TBX-3, the Gene Mutated in Ulnar-Mammary Syndrome, Is a Negative Regulator of p19 and Inhibits Senescence
Open accessAbstract
Prolonged culturing of rodent cells in vitro activates p19(ARF) (named p14(ARF) in man), resulting in a p53-dependent proliferation arrest known as senescence. The p19(ARF)-Mdm2-p53 pathway also serves to protect primary cells against oncogenic transformation. We have used a genetic screen in mouse neuronal cells, conditionally immortalized by a temperature-sensitive mutant of SV40 large T antigen, to identify genes that allow bypass of senescence. Using retroviral cDNA expression libraries, we have identified TBX-3 as a potent inhibitor of senescence. TBX-3 is a T-box gene, which is found mutated in the human developmental disorder Ulnar-Mammary Syndrome. We have shown that TBX-3 potently represses expression of both mouse p19(ARF) and human p14(ARF). We have also shown here that point mutants of TBX-3, which are found in Ulnar-Mammary Syndrome, have lost the ability to inhibit senescence and fail to repress mouse p19(ARF) and human p14(ARF) expression. These data suggest that the hypoproliferative features of this genetic disorder may be caused, at least in part, by deregulated expression of p14(ARF).
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TBX3 functions primarily as a transcriptional repressor and initial reports suggested that it can promote proliferation by repressing the cell cycle regulators p14/p19ARF and p21.
“TBX3 functions primarily as a transcriptional repressor and initial reports suggested that it can promote proliferation by repressing the cell cycle regulators p14/p19ARF and p21 [60–62].”
From The oncoprotein TBX3 is controlling severity in experimental arthritis (2019) · cites this paper as [61]
The Results section ('TBX-3 Down-regulates p19 ARF'; page unavailable) reports TBX-3-mediated repression of the human p14 ARF promoter and reduced p19 ARF expression. The Discussion says TBX-3 drives proliferation and inhibits senescence, consistent with that part of the claim. The passages found do not show that TBX-3 represses p21, so this source does not support the claim in full. (LLM, conf=0.87)
Experimental — accuracy not yet measuredTbx3 is a transcriptional repressor for p19ARF and p14ARF.
“Tbx3 is known as a transcriptional repressor for p19 ARF (Cdkn2a -Mouse Genome Informatics) and p14 ARF (the human ortholog of p19 ARF )”
From Tbx3 controls the fate of hepatic progenitor cells in liver development by suppressing <i>p19ARF</i> expression (2008) · cites this paper as Brummelkamp et al., 2002
p19ARF and p14ARF are tumor suppressor genes that stabilize p53 via inactivation of Mdm2 in response to oncogenic stresses.
“the tumor suppressor genes that stabilize p53 (Trp53) via inactivation of Mdm2 in response to a variety of oncogenic stresses (Honda and Yasuda, 1999;Brummelkamp et al., 2002;Lingbeek et al., 2002;Kim and Sharpless, 2006).”
From Tbx3 controls the fate of hepatic progenitor cells in liver development by suppressing <i>p19ARF</i> expression (2008) · cites this paper as Brummelkamp et al., 2002
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Cites
p53, the cellular gatekeeper for growth and division
Levine, A. J. (1997) · Cell · doi:10.1016/s0092-8674(00)81871-1 · Cited by 7,693 · see citing works
Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a
Serrano, M., Lin, A. W., McCurrach, M. E., Beach, D., & Lowe, S. W. (1997) · Cell · doi:10.1016/s0092-8674(00)81902-9 · Cited by 5,178 · see citing works
Lane, D. P. (1992) · Nature · doi:10.1038/358015a0 · Cited by 5,138 · see citing works
Zhang, Y., Xiong, Y., & Yarbrough, W. G. (1998) · Cell · doi:10.1016/s0092-8674(00)81401-4 · Cited by 1,626 · see citing works
