The DNA damage response at eroded telomeres and tethering to the nuclear pore complex

Nature Cell Biology

Volumn 11, Issue 8, 2009, Pages 980-987

  Khadaroo, Basheer ^a   Teixeira, M Teresa ^b   Luciano, Pierre ^a   Eckert Boulet, Nadine ^c   Germann, Susanne M ^c   Simon, Marie Noelle ^a   Gallina, Irene ^c   Abdallah, Pauline ^b   Gilson, Eric ^b   Géli, Vincent ^a   Lisby, Michael ^c  

^a CNRS   (France)

^b UNIVERSITÉ LYON 1   (France)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CHECKPOINT KINASE 1; DERMCIDIN; DERMCIDIN 2; MRE11 PROTEIN; PROTEIN CDC13; PROTEIN RPA; RAD52 PROTEIN; REPLICATION FACTOR A; SUMO PROTEIN; TELOMERASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA DAMAGE; DNA HYBRIDIZATION; DNA REPAIR; GENE CASSETTE; GENE EXPRESSION; GENE FUNCTION; GENE INACTIVATION; GENE REPLICATION; HAPLOIDY; IMMUNOPRECIPITATION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE; PLASMID; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; SENESCENCE; TELOMERE; YEAST;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL CYCLE PROTEINS; CHROMATIN IMMUNOPRECIPITATION; DNA DAMAGE; DNA REPAIR; DNA, SINGLE-STRANDED; G2 PHASE; HAPLOIDY; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MUTATION; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINANT FUSION PROTEINS; REPLICATION PROTEIN A; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERASE; TELOMERE; TELOMERE-BINDING PROTEINS;

EUKARYOTA;

EID: 68249091644     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1910     Document Type: Article

References (31)

1. Gilson, E. & Geli, V. How telomeres are replicated. Nature Rev. Mol. Cell Biol. 8, 825-838 (2007).
2. Wellinger, R. J., Wolf, A. J. & Zakian, V. A. Saccharomyces telomeres acquire single-strand TG1-3 tails late in S phase. Cell 72, 51-60 (1993).
3. Larrivee, M., LeBel, C. & Wellinger, R. J. The generation of proper constitutive G-tails on yeast telomeres is dependent on the MRX complex. Genes Dev. 18, 1391-1396 (2004).
4. Vodenicharov, M. D. & Wellinger, R. J. DNA degradation at unprotected telomeres in yeast is regulated by the CDK1 (Cdc28/Clb) cell-cycle kinase. Mol. Cell 24, 127-137 (2006).
5. Bertuch, A. A. & Lundblad, V. The Ku heterodimer performs separable activities at double-strand breaks and chromosome termini. Mol. Cell. Biol. 23, 8202-8215 (2003).
6. Negrini, S., Ribaud, V., Bianchi, A. & Shore, D. DNA breaks are masked by multiple Rap1 binding in yeast: Implications for telomere capping and telomerase regulation. Genes Dev. 21, 292-302 (2007).
7. Longhese, M. P. DNA damage response at functional and dysfunctional telomeres. Genes Dev. 22, 125-140 (2008).
8. Hug, N. & Lingner, J. Telomere length homeostasis. Chromosoma 115, 413-425 (2006).
9. Lundblad, V. & Szostak, J. W. A mutant with a defect in telomere elongation leads to senescence in yeast. Cell 57, 633-643 (1989).
10. Grandin, N., Bailly, A. & Charbonneau, M. Activation of Mrc1, a mediator of the replication checkpoint, by telomere erosion. Biol. Cell 97, 799-814 (2005).
11. d'Adda di Fagagna, F. et al. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426, 194-198 (2003).
12. Takai, H., Smogorzewska, A. & de Lange, T. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13, 1549-1556 (2003).
13. Bhattacharyya, M. K. & Lustig, A. J. Telomere dynamics in genome stability. Trends Biochem. Sci. 31, 114-122 (2006).
14. Le, S., Moore, J. K., Haber, J. E. & Greider, C. W. RAD50 and RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics 152, 143-152 (1999).
15. Krogh, B. & Symington, L. Recombination proteins in yeast. Annu. Rev. Genet. 38, 233-271 (2004).
16. Lisby, M., Barlow, J. H., Burgess, R. C. & Rothstein, R. Choreography of the DNA damage response; spatiotemporal relationships among checkpoint and repair proteins. Cell 118, 699-713 (2004).
17. Lisby, M., Mortensen, U. H. & Rothstein, R. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nature Cell Biol. 5, 572-577 (2003).
18. Marcand, S., Brevet, V. & Gilson, E. Progressive cis-inhibition of telomerase upon telomere elongation. EMBO J. 18, 3509-3519 (1999).
19. Gotta, M. et al. The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae. J. Cell Biol. 134, 1349-1363 (1996).
20. Polotnianka, R. M., Li, J. & Lustig, A. J. The yeast Ku heterodimer is essential for protection of the telomere against nucleolytic and recombinational activities. Curr. Biol. 8, 831-834 (1998).
21. Adams Martin, A., Dionne, I., Wellinger, R. J. & Holm, C. The function of DNA polymerase alpha at telomeric G tails is important for telomere homeostasis. Mol. Cell. Biol. 20, 786-796 (2000).
22. Doye, V., Wepf, R. & Hurt, E. C. A novel nuclear pore protein Nup133p with distinct roles in poly(A)+ RNA transport and nuclear pore distribution. EMBO J. 13, 6062-6075 (1994).
23. Nugent, C. I., Hughes, T. R., Lue, N. F. & Lundblad, V. Cdc13p: A single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274, 249-252 (1996).
24. Lin, J. J. & Zakian, V. A. The Saccharomyces CDC13 protein is a single-strand TG1-3 telomeric DNA-binding protein in vitro that affects telomere behavior in vivo. Proc. Natl. Acad. Sci. USA 93, 13760-13765 (1996).
25. Hackett, J. A. & Greider, C. W. End resection initiates genomic instability in the absence of telomerase. Mol. Cell. Biol. 23 8450-8461 (2003).
26. Chang, M., Arneric, M. & Lingner, J. Telomerase repeat addition processivity is increased at critically short telomeres in a Tel1-dependent manner in Saccharomyces cerevisiae. Genes Dev. 21, 2485-2494 (2007).
27. Nagai, S. et al. Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322 597-602 (2008).
28. Sherman, F., Fink, G. R. & Hicks, J. B. Methods in Yeast Genetics. (Cold Spring Harbor Laboratory, 1986).
29. Belli, G., Gari, E., Aldea, M. & Herrero, E. Functional analysis of yeast essential genes using a promoter-substitution cassette and the tetracycline-regulatable dual expression system. Yeast 14, 1127-1138 (1998).
30. Lisby, M., Rothstein, R. & Mortensen, U. H. Rad52 forms DNA repair and recombination centers during S phase. Proc. Natl. Acad. Sci. USA 98, 8276-8282 (2001).
31. Forstemann, K., Hoss, M. & Lingner, J. Telomerase-dependent repeat divergence at the 3′ ends of yeast telomeres. Nucl. Acids Res. 28, 2690-2694 (2000).