The role of T‑box genes in the tumorigenesis and progression of cancer (Review)
- Authors:
- Fangyuan Chang
- Peipei Xing
- Fengju Song
- Xiaoling Du
- Guowen Wang
- Kexin Chen
- Jilong Yang
-
Affiliations: Bone and Soft Tissue Tumor Department, Tianjin Medical University Cancer Institute & Hospital, Tianjin 300060, P.R. China, National Clinical Research Center for Cancer, Tianjin Medical University Cancer Institute & Hospital, Tianjin 300060, P.R. China, Department of Diagnostics, Tianjin Medical University, Tianjin 300061, P.R. China - Published online on: October 19, 2016 https://doi.org/10.3892/ol.2016.5296
- Pages: 4305-4311
-
Copyright: © Chang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Lu J, Li XP, Dong Q, Kung HF and He ML: TBX2 and TBX3: The special value for anticancer drug targets. Biochim Biophys Acta. 1806:268–274. 2010.PubMed/NCBI | |
Abrahams A, Parker MI and Prince S: The T-box transcription factor Tbx2: Its role in development and possible implication in cancer. IUBMB Life. 62:92–102. 2010.PubMed/NCBI | |
Takeuchi JK, Koshiba-Takeuchi K, Suzuki T, Kamimura M, Ogura K and Ogura T: Tbx5 and Tbx4 trigger limb initiation through activation of the Wnt/Fgf signaling cascade. Development. 130:2729–2739. 2003. View Article : Google Scholar : PubMed/NCBI | |
Kispert A and Hermann BG: The Brachyury gene encodes a novel DNA binding protein. EMBO J. 12:4898–4899. 1993.PubMed/NCBI | |
MÜller CW and Herrmann BG: Crystallographic structure of the T domain-DNA complex of the Brachyury transcription factor. Nature. 389:884–888. 1997. View Article : Google Scholar : PubMed/NCBI | |
Ruvinsky I and Gibson-Brown JJ: Genetic and developmental bases of serial homology in vertebrate limb evolution. Development. 127:5233–5244. 2000.PubMed/NCBI | |
Tada M and Smith JC: T-targets: Clues to understanding the functions of T-box proteins. Dev Growth Differ. 43:1–11. 2001. View Article : Google Scholar : PubMed/NCBI | |
Papaioannou VE: The T-box gene family: Emerging roles in development, stem cells and cancer. Development. 141:3819–3833. 2014. View Article : Google Scholar : PubMed/NCBI | |
Stein RA: A new TBX gene linked to human disease. Clin Genet. 76:23–24. 2009. View Article : Google Scholar : PubMed/NCBI | |
Naiche LA, Harrelson Z, Kelly RG and Papaioannou VE: T-box genes in vertebrate development. Annu Rev Genet. 39:219–239. 2005. View Article : Google Scholar : PubMed/NCBI | |
Morley RH, Lachani K, Keefe D, Gilchrist MJ, Flicek P, Smith JC and Wardle FC: A gene regulatory network directed by zebrafish No tail accounts for its roles in mesoderm formation. Proc Natl Acad Sci USA. 106:3829–3834. 2009. View Article : Google Scholar : PubMed/NCBI | |
Gentsch GE, Owens ND, Martin SR, Piccinelli P, Faial T, Trotter MW, Gilchrist MJ and Smith JC: In vivo T-box transcription factor profiling reveals joint regulation of embryonic neuromesodermal bipotency. Cell Rep. 4:1185–1196. 2013. View Article : Google Scholar : PubMed/NCBI | |
Lolas M, Valenzuela PD, Tjian R and Liu Z: Charting Brachyury-mediated developmental pathways during early mouse embryogenesis. Proc Natl Acad Sci USA. 111:4478–4483. 2014. View Article : Google Scholar : PubMed/NCBI | |
Papaioannou VE and Silver LM: The T-box gene family. Bioessays. 20:9–19. 1998. View Article : Google Scholar : PubMed/NCBI | |