Jacobs, J. J. L., Kieboom, K., Marino, S., DePinho, R. A., & van Lohuizen, M. (1999) · Nature · doi:10.1038/16476 · Cited by 1,580 · see citing works
Tumor Suppression at the Mouse INK4a Locus Mediated by the Alternative Reading Frame Product p19
Kamijo, T., Zindy, F., Roussel, M. F., Quelle, D. E., Downing, J. R., Ashmun, R. A., Grosveld, G., & Sherr, C. J. (1997) · Cell · doi:10.1016/s0092-8674(00)80452-3 · Cited by 1,566 · see citing works
Pomerantz, J., Schreiber-Agus, N., Liégeois, N. J., Silverman, A., Alland, L., Chin, L., Potes, J., Chen, K., Orlow, I., Lee, H.-W., et al. (1998) · Cell · doi:10.1016/s0092-8674(00)81400-2 · Cited by 1,521 · see citing works
Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization
Zindy, F., Eischen, C. M., Randle, D. H., Kamijo, T., Cleveland, J. L., Sherr, C. J., & Roussel, M. F. (1998) · Genes & Development · doi:10.1101/gad.12.15.2424 · Cited by 1,245 · see citing works
Post‐translational modifications and activation of p53 by genotoxic stresses
Appella, E., & Anderson, C. W. (2001) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2001.02225.x · Cited by 1,071 · see citing works
Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Myc-induced apoptosis via INK4a/ARFPreprint
Jacobs, J. J. L., Scheijen, B., Voncken, J. W., Kieboom, K., Berns, A. J. M., & van Lohuizen, M. (1999) · Genes & Development · doi:10.1101/gad.13.20.2678 · Cited by 1,060 · see citing works
p14ARF links the tumour suppressors RB and p53
Bates, S., Phillips, A. C., Clark, P. A., Stott, F., Peters, G., Ludwig, R. L., & Vousden, K. H. (1998) · Nature · doi:10.1038/25867 · Cited by 918 · see citing works
Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis
Eischen, C. M., Weber, J. D., Roussel, M. F., Sherr, C. J., & Cleveland, J. L. (1999) · Genes & Development · doi:10.1101/gad.13.20.2658 · Cited by 819 · see citing works
Sherr, C. J., & DePinho, R. A. (2000) · Cell · doi:10.1016/s0092-8674(00)00046-5 · Cited by 745 · see citing works
Association of p19ARF with Mdm2 inhibits ubiquitin ligase activity of Mdm2 for tumor suppressor p53
Honda, R., & Yasuda, H. (1999) · The EMBO Journal · doi:10.1093/emboj/18.1.22 · Cited by 724 · see citing works
p19ARF links the tumour suppressor p53 to Ras
Palmero, I., Pantoja, C., & Serrano, M. (1998) · Nature · doi:10.1038/25870 · Cited by 617 · see citing works
Dominant phenotypes produced by the HD mutation in STHdhQ111 striatal cells
Trettel, F. (2000) · Human Molecular Genetics · doi:10.1093/hmg/9.19.2799 · Cited by 614 · see citing works
Self-citationE1A signaling to p53 involves the p19ARFtumor suppressorPreprint
de Stanchina, E., McCurrach, M. E., Zindy, F., Shieh, S.-Y., Ferbeyre, G., Samuelson, A. V., Prives, C. L., Roussel, M. F., Sherr, C. J., & Lowe, S. W. (1998) · Genes & Development · doi:10.1101/gad.12.15.2434 · Cited by 607 · see citing works
Sage, J., Mulligan, G. J., Attardi, L. D., Miller, A., Chen, S., Williams, B., Theodorou, E., & Jacks, T. (2000) · Genes & Development · doi:10.1101/gad.843200 · Cited by 582 · 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
P19 ARF stabilizes p53 by blocking nucleo-cytoplasmic shuttling of Mdm2
Tao, W., & Levine, A. J. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.12.6937 · Cited by 539 · see citing works
twist is a potential oncogene that inhibits apoptosis
Maestro, R., Tos, A. P. D., Hamamori, Y., Krasnokutsky, S., Sartorelli, V., Kedes, L., Doglioni, C., Beach, D. H., & Hannon, G. J. (1999) · Genes & Development · doi:10.1101/gad.13.17.2207 · Cited by 516 · see citing works
(1993) · PubMed · Cited by 469 · see citing works
INK4a/ARF mutations accelerate lymphomagenesis and promote chemoresistance by disabling p53
