Prethymic T‐cell development defined by the expression of paired immunoglobulin‐like receptors
Open accessAbstract
T cells are produced in the thymus from progenitors of extrathymic origin. As no specific markers are available, the developmental pathway of progenitors preceding thymic colonization remains unclear. Here we show that progenitors in murine fetal liver and blood, which are capable of giving rise to T cells, NK cells and dendritic cells, but not B cells, can be isolated by their surface expression of paired immunoglobulin-like receptors (PIR). PIR expression is maintained until the earliest intrathymic stage, then downregulated before the onset of CD25 expression. Unlike intrathymic progenitors, generation of prethymic PIR(+) progenitors does not require Hes1-mediated Notch signaling. These findings disclose a prethymic stage of T-cell development programmed for immigration of the thymus, which is genetically separable from intrathymic stages.
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This difference is now understood to be intrinsically programmed and due to an altered pathway of differentiation in the first-wave cells, which results in T-cell lineage commitment even before entry into the thymus.
“This is now understood to be intrinsically programmed (136) and due to an altered pathway of differentiation in the first-wave cells, which results in T-cell lineage commitment even before entry into the thymus (137–139).”
From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [138]
The Results report that commitment to the T/NK/DC lineage occurs in extrathymic organs, and the Discussion describes prethymic progenitors as genetically distinct from intrathymic ones. But the Discussion says these progenitors *may* represent the first phase of thymic immigration; it does not establish an altered differentiation pathway specific to first-wave cells or exclusive commitment to the T-cell lineage. The separate claim of intrinsic programming is attached to citation 136, not this source. (LLM, conf=0.85)
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Cites
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
Han, H., Tanigaki, K., Yamamoto, N., Kuroda, K., Yoshimoto, M., Nakahata, T., Ikuta, K., & Honjo, T. (2002) · International Immunology · doi:10.1093/intimm/dxf030 · Cited by 587 · see citing works
Thymopoiesis 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
Porritt, H. E., Rumfelt, L. L., Tabrizifard, S., Schmitt, T. M., Zúñiga-Pflücker, J. C., & Petrie, H. T. (2004) · Immunity · doi:10.1016/j.immuni.2004.05.004 · Cited by 432 · 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
A novel pair of immunoglobulin-like receptors expressed by B cells and myeloid cells
Kubagawa, H., Burrows, P. D., & Cooper, M. D. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.10.5261 · Cited by 319 · 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
Deltex1 Redirects Lymphoid Progenitors to the B Cell Lineage by Antagonizing Notch1
Izon, D. J., Aster, J. C., He, Y., Weng, A. P., Karnell, F. G., Patriub, V., Xu, L., Bakkour, S., Rodríguez, C. E., Allman, D., et al. (2002) · Immunity · doi:10.1016/s1074-7613(02)00271-6 · Cited by 243 · see citing works
Matsuzaki, Y., Gyotoku, J.-I., Ogawa, M., Nishikawa, S., Katsura, Y., Gachelin, G., & Nakauchi, H. (1993) · The Journal of Experimental Medicine · doi:10.1084/jem.178.4.1283 · Cited by 224 · see citing works
Self-citationCell kinetics in the fetal mouse thymus: precursor cell input, proliferation, and emigration.
