TBX3 Promotes Human Embryonic Stem Cell Proliferation and Neuroepithelial Differentiation in a Differentiation Stage-Dependent Manner
Open accessAbstract
T-box 3 (Tbx3) is a member of the T-box family of genes. Mutations that result in the haploinsufficiency of TBX3 cause ulnar mammary syndrome in humans characterized by mammary gland hypoplasia as well as other congenital defects. In mice, homozygous mutations are embryonic lethal, suggesting that Tbx3 is essential for embryo development. Studies in mice have shown that Tbx3 is essential in the maintenance of mouse embryonic stem cell (ESC) self-renewal and in their differentiation into extraembryonic endoderm (ExEn). The role TBX3 plays in regulating human ESCs (hESCs) has not been explored. Since mouse and hESCs are known to represent distinct pluripotent states, it is important to address the role of TBX3 in hESC self-renewal and differentiation. Using overexpression and knockdown strategies, we found that TBX3 overexpression promotes hESC proliferation possibly by repressing the expression of both NFκBIB and p14ARF, known cell cycle regulators. During differentiation, TBX3 knockdown resulted in decreased neural rosette formation and in decreased expression of neuroepithelial and neuroectoderm markers (PAX6, LHX2, FOXG1, and RAX). Taken together, our data suggest a role for TBX3 in hESC proliferation and reveal an unrecognized novel role of TBX3 in promoting neuroepithelial differentiation. Our results suggest that TBX3 plays distinct roles in regulating self-renewal and differentiation in both hESCs and mouse ESCs.
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 can enhance the proliferation of human embryonic stem cells by inhibiting p14ARF and NF-κB.
“TBX3 can enhance the proliferation of human embryonic stem cells by inhibiting p14ARF and NF-κB, which are regulators of the NF-κB signaling pathway 61.”
From TBX3 shapes an immunosuppressive microenvironment and induces immunotherapy resistance (2025) · cites this paper as [61]
The Results and Discussion report that TBX3 over-expression increases human embryonic stem cell proliferation and represses p14ARF. They identify the other repressed molecule as NFκBIB, an inhibitor of NF-κB—not NF-κB itself—and describe the proposed mechanism as possible rather than established. (LLM, conf=0.89)
Experimental — accuracy not yet measured
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
Embryonic Stem Cell Lines Derived from Human Blastocysts
Thomson, J. A., Itskovitz‐Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S., & Jones, J. M. (1998) · Science · doi:10.1126/science.282.5391.1145 · Cited by 15,947 · see citing works
Nuclear factor-κB in cancer development and progression
Karin, M. (2006) · Nature · doi:10.1038/nature04870 · Cited by 3,519 · see citing works
CNS stem cells express a new class of intermediate filament protein
Lendahl, U., Zimmerman, L. B., & McKay, R. D. G. (1990) · Cell · doi:10.1016/0092-8674(90)90662-x · Cited by 3,164 · see citing works
New cell lines from mouse epiblast share defining features with human embryonic stem cells
Tesar, P. J., Chenoweth, J. G., Brook, F. A., Davies, T. J., Evans, E. P., Mack, D. L., Gardner, R. L., & McKay, R. D. G. (2007) · Nature · doi:10.1038/nature05972 · Cited by 2,153 · see citing works
Ying, Q.-L., Nichols, J., Chambers, I., & Smith, A. G. (2003) · Cell · doi:10.1016/s0092-8674(03)00847-x · Cited by 2,114 · see citing works
Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells
Williams, R. L., Hilton, D. J., Pease, S., Willson, T. A., Stewart, C. L., Gearing, D. P., Wagner, E. F., Metcalf, D., Nicola, N. A., & Gough, N. M. (1988) · Nature · doi:10.1038/336684a0 · Cited by 1,997 · see citing works
Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells.
Park, I.-K., Qian, D., Kiel, M., Becker, M. W., Pihalja, M., Weissman, I. L., Morrison, S. J., & Clarke, M. F. (2003) · Nature · doi:10.1038/nature01587 · Cited by 1,871 · see citing works
Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation
Molofsky, A. V., Pardal, R., Iwashita, T., Park, I.-K., Clarke, M. F., & Morrison, S. J. (2003) · Nature · doi:10.1038/nature02060 · Cited by 1,301 · see citing works
BMP4 initiates human embryonic stem cell differentiation to trophoblast
Xu, R., Chen, X., Li, D. S., Li, R., Addicks, G. C., Glennon, C., Zwaka, T. P., & Thomson, J. A. (2002) · Nature Biotechnology · doi:10.1038/nbt761 · Cited by 1,118 · see citing works
The Ink4/Arf locus is a barrier for iPS cell reprogramming
Li, H., Collado, M., Villasante, A., Strati, K., Ortega, S., Cañamero, M., Blasco, M. A., & Serrano, M. (2009) · Nature · doi:10.1038/nature08290 · Cited by 968 · 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
Hanna, J. H., Cheng, A. W., Saha, K., Kim, J., Lengner, C. J., Soldner, F., Cassady, J. P., Muffat, J., Carey, B. W., & Jaenisch, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1004584107 · Cited by 840 · see citing works
Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses
Shi, Y., Kirwan, P., Smith, J., Robinson, H. P. C., & Livesey, F. J. (2012) · Nature Neuroscience · doi:10.1038/nn.3041 · Cited by 813 · see citing works
Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage
Elkabetz, Y., Panagiotakos, G., Al Shamy, G., Socci, N. D., Tabar, V., & Studer, L. (2008) · Genes & Development · doi:10.1101/gad.1616208 · Cited by 677 · see citing works
Modeling early retinal development with human embryonic and induced pluripotent stem cells
Meyer, J. S., Shearer, R. L., Capowski, E. E., Wright, L. S., Wallace, K. A., McMillan, E., Zhang, S., & Gamm, D. M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905245106 · Cited by 601 · see citing works
Itoh, M., Nagafuchi, A., Yonemura, S., Kitani-Yasuda, T., Tsukita, S., & Tsukita, S. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.121.3.491 · Cited by 576 · see citing works
Specification of the vertebrate eye by a network of eye field transcription factors
Zuber, M. E., Gestri, G., Viczian, A. S., Barsacchi, G., & Harris, W. A. (2003) · Development · doi:10.1242/dev.00723 · Cited by 541 · see citing works
Mutations in human TBX3 alter limb, apocrine and genital development in ulnar-mammary syndrome
Bamshad, M., Lin, R. C., Law, D. J., Watkins, W. S., Krakowiak, P. A., Moore, M. E., Franceschini, P., Lala, R., Holmes, L. B., Gebuhr, T. C., et al. (1997) · Nature Genetics · doi:10.1038/ng0797-311 · Cited by 540 · see citing works
Musashi1: An Evolutionally Conserved Marker for CNS Progenitor Cells Including Neural Stem Cells
Kaneko, Y., Sakakibara, S., Imai, T., Suzuki, A., Nakamura, Y., Sawamoto, K., Ogawa, Y., Toyama, Y., Miyata, T., & Okano, H. (2000) · Developmental Neuroscience · doi:10.1159/000017435 · Cited by 519 · see citing works
Pax6 is a human neuroectoderm cell fate determinant
Zhang, X., Huang, C. T., Chen, J., Pankratz, M. T., Xi, J., Li, J., Yang, Y., LaVaute, T. M., Li, X.-J., Ayala, M., et al. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.04.017 · Cited by 480 · see citing works
LIF/STAT3 Signaling Fails to Maintain Self‐Renewal of Human Embryonic Stem Cells
Daheron, L. M., Opitz, S. L., Zaehres, H., Lensch, M. W., Andrews, P. W., Itskovitz‐Eldor, J., & Daley, G. Q. (2004) · Stem Cells · doi:10.1634/stemcells.22-5-770 · Cited by 470 · see citing works
Armstrong, L., Hughes, O. R., Yung, S., Hyslop, L., Stewart, R., Wappler, I., Peters, H., Walter, T., Stojković, P., Evans, J., et al. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddl112 · Cited by 365 · see citing works
Short-term BMP-4 treatment initiates mesoderm induction in human embryonic stem cells
Zhang, P., Li, J., Tan, Z., Wang, C., Liu, T., Chen, L., Yong, J., Jiang, W., Sun, X., Du, L., et al. (2007) · Blood · doi:10.1182/blood-2007-02-074120 · Cited by 319 · see citing works
Pankratz, M. T., Li, X.-J., LaVaute, T. M., Lyons, E. A., Chen, X., & Zhang, S. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0707 · Cited by 315 · 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
Nuclear Factor-κB in Development, Prevention, and Therapy of Cancer
Waes, C. V. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-2221 · Cited by 293 · 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
Vallier, L., Touboul, T., Chng, Z., Brimpari, M., Hannan, N. R. F., Millan, E. J., Smithers, L. E., Trotter, M. W. B., Rugg‐Gunn, P. J., Weber, A., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006082 · Cited by 251 · see citing works
Zfx Controls the Self-Renewal of Embryonic and Hematopoietic Stem Cells
Galan-Caridad, J. M., Harel, S., Arenzana, T. L., Hou, Z. E., Doetsch, F. K., Mirny, L. A., & Reizis, B. (2007) · Cell · doi:10.1016/j.cell.2007.03.014 · Cited by 244 · see citing works
The NF-κB/IκB signaling system: A molecular target in breast cancer therapy
Wu, J. T., & Kral, J. G. (2004) · Journal of Surgical Research · doi:10.1016/j.jss.2004.06.006 · Cited by 204 · see citing works
T-box genes in human disorders
Packham, E. A. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg077 · Cited by 202 · see citing works
Neural differentiation of human embryonic stem cells
Dhara, S. K., & Stice, S. L. (2008) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21891 · Cited by 179 · see citing works
Wilson, V., & Conlon, F. (2002) · Genome Biology · doi:10.1186/gb-2002-3-6-reviews3008 · Cited by 179 · see citing works
The Spectrum of Mutations in TBX3: Genotype/Phenotype Relationship in Ulnar-Mammary Syndrome
Bamshad, M., Le, T., Watkins, W. S., Dixon, M. E., Kramer, B. E., Roeder, A. D., Carey, J. C., Root, S., Schinzel, A., Van Maldergem, L., et al. (1999) · The American Journal of Human Genetics · doi:10.1086/302417 · Cited by 175 · see citing works
Sirtuin 1 regulation of developmental genes during differentiation of stem cells
Calvanese, V., Lara, E., Suárez-Álvarez, B., Dawud, R. A., Vázquez–Chantada, M., Martínez‐Chantar, M. L., Embade, N., López‐Nieva, P., Horrillo, A., Hmadcha, A., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1001399107 · Cited by 164 · see citing works
Rizo, A., Olthof, S. G. M., Han, L., Vellenga, E., de Haan, G., & Schuringa, J. J. (2009) · Blood · doi:10.1182/blood-2009-03-209734 · Cited by 163 · see citing works
Lingbeek, M. E., Jacobs, J. J. L., & van Lohuizen, M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m200403200 · Cited by 160 · see citing works
Brummelkamp, T. R., Kortlever, R. M., Lingbeek, M., Trettel, F., MacDonald, M. E., van Lohuizen, M., & Bernards, R. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110492200 · Cited by 154 · see citing works
Tbx Genes Specify Posterior Digit Identity through Shh and BMP Signaling
Suzuki, T., Takeuchi, J., Koshiba-Takeuchi, K., & Ogura, T. (2004) · Developmental Cell · doi:10.1016/s1534-5807(03)00401-5 · Cited by 148 · see citing works
Gerrard, L., Zhao, D., Clark, A. J., & Cui, W. (2005) · Stem Cells · doi:10.1634/stemcells.2004-0102 · Cited by 146 · see citing works
Fan, W., Huang, X., Chen, C., Gray, J., & Huang, T. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0615 · Cited by 136 · see citing works
Self-citationHe, M.-L., Wen, L., Campbell, C. E., Wu, J. Y., & Rao, Y. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.18.10212 · Cited by 120 · see citing works
Gualdoni, S., Baron, M., Lakowski, J., Decembrini, S., Smith, A. J., Pearson, R. A., Ali, R. R., & Sowden, J. C. (2010) · Stem Cells · doi:10.1002/stem.423 · Cited by 109 · see citing works
Carlson, H. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.21.2403 · Cited by 108 · see citing works
Human ESC-derived Neural Rosettes and Neural Stem Cell ProgressionPreprint
Elkabetz, Y., & Studer, L. (2008) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2008.73.052 · Cited by 105 · see citing works
TBX3 Is Overexpressed in Breast Cancer and Represses p14ARF by Interacting with Histone Deacetylases
Yarosh, W., Barrientos, T., Esmailpour, T., Lin, L., Carpenter, P. M., Osann, K., Anton-Culver, H., & Huang, T. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-5012 · Cited by 105 · see citing works
Self-citationThe ins and outs of virulence gene expression: Mg2 as a regulatory signal
Groisman, E. A. (1998) · BioEssays · doi:10.1002/(sici)1521-1878(199801)20:1 · Cited by 100 · see citing works
Behesti, H., Holt, J. K. L., & Sowden, J. C. (2006) · BMC Developmental Biology · doi:10.1186/1471-213x-6-62 · Cited by 98 · see citing works
The Role of Tbx2 and Tbx3 in Mammary Development and Tumorigenesis
Rowley, M., Grothey, E., & Couch, F. J. (2004) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1023/b:jomg.0000037156.64331.3f · Cited by 97 · see citing works
Human neural progenitor cells derived from embryonic stem cells in feeder-free cultures
Dhara, S. K., Hasneen, K., Machacek, D. W., Boyd, N. L., Rao, R. R., & Stice, S. L. (2008) · Differentiation · doi:10.1111/j.1432-0436.2007.00256.x · Cited by 94 · see citing works
Lu, R., Yang, A., & Jin, Y. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.202150 · Cited by 80 · see citing works
Regulation of Tbx3 expression by anteroposterior signalling in vertebrate limb development.
Tümpel, S., Sanz-Ezquerro, J., Isaac, A., Eblaghie, M. C., Dobson, J., & Tickle, C. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0762 · Cited by 76 · see citing works
Storm, M. P., Kumpfmueller, B., Thompson, B. A. N., Kolde, R., Vilo, J., Hummel, O., Schulz, H., & Welham, M. J. (2009) · Stem Cells · doi:10.1002/stem.3 · Cited by 73 · see citing works
Generation of Functional Eyes from Pluripotent Cells
Viczian, A. S., Solessio, E. C., Lyou, Y., & Zuber, M. E. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000174 · Cited by 68 · see citing works
Kang, H., Kim, Y.-E., Kwon, H., Sok, D., & Lee, Y. (2007) · Stem Cells and Development · doi:10.1089/scd.2007.0014 · Cited by 65 · see citing works
TBX3 and its splice variant TBX3 + exon 2a are functionally similar
Hoogaars, W. M. H., Barnett, P., Rodríguez, M., Clout, D. E. W., Moorman, A. F. M., Goding, C. R., & Christoffels, V. M. (2008) · Pigment Cell & Melanoma Research · doi:10.1111/j.1755-148x.2008.00461.x · Cited by 62 · see citing works
Analysis of genetic and epigenetic processes that influence p14ARF expression in breast cancer
Silva, J., Domínguez, G., Silva, J. M., García, J. M., Gallego, I., Corbacho, C., Provencio, M., España, P., & Bonilla, F. (2001) · Oncogene · doi:10.1038/sj.onc.1204617 · Cited by 50 · see citing works
Loss of Tbx2 delays optic vesicle invagination leading to small optic cups
Behesti, H., Papaioannou, V. E., & Sowden, J. C. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.06.026 · Cited by 41 · see citing works
Klopocki, E., Neumann, L. M., Tönnies, H., Ropers, H., Mundlos, S., & Ullmann, R. (2006) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201696 · Cited by 40 · see citing works
Platonova, N., Scotti, M., Babich, P. S., Bertoli, G. R., Mento, E., Meneghini, V., Egeo, A., Zucchi, I., & Merlo, G. R. (2007) · Cell and Tissue Research · doi:10.1007/s00441-006-0364-4 · Cited by 37 · see citing works
Liu, J., Esmailpour, T., Shang, X., Gülşen, G., Liu, A., & Huang, T. (2011) · BMC Developmental Biology · doi:10.1186/1471-213x-11-65 · Cited by 34 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 3
- [2]Papaioannou VE Silver LM The T-box gene family BIOESSAYS 1998 20 9 19 9504043
- [27]Lu R Yang A Jin Y Dual functions of T-box 3 (Tbx3) in the control of self-renewal and extraembryonic endoderm differentiation in mouse embryonic stem cells J BIOL CHEM 2011 286 8425 8436 21189255 PMC3048727
- [57]Karin M Nuclear factor-kappaB in cancer development and progression NATURE 2006 441 431 436 16724054
Cited by
Sorted by citations
The T-box gene family: emerging roles in development, stem cells and cancer
Papaioannou, V. E. (2014) · Development · doi:10.1242/dev.104471 · Cited by 293 · see citing works
Kempf, H., Olmer, R., Kropp, C., Rückert, M., Jara-Avaca, M., Diaz, D. R., Franke, A., Elliott, D. A., Wojciechowski, D., Fischer, M., et al. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.09.017 · Cited by 211 · see citing works
Wang, J., Kollárik, M., Ru, F., Sun, H., McNeil, B. D., Dong, X., Stephens, G. L., Korolevich, S., Brohawn, P. Z., Kolbeck, R., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0185985 · Cited by 94 · see citing works
Riazifar, H., Jia, Y., Chen, J., LYNCH, G. S., & Huang, T. (2014) · Stem Cells Translational Medicine · doi:10.5966/sctm.2013-0147 · Cited by 90 · see citing works
Self-citationDifferentiation of Human Breast-Milk Stem Cells to Neural Stem Cells and Neurons
Hosseini, S. M., Talaei‐Khozani, T., Sani, M., & Owrangi, B. (2014) · Neurology Research International · doi:10.1155/2014/807896 · Cited by 80 · see citing works
Human Breast Milk: Bioactive Components, from Stem Cells to Health Outcomes
Bardanzellu, F., Peroni, D. G., & Fanos, V. (2020) · Current Nutrition Reports · doi:10.1007/s13668-020-00303-7 · Cited by 67 · see citing works
Patriarchi, T., Amabile, S., Frullanti, E., Landucci, E., Rizzo, C. L., Ariani, F., Costa, M., Olimpico, F., Hell, J. W., Vaccarino, F. M., et al. (2015) · European Journal of Human Genetics · doi:10.1038/ejhg.2015.216 · Cited by 66 · see citing works
Isolation and identification of age-related DNA methylation markers for forensic age-prediction.
Yi, S.-H., Xu, L.-C., Mei, K., Yang, R.-Z., & Huang, D.-X. (2014) · Forensic Science International: Genetics · doi:10.1016/j.fsigen.2014.03.006 · Cited by 62 · see citing works
Sharma, R., Livesey, M., Wyllie, D., Proudfoot, C., Whitelaw, C., Hay, D., & Donadeu, F. X. (2014) · Stem Cells and Development · doi:10.1089/scd.2013.0565 · Cited by 49 · see citing works
McCalla, S. G., Siahpirani, A. F., Li, J., Pyne, S., Stone, M., Periyasamy, V., Shin, J., & Roy, S. (2023) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkad004 · Cited by 50 · see citing works
The T-Box transcription factor 3 in development and cancer
Willmer, T., Cooper, A., Peres, J., Omar, R., & Prince, S. (2017) · BioScience Trends · doi:10.5582/bst.2017.01043 · Cited by 44 · see citing works
The 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
Davenport, K. M., Ortega, M. S., Liu, H., O’Neil, E. V., Kelleher, A. M., Warren, W. C., & Spencer, T. E. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2221526120 · Cited by 40 · see citing works
Unique expression patterns of multiple key genes associated with the evolution of mammalian flight
Wang, Z., Dai, M., Wang, Y., Cooper, K. L., Zhu, T., Dong, D., Zhang, J., & Zhang, S. Y. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.3133 · Cited by 38 · see citing works
Willmer, T., Hare, S., Peres, J., & Prince, S. (2016) · Cell Division · doi:10.1186/s13008-016-0019-0 · Cited by 38 · see citing works
Liu, Y., Ma, Y., Yang, J., Cheng, D., Liu, X., Ma, X., West, F. D., & Wang, H. (2013) · Stem Cell Reviews and Reports · doi:10.1007/s12015-013-9485-9 · Cited by 36 · see citing works
Yao, H., Hannum, D. F., Zhai, Y., Hill, S. F., Albanus, R. D., Lou, W., Skidmore, J. M., Sanchez, G. J., Saiakhova, A., Bielas, S. L., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-74537-4 · Cited by 35 · see citing works
The T-Box factor TBX3 is important in S-phase and is regulated by c-Myc and cyclin A-CDK2
Willmer, T., Peres, J., Mowla, S., Abrahams, A., & Prince, S. (2015) · Cell Cycle · doi:10.1080/15384101.2015.1080398 · Cited by 32 · see citing works
Song, H., Liu, J., Wu, X., Zhou, Y., Chen, X., Chen, J., Deng, K., Mao, C., Huang, S.-H., & Liu, Z. (2019) · Aging · doi:10.18632/aging.102427 · Cited by 28 · see citing works
Epigenomic Landscapes of hESC-Derived Neural Rosettes: Modeling Neural Tube Formation and Diseases
Valensisi, C., Andrus, C. R., Buckberry, S., Jayavelu, N. D., Lund, R., Lister, R., & Hawkins, R. D. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.07.036 · Cited by 23 · see citing works
Vishnubalaji, R., Shaath, H., Al-Alwan, M. M., Abdelalim, E. M., & Alajez, N. M. (2022) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2022.10.007 · Cited by 21 · see citing works
Zhao, D., Wu, Y., & Chen, K. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.01.093 · Cited by 20 · see citing works
Miyoshi, K., Horiguchi, T., Tanimura, A., Hagita, H., & Noma, T. (2015) · BioMed Research International · doi:10.1155/2015/121575 · Cited by 20 · see citing works
Decoding the Pluripotency Network: The Emergence of New Transcription Factors
Lee, K. N., Wong, W. S., & Feng, B. (2013) · Biomedicines · doi:10.3390/biomedicines1010049 · Cited by 20 · see citing works
Loss of TBX3 enhances pancreatic progenitor generation from human pluripotent stem cells
Mukherjee, S., French, D. L., & Gadue, P. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.09.004 · Cited by 17 · see citing works
Moghadam, E. R., Zarrin, V., Mahmoodzadeh, A., Owrang, M., & Talaei‐Khozani, T. (2021) · Current Stem Cell Research & Therapy · doi:10.2174/1574888x16666210622125309 · Cited by 17 · see citing works
How the pterosaur got its wings
Tokita, M. (2014) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12150 · Cited by 16 · see citing works
Tykwinska, K., Lauster, R., Knaus, P. I., & Rosowski, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070612 · Cited by 15 · see citing works
Tbx3 represses bmp4 expression and, with Pax6, is required and sufficient for retina formation
Motahari, Z., Luna, R. I. M., Viczian, A. S., & Zuber, M. E. (2016) · Development · doi:10.1242/dev.130955 · Cited by 15 · see citing works
Genetic and functional analysis of the TBX3 gene promoter in indirect inguinal hernia
Zhao, Z., Tian, W., Wang, L., Wang, H., Qin, X., Xing, Q., Pang, S., & Yan, B. (2014) · Gene · doi:10.1016/j.gene.2014.10.031 · Cited by 14 · see citing works
The complex etiology of autism spectrum disorder due to missense mutations of CHD8
Shiraishi, T., Katayama, Y., Nishiyama, M., Shoji, H., Miyakawa, T., Mizoo, T., Matsumoto, A., Hijikata, A., Shirai, T., Mayanagi, K., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02491-y · Cited by 12 · see citing works
TBX3 Knockdown Decreases Reprogramming Efficiency of Human Cells
Klingenstein, M., Raab, S., Achberger, K., Kleger, A., Liebau, S., & Linta, L. (2016) · Stem Cells International · doi:10.1155/2016/6759343 · Cited by 11 · see citing works
Genetic analysis of the TBX3 gene promoter in ventricular septal defects
Chen, D., Qiao, Y., Meng, H., Pang, S., Huang, W., Zhang, H., & Yan, B. (2012) · Gene · doi:10.1016/j.gene.2012.10.066 · Cited by 11 · see citing works
DNA methylation profiling in recurrent miscarriage
Pi, L., Zhang, Z., Gu, Y., Wang, X., Wang, J., Xu, J., Liu, J., Zhang, X., & Du, J. (2020) · PeerJ · doi:10.7717/peerj.8196 · Cited by 11 · see citing works
Ruan, Y., Wang, J., Yu, M., Wang, F., Wang, J., Xu, Y., Liu, L., Cheng, Y., Yang, R., Zhang, C., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-04700-w · Cited by 11 · see citing works
Breast milk stem cells: four questions looking for an answer
Faa, G., Fanos, V., Puddu, M., Reali, A., Dessì, A., Pichiri, G., Gerosa, C., & Fanni, D. (2016) · Journal of pediatric and neonatal individualized medicine · doi:10.7363/050203 · 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
Engineering Mammary Gland in Vitro Models for Cancer Diagnostics and Therapy
Campbell, J. J., Hume, R. D., & Watson, C. J. (2014) · Molecular Pharmaceutics · doi:10.1021/mp500121c · Cited by 9 · see citing works
Replicable Expansion and Differentiation of Neural Precursors from Adult Canine Skin
Duncan, T., Lowe, A., Sidhu, K., Sachdev, P. S., Lewis, T., Lin, R. C. Y., Sytnyk, V., & Valenzuela, M. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.07.008 · Cited by 9 · see citing works
TBX3 shapes an immunosuppressive microenvironment and induces immunotherapy resistance
Liu, Z., Zhang, C., Xiao, J., He, Y., Liang, H., Huang, J., Cai, Z., Yi, Z., Chen, M., Li, Y., et al. (2025) · Theranostics · doi:10.7150/thno.103175 · Cited by 8 · see citing works
Potential of breastmilk in stem cell research
Tripathy, S., Singh, S., & Das, S. K. (2019) · Cell and Tissue Banking · doi:10.1007/s10561-019-09791-6 · Cited by 8 · 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
Li, N., Du, Z., Li, Y., Xu, W., Yang, Y., Peng, H., Song, T., Qin, Q., Huining, L., & Hua, J. (2021) · Stem Cells International · doi:10.1155/2021/4968649 · Cited by 4 · see citing works
Kibschull, M., Lye, S. J., Okino, S. T., & Sarras, H. (2015) · Systems Biology in Reproductive Medicine · doi:10.3109/19396368.2015.1062578 · Cited by 4 · see citing works
CELLoGeNe - An energy landscape framework for logical networks controlling cell decisions
Andersson, E., Sjö, M. S., Kaji, K., & Olariu, V. (2022) · iScience · doi:10.1016/j.isci.2022.104743 · Cited by 3 · see citing works
Moazeny, M., Dehbashi, M., Hojati, Z., & Esmaeili, F. (2022) · Molecular Biology Reports · doi:10.1007/s11033-022-08166-7 · Cited by 3 · see citing works
Yu, Z., Zhang, W., Zhang, X., Xu, D., & Wang, N. (2020) · Molecular Medicine Reports · doi:10.3892/mmr.2020.11237 · Cited by 2 · see citing works
Progress in human embryonic stem cell research and aging
Patni, A. P., Joseph, J. P., Macrin, D., & Devi, A. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-820071-1.00003-7 · Cited by 1 · 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
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
Regulation of anoikis by oncogenic pathways
Park, S. H. (2013) · doi:10.33915/etd.3658
Frazier, S. E. D., Pedersen, S. K., Vøls, K. K., Lie, M., Quintana, C., Nielsen, F., Wrona, A., Jaberi, E., Willenbrock, H., Chen, Q., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.11.30.691418
Nanog 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
Ontogeny of the enteric nervous system
Boismoreau, F. (2020) · doi:10.70675/b24ef52fz17c8z48e3za3afz5cc386550b86
- Authors
- Esmailpour, T., & Huang, T.
- Affiliations
- University of California, Irvine (US)
- Corresponding author
- Huang, Taosheng
- ORCID
- Huang, Taosheng
- Venue
- Stem Cells
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-09-20
- Volume
- 30
- Issue
- 10
- Pages
- 2152-2163
- ISSN
- 1066-5099 (ISSN-L)
- 1549-4918
- PMC
- PMC3517731
- OpenAlex
- W1936556660
- Cited by
- 54
- References
- 62
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 1 · 2023: 4 · 2022: 3 · 2021: 5 · 2020: 5 · 2019: 2 · 2018: 2 · 2017: 4 · 2016: 3 · 2015: 5 · 2014: 11 · 2013: 4 · 2012: 1
- FWCI
- 2.70
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Stem Cells (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (R01CA121876)
- 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 › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- TBX3, human embryonic stem cells, cell proliferation, neuroepithelial differentiation, self-renewal, p14ARF, ulnar-mammary syndrome, T-box transcription factor
- MeSH terms
- Animals, Cell Differentiation, Ectoderm, Endoderm, Epithelial Cells, Humans, Neurons, Signal Transduction, Biomarkers, Gene Expression Regulation, Developmental, I-kappa B Proteins, T-Box Domain Proteins, Tumor Suppressor Protein p14ARF, Cell Proliferation, Mice, Embryonic Stem Cells
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
