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Science 1 December 1995:
Vol. 270. no. 5241, pp. 1488 - 1491
DOI: 10.1126/science.270.5241.1488
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Reports

Yeast Checkpoint Genes in DNA Damage Processing: Implications for Repair and Arrest

David Lydall and Ted Weinert

Yeast checkpoint control genes were found to affect processing of DNA damage as well as cell cycle arrest. An assay that measures DNA damage processing in vivo showed that the checkpoint genes RAD17, RAD24, and MEC3 activated an exonuclease that degrades DNA. The degradation is probably a direct consequence of checkpoint protein function, because RAD17 encodes a putative 3`-5` DNA exonuclease. Another checkpoint gene, RAD9, had a different role: It inhibited the degradation by RAD17, RAD24, and MEC3. A model of how processing of DNA damage may be linked to both DNA repair and cell cycle arrest is proposed.


Department of Molecular and Cellular Biology, University of Arizona, Tucson AZ 85721, USA.


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C. B. Bennett, J. R. Snipe, J. W. Westmoreland, and M. A. Resnick (2001)
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The set1{Delta} mutation unveils a novel signaling pathway relayed by the Rad53-dependent hyperphosphorylation of replication protein A that leads to transcriptional activation of repair genes.
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Fission Yeast Rad17 Associates with Chromatin in Response to Aberrant Genomic Structures.
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Phosphorylation of the replication protein A large subunit in the Saccharomyces cerevisiae checkpoint response.
G. S. Brush and T. J. Kelly (2000)
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Role for the Silencing Protein Dot1 in Meiotic Checkpoint Control.
P. A. San-Segundo and G. S. Roeder (2000)
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Sgs1 Helicase Activity Is Required for Mitotic but Apparently Not for Meiotic Functions.
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Mol. Cell. Biol. 20, 6399-6409
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Rfc5, in Cooperation with Rad24, Controls DNA Damage Checkpoints throughout the Cell Cycle in Saccharomyces cerevisiae.
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Mol. Cell. Biol. 20, 5888-5896
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Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes.
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DNA Repair Protein Rad55 Is a Terminal Substrate of the DNA Damage Checkpoints.
V. I. Bashkirov, J. S. King, E. V. Bashkirova, J. Schmuckli-Maurer, and W.-D. Heyer (2000)
Mol. Cell. Biol. 20, 4393-4404
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Involvement of the Checkpoint Protein Mec1p in Silencing of Gene Expression at Telomeres in Saccharomyces cerevisiae.
R. J. Craven and T. D. Petes (2000)
Mol. Cell. Biol. 20, 2378-2384
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Involvement of the PP2C-Like Phosphatase Ptc2p in the DNA Checkpoint Pathways of Saccharomyces cerevisiae.
M.-C. Marsolier, P. Roussel, C. Leroy, and C. Mann (2000)
Genetics 154, 1523-1532
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A CAF-1-PCNA-Mediated Chromatin Assembly Pathway Triggered by Sensing DNA Damage.
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Mol. Cell. Biol. 20, 1206-1218
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CAF-1 and the inheritance of chromatin states: at the crossroads of DNA replication and repair.
P Ridgway and G Almouzni (2000)
J. Cell Sci. 113, 2647-2658
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A novel mutant allele of the chromatin-bound fission yeast checkpoint protein Rad17 separates the DNA structure checkpoints.
D Griffiths, M Uchiyama, P Nurse, and T. Wang (2000)
J. Cell Sci. 113, 1075-1088
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Details and Concerns Regarding the G2/M DNA Damage Checkpoint in Budding Yeast.
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Cold Spring Harb Symp Quant Biol 65, 433-442
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A Conserved Role for the Hus1 Checkpoint Protein in Eukaryotic Genome Maintenance.
R.S. WEISS, P. LEDER, and T. ENOCH (2000)
Cold Spring Harb Symp Quant Biol 65, 457-466
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Saccharomyces cerevisiae Checkpoint Genes MEC1, RAD17 and RAD24 Are Required for Normal Meiotic Recombination Partner Choice.