Jotereau, F., Heuze, F., Salomon-Vie, V., & Gascan, H. (1987) · The Journal of Immunology · doi:10.4049/jimmunol.138.4.1026 · Cited by 219 · see citing works
The bHLH gene Hes1 is essential for expansion of early T cell precursorsPreprint
Tomita, K., Hattori, M., Nakamura, E., Nakanishi, S., Minato, N., & Kageyama, R. (1999) · Genes & Development · doi:10.1101/gad.13.9.1203 · Cited by 209 · see citing works
Self-citationCirculating hematopoietic progenitors with T lineage potential
Schwarz, B. A., & Bhandoola, A. (2004) · Nature Immunology · doi:10.1038/ni1101 · Cited by 206 · see citing works
Martin, 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
Redefinition of lymphoid progenitors
Katsura, Y. (2002) · Nature reviews. Immunology · doi:10.1038/nri721 · Cited by 194 · see citing works
Self-citationA Role for Pref-1 and HES-1 in Thymocyte Development
Kaneta, M., Osawa, M., Osawa, M., Sudo, K., Nakauchi, H., Farr, A. G., & Takahama, Y. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.1.256 · Cited by 194 · see citing works
Rodewald, H.-R., Kretzschmar, K., Takeda, S., Hohl, C. M., & Dessing, M. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06743.x · Cited by 193 · see citing works
Koch, U., Lacombe, T. A., Holland, D., Bowman, J. L., Cohen, B. L., Egan, S. E., & Guidos, C. J. (2001) · Immunity · doi:10.1016/s1074-7613(01)00189-3 · Cited by 193 · see citing works
Circulation of Hematopoietic Progenitors in the Mouse Embryo
Delassus, S., & Cumano, A. (1996) · Immunity · doi:10.1016/s1074-7613(00)80302-7 · Cited by 192 · 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
Nishikawa, S., Ogawa, M., Nishikawa, S., Kunisada, T., & Kodama, H. (1988) · European Journal of Immunology · doi:10.1002/eji.1830181117 · Cited by 174 · see citing works
Impaired dendritic cell maturation and increased TH2 responses in PIR-B−/− mice
Ujike, A., Takeda, K., Nakamura, A., Ebihara, S., Akiyama, K., & Takai, T. (2002) · Nature Immunology · doi:10.1038/ni801 · Cited by 170 · 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
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
Self-citationBalciunaite, G., Ceredig, R., & Rolink, A. G. (2005) · Blood · doi:10.1182/blood-2004-08-3087 · Cited by 158 · see citing works
T Cell Progenitors Emerge Earlier Than B Cell Progenitors in the Murine Fetal Liver
Kawamoto, H., Ikawa, T., Ohmura, K., Fujimoto, S., & Katsura, Y. (2000) · Immunity · doi:10.1016/s1074-7613(00)80196-x · Cited by 157 · see citing works
Self-citationHattori, N., Kawamoto, H., Fujimoto, S., Kuno, K., & Katsura, Y. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.184.3.1137 · Cited by 142 · see citing works
Self-citationKawamoto, H. (1997) · International Immunology · doi:10.1093/intimm/9.7.1011 · Cited by 141 · see citing works
Self-citationTwo distinct steps of immigration of hematopoietic progenitors into the early thymus anlage
Itoi, M., Kawamoto, H., Katsura, Y., & Amagai, T. (2001) · International Immunology · doi:10.1093/intimm/13.9.1203 · Cited by 139 · see citing works
Self-citationAkashi, 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
Exacerbated graft-versus-host disease in Pirb−/− mice
Nakamura, A., Kobayashi, E., & Takai, T. (2004) · Nature Immunology · doi:10.1038/ni1074 · Cited by 123 · see citing works
Constitutive tyrosine phosphorylation of the inhibitory paired Ig-like receptor PIR-B
Ho, L. H., Uehara, T., Chen, C., Kubagawa, H., & Cooper, M. D. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.26.15086 · Cited by 103 · see citing works
Self-citation`Green mice' and their potential usage in biological research
Ikawa, M., Yamada, S., Nakanishi, T., & Okabe, M. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00593-6 · Cited by 100 · see citing works
Identification of the earliest prethymic bipotent T/NK progenitor in murine fetal liver
Douagi, I., Colucci, F., Santo, J. P. D., & Cumano, A. (2002) · Blood · doi:10.1182/blood.v99.2.463 · Cited by 98 · see citing works
Requirement for the Thymus in αβ T Lymphocyte Lineage Commitment
Carlyle, J. R., & Zúñiga‐Pflücker, J. C. (1998) · Immunity · doi:10.1016/s1074-7613(00)80601-9 · Cited by 96 · see citing works
Enumeration and characterization of DJH structures in mouse fetal liver.
