennington, D. J. (2007) · Nature Immunology · doi:10.1038/ni1436 · Cited by 140 · see citing works
Models of haematopoiesis: seeing the wood for the trees
Ceredig, R. H., Rolink, A. G., & Brown, G. (2009) · Nature reviews. Immunology · doi:10.1038/nri2525 · Cited by 123 · see citing works
Self-citationWeerkamp, F., Baert, M. R. M., Brugman, M. H., Dik, W. A., de Haas, E. F. E., Visser, T. P., de Groot, C. J. M., Wagemaker, G., van Dongen, J. J. M., & Staal, F. J. T. (2005) · Blood · doi:10.1182/blood-2005-08-3412 · Cited by 114 · see citing works
Two waves of distinct hematopoietic progenitor cells colonize the fetal thymus
Ramond, C., Berthault, C., Burlen-Defranoux, O., de Sousa, A. P., Guy-Grand, D., Vieira, P., Pereira, P., & Cumano, A. (2014) · Nature Immunology · doi:10.1038/ni.2782 · Cited by 110 · 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
Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development
Rothenberg, E. V., Hosokawa, H., & Ungerbäck, J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00228 · Cited by 99 · see citing works
Molecular Dissection of Prethymic Progenitor Entry into the T Lymphocyte Developmental Pathway
Tydell, C. C., David-Fung, E.-S., Moore, J. E., Rowen, L., Taghon, T., & Rothenberg, E. V. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.1.421 · Cited by 99 · see citing works
Heinzel, K., Benz, C., Martins, V. C., Haidl, I. D., & Bleul, C. C. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.2.858 · Cited by 99 · see citing works
The role of Notch and IL‐7 signaling in early thymocyte proliferation and differentiation
Balc̆iūnaite, G., Ceredig, R. H., Fehling, H. J., Zúñiga‐Pflücker, J. C., & Rolink, A. G. (2005) · European Journal of Immunology · doi:10.1002/eji.200425822 · Cited by 98 · see citing works
Self-citationHematopoietic progenitor migration to the adult thymus
Zlotoff, D. A., & Bhandoola, A. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05881.x · Cited by 98 · 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
Kawamoto, H., Ikawa, T., Masuda, K., Wada, H., & Katsura, Y. (2010) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00959.x · Cited by 89 · see citing works
Identification of a T Lineage-Committed Progenitor in Adult Blood
Krueger, A., & von Boehmer, H. (2007) · Immunity · doi:10.1016/j.immuni.2006.12.004 · Cited by 85 · see citing works
Rothenberg, E. V. (2007) · Immunity · doi:10.1016/j.immuni.2007.06.005 · Cited by 83 · see citing works
Multilayered specification of the T-cell lineage fate.
Rothenberg, E. V., Zhang, J., & Li, L. (2010) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00964.x · Cited by 81 · see citing works
Stabilized β-Catenin in Thymic Epithelial Cells Blocks Thymus Development and Function
Žuklys, S., Gill, J. W., Keller, M. P., Hauri-Hohl, M. M., Zhanybekova, S., Balc̆iūnaite, G., Na, K.-J., Jeker, L. T., Hafen, K., Tsukamoto, N., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0713723 · Cited by 81 · see citing works
At the crossroads: diverse roles of early thymocyte transcriptional regulators
Anderson, M. K. (2006) · Immunological Reviews · doi:10.1111/j.0105-2896.2006.00352.x · Cited by 81 · see citing works
Regulation of Notch signaling during T‐ and B‐cell development by O‐fucose glycans
Stanley, P., & Guidos, C. J. (2009) · Immunological Reviews · doi:10.1111/j.1600-065x.2009.00791.x · Cited by 80 · see citing works
Massa, S., Balc̆iūnaite, G., Ceredig, R. H., & Rolink, A. G. (2006) · European Journal of Immunology · doi:10.1002/eji.200535760 · Cited by 80 · see citing works