Schmitt, C. A., McCurrach, M. E., de Stanchina, E., Wallace-Brodeur, R. R., & Lowe, S. W. (1999) · Genes & Development · doi:10.1101/gad.13.20.2670 · Cited by 458 · see citing works
Dannenberg, J.-H., van Rossum, A., Schuijff, L., & te Riele, H. (2000) · Genes & Development · doi:10.1101/gad.847700 · Cited by 413 · see citing works
Dimri, G. P., Itahana, K., Acosta, M., & Campisi, J. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.1.273-285.2000 · Cited by 393 · see citing works
Jacobs, J. J. L., Keblusek, P., Robanus-Maandag, E., Kristel, P., Lingbeek, M., Nederlof, P. M., van Welsem, T., van de Vijver, M. J., Koh, E. Y., Daley, G. Q., et al. (2000) · Nature Genetics · doi:10.1038/81583 · Cited by 368 · see citing works
Self-citationDAP kinase activates a p19ARF/p53-mediated apoptotic checkpoint to suppress oncogenic transformation
Raveh, T., Droguett, G., Horwitz, M. S., DePinho, R. A., & Kimchi, A. (2001) · Nature Cell Biology · doi:10.1038/35050500 · Cited by 361 · see citing works
JunD Protects Cells from p53-Dependent Senescence and Apoptosis
Weitzman, J. B., Fiette, L., Matsuo, K., & Yaniv, M. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00109-x · Cited by 269 · see citing works
Pantoja, C., & Serrano, M. (1999) · Oncogene · doi:10.1038/sj.onc.1202880 · Cited by 201 · 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
Brachyury-Related Transcription Factor Tbx2 and Repression of the Melanocyte-Specific TRP-1 Promoter
Carreira, S., Dexter, T. J., Yavuzer, U., Easty, D. J., & Goding, C. R. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.9.5099 · Cited by 173 · see citing works
Inoue, K., Roussel, M. F., & Sherr, C. J. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.7.3993 · Cited by 144 · see citing works
He, 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
Alkema, M. J., Jacobs, H., van Lohuizen, M., & Berns, A. J. M. (1997) · Oncogene · doi:10.1038/sj.onc.1201262 · Cited by 118 · see citing works
Inoue, K., Wen, R., Rehg, J. E., Adachi, M., Cleveland, J. L., Roussel, M. F., & Sherr, C. J. (2000) · Genes & Development · doi:10.1101/gad.14.14.1797 · Cited by 107 · see citing works
Inhibition of v-Abl transformation by p53 and p19ARF
Cong, F., Zou, X., Hinrichs, K., Calame, K. L., & Goff, S. P. (1999) · Oncogene · doi:10.1038/sj.onc.1203290 · Cited by 37 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- Tao, W. & Levine, A. J. (1999) Proc. Natl. Acad. Sci. U. S. A. 96, 6937-6941
- He, M., Wen, L., Campbell, C. E., Wu, J. Y. & Rao, Y. (1999) Proc. Natl. Acad. Sci. U. S. A. 96, 10212-10217
- Inoue, K., Roussel, M. F. & Sherr, C. J. (1999) Proc. Natl. Acad. Sci. U. S. A. 96, 3993-3998
Cited by
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A large-scale RNAi screen in human cells identifies new components of the p53 pathway
Berns, K., Hijmans, E. M., Mullenders, J., Brummelkamp, T. R., Velds, A., Heimerikx, M., Kerkhoven, R. M., Madiredjo, M., Nijkamp, W., Weigelt, B., et al. (2004) · Nature Cell Biology · doi:10.1038/nature02371 · Cited by 1,059 · see citing works
Self-citationRegulation of the INK4b–ARF–INK4a tumour suppressor locus: all for one or one for all
Gil, J., & Peters, G. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1987 · Cited by 843 · see citing works
Expression Profiling Reveals Novel Pathways in the Transformation of Melanocytes to Melanomas
Hoek, K. S., Rimm, D. L., Williams, K. R., Zhao, H., Ariyan, S., Lin, A., Kluger, H. M., Berger, A. J., Cheng, E., Trombetta, E. S., et al. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0731 · Cited by 478 · see citing works
Myc pathways provoking cell suicide and cancer
Nilsson, J. A., & Cleveland, J. L. (2003) · Oncogene · doi:10.1038/sj.onc.1207261 · Cited by 462 · see citing works
Expression profiling reveals novel pathways in the transformation of Melanocytes to Melanomas.
