Distinct roles of yeast MEC and RAD checkpoint genes in transcriptional induction after DNA damage and implications for function

Molecular Biology of the Cell

Volumn 7, Issue 5, 1996, Pages 703-718

  Kiser, Gretchen L ^a   Weinert, Ted A ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MESSENGER RNA;

ARTICLE; CELL CYCLE; CELL DIVISION; CELL STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; FLUORESCENCE; GENE; GENE FUNCTION; GENETIC TRANSCRIPTION; MICROSCOPY; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; YEAST;

EUKARYOTA; SACCHAROMYCETALES;

EID: 0029965718     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.7.5.703     Document Type: Article

References (80)

1. Allen, J.B., Zhou, Z., Siede, W., Friedberg, E.C., and Elledge, S.J (1995). The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev. 8, 2401-2415.
2. cdc2+ tyrosine phosphorylation is not required for entry into mitosis in S. cerevisiae. Nature 355, 368-371.
3. Anderson, C.W. (1993). DNA damage and the DNA-activated protein kinase. Trends Biochem. Sci. 18, 433-437.
4. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (1990). Current Protocols in Molecular Biology, New York: Greene Publishing Associates and Wiley-Interscience, John Wiley and Sons.
5. Beamish, H., and Lavin, M.F. (1994). Radiosensitivity in ataxia-telangiectasia: anomalies in radiation-induced cell cycle delay. Int. J. Radiat. Biol. 65, 175-184.
6. Blunt, T., et al. (1995). Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation Cell 80, 813-823.
7. Boubnov, N.V., and Weaver, D.T. (1995). scid cells are deficient in Ku and replication protein A phosphorylation by the DNA-dependent protein kinase. Mol. Cell. Biol. 15, 5700-5706.
8. Caponigro, G., Muhlrad, D., and Parker, R. (1993). A small segment of the MATα1 transcript promotes mRNA decay in Saccharomyces cerevisiae: a stimulatory role for rare codons. Mol. Cell. Biol. 13, 5141-5148.
9. Cole, G.M., Schild, D., Lovett, S.T., and Mortimer, R.K. (1987). Regulation of RAD54- and RAD52-lacz gene fusions in Saccharomyces cerevisise in response to DNA damage. Mol. Cell. Biol. 7, 1078-1084.
10. Dhanci, R., et al. (1994). PI-3 kinase is a dual specificity enzyme: autoregulation by an intrinsic protein-serine kinase activity. EMBO J. 13, 522-533
11. Elledge, S.J., and Davis, R.W. (1989a). DNA damage induction of ribonucleotide reductase. Mol. Cell. Biol. 9, 4932-4940.
12. Elledge, S.J., and Davis, R.W. (1989b). Identification of the DNA damage-responsive element of RNR2 and evidence that four distinct cellular factors bind it. Mol. Cell. Biol. 9, 5373-5386.
13. Elledge, S.J., and Davis, R.W. (1990). Two genes differentially regulated in the cell cycle and by DNA-damaging agents encode alternative regulatory subunits of ribonucleotide reductase. Genes Dev. 4, 740-751.
14. Enoch, T., and Nurse, P. (1990). Mutation of fission yeast cell cycle control gene abolishes dependence of mitosis on DNA replication. Cell 60, 665-673.
15. Feinberg, A.P., and Vogelstein, B. (1983). A technique for radiolabeling DNA restriction fragments to a high specific activity. Anal. Biochem. 132, 6-13.
16. Feldmann, H., and Winnacker, E.L. (1993). A putative homologue of the human autoantigen Ku from Saccharomyces cerevisiae. J. Biol. Chem. 268, 12895-12900.
17. Friedberg, E.C. (1985). DNA Repair, New York: W.H. Freeman and Company.
18. Gottlieb, T.M., and Jackson, S.P. (1993). The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell 72, 131-142.
