Telomerase modulates Wnt signalling by association with target gene chromatin

Nature

Volumn 460, Issue 7251, 2009, Pages 66-72

  Park, Jae Il ^a   Venteicher, Andrew S ^a   Hong, Ji Yeon ^b   Choi, Jinkuk ^a   Jun, Sohee ^a   Shkreli, Marina ^a   Chang, Woody ^a   Meng, Zhaojing ^c   Cheung, Peggie ^a   Ji, Hong ^b   Mclaughlin, Margaret ^d   Veenstra, Timothy D ^c   Nusse, Roel ^a   Mccrea, Pierre D ^b   Artandi, Steven E ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c SAIC FREDERICK INC   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; BRG1 PROTEIN; MESSENGER RNA; PROTEIN SWI; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR SNF; WNT PROTEIN;

CYTOLOGY; ENZYME ACTIVITY; GENE EXPRESSION; SIGNALING; TUMOR;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; CELL PROLIFERATION; CELL RENEWAL; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPLEX FORMATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GASTROINTESTINAL TRACT; GENE ACTIVATION; GENE CONTROL; GENE OVEREXPRESSION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SOMITE; STEM CELL; VERTEBRA; XENOPUS;

ANIMALS; BETA CATENIN; CELL LINE; CHORISTOMA; CHROMATIN; DNA HELICASES; GENES, REPORTER; HELA CELLS; HUMANS; INTESTINE, SMALL; MICE; NUCLEAR PROTEINS; OOCYTES; PLASMIDS; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; SOMITES; TELOMERASE; TRANSCRIPTION FACTORS; WNT PROTEINS; XENOPUS LAEVIS;

MUS; XENOPUS LAEVIS;

EID: 67650065306     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature08137     Document Type: Review

References (51)

1. Reya, T. & Clevers, H. Wnt signalling in stem cells and cancer. Nature 434, 843-850 (2005).
2. Gat, U., DasGupta, R., Degenstein, L. & Fuchs, E. De Novo hair follicle morphogenesis and hair tumors in mice expressing a truncated b-catenin in skin. Cell 95, 605-614 (1998).
3. Van Mater, D., Kolligs, F. T., Dlugosz, A. A. & Fearon, E. R. Transient activation of b-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).
4. Lo Celso, C., Prowse, D. M. & Watt, F. M. Transient activation of b-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).
5. Sarin, K. Y. et al. Conditional telomerase induction causes proliferation of hair follicle stem cells. Nature 436, 1048-1052 (2005).
6. Flores, I., Cayuela, M. L. & Blasco, M. A. Effects of telomerase and telomere length on epidermal stem cell behavior. Science 309, 1253-1256 (2005).
7. Polakis, P. The many ways of Wnt in cancer. Curr. Opin. Genet. Dev. 17, 45-51 (2007).
8. Maser, R.S. & DePinho, R.A. Connecting chromosomes, crisis, and cancer. Science 297, 565-569 (2002).
9. Smogorzewska,A. & deLange,T. Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem. 73, 177-208 (2004).
10. Choi, J. et al. TERT promotes epithelial proliferation through transcriptiona control of a Myc- and Wnt-related developmental program. PLoS Genet. 4, e10 (2008).
11. Artandi, S. E. et al. Constitutive telomerase expression promotes mammary carcinomas in agingmice. Proc. Natl Acad. Sci. USA 99, 8191-8196 (2002).
12. Gonzalez-Suarez, E. et al. Increased epidermal tumors and increased skin wound healing in transgenic mice overexpressing the catalytic subunit of telomerase,
13. mTERT, in basal keratinocytes. EMBO J. 20, 2619-2630 (2001).
14. Stewart, S. A. et al. Telomerase contributes to tumorigenesis by a telomere length-independent mechanism. Proc. Natl Acad. Sci. USA 99, 12606-12611 (2002).
15. 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).
16. Armstrong, L. et al. Overexpression of telomerase confers growth advantage, stressresistance, and enhanced differentiation of ESCs toward the hematopoietic lineage. Stem Cells 23, 516-529 (2005).
17. Imamura, S. et al. A non-canonical function of zebrafish telomerase reverse transcriptase is required for developmental hematopoiesis. PLoSONE3, e3364 (2008).
18. 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).
19. Lee, J. et al. TERT promotes cellular and organismal survival independently of telomerase activity. Oncogene 27, 3754-3760 (2008).
20. Masutomi, K. et al. The telomerase reverse transcriptase regulates chromatin state and DNA damage responses. Proc. Natl Acad. Sci. USA 102, 8222-8227 (2005).
21. Venteicher, A. S., Meng, Z., Mason, P. J., Veenstra, T. D. & Artandi, S. E. Identification of ATPases pontin and reptin as telomerase components essential forholoenzyme assembly. Cell 132, 945-957 (2008).
22. Wu, J. I., Lessard, J. & Crabtree, G. R. Understanding the words of chromatin regulation. Cell 136, 200-206(2009).
23. 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).
24. Barker, N. et al. The chromatin remodelling factor Brg-1interacts withβ-cateninto promote target gene activation. EMBO J. 20, 4935-4943 (2001).
25. Major, M. B. et al. New regulators of Wnt/b-catenin signaling revealed by integrative molecular screening. Sci Signal 1, ra12 (2008).
26. Henriksson,M. &Luscher,B. Proteins of the Myc network: essential regulators of cell growth and differentiation. Adv. Cancer Res. 68, 109-182 (1996).
27. 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).
28. 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).
29. Ventura, A. et al. Restoration of p53 function leads to tumour regression in vivo. Nature 445, 661-665 (2007).
30. 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).
31. Huelsken,J.et al. Requirement for β-catenin in anterior-posterior axis formation in mice. J. Cell Biol. 148, 567-578 (2000).
32. 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).
33. Kao, K. R. & Elinson, R. P. The entire mesodermal mantle behaves as Spemann' organizer in dorsoanterior enhanced Xenopuslaevis embryos. Dev. Biol. 127, 64-77 (1988).
34. 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).
35. Dubrulle,J. &Pourquie,O.Couplingsegmentation to axis formation. Development 131, 5783-5793 (2004).
36. 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).
37. 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).
38. 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).
39. 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).
40. Lee,H.-W. et al. Essential role of mouse telomerase in highly proliferative organs. Nature 392, 569-574 (1998).
41. 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).
42. Lohnes,D. TheCdx1 homeodomain protein: an integrator of posterior signaling in the mouse. Bioessays 25, 971-980 (2003).
43. 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).
44. Rajaraman, S. et al. Telomere uncApplng in progenitor cells with critical telomere shortening is coupled to S-phase progression in vivo. Proc. Natl Acad. Sci. USA 104, 17747-17752 (2007).
45. Willert, K. & Jones, K. A. Wnt signaling: is the party in the nucleus? Genes Dev. 20, 1394-1404(2006).
46. 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).
47. Firestein, R. et al. CDK8 is a colorectal cancer oncogene that regulates b-catenin activity. Nature 455, 547-551 (2008).
48. Carrera, I., Janody, F., Leeds, N., Duveau, F. & Treisman, J. E. Pygopus activates Wingless target gene transcription through the mediator complex subunits Med12 andMed13. Proc. Natl Acad. Sci. USA 105, 6644-6649 (2008).
49. 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).
50. Wong, K.-K. et al. Telomere dysfunction impairs DNA repair and enhances sensitivity to ionizing radiation. Nature Genet. 26, 85-88 (2000).
51. Armanios, M. Syndromes of telomere shortening. Annu. Rev. Genomics Hum. Genet. doi:10.1146/annurev-genom-082908-150046 (2009).