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Regulation ofSNM1, an inducibleSaccharomyces cerevisiae gene required for repair of DNA cross-links

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Abstract

The interstrand cross-link repair geneSNM1 ofSaccharomyces cerevisiae was examined for regulation in response to DNA-damaging agents. Induction ofSNM1-lacZ fusions was detected in response to nitrogen mustard, cis-platinum (II) diamine dichloride, UV light, and 8-methoxypsoralen + UVA, but not after heat-shock treatment or incubation with 2-dimethyl-aminoethylchloride, methylmethane sulfonate or 4-nitroquinoline-N-oxide. The promoter ofSNM1 contains a 15 bp motif, which shows homology to the DRE2 box of theRAD2 promoter. Similar motifs have been found in promoter regions of other damage-inducible DNA repair genes. Deletion of this motif results in loss of inducibility ofSNM1. Also, a putative negative up-stream regulation sequence was found to be responsible for repression of constitutive transcription ofSNM1. Surprisingly, no inducibility ofSNM1 was found after treatment with DNA-damaging agents in strains without an intactDUN1 gene, while regulation seems unchanged insad1 mutants.

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References

  • Allen JB, Zhou Z, Siede W, Friedberg EC, Elledge SJ (1994) TheSAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev 8:2416–428

    PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment tool. J Mol Biol 215:403–410

    Article  PubMed  Google Scholar 

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1989) Current protocols in molecular biology. John Wiley and Sons, New York

    Google Scholar 

  • Basile G, Aker M, Mortimer RK (1992) Nucleotide sequence and transcriptional regulation of the yeast recombinational repair geneRAD51. Mol Cell Biol 12:3235–3246

    PubMed  Google Scholar 

  • Ben Hur E, Song P-S (1984) The photochemistry and photobiology of furocoumarins (psoralens). Adv Radiation Biol 11:131–171

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    PubMed  Google Scholar 

  • Brendel M, Ruhland A (1984) Relationships between functionality and genetic toxicology of selected DNA-damaging agents. Mutation Res 133:51–85

    PubMed  Google Scholar 

  • Cassier-Chauvat C, Moustacchi E (1988) Allelism betweenpso1-1 andrev3-1 mutants and betweenpso2-1 andsnm1 mutants inSaccharomyces cerevisiae. Curr Genet 13:37–40

    Article  PubMed  Google Scholar 

  • Clifton D, Weinstock SB, Fraenkel DG (1978) Glycolysis mutants inSaccharomyces cerevisiae. Genetics 88:1–11

    PubMed  Google Scholar 

  • Cole GM, Schild D, Lovett ST, Mortimer RM (1987) Regulation ofRAD54- andRAD52-lacZ gene fusions inSaccharomyces cerevisiae in response to DNA damage. Mol Cell Biol 7:1078–1084

    PubMed  Google Scholar 

  • Eastman A (1987) The formation, isolation and characterization of DNA adducts produced by anticancer platinum complexes. Pharmacol Ther 34:155–166

    Article  PubMed  Google Scholar 

  • Elledge SJ, Davis RW (1987) Identification and isolation of the gene encoding the small subunit of ribonucleotide reductase fromSaccharomyces cerevisiae: DNA damage-inducible gene required for mitotic viability. Mol Cell Biol 7:2783–2793

    PubMed  Google Scholar 

  • Elledge SJ, Zhou Z, Allen JB (1992) Ribonucleotide reductase: regulation, regulation, regulation. Trends Biochem Sci 17:119–123

    Article  PubMed  Google Scholar 

  • Feinberg AP, Vogelstein B (1984) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 137:266–267

    Article  PubMed  Google Scholar 

  • Fleer R, Brendel M (1979) Formation and fate of cross-links induced by polyfunctional anticancer drugs in yeast. Mol Gen Genet 176:41–52

    Article  PubMed  Google Scholar 

  • Friedberg EC (1988) Desoxynucleic acid repair in the yeastSaccharomyces cerevisiae. Microbiol Rev 52:70–102

    PubMed  Google Scholar 

  • Haase E, Riehl D, Mack M, Brendel M (1989) Molecular cloning ofSNM1, a yeast gene responsible for a specific step in the repair of cross-linked DNA. Mol Gen Genet 218:64–71

