A Dynamic Role of TBX3 in the Pluripotency Circuitry
Open accessAbstract
Pluripotency represents a cell state comprising a fine-tuned pattern of transcription factor activity required for embryonic stem cell (ESC) self-renewal. TBX3 is the earliest expressed member of the T-box transcription factor family and is involved in maintenance and induction of pluripotency. Hence, TBX3 is believed to be a key member of the pluripotency circuitry, with loss of TBX3 coinciding with loss of pluripotency. We report a dynamic expression of TBX3 in vitro and in vivo using genetic reporter tools tracking TBX3 expression in mouse ESCs (mESCs). Low TBX3 levels are associated with reduced pluripotency, resembling the more mature epiblast. Notably, TBX3-low cells maintain the intrinsic capability to switch to a TBX3-high state and vice versa. Additionally, we show TBX3 to be dispensable for induction and maintenance of naive pluripotency as well as for germ cell development. These data highlight novel facets of TBX3 action in mESCs.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
TBX3 is critically involved in pluripotency maintenance and lineage-specific exit from the pluripotency circuitry in mouse embryonic stem cells.
“Finally, TBX3 is not only critically involved in pluripotency maintenance but also in lineage-specific exit from the pluripotency circuitry in mouse embryonic stem cells [11–17].”
From TBX3 is dynamically expressed in pancreatic organogenesis and fine-tunes regeneration (2023) · cites this paper as [11]
The Results section on lineage commitment reports that removing TBX3 changes differentiation in mouse ESCs, supporting its role in lineage-specific exit. But the Discussion explicitly says TBX3 is dispensable for maintaining pluripotency, contrary to the claim that it is critically required for maintenance. No page numbers are available in our copy. (LLM, conf=0.91)
Experimental — accuracy not yet measuredTbx3 seems expressed in a gradient in the pericentral zone.
“Tbx3, which has been shown to act in a dosage-sensitive manner in other contexts (50), seems to be expressed in a gradient in the pericentral zone (SI Appendix, Fig. S1A).”
From Wnt signaling regulates hepatocyte cell division by a transcriptional repressor cascade (2022) · cites this paper as [50]
Tbx3 acts in a dosage-sensitive manner in other contexts.
“Tbx3, which has been shown to act in a dosage-sensitive manner in other contexts (50)”
From Wnt signaling regulates hepatocyte cell division by a transcriptional repressor cascade (2022) · cites this paper as [50]
The Tbx3-Venus reporter system is validated.
“To visualize the activity of the murine Tbx3 promoter at the protein level, we used a validated Tbx3-Venus (Tbx3tm1(Venus)Vmc) [11, 42–47] reporter system (Fig. 2a).”
From TBX3 is dynamically expressed in pancreatic organogenesis and fine-tunes regeneration (2023) · cites this paper as [11]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Takahashi, K., & Yamanaka, S. (2006) · Cell · doi:10.1016/j.cell.2006.07.024 · Cited by 26,673 · see citing works
Spatial partitioning of the regulatory landscape of the X-inactivation centre
Nora, E. P., Lajoie, B. R., Schulz, E. G., Giorgetti, L., Okamoto, I., Servant, N., Piolot, T., van Berkum, N. L., Meisig, J., Sedat, J., et al. (2012) · Nature · doi:10.1038/nature11049 · Cited by 2,895 · see citing works
Nanog safeguards pluripotency and mediates germline development
Chambers, I., Silva, J. C. R., Colby, D., Nichols, J., Nijmeijer, B., Robertson, M., Vrána, J., Jones, K., Grotewold, L., & Smith, A. G. (2007) · Nature · doi:10.1038/nature06403 · Cited by 1,635 · see citing works
Single-Cell RNA-Seq Reveals Dynamic, Random Monoallelic Gene Expression in Mammalian Cells
Deng, Q., Ramsköld, D., Reinius, B., & Sandberg, R. (2014) · Science · doi:10.1126/science.1245316 · Cited by 1,345 · see citing works
Embryonic stem cell potency fluctuates with endogenous retrovirus activity
Macfarlan, T. S., Gifford, W. D., Driscoll, S. P., Lettieri, K., Rowe, H. M., Bonanomi, D., Firth, A. L., Singer, O., Trono, D., & Pfaff, S. L. (2012) · Nature · doi:10.1038/nature11244 · Cited by 1,109 · see citing works
Dissecting self-renewal in stem cells with RNA interference
Ivanova, N., Dobrin, R., Lu, R., Kotenko, I., Levorse, J. M., DeCoste, C. J., Schafer, X., Lun, Y., & Lemischka, I. R. (2006) · Nature · doi:10.1038/nature04915 · Cited by 959 · see citing works
A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells
Niwa, H., Ogawa, K., Shimosato, D., & Adachi, K. (2009) · Nature · doi:10.1038/nature08113 · Cited by 872 · see citing works
Self-citationGuo, G., Huss, M., Tong, G. Q., Wang, C., Sun, L., Clarke, N. D., & Robson, P. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.02.012 · Cited by 806 · see citing works
Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells
Stadtfeld, M., Apostolou, E., Akutsu, H., Fukuda, A., Follett, P., Natesan, S., Kono, T., Shioda, T., & Hochedlinger, K. (2010) · Nature · doi:10.1038/nature09017 · Cited by 801 · see citing works
limmaGUI: A graphical user interface for linear modeling of microarray data
Wettenhall, J. M., & Smyth, G. K. (2004) · Bioinformatics · doi:10.1093/bioinformatics/bth449 · Cited by 720 · see citing works
Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation
Baubec, T., Colombo, D. F., Wirbelauer, C., Schmidt, J., Burger, L., Krebs, A. R., Akalin, A., & Schübeler, D. (2015) · Nature · doi:10.1038/nature14176 · Cited by 705 · see citing works
Hayashi, K., Lopes, S. M. C. D. S., Tang, F., & Surani, M. A. (2008) · Cell stem cell · doi:10.1016/j.stem.2008.07.027 · Cited by 649 · see citing works
Senescence impairs successful reprogramming to pluripotent stem cells
Banito, A., Rashid, S. T., Acosta, J. C., Li, S., Pereira, C. F., Geti, I., Pinho, S., Silva, J. C., Azuara, V., Walsh, M., et al. (2009) · Genes & Development · doi:10.1101/gad.1811609 · Cited by 642 · see citing works
Regulated Fluctuations in Nanog Expression Mediate Cell Fate Decisions in Embryonic Stem Cells
Kalmár, T., Lim, C. L., Hayward, P. C., Descalzo, S. M., Nichols, J., García‐Ojalvo, J., & Arias, A. M. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000149 · Cited by 541 · see citing works
Identification and characterization of subpopulations in undifferentiated ES cell culture
Toyooka, Y., Shimosato, D., Murakami, K., Takahashi, K., & Niwa, H. (2008) · Development · doi:10.1242/dev.017400 · Cited by 525 · see citing works
Stochastic patterning in the mouse pre-implantation embryo
Dietrich, J. E., & Hiiragi, T. (2007) · Development · doi:10.1242/dev.003798 · Cited by 503 · see citing works
Defining the three cell lineages of the human blastocyst by single-cell RNA-seq
Blakeley, P., Fogarty, N. M. E., del Valle, I., Wamaitha, S. E., Hu, T. X., Elder, K. T., Snell, P., Christie, L., Robson, P., & Niakan, K. K. (2015) · Development · doi:10.1242/dev.123547 · Cited by 466 · see citing works
The Nature of Embryonic Stem Cells
Martello, G., & Smith, A. G. (2014) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100913-013116 · Cited by 428 · see citing works
Defining an essential transcription factor program for naïve pluripotency
Dunn, S.-J., Martello, G., Yordanov, B., Emmott, S., & Smith, A. G. (2014) · Science · doi:10.1126/science.1248882 · Cited by 370 · see citing works
The ground state of pluripotency
Wray, J. P., Kalkan, T., & Smith, A. G. (2010) · Biochemical Society Transactions · doi:10.1042/bst0381027 · Cited by 353 · see citing works
Regulatory networks define phenotypic classes of human stem cell lines
Müller, F.-J., Laurent, L. C., Kostka, D., Ulitsky, I., Williams, R., Lu, C., Park, I.-H., Rao, M. S., Shamir, R., Schwartz, P. H., et al. (2008) · Nature · doi:10.1038/nature07213 · Cited by 343 · see citing works
Pluripotency factors regulate definitive endoderm specification through eomesoderminPreprint
Teo, A. K. K., Arnold, S. J., Trotter, M. W. B., Brown, S. E., Ang, L. T., Chng, Z., Robertson, E. J., Dunn, N. R., & Vallier, L. (2011) · Genes & Development · doi:10.1101/gad.607311 · Cited by 338 · see citing works
Esrrb Is a Direct Nanog Target Gene that Can Substitute for Nanog Function in Pluripotent Cells
Festuccia, N., Osorno, R., Halbritter, F., Karwacki-Neisius, V., Navarro, P., Colby, D., Wong, F. C. K., Yates, A., Tomlinson, S. R., & Chambers, I. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.08.002 · Cited by 322 · see citing works
Defining the three cell lineages of the human blastocyst by single-cell RNA-seq
Blakeley, P., Fogarty, N. M. E., del Valle, I., Wamaitha, S. E., Hu, T. X., Elder, K. T., Snell, P., Christie, L., Robson, P., & Niakan, K. K. (2015) · Development · doi:10.1242/dev.131235 · Cited by 316 · see citing works
Davenport, T. G., Jerome-Majewska, L. A., & Papaioannou, V. E. (2003) · Development · doi:10.1242/dev.00431 · Cited by 295 · see citing works
Tbx3 improves the germ-line competency of induced pluripotent stem cells
Han, J., Yuan, P., Yang, H., Zhang, J., Soh, B. S., Li, P., Lim, S. L., Cao, S., Tay, J., Orlov, Y. L., et al. (2010) · Nature · doi:10.1038/nature08735 · Cited by 285 · see citing works