Chang, Y., Paige, C. J., & Wu, G. E. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05241.x · Cited by 96 · see citing works
Activating and inhibitory nature of the murine paired immunoglobulin‐like receptor family
Takai, T., & Ono, M. (2001) · Immunological Reviews · doi:10.1034/j.1600-065x.2001.1810118.x · Cited by 89 · see citing works
Lu, M. M., Kawamoto, H., Katsube, Y., Ikawa, T., & Katsura, Y. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.7.3519 · Cited by 84 · see citing works
Self-citationKawamoto, H., Ohmura, K., & Katsura, Y. (1998) · PubMed · Cited by 83 · see citing works
Self-citationUnique Properties of Fetal Lymphoid Progenitors Identified According to RAG1 Gene Expression
Yokota, T., Kouro, T., Hirose, J., Igarashi, H., Garrett, K. P., Gregory, S. C., Sakaguchi, N., Owen, J. J. T., & Kincade, P. W. (2003) · Immunity · doi:10.1016/s1074-7613(03)00231-0 · Cited by 78 · see citing works
Kawamoto, H., Ohmura, K., & Katsura, Y. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.8.3799 · Cited by 73 · see citing works
Self-citationOhmura, K., Kawamoto, H., Fujimoto, S., Ozaki, S., Nakao, K., & Katsura, Y. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.9.4788 · Cited by 69 · see citing works
Self-citationThymic Anlage Is Colonized by Progenitors Restricted to T, NK, and Dendritic Cell Lineages
Masuda, K., Itoi, M., Amagai, T., Minato, N., Katsura, Y., & Kawamoto, H. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.5.2525 · Cited by 68 · see citing works
Self-citationKawamoto, H., Ohmura, K., Fujimoto, S., & Katsura, Y. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.5.2725 · Cited by 68 · see citing works
Self-citationT/NK Bipotent Progenitors in the Thymus Retain the Potential to Generate Dendritic Cells
Shen, H. Q., Lu, M. M., Ikawa, T., Masuda, K., Ohmura, K., Minato, N., Katsura, Y., & Kawamoto, H. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.7.3401 · Cited by 63 · see citing works
Self-citationHarman, B. C., Jenkinson, E. J., & Anderson, G. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.3.1299 · Cited by 63 · see citing works
In vitro development of B cells and macrophages from early mouse fetal thymocytes
Péault, B., Khazaal, I., & Weissman, I. L. (1994) · European Journal of Immunology · doi:10.1002/eji.1830240345 · Cited by 61 · see citing works
Identification of the earliest prethymic T-cell progenitors in murine fetal blood
Ikawa, T., Masuda, K., Lu, M. M., Minato, N., Katsura, Y., & Kawamoto, H. (2003) · Blood · doi:10.1182/blood-2003-06-1797 · Cited by 58 · see citing works
Self-citationHattori, N., Kawamoto, H., & Katsura, Y. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.184.5.1901 · Cited by 51 · see citing works
Self-citationMany roads, one destination for T cell progenitors
Petrie, H. T., & Kincade, P. W. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050990 · Cited by 45 · see citing works
Kawamoto, H., Ohmura, K., Fujimoto, S., Lu, M. M., Ikawa, T., & Katsura, Y. (2003) · European Journal of Immunology · doi:10.1002/eji.200323461 · Cited by 44 · see citing works
Self-citationDunon, D., Allioli, N., Vainio, O., Ody, C., & Imhof, B. A. (1999) · Blood · doi:10.1182/blood.v93.7.2234 · Cited by 41 · see citing works
Paired Immunoglobulin-like Receptors of Activating and Inhibitory Types
Kubagawa, H., Cooper, M. D., Chen, C., Ho, L. H., Alley, T. L., Hurez, V. J., Tun, T., Uehara, T., Shimada, T., & Burrows, P. D. (1999) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-58537-1_12 · Cited by 39 · see citing works
Self-citationDejbakhsh‐Jones, S., García‐Ojeda, M. E., Chatterjea, D., Zeng, D., & Strober, S. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.131559798 · Cited by 38 · see citing works
