Two routes to senescence revealed by real-time analysis of telomerase-negative single lineages

Nature Communications

Volumn 6, Issue , 2015, Pages

  Xu, Zhou ^a,b   Fallet, Emilie ^a,b   Paoletti, Camille ^c   Fehrmann, Steffen ^c   Charvin, Gilles ^c   Teixeira, Maria Teresa ^a,b  

^a CNRS   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL ENZYME; RAD51 PROTEIN; TELOMERASE; DNA DIRECTED DNA POLYMERASE; POL32 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ASSAY; CELLS AND CELL COMPONENTS; CHROMOSOME; ENZYME ACTIVITY; EUKARYOTE; GENOMICS; IMAGING METHOD; INJURY; REAL TIME; SENESCENCE; YEAST;

ANALYTICAL EQUIPMENT; ARTICLE; CELL AGING; CELL CYCLE; CELL DIVISION; CELL FATE; CELL LINEAGE; CELL VIABILITY; CHROMOSOME DAMAGE; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; ENZYME INHIBITION; EUKARYOTE; MICROFLUIDIC DEVICE; NONHUMAN; SACCHAROMYCES CEREVISIAE; TELOMERE; TELOMERE HOMEOSTASIS; YEAST CELL; CELL CYCLE CHECKPOINT; DNA REPAIR; DNA STRAND BREAKAGE; FLUORESCENCE MICROSCOPY; GENETICS; LAB ON A CHIP; METABOLISM; PHASE CONTRAST MICROSCOPY; SOUTHERN BLOTTING; TELOMERE SHORTENING; TIME LAPSE IMAGING;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

BLOTTING, SOUTHERN; CELL CYCLE CHECKPOINTS; CELL DIVISION; CELL LINEAGE; DNA BREAKS; DNA REPAIR; DNA-DIRECTED DNA POLYMERASE; LAB-ON-A-CHIP DEVICES; MICROSCOPY, FLUORESCENCE; MICROSCOPY, PHASE-CONTRAST; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERASE; TELOMERE; TELOMERE SHORTENING; TIME-LAPSE IMAGING;

EID: 84937010972     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8680     Document Type: Article

References (50)