19. Gottlieb, T.M., and Jackson, S.P. (1994). Protein kinases and DNA damage. Trends Biochem. Sci. 19, 512-515.
20. Harder, J., and Follmann, H. (1990). Identification of a free radical and oxygen dependence of ribonucleotide reductase in yeast. Free Radical Res. Commun. 10, 281-286.
21. Hartley, K.O., Gell, D., Smith, G.C., Zhang, H., Divecha, N., Connelly, M.A., Admon, A., Lees-Miller, S.P., Anderson, C.W., and Jackson, S.P. (1995). DNA-dependent protein kinase catalytic subunit: a relative of phosphatidylinositol 3-kinase and the ataxia telangiectasia gene product. Cell 82, 849-856.
22. Hartwell, L.H., and Kastan, M.B. (1994). Cell cycle control and cancer. Science 266, 1821-1828.
23. Heald, R., McLoughlin, M., and McKeon, F. (1993). Human Wee1 maintains mitotic timing by protecting the nucleus from cytoplasmically activated Cdc2 kinase Cell 74, 463-474.
24. Hereford, L.M., Osley, M.A., Ludwig, J.R.I., and McLaughlin, C.S. (1981). Cell-cycle regulation of yeast histone mRNA. Cell 24, 367-375.
25. Herrick, D., Parker, R., and Jacobson, A. (1990). Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 2269-2284.
26. Johnston, L.H., and Nasmyth, K.A. (1978). Saccharomyces cerevisiae cell cycle mutant cdc9 is defective in DNA ligase. Nature 274, 891-893.
27. Kastan, M.B., Onyekwere, O., Sidransky, D., Vogelstein, B., and Craig, R.W. (1991). Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51, 6304-6311.
28. Kato, R., and Ogawa, H. (1994). An essential gene, ESR1, is required for mitotic cell growth, DNA repair and meiotic recombination in Saccharomyces cerevisiae. Nucleic Acids Res. 22, 3104-3112.
29. Kuerbitz, S.J., Plunkett, B.S., Walsh, W.V., and Kastan, M.B. (1992). Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc. Natl. Acad. Sci. USA 89, 7491-7495.
30. Li, R., and Murray, A.W. (1991). Feedback control of mitosis in budding yeast. Cell 66, 519-531.
31. Lydall, D., and Weinert, T. (1995). Yeast checkpoint genes in DNA damage processing: implications for repair and arrest. Science 270, 1488-1491.
32. McClanahan, T., and McEntee, K. (1984). Specific transcripts are elevated in Saccharomyces cerevisiae in response to DNA damage. Mol. Cell. Biol. 4, 2356-2363.
33. McClanahan, T., and McEntee, K. (1986). DNA damage and heat shock dually regulate genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 6, 90-96.
34. Meeks-Wagner, D., and Hartwell, L.H. (1986). Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission. Cell 44, 43-52.
35. Moll, T., Tebb, G., Surana, U., Robitsch, H., and Nasmyth, K. (1991). The role of phosphorylation and the CDC28 protein kinase in cell cycle-regulated nuclear import of the S. cerevisiae transcription factor SW15 Cell 66, 743-758.
36. Morozov, V.E., Falzon, M., Anderson, C.W., and Kuff, E.L. (1994). DNA-dependent protein kinase is activated by nicks and larger single-stranded gaps. J. Biol. Chem. 269, 16684-16688.
37. Morrow, D.M., Tagle, D.A., Shiloh, Y., Collins, F.S., and Hieter, P. (1995). TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene Mec1. Cell 82, 831-840.
38. Murakami, H., and Okayama, H. (1995). A kinase from fission yeast responsible for blocking mitosis in S phase. Nature 374, 817-819.
39. Murray, A.W. (1991). Coordinating cell cycle events. Cold Spring Harbor Symp. Quant. Biol. 56, 399-408.
40. Murray, A.W. (1992). Creative blocks: cell-cycle checkpoints and feedback controls. Nature 359, 599-604.