Mowla S, Pinnock R, Leaner VD, Goding CR and Prince S: PMA-induced up-regulation of TBX3 is mediated by AP-1 and contributes to breast cancer cell migration. Biochem J. 433:145–153. 2011. View Article : Google Scholar : PubMed/NCBI | |
Lingbeek ME, Jacobs JJ and van Lohuizen M: The T-box repressors TBX2 and TBX3 specifically regulate the tumor suppressor gene p14ARF via a variant T-site in the initiator. J Biol Chem. 277:26120–26127. 2002. View Article : Google Scholar : PubMed/NCBI | |
Davenport TG, Jerome-Majewska LA and Papaioannou VE: Mammary gland, limb and yolk sac defects in mice lacking Tbx3, the gene mutated in human ulnar mammary syndrome. Development. 130:2263–2273. 2003. View Article : Google Scholar : PubMed/NCBI | |
Rowley M, Grothey E and Couch FJ: The role of Tbx2 and Tbx3 in mammary development and tumorigenesis. J Mammary Gland Biol Neoplasia. 9:109–118. 2004. View Article : Google Scholar : PubMed/NCBI | |
Fan W, Huang X, Chen C, Gray J and Huang T: TBX3 and its isoform TBX3+2a are functionally distinctive in inhibition of senescence and are overexpressed in a subset of breast cancer cell lines. Cancer Res. 64:5132–5139. 2004. View Article : Google Scholar : PubMed/NCBI | |
Li J, Weinberg MS, Zerbini L and Prince S: The oncogenic TBX3 is a downstream target and mediator of the TGF-β1 signaling pathway. Mol Biol Cell. 24:3569–3576. 2013. View Article : Google Scholar : PubMed/NCBI | |
Peres J, Davis E, Mowla S, Bennett DC, Li JA, Wansleben S and Prince S: The highly homologous T-Box transcription factors, TBX2 and TBX3, have distinct roles in the oncogenic process. Genes Cancer. 1:272–282. 2010. View Article : Google Scholar : PubMed/NCBI | |
Boyd SC, Mijatov B, Pupo GM, Tran SL, Gowrishankar K, Shaw HM, Goding CR, Scolyer RA, Mann GJ, Kefford RF, et al: Oncogenic B-RAF(V600E) signaling induces the T-Box3 transcriptional repressor to repress E-cadherin and enhance melanoma cell invasion. J Invest Dermatol. 133:1269–1277. 2013. View Article : Google Scholar : PubMed/NCBI | |
Rodriguez M, Aladowicz E, Lanfrancone L and Goding CR: Tbx3 represses E-cadherin expression and enhances melanoma invasiveness. Cancer Res. 68:7872–7881. 2008. View Article : Google Scholar : PubMed/NCBI | |
Mowla S, Pinnock R, Leaner VD, Goding CR and Prince S: PMA-induced up-regulation of TBX3 is mediated by AP-1 and contributes to breast cancer cell migration. Biochem J. 433:145–153. 2011. View Article : Google Scholar : PubMed/NCBI | |
Jackson D, Zheng Y, Lyo D, Shen Y, Nakayama K, Nakayama KI, Humphries MJ, Reyland ME and Foster DA: Suppression of cell migration by protein kinase Cdelta. Oncogene. 24:3067–3072. 2005. View Article : Google Scholar : PubMed/NCBI | |
Wang ZG, Delva L, Gaboli M, Rivi R, Giorgio M, Cordon-Cardo C, Grosveld F and Pandolfi PP: Role of PML in cell growth and the retinoic acid pathway. Science. 279:1547–1551. 1998. View Article : Google Scholar : PubMed/NCBI | |
Gurrieri C, Capodieci P, Bernardi R, Scaglioni PP, Nafa K, Rush LJ, Verbel DA, Cordon-Cardo C and Pandolfi PP: Loss of the tumor suppressor PML in human cancers of multiple histologic origins. J Natl Cancer Inst. 96:269–279. 2004. View Article : Google Scholar : PubMed/NCBI | |