1. Hayflick, L. The limited in vitro lifetime of human diploid cell strains. Exp. Cell Res. 37, 614-636 (1965).
2. Harley, C. B., Futcher, A. B. & Greider, C. W. Telomeres shorten during ageing of human fibroblasts. Nature 345, 458-460 (1990).
3. d'Adda di Fagagna, F. et al. A DNA damage checkpoint response in telomereinitiated senescence. Nature 426, 194-198 (2003).
4. Campisi, J. & d'Adda di Fagagna, F. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 8, 729-740 (2007).
5. Lundblad, V. & Szostak, J. W. A mutant with a defect in telomere elongation leads to senescence in yeast. Cell 57, 633-643 (1989).
6. Teixeira, M. T. Saccharomyces cerevisiae as a model to study replicative senescence triggered by telomere shortening. Front. Oncol. 3, 101 (2013).
7. Lundblad, V. & Blackburn, E. H. An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell 73, 347-360 (1993).
8. Shay, J. W., Reddel, R. R. & Wright, W. E. Cancer. Cancer and telomeres-an ALTernative to telomerase. Science 336, 1388-1390 (2012).
9. Gunes, C. & Rudolph, K. L. The role of telomeres in stem cells and cancer. Cell 152, 390-393 (2013).
10. Xu, Z., Duc, K. D., Holcman, D. & Teixeira, M. T. The length of the shortest telomere as the major determinant of the onset of replicative senescence. Genetics 194, 847-857 (2013).
11. Abdallah, P. et al. A two-step model for senescence triggered by a single critically short telomere. Nat. Cell Biol. 11, 988-993 (2009).
12. Soudet, J., Jolivet, P. & Teixeira, M. T. Elucidation of the DNA end-replication problem in Saccharomyces cerevisiae. Mol. Cell 53, 954-964 (2014).
13. Smith, J. R. & Whitney, R. G. Intraclonal variation in proliferative potential of human diploid fibroblasts: stochastic mechanism for cellular aging. Science 207, 82-84 (1980).
14. Enomoto, S., Glowczewski, L. & Berman, J. MEC3, MEC1, and DDC2 are essential components of a telomere checkpoint pathway required for cell cycle arrest during senescence in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 2626-2638 (2002).
15. Ijpma, A. S. & Greider, C. W. Short telomeres induce a DNA damage response in Saccharomyces cerevisiae. Mol. Biol. Cell 14, 987-1001 (2003).
16. Fehrmann, S. et al. Aging yeast cells undergo a sharp entry into senescence unrelated to the loss of mitochondrial membrane potential. Cell Rep. 5, 1589-1599 (2013).
17. Mortimer, R. K. & Johnston, J. R. Life span of individual yeast cells. Nature 183, 1751-1752 (1959).
18. Voth, W. P., Olsen, A. E., Sbia, M., Freedman, K. H. & Stillman, D. J. ACE2, CBK1, and BUD4 in budding and cell separation. Eukaryot. Cell 4, 1018-1028 (2005).
19. Lebel, C. et al. Telomere maintenance and survival in Saccharomyces cerevisiae in the absence of telomerase and RAD52. Genetics 182, 671-684 (2009).
20. Low, K. C. & Tergaonkar, V. Telomerase: central regulator of all of the hallmarks of cancer. Trends Biochem. Sci. 38, 426-34 (2013).
21. Lingner, J. et al. Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276, 561-567 (1997).
22. Box, G. E. P., Jenkins, G. M. & Reinsel, G. C. Time Series Analysis: Forecasting and Control (Wiley, 2008).
23. Zhao, X., Muller, E. G. & Rothstein, R. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol. Cell 2, 329-340 (1998).
24. Toczyski, D. P., Galgoczy, D. J. & Hartwell, L. H. CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90, 1097-1106 (1997).
25. Fallet, E. et al. Length-dependent processing of telomeres in the absence of telomerase. Nucleic Acids Res. 42, 3648-3665 (2014).
26. 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).
27. Lendvay, T. S., Morris, D. K., Sah, J., Balasubramanian, B. & Lundblad, V. Senescence mutants of Saccharomyces cerevisiae with a defect in telomere replication identify three additional EST genes. Genetics 144, 1399-1412 (1996).
28. Meyer, D. H. & Bailis, A. M. Telomerase deficiency affects the formation of chromosomal translocations by homologous recombination in Saccharomyces cerevisiae. PLoS ONE 3, e3318 (2008).
29. Kolodner, R. D., Putnam, C. D. & Myung, K. Maintenance of genome stability in Saccharomyces cerevisiae. Science 297, 552-557 (2002).
30. Khadaroo, B. et al. The DNA damage response at eroded telomeres and tethering to the nuclear pore complex. Nat. Cell Biol. 11, 980-987 (2009).
31. 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).
32. Lydeard, J. R., Jain, S., Yamaguchi, M. & Haber, J. E. Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448, 820-823 (2007).
33. Hackett, J. A., Feldser, D. M. & Greider, C. W. Telomere dysfunction increases mutation rate and genomic instability. Cell 106, 275-286 (2001).
34. Hackett, J. A. & Greider, C. W. End resection initiates genomic instability in the absence of telomerase. Mol. Cell Biol. 23, 8450-8461 (2003).
35. Churikov, D., Charifi, F., Simon, M. N. & Geli, V. Rad59-facilitated acquisition of y' elements by short telomeres delays the onset of senescence. PLoS Genet. 10, e1004736 (2014).
36. Sandell, L. L. & Zakian, V. A. Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell 75, 729-739 (1993).
37. Larrivee, M. & Wellinger, R. J. Telomerase- and capping-independent yeast survivors with alternate telomere states. Nat. Cell Biol. 8, 741-747 (2006).
38. Payen, C., Koszul, R., Dujon, B. & Fischer, G. Segmental duplications arise from Pol32-dependent repair of broken forks through two alternative replication-based mechanisms. PLoS Genet. 4, e1000175 (2008).
39. Vasan, S., Deem, A., Ramakrishnan, S., Argueso, J. L. & Malkova, A. Cascades of genetic instability resulting from compromised break-induced replication. PLoS Genet. 10, e1004119 (2014).
40. Costantino, L. et al. Break-induced replication repair of damaged forks induces genomic duplications in human cells. Science 343, 88-91 (2014).
41. Branzei, D. & Foiani, M. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 11, 208-219 (2010).
42. Gonzalez-Prieto, R., Munoz-Cabello, A. M., Cabello-Lobato, M. J. & Prado, F. Rad51 replication fork recruitment is required for DNA damage tolerance. EMBO J. 32, 1307-1321 (2013).
43. Ivessa, A. S., Zhou, J. Q., Schulz, V. P., Monson, E. K. & Zakian, V. A. Saccharomyces Rrm3p, a 5' to 3' DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 16, 1383-1396 (2002).
44. Lee, J. Y., Kozak, M., Martin, J. D., Pennock, E. & Johnson, F. B. Evidence that RecQ helicase slows senescence by resolving recombining telomeres. PLoS Biol. 5, 1334-1344 (2007).
45. Gao, H., Moss, D. L., Parke, C., Tatum, D. & Lustig, A. J. The Ctf18RFC clamp loader is essential for telomere stability in telomerase-negative and mre11 mutant alleles. PLoS ONE 9, e88633 (2014).
46. Makovets, S., Herskowitz, I. & Blackburn, E. H. Anatomy and dynamics of DNA replication fork movement in yeast telomeric regions. Mol. Cell Biol. 24, 4019-4031 (2004).
47. Deem, A. et al. Break-induced replication is highly inaccurate. PLoS Biol. 9, e1000594 (2011).
48. Huang, M. E., Rio, A. G., Galibert, M. D. & Galibert, F. Pol32, a subunit of Saccharomyces cerevisiae DNA polymerase delta, suppresses genomic deletions and is involved in the mutagenic bypass pathway. Genetics 160, 1409-1422 (2002).
49. Smith, C. E., Lam, A. F. & Symington, L. S. Aberrant double-strand break repair resulting in half crossovers in mutants defective for Rad51 or the DNA polymerase {delta} complex. Mol. Cell Biol. 29, 1432-41 (2009).
50. Romano, G. H. et al. Environmental stresses disrupt telomere length homeostasis. PLoS Genet. 9, e1003721 (2013).