Miyazaki, M., Kawamoto, H., Kato, Y., Itoi, M., Miyazaki, K., Masuda, K., Tashiro, S., Ishihara, H., Igarashi, K., Amagai, T., et al. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.5.2507 · Cited by 37 · see citing works
Self-citationMajor T Cell Progenitor Activity in Bone Marrow–derived Spleen Colonies
Lancrin, C., Schneider, E., Lambolez, F., Arcangeli, M.-L., Cordier, C., Rocha, B., & Ezine, S. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20011475 · Cited by 34 · see citing works
B-cell development in the thymus is limited by inhibitory signals from the thymic microenvironment
Hashimoto, Y. K., Montecino‐Rodriguez, E., Leathers, H., Stephan, R. P., & Dorshkind, K. A. (2002) · Blood · doi:10.1182/blood-2002-03-0733 · Cited by 21 · see citing works
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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
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
Self-citationBöiers, C., Carrelha, J., Lutteropp, M., Luc, S., Green, J. C. A., Azzoni, E., Woll, P. S., Mead, A. J., Hultquist, A., Swiers, G., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.08.012 · Cited by 279 · see citing works
Liu, C., Saito, F., Liu, Z., Lei, Y. L., Uehara, S., Love, P. E., Lipp, M., Kondo, S., Manley, N. R., & Takahama, Y. (2006) · Blood · doi:10.1182/blood-2006-05-024190 · Cited by 198 · see citing works
Oguro, H., Yuan, J., Ichikawa, H., Ikawa, T., Yamazaki, S., Kawamoto, H., Nakauchi, H., & Iwama, A. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.01.005 · Cited by 186 · see citing works
Self-citationAutonomous murine T-cell progenitor production in the extra-embryonic yolk sac before HSC emergence
Yoshimoto, M., Porayette, P., Glosson, N. L., Conway, S. J., Carlesso, N., Cardoso, A. A., Kaplan, M. H., & Yoder, M. C. (2012) · Blood · doi:10.1182/blood-2011-12-397489 · Cited by 178 · 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
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
Higashi, A. Y., Ikawa, T., Muramatsu, M., Economides, A. N., Niwa, A., Okuda, T., Murphy, A. J., Rojas, J., Heike, T., Nakahata, T., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0802413 · Cited by 143 · see citing works
Self-citationRecurrent SPI1 (PU.1) fusions in high-risk pediatric T cell acute lymphoblastic leukemia
Seki, M., Kimura, S., Isobe, T., Yoshida, K., Ueno, H., Nakajima-Takagi, Y., Wang, C., Lin, L., Kon, A., Suzuki, H., et al. (2017) · Nature Genetics · doi:10.1038/ng.3900 · Cited by 138 · see citing works
Self-citationCalderón, L., & Boehm, T. L. J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016428108 · Cited by 125 · see citing works
Kawamoto, H., & Katsura, Y. (2009) · Trends in Immunology · doi:10.1016/j.it.2009.03.001 · Cited by 118 · see citing works
Self-citationPeripheral PDGFRα+gp38+ mesenchymal cells support the differentiation of fetal liver–derived ILC2
Koga, S., Hozumi, K., Hirano, K.-I., Yazawa, M., Terooatea, T. W., Minoda, A., Nagasawa, T., Koyasu, S., & Moro, K. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20172310 · Cited by 116 · see citing works
A silent chemokine receptor regulates steady-state leukocyte homing in vivo
Heinzel, K., Benz, C., & Bleul, C. C. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608274104 · Cited by 107 · see citing works
Obaldia, M. E. D., Bell, J. J., Wang, X., Harly, C., Yashiro–Ohtani, Y., DeLong, J. H., Zlotoff, D. A., Sultana, D. A., Pear, W. S., & Bhandoola, A. (2013) · Nature Immunology · doi:10.1038/ni.2760 · Cited by 101 · 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
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