41. Nagasawa, H., Latt, S.A., Lalande, M.E., and Little, J.B. (1985). Effects of x-irradiation on cell-cycle progression, induction of chromosomal aberrations and cell killing in ataxia-telangiectasia (AT) fibroblasts. Mutat. Res. 148, 71-82.
42. Nasr, F., Becam, A.-M., Slonimski, P.P., and Herbert, C.J. (1994). YBR1012 an essential gene from S. cerevisiae: construction of an RNA antisense conditional allele and isolation of a multicopy suppressor. C.R. Acad. Sci. Paris 317, 607-613.
43. Navas, T.A., Zhou, Z., and Elledge, S.J. (1995). DNA polymerase ε links the DNA replication machinery to the S phase checkpoint. Cel 80, 1-20.
44. Nelson, W.G., and Kastan, M.B. (1994). DNA strand breaks: the DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol. Cell. Biol. 14, 1815-1823.
45. Nurse, P. (1990). Universal control mechanism regulating onset of M-phase. Nature 344, 503-508.
46. Painter, R.B., and Young, R.B. (1980). Radiosensitivity in ataxia-telangiectasia: a new explanation. Proc. Natl. Acad. Sci. USA 77, 7315-7317.
47. Papathanasiou, M.A., Kerr, N.C.K., Robbins, J.H., McBride, O.W., Alamo, I., Jr., Barrett, S.F., Hickson, J.D., and Fornace, A.J., Jr. (1991). Induction by ionizing radiation of the gadd45 gene in cultured human cells: lack of mediation by protein kinase C. Mol. Cell. Biol. 11, 1009-1016.
48. Paulovich, A.G., and Hartwell, L.H. (1995). A checkpoint regulates the rate of progression though the S phase in S. cerevisiae in response to DNA damage. Cell 82, 841-847.
49. Pringle, J.R., Preston, R.A., Adams, A.E.M., Stearns, T., Drubin, D.G., Haarer, B.K., and Jones, E.W. (1989). Fluorescence microscopy materials and methods for yeast. Methods Cell Biol. 31, 357-432.
50. Rathmell, W.K., and Chu, G. (1994). Involvement of the Ku autoantigen in the cellular response to DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 91, 7623-7627.
51. Robinson, G., Nicolet, C., Kalainov, D., and Friedberg, E. (1986). A yeast excision-repair gene is inducible by DNA damaging agents. Proc. Natl. Acad. Sci. USA 83, 1842-1846.
52. Ruby, S.W., and Szostak, J.W. (1985). Specific Saccharomyces cerevisiae genes are expressed in response to DNA-damaging agents. Mol. Cell. Biol. 5, 75-84.
53. Rudolph, N.S., and Latt, S.A. (1989). Flow cytometric analysis of x-ray sensitivity in ataxia-telangiectasia. Mutat. Res. 211, 31-41.
54. Sandell, L.L., and Zakian, V.A. (1993). Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell 75, 729-739.
55. Savitsky, K., et al. (1995). A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268, 1749-1753.
56. Schiestl, R.H., and Gietz, R.D. (1989). High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet 16, 339-346.
57. Schild, D., Glassner, B.J., Mortimer, R.K., Carlson, M., and Laurent, B.C. (1992). Identification of RAD16, a yeast excision repair gene homologous to the recombinational repair gene RAD54 and to the SNF2 gene involved in transcriptional activation. Yeast 8, 385-395.
58. + gene, involved in DNA damage and DNA synthesis checkpoints. Gene 119, 83-89.
59. Sheldrick, K.S., and Carr, A.M. (1993). Feedback controls and G2 checkpoints: fission yeast as a model system. BioEssays 15, 775-782.
60. Sherman, F., Fink, G.R., and Hicks, J.B. (1986). Methods in Yeast Genetics, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