Martin N, Benhamed M, Nacerddine K, Demarque MD, van Lohuizen M, Dejean A and Bischof O: Physical and functional interaction between PML and TBX2 in the establishment of cellular senescence. EMBO J. 31:95–109. 2012. View Article : Google Scholar : PubMed/NCBI | |
Pomerantz J, Schreiber-Agus N, Liégeois NJ, Silverman A, Alland L, Chin L, Potes J, Chen K, Orlow I, Lee HW, et al: The Ink4a tumor suppressor gene product, p19Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell. 92:713–723. 1998. View Article : Google Scholar : PubMed/NCBI | |
Stott FJ, Bates S, James MC, McConnell BB, Starborg M, Brookes S, Palmero I, Ryan K, Hara E, Vousden KH and Peters G: The alternative product from the human CDKN2A locus, p14(ARF), participates in a regulatory feedback loop with p53 and MDM2. EMBO J. 17:5001–5014. 1998. View Article : Google Scholar : PubMed/NCBI | |
Prince S, Carreira S, Vance KW, Abrahams A and Goding CR: Tbx2 directly represses the expression of the p21(WAF1) cyclin-dependent kinase inhibitor. Cancer Res. 64:1669–1674. 2004. View Article : Google Scholar : PubMed/NCBI | |
Gitenay D and Baron VT: Is EGR1 a potential target for prostate cancer therapy? Future Oncol. 5:993–1003. 2009. View Article : Google Scholar : PubMed/NCBI | |
Krones-Herzig A, Adamson E and Mercola D: Early growth response 1 protein, an upstream gatekeeper of the p53 tumor suppressor, controls replicative senescence. Proc Natl Acad Sci USA. 100:3233–3238. 2003. View Article : Google Scholar : PubMed/NCBI | |
Redmond KL, Crawford NT, Farmer H, D'Costa ZC, O'Brien GJ, Buckley NE, Kennedy RD, Johnston PG, Harkin DP and Mullan PB: T-box 2 represses NDRG1 through an EGR1-dependent mechanism to drive the proliferation of breast cancer cells. Oncogene. 29:3252–3262. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zhu B, Zhang M, Byrum SD, Tackett AJ and Davie JK: TBX2 blocks myogenesis and promotes proliferation in rhabdomyosarcoma cells. Int J Cancer. 135:785–797. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ruas M and Peters G: The p16INK4a/CDKN2A tumor suppressor and its relatives. Biochim Biophys Acta. 1378:F115–F177. 1998.PubMed/NCBI | |
Vance KW, Carreira S, Brosch G and Goding CR: Tbx2 is overexpressed and plays an important role in maintaining proliferation and suppression of senescence in melanomas. Cancer Res. 65:2260–2268. 2005. View Article : Google Scholar : PubMed/NCBI | |
Basson CT, Bachinsky DR, Lin RC, Levi T, Elkins JA, Soults J, Grayzel D, Kroumpouzou E, Traill TA, Leblanc-Straceski J, et al: Mutations in human TBX5 [corrected] cause limb and cardiac malformation in Holt-Oram syndrome. Nat Genet. 15:30–35. 1997. View Article : Google Scholar : PubMed/NCBI | |
He ML, Chen Y, Peng Y, Jin D, Du D, Wu J, Lu P, Lin MC and Kung HF: Induction of apoptosis and inhibition of cell growth by developmental regulator hTBX5. Biochem Biophys Res Commun. 297:185–192. 2002. View Article : Google Scholar : PubMed/NCBI | |
Liu WK, Jiang XY and Zhang ZX: Expression of PSCA, PIWIL1, and TBX2 in endometrial adenocarcinoma. Onkologie. 33:241–245. 2010. View Article : Google Scholar : PubMed/NCBI | |
Glozak MA, Sengupta N, Zhang X and Seto E: Acetylation and deacetylation of non-histone proteins. Gene. 363:15–23. 2005. View Article : Google Scholar : PubMed/NCBI | |
