TRF1 controls telomere length and mitotic fidelity in epithelial homeostasis

Molecular and Cellular Biology

Volumn 29, Issue 6, 2009, Pages 1608-1625

  Muñoz, Purificacion ^a,c   Blanco, Raquel ^a   De Carcer, Guillermo ^a   Schoeftner, Stefan ^a   Benetti, Roberta ^a,d   Flores, Juana M ^b   Malumbres, Marcos ^a   Blasco, Maria A ^a  

^a Centro Nacional de Investigaciones Oncológicas   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c CATALAN INSTITUTE OF ONCOLOGY   (Spain)

^d Laboratorio Nazionale Centro Universitario Biotecnologie (LNCIB)   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BUB1 RELATED PROTEIN; NUCLEASE; PROTEIN MAD2; TELOMERIC REPEAT BINDING FACTOR 1; UNCLASSIFIED DRUG; XPF NUCLEASE;

ANIMAL TISSUE; ARTICLE; EPITHELIUM CELL; HOMEOSTASIS; MITOSIS RATE; MITOSIS SPINDLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TELOMERE;

ANIMALS; CELL CYCLE PROTEINS; CELLS, CULTURED; DNA DAMAGE; DNA-BINDING PROTEINS; ENDONUCLEASES; EPIDERMIS; EPITHELIUM; HOMEOSTASIS; KERATINOCYTES; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MITOSIS; MITOTIC SPINDLE APPARATUS; PROTEIN-SERINE-THREONINE KINASES; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 1; TELOMERIC REPEAT BINDING PROTEIN 2;

MAMMALIA; MUS;

EID: 62849084852     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01339-08     Document Type: Article

References (59)

