Abrupt telomere losses and reduced end-resection can explain accelerated senescence of Smc5/6 mutants lacking telomerase

DNA Repair

Volumn 10, Issue 3, 2011, Pages 271-282

  Noël, Jean François ^a   Wellinger, Raymund J ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

G tail; Replication; Senescence; Smc5; Smc6; Telomere

Indexed keywords

CHROMOSOME PROTEIN; PROTEIN STRUCTURAL MAINTENANCE OF CHROMOSOME 5; PROTEIN STRUCTURAL MAINTENANCE OF CHROMOSOME 6; SINGLE STRANDED DNA; TELOMERASE; UNCLASSIFIED DRUG;

ARTICLE; CELL DIVISION; CELL MUTANT; CELL SURVIVAL; CHROMOSOME STRUCTURE; DNA REPAIR; DNA REPLICATION; GENE MUTATION; GENETIC CODE; GROWTH DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SENESCENCE; TELOMERE; YEAST;

CELL CYCLE PROTEINS; CELL PROLIFERATION; CHROMOSOME BREAKAGE; DNA REPLICATION; DNA, FUNGAL; DNA-BINDING PROTEINS; MUTATION; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUMO-1 PROTEIN; TELOMERASE; TELOMERE; TELOMERE-BINDING PROTEINS;

SACCHAROMYCETALES;

EID: 79951851419     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2010.11.010     Document Type: Article

References (76)