Self-citationPrethymic T‐cell development defined by the expression of paired immunoglobulin‐like receptors
Masuda, K., Kubagawa, H., Ikawa, T., Chen, C., Kakugawa, K., Hattori, M., Kageyama, R., Cooper, M. D., Minato, N., Katsura, Y., et al. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600878 · Cited by 79 · see citing works
Lu, M., Tayu, R., Ikawa, T., Masuda, K., Matsumoto, I., Mugishima, H., Kawamoto, H., & Katsura, Y. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.9.5848 · Cited by 79 · see citing works
Cytokines, Transcription Factors, and the Initiation of T-Cell DevelopmentPreprint
Hosokawa, H., & Rothenberg, E. V. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a028621 · Cited by 79 · see citing works
T Cell Lineage Determination Precedes the Initiation of <i>TCR</i> β Gene Rearrangement
Masuda, K., Kakugawa, K., Nakayama, T., Minato, N., Katsura, Y., & Kawamoto, H. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.6.3699 · Cited by 77 · see citing works
Maillard, I. P., Schwarz, B. A., Sambandam, A., Fang, T., Shestova, O. E., Xu, L., Bhandoola, A., & Pear, W. S. (2006) · Blood · doi:10.1182/blood-2005-08-3454 · Cited by 76 · see citing works
Early decisions in lymphoid development
Ye, M., & Graf, T. (2007) · Current Opinion in Immunology · doi:10.1016/j.coi.2007.02.007 · Cited by 74 · see citing works
Programming for T-lymphocyte fates: modularity and mechanismsPreprint
Rothenberg, E. V. (2019) · Genes & Development · doi:10.1101/gad.327163.119 · Cited by 74 · see citing works
T-lymphoid, megakaryocyte, and granulocyte development are sensitive to decreases in CBFβ dosage.
Talebian, L., Li, Z., Guo, Y., Gaudet, J., Speck, M. E., Sugiyama, D., Kaur, P., Pear, W. S., Maillard, I., & Speck, N. A. (2007) · Blood · doi:10.1182/blood-2006-05-021188 · Cited by 70 · see citing works
Primitive Lymphoid Progenitors in Bone Marrow with T Lineage Reconstituting Potential
Perry, S. S., Welner, R. S., Kouro, T., Kincade, P. W., & Sun, X.-H. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.5.2880 · Cited by 65 · see citing works
A close developmental relationship between the lymphoid and myeloid lineages
Kawamoto, H. (2006) · Trends in Immunology · doi:10.1016/j.it.2006.02.004 · Cited by 64 · see citing works
Zohren, F., Souroullas, G. P., Luo, M., Gerdemann, U., Imperato, M. R., Wilson, N. K., Göttgens, B., Lukov, G. L., & Goodell, M. A. (2012) · Nature Immunology · doi:10.1038/ni.2365 · Cited by 63 · see citing works
Progression of regulatory gene expression states in fetal and adult pro-T-cell development
David‐Fung, E., Yui, M. A., Morales, M., Wang, H., Taghon, T., Diamond, R. A., & Rothenberg, E. V. (2006) · Immunological Reviews · doi:10.1111/j.0105-2896.2006.00355.x · Cited by 60 · see citing works
Veinotte, L. L., Greenwood, C. P., Mohammadi, N., Parachoniak, C. A., & Takei, F. (2005) · Blood · doi:10.1182/blood-2005-07-2797 · Cited by 58 · see citing works
Regulation of intrathymic T‐cell development by Lunatic Fringe– Notch1 interactions
Visan, I., Yuan, J. S., Tan, J. B. L., Cretegny, K., & Guidos, C. J. (2006) · Immunological Reviews · doi:10.1111/j.0105-2896.2006.00360.x · Cited by 58 · see citing works
Early T cell development and the pitfalls of potential
Schlenner, S., & Rodewald, H.-R. (2010) · Trends in Immunology · doi:10.1016/j.it.2010.06.002 · Cited by 57 · see citing works
The thymus and T-cell commitment: the right niche for Notch?