1. Ancelin, K., M. Brunori, S. Bauwens, C. E. Koering, C. Brun, M. Ricoul, J. P. Pommier, L. Sabatier, and E. Gilson. 2002. Targeting assay to study the cis functions of human telomeric proteins: evidence for inhibition of telomerase by TRF1 and for activation of telomere degradation by TRF2. Mol. Cell. Biol. 22:3474-3487.
2. Azzalin, C. M., P. Reichenbach, L. Khoriauli, E. Giulotto, and J. Lingner. 2007. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318:798-801.
3. Bailey, S. M., M. A. Brenneman, and E. H. Goodwin. 2004. Frequent recombination in telomeric DNA may extend the proliferative life of telomerase-negative cells. Nucleic Acids Res. 32:3743-3751.
4. Barrandon, Y., and H. Green. 1987. Three clonal types of keratinocyte with different capacities for multiplication. Proc. Natl. Acad. Sci. USA 84:2302-2306.
5. Bechter, O. E., Y. Zou, W. Walker, W. E. Wright, and J. W. Shay. 2004. Telomeric recombination in mismatch repair deficient human colon cancer cells after telomerase inhibition. Cancer Res. 64:3444-3451.
6. Benetti, R., S. Gonzalo, I. Jaco, G. Schotta, P. Klatt, T. Jenuwein, and M. A. Blasco. 2007. Suv4-20h deficiency results in telomere elongation and derepression of telomere recombination. J. Cell Biol. 178:925-936.
7. Blanco, R., P. Munoz, J. M. Flores, P. Klatt, and M. A. Blasco. 2007. Telomerase abrogation dramatically accelerates TRF2-induced epithelial carcinogenesis. Genes Dev. 21:206-220.
8. Blasco, M. A., H. W. Lee, M. P. Hande, E. Samper, P. M. Lansdorp, R. A. DePinho, and C. W. Greider. 1997. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91:25-34.
9. Broccoli, D., A. Smogorzewska, L. Chong, and T. de Lange. 1997. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat. Genet. 17:231-235.
10. Canudas, S., B. R. Houghtaling, J. Y. Kim, J. N. Dynek, W. G. Chang, and S. Smith. 2007. Protein requirements for sister telomere association in human cells. EMBO J. 26:4867-4878.
11. Celli, G. B., and T. de Lange. 2005. DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat. Cell Biol. 7:712-718.
12. Cook, B. D., J. N. Dynek, W. Chang, G. Shostak, and S. Smith. 2002. Role for the related poly(ADP-ribose) polymerases tankyrase 1 and 2 at human telomeres. Mol. Cell. Biol. 22:332-342.
13. Chan, S. W., and E. H. Blackburn. 2002. New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene 21:553-563.
14. Chen, Y., Y. Yang, M. van Overbeek, J. R. Donigian, P. Baciu, T. de Lange, and M. Lei. 2008. A shared docking motif in TRF1 and TRF2 used for differential recruitment of telomeric proteins. Science 319:1092-1096.
15. Chiang, Y. J., M. L. Nguyen, S. Gurunathan, P. Kaminker, L. Tessarollo, J. Campisi, and R. J. Hodes. 2006. Generation and characterization of telomere length maintenance in tankyrase 2-deficient mice. Mol. Cell. Biol. 26:2037-2043.
16. d'Adda di Fagagna, F., P. M. Reaper, L. Clay-Farrace, H. Fiegler, P. Carr, T. Von Zglinicki, G. Saretzki, N. P. Carter, and S. P. Jackson. 2003. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426:194-198.
17. de Laat, W. L., N. G. Jaspers, and J. H. Hoeijmakers. 1999. Molecular mechanism of nucleotide excision repair. Genes Dev. 13:768-785.
18. de Lange, T. 2005. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19:2100-2110.
19. Donigian, J. R., and T. de Lange. 2007. The role of the poly(ADP-ribose) polymerase tankyrase1 in telomere length control by the TRF1 component of the shelterin complex. J. Biol. Chem. 282:22662-22667.
20. Dunham, M. A., A. A. Neumann, C. L. Fasching, and R. R. Reddel. 2000. Telomere maintenance by recombination in human cells. Nat. Genet. 26:447-450.
21. Fairall, L., L. Chapman, H. Moss, T. de Lange, and D. Rhodes. 2001. Structure of the TRFH dimerization domain of the human telomeric proteins TRF1 and TRF2. Mol. Cell 8:351-361.
22. Flores, I., M. L. Cayuela, and M. A. Blasco. 2005. Effects of telomerase and telomere length on epidermal stem cell behavior. Science 309:1253-1256.
23. Garcia-Cao, I., M. Garcia-Cao, A. Tomas-Loba, J. Martin-Caballero, J. M. Flores, P. Klatt, M. A. Blasco, and M. Serrano. 2006. Increased p53 activity does not accelerate telomere-driven ageing. EMBO Rep. 7:546-552.
24. Reference deleted.
25. Gonzalo, S., I. Jaco, M. F. Fraga, T. Chen, E. Li, M. Esteller, and M. A. Blasco. 2006. DNA methyltransferases control telomere length and telomere recombination in mammalian cells. Nat. Cell Biol. 8:416-424.
26. Herrera, E., E. Samper, J. Martin-Caballero, J. M. Flores, H. W. Lee, and M. A. Blasco. 1999. Disease states associated with telomerase deficiency appear earlier in mice with short telomeres. EMBO J. 18:2950-2960.
27. Hsiao, S. J., M. F. Poitras, B. D. Cook, Y. Liu, and S. Smith. 2006. Tankyrase 2 poly(ADP-ribose) polymerase domain-deleted mice exhibit growth defects but have normal telomere length and capping. Mol. Cell. Biol. 26:2044-2054.
28. Hsiao, S. J., and S. Smith. 2008. Tankyrase function at telomeres, spindle poles, and beyond. Biochimie 90:83-92.
29. Karlseder, J., L. Kachatrian, H. Takai, K. Mercer, S. Hingorani, T. Jacks, and T. de Lange. 2003. Targeted deletion reveals an essential function for the telomere length regulator Trf1. Mol. Cell. Biol. 23:6533-6541.
30. Koering, C. E., A. Pollice, M. P. Zibella, S. Bauwens, A. Puisieux, M. Brunori, C. Brun, L. Martins, L. Sabatier, J. F. Pulitzer, and E. Gilson. 2002. Human telomeric position effect is determined by chromosomal context and telomeric chromatin integrity. EMBO Rep. 3:1055-1061.
