DNA damage checkpoints update: Getting molecular

Current Opinion in Genetics and Development

Volumn 8, Issue 2, 1998, Pages 185-193

  Weinert, Ted ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOCHEMISTRY; CELL CYCLE; DNA DAMAGE; DNA REPLICATION; EUKARYOTE; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; YEAST;

EID: 0032055349     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(98)80140-8     Document Type: Article

References (72)

1. Friedberg EC, Walker GC, Siede W: DNA repair and mutagenesis. 2nd edition. Washington, DC: ASM Press; 1995.
2. Paulovich AG, Toczyski DP, Hartwell LH. When checkpoints fail. of special interest Cell. 88:1997;315-321 A minireview covering many aspects of yeast checkpoint controls, including why checkpoint mutant cells suffer genetic instability, and discussions of relevant studies of instability in mammalian cells.
3. Hartwell LH, Kastan MB. Cell cycle control and cancer. Science. 266:1994;1821-1828.
4. Hartwell LH, Szankasi P, Roberts CJ, Murray AW, Friend SH. Integrating genetic approaches into the discovery of anticancer drugs. of outstanding interest Science. 278:1997;1064-1068 A discussion from authors at the 'Seattle Project' on how the study of yeast mutants and pathways may contribute to cancer therapy. This presents specific strategies now in use, using specific mutants in yeast DNA damage responses that even involving drug screening.
5. Weinert TA, Hartwell LH. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science. 241:1988;317-322.
6. Hartwell LH, Weinert TA. Checkpoints: controls that ensure the orger of cell cycle events. Science. 241:1988;317-322.
7. Elledge SJ. Cell cycle checkpoints: preventing an identity crisis. Science. 274:1996;1664-1672.
8. Carr AM. Control of cell cycle arrest by Mec1sc/Rad3sp DNA structure checkpoint pathway. Curr Opin Genet Dev. 7:1997;93-98.
9. Stewart E, Enoch T. S-phase and DNA-damage checkpoints: a tale of two yeasts. Curr Opin Cell Biol. 8:1996;781-787.
10. Navas TA, Zhou Z, Elledge SJ. DNA polymerase epsilon links the DNA replication machinery to the S phase checkpoint. Cell. 80:1995;29-39.
11. D'Urso G, Graliert B, Nurse P. DNA polymerase alpha, a component of the replication initiation complex, is essential for the checkpoint coupling S phase to mitosis in fission yeast. J Cell Sci. 108:1995;3109-3118.
12. Weinert T. A DNA damage checkpoint meets the cell cycle engine. Science. 277:1997;1450-1451.
13. Garvik BM, Carson M, Hartwell LH. 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.
14. Lydall D, Nikolsky Y, Bishop DK, Weinert T. A meiotic recombination checkpoint controlled by mitotic checkpoint genes. of special interest Nature. 383:1996;840-843 This study shows that some but not all mitotic checkpoint genes have a role in arrest during meiotic recombination. This study is one of several, including those of the mammalian ATM gene, evaluating complex roles of checkpoint controls in meiosis.
15. Lydall D, Weinert T. Yeast checkpoint genes in DNA damage processing: implications for repair and arrest. Science. 270:1995;1488-1491.
16. Lydall D, Weinert T. From DNA damage to cell cycle arrest and suicide: a budding yeast perspective. Curr Opin Genet Dev. 6:1996;4-11.
17. Morrow DM, Tagle DA, Shiloh Y, Collins FS, Hieter P. TEL1, an S. cerevisiae homolog of the human gene mutated in Ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1. Cell. 82:1995;831-840.
18. Sanchez Y, Desany BA, Jones WJ, Liu Q, Wang B, Elledge S. Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. of special interest. of outstanding interest Science. 271:1996;357-360 These works [18,20] are the first two studies in budding yeast to document phosphorylation of checkpoint proteins requiring checkpoint proteins after damage (see also [19,21,23,24,27]).
19. Sugimoto K, Ando S, Shimomura T, Matsumoto K. Rfc5, a relication factor C component, is required for regulation of Rad53 protein kinase in the yeast checkpoint pathway. of special interest Mol Cell Biol. 17:1997;5905-5914 This study shows that RFC5, a gene with essential roles in DNA replication and repair, also has a role in checkpoint responses. This study, and that of RPA mutants [71] indicate that genes essential in replication and repair are involved in checkpoint signaling as well.