Hoek, K. S., Rimm, D. L., Williams, K. R., Zhao, H., Ariyan, S., Lin, A. J., Kluger, H. M., Berger, A. J., Cheng, E., Trombetta, E. S., et al. (2004) · Pigment Cell Research · doi:10.1111/j.1600-0749.2004.00175_12.x · Cited by 412 · see citing works
Tbx3 controls the sinoatrial node gene program and imposes pacemaker function on the atria
Hoogaars, W. M. H., Engel, A., Brons, J. F., Verkerk, A. O., de Lange, F. J., Wong, L. Y. E., Bakker, M. L., Clout, D. E., Wakker, V., Barnett, P., et al. (2007) · Genes & Development · doi:10.1101/gad.416007 · Cited by 409 · see citing works
Role of the proto-oncogene Pokemon in cellular transformation and ARF repression
Maeda, T., Hobbs, R. M., Merghoub, T., Guernah, I., Zelent, A., Cordon‐Cardo, C., Teruya‐Feldstein, J., & Pandolfi, P. P. (2005) · Nature · doi:10.1038/nature03203 · Cited by 399 · see citing works
Molecular Pathway for the Localized Formation of the Sinoatrial Node
Mommersteeg, M. T. M., Hoogaars, W. M. H., Prall, O. W. J., Vries, C. D. G.-D., Wiese, C., Clout, D. E. W., Papaioannou, V. E., Brown, N. A., Harvey, R. P., Moorman, A. F. M., et al. (2007) · Circulation Research · doi:10.1161/01.res.0000258019.74591.b3 · Cited by 369 · 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
Reversal of Senescence in Mouse Fibroblasts through Lentiviral Suppression of p53
Dirac, A. M. G., & Bernards, R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.c300023200 · Cited by 254 · see citing works
Self-citationVance, K. W., Carreira, S., Brosch, G., & Goding, C. R. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-3045 · Cited by 228 · see citing works
Cai, C., Zhou, W., Yang, L., Bu, L., Qyang, Y., Zhang, X., Li, X., Rosenfeld, M. G., Chen, J., & Evans, S. Μ. (2005) · Development · doi:10.1242/dev.01832 · Cited by 222 · 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
Genetic variation in T-box binding element functionally affects SCN5A/SCN10A enhancer
van den Boogaard, M., Wong, L. Y. E., Tessadori, F., Bakker, M. L., Dreizehnter, L., Wakker, V., Bezzina, C. R., Hoen, P. A. C. ’., Bakkers, J., Barnett, P., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci62613 · Cited by 200 · see citing works
Repression of the Arf tumor suppressor by E2F3 is required for normal cell cycle kineticsPreprint
Aslanian, A., Iaquinta, P. J., Verona, R. I., & Lees, J. A. (2004) · Genes & Development · doi:10.1101/gad.1196704 · Cited by 170 · see citing works
Tbx2 Directly Represses the Expression of the p21WAF1 Cyclin-Dependent Kinase Inhibitor
Prince, S., Carreira, S., Vance, K. W., Abrahams, A., & Goding, C. R. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-3286 · Cited by 160 · 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
Self-citationRenard, C.-A., Labalette, C., Armengol, C., Cougot, D., Wei, Y., Cairo, S., Pineau, P., Neuveut, C., de Reyniès, A., Dejean, A., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-2344 · Cited by 157 · see citing works
“target of Tbx2/Tbx3 has linked these transcriptional repressors to the control of cell cycle and senescence and to the antiproliferative response delivered by the ARF-Mdm2-p53 pathway in tumorigenesis (25, 26 ).”
BackgroundMethodInfluentialTbx3 Represses E-Cadherin Expression and Enhances Melanoma Invasiveness
Rodriguez, M., Aladowicz, E., Lanfrancone, L., & Goding, C. R. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0301 · Cited by 157 · see citing works
Salminen, A., Kaarniranta, K., Hiltunen, M. O., & Kauppinen, A. (2014) · Journal of Molecular Medicine · doi:10.1007/s00109-014-1182-x · Cited by 146 · see citing works
Suzuki, A., Sekiya, S., Büscher, D., Izpisúa Belmonte, J. C., & Taniguchi, H. (2008) · Development · doi:10.1242/dev.016634 · Cited by 136 · see citing works
The T‐box transcription factor Tbx2: Its role in development and possible implication in cancer
Abrahams, A., Parker, M. I., & Prince, S. (2009) · IUBMB Life · doi:10.1002/iub.275 · Cited by 121 · see citing works
TSPYL5 suppresses p53 levels and function by physical interaction with USP7.
Epping, M. T., Meijer, L. A. T., Krijgsman, O., Bos, J. L., Pandolfi, P. P., & Bernards, R. (2011) · Nature Cell Biology · doi:10.1038/ncb2142 · Cited by 117 · see citing works
Self-citationRegulation of ploidy and senescence by the AMPK‐related kinase NUAK1
Humbert, N., Navaratnam, N., Augert, A., Da Costa, M., Martien, S., Wang, J., Martinez, D., Abbadie, C., Carling, D., de Launoit, Y., et al. (2010) · The EMBO Journal · doi:10.1038/emboj.2009.342 · Cited by 115 · see citing works
Production of complex nucleic acid libraries using highly parallel in situ oligonucleotide synthesis
Cleary, M. A., Kilian, K. A., Wang, Y., Bradshaw, J., Cavet, G., Ge, W., Kulkarni, A., Paddison, P. J., Chang, K., Sheth, N. U., et al. (2004) · Nature Methods · doi:10.1038/nmeth724 · Cited by 108 · see citing works
Cellular senescence: hot or what?