Aurbach-Klipper, Y., Wasserman, M., Braunspiegel-Weintrob, N., Borstein, D., Peleg, S., ASSA, S., Karp, M., Benjamini, Y., Hochberg, Y., & Laron, Z. (1995) · Medical Hypotheses · doi:10.1016/0306-9877(95)90228-7 · Cited by 258 · see citing works
Control of ground-state pluripotency by allelic regulation of Nanog
Miyanari, Y., & Torres‐Padilla, M. (2012) · Nature · doi:10.1038/nature10807 · Cited by 231 · see citing works
Epiblast Stem Cell Subpopulations Represent Mouse Embryos of Distinct Pregastrulation Stages
Han, D., Tàpia, N., Joo, J. Y., Greber, B., Araúzo-Bravo, M. J., Bernemann, C., Ko, K., Wu, G., Stehling, M., Tae, J., et al. (2010) · Cell · doi:10.1016/j.cell.2010.10.015 · Cited by 203 · see citing works
Self-citationBakker, M. L., Boukens, B. J., Mommersteeg, M. T. M., Brons, J. F., Wakker, V., Moorman, A. F. M., & Christoffels, V. M. (2008) · Circulation Research · doi:10.1161/circresaha.107.169565 · Cited by 199 · see citing works
Transcription factor heterogeneity in pluripotent stem cells: a stochastic advantage
Torres‐Padilla, M., & Chambers, I. (2014) · Development · doi:10.1242/dev.102624 · Cited by 198 · see citing works
Oct4 Cell-Autonomously Promotes Primitive Endoderm Development in the Mouse Blastocyst
Frum, T., Halbisen, M. A., Wang, C., Amiri, H., Robson, P., & Ralston, A. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.05.004 · Cited by 194 · see citing works
Radzisheuskaya, A., Chia, G., dos Santos, R. L., Theunissen, T. W., Castro, L. F. C., Nichols, J., & Silva, J. (2013) · Nature Cell Biology · doi:10.1038/ncb2742 · Cited by 191 · see citing works
Karwacki-Neisius, V., Göke, J., Osorno, R., Halbritter, F., Ng, J. H., Weiße, A. Y., Wong, F. C. K., Gagliardi, A., Mullin, N. P., Festuccia, N., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.04.023 · Cited by 177 · see citing works
Kurek, D., Neagu, A., Tastemel, M., Tüysüz, N., Lehmann, J., van de Werken, H. J. G., Philipsen, S., van der Linden, R., Maas, A., van IJcken, W. F. J., et al. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.11.007 · Cited by 157 · see citing works
Czechanski, A., Byers, C., Greenstein, I., Schrode, N., Donahue, L. R., Hadjantonakis, A., & Reinholdt, L. G. (2014) · Nature Protocols · doi:10.1038/nprot.2014.030 · Cited by 156 · see citing works
Generation ofstella-GFP transgenic mice: A novel tool to study germ cell development
Payer, B., Lopes, S. M. C. D. S., Barton, S. C., Lee, C. G. L., Saitou, M., & Surani, M. A. (2006) · genesis · doi:10.1002/gene.20187 · Cited by 150 · see citing works
Derivation of mouse embryonic stem cells
Bryja, V., Bonilla, S., & Arenas, E. (2006) · Nature Protocols · doi:10.1038/nprot.2006.355 · Cited by 139 · see citing works
Nanog-dependent feedback loops regulate murine embryonic stem cell heterogeneity
MacArthur, B. D., Sevilla, A., Lenz, M., Müller, F.-J., Schuldt, B. M., Schuppert, A., Ridden, S. J., Stumpf, P. S., Fidalgo, M., Ma’ayan, A., et al. (2012) · Nature Cell Biology · doi:10.1038/ncb2603 · Cited by 137 · see citing works
Stochastic NANOG fluctuations allow mouse embryonic stem cells to explore pluripotency
Abranches, E., Guedes, A. M. V., Moravec, M., Maamar, H., Svoboda, P., Raj, A., & Henrique, D. (2014) · Development · doi:10.1242/dev.108910 · Cited by 134 · see citing works
Heterogeneities in Nanog Expression Drive Stable Commitment to Pluripotency in the Mouse Blastocyst
Xenopoulos, P., Kang, M., Puliafito, A., Talia, S. D., & Hadjantonakis, A. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.02.010 · Cited by 124 · see citing works
Loss of ATM accelerates pancreatic cancer formation and epithelial–mesenchymal transition
Russell, R., Perkhofer, L., Liebau, S., Lin, Q., Lechel, A., Feld, F. M., Hessmann, E., Gaedcke, J., Güthle, M., Zenke, M., et al. (2015) · Nature Communications · doi:10.1038/ncomms8677 · Cited by 109 · see citing works
Self-citationGertsenstein, M., Nutter, L. M. J., Reid, T., Pereira, M., Stanford, W. L., Rossant, J., & Nagy, A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011260 · Cited by 108 · see citing works
Schrode, N., Xenopoulos, P., Piliszek, A., Frankenberg, S., Płusa, B., & Hadjantonakis, A. (2013) · genesis · doi:10.1002/dvg.22368 · Cited by 107 · see citing works
Bernemann, C., Greber, B., Ko, K., Sterneckert, J. L., Han, D., Araúzo-Bravo, M. J., & Schöler, H. R. (2011) · Stem Cells · doi:10.1002/stem.709 · Cited by 105 · see citing works