20. Sun Z, Fay DS, Marini F, Foiani M, Stern DF. Spk1/Rad53 is regulated by Mec1-dependent protein phosphorylation in DNA replication and damage checkpoint pathways. of outstanding interest Genes Dev. 10:1996;395-406 See annotation to [18].
21. 2/M arrest, requires MEC1 but not RAD53. A model ensues that is essential as shown in Figure 2C.
22. Kiser GL, Weinert TA. Distinct roles of yeast MEC and RAD checkpoint genes in transcriptional induction after DNA damage and implications for function. Mol Biol Cell. 7:1996;703-718.
23. 2/M responses, and show that Ddc1p too becomes phosphorylated after DNA damage.
24. 1/S checkpoint, no less (see Figure 2a).
25. Zhou Z, Elledge SJ. DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell. 75:1993;1119-1127.
26. Brush G, Morrow DM, Heiter P, Kelly TJ. The ATM homologue MEC1 is required for phosphorylation of replication protein A in yeast. Proc Natl Acad Sci USA. 93:1996;15075-15080.
27. 2/M checkpoint (discussed in [12]).
28. 1 checkpoint control in the yeast Saccharomyces cerevisiae following exposure to DNA-damaging agents. Genetics. 138:1994;271-281.
29. 1/S checkpoint appears to sense nucleotide depletion, a signal apparently distinct from DNA damage. This study is complete with a metabolic chart and inhibitors used to test the metabolites that activate the reversible arrest.
30. 1 cell cycle arrest induced by ribonucleotide depletion in the absence of detectable DNA damage. Genes Dev. 10:1996;934-947.
31. CDC2, discussed in [12].
32. Paulovich AG, Margulies RU, Garvik BM, Hartwell LH. RAD9, RAD17, and RAD24 are required for S phase regulation in Saccharomyces cerevisiae in response to DNA damage. of outstanding interest Genetics. 145:1997;45-62 An incredibly detailed analysis of the intra-S phase checkpoint in which the authors analyse the delay of DNA replication in no less than 25 isogenic yeast mutants defective in aspects of DNA repair. The goal was to identify other repair pathways that may feed in to the checkpoint response that delays DNA replication after damage. Such detailed analyses are important, and will become typical as yeast pathways of specific responses are detailed.
33. Longhese MP, Frashini R, Plevano P, Lucchini G. Yeast pip3/mec3 mutants fail to delay entry into S phase and to slow DNA replication in response to DNA damage, and they define a functional link between Mec3 and DNA Primase. Mol Cell Biol. 16:1996;3235-3244.
34. Paulovich AG, Hartwell LH. A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell. 82:1995;841-847.
35. Bousset K, Diffley J. The Cdc7 protein kinase is required for origin firing during S phase. of special interest Genes Dev. 12:1998;480-490 See accompanying paper by Donaldson et al. [72].
36. Enoch T, Carr AM, Nurse P. Fission yeast genes involved in coupling mitosis to completion of DNA replication. Genes Dev. 6:1992;2035-2046.
37. Sandell LL, Zakian VA. Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell. 75:1993;729-739.
38. Toczyski DP, Galgoczy DJ, Hartwell LH. CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. of outstanding interest Cell. 90:1997;1097-1106 This study describes adaptation, a novel and important checkpoint-related response. When cells have unrepairable damage they do not remain arrested forever, rather they resume cell cycle progression. The pathway of adaptation may prove very important in cancer progression, especially in cells that have repair defects (e.g. XP) and thus unrepairable damage.
39. Cohen-Fix O, Peters J-M, Kirschner MW, Koshland D. Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev. 10:1996;3081-3093.
40. Cohen-Fix O, Koshland D. The metaphase-to-anaphase transition: avoiding a mid-life crisis. Curr Opin Cell Biol. 9:1997;800-807.
41. Guacci V, Hogan E, Koshland D. Chromosome condensation and sister chromatid pairing in budding yeast. J Cell Biol. 125:1994;517-530.
42. cdc28 tyrosine phosphorylation is not required for entry into mitosis in S. cerevisiae. Nature. 355:1992;368-371.
43. 2/M checkpoint in budding yeast. This study reports that PDS1, an anaphase inhibitor, has roles in both the DNA damage and spindle assembly checkpoints.
44. Yang SS, Yeh E, Salmon ED, Bloom K. Identification of a mid-anaphase checkpoint in budding yeast. J Cell Biol. 136:1997;345-354.
45. Weber L, Byers BA. RAD9-dependent checkpoint blocks meiosis in cdc13 yeast cells. Genetics. 131:1992;55-63.