Jenkinson, E. J., Jenkinson, W. E., Rossi, S. W., & Anderson, G. (2006) · Nature reviews. Immunology · doi:10.1038/nri1883 · Cited by 54 · see citing works
Weerkamp, F., Pike‐Overzet, K., & Staal, F. J. T. (2006) · Trends in Immunology · doi:10.1016/j.it.2006.01.006 · Cited by 51 · see citing works
Tissue-specific NK cell populations and their origin
Lysakova-Devine, T., & O’Farrelly, C. (2014) · Journal of Leukocyte Biology · doi:10.1189/jlb.1ru0514-241r · Cited by 50 · see citing works
Qian, L., Bajaña, S., Georgescu, C., Peng, V., Wang, H., Adrianto, I., Colonna, M., Alberola‐Ila, J., Wren, J. D., & Sun, X.-H. (2019) · The Journal of Experimental Medicine · doi:10.1084/jem.20182100 · Cited by 50 · see citing works
Ceredig, R. H., Rauch, M., Balc̆iūnaite, G., & Rolink, A. G. (2006) · Blood · doi:10.1182/blood-2005-10-006643 · Cited by 49 · see citing works
Self-citationTransient Notch signaling induces NK cell potential in Pax5‐deficient pro‐B cells
Carotta, S., Brady, J., Wu, L., & Nutt, S. L. (2006) · European Journal of Immunology · doi:10.1002/eji.200636325 · Cited by 48 · see citing works
Early T-cell progenitors are the major granulocyte precursors in the adult mouse thymus
De Obaldia, M. E., Bell, J. J., & Bhandoola, A. (2013) · Blood · doi:10.1182/blood-2012-08-451773 · Cited by 44 · see citing works
T lineage progenitors: the earliest steps en route to T lymphocytes
Wu, L. (2006) · Current Opinion in Immunology · doi:10.1016/j.coi.2006.01.006 · Cited by 44 · see citing works
Competition and collaboration: GATA-3, PU.1, and Notch signaling in early T-cell fate determination
Rothenberg, E. V., & Scripture-Adams, D. D. (2008) · Seminars in Immunology · doi:10.1016/j.smim.2008.07.006 · Cited by 43 · see citing works
Oncogenes, Proto-Oncogenes, and Lineage Restriction of Cancer Stem Cells
Brown, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22189667 · Cited by 41 · see citing works
T‐cell development: an extrathymic perspective
Blais, M., Louis, I., & Perreault, C. (2006) · Immunological Reviews · doi:10.1111/j.0105-2896.2006.00341.x · Cited by 38 · see citing works
Untangling the T branch of the hematopoiesis tree
Chi, A. W., Bell, J. J., Zlotoff, D. A., & Bhandoola, A. (2009) · Current Opinion in Immunology · doi:10.1016/j.coi.2009.01.012 · Cited by 37 · see citing works
Hematopoiesis and T‐cell specification as a model developmental system
Rothenberg, E. V., Kueh, H. Y., Yui, M. A., & Zhang, J. A. (2016) · Immunological Reviews · doi:10.1111/imr.12417 · Cited by 36 · see citing works
Bosco, N., Swee, L. K., Bénard, A., Ceredig, R. H., & Rolink, A. G. (2010) · Experimental Hematology · doi:10.1016/j.exphem.2009.12.006 · Cited by 36 · see citing works
Self-citationGutiérrez, A., & Kentsis, A. (2018) · British Journal of Haematology · doi:10.1111/bjh.15129 · Cited by 35 · see citing works
Single-cell insights into the hematopoietic generation of T-lymphocyte precursors in mouse and human
Rothenberg, E. V. (2021) · Experimental Hematology · doi:10.1016/j.exphem.2020.12.005 · Cited by 35 · see citing works
The intrathymic crossroads of T and NK cell differentiation
Wolterink, R. G. J. K., García‐Ojeda, M. E., Vosshenrich, C. A. J., Hendriks, R. W., & Santo, J. P. D. (2010) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00960.x · Cited by 34 · see citing works
The potential involvement of Notch signaling in NK cell development
Rolink, A. G., Balc̆iūnaite, G., Demolière, C., & Ceredig, R. H. (2006) · Immunology Letters · doi:10.1016/j.imlet.2006.07.005 · Cited by 34 · see citing works
Self-citationBocelli‐Tyndall, C., Barbero, A., Candrian, C., Ceredig, R. H., Tyndall, A., & Martín, I. (2006) · Journal of Cellular Physiology · doi:10.1002/jcp.20789 · Cited by 34 · see citing works
Self-citationThe B lineage potential of thymus settling progenitors is critically dependent on mouse age