Self-citationFaddah, D. A., Wang, H., Cheng, A. W., Yarden Katz, A., Buganim, Y., & Jaenisch, R. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.04.019 · Cited by 104 · see citing works
Horsthuis, T., Buermans, H. P. J., Brons, J. F., Verkerk, A. O., Bakker, M. L., Wakker, V., Clout, D. E. W., Moorman, A. F. M., Hoen, P. A. C. ’., & Christoffels, V. M. (2009) · Circulation Research · doi:10.1161/circresaha.108.192443 · Cited by 91 · see citing works
Kartikasari, A. E. R., Zhou, J. X., Kanji, M. S., Chan, D. N., Sinha, A., Grapin‐Botton, A., Magnuson, M. A., Lowry, W. E., & Bhushan, A. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.78 · Cited by 90 · see citing works
Coordinated control of senescence by lncRNA and a novel T-box3 co-repressor complex
Pavan Kumar, P., Emechebe, U., Smith, R. A., Franklin, S., Moore, B., Yandell, M. D., Lessnick, S. L., & Moon, A. (2014) · eLife · doi:10.7554/elife.02805 · Cited by 86 · see citing works
Self-citationLu, R., Yang, A., & Jin, Y. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.202150 · Cited by 80 · see citing works
Sugimoto, M., Kondo, M., Koga, Y., Shiura, H., Ikeda, R., Hirose, M., Ogura, A., Murakami, A., Yoshiki, A., Lopes, S. M. C. D. S., et al. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.02.014 · Cited by 79 · see citing works
TBX3 Directs Cell-Fate Decision toward Mesendoderm
Weidgang, C. E., Russell, R., Tata, P. R., Kühl, S. J., Illing, A., Müller, M., Lin, Q., Brunner, C., Boeckers, T. M., Bauer, K., et al. (2013) · Stem Cell Reports · doi:10.1016/j.stemcr.2013.08.002 · Cited by 78 · see citing works
Self-citationTranscriptome-wide Variability in Single Embryonic Development Cells
Piras, V., Tomita, M., & Selvarajoo, K. (2014) · Scientific Reports · doi:10.1038/srep07137 · Cited by 73 · see citing works
Chen, Y., Blair, K. A., & Smith, A. G. (2013) · Stem Cell Reports · doi:10.1016/j.stemcr.2013.07.003 · Cited by 68 · see citing works
Rebuilding Pluripotency from Primordial Germ Cells
Leitch, H. G., Nichols, J., Humphreys, P. D., Mulas, C., Martello, G., Lee, C. Y., Jones, K., Surani, M. A., & Smith, A. G. (2013) · Stem Cell Reports · doi:10.1016/j.stemcr.2013.03.004 · Cited by 67 · see citing works
Nishiyama, A., Sharov, A. A., Piao, Y., Amano, M., Amano, T., Hoang, H. G., Binder, B. Y. K., Tapnio, R., Bassey, U. C., Malinou, J. N., et al. (2013) · Scientific Reports · doi:10.1038/srep01390 · Cited by 65 · see citing works
Linta, L., Stockmann, M., Kleinhans, K. N., Böckers, A., Storch, A., Zaehres, H., Lin, Q., Barbi, G., Böckers, T. M., Kleger, A., et al. (2012) · Stem Cells and Development · doi:10.1089/scd.2011.0026 · Cited by 65 · see citing works
Self-citationXu, X., Smorag, L., Nakamura, T., Kimura, T., Dressel, R., Fitzner, A., Tan, X., Linke, M., Zechner, U., Engel, W., et al. (2015) · Nature Communications · doi:10.1038/ncomms7008 · Cited by 61 · see citing works
Kleger, A., Mahaddalkar, P. U., Katz, S., Lechel, A., Joo, J. Y., Loya, K., Lin, Q., Hartmann, D., Liebau, S., Kraus, J. M., et al. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.01.004 · Cited by 51 · see citing works
Self-citationTbx3 Controls Dppa3 Levels and Exit from Pluripotency toward Mesoderm
Waghray, A., Saiz, N., Jayaprakash, A. D., Freire, A. G., Papatsenko, D., Pereira, C.-F., Lee, D.-F., Brosh, R., Chang, B., Darr, H., et al. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.05.009 · Cited by 50 · see citing works
Papatsenko, D., Darr, H., Kulakovskiy, I. V., Waghray, A., Makeev, V. J., MacArthur, B. D., & Lemischka, I. R. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.07.004 · Cited by 43 · see citing works
Lee, D., Su, J., Sevilla, A., Gingold, J. A., Schaniel, C., & Lemischka, I. R. (2012) · Nature Protocols · doi:10.1038/nprot.2012.018 · Cited by 41 · see citing works
Developmental and Functional Nature of Human iPSC Derived Motoneurons
Stockmann, M., Linta, L., Föhr, K. J., Boeckers, A., Ludolph, A. C., Kuh, G. F., Udvardi, P. T., Proepper, C., Storch, A., Kleger, A., et al. (2011) · Stem Cell Reviews and Reports · doi:10.1007/s12015-011-9329-4 · Cited by 39 · see citing works
Self-citationMouse Tbx3 Mutants Suggest Novel Molecular Mechanisms for Ulnar-Mammary Syndrome
Frank, D. U., Emechebe, U., Thomas, K. R., & Moon, A. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067841 · Cited by 39 · cited 12× · see citing works
“They also successfully formed all-PSC-derived mouse embryos in a 4n assay displaying the reported TBX3-null phenotypes (Davenport et al., 2003; Frank et al., 2013).”