Evan, G. I., & di Fagagna, F. D. (2009) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2008.11.009 · Cited by 109 · see citing works
Li, Y., Zhang, H., Choi, S. C., Litingtung, Y., & Chiang, C. C. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.03.009 · Cited by 107 · 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
Cardiovascular development: towards biomedical applicability
Hoogaars, W. M. H., Barnett, P., Moorman, A. F. M., & Christoffels, V. M. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-6518-z · Cited by 102 · see citing works
Carlson, H., Ota, S., Song, Y., Chen, Y., & Hurlin, P. J. (2002) · Oncogene · doi:10.1038/sj.onc.1205476 · Cited by 102 · 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
“Furthermore, Fan et al. (2004) showed that Tbx3, and not its isoform Tbx3+2a, could immortalise MEFs and Brummelkamp et al. (2002) identified Tbx3 as a key anti-senescence factor in a genetic screen of conditionally immortalised mouse striatal cells.”
BackgroundBehesti, 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
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
Wu, M., Hernandez, M., Shen, S., Sabo, J. K., Kelkar, D., Wang, J., O’Leary, R., Phillips, G. R., Cate, H. S., & Casaccia, P. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.4876-11.2012 · Cited by 89 · see citing works
Peres, J., Davis-Marcisak, E. F., Mowla, S., Bennett, D. C., Li, J., Wansleben, S. M., & Prince, S. (2010) · Genes & Cancer · doi:10.1177/1947601910365160 · Cited by 89 · 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
Replicative senescence revisited.
Marcotte, R., & Wang, E. (2002) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/57.7.b257 · Cited by 86 · see citing works
Jerome‐Majewska, L. A., Jenkins, G. P., Ernstoff, E., Zindy, F., Sherr, C. J., & Papaioannou, V. E. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20575 · Cited by 85 · see citing works
Confirmation of a BRAF mutation‐associated gene expression signature in melanoma
Johansson, P. A., Pavey, S. J., & Hayward, N. K. (2007) · Pigment Cell Research · doi:10.1111/j.1600-0749.2007.00375.x · Cited by 83 · see citing works
Increased expression of cSHMT, Tbx3 and utrophin in plasma of ovarian and breast cancer patients
Lomnytska, M., Dubrovska, A., Hellman, U., Volodko, N., & Souchelnytskyi, S. (2006) · International Journal of Cancer · doi:10.1002/ijc.21332 · Cited by 83 · see citing works
Signalling Pathways Implicated in Early Mammary Gland Morphogenesis and Breast Cancer
Howard, B. A., & Ashworth, A. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020112 · Cited by 81 · see citing works
Akt and 14-3-3η regulate Miz1 to control cell-cycle arrest after DNA damage
Wanzel, M., Kleine‐Kohlbrecher, D., Herold, S., Hock, A., Berns, K., Park, J., Hemmings, B. A., & Eilers, M. (2004) · Nature Cell Biology · doi:10.1038/ncb1202 · Cited by 77 · see citing works
Ageing as developmental decay: insights from p16INK4a.