Dokmanovic M and Marks PA: Prospects: Histone deacetylase inhibitors. J Cell Biochem. 96:293–304. 2005. View Article : Google Scholar : PubMed/NCBI | |
Puri PL, Iezzi S, Stiegler P, Chen TT, Schiltz RL, Muscat GE, Giordano A, Kedes L, Wang JY and Sartorelli V: Class I histone deacetylases sequentially interact with MyoD and pRb during skeletal myogenesis. Mol Cell. 8:885–897. 2001. View Article : Google Scholar : PubMed/NCBI | |
Zhang X, Ozawa Y, Lee H, Wen YD, Tan TH, Wadzinski BE and Seto E: Histone deacetylase 3 (HDAC3) activity is regulated by interaction with protein serine/threonine phosphatase 4. Genes Dev. 19:827–839. 2005. View Article : Google Scholar : PubMed/NCBI | |
Pan LN, Lu J and Huang B: HDAC inhibitors: A potential new category of anti-tumor agents. Cell Mol Immunol. 4:337–343. 2007.PubMed/NCBI | |
Hosford SR and Miller TW: Clinical potential of novel therapeutic targets in breast cancer: CDK4/6, Src, JAK/STAT, PARP, HDAC, and PI3K/AKT/mTOR pathways. Pharmgenomics Pers Med. 7:203–215. 2014.PubMed/NCBI | |
Yarosh W, Barrientos T, Esmailpour T, Lin L, Carpenter PM, Osann K, Anton-Culver H and Huang T: TBX3 is overexpressed in breast cancer and represses p14 ARF by interacting with histone deacetylases. Cancer Res. 68:693–699. 2008. View Article : Google Scholar : PubMed/NCBI | |
Burgucu D, Guney K, Sahinturk D, Ozbudak IH, Ozel D, Ozbilim G and Yavuzer U: Tbx3 represses PTEN and is over-expressed in head and neck squamous cell carcinoma. BMC Cancer. 12:4812012. View Article : Google Scholar : PubMed/NCBI | |
Moral M and Paramio JM: Akt pathway as a target for therapeutic intervention in HNSCC. Histol Histopathol. 23:1269–1278. 2008.PubMed/NCBI | |
Palena C, Polev DE, Tsang KY, Fernando RI, Litzinger M, Krukovskaya LL, Baranova AV, Kozlov AP and Schlom J: The human T-box mesodermal transcription factor Brachyury is a candidate target for T-cell-mediated cancer immunotherapy. Clin Cancer Res. 13:2471–2478. 2007. View Article : Google Scholar : PubMed/NCBI | |
Shimoda M, Sugiura T, Imajyo I, Ishii K, Chigita S, Seki K, Kobayashi Y and Shirasuna K: The T-box transcription factor Brachyury regulates epithelial-mesenchymal transition in association with cancer stem-like cells in adenoid cystic carcinoma cells. BMC Cancer. 12:3772012. View Article : Google Scholar : PubMed/NCBI | |
Grünert S, Jechlinger M and Beug H: Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nat Rev Mol Cell Biol. 4:657–665. 2003. View Article : Google Scholar : PubMed/NCBI | |
Nieto MA: The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol. 3:155–166. 2002. View Article : Google Scholar : PubMed/NCBI | |
Bolós V, Peinado H, Pérez-Moreno MA, Fraga MF, Esteller M and Cano A: The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: A comparison with Snail and E47 repressors. J Cell Sci. 116:499–511. 2003. View Article : Google Scholar : PubMed/NCBI | |
Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A and Weinberg RA: Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 117:927–939. 2004. View Article : Google Scholar : PubMed/NCBI | |
Wang B, Lindley LE, Fernandez-Vega V, Rieger ME, Sims AH and Briegel KJ: The T box transcription factor TBX2 promotes epithelial-mesenchymal transition and invasion of normal and malignant breast epithelial cells. PLoS One. 7:e413552012. View Article : Google Scholar : PubMed/NCBI | |