1. Nasmyth K., Haering C.H. The structure and function of SMC and kleisin complexes. Annu. Rev. Biochem. 2005, 74:595-648.
2. Losada A., Hirano T. Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev. 2005, 19:1269-1287.
3. Haering C.H., Lowe J., Hochwagen A., Nasmyth K. Molecular architecture of SMC proteins and the yeast cohesin complex. Mol. Cell 2002, 9:773-788.
4. Cobbe N., Heck M.M. The evolution of SMC proteins: phylogenetic analysis and structural implications. Mol. Biol. Evol. 2004, 21:332-347.
5. Losada A. The regulation of sister chromatid cohesion. Biochim. Biophys. Acta 2008, 1786:41-48.
6. Onn I., Heidinger-Pauli J.M., Guacci V., Unal E., Koshland D.E. Sister chromatid cohesion: a simple concept with a complex reality. Annu. Rev. Cell Dev. Biol. 2008, 24:105-129.
7. Nasmyth K., Haering C.H. Cohesin: its roles and mechanisms. Annu. Rev. Genet. 2009, 43:525-558.
8. Hirano T. Condensins: organizing and segregating the genome. Curr. Biol. 2005, 15:R265-275.
9. Hudson D.F., Marshall K.M., Earnshaw W.C., Condensin Architect of mitotic chromosomes. Chromosome Res. 2009, 17:131-144.
10. De Piccoli G., Torres-Rosell J., Aragon L. The unnamed complex: what do we know about Smc5-Smc6?. Chromosome Res. 2009, 17:251-263.
11. Nasim A., Smith B.P. Genetic control of radiation sensitivity in Schizosaccharomyces pombe. Genetics 1975, 79:573-582.
12. Prakash L., Prakash S. Isolation and characterization of MMS-sensitive mutants of Saccharomyces cerevisiae. Genetics 1977, 86:33-55.
13. Lehmann A.R., Walicka M., Griffiths D.J., Murray J.M., Watts F.Z., McCready S., Carr A.M. The rad18 gene of Schizosaccharomyces pombe defines a new subgroup of the SMC superfamily involved in DNA repair. Mol. Cell. Biol. 1995, 15:7067-7080.
14. Hazbun T.R., Malmstrom L., Anderson S., Graczyk B.J., Fox B., Riffle M., Sundin B.A., Aranda J.D., McDonald W.H., Chiu C.H., Snydsman B.E., Bradley P., Muller E.G., Fields S., Baker D., Yates J.R., Davis T.N. Assigning function to yeast proteins by integration of technologies. Mol. Cell 2003, 12:1353-1365.
15. Sergeant J., Taylor E., Palecek J., Fousteri M., Andrews E.A., Sweeney S., Shinagawa H., Watts F.Z., Lehmann A.R. Composition and architecture of the Schizosaccharomyces pombe Rad18 (Smc5-6) complex. Mol. Cell. Biol. 2005, 25:172-184.
16. Taylor E.M., Copsey A.C., Hudson J.J., Vidot S., Lehmann A.R. Identification of the proteins, including MAGEG1, that make up the human SMC5-6 protein complex. Mol. Cell. Biol. 2008, 28:1197-1206.
17. Pebernard S., Wohlschlegel J., McDonald W.H., Yates J.R., Boddy M.N. The Nse5-Nse6 dimer mediates DNA repair roles of the Smc5-Smc6 complex. Mol. Cell. Biol. 2006, 26:1617-1630.
18. Hu B., Liao C., Millson S.H., Mollapour M., Prodromou C., Pearl L.H., Piper P.W., Panaretou B. Qri2/Nse4, a component of the essential Smc5/6 DNA repair complex. Mol. Microbiol. 2005, 55:1735-1750.
19. Zhao X., Blobel G. A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:4777-4782.
20. Andrews E.A., Palecek J., Sergeant J., Taylor E., Lehmann A.R., Watts F.Z., Nse2 a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage. Mol. Cell. Biol. 2005, 25:185-196.
21. Potts P.R., Yu H. Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol. Cell. Biol. 2005, 25:7021-7032.
22. Potts P.R., Yu H. The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat. Struct. Mol. Biol. 2007, 14:581-590.
23. Pebernard S., Schaffer L., Campbell D., Head S.R., Boddy M.N. Localization of Smc5/6 to centromeres and telomeres requires heterochromatin and SUMO, respectively. EMBO J. 2008, 27:3011-3023.
24. Grandin N., Charbonneau M. Protection against chromosome degradation at the telomeres. Biochimie 2008, 90:41-59.
25. Palm W., de Lange T. How shelterin protects mammalian telomeres. Annu. Rev. Genet. 2008, 42:301-334.
26. Autexier C., Lue N.F. The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem. 2006, 75:493-517.
27. Gilson E., Geli V. How telomeres are replicated. Nat. Rev. Mol. Cell. Biol. 2007, 8:825-838.
28. Bryan T.M., Englezou A., Gupta J., Bacchetti S., Reddel R.R. Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J. 1995, 14:4240-4248.