Ceredig, R. H., Bosco, N., & Rolink, A. G. (2007) · European Journal of Immunology · doi:10.1002/eji.200636728 · Cited by 33 · see citing works
Self-citationHes1 Potentiates T Cell Lymphomagenesis by Up-Regulating a Subset of Notch Target Genes
Dudley, D. D., Wang, H.-C., & Sun, X.-H. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006678 · Cited by 33 · see citing works
Tussiwand, R., Engdahl, C., Gehre, N., Bosco, N., Ceredig, R., & Rolink, A. G. (2011) · European Journal of Immunology · doi:10.1002/eji.201141824 · Cited by 32 · see citing works
Self-citationSmeets, M. F. M. A., Chan, A. C., Dagger, S. A., Bradley, C. K., Wei, A. H., & Izon, D. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062346 · Cited by 30 · see citing works
Feeding the fire: the role of defective bone marrow function in exacerbating thymic involution
Dudakov, J. A., Khong, D., Boyd, R. L., & Chidgey, A. P. (2010) · Trends in Immunology · doi:10.1016/j.it.2010.02.002 · Cited by 30 · see citing works
Gehre, N., Nusser, A., von Muenchow, L., Tussiwand, R., Engdahl, C., Capoferri, G., Bosco, N., Ceredig, R. H., & Rolink, A. G. (2014) · European Journal of Immunology · doi:10.1002/eji.201444681 · Cited by 29 · see citing works
Self-citationTranscriptional network dynamics in early T cell development
Shin, B., Chang, S. J., MacNabb, B. W., & Rothenberg, E. V. (2024) · The Journal of Experimental Medicine · doi:10.1084/jem.20230893 · Cited by 28 · see citing works
Unique subset of natural killer cells develops from progenitors in lymph node
Veinotte, L. L., Halim, T. Y. F., & Takei, F. (2008) · Blood · doi:10.1182/blood-2007-04-087577 · Cited by 28 · see citing works
Responsiveness of Developing T Cells to IL-7 Signals Is Sustained by miR-17∼92
Regelin, M., Blume, J., Pommerencke, J., Vakilzadeh, R., Witzlau, K., Łyszkiewicz, M., Ziętara, N., Saran, N., Schambach, A., & Krueger, A. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402248 · Cited by 27 · see citing works
Chi, A. W. S., Chavez, A., Xu, L., Weber, B., Shestova, O. E., Schaffer, A., Wertheim, G. B. W., Pear, W. S., Izon, D. J., & Bhandoola, A. (2011) · Blood · doi:10.1182/blood-2010-09-309989 · Cited by 26 · see citing works
Gui, J., Morales, A. J., Maxey, S. E., Bessette, K. A., Ratcliffe, N. R., Kelly, J. A., & Craig, R. W. (2011) · International Immunology · doi:10.1093/intimm/dxr073 · Cited by 26 · see citing works
The Human Thymus Is Enriched for Autoreactive B Cells
Rother, M. B., Schreurs, M. W. J., Kroek, R., Bartol, S. J. W., van Dongen, J. J. M., & van Zelm, M. C. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1501992 · Cited by 25 · see citing works
Modeling the Hematopoietic Landscape
Brown, G., & Ceredig, R. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00104 · Cited by 25 · see citing works
Self-citationEliciting the T cell fate with Notch
Sultana, D. A., Bell, J. J., Zlotoff, D. A., Obaldia, M. E. D., & Bhandoola, A. (2010) · Seminars in Immunology · doi:10.1016/j.smim.2010.04.011 · Cited by 24 · see citing works
Viganò, M., Ivánek, R., Balwierz, P. J., Berninger, P., van Nimwegen, E., Karjalainen, K., & Rolink, A. G. (2013) · European Journal of Immunology · doi:10.1002/eji.201344022 · Cited by 23 · see citing works
Self-citationCheng, M., Charoudeh, H. N., Brodin, P., Tang, Y., Lakshmikanth, T., Höglund, P., Jacobsen, S. E. W., & Sitnicka, E. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.182.3.1460 · Cited by 23 · see citing works
Visan, I., Yuan, J. S., Liu, Y. M., Stanley, P., & Guidos, C. J. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1002008 · Cited by 20 · see citing works
Closer to the Source: Notch and the Nature of Thymus-Settling Cells
Zediak, V. P., Maillard, I. P., & Bhandoola, A. (2005) · Immunity · doi:10.1016/j.immuni.2005.08.008 · Cited by 20 · see citing works
Versatility of stem and progenitor cells and the instructive actions of cytokines on hematopoiesis.