Wansleben S, Davis E, Peres J and Prince S: A novel role for the anti-senescence factor TBX2 in DNA repair and cisplatin resistance. Cell Death Dis. 4:e8462013. View Article : Google Scholar : PubMed/NCBI | |
Reya T and Clevers H: Wnt signalling in stem cells and cancer. Nature. 434:843–850. 2005. View Article : Google Scholar : PubMed/NCBI | |
Clevers H: Wnt/beta-catenin signaling in development and disease. Cell. 127:469–480. 2006. View Article : Google Scholar : PubMed/NCBI | |
Renard CA, Labalette C, Armengol C, Cougot D, Wei Y, Cairo S, Pineau P, Neuveut C, de Reyniès A, Dejean A, et al: Tbx3 is a downstream target of the Wnt/beta-catenin pathway and a critical mediator of beta-catenin survival functions in liver cancer. Cancer Res. 67:901–910. 2007. View Article : Google Scholar : PubMed/NCBI | |
Fong SH, Emelyanov A, Teh C and Korzh V: Wnt signalling mediated by Tbx2b regulates cell migration during formation of the neural plate. Development. 132:3587–3596. 2005. View Article : Google Scholar : PubMed/NCBI | |
Manning BD and Cantley LC: AKT/PKB signaling: Navigating downstream. Cell. 129:1261–1274. 2007. View Article : Google Scholar : PubMed/NCBI | |
Brazil DP, Park J and Hemmings BA: PKB binding proteins. Getting in on the Akt. Cell. 111:293–303. 2002. View Article : Google Scholar : PubMed/NCBI | |
Stahl JM, Sharma A, Cheung M, Zimmerman M, Cheng JQ, Bosenberg MW, Kester M, Sandirasegarane L and Robertson GP: Deregulated Akt3 activity promotes development of malignant melanoma. Cancer Res. 64:7002–7010. 2004. View Article : Google Scholar : PubMed/NCBI | |
Cheung M, Sharma A, Madhunapantula SV and Robertson GP: Akt3 and mutant V600E B-Raf cooperate to promote early melanoma development. Cancer Res. 68:3429–3439. 2008. View Article : Google Scholar : PubMed/NCBI | |
Peres J, Mowla S and Prince S: The T-box transcription factor, TBX3, is a key substrate of AKT3 in melanomagenesis. Oncotarget. 6:1821–1833. 2015. View Article : Google Scholar : PubMed/NCBI | |
Paxton C, Zhao H, Chin Y, Langner K and Reecy J: Murine Tbx2 contains domains that activate and repress gene transcription. Gene. 283:117–24. 2002. View Article : Google Scholar : PubMed/NCBI | |
Zhou Y, Du W, Koretsky T, Bagby GC and Pang Q: TAT-mediated intracellular delivery of NPM-derived peptide induces apoptosis in leukemic cells and suppresses leukemogenesis in mice. Blood. 112:2474–2483. 2008. View Article : Google Scholar : PubMed/NCBI | |
Fåhraeus R, Laín S, Ball KL and Lane DP: Characterization of the cyclin-dependent kinase inhibitory domain of the INK4 family as a model for a synthetic tumour suppressor molecule. Oncogene. 16:587–596. 1998. View Article : Google Scholar : PubMed/NCBI | |
Bonfanti M, Taverna S, Salmona M, D'Incalci M and Broggini M: p21WAF1-derived peptides linked to an internalization peptide inhibit human cancer cell growth. Cancer Res. 57:1442–1446. 1997.PubMed/NCBI | |
Douglas NC and Papaioannou VE: The T-box transcription factors TBX2 and TBX3 in mammary gland development and breast cancer. J Mammary Gland Biol Neoplasia. 18:143–147. 2013. View Article : Google Scholar : PubMed/NCBI |