Martin, N., Beach, D., & Gil, J. (2014) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.09.008 · Cited by 76 · see citing works
The T-box Transcription Factors TBX2 and TBX3 in Mammary Gland Development and Breast Cancer
Douglas, N. C., & Papaioannou, V. E. (2013) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-013-9282-8 · Cited by 76 · see citing works
Brun, C., Jean‐Louis, F., Oddos, T., Bagot, M., Bensussan, A., & Michel, L. (2015) · Experimental Dermatology · doi:10.1111/exd.12874 · Cited by 75 · see citing works
Trowe, M.-O., Zhao, L., Weiss, A.-C., Christoffels, V., Epstein, D. J., & Kispert, A. (2013) · Development · doi:10.1242/dev.094524 · Cited by 72 · see citing works
Mutually Exclusive Inactivation of DMP1 and ARF/p53 in Lung Cancer
Mallakin, A., Sugiyama, T., Taneja, P., Matise, L. A., Frazier, D. P., Choudhary, M., Hawkins, G. A., D'Agostino, R. B., Willingham, M. C., & Inoue, K. (2007) · Cancer Cell · doi:10.1016/j.ccr.2007.08.034 · Cited by 72 · see citing works
T-box transcription factors in cancer biology
Wansleben, S. M., Peres, J., Hare, S., Goding, C. R., & Prince, S. (2014) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2014.08.004 · Cited by 63 · see citing works
Wang, B., Lindley, L. E., Fernández-Vega, V., Rieger, M. E., Sims, A. H., & Briegel, K. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041355 · Cited by 64 · 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
TBX2 and TBX3: The special value for anticancer drug targets
Lu, J., Li, X.-P., Dong, Q., Kung, H.-F., & He, M.-L. (2010) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2010.07.001 · Cited by 57 · see citing works
Diverse functional networks of <i>Tbx3</i> in development and disease
Washkowitz, A. J., Gavrilov, S., Begum, S., & Papaioannou, V. E. (2012) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1162 · Cited by 58 · see citing works
Chapter 4 Mouse Models of Congenital Cardiovascular Disease
Moon, A. (2008) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(08)00604-2 · Cited by 56 · see citing works
The oncogenic TBX3 is a downstream target and mediator of the TGF-β1 signaling pathway
Li, J., Weinberg, M. S., Zerbini, L., & Prince, S. (2013) · Molecular Biology of the Cell · doi:10.1091/mbc.e13-05-0273 · Cited by 56 · see citing works
ITO, A., ASAMOTO, M., HOKAIWADO, N., TAKAHASHI, S., & SHIRAI, T. (2005) · Cancer Letters · doi:10.1016/j.canlet.2004.07.051 · Cited by 55 · see citing works
Ectopic Tbx2 expression results in polyploidy and cisplatin resistance
Davis-Marcisak, E. F., Teng, H., Bilican, B., Parker, M. I., Liu, B., Carriera, S., Goding, C. R., & Prince, S. (2007) · Oncogene · doi:10.1038/sj.onc.1210701 · Cited by 55 · see citing works
Esmailpour, T., & Huang, T. (2012) · Stem Cells · doi:10.1002/stem.1187 · Cited by 54 · see citing works
Boyd, S. C., Mijatov, B., Pupo, G. M., Tran, S. L., Gowrishankar, K., Shaw, H. M., Goding, C. R., Scolyer, R. A., Mann, G. J., Kefford, R. F., et al. (2013) · Journal of Investigative Dermatology · doi:10.1038/jid.2012.421 · Cited by 53 · see citing works
Tbx3 represses PTEN and is over-expressed in head and neck squamous cell carcinoma
Burgucu, D., Guney, K., Sahinturk, D., Ozbudak, I. H., Ozel, D., Ozbilim, G., & Yavuzer, U. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-481 · Cited by 52 · see citing works
Functions of Myc:Max in the Control of Cell Proliferation and Tumorigenesis
Hurlin, P. J., & Dezfouli, S. (2004) · International review of cytology · doi:10.1016/s0074-7696(04)38004-6 · Cited by 52 · see citing works
The T-box transcription factor, TBX3, is sufficient to promote melanoma formation and invasion
Peres, J., & Prince, S. (2013) · Molecular Cancer · doi:10.1186/1476-4598-12-117 · Cited by 50 · see citing works
Nijwening, J. H., Geutjes, E.-J., Bernards, R., & Beijersbergen, R. L. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025235 · Cited by 50 · see citing works
Self-citationT-Box Genes in Human Development and Disease
Ghosh, T. K., Brook, J. D., & Wilsdon, A. (2016) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2016.08.006 · Cited by 48 · see citing works