BackgroundMethodResultInfluentialSelf-citationSuccessful Reprogramming of Epiblast Stem Cells by Blocking Nuclear Localization of β-Catenin
Murayama, H., Masaki, H., Sato, H., Hayama, T., Yamaguchi, T., & Nakauchi, H. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.12.003 · Cited by 30 · see citing works
Dynamic expression of Tbx2 subfamily genes in development of the mouse reproductive system
Douglas, N. C., Heng, K., Sauer, M. V., & Papaioannou, V. E. (2011) · Developmental Dynamics · doi:10.1002/dvdy.23710 · Cited by 24 · see citing works
Kunasegaran, K., Ho, V., Chang, T. H. T., De Silva, D., Bakker, M. L., Christoffels, V. M., & Pietersen, A. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110191 · Cited by 18 · see citing works
A Fresh Look on T-Box Factor Action in Early Embryogenesis (T-Box Factors in Early Development)
Bertolessi, M., Linta, L., Seufferlein, T. T. W., Kleger, A., & Liebau, S. (2015) · Stem Cells and Development · doi:10.1089/scd.2015.0102 · Cited by 10 · see citing works
Self-citationInvestigating the Role of Tbx4 in the Female Germline in Mice1
Douglas, N. C., Arora, R., Chen, C. Y., Sauer, M. V., & Papaioannou, V. E. (2013) · Biology of Reproduction · doi:10.1095/biolreprod.113.107649 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Excluding Oct4 from Yamanaka Cocktail Unleashes the Developmental Potential of iPSCs
Velychko, S., Adachi, K., Kim, K.-P., Hou, Y., MacCarthy, C. M., Wu, G., & Schöler, H. R. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.10.002 · Cited by 131 · see citing works
Self-citationSingle-cell measurement of higher-order 3D genome organization with scSPRITE
Arrastia, M. V., Jachowicz, J. W., Ollikainen, N., Curtis, M. S., Lai, C., Quinodoz, S. A., Selck, D. A., Ismagilov, R. F., & Guttman, M. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-00998-1 · Cited by 126 · see citing works
The roles and regulation of TBX3 in development and disease
Khan, S. F., Damerell, V., Omar, R., Du Toit, M., Khan, M., Maranyane, H. M., Mlaza, M., Bleloch, J., Bellis, C., Sahm, B. D. B., et al. (2020) · Gene · doi:10.1016/j.gene.2019.144223 · Cited by 99 · see citing works
“Interestingly, two studies showed that Tbx3/TBX3 is not entirely critical for the tenacity or generation of iPSCs (Klingenstein et al., 2016; Russell et al., 2015).”
BackgroundThe principles that govern transcription factor network functions in stem cells
Niwa, H. (2018) · Development · doi:10.1242/dev.157420 · Cited by 74 · see citing works
From pluripotency to totipotency: an experimentalist's guide to cellular potency
Riveiro, A. R., & Brickman, J. M. (2020) · Development · doi:10.1242/dev.189845 · Cited by 64 · see citing works
Disruption of GRIN2B Impairs Differentiation in Human Neurons
Bell, S., Maussion, G., Jefri, M., Peng, H., Théroux, J., Silveira, H., Soubannier, V., Wu, H., Hu, P., Galat, Y., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.05.018 · Cited by 67 · see citing works
Dong, C., Fu, S., Karvas, R. M., Chew, B., Fischer, L. A., Xing, X., Harrison, J. K., Popli, P., Kommagani, R., Wang, T., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-30207-9 · Cited by 58 · see citing works
Hulett, R. E., Kimura, J. O., Bolanos, D. M., Luo, Y., Rivera-López, C., Ricci, L., & Srivastava, M. (2023) · Nature Communications · doi:10.1038/s41467-023-38016-4 · Cited by 55 · see citing works
Transitions in cell potency during early mouse development are driven by Notch
Menchero, S., Lopez-Izquierdo, A., Rollán, I., de Aja, J. S., Andreu, M. J., Kang, M., Adan, J., Benedito, R., Rayón, T., Hadjantonakis, A., et al. (2019) · eLife · doi:10.7554/elife.42930 · Cited by 48 · see citing works
Lu, Y., Kweon, S., Cai, Q., Tanikawa, C., Shu, X., Jia, W., Xiang, Y., Huyghe, J. R., Harrison, T. A., Kim, J., et al. (2019) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-19-0755 · Cited by 44 · see citing works
Bernardo, A. S., Jouneau, A., Marks, H., Kensche, P. R., Kobolák, J., Freude, K., Hall, V. J., Fehér, A., Polgár, Z., Sartori, C., et al. (2018) · Biology Open · doi:10.1242/bio.033282 · Cited by 42 · see citing works
Optimization of Cas9 activity through the addition of cytosine extensions to single-guide RNAs
Kawamata, M., Suzuki, H. I., Kimura, R., & Suzuki, A. (2023) · Nature Biomedical Engineering · doi:10.1038/s41551-023-01011-7 · Cited by 42 · see citing works
Embryonic origins of adult pluripotent stem cells
Kimura, J. O., Bolanos, D. M., Ricci, L., & Srivastava, M. (2022) · Cell · doi:10.1016/j.cell.2022.11.008 · Cited by 38 · see citing works
Perkhofer, L., Walter, K., Costa, I. G., Carrasco, M. C. R., Eiseler, T., Hafner, S., Genze, F., Zenke, M., Bergmann, W., Illing, A., et al. (2016) · Stem Cell Research · doi:10.1016/j.scr.2016.08.007 · Cited by 39 · see citing works
Self-citationThe special stemness functions of Tbx3 in stem cells and cancer development
Dong, L., Lyu, X., Faleti, O. D., & He, M.-L. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.09.010 · Cited by 41 · see citing works
Ichimura, H., Kadota, S., Kashihara, T., Yamada, M., Ito, K., Kobayashi, H., Tanaka, Y., Shiba, N., Chuma, S., Tohyama, S., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-68373-9 · Cited by 36 · see citing works
Esrrb extinction triggers dismantling of naïve pluripotency and marks commitment to differentiation
Festuccia, N., Halbritter, F., Corsinotti, A., Gagliardi, A., Colby, D., Tomlinson, S. R., & Chambers, I. (2018) · The EMBO Journal · doi:10.15252/embj.201695476 · Cited by 33 · see citing works
Capturing Human Naïve Pluripotency in the Embryo and in the Dish
Zimmerlin, L., Park, T. S., & Zambidis, E. T. (2017) · Stem Cells and Development · doi:10.1089/scd.2017.0055 · Cited by 31 · see citing works
Djeghloul, D., Dimond, A., Cheriyamkunnel, S., Kramer, H. B., Patel, B., Brown, K., Montoya, A., Whilding, C., Wang, Y.-F., Futschik, M., et al. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-00943-7 · Cited by 25 · see citing works
Wnt signaling regulates hepatocyte cell division by a transcriptional repressor cascade
Jin, Y., Anbarchian, T., Wu, P., Sarkar, A., Fish, M., Peng, W. C., & Nusse, R. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2203849119 · Cited by 26 · see citing works
“Tbx3, which has been shown to act in a dosage-sensitive manner in other contexts (50), seems to be expressed in a gradient in the pericentral zone (SI Appendix, Fig.”
