nature.com

Telomerase modulates Wnt signalling by association with target gene chromatin - Nature

  • ️Artandi, Steven E.
  • ️Thu Jul 02 2009
  • Reya, T. & Clevers, H. Wnt signalling in stem cells and cancer. Nature 434, 843–850 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  • Gat, U., DasGupta, R., Degenstein, L. & Fuchs, E. De Novo hair follicle morphogenesis and hair tumors in mice expressing a truncated β-catenin in skin. Cell 95, 605–614 (1998)

    Article  CAS  PubMed  Google Scholar 

  • Van Mater, D., Kolligs, F. T., Dlugosz, A. A. & Fearon, E. R. Transient activation of β-catenin signaling in cutaneous keratinocytes is sufficient to trigger the active growth phase of the hair cycle in mice. Genes Dev. 17, 1219–1224 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lo Celso, C., Prowse, D. M. & Watt, F. M. Transient activation of β-catenin signalling in adult mouse epidermis is sufficient to induce new hair follicles but continuous activation is required to maintain hair follicle tumours. Development 131, 1787–1799 (2004)

    Article  CAS  PubMed  Google Scholar 

  • Sarin, K. Y. et al. Conditional telomerase induction causes proliferation of hair follicle stem cells. Nature 436, 1048–1052 (2005)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Flores, I., Cayuela, M. L. & Blasco, M. A. Effects of telomerase and telomere length on epidermal stem cell behavior. Science 309, 1253–1256 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  • Polakis, P. The many ways of Wnt in cancer. Curr. Opin. Genet. Dev. 17, 45–51 (2007)

    Article  CAS  PubMed  Google Scholar 

  • Maser, R. S. & DePinho, R. A. Connecting chromosomes, crisis, and cancer. Science 297, 565–569 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  • Smogorzewska, A. & de Lange, T. Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem. 73, 177–208 (2004)

    Article  CAS  PubMed  Google Scholar 

  • Choi, J. et al. TERT promotes epithelial proliferation through transcriptional control of a Myc- and Wnt-related developmental program. PLoS Genet. 4, e10 (2008)

    Article  PubMed  PubMed Central  Google Scholar 

  • Artandi, S. E. et al. Constitutive telomerase expression promotes mammary carcinomas in aging mice. Proc. Natl Acad. Sci. USA 99, 8191–8196 (2002)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez-Suarez, E. et al. Increased epidermal tumors and increased skin wound healing in transgenic mice overexpressing the catalytic subunit of telomerase, mTERT, in basal keratinocytes. EMBO J. 20, 2619–2630 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stewart, S. A. et al. Telomerase contributes to tumorigenesis by a telomere length-independent mechanism. Proc. Natl Acad. Sci. USA 99, 12606–12611 (2002)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith, L. L., Coller, H. A. & Roberts, J. M. Telomerase modulates expression of growth-controlling genes and enhances cell proliferation. Nature Cell Biol. 5, 474–479 (2003)

    Article  CAS  PubMed  Google Scholar 

  • Armstrong, L. et al. Overexpression of telomerase confers growth advantage, stress resistance, and enhanced differentiation of ESCs toward the hematopoietic lineage. Stem Cells 23, 516–529 (2005)

    Article  CAS  PubMed  Google Scholar 

  • Imamura, S. et al. A non-canonical function of zebrafish telomerase reverse transcriptase is required for developmental hematopoiesis. PLoS ONE 3, e3364 (2008)

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Yang, C. et al. A key role for telomerase reverse transcriptase unit in modulating human embryonic stem cell proliferation, cell cycle dynamics, and in vitro differentiation. Stem Cells 26, 850–863 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Lee, J. et al. TERT promotes cellular and organismal survival independently of telomerase activity. Oncogene 27, 3754–3760 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Masutomi, K. et al. The telomerase reverse transcriptase regulates chromatin state and DNA damage responses. Proc. Natl Acad. Sci. USA 102, 8222–8227 (2005)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Venteicher, A. S., Meng, Z., Mason, P. J., Veenstra, T. D. & Artandi, S. E. Identification of ATPases pontin and reptin as telomerase components essential for holoenzyme assembly. Cell 132, 945–957 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, J. I., Lessard, J. & Crabtree, G. R. Understanding the words of chromatin regulation. Cell 136, 200–206 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, Y. L. et al. Immunodetection of human telomerase reverse-transcriptase (hTERT) re-appraised: nucleolin and telomerase cross paths. J. Cell Sci. 119, 2797–2806 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Barker, N. et al. The chromatin remodelling factor Brg-1 interacts with β-catenin to promote target gene activation. EMBO J. 20, 4935–4943 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Major, M. B. et al. New regulators of Wnt/β-catenin signaling revealed by integrative molecular screening. Sci Signal 1, ra12 (2008)

    PubMed  Google Scholar 

  • Henriksson, M. & Luscher, B. Proteins of the Myc network: essential regulators of cell growth and differentiation. Adv. Cancer Res. 68, 109–182 (1996)

    Article  CAS  PubMed  Google Scholar 

  • Korinek, V. et al. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nature Genet. 19, 379–383 (1998)

    Article  CAS  PubMed  Google Scholar 

  • Lustig, B. et al. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell. Biol. 22, 1184–1193 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ventura, A. et al. Restoration of p53 function leads to tumour regression in vivo . Nature 445, 661–665 (2007)

    CAS  PubMed  Google Scholar 

  • McMahon, A. P. & Moon, R. T. Ectopic expression of the proto-oncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis. Cell 58, 1075–1084 (1989)

    Article  CAS  PubMed  Google Scholar 

  • Huelsken, J. et al. Requirement for β-catenin in anterior-posterior axis formation in mice. J. Cell Biol. 148, 567–578 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heasman, J. et al. Overexpression of cadherins and underexpression of β-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79, 791–803 (1994)

    Article  CAS  PubMed  Google Scholar 

  • Kao, K. R. & Elinson, R. P. The entire mesodermal mantle behaves as Spemann’ organizer in dorsoanterior enhanced Xenopus laevis embryos. Dev. Biol. 127, 64–77 (1988)

    Article  CAS  PubMed  Google Scholar 

  • Yoshikawa, Y., Fujimori, T., McMahon, A. P. & Takada, S. Evidence that absence of Wnt-3a signaling promotes neuralization instead of paraxial mesoderm development in the mouse. Dev. Biol. 183, 234–242 (1997)

    Article  CAS  PubMed  Google Scholar 

  • Dubrulle, J. & Pourquie, O. Coupling segmentation to axis formation. Development 131, 5783–5793 (2004)

    Article  CAS  PubMed  Google Scholar 

  • Greco, T. L. et al. Analysis of the vestigial tail mutation demonstrates that Wnt-3a gene dosage regulates mouse axial development. Genes Dev. 10, 313–324 (1996)

    Article  CAS  PubMed  Google Scholar 

  • Ikeya, M. & Takada, S. Wnt-3a is required for somite specification along the anteroposterior axis of the mouse embryo and for regulation of cdx-1 expression. Mech. Dev. 103, 27–33 (2001)

    Article  CAS  PubMed  Google Scholar 

  • Pownall, M. E., Tucker, A. S., Slack, J. M. & Isaacs, H. V. eFGF, Xcad3 and Hox genes form a molecular pathway that establishes the anteroposterior axis in Xenopus . Development 122, 3881–3892 (1996)

    CAS  PubMed  Google Scholar 

  • Houle, M., Prinos, P., Iulianella, A., Bouchard, N. & Lohnes, D. Retinoic acid regulation of Cdx1: an indirect mechanism for retinoids and vertebral specification. Mol. Cell. Biol. 20, 6579–6586 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, H.-W. et al. Essential role of mouse telomerase in highly proliferative organs. Nature 392, 569–574 (1998)

    Article  ADS  CAS  PubMed  Google Scholar 

  • Erdmann, N., Liu, Y. & Harrington, L. Distinct dosage requirements for the maintenance of long and short telomeres in mTert heterozygous mice. Proc. Natl Acad. Sci. USA 101, 6080–6085 (2004)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Lohnes, D. The Cdx1 homeodomain protein: an integrator of posterior signaling in the mouse. Bioessays 25, 971–980 (2003)

    Article  CAS  PubMed  Google Scholar 

  • Farazi, P. A., Glickman, J., Horner, J. & Depinho, R. A. Cooperative interactions of p53 mutation, telomere dysfunction, and chronic liver damage in hepatocellular carcinoma progression. Cancer Res. 66, 4766–4773 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Rajaraman, S. et al. Telomere uncapping in progenitor cells with critical telomere shortening is coupled to S-phase progression in vivo . Proc. Natl Acad. Sci. USA 104, 17747–17752 (2007)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Willert, K. & Jones, K. A. Wnt signaling: is the party in the nucleus? Genes Dev. 20, 1394–1404 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Daniels, D. L. & Weis, W. I. β-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nature Struct. Mol. Biol. 12, 364–371 (2005)

    Article  CAS  Google Scholar 

  • Firestein, R. et al. CDK8 is a colorectal cancer oncogene that regulates β-catenin activity. Nature 455, 547–551 (2008)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Carrera, I., Janody, F., Leeds, N., Duveau, F. & Treisman, J. E. Pygopus activates Wingless target gene transcription through the mediator complex subunits Med12 and Med13. Proc. Natl Acad. Sci. USA 105, 6644–6649 (2008)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, S., Xu, X., Hecht, A. & Boyer, T. G. Mediator is a transducer of Wnt/β-catenin signaling. J. Biol. Chem. 281, 14066–14075 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Wong, K.-K. et al. Telomere dysfunction impairs DNA repair and enhances sensitivity to ionizing radiation. Nature Genet. 26, 85–88 (2000)

    Article  CAS  PubMed  Google Scholar 

  • Armanios, M. Syndromes of telomere shortening. Annu. Rev. Genomics Hum. Genet. 10.1146/annurev-genom-082908-150046 (2009)