31. Liu, D., M. S. O'Connor, J. Qin, and Z. Songyang. 2004. Telosome, a mammalian telomere-associated complex formed by multiple telomeric proteins. J. Biol. Chem. 279:51338-51342.
32. Loayza, D., and T. De Lange. 2003. POT1 as a terminal transducer of TRF1 telomere length control. Nature 423:1013-1018.
33. Matsutani, N., H. Yokozaki, E. Tahara, H. Tahara, H. Kuniyasu, K. Haruma, K. Chayama, and W. Yasui. 2001. Expression of telomeric repeat binding factor 1 and 2 and TRF1-interacting nuclear protein 2 in human gastric carcinomas. Int. J. Oncol. 19:507-512.
34. Modesti, M., and R. Kanaar. 2001. DNA repair: spot(light)s on chromatin. Curr. Biol. 11:R229-R232.
35. Munoz, P., R. Blanco, J. M. Flores, and M. A. Blasco. 2005. XPF nuclease-dependent telomere loss and increased DNA damage in mice overexpressing TRF2 result in premature aging and cancer. Nat. Genet. 37:1063-1071.
36. Muntoni, A., and R. R. Reddel. 2005. The first molecular details of ALT in human tumor cells. Hum. Mol. Genet. 14(Spec. No. 2):R191-R196.
37. Muramatsu, Y., T. Ohishi, M. Sakamoto, T. Tsuruo, and H. Seimiya. 2007. Cross-species difference in telomeric function of tankyrase 1. Cancer Sci. 98:850-857.
38. Murillas, R., F. Larcher, C. J. Conti, M. Santos, A. Ullrich, and J. L. Jorcano. 1995. Expression of a dominant negative mutant of epidermal growth factor receptor in the epidermis of transgenic mice elicits striking alterations in hair follicle development and skin structure. EMBO J. 14:5216-5223.
39. Musaro, M., L. Ciapponi, B. Fasulo, M. Gatti, and G. Cenci. 2008. Unprotected Drosophila melanogaster telomeres activate the spindle assembly checkpoint. Nat. Genet. 40:362-366.
40. Nakamura, M., X. Z. Zhou, S. Kishi, I. Kosugi, Y. Tsutsui, and K. P. Lu. 2001. A specific interaction between the telomeric protein Pin2/TRF1 and the mitotic spindle. Curr. Biol. 11:1512-1516.
41. Oh, B. K., Y. J. Kim, C. Park, and Y. N. Park. 2005. Up-regulation of telomere-binding proteins, TRF1, TRF2, and TIN2 is related to telomere shortening during human multistep hepatocarcinogenesis. Am. J. Pathol. 166:73-80.
42. Petit, C., and A. Sancar. 1999. Nucleotide excision repair: from E. coli to man. Biochimie 81:15-25.
43. Prime, G., and D. Markie. 2005. The telomere repeat binding protein Trf1 interacts with the spindle checkpoint protein Mad1 and Nek2 mitotic kinase. Cell Cycle 4:121-124.
44. Samper, E., F. A. Goytisolo, P. Slijepcevic, P. P. van Buul, and M. A. Blasco. 2000. Mammalian Ku86 protein prevents telomeric fusions independently of the length of TTAGGG repeats and the G-strand overhang. EMBO Rep. 1:244-252.
45. Savage, S. A., R. T. Calado, Z. T. Xin, H. Ly, N. S. Young, and S. J. Chanock. 2006. Genetic variation in telomeric repeat binding factors 1 and 2 in aplastic anemia. Exp. Hematol. 34:664-671.
46. Savage, S. A., N. Giri, G. M. Baerlocher, N. Orr, P. M. Lansdorp, and B. P. Alter. 2008. TINF2, a component of the shelterin telomere protection complex, is mutated in dyskeratosis congenita. Am. J. Hum. Genet. 82:501-509.
47. Schoeftner, S., and M. A. Blasco. 2008. Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat. Cell Biol. 10:228-236.
48. Siegl-Cachedenier, I., I. Flores, P. Klatt, and M. A. Blasco. 2007. Telomerase reverses epidermal hair follicle stem cell defects and loss of long-term survival associated with critically short telomeres. J. Cell Biol. 179:277-290.
49. Smith, S., I. Giriat, A. Schmitt, and T. de Lange. 1998. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science 282:1484-1487.
50. Smogorzewska, A., B. van Steensel, A. Bianchi, S. Oelmann, M. R. Schaefer, G. Schnapp, and T. de Lange. 2000. Control of human telomere length by TRF1 and TRF2. Mol. Cell. Biol. 20:1659-1668.
51. Takai, H., A. Smogorzewska, and T. de Lange. 2003. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13:1549-1556.
52. van Steensel, B., and T. de Lange. 1997. Control of telomere length by the human telomeric protein TRF1. Nature 385:740-743.
53. van Steensel, B., A. Smogorzewska, and T. de Lange. 1998. TRF2 protects human telomeres from end-to-end fusions. Cell 92:401-413.
54. Wang, R. C., A. Smogorzewska, and T. de Lange. 2004. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119:355-368.
55. Wu, L., A. S. Multani, H. He, W. Cosme-Blanco, Y. Deng, J. M. Deng, O. Bachilo, S. Pathak, H. Tahara, S. M. Bailey, R. R. Behringer, and S. Chang. 2006. Pot1 deficiency initiates DNA damage checkpoint activation and aberrant homologous recombination at telomeres. Cell 126:49-62.
56. Xin, H., D. Liu, M. Wan, A. Safari, H. Kim, W. Sun, M. S. O'Connor, and Z. Songyang. 2007. TPP1 is a homologue of ciliate TEBP-beta and interacts with POT1 to recruit telomerase. Nature 445:559-562.
57. Ye, J. Z., D. Hockemeyer, A. N. Krutchinsky, D. Loayza, S. M. Hooper, B. T. Chait, and T. de Lange. 2004. POT1-interacting protein PIP1: a telomere length regulator that recruits POT1 to the TIN2/TRF1 complex. Genes Dev. 18:1649-1654.
58. Zhu, X. D., L. Niedernhofer, B. Kuster, M. Mann, J. H. Hoeijmakers, and T. de Lange. 2003. ERCC1/XPF removes the 3′ overhang from uncapped telomeres and represses formation of telomeric DNA-containing double minute chromosomes. Mol. Cell 12:1489-1498.
59. Zijlmans, J. M., U. M. Martens, S. S. Poon, A. K. Raap, H. J. Tanke, R. K. Ward, and P. M. Lansdorp. 1997. Telomeres in the mouse have large interchromosomal variations in the number of T2AG3 repeats. Proc. Natl. Acad. Sci. USA 94:7423-7428.