Mrc1 protects uncapped budding yeast telomeres from exonuclease EXO1

DNA Repair

Volumn 6, Issue 11, 2007, Pages 1607-1617

  Tsolou, Avgi ^a   Lydall, David ^a  

^a WELLCOME RESEARCH LABORATORIES   (United Kingdom)

Author keywords

CDC13; EXO1; Mrc1; ssDNA; Telomere; YKU70

Indexed keywords

CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; DOUBLE STRANDED DNA; EXONUCLEASE; EXONUCLEASE 1; MEDIATOR OF REPLICATION CHECKPOINT 1; PROTEIN RAD9; RIBONUCLEOTIDE REDUCTASE; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; SOUTHERN BLOTTING; TELOMERE; WESTERN BLOTTING; YEAST CELL;

CELL CYCLE; CELL CYCLE PROTEINS; CYCLIN B; DNA, SINGLE-STRANDED; EXODEOXYRIBONUCLEASES; FUNGAL PROTEINS; MUTATION; SACCHAROMYCETALES; TELOMERE;

SACCHAROMYCETALES;

EID: 35349012676     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2007.05.010     Document Type: Article

References (59)

1. de Lange T. Protection of mammalian telomeres. Oncogene 21 (2002) 532-540
2. Blackburn E.H. Switching and signaling at the telomere. Cell 106 (2001) 661-673
3. d'Adda di Fagagna F., Teo S.H., and Jackson S.P. Functional links between telomeres and proteins of the DNA-damage response. Genes Dev. 18 (2004) 1781-1799
4. Lydall D. Hiding at the ends of yeast chromosomes: telomeres, nucleases and checkpoint pathways. J. Cell Sci. 116 (2003) 4057-4065
5. Cooper J.P. Telomere transitions in yeast: the end of the chromosome as we know it. Curr. Opin. Genet. Dev. 10 (2000) 169-177
6. Grandin N., Damon C., and Charbonneau M. Ten1 functions in telomere end protection and length regulation in association with Stn1 and Cdc13. EMBO J. 20 (2001) 1173-1183
7. Grandin N., Reed S.I., and Charbonneau M. Stn1, a new Saccharomyces cerevisiae protein, is implicated in telomere size regulation in association with Cdc13. Genes Dev. 11 (1997) 512-527
8. Pennock E., Buckley K., and Lundblad V. Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 104 (2001) 387-396
9. Larrivee M., and Wellinger R.J. Telomerase- and capping-independent yeast survivors with alternate telomere states. Nat. Cell Biol. 8 (2006) 741-747
10. Petreaca R.C., Chiu H.C., Eckelhoefer H.A., Chuang C., Xu L., and Nugent C.I. Chromosome end protection plasticity revealed by Stn1p and Ten1p bypass of Cdc13p. Nat. Cell Biol. 8 (2006) 748-755
11. Zubko M.K., and Lydall D. Linear chromosome maintenance in the absence of essential telomere-capping proteins. Nat. Cell Biol. 8 (2006) 734-740
12. Garvik B., Carson M., and Hartwell L. Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol. Cell Biol. 15 (1995) 6128-6138
13. Lydall D., and Weinert T. Yeast checkpoint genes in DNA damage processing: implications for repair and arrest. Science 270 (1995) 1488-1491
14. Polotnianka R.M., Li J., and Lustig A.J. The yeast Ku heterodimer is essential for protection of the telomere against nucleolytic and recombinational activities. Curr. Biol. 8 (1998) 831-834
15. Verdun R.E., and Karlseder J. The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 127 (2006) 709-720
16. Nyberg K.A., Michelson R.J., Putnam C.W., and Weinert T.A. Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36 (2002) 617-656
17. Alcasabas A.A., Osborn A.J., Bachant J., Hu F., Werler P.J., Bousset K., Furuya K., Diffley J.F., Carr A.M., and Elledge S.J. Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat. Cell Biol. 3 (2001) 958-965
18. Osborn A.J., and Elledge S.J. Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev. 17 (2003) 1755-1767
19. Calzada A., Hodgson B., Kanemaki M., Bueno A., and Labib K. Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication fork. Genes Dev. 19 (2005) 1905-1919
20. Szyjka S.J., Viggiani C.J., and Aparicio O.M. Mrc1 is required for normal progression of replication forks throughout chromatin in S. cerevisiae. Mol. Cell 19 (2005) 691-697
21. Tourriere H., Versini G., Cordon-Preciado V., Alabert C., and Pasero P. Mrc1 and Tof1 promote replication fork progression and recovery independently of Rad53. Mol. Cell 19 (2005) 699-706
22. Katou Y., Kanoh Y., Bando M., Noguchi H., Tanaka H., Ashikari T., Sugimoto K., and Shirahige K. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424 (2003) 1078-1083
23. Grandin N., Bailly A., and Charbonneau M. Activation of Mrc1, a mediator of the replication checkpoint, by telomere erosion. Biol. Cell 97 (2005) 799-814
24. Tong A.H., Evangelista M., Parsons A.B., Xu H., Bader G.D., Page N., Robinson M., Raghibizadeh S., Hogue C.W., Bussey H., Andrews B., Tyers M., and Boone C. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294 (2001) 2364-2368
25. Downey M., Houlsworth R., Maringele L., Rollie A., Brehme M., Galicia S., Guillard S., Partington M., Zubko M.K., Krogan N.J., Emili A., Greenblatt J.F., Harrington L., Lydall D., and Durocher D. A genome-wide screen identifies the evolutionarily conserved KEOPS complex as a telomere regulator. Cell 124 (2006) 1155-1168
26. Adams A., Gottshcling D.E., Kaiser C.A., and Stearns T. Methods in Yeast Genetics (1997), Cold Spring Harbor Laboratory Press, New York
27. Longtine M.S., McKenzie III A., Demarini D.J., Shah N.G., Wach A., Brachat A., Philippsen P., and Pringle J.R. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 (1998) 953-961
28. Gietz R.D., Schiestl R.H., Willems A.R., and Woods R.A. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11 (1995) 355-360
29. Chen D.C., Yang B.C., and Kuo T.T. One-step transformation of yeast in stationary phase. Curr. Genet. 21 (1992) 83-84
30. Foiani M., Liberi G., Piatti S., and Plevani P. Saccharomyces cerevisiae as a model system to study DNA replication. Eukaryotic DNA Replication: A Practical Approach (1999), Oxford University Press, Oxford pp. 185-200
31. Blankley R., and Lydall D. A domain of Rad9 specifically required for activation of Chk1 in budding yeast. J. Cell Sci. 117 (2004) 601-608
32. Sweeney F.D., Yang F., Chi A., Shabanowitz J., Hunt D.F., and Durocher D. Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Curr. Biol. 15 (2005) 1364-1375
33. Woods A., Sherwin T., Sasse R., MacRae T.H., Baines A.J., and Gull K. Definition of individual components within the cytoskeleton of Trypanosoma brucei by a library of monoclonal antibodies. J. Cell Sci. 93 Pt 3 (1989) 491-500
34. Tsubouchi H., and Ogawa H. Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol. Biol. Cell 11 (2000) 2221-2233
35. Zubko M.K., Maringele L., Foster S.S., and Lydall D. Detecting repair intermediates in vivo: effects of DNA damage response genes on single-stranded DNA accumulation at uncapped telomeres in budding yeast. Methods Enzymol. 409 (2006) 285-300
36. Maringele L., and Lydall D. EXO1-dependent single-stranded DNA at telomeres activates subsets of DNA damage and spindle checkpoint pathways in budding yeast yku70Δ mutants. Genes Dev. 16 (2002) 1919-1933
37. Booth C., Griffith E., Brady G., and Lydall D. Quantitative amplification of single-stranded DNA (QAOS) demonstrates that cdc13-1 mutants generate ssDNA in a telomere to centromere direction. Nucl. Acids Res. 29 (2001) 4414-4422
38. Nugent C.I., Hughes T.R., Lue N.F., and Lundblad V. Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274 (1996) 249-252
39. Zubko M.K., Guillard S., and Lydall D. Exo1 and Rad24 differentially regulate generation of ssDNA at telomeres of Saccharomyces cerevisiae cdc13-1 mutants. Genetics 168 (2004) 103-115
40. Jia X., Weinert T., and Lydall D. Mec1 and Rad53 inhibit formation of single-stranded DNA at telomeres of Saccharomyces cerevisiae cdc13-1 mutants. Genetics 166 (2004) 753-764
41. Weinert T.A., Kiser G.L., and Hartwell L.H. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev. 8 (1994) 652-665
42. Foster S.S., Zubko M.K., Guillard S., and Lydall D. MRX protects telomeric DNA at uncapped telomeres of budding yeast cdc13-1 mutants. DNA Repair (Amst.) 5 (2006) 840-851
43. Fisher T.S., and Zakian V.A. Ku: a multifunctional protein involved in telomere maintenance. DNA Repair (Amst.) 4 (2005) 1215-1226
44. Mohanty B.K., Bairwa N.K., and Bastia D. The Tof1p-Csm3p protein complex counteracts the Rrm3p helicase to control replication termination of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 897-902
45. Gardner R., Putnam C.W., and Weinert T. RAD53, DUN1 and PDS1 define two parallel G(2)/M checkpoint pathways in budding yeast. EMBO J. 18 (1999) 3173-3185
46. Sanchez Y., Bachant J., Wang H., Hu F., Liu D., Tetzlaff M., and Elledge S.J. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 286 (1999) 1166-1171
47. Chabes A., Domkin V., and Thelander L. Yeast Sml1, a protein inhibitor of ribonucleotide reductase. J. Biol. Chem. 274 (1999) 36679-36683
48. Zhao X., Muller E.G., and Rothstein R. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol. Cell 2 (1998) 329-340
49. Adams A.K., and Holm C. Specific DNA replication mutations affect telomere length in Saccharomyces cerevisiae. Mol. Cell Biol. 16 (1996) 4614-4620
50. Adams Martin A., Dionne I., Wellinger R.J., and Holm C. The function of DNA polymerase alpha at telomeric G tails is important for telomere homeostasis. Mol. Cell Biol. 20 (2000) 786-796
51. Carson M.J., and Hartwell L. CDC17: an essential gene that prevents telomere elongation in yeast. Cell 42 (1985) 249-257
52. Grossi S., Puglisi A., Dmitriev P.V., Lopes M., and Shore D. Pol12, the B subunit of DNA polymerase alpha, functions in both telomere capping and length regulation. Genes Dev. 18 (2004) 992-1006
53. Grandin N., and Charbonneau M. Mrc1, a non-essential DNA replication protein, is required for telomere end protection following loss of capping by Cdc13, Yku or telomerase. Mol. Genet. Genomics 277 (2007) 685-699
54. Maringele L., and Lydall D. EXO1 plays a role in generating type I and type II survivors in budding yeast. Genetics 166 (2004) 1641-1649
55. DuBois M.L., Haimberger Z.W., McIntosh M.W., and Gottschling D.E. A quantitative assay for telomere protection in saccharomyces cerevisiae. Genetics 161 (2002) 995-1013
56. Makovets S., Herskowitz I., and Blackburn E.H. Anatomy and dynamics of DNA replication fork movement in yeast telomeric regions. Mol. Cell Biol. 24 (2004) 4019-4031
57. Miller K.M., Rog O., and Cooper J.P. Semi-conservative DNA replication through telomeres requires Taz1. Nature 440 (2006) 824-828
58. Cotta-Ramusino C., Fachinetti D., Lucca C., Doksani Y., Lopes M., Sogo J., and Foiani M. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell 17 (2005) 153-159
59. Vodenicharov M.D., and Wellinger R.J. DNA degradation at unprotected telomeres in yeast is regulated by the CDK1 (Cdc28/Clb) cell-cycle kinase. Mol. Cell 24 (2006) 127-137