BackgroundWang, M., Tang, L. F. P., Liu, D., Ying, Q., & Ye, S. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.803254 · Cited by 25 · see citing works
The spatial binding model of the pioneer factor Oct4 with its target genes during cell reprogramming
Li, H., Ta, N., Long, C., Zhang, Q.-T., Li, S., Liu, S., Yang, L., & Zuo, Y. (2019) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2019.09.002 · Cited by 23 · see citing works
Yi, C., Song, H., Liang, H., Ran, Y., Tang, J., Chen, E., Li, F., Fu, L., Wang, Y.-Q., Chen, F., et al. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.130220 · Cited by 21 · see citing works
Wang, X. L., Ping, C., Tan, P., Sun, C., Liu, G., Liu, T., Yang, S., Si, Y., Zhao, L., Hu, Y., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2020104729 · Cited by 19 · see citing works
Post-Transcriptional Regulation of Molecular Determinants during Cardiogenesis
Lozano-Velasco, E., García‐Padilla, C., Muñoz-Gallardo, M. D. M., Martínez-Amaro, F. J., Caño-Carrillo, S., Castillo-Casas, J. M., Sánchez–Fernández, C., Aránega, A. E., & Franco, D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052839 · Cited by 20 · see citing works
Chen, Z., Guo, X., Tao, R., Huyghe, J. R., Law, P., Fernández–Rozadilla, C., Ping, J., Jia, G., Long, J., Li, C., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-47399-x · Cited by 21 · see citing works
Derivation of induced pluripotent stem cells from ferret somatic cells
Gao, J., Petraki, S., Sun, X., Brooks, L. A., Lynch, T. J., Hsieh, C., Elteriefi, R., Lorenzana, Z., Punj, V., Engelhardt, J. F., et al. (2020) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00456.2019 · Cited by 19 · see citing works
Liu, Y., Lu, P., Wang, Y., Morrow, B. E., Zhou, B., & Zheng, D. (2019) · Journal of the American Heart Association · doi:10.1161/jaha.119.012941 · Cited by 15 · see citing works
Arnold, F., Mahaddalkar, P. U., Kraus, J. M., Zhong, X., Bergmann, W., Srinivasan, D., Gout, J., Roger, E., Beutel, A. K., Zizer, E., et al. (2021) · Advanced Science · doi:10.1002/advs.202100626 · Cited by 18 · see citing works
Self-citationWang, D., Sang, H., Zhang, K., Nie, Y., Zhao, S., Zhang, Y., He, N., Wang, Y., Xu, Y., Xie, X., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.16112 · Cited by 13 · see citing works
Shared features of blastula and neural crest stem cells evolved at the base of vertebrates
York, J. R., Rao, A. N., Huber, P. B., Schock, E. N., Montequin, A., Rigney, S., & LaBonne, C. (2024) · Nature Ecology & Evolution · doi:10.1038/s41559-024-02476-8 · Cited by 11 · see citing works
Ke, M., He, Q., Hong, D., Li, O., Zhu, M. ⁄., Ou, W., He, Y., & Wu, Y. (2018) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2018.3610 · Cited by 11 · see citing works
Li, Q. V., Rosen, B. P., & Huangfu, D. (2019) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1464 · Cited by 13 · see citing works
Bcl-2 Overexpression Induces Neurite Outgrowth via the Bmp4/Tbx3/NeuroD1 Cascade in H19-7 Cells
Lee, Y. Y., Choi, H. J., Lee, S. Y., Park, S., Kang, M.-J., Han, J., & Han, J. (2019) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-019-00732-1 · Cited by 11 · see citing works
Xie, S., Choudhari, S., Wu, C., Abramson, K., Corcoran, D. L., Gregory, S. G., Thimmapuram, J., Guilak, F., & Little, D. (2023) · The FASEB Journal · doi:10.1096/fj.202201413r · Cited by 10 · see citing works
Климанова, Е. А., Sidorenko, S. V., Smolyaninova, L. V., Капилевич, Л. В., Gusakova, S. V., Lopina, O. D., & Orlov, S. N. (2019) · Current topics in membranes · doi:10.1016/bs.ctm.2019.01.006 · Cited by 10 · see citing works
Reprogramming to pluripotency does not require transition through a primitive streak-like state
Raab, S., Klingenstein, M., Möller, A., Illing, A., Tošić, J., Breunig, M., Kuales, G., Linta, L., Seufferlein, T. T. W., Arnold, S. J., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-15187-x · Cited by 9 · see citing works
Self-citationHuang, Y., Zhu, H., Ji, X., Chen, Y., Zhang, Y., Huang, R., Xie, J., & Dong, P. (2019) · Oncology Letters · doi:10.3892/ol.2019.11089 · Cited by 9 · see citing works
Epigenome-wide effects of vitamin D on asthma bronchial epithelial cells
Boutaoui, N., Puranik, S., Zhang, R., Wang, T., Hui, D. H., Brehm, J. M., Forno, E., Chen, W., & Celedon, J. C. (2019) · Epigenetics · doi:10.1080/15592294.2019.1622993 · Cited by 8 · see citing works