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
Self-citationGuo, Y., Maillard, I. P., Chakraborti, S., Rothenberg, E. V., & Speck, N. A. (2008) · Blood · doi:10.1182/blood-2007-10-120261 · Cited by 75 · see citing works
Furusawa, J.-I., Mizoguchi, I., Chiba, Y., Hisada, M., Kobayashi, F., Yoshida, H., Nakae, S., Tsuchida, A., Matsumoto, T., Ema, H., et al. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005507 · Cited by 71 · 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
Self-citationRothenberg, E. V., Ungerbäck, J., & Champhekar, A. (2016) · Advances in Immunology · doi:10.1016/bs.ai.2015.09.002 · Cited by 61 · see citing works
Initial seeding of the embryonic thymus by immune-restricted lympho-myeloid progenitors
Luis, T. C., Luc, S., Mizukami, T., Boukarabila, H., Thongjuea, S., Woll, P. S., Azzoni, E., Giustacchini, A., Lutteropp, M., Bouriez‐Jones, T., et al. (2016) · Nature Immunology · doi:10.1038/ni.3576 · Cited by 62 · see citing works
LRF-mediated Dll4 repression in erythroblasts is necessary for hematopoietic stem cell maintenance
Lee, S.-U., Maeda, M., Ishikawa, Y., Li, S. M., Wilson, A., Jubb, A. M., Sakurai, N., Weng, L., Fiorini, E., Radtke, F., et al. (2012) · Blood · doi:10.1182/blood-2012-03-418103 · Cited by 54 · see citing works
Self-citationThe 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
Tsuji, M., Shinkura, R., Kuroda, K., Yabe, D., & Honjo, T. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610520104 · 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
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Self-citationWatarai, H., Rybouchkin, A., Hongo, N., Nagata, Y., Sakata, S., Sekine-Kondo, E., Dashtsoodol, N., Tashiro, T., Fujii, S., Shimizu, K., et al. (2009) · Blood · doi:10.1182/blood-2009-04-217729 · Cited by 45 · see citing works
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Zhang, S., & Bhandoola, A. (2013) · Current topics in microbiology and immunology · doi:10.1007/82_2013_324 · Cited by 42 · see citing works
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Torii, I., Oka, S., Hotomi, M., Benjamin, W. H., Takai, T., Kearney, J. F., Briles, D. E., & Kubagawa, H. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.6.4229 · Cited by 33 · see citing works
Self-citationMeek, B., Cloosen, S., Borsotti, C., van Elssen, C. H. M. J., Vanderlocht, J., Schnijderberg, M. C. A., van der Poel, M., Leewis, B., Hesselink, R. P., Manz, M. G., et al. (2009) · Blood · doi:10.1182/blood-2009-05-223990 · Cited by 32 · see citing works
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Takai, T., Nakamura, A., & Endo, S. (2011) · BioMed Research International · doi:10.1155/2011/275302 · Cited by 32 · see citing works
Matsushita, H., Endo, S., Kobayashi, E., Sakamoto, Y., Kobayashi, K., Kitaguchi, K., Kuroki, K., Söderhäll, A., Maenaka, K., Nakamura, A., et al. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.157859 · Cited by 31 · see citing works
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Masuda, K., Germeraad, W. T. V., Satoh, R., Itoi, M., Ikawa, T., Minato, N., Katsura, Y., van Ewijk, W., & Kawamoto, H. (2009) · Molecular Immunology · doi:10.1016/j.molimm.2009.01.015 · Cited by 25 · see citing works
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Tenno, M., Kojo, S., Lawir, D.-F., Hess, I., Shiroguchi, K., Ebihara, T., Endo, T. A., Muroi, S., Satoh, R., Kawamoto, H., et al. (2018) · The Journal of Experimental Medicine · doi:10.1084/jem.20171221 · Cited by 23 · see citing works
Self-citationWang, C., Oshima, M., Sashida, G., Tomioka, T., Hasegawa, N., Mochizuki‐Kashio, M., Nakajima‐Takagi, Y., Kusunoki, Y., Kyoizumi, S., Imai, K., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132041 · Cited by 21 · see citing works