61. Siede, W., Friedberg, A.S., Dianova, I., and Friedberg, E.C. (1994). Characterization of G1 checkpoint control in the yeast Saccharomyces cerevisiae following exposure to DNA-damaging agents. Genetics 138, 271-281.
62. Siede, W., Friedberg, A.S., and Friedberg, E.C. (1993). RAD9-dependent G1 arrest defines a second checkpoint for damaged DNA in the cell cycle of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 90, 7985-7989.
63. Siede, W., and Friedberg, E.C. (1992). Regulation of the yeast RAD2 gene: DNA damage-dependent induction correlates with protein binding to regulatory sequences and their deletion influences survival. Mol. Gen Genet. 232, 247-256.
64. cdc28. Nature 355, 365-368.
65. Stack, J.H., and Emr, S.D. (1994). Vps34 required for yeast vacuolar protein sorting is a multiple specificity kinase that exhibits both protein kinase and phosphatidylinositol-specific PI 3-kinase activities. J Biol. Chem. 269, 31552-31562.
66. Stern, D.F., Zheng, P., Beidler, D.R., and Zerillo, C. (1991). Spk1, a new kinase from Saccharomyces cerevisiae, phosphorylates proteins on serine, threonine, and tyrosine. Mol. Cell. Biol. 11, 987-1001.
67. Taccioli, G.E., Gottlieb, T.M., Blunt, T., Priestley, A., Demengeot, J., Mizuta, R., Lehmann, A.R., Alt, F.W., Jackson, S.P., and Jeggo, P.A. (1994). Ku80: product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science 265, 1442-1445.
68. Thomas, P.S. (1980). Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc. Natl. Acad. Sci. USA 77, 5201-5205.
69. Treger, J.M., Heichman, K.A., and McEntee, K. (1988). Expression of the yeast UBI4 gene increases in response to DNA-damaging agents and in meiosis. Mol. Cell. Biol. 8, 1132-1136.
70. Treger, J.M., and McEntee, K. (1990). Structure of the DNA damage-inducible gene DDR48 and evidence for its role in mutagenesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 3174-3184.
71. Weinert, T.A., and Hartwell, L.H. (1988). The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241, 317-322.
72. Weinert, T.A., and Hartwell, L.H. (1990). Characterization of RAD9 of Saccharomyces cerevisiae and evidence that its function acts post-translationally in cell cycle arrest after DNA damage. Mol. Cell. Biol 10, 6554-6564.
73. Weinert, T.A., and Hartwell, L.H. (1993). Cell cycle arrest of cdc mutants and specificity of the RAD9 checkpoint. Genetics 134, 63-80.
74. Weinert, T.A., Kiser, G.L., and Hartwell, L.H. (1994). Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev. 8, 652-665.
75. Weinert, T A., and Lydall, D. (1993). Cell cycle checkpoints, genetic instability and cancer. Semin. Cancer Biol. 4, 129-140.
76. Witkin, E.M. (1991). RecA protein in the SOS response: milestones and mysteries. Biochimie 73, 133-141.
77. Yagle, K , and McEntee, K. (1990). The DNA damage-inducible gene DIN1 of Saccharomyces cerevisiae encodes a regulatory subunit of ribonucleotide reductase and is identical to RNR3. Mol. Cell. Biol. 10, 5553-5557.
78. Zheng, P., Fay, D.S., Burton, J., Xiao, H., Pinkham, J.L., and Stern, D.F. (1993). SPK1 is an essential S-phase-specific gene of Saccharomyces cerevisiae that encodes a nuclear serine/threonine/tyrosine kinase. Mol. Cell. Biol. 13, 5829-5842.
79. Zhou, Z., and Elledge, S J (1992). Isolation of crt mutants constitutive for transcription of the DNA damage-inducible gene RNR3 in Saccharomyces cerevisiae. Genetics 131, 851-866.
80. Zhou, Z., and Elledge, S.J. (1993). DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell 75, 1119-1127.