    Article  PubMed  Google Scholar 

  • Henriques JAP, Brendel M (1990) The role ofPSO andSNM genes in DNA repair of the yeastSaccharomyces cerevisiae. Curr Genet 18:387–393

    Article  PubMed  Google Scholar 

  • Hill JE, Myers AM, Koerner TJ, Tzagoloff A (1986) Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast 2:163–167

    Article  PubMed  Google Scholar 

  • Hurd HK, Roberts JW (1989) Upstream regulatory sequences of the yeastRNR2 gene include a repression sequence and an activation site that binds the RAP1 protein. Mol Cell Biol 9:5359–5372

    PubMed  Google Scholar 

  • Jachymczyk WJ, von Borstel RC, Mowat MRA, Hastings PJ (1981) Repair of interstrand cross-links in DNA ofSaccharomyces cerevisiae requires two systems for DNA repair: theRAD3 system and theRAD51 system. Mol Gen Genet 182:196–205

    Article  PubMed  Google Scholar 

  • Jones JS, Prakash L (1991) Transcript levels of theSaccharomyces cerevisiae DNA repair geneRAD18 increase in UV irradiated cells and during meiosis but not during the mitotic cell cycle. Nucleic Acids Res 19:893–898

    PubMed  Google Scholar 

  • Jones JS, Weber S, Prakash L (1988) TheSaccharomyces cerevisiae RAD18 gene encodes a protein that contains potential zinc finger domains for nucleic acid binding and a putative nucleotide binding sequence. Nucleic Acids Res 16:7119–7131

    PubMed  Google Scholar 

  • Love JD, Nguyen HT, Or A, Attri AK, Minton KW (1986) UV-induced interstrand cross-linking of d(GT)n d(CA)n is facilitated by a structural transition. J Biol Chem 261:10051–10057

    PubMed  Google Scholar 

  • Madura K, Prakash S (1990) Transcript levels of theSaccharomyces cerevisiae DNA repair geneRAD23 increase in response to UV light and in meiosis but remain constant in the mitotic cell cycle. Nucleic Acids Res 18:4737–4774

    PubMed  Google Scholar 

  • Madura K, Prakash S, Prakash L (1990) Expression of theSaccharomyces cerevisiae DNA repair geneRAD6 that encodes a ubiquitin conjugating enzyme, increases in response to DNA damage and in meiosis but remains constant during the mitotic cell cycle. Nucleic Acids Res 18:771–778

    PubMed  Google Scholar 

  • McClanahan T, McEntee K (1986) DNA damage and heat shock dually regulate genes inSaccharomyces cerevisiae. Mol Cell Biol 6:90–96

    PubMed  Google Scholar 

  • Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Naumowski L, Friedberg EC (1984)Saccharomyces cerevisiae RAD2 gene: isolation, subcloning, and partial characterisation. Mol Cell Biol 4:290–295

    PubMed  Google Scholar 

  • Naumowski L, Chu G, Berg P, Friedberg EC (1985)RAD3 gene ofSaccharomyces cerevisiae: nucleotide sequence of wild-type and mutant alleles, transcript mapping, and aspects of gene regulation. Mol Cell Biol 5:17–26

    PubMed  Google Scholar 

  • Perozzi G, Prakash S (1986)RAD7 gene ofSaccharomyces cerevisiae: transcripts, nucleotide sequence analysis, and functional relationship between theRAD7 andRAD23 gene products. Mol Cell Biol 6:1497–1507

    PubMed  Google Scholar 

  • Peterson TA, Prakash L, Osley MA, Reed SI (1985) Regulation ofCDC9, theSaccharomyces cerevisiae gene that encodes DNA ligase. Mol Cell Biol 5:226–235

    PubMed  Google Scholar 

  • Richter D, Niegemann E, Brendel M (1992) Molecular structure of the DNA cross-link repair geneSNM1 (PSO2) of the yeastSaccharomyces cerevisiae. Mol Gen Genet 231:194–200

    PubMed  Google Scholar 

  • Richter D (1992) Molekulargenetische Strukturanalysen am DNA-ReparaturgenSNM1 beiSaccharomyces cerevisiae. Ph.D. Thesis, J.W. Goethe-Universität, Frankfurt am Main, FRG

    Google Scholar 

  • Roberts JG (1978) The repair of DNA modified by cytotoxic, mutagenic and carcinogenic chemicals. Adv Radiat Biol 9:211–235