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Chidgey, A. P., & Boyd, R. L. (2006) · Nature Immunology · doi:10.1038/ni1006-1013 · Cited by 18 · see citing works
Montecino-Rodriguez, E., Casero, D., Fice, M., Le, J., & Dorshkind, K. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701336 · Cited by 17 · see citing works
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MacNabb, B. W., & Rothenberg, E. V. (2023) · Immunological Reviews · doi:10.1111/imr.13190 · Cited by 16 · see citing works
Desanti, G. E., Jenkinson, W. E., Parnell, S. M., Boudil, A., Gautreau‐Rolland, L., Eksteen, B., Ezine, S., Lane, P. J. L., Jenkinson, E. J., & Anderson, G. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1002686 · Cited by 16 · see citing works
Xing, Y., Wang, X., Igarashi, H., Kawamoto, H., & Sakaguchi, N. (2008) · Molecular Immunology · doi:10.1016/j.molimm.2007.10.028 · Cited by 15 · see citing works
Self-citationShin, B., & Rothenberg, E. V. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1108368 · Cited by 15 · see citing works
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Ganuza, M., Clements, W. K., & McKinney‐Freeman, S. (2021) · Blood · doi:10.1182/blood.2020009839 · Cited by 14 · see citing works
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Nakajima‐Takagi, Y., Oshima, M., Takano, J., Koide, S., Itokawa, N., Uemura, S., Yamashita, M., Andoh, S., Aoyama, K., Isshiki, Y., et al. (2023) · eLife · doi:10.7554/elife.83004 · Cited by 12 · see citing works
Self-citation今田, 道., Masuda, K., Satoh, R., Ito, Y., Goto, Y., Matsuoka, T., Endo, S., Nakamura, A., Kawamoto, H., & Takai, T. (2009) · International Immunology · doi:10.1093/intimm/dxp081 · Cited by 12 · see citing works
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Александрович, Р. С., & Lagarkova, M. A. (2019) · Biochemistry (Moscow) · doi:10.1134/s0006297919030027 · Cited by 11 · see citing works
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Kato, M., Masuda, K., Kakugawa, K., Kawamoto, H., Mugishima, H., & Katsura, Y. (2007) · European Journal Of Haematology · doi:10.1111/j.1600-0609.2007.00991.x · Cited by 7 · see citing works
Self-citationRothe, K., Raulien, N., Köhler, G., Pierer, M., Quandt, D., & Wagner, U. G. (2017) · European Journal of Immunology · doi:10.1002/eji.201646747 · Cited by 6 · see citing works
Rizq, O., Mimura, N., Oshima, M., Momose, S., Takayama, N., Itokawa, N., Koide, S., Shibamiya, A., Miyamoto-Nagai, Y., Rizk, M., et al. (2023) · Leukemia · doi:10.1038/s41375-023-01928-7 · Cited by 5 · see citing works
Li, X.-Q., Peng, W.-S., Qi, C., Zhang, H., Gao, M.-L., Wang, H., & Ren, F. (2015) · Neural Regeneration Research · doi:10.4103/1673-5374.160111 · Cited by 5 · see citing works
Sakaguchi, H., Matsuda, M., & Iwanami, N. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1517467 · Cited by 4 · see citing works
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Rothe, K., Quandt, D., Köhler, G., Jasinski‐Bergner, S., Seliger, B., Pierer, M., & Wagner, U. G. (2019) · Lara D. Veeken · doi:10.1093/rheumatology/kez256 · Cited by 4 · see citing works
Kugii, Y., Kuroki, Y., Hara, Y., Goitsuka, R., & Nakano, N. (2023) · The Journal of Immunology · doi:10.4049/jimmunol.2200748 · Cited by 1 · see citing works
Otsuka, R., Wada, H., Sasaki, A., Tsuji, H., Murata, T., Hasegawa, Y., Kaitani, A., Kitaura, J., & Seino, K. (2026) · Transplantation · doi:10.1097/tp.0000000000005795 · Cited by 1 · see citing works
Shibuya, K., & Nakano, N. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.08.155 · Cited by 1 · see citing works