J. M. Grushcow, T. M. Holzen, K. J. Park, T. Weinert, M. Lichten, and D. K. Bishop (1999)
Genetics 153, 607-620
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D. A. Thompson and F. W. Stahl (1999)
Genetics 153, 621-641
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Multiple Pathways of Recombination Induced by Double-Strand Breaks in Saccharomyces cerevisiae.
F. Paques and J. E. Haber (1999)
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Lesions in Many Different Spindle Components Activate the Spindle Checkpoint in the Budding Yeast Saccharomyces cerevisiae.
K. G. Hardwick, R. Li, C. Mistrot, R.-H. Chen, P. Dann, A. Rudner, and A. W. Murray (1999)
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K. M. Hyland, J. Kingsbury, D. Koshland, and P. Hieter (1999)
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RAD53 Regulates DBF4 Independently of Checkpoint Function in Saccharomyces cerevisiae.
P. R. Dohrmann, G. Oshiro, M. Tecklenburg, and R. A. Sclafani (1999)
Genetics 151, 965-977
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Role of a Complex Containing Rad17, Mec3, and Ddc1 in the Yeast DNA Damage Checkpoint Pathway.
T. Kondo, K. Matsumoto, and K. Sugimoto (1999)
Mol. Cell. Biol. 19, 1136-1143
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Evidence for novel cell cycle checkpoints in trypanosomes: kinetoplast segregation and cytokinesis in the absence of mitosis.
A Ploubidou, D. Robinson, R. Docherty, E. Ogbadoyi, and K Gull (1999)
J. Cell Sci. 112, 4641-4650
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Human Homologs of Schizosaccharomyces pombe Rad1, Hus1, and Rad9 Form a DNA Damage-responsive Protein Complex.
E. Volkmer and L. M. Karnitz (1999)
J. Biol. Chem. 274, 567-570
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The SFP1 Gene Product of Saccharomyces cerevisiae Regulates G2/M Transitions During the Mitotic Cell Cycle and DNA-Damage Response.
Z. Xu and D. Norris (1998)
Genetics 150, 1419-1428
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Role of the Putative Zinc Finger Domain of Saccharomyces cerevisiae DNA Polymerase epsilon  in DNA Replication and the S/M Checkpoint Pathway.
R. Dua, D. L. Levy, and J. L. Campbell (1998)
J. Biol. Chem. 273, 30046-30055
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Dna2 of Saccharomyces cerevisiae Possesses a Single-stranded DNA-specific Endonuclease Activity That Is Able to Act on Double-stranded DNA in the Presence of ATP.
S.-H. Bae, E. Choi, K.-H. Lee, J. S. Park, S.-H. Lee, and Y.-S. Seo (1998)
J. Biol. Chem. 273, 26880-26890
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Functional and Physical Interaction between Rad24 and Rfc5 in the Yeast Checkpoint Pathways.
T. Shimomura, S. Ando, K. Matsumoto, and K. Sugimoto (1998)
Mol. Cell. Biol. 18, 5485-5491
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The Saccharomyces cerevisiae RAD9, RAD17, RAD24 and MEC3 Genes Are Required for Tolerating Irreparable, Ultraviolet-Induced DNA Damage.
A. G. Paulovich, C. D. Armour, and L. H. Hartwell (1998)
Genetics 150, 75-93
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Human and mouse homologs of Schizosaccharomyces pombe rad1+ and Saccharomyces cerevisiae RAD17: linkage to checkpoint control and mammalian meiosis.
R. Freire, J. R. Murguía, M. Tarsounas, N. F. Lowndes, P. B. Moens, and S. P. Jackson (1998)
Genes & Dev. 12, 2560-2573
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A Human Homologue of the Schizosaccharomyces pombe rad1+ Checkpoint Gene Encodes an Exonuclease.
A. E. Parker, I. Van de Weyer, M. C. Laus, I. Oostveen, J. Yon, P. Verhasselt, and W. H. M. L. Luyten (1998)
J. Biol. Chem. 273, 18332-18339
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Identification of a Human Homologue of the Schizosaccharomyces pombe rad17+ Checkpoint Gene.
A. E. Parker, I. Van de Weyer, M. C. Laus, P. Verhasselt, and W. H. M. L. Luyten (1998)
J. Biol. Chem. 273, 18340-18346
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Rad53 FHA Domain Associated with Phosphorylated Rad9 in the DNA Damage Checkpoint.
Z. Sun, J. Hsiao, D. S. Fay, and D. F. Stern (1998)
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L. K. Lewis, J. M. Kirchner, and M. A. Resnick (1998)
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Regulation of Telomere Length by Checkpoint Genes in Schizosaccharomyces pombe.
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