Palumbo, S. L., Tsai, T.-L., & Li, W. (2013) · Stem Cells and Development · doi:10.1089/scd.2013.0294 · Cited by 48 · see citing works
Govoni, K. E., Lee, S. K., Chadwick, R. B., Yu, H., Kasukawa, Y., Baylink, D. J., & Mohan, S. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00592.2005 · Cited by 47 · see citing works
Cabeza-Arvelaiz, Y., & Schiestl, R. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044700 · Cited by 46 · see citing works
UV-mediated Regulation of the Anti-senescence Factor Tbx2
Abrahams, A., Mowla, S., Parker, M. I., Goding, C. R., & Prince, S. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m705651200 · Cited by 45 · see citing works
Kaiser, M., Wojahn, I., Rudat, C., Lüdtke, T. H., Christoffels, V., Moon, A., Kispert, A., & Trowe, M.-O. (2021) · Development · doi:10.1242/dev.195651 · Cited by 42 · see citing works
How to become immortal: let MEFs count the ways
Odell, A. F., Askham, J. M., Whibley, C., & Hollstein, M. (2010) · Aging · doi:10.18632/aging.100129 · Cited by 44 · see citing works
Cell cycle regulation of the T-box transcription factor tbx2
Bilican, B., & Goding, C. R. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.03.033 · Cited by 44 · see citing works
Morphogenesis of the Vertebrate Heart
Hoogaars, W. M. H., Christoffels, V. M., & Moorman, A. F. M. (2007) · Advances in developmental biology · doi:10.1016/s1574-3349(07)18002-9 · Cited by 43 · see citing works
Boellmann, F., Zhang, L., M.A., H. J. C. I., Schroth, G. P., Kenyon, E. M., Andersen, M. E., & Thomas, R. S. (2010) · Toxicological Sciences · doi:10.1093/toxsci/kfq225 · Cited by 41 · see citing works
TBX3 Regulates Splicing In Vivo: A Novel Molecular Mechanism for Ulnar-Mammary Syndrome
P., P. K., Franklin, S., Emechebe, U., Hu, H., Moore, B., Lehman, C. W., Yandell, M., & Moon, A. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004247 · Cited by 41 · see citing works
Govoni, K. E., Linares, G. R., Chen, S., Pourteymoor, S., & Mohan, S. (2008) · Journal of Cellular Biochemistry · doi:10.1002/jcb.22035 · Cited by 39 · see citing works
Amir, S., Simion, C., Umeh-Garcia, M., Krig, S., Moss, T., Carraway, K. L., & Sweeney, C. (2016) · British Journal of Cancer · doi:10.1038/bjc.2016.73 · Cited by 38 · see citing works
Mowla, S., Pinnock, R., Leaner, V. D., Goding, C. R., & Prince, S. (2011) · Biochemical Journal · doi:10.1042/bj20100886 · Cited by 38 · 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
Willmer, T., Hare, S., Peres, J., & Prince, S. (2016) · Cell Division · doi:10.1186/s13008-016-0019-0 · Cited by 38 · see citing works
Emechebe, U., Kumar P, P., Rozenberg, J. M., Moore, B., Firment, A., Mirshahi, T., & Moon, A. M. (2016) · eLife · doi:10.7554/elife.07897 · Cited by 36 · see citing works
Humtsoe, J. O., Koya, E., Pham, E., Aramoto, T., Zuo, J., Ishikawa, T., & Kramer, R. H. (2011) · Experimental Cell Research · doi:10.1016/j.yexcr.2011.11.011 · Cited by 36 · see citing works
Tripaldi, R., Stuppia, L., & Alberti, S. (2013) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2013.02.002 · Cited by 36 · 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
Early growth response 2 (EGR2) is a novel regulator of the senescence programme
Tyler, E. J., del Arroyo, A. G., Wallis, R., Hughes, B., Garbe, J. C., Stampfer, M. R., Koh, J., Lowe, R., Philpott, M. P., & Bishop, C. L. (2021) · Aging Cell · doi:10.1111/acel.13318 · Cited by 34 · see citing works
Advances in melanoma senescence and potential clinical application
Giuliano, S., Ohanna, M., Ballotti, R., & Bertolotto, C. (2010) · Pigment Cell & Melanoma Research · doi:10.1111/j.1755-148x.2010.00820.x · Cited by 34 · see citing works
Mosca, E., Bertoli, G. R., Piscitelli, E., Vilardo, L., Reinbold, R. A., Zucchi, I., & Milanesi, L. (2009) · BMC Bioinformatics · doi:10.1186/1471-2105-10-s12-s8 · Cited by 31 · see citing works
Embryonic transcription factors in human breast cancer
Briegel, K. J. (2006) · IUBMB Life · doi:10.1080/15216540600686870 · Cited by 32 · see citing works
Tarunina, M., Alger, L., Chu, G., Münger, K., Gudkov, A. V., & Jat, P. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.24.10792-10801.2004 · Cited by 31 · see citing works
Sox4 mediates Tbx3 transcriptional regulation of the gap junction protein Cx43
Boogerd, C. J. J., Wong, L. Y. E., van den Boogaard, M., Bakker, M. L., Tessadori, F., Bakkers, J., Hoen, P. A. C. ’., Moorman, A. F. M., Christoffels, V. M., & Barnett, P. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0693-7 · Cited by 30 · see citing works
Acquaah-Mensah, G. K., Malhotra, D., Vulimiri, M., McDermott, J., & Biswal, S. S. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002597 · Cited by 28 · see citing works
Zhang, J., He, M., Dong, Q., Xie, W., Chen, Y., Lin, M. C. M., Leung, P., Zhang, Y., & Kung, H. (2010) · Integrative Cancer Therapies · doi:10.1177/1534735410373921 · Cited by 28 · see citing works
Suppression of the p53-Dependent Replicative Senescence Response by Lysophosphatidic Acid Signaling
Kortlever, R. M., Brummelkamp, T. R., van Meeteren, L. A., Moolenaar, W. H., & Bernards, R. (2008) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-08-0066 · Cited by 27 · see citing works
Self-citationLee, H. S., Cho, H. H., Kim, H. K., Bae, Y. C., Baik, H. S., & Jung, J. S. (2006) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-006-9306-4 · Cited by 27 · see citing works
Shen, J., Lu, J., Sui, L., Wang, D., Yin, M., Hoffmann, I., Legler, A., & Pflugfelder, G. O. (2014) · Oncotarget · doi:10.18632/oncotarget.2426 · Cited by 22 · see citing works
The transcriptional regulator TBX3 promotes progression from non-invasive to invasive breast cancer
Krstic, M., Macmillan, C. D., Leong, H. S., Clifford, A. G., Souter, L. H., Dales, D. W., Postenka, C. O., Chambers, A. F., & Tuck, A. B. (2016) · BMC Cancer · doi:10.1186/s12885-016-2697-z · Cited by 23 · see citing works
Medeiros, M. K., Zheng, X., Novák, P., Wnek, S. M., Chyan, V., Escudero‐Lourdes, C., & Gandolfi, A. J. (2011) · Toxicology · doi:10.1016/j.tox.2011.11.002 · Cited by 22 · see citing works
Willmer, T., Cooper, A., Sims, D., Govender, D., & Prince, S. (2016) · Oncogenesis · doi:10.1038/oncsis.2016.11 · Cited by 21 · see citing works
COL1A2 is a TBX3 target that mediates its impact on fibrosarcoma and chondrosarcoma cell migration
Omar, R., Cooper, A., Maranyane, H. M., Zerbini, L., & Prince, S. (2019) · Cancer Letters · doi:10.1016/j.canlet.2019.06.004 · Cited by 21 · see citing works
Putative Breast Cancer Driver Mutations in TBX3 Cause Impaired Transcriptional Repression
Fischer, K. H., & Pflugfelder, G. O. (2015) · Frontiers in Oncology · doi:10.3389/fonc.2015.00244 · Cited by 20 · see citing works
Alternative splicing of T-box transcription factor genes
DeBenedittis, P., & Jiao, K. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.08.010 · Cited by 20 · see citing works
- Authors
- Brummelkamp, T. R., Kortlever, R. M., Lingbeek, M., Trettel, F., MacDonald, M. E., van Lohuizen, M., & Bernards, R.
- Affiliations
- The Netherlands Cancer Institute (NL)
- Massachusetts General Hospital (US)
- Corresponding author
- Bernards, René
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2002-02
- Volume
- 277
- Issue
- 8
- Pages
- 6567-6572
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W1986820083
- Cited by
- 154
- References
- 36
- Citations by year
- 2026: 1 · 2023: 2 · 2022: 5 · 2021: 8 · 2020: 2 · 2019: 3 · 2018: 1 · 2016: 7 · 2015: 3 · 2014: 11 · 2013: 13 · 2012: 11
- FWCI
- 6.00
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion, cc-by)
- Funders
- KWF Kankerbestrijding
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (NS32765, R01NS032765)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- ulnar-mammary syndrome, p19ARF, p14ARF, cellular senescence, senescence bypass, p53, MDM2, T-box transcription factor, point mutations, neurons, oncogenic transformation
- MeSH terms
- Aging, Animals, Bone Diseases, Breast Diseases, Cell Line, Cells, Cultured, Chlorocebus aethiops, Corpus Striatum, Embryo, Mammalian, Female, Gene Expression Regulation, Humans, Mutation, Placenta, Pregnancy, Promoter Regions, Genetic, Retroviridae, Suppression, Genetic, Syndrome, Transfection, Gene Library, Genes, p53, COS Cells, Cyclin-Dependent Kinase Inhibitor p16, Genes, p16, T-Box Domain Proteins, Tumor Suppressor Protein p14ARF, Mice
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