Brown, G., Mooney, C. J., Servera, L. A., von Muenchow, L., Toellner, K., Ceredig, R. H., & Rolink, A. G. (2015) · PubMed · doi:10.3109/10408363.2015.1021412 · Cited by 19 · see citing works
Self-citation2016 Revision to the WHO classification of acute lymphoblastic leukemia
Wang, S., & He, G. (2016) · Journal of Translational Internal Medicine · doi:10.1515/jtim-2016-0040 · Cited by 19 · see citing works
Liu, S., Cui, Q., Dai, H., Song, B., Cui, W., Xue, S., Qiu, H., Miao, M., Jin, Z., Li, C., et al. (2021) · Transplantation and Cellular Therapy · doi:10.1016/j.jtct.2021.02.032 · Cited by 19 · see citing works
ETP‐ALL with aberrant B marker expression: Case series and a brief review of literature
Garg, S., Gupta, S. K., Bakhshi, S., Mallick, S., & Kumar, L. (2018) · International Journal of Laboratory Hematology · doi:10.1111/ijlh.12942 · Cited by 17 · see citing works
The potential role of the thymus in immunotherapies for acute myeloid leukemia
Hino, C., Xu, Y., Xiao, J., Baylink, D. J., Reeves, M. E., & Cao, H. L. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1102517 · Cited by 17 · see citing works
Early lymphocyte development in bone marrow and thymus
Rolink, A. G., Massa, S., Balc̆iūnaite, G., & Ceredig, R. H. (2006) · Swiss Medical Weekly · doi:10.4414/smw.2006.11413 · Cited by 17 · see citing works
Self-citationInside the biology of early T-cell precursor acute lymphoblastic leukemia: the perfect trick
Tarantini, F., Cumbo, C., Anelli, L., Zagaria, A., Specchia, G., Musto, P., & Albano, F. (2021) · Biomarker Research · doi:10.1186/s40364-021-00347-z · Cited by 16 · see citing works
- Authors
- Balciunaite, G., Ceredig, R., & Rolink, A. G.
- Affiliations
- From the Developmental and Molecular Immunology, Department of Clinical and Biological Sciences (DKBW), University of Basel, Basel, Switzerland; and U548 INSERM, DRDC, CEA-G, Grenoble, France.
- Inserm (FR)
- ORCID
- Ceredig, Rhodri
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2005-03-01
- Volume
- 105
- Issue
- 5
- Pages
- 1930-1936
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- OpenAlex
- W2062319579
- Cited by
- 158
- References
- 55
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 3 · 2023: 2 · 2022: 3 · 2021: 7 · 2020: 3 · 2019: 9 · 2018: 6 · 2017: 2 · 2016: 6 · 2015: 4 · 2014: 5 · 2013: 6 · 2012: 3
- FWCI
- 5.77
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Blood (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- T cell development, double-negative thymocytes, CD4+CD8+ thymocytes, macrophage development, natural killer cell development, CD117, fetal thymus organ culture, gene transcription, single-hit kinetics
- MeSH terms
- Animals, B-Lymphocytes, Cells, Cultured, Hematopoietic Stem Cells, Immune System, Killer Cells, Natural, Kinetics, Macrophages, T-Lymphocytes, Thymus Gland, Immunophenotyping, Cell Lineage, Leukopoiesis, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