46. Xu L, Weiner BM, Kleckner N. Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev. 11:1997;106-118.
47. Roeder GS. Meiotic chromosomes: it takes two to tango. Genes Dev. 11:1997;2600-2621.
48. Allen JB, Zhou Z, Siede W, Friedberg EC, Elledge SJ. The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev. 8:1994;2416-2428.
49. Aboussekhra A, Vialard JE, Morrison DE, de la Torre-Ruiz MA, Cernakova L, Fabre F, Lowndes NF. A novel role for the budding yeast RAD9 checkpoint gene in DNA damage-dependent transcription. EMBO J. 15:1996;3912-3922.
50. Ho Y, Mason S, Kobayashi R, Hoekstra M, Andrews B. Role of casein kinase I isoform, Hrr25, and the cell cycle-regulatory transcription factor, SBF, in the transcriptional response to DNA damage in Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 94:1997;581-586.
51. Rotman G, Shiloh Y. Ataxia-talangiectasia: is ATM a sensor of oxidative damage and stress? of outstanding interest Bioessays. 19:1997;911-917 A review that discusses how ATM may have a primary role in oxidative stress, and perhaps not in DNA damage responses per se. If true, this will alter interpretations of certain atm mutant phenotypes, and especially those having to do with neuronal cell death. Regulation of oxidative stress in yeast could plausibly be MEC1's essential function too.
52. 1/M-phase checkpoint. Mol Cell Biol. 15:1995;5312-5321.
53. 1 is important for the onset of S phase and for preventing a 'reductional' anaphase in the budding yeast S. cerevisiae. EMBO J. 14:1995;3788-3799.
54. Kelley TJ, Martin GS, Forsburg SL, Stephensen RJ, Russo A, Nurse P. The fission yeast cdc18+ gene product couples S phase to START and mitosis. Cell. 74:1993;371-382.
55. Saka Y, Yanagida M. Fission yeast cut5+, required for S phase onset and M phase restraint, is identical to the radiation-damage repair gene rad4+. Cell. 74:1993;383-393.
56. Bueno A, Russell P. Dual functions of CDC6: a yeast protein required for DNA replication also inhibits nuclear division. EMBO J. 11:1992;2167-2176.
57. 2/M checkpoint response.
58. cdc28. Nature. 355:1992;365-368.
59. Lew DJ, Reed SI. A cell cycle checkpoint monitors cell morphogenesis in budding yeast. J Cell Biol. 129:1995;739-749.
60. CDC28 as a mechanism of arrest (see [42,58]).
61. Lieberman HB, Hopkins KM, Nass M, Demetrick D, Davey S. A human homolog of the Schizosaccharomyces pombe rad9+ checkpoint control gene. Proc Natl Acad Sci USA. 93:1996;13890-13895.
62. Pati D, Keller C, Groudine M, Plon SE. Reconstitution of a MEC1-independent checkpoint in yeast by expression of a novel human fork head cDNA. of special interest Mol Cell Biol. 17:1997;3037-3046 This study describes isolation of the mammalian gene fragment called CHES1 that has the remarkable property of suppressing arrest defects in both sensor mutants (rad9) and signaler mutants (mec1). How CHES1 acts in yeast is unknown.
63. Hofmann K, Bucher P. The FHA domain: a putative nuclear signalling domain found in protein kinases and transcription factors. Trends Biochem Sci. 1995.
64. Callebaut I, Mornon J-P. From BRCA1 to RAP1: a widespread BRCT module closely associated with DNA repair. FEBS Lett. 400:1997;25-30.
65. Weinert TA, Lydall D. Cell cycle checkpoints, genetic instability and cancer. Semin Cancer Biol. 4:1993;129-140.
66. Wilson J, Wilson S, Warr N, Watts FZ. Isolation and characterization of the Schizosaccharomyces pombe rhp9 gene: a gene required for the DNA damage but not the replication checkpoint. Nucleic Acids Res. 25:1997;2138-2145.
67. Weinert TA, Hartwell LH. Cell cycle arrest of cdc mutants and specificity of the RAD9 checkpoint. Genetics. 134:1993;63-80.
68. 2/M checkpoint genes in S. cerevisiae and further evidence for roles in DNA replication and/or repair. Mol Gen Genet. 256:1997;638-651.
69. Griffiths DJG, Barbet NC, McCready S, Lehmann AR, Carr AM. Fission Yeast rad17: a homologue of budding yeast RAD24 that shares regions of sequence similarity with DNA polymerase accessory proteins. EMBO J. 14:1995;101-112.
70. Weinert TA, Kiser GL, Hartwell LH. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev. 8:1994;652-665.
71. 2/M arrest.
72. Donaldson A, Fangman WL, Brewer BJ. Cdc7 is required throughout the yeast S phase to activate replication origins. Genes Dev. 12:1998;491-501.