    Google Scholar 

  • Robinson GW, Nicolet CM, Kalainov D, Friedberg EC (1986) A yeast excision-repair gene is inducible by DNA damaging agents. Proc Natl Acad Sci USA 83:1842–1846

    PubMed  Google Scholar 

  • Ruhland A, Brendel M (1979) Mutagenesis by cytostatic alkylating agents in yeast strains of differing repair capacities. Genetics 92:83–97

    PubMed  Google Scholar 

  • Ruhland A, Kircher M, Wilborn F, Brendel M (1981) A yeast mutant specifically sensitive to bifunctional alkylation. Mutation Res 91:457–462

    Article  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual (2nd edn) Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Sancar GB (1985) Sequence of theSaccharomyces cerevisiae PHR1 gene and homology of thePHR1 photolyase to theE. coli photolyase. Nucleic Acids Res 13:8231–8246

    PubMed  Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    PubMed  Google Scholar 

  • Sebastian J, Kraus B, Sancar GB (1990) Expression of the yeastPHR1 gene is induced by DNA-damaging agents. Mol Cell Biol 10:4630–4637

    PubMed  Google Scholar 

  • Siede W, Brendel M (1982) Interactions among genes controlling sensitivity to radiation (RAD) and to alkylation by nitrogen mustard (SNM) in yeast. Curr Genet 5:33–38

    Article  Google Scholar 

  • Siede W, Friedberg EC (1992) Regulation of the yeastRAD2 gene: DNA damage-dependent induction correlates with protein binding to regulatory sequences and their deletion influences survival. Mol Gen Genet 232:247–256

    PubMed  Google Scholar 

  • Siede W, Robinson GW, Kalainow D, Malley T, Friedberg EC (1989) Regulation of theRAD2 gene ofSaccharomyces cerevisiae. Mol Microbiol 3:1697–1707

    PubMed  Google Scholar 

  • Treger JM, Heichman KA, McEntee K (1988) Expression of the yeastUBI4 gene increases in response to DNA-damaging agents and in meiosis. Mol Cell Biol 8:1132–1136

    PubMed  Google Scholar 

  • Watkins JF, Sung P, Prakash L, Prakash S (1993) TheSaccharomyces cerevisiae DNA repair geneRAD23 encodes a nuclear protein containing a ubiquitin-like domain required for biological function. Mol Cell Biol 13:7757–7765

    PubMed  Google Scholar 

  • Way JC, Davis MA, Morisato D, Roberts DE, Kleckner N (1984) New Tn10 derivatives for transposon mutagenesis and for construction oflacZ operon fusions by transposition. Gene 32:369–379

    Article  PubMed  Google Scholar 

  • Wilborn F, Brendel M (1989) Formation and stability of interstrand cross-links induced by cis- and trans-diaminedichloroplatinum(II) in the DNA ofSaccharomyces cerevisiae strains differing in repair capacity. Curr Genet 16:331–338

    Article  PubMed  Google Scholar 

  • Wolter R, Richter D, Niegemann E, Brendel M (1994) Molecular characterisation ofGTP1, aSaccharomyces cerevisiae gene encoding a small GTP-binding protein. Curr Genet 26:564–566

    Article  PubMed  Google Scholar 

  • Xiao W, Singh KK, Chen B, Samson L (1993) A common element involved in transcriptional regulation of two DNA alkylation repair genes (MAG andMGT1) ofSaccharomyces cerevisiae. Mol Cell Biol 13:7213–7221

    PubMed  Google Scholar 

  • Yagle K, McEntee K (1990) The DNA damage-inducible geneDIN1 ofSaccharomyces cerevisiae encodes a regulatory subunit of ribonucleotide reductase and is identical toRNR3. Mol Cell Biol 10:5553–5557

    PubMed  Google Scholar 

  • Zhou Z, Elledge SJ (1993)DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell 75:1119–1127

    Article  PubMed  Google Scholar 

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Communicated by C. P. Hollenberg

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Wolter, R., Siede, W. & Brendel, M. Regulation ofSNM1, an inducibleSaccharomyces cerevisiae gene required for repair of DNA cross-links. Molec. Gen. Genet. 250, 162–168 (1996). https://doi.org/10.1007/BF02174175

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  • DOI: https://doi.org/10.1007/BF02174175

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