Ezine, S., Gautreau‐Rolland, L., Parcelier, A., & Canque, B. (2009) · Humana Press eBooks · doi:10.1007/978-1-60327-347-3_4 · Cited by 1 · see citing works
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Kubagawa, H., Chen, C., Torii, I., Cooper, M. D., Masuda, K., Katsura, Y., & Kawamoto, H. (2008) · Springer eBooks · doi:10.1007/978-4-431-73884-8_3
Self-citationUnderstanding T cell recovery following thymus injury
Zhang, S. (2014) · Scholarly Commons (University of Pennsylvania)
Katsura, Y., Kawamoto, H., Germeraad, W. T. V., Bos, G. M. J., Schnijderberg, C. A., van der Poel, M., Leewis, B., Hesselink, R. P., Manz, M. G., Meek, B., et al. (2010)
Self-citationResearch Highlights: Immunomodulation
Wada, H., Kojo, S., & Seino, K. (2009) · Immunotherapy · doi:10.2217/imt.09.49
hematopoietic stem cell maintenance LRF-mediated Dll4 repression in erythroblasts is necessary for
Chen, C., Maeda, T., Weng, L., Fiorini, E., Radtke, F., Yan, M., MacDonald, H. R., Lee, S., Maeda, M., Ishikawa, Y., et al. (2013)
Self-citationTranscriptional Regulation of T Cell Lineage Commitment
Rothenberg, E. V. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-374279-7.04006-6
Generation and Regeneration of T Cells
Kawamoto, H., Ikawa, T., Maeda, T., & Masuda, K. (2016) · Springer eBooks · doi:10.1007/978-4-431-56027-2_2
Self-citationThe Heart of the Machine: Construction of T Cell Identity, Made Accessible
Rothenberg, E. V. (2022) · The Journal of Immunology · doi:10.4049/jimmunol.2200264
Transcriptional Regulation of T-Cell Lineage Commitment
Rothenberg, E. V. (2024) · Elsevier eBooks · doi:10.1016/b978-0-128-24465-4.00018-1
Bennett, L. F., Yu, W., Chen, C.-H., An, H. H., Tober, J. M., Tan, K., & Speck, N. A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.23.671940
Self-citationScagliotti, A., Depetro, I., Tiberi, G., Villegas, P. A. D., Candiello, E., & Cappello, P. (2026) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-026-03796-2
A study of the variation of leukocyte immunoglobulin-like receptors on antigen-presenting cells
Yong, P. (2013) · UPT. Syiah Kuala University Library (Syiah Kuala University)
Cellular immunotherapy : from stem cell to lymphocyte
Huijskens, M. J. A. J. (2015) · doi:10.26481/dis.20150212mh
- Authors
- Masuda, K., Kubagawa, H., Ikawa, T., Chen, C., Kakugawa, K., Hattori, M., Kageyama, R., Cooper, M. D., Minato, N., Katsura, Y., & Kawamoto, H.
- Affiliations
- Kyoto University (JP)
- University of Alabama (US)
- RIKEN (JP)
- Nihon University (JP)
- Corresponding author
- Kawamoto, Hiroshi
- ORCID
- Venue
- The EMBO Journal
- Published
- 2005-11-17
- Volume
- 24
- Issue
- 23
- Pages
- 4052-4060
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC1356317
- OpenAlex
- W1889701339
- Cited by
- 79
- References
- 56
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 2 · 2023: 5 · 2022: 2 · 2021: 2 · 2019: 4 · 2018: 3 · 2017: 3 · 2016: 4 · 2015: 4 · 2014: 2 · 2013: 5 · 2012: 3
- FWCI
- 2.37
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Keywords
- thymus colonization, natural killer cells, dendritic cells, CD25, Hes1, Notch signaling, thymic emigration, T cell progenitors
- MeSH terms
- Transcription Factor HES-1, Animals, Cell Differentiation, Cells, Cultured, Dendritic Cells, Killer Cells, Natural, Liver, Mice, Inbred BALB C, Mice, Inbred C57BL, Mice, Inbred ICR, Mice, Transgenic, Receptors, Antigen, T-Cell, Receptors, Immunologic, Stem Cells, T-Lymphocytes, Thymus Gland, Signal Transduction, Homeodomain Proteins, Cell Lineage, Mice, Basic Helix-Loop-Helix Transcription Factors, Basic Helix-Loop-Helix Proteins, Receptors, Notch
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