Aloisio, F. M., & Barber, D. L. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.05.002 · Cited by 7 · see citing works
Jauregi‐Miguel, A., Söderholm, S., Weiss, T., Nordin, A., Ghezzi, V., Brütsch, S. M., Pagella, P., van de Grift, Y. B. C., Zambanini, G., Ulisse, J., et al. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2419691122 · Cited by 6 · see citing works
A suboptimal OCT4-SOX2 binding site facilitates the naïve-state specific function of a Klf4 enhancer
Waite, J. B., Boytz, R., Traeger, A. R., Lind, T. M., Lumbao-Conradson, K., & Torigoe, S. E. (2024) · PLoS ONE · doi:10.1371/journal.pone.0311120 · Cited by 6 · see citing works
Dries, R., Stryjewska, A., Coddens, K., Okawa, S., Notelaers, T., Birkhoff, J. C., Dekker, M. R., Verfaillie, C. M., del Sol, A., Mulugeta, E., et al. (2019) · Stem Cells · doi:10.1002/stem.3111 · Cited by 6 · see citing works
TBX3 is dynamically expressed in pancreatic organogenesis and fine-tunes regeneration
Melzer, M. K., Schirge, S., Gout, J., Arnold, F., Srinivasan, D., Burtscher, I., Allgöwer, C., Mulaw, M., Zengerling, F., Günes, C., et al. (2023) · BMC Biology · doi:10.1186/s12915-023-01553-x · Cited by 5 · see citing works
Self-citationDCP1A, a MEK substrate, regulates the self-renewal and differentiation of mouse embryonic stem cells
Yu, J., Zhao, N., Wang, Y., Ding, N., Guo, Z., He, Z., Zhang, Q., Zhang, J., Yang, X., Zhang, M., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.115058 · Cited by 5 · see citing works
Dey, C., Raina, K., Thool, M., Adhikari, P., Haridhasapavalan, K. K., Sundaravadivelu, P. K., Venkatesan, V., Gogoi, R., Selvaraju, S., & Thummer, R. P. (2021) · Elsevier eBooks · doi:10.1016/b978-0-323-90059-1.00007-5 · Cited by 5 · see citing works
Fetal Mammary Gland Development and Offspring’s Breast Cancer Risk in Adulthood
Mabasa, L., Kotze, A., Sangweni, N. F., Willmer, T., Gabuza, K., Patel, O., Omoruyi, S. I., Burns, A., & Johnson, R. (2025) · Biology · doi:10.3390/biology14020106 · Cited by 4 · see citing works
Characterization of an eye field-like state during optic vesicle organoid development
Owen, L. J., Rainger, J. K., Bengani, H., Kilanowski, F. M., FitzPatrick, D. R., & Papanastasiou, A. S. (2023) · Development · doi:10.1242/dev.201432 · Cited by 4 · see citing works
Jauregi‐Miguel, A., Söderholm, S., Weiss, T., Nordin, A., Ghezzi, V., Brütsch, S. M., Pagella, P., van de Grift, Y. B. C., Zambanini, G., Ulisse, J., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.18.571901 · Cited by 3 · see citing works
Li, X., Chen, P., Ji, J.-X., Duan, Q., Cao, J., Huang, R., & Ye, S.-D. (2023) · Cell & Bioscience · doi:10.1186/s13578-023-01096-2 · Cited by 2 · see citing works
KDM3A and KDM3B regulate alternative splicing in mouse pluripotent stem cells
Dillingham, C. M., Cormaty, H., Morgan, E. C., Tak, A. I., Esgdaille, D. E., Boutz, P. L., & Sridharan, R. (2025) · iScience · doi:10.1016/j.isci.2025.112612 · Cited by 1 · see citing works
Menchero, S. (2019) · doi:10.4321/repisalud.7169 · Cited by 1 · see citing works
KDM3A and KDM3B Maintain Naïve Pluripotency Through the Regulation of Alternative SplicingPreprint
Dillingham, C. M., Cormaty, H., Morgan, E. C., Tak, A. I., Esgdaille, D. E., Boutz, P. L., & Sridharan, R. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.31.543088 · Cited by 1 · see citing works
Jin, G., Porello, E. A. L., Zhang, J., & Lim, B. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.17.643751 · Cited by 1 · see citing works
Lost but Still Missed: A New Chapter about TBX3 in Pluripotency and Fate Decision
Ilg, M. M., Muller, M., Liebau, S., & Kleger, A. (2016) · Journal of Cell Signaling · doi:10.4172/2576-1471.1000105
Self-citationGarbutt, T. A., Konganti, K., Konneker, T., Hillhouse, A., Phelps, D. W., Jones, A., Aylor, D. L., & Threadgill, D. W. (2020) · Mammalian Genome · doi:10.1007/s00335-020-09849-x
Programmable downsizing of CRISPR-Cas9 activity for precise and safe genome editingPreprint
Kawamata, M., Suzuki, H. I., Kimura, R., & Suzuki, A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.31.361733
Modellsysteme in der gastroenterologischen Forschung
Arnold, F., & Kleger, A. (2021) · Der Pathologe · doi:10.1007/s00292-021-00996-9
Self-citationFaculty Opinions recommendation of Disruption of GRIN2B impairs differentiation in human neurons.
Traynelis, S. F. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.733506834.793567065
Melzer, M. K., Schirge, S., Gout, J., Arnold, F., Srinivasan, D., Burtscher, I., Allgöwer, C., Mulaw, M., Zengerling, F., Güneş, Ç., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26576153
Self-citationLi, X., Chen, P., Ji, J., Duan, Q., Cao, J., Huang, R. C. C., & Ye, S. (2023) · Figshare · doi:10.6084/m9.figshare.23908832
Melzer, M. K., Schirge, S., Gout, J., Arnold, F., Srinivasan, D., Burtscher, I., Allgöwer, C., Mulaw, M., Zengerling, F., Güneş, Ç., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26576156
Self-citationMelzer, M. K., Schirge, S., Gout, J., Arnold, F., Srinivasan, D., Burtscher, I., Allgöwer, C., Mulaw, M., Zengerling, F., Güneş, Ç., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26576162
Self-citationMelzer, M. K., Schirge, S., Gout, J., Arnold, F., Srinivasan, D., Burtscher, I., Allgöwer, C., Mulaw, M., Zengerling, F., Güneş, Ç., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26576159
Self-citationNanog mediated control of TBX3-GATA6 circuitry in primitive endoderm differentiation of mESCs
Wu, H., Ye, Y., Dai, H., Chen, P., Yang, T., Li, Z., Li, L., Parsania, C., Ding, J., Zhang, M., et al. (2026) · EMBO Reports · doi:10.1038/s44319-026-00707-6
AMPK-p38 axis converts human pluripotent stem cells to naive state
Yang, Z., Liu, Y., Xu, H., Yamane, J., Hotta, A., Fujibuchi, W., & Yamashita, J. K. (2026) · iScience · doi:10.1016/j.isci.2026.115569
LIF signaling pathway regulates the heterogeneous Sox2 transcriptional dynamics in mESCs
Jin, G., Porello, E. A. L., Zhang, J., Vidal, J. A., & Lim, B. (2026) · Scientific Reports · doi:10.1038/s41598-026-46330-2 · Cited by 1 · see citing works
Liao, Y., Yang, J., Kuo, H., Chen, Y., Lin, Y., Sachdev, S., Kim, D., Roberts, R. M., Yuan, Y., & Ezashi, T. (2026) · FEBS Journal · doi:10.1111/febs.70733
- Authors
- Russell, R., Ilg, M., Lin, Q., Wu, G., Lechel, A., Bergmann, W., Eiseler, T., Linta, L., Kumar P., P., Klingenstein, M., Adachi, K., Hohwieler, M., Sakk, O., Raab, S., Moon, A., Zenke, M., Seufferlein, T., Schöler, H. R., Illing, A., Liebau, S., & Kleger, A.
- Affiliations
- Universität Ulm (DE)
- RWTH Aachen University (DE)
- Max Planck Institute for Molecular Biomedicine (DE)
- University of Tübingen (DE)
- Geisinger Medical Center (US)
- Corresponding author
- Kleger, Alexander
- ORCID
- Venue
- Stem Cell Reports
- Publisher
- Elsevier BV
- Published
- 2015-12
- Volume
- 5
- Issue
- 6
- Pages
- 1155-1170
- ISSN
- 2213-6711 (ISSN-L)
- PMC
- PMC4682344
- OpenAlex
- W2191957884
- Cited by
- 66
- References
- 69
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 6 · 2023: 10 · 2022: 5 · 2021: 5 · 2020: 6 · 2019: 14 · 2018: 6 · 2017: 4 · 2016: 2
- FWCI
- 1.74
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Stem Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Max Planck Institute for Plasma Physics (submittedVersion)
- RWTH Publications (RWTH Aachen) (submittedVersion, other-oa)
- RWTH Publications (RWTH Aachen)
- Funders
- Deutsche Forschungsgemeinschaft (BO1718/4-1, K.L. 2544/1-1, ZE432/5-2)
- Else Kröner-Fresenius-Stiftung (2011_A200)
- Medizinischen Fakultät, Eberhard Karls Universität Tübingen
- Baden-Württemberg Stiftung
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- TBX3, pluripotency, embryonic stem cells, T-box transcription factor, naive pluripotency, epiblast, self-renewal, germ cell development, transcriptional circuitry
- MeSH terms
- Mouse Embryonic Stem Cells, Animals, Cells, Cultured, Gene Deletion, T-Box Domain Proteins, Cell Proliferation, Mice, Cellular Reprogramming
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