29. Dunham M.A., Neumann A.A., Fasching C.L., Reddel R.R. Telomere maintenance by recombination in human cells. Nat. Genet. 2000, 26:447-450.
30. Bailey S.M., Brenneman M.A., Goodwin E.H. Frequent recombination in telomeric DNA may extend the proliferative life of telomerase-negative cells. Nucleic Acids Res. 2004, 32:3743-3751.
31. Cesare A.J., Reddel R.R. Alternative lengthening of telomeres: models, mechanisms and implications. Nat. Rev. Genet. 2010, 11:319-330.
32. Yeager T.R., Neumann A.A., Englezou A., Huschtscha L.I., Noble J.R., Reddel R.R. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 1999, 59:4175-4179.
33. Onoda F., Takeda M., Seki M., Maeda D., Tajima J., Ui A., Yagi H., Enomoto T. SMC6 is required for MMS-induced interchromosomal and sister chromatid recombinations in Saccharomyces cerevisiae. DNA Repair (Amst) 2004, 3:429-439.
34. Cost G.J., Cozzarelli N.R. Smc5p promotes faithful chromosome transmission and DNA repair in Saccharomyces cerevisiae. Genetics 2006, 172:2185-2200.
35. Torres-Rosell J., De Piccoli G., Cordon-Preciado V., Farmer S., Jarmuz A., Machin F., Pasero P., Lisby M., Haber J.E., Aragon L. Anaphase onset before complete DNA replication with intact checkpoint responses. Science 2007, 315:1411-1415.
36. De Piccoli G., Cortes-Ledesma F., Ira G., Torres-Rosell J., Uhle S., Farmer S., Hwang J.Y., Machin F., Ceschia A., McAleenan A., Cordon-Preciado V., Clemente-Blanco A., Vilella-Mitjana F., Ullal P., Jarmuz A., Leitao B., Bressan D., Dotiwala F., Papusha A., Zhao X., Myung K., Haber J.E., Aguilera A., Aragon L. Smc5-Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination. Nat. Cell Biol. 2006, 8:1032-1034.
37. Lindroos H.B., Strom L., Itoh T., Katou Y., Shirahige K., Sjogren C. Chromosomal association of the Smc5/6 complex reveals that it functions in differently regulated pathways. Mol. Cell 2006, 22:755-767.
38. Branzei D., Sollier J., Liberi G., Zhao X., Maeda D., Seki M., Enomoto T., Ohta K., Foiani M. Ubc9- and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 2006, 127:509-522.
39. Ampatzidou E., Irmisch A., O'Connell M.J., Murray J.M. Smc5/6 is required for repair at collapsed replication forks. Mol. Cell. Biol. 2006, 26:9387-9401.
40. Irmisch A., Ampatzidou E., Mizuno K., O'Connell M.J., Murray J.M. Smc5/6 maintains stalled replication forks in a recombination-competent conformation. EMBO J. 2009, 28:144-155.
41. Sollier J., Driscoll R., Castellucci F., Foiani M., Jackson S.P., Branzei D. The Saccharomyces cerevisiae Esc2 and Smc5-6 proteins promote sister chromatid junction-mediated intra-S repair. Mol. Biol. Cell 2009, 20:1671-1682.
42. Chavez A., George V., Agrawal V., Johnson F.B. Sumoylation and the structural maintenance of chromosomes (Smc) 5/6 complex slow senescence through recombination intermediate resolution. J. Biol. Chem. 2010, 285:11922-11930.
43. Bermudez-Lopez M., Ceschia A., de Piccoli G., Colomina N., Pasero P., Aragon L., Torres-Rosell J. The Smc5/6 complex is required for dissolution of DNA-mediated sister chromatid linkages. Nucleic Acids Res. 2010.
44. Torres-Rosell J., Machin F., Farmer S., Jarmuz A., Eydmann T., Dalgaard J.Z., Aragon L. SMC5, SMC6 genes are required for the segregation of repetitive chromosome regions. Nat. Cell Biol. 2005, 7:412-419.
45. Beeler T., Gable K., Zhao C., Dunn T. A novel protein, CSG2p, is required for Ca2+ regulation in Saccharomyces cerevisiae. J. Biol. Chem. 1994, 269:7279-7284.
46. Johnson F.B., Marciniak R.A., McVey M., Stewart S.A., Hahn W.C., Guarente L. The Saccharomyces cerevisiae WRN homolog Sgs1p participates in telomere maintenance in cells lacking telomerase. EMBO J. 2001, 20:905-913.
47. Wellinger R.J., Wolf A.J., Zakian V.A. Saccharomyces telomeres acquire single-strand TG1-3 tails late in S phase. Cell 1993, 72:51-60.
48. Louis E.J., Haber J.E. The structure and evolution of subtelomeric Y' repeats in Saccharomyces cerevisiae. Genetics 1992, 131:559-574.
49. Lundblad V., Blackburn E.H. An alternative pathway for yeast telomere maintenance rescues est1-senescence. Cell 1993, 73:347-360.
50. Teng S.C., Zakian V.A. Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol. Cell. Biol. 1999, 19:8083-8093.
51. Forstemann K., Hoss M., Lingner J. Telomerase-dependent repeat divergence at the 3' ends of yeast telomeres. Nucleic Acids Res. 2000, 28:2690-2694.
52. Lee J.Y., Kozak M., Martin J.D., Pennock E., Johnson F.B. Evidence that a RecQ helicase slows senescence by resolving recombining telomeres. PLoS Biol. 2007, 5:e160.
53. Dionne I., Wellinger R.J. Cell cycle-regulated generation of single-stranded G-rich DNA in the absence of telomerase. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:13902-13907.
54. Lundblad V., Szostak J.W. A mutant with a defect in telomere elongation leads to senescence in yeast. Cell 1989, 57:633-643.
55. Singer M.S., Gottschling D.E. TLC1: template RNA component of Saccharomyces cerevisiae telomerase. Science 1994, 266:404-409.
56. Le S., Moore J.K., Haber J.E., Greider C.W., RAD50 RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics 1999, 152:143-152.
57. Paques F., Haber J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 1999, 63:349-404.
58. Wang S.S., Zakian V.A. Sequencing of Saccharomyces telomeres cloned using T4 DNA polymerase reveals two domains. Mol. Cell. Biol. 1990, 10:4415-4419.
59. Teixeira M.T., Arneric M., Sperisen P., Lingner J. Telomere length homeostasis is achieved via a switch between telomerase- extendible and -nonextendible states. Cell 2004, 117:323-335.
60. 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. 2007, 21:2485-2494.
61. Fisher T.S., Zakian V.A. Ku: a multifunctional protein involved in telomere maintenance. DNA Repair (Amst) 2005, 4:1215-1226.
62. Daley J.M., Palmbos P.L., Wu D., Wilson T.E. Nonhomologous end joining in yeast. Annu. Rev. Genet. 2005, 39:431-451.
63. Grandin N., Damon C., Charbonneau M. Ten1 functions in telomere end protection and length regulation in association with Stn1 and Cdc13. EMBO J. 2001, 20:1173-1183.
64. Grandin N., Reed S.I., Charbonneau M., Stn1 a new Saccharomyces cerevisiae protein, is implicated in telomere size regulation in association with Cdc13. Genes Dev. 1997, 11:512-527.
65. Garvik B., Carson M., Hartwell L., Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol. Cell. Biol. 1995, 15:6128-6138.
66. 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 1996, 274:249-252.
67. Lydall D., Weinert T. Yeast checkpoint genes in DNA damage processing: implications for repair and arrest. Science 1995, 270:1488-1491.
68. Gravel S., Larrivee M., Labrecque P., Wellinger R.J., Yeast Ku as a regulator of chromosomal DNA end structure. Science 1998, 280:741-744.
69. 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. 1998, 8:831-834.
70. Teo S.H., Jackson S.P. Telomerase subunit overexpression suppresses telomere-specific checkpoint activation in the yeast yku80 mutant. EMBO Rep. 2001, 2:197-202.
71. Raghuraman M.K., Brewer B.J., Fangman W.L. Cell cycle-dependent establishment of a late replication program. Science 1997, 276:806-809.
72. Abdallah P., Luciano P., Runge K.W., Lisby M., Geli V., Gilson E., Teixeira M.T. A two-step model for senescence triggered by a single critically short telomere. Nat. Cell Biol. 2009, 11:988-993.
73. Khadaroo B., Teixeira M.T., Luciano P., Eckert-Boulet N., Germann S.M., Simon M.N., Gallina I., Abdallah P., Gilson E., Geli V., Lisby M. The DNA damage response at eroded telomeres and tethering to the nuclear pore complex. Nat. Cell Biol. 2009, 11:980-987.
74. Hwang J.Y., Smith S., Ceschia A., Torres-Rosell J., Aragon L., Myung K. Smc5-Smc6 complex suppresses gross chromosomal rearrangements mediated by break-induced replications. DNA Repair (Amst) 2008, 7:1426-1436.
75. Potts P.R., Porteus M.H., Yu H. Human SMC5/6 complex promotes sister chromatid homologous recombination by recruiting the SMC1/3 cohesin complex to double-strand breaks. EMBO J. 2006, 25:3377-3388.
76. Gartenberg M.R. Life on the edge: telomeres and persistent DNA breaks converge at the nuclear periphery. Genes Dev. 2009, 23:1027-1031.