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Involvement of umuDC ST genes in nitropyrene-induced -CG frameshift mutagenesis at the repetitive CG sequence in the hisD3052 allele of Salmonella typhimurium

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Abstract

Expression of the umuDC operon is required for UV and most chemical mutagenesis in Escherichia coli. The closely related species Salmonella typhimurium has two sets of umuDC-like operons, umuDC ST on the chromosome and samAB on a 60-MDa cryptic plasmid. The roles of theumuDC-like operons in chemically induced frameshift mutagenesis of the hisD3052 allele of S. typhimurium were investigated. Introduction of a pBR322-derived plasmid carrying umuDCST increased the rate of reversion of hisD3052, following treatment with 1-nitropyrene (1-NP) or 1,8-dinitropyrene (1,-8DNP) tenfold and fivefold, respectively, whereas it did not substantially increase the rate of reversion induced by other frameshift mutagens, i.e. 2-nitrofluorene (2NF) and 2-amino- 3-methyldipyrido[1,2-a:3 ′,2′-d]imi-dazole (Glu-P-1). Introduction of a pBR322-derived plasmid carrying samAB did not increase the incidence of reversion of hisD3052 observed with any of the mutagens examined. Deletion of umuDC STSubstantially lowered the reversion rate induced by l-NP or 1,8-DNP, but it did not affect reversion induced by 2-NF, Glu-P-1 or N-hydroxyacetylaminofluorene (N-OH-AAF). Deletion of samAB had little impact on reversion incidence induced by any of the five frameshift mutagens. DNA amplification using the polymerase chain reaction technique followed by restriction enzyme analysis using BssHII, suggested that the mutations induced by the five frameshift mutagens were all CG deletions at the CGCGCGCG sequence in hisD3052. These results suggest that umuDCST, but not samAB, is involved in the -2 frameshift mutagenesis induced by l-NP and 1,8-DNP at the repetitive CG sequence, whereas neither operon participates in induction of the same type of mutations by 2-NF, Glu-P-1 or N-OH-AAF.

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References

  • Andrews PJ, Quilliam MA, McCarry BE, Bryant DW, McCalla DR (1986) Identification of the DNA adduct formed by metabolism of 1,8-dinitropyrene in Salmonella typhimurium. Carcinogenesis 7:105–110

    Article  CAS  Google Scholar 

  • Battista JR, Nohmi T, Donnelly CE, Walker GC (1988) Role of UmuD and UmuC in UV and chemical mutagenesis. In: Friedberg EC, Hanawalt PC (eds) Mechanisms and consequences of DNA damage processing. Alan R. Liss, New York, pp 455–459

    Google Scholar 

  • Battista JR, Ohta T, Nohmi T, Sun W, Walker GC (1990) Dominant negative umuDmutations decreasing RecA-mediated cleavage suggest roles for intact UmuD in modulation of SOS mutagenesis. Proc Natl Acad Sci USA 87:7190–7194

    Article  CAS  Google Scholar 

  • Belguise-Valladier P, Maki H, Sekiguchi M, Fuchs RPP (1994) Effect of single DNA lesions on in vitro replication with DNA polymerase III holoenzyme: comparison with other polymerases. J Mol Biol 236:151–164

    Article  CAS  Google Scholar 

  • Bell DA, Levine JG, DeMarini DM (1991) DNA sequence analysis of revertants of the hisD3052 allele of Salmonella typhimurium TA98 using the polymerase chain reaction and direct sequencing: application to 1-nitropyrene-induced revertants. Mutat Res 252:35–44

    Article  CAS  Google Scholar 

  • Bintz R, Fuchs RPP (1990) Induction of −2 frameshift mutations within alternating GC sequences by carcinogens that bind to the C8 position of guanine residues: development of a specific mutation assay. Mol Gen Genet 221:331–338

    Article  CAS  Google Scholar 

  • Birnboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523

    Article  CAS  Google Scholar 

  • Bridges BA, Woodgate R (1985) Mutagenic repair in Escherichia coli: Products of the recA gene and of the umuD and umuC genes at different steps in UV-induced mutagenesis. Proc Natl Acad Sci USA 82:4193–4197

    Article  CAS  Google Scholar 

  • Burckhardt SE, Woodgate R, Scheuermann RH, Echols H (1988) UmuD mutagenesis protein of Escherichia coli: overproduction, purification, and cleavage by RecA. Proc Natl Acad Sci USA 85:1811–1815

    Article  CAS  Google Scholar 

  • Carlomagno MS, Chiariotti L, Alifano P, Nappo AG, Bruni CB (1988) Structure and function of the Salmonella typhimurium and Escherichia coli K-12 histidine operons. J Mol Biol 203:585–606

    Article  CAS  Google Scholar 

  • Donnelly CE, Walker GC (1989) groE mutants of Escherichia coli are defective in umuDC-dependent UV mutagenesis. J Bacteriol 171:6117–6125

    Article  CAS  Google Scholar 

  • Donnelly CE, Walker GC (1992) Coexpression of UmuD' with UmuC suppresses the UV mutagenesis deficiency of groE mutants. J Bacteriol 174:3133–3139

    Article  CAS  Google Scholar 

  • Echols H, Goodman MF (1991) Fidelity mechanism in DNA replication. Annu Rev Biochem 60:477–511

    Article  CAS  Google Scholar 

  • Eguchi Y, Ogawa T, Ogawa H (1988) Cleavage of bacteriophage and phi80 CI repressor by RecA protein. J Mol Biol 202:565–574

    Article  CAS  Google Scholar 

  • Elledge SJ, Walker GC (1983) Proteins required for ultraviolet light and chemical mutagenesis: identification of the products of the umuC locus of E. coli. J Mol Biol 164:175–192

    Article  CAS  Google Scholar 

  • Evans FE, Miller DW, Beland FA (1980) Sensitivity of the conformation of deoxyguanosine to binding at the C-8 position by N-acetylated and unacetylated 2-aminofluorene. Carcinogenesis 1:955–959

    Article  CAS  Google Scholar 

  • Foster PL, Groopman JD, Eisenstadt E (1988) Induction of base substitution mutations by aflatoxin B1 is MucAB dependent in Escherichia coli. J Bacteriol 170:3415–3420

    Article  CAS  Google Scholar 

  • Howard PC, Heflich RH, Evans FE, Beