Exo1 and Rad24 differentially regulate generation of ssDNA at telomeres of Saccharomyces cerevisiae cdc13-1 mutants

Genetics

Volumn 168, Issue 1, 2004, Pages 103-115

  Zubko, Mikhajlo K ^a   Guillard, Sandrine ^b   Lydall, David ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; MRE11 PROTEIN; NUCLEASE; PROTEIN DIN7; PROTEIN EXO1; PROTEIN MSH2; PROTEIN NUC1; PROTEIN RAD2; PROTEIN RAD24; PROTEIN RAD27; PROTEIN RAD9; PROTEIN XRS2; PROTEIN YEN1; RAD50 PROTEIN; RAD52 PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; COMPARATIVE STUDY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; ENZYME REGULATION; FUNGAL STRAIN; FUNGUS GROWTH; FUNGUS MUTANT; GENE CONTROL; GENE DELETION; GROWTH INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; TELOMERE; TEMPERATURE; TEMPERATURE SENSITIVE MUTANT;

CELL CYCLE; CELL CYCLE PROTEINS; COLONY COUNT, MICROBIAL; DNA PRIMERS; DNA REPAIR; DNA, SINGLE-STRANDED; EXODEOXYRIBONUCLEASES; GENES, CDC; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, GENETIC; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERE; TELOMERE-BINDING PROTEINS; TEMPERATURE;

FUNGI; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 5144219712     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.104.027904     Document Type: Article

References (72)

1. ADAMS, A., D. E. GOTTSHCLING, C. A. KAISER and T. STEARNS, 1997 Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. AQUILINA, G., M. CRESCENZI and M. BIGNAMI, 1999 Mismatch repair, G(2)/M cell cycle arrest and lethality after DNA damage. Carcinogenesis 20: 2317-2326.
3. BESSHO, T., and A. SANCAR, 2000 Human DNA damage checkpoint protein hRAD9 is a 3′ to 5′ exonuclease. J. Biol. Chem. 275: 7451-7454.
4. BLACKBURN, E. H., 2001 Switching and signaling at the telomere. Cell 106: 661-673.
5. BOOTH, C., E. GRIFFITH, G. BRADY and D. LYDALL, 2001 Quantitative amplification of single-stranded DNA (QAOS) demonstrates that cdc13-1 mutants generate ssDNA in a telomere to centromere direction. Nucleic Acids Res. 29: 4414-4422.
6. CERVANTES, R. B., and V. LUNDBLAD, 2002 Mechanisms of chromosome-end protection, Curr. Opin. Cell Biol. 14: 351-356.
7. DAVIS, T. W., C. WILSON-VAN PATTEN, M. MEYERS, K. A. KUNUGI, S. CUTHILL et al., 1998 Defective expression of the DNA mismatch repair protein, MLH1, alters G2-M cell cycle checkpoint arrest following ionizing radiation. Cancer Res. 58: 767-778.
8. DIEDE, S. J., and D. E. GOTTSCHLING, 2001 Exonuclease activity is required for sequence addition and Cdc13p loading at a de novo telomere. Curr. Biol. 11: 1336-1340.
9. ELLISON, V., and B. STILLMAN, 2003 Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5′ recessed DNA. PLoS Biol. 1: E33.
10. FAN, H. Y., K. K. CHENG and H. L. KLEIN, 1996 Mutations in the RNA polymerase II transcription machinery suppress the hyper-recombination mutant hpr1 delta of Saccharomyces cerevisiae. Genetics 142: 749-759.
11. FERREIRA, M. G., K. M. MILLER and J. P. COOPER, 2004 Indecent exposure: when telomeres become uncapped. Mol. Cell 13: 7-18.
12. FIORENTINI, P., K. N. HUANG, D. X. TISHKOFF, R. D. KOLODNER and L. S. SYMINGTON, 1997 Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol. Cell. Biol. 17: 2764-2773.
13. FREIRE, R., J. R. MURGUIA, M. TARSOUNAS, N. F. LOWNDES, P. B. MOENS et al., 1998 Human and mouse homologs of Schizosaccharomyces pombe rad1(+) and Saccharomyces cerevisiae RAD17: linkage to checkpoint control and mammalian meiosis. Genes Dev. 12: 2560-2573.
14. GARVIK, B., M. CARSON and L. HARTWELL, 1995 Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint Mol. Cell. Biol. 15: 6128-6138.
15. GILBERT, C. S., C. M. GREEN and N. F. LOWNDES, 2001 Budding yeast Rad9 is an ATP-dependent Rad53 activating machine. Mol. Cell 8: 129-136.
16. GRANDIN, N., C. DAMON and M. CHARBONNEAU, 2001 Cdc13 prevents telomere uncapping and Rad50-dependent homologous recombination. EMBO J. 20: 6127-6139.
17. GREEN, C. M., H. ERDJUMENT-BROMAGE, P. TEMPST and N. F. LOWNDES, 2000 A novel Rad24 checkpoint protein complex closely related to replication factor C. Curr. Biol. 10: 39-42.
18. HARRINGTON, L., 2004 Those dam-aged telomeres! Curr. Opin. Genet. Dev. 14: 22-28.
19. HARTWELL, L. H., and T. A. WEINERT, 1989 Checkpoints: controls that ensure the order of cell cycle events. Science 246: 629-634.
20. HOROWITZ, H., P. THORBURN and J. E. HABER, 1984 Rearrangements of highly polymorphic regions near telomeres of Saccharomyces cerevisiae. Mol. Cell. Biol. 4: 2509-2517.
21. HUANG, L. C., K. C. CLARKIN and G. M. WAHL, 1996 Sensitivity and selectivity of the DNA damage sensor responsible for activating p53-dependent G1 arrest. Proc. Natl. Acad. Sci. USA 93: 4827-4832.
22. JIA, X., T. WEINERT and D. LYDALL, 2004 Mec1 and Rad53 inhibit formation of single-stranded DNA at telomeres of Saccharomyces cerevisiae cdc13-1 mutants. Genetics 166: 753-764.
23. JOHNSON, R. E., G. K. KOVVALI, L. PRAKASH and S. PRAKASH, 1998 Role of yeast Rth1 nuclease and its homologs in mutation avoidance, DNA repair, and DNA replication. Curr. Genet. 34: 21-29.
24. KHAZANEHDARI, K. A., and R. H. BORTS, 2000 EXO1 and MSH4 differentially affect crossing-over and segregation. Chromosoma 109: 94-102.
25. KIRKPATRICK, D. T., J. R. FERGUSON, T. D. PETES and L. S. SYMINGTON, 2000 Decreased meiotic intergenic recombination and increased meiosis I nondisjunction in exo1 mutants of Saccharomyces cerevisiae. Genetics 156: 1549-1557.
26. KONDO, T., T. WAKAYAMA, T. NAIKI, K. MATSUMOTO and K. SUGIMOTO, 2001 Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science 294: 867-870.
27. LEE, B. I., and D. M. WILSON 3RD, 1999 The RAD2 domain of human exonuclease 1 exhibits 5′ to 3′ exonuclease and flap structure-specific endonuclease activities. J. Biol. Chem. 274: 37763-37769.
28. LEE, S. E., J. K. MOORE, A. HOLMES, K. UMEZU, R. D. KOLODNER et al., 1998 Saccharomyces Ku70, Mre11/Rad50, and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94: 399-409.
29. LEE, S. E., D. A. BRESSAN, J. H. J. PETRINI and J. E. HABER, 2002 Complementation between N-terminal Saccharomyces cerevisiae mre11 alleles in DNA repair and telomere length maintenance. DNA Repair 1: 27-40.
30. LEROY, C., S. E. LEE, M. B. VAZE, F. OCHSENBIEN, R. GUEROIS et al., 2003 PP2C phosphatases Ptc2 and Ptc3 are required for DNA checkpoint inactivation after a double-strand break. Mol. Cell 11: 827-835.
31. LEWIS, L. K., G. KARTHIKEYAN, J. W. WESTMORELAND and M. A. RESNICK, 2002 Differential suppression of DNA repair deficiencies of yeast rad50, mre11 and xrs2 mutants by EXO1 and TLC1 (the RNA component of telomerase). Genetics 160: 49-62.
32. LINDSEY-BOLTZ, L. A., V. P. BERMUDEZ, J. HURWITZ and A. SANCAR, 2001 Purification and characterization of human DNA damage checkpoint Rad complexes. Proc. Natl. Acad. Sci. USA 98: 11236-11241.
33. LOUIS, E. J., E. S. NAUMOVA, A. LEE, G. NAUMOV and J. E. HABER, 1994 The chromosome end in yeast: its mosaic nature and influence on recombinational dynamics. Genetics 136: 789-802.
34. LOWNDES, N. F., and J. R. MURGUIA, 2000 Sensing and responding to DNA damage. Curr. Opin. Genet. Dev. 10: 17-25.
35. LUHR, B., J. SCHELLER, P. MEYER and W. KRAMER, 1998 Analysis of in vivo correction of defined mismatches in the DNA mismatch repair mutants msh2, msh3 and msh6 of Saccharomyces cerevisiae. Mol. Gen. Genet. 257: 362-367.
36. LYDALL, D., 2003 Hiding at the ends of yeast chromosomes: telomeres, nucleases and checkpoint pathways. J. Cell Sci. 116: 4057-4065.
37. LYDALL, D., and T. WEINERT, 1995 Yeast checkpoint genes in DNA damage processing: implications for repair and arrest. Science 270: 1488-1491.
38. LYDALL, D., and T. WEINERT, 1997a G2/M checkpoint genes of Saccharomyces cerevisiae: further evidence for roles in DNA replication and/or repair. Mol. Gen. Genet. 256: 638-651.
39. LYDALL, D., and T. WEINERT, 1997b Use of cdc13-1-induced DNA damage to study effects of checkpoint genes on DNA damage processing. Methods Enzymol. 283: 410-424.
40. MAJKA, J., and P. M. BURGERS, 2003 Yeast Rad17/Mec3/Ddc1: a sliding clamp for the DNA damage checkpoint. Proc. Natl. Acad. Sci. USA 100: 2249-2254.
41. MARINGELE, L., and D. LYDALL, 2002 EXO1-dependent single-stranded DNA at telomeres activates subsets of DNA damage and spindle checkpoint pathways in budding yeast yku70Δ mutants. Genes Dev. 16: 1919-1933.
42. MARTI, T. M., C. KUNZ and O. FLECK, 2002 DNA mismatch repair and mutation avoidance pathways. J. Cell. Physiol. 191: 28-41.
43. MELO, J. A., J. COHEN and D. P. TOCZYSKI, 2001 Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 15: 2809-2821.
44. MOREAU, S., E. A. MORGAN and L. S. SYMINGTON, 2001 Overlapping functions of the Saccharomyces cerevisiae Mre11, Exo1 and Rad27 nucleases in DNA metabolism. Genetics 159: 1423-1433.
45. NAURECKIENE, S., and W. K. HOLLOMAN, 1999 DNA hydrolytic activity associated with the Ustilago maydis REC1 gene product analyzed on hairpin oligonucleotide substrates. Biochemistry 38: 14379-14386.
46. NUGENT, C. I., G. BOSCO, L. O. ROSS, S. K. EVANS, A. P. SALINGER et al., 1998 Telomere maintenance is dependent on activities required for end repair of double-strand breaks. Curr. Biol. 8: 657-660.
47. NUGENT, C. I., T. R. HUGHES, N. F. LUE and V. LUNDBLAD, 1996 Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274: 249-252.
48. NYBERG, K. A., R. J. MICHELSON, C. W. PUTNAM and T. A. WEINERT, 2002 Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36: 617-656.
49. PAQUES, F., and J. E. HABER, 1999 Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63: 349-404.
50. POLOTNIANKA, R. M., J. LI and A. J. LUSTIG, 1998 The yeast Ku heterodimer is essential for protection of the telomere against nucleolytic and recombinational activities. Curr. Biol. 8: 831-834.
51. PRYDE, F. E., and E. J. LOUIS, 1999 Limitations of silencing at native yeast telomeres. EMBO J. 18: 2538-2550.
52. PRYDE, F. E., H. C. GORHAM and E. J. LOUIS, 1997 Chromosome ends: all the same under their caps. Curr. Opin. Genet. Dev. 7: 822-828.
53. RIZKI, A., and V. LUNDBLAD, 2001 Defects in mismatch repair promote telomerase-independent proliferation. Nature 411: 713-716.
54. ROUSE, J., and S. P. JACKSON, 2002 Lcd1p recruits Meclp to DNA lesions in vitro and in vivo. Mol. Cell 9: 857-869.
55. SOGO, J. M., M. LOPES and M. FOIANI, 2002 Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602.
56. STRATHDEE, G., O. J. SANSOM, A. SIM, A. R. CLARKE and R. BROWN, 2001 A role for mismatch repair in control of DNA ploidy following DNA damage. Oncogene 20: 1923-1927.
57. SZANKASI, P., and G. R. SMITH, 1995 A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science 267: 1166-1169.
58. TISHKOFF, D. X., A. L. BOERGER, P. BERTRAND, N. FILOSI, G. M. GAIDA et al., 1997 Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2. Proc. Natl. Acad. Sci. USA 94: 7487-7492.
59. TOCZYSKI, D. P., D. J. GALGOCZY and L. H. HARTWELL, 1997 CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90: 1097-1106.
60. TOMITA, K., A. MATSUURA, T. CASPARI, A. M. CARR, Y. AKAMATSU et al., 2003 Competition between the Rad50 complex and the Ku heterodimer reveals a role for Exo1 in processing double-strand breaks but not telomeres. Mol. Cell. Biol. 23: 5186-5197.
61. TRAN, P. T., N. ERDENEZ, S. DUDLEY and R. M. LISKAY, 2002 Characterization of nuclease-dependent functions of Exo1 p in Saccharomyces cerevisiae. DNA Repair 1: 895-912.
62. TSUBOUCHI, H., and H. OGAWA, 2000 Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol. Biol. Cell 11: 2221-2233.
63. TSUKAMOTO, Y., A. K. TAGGART and V. A. ZAKIAN, 2001 The role of the Mre11-Rad50-Xrs2 complex in telomerase-mediated lengthening of Saccharomyces cerevisiae telomeres. Curr. Biol. 11: 1328-1335.
64. USUI, T., H. OGAWA and J. H. PETRINI, 2001 A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol. Cell 7: 1255-1266.
65. VAZE, M. B., A. PELLICIOLI, S. E. LEE, G. IRA, G. LIBERI et al., 2002 Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol. Cell 10: 373-385.
66. WANG, Y., and J. QIN, 2003 MSH2 and ATR form a signaling module and regulate two branches of the damage response to DNA methylation. Proc. Natl. Acad. Sci. USA 100: 15387-15392.
67. WEINERT, T. A., and L. H. HARTWELL, 1993 Cell cycle arrest of cdc mutants and specificity of the RAD9 checkpoint. Genetics 134: 63-80.
68. WINZELER, E. A., C. I. CASTILLO-DAVIS, G. OSHIRO, D. LIANG, D. R. RICHARDS et al., 2003 Genetic diversity in yeast assessed with whole-genome oligonucleotide arrays. Genetics 163: 79-89.
69. YAN, T., J. E. SCHUPP, H. S. HWANG, M. W. WAGNER, S. E. BERRY et al., 2001 Loss of DNA mismatch repair imparts defective cdc2 signaling and G(2) arrest responses without altering survival after ionizing radiation. Cancer Res. 61: 8290-8297.
70. ZHOU, B. B., and S. J. ELLEDGE, 2000 The DNA damage response: putting checkpoints in perspective. Nature 408: 433-439.
71. ZOU, L., and S. J. ELLEDGE, 2003 Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.
72. ZOU, L., D. CORTEZ and S. J. ELLEDGE, 2002 Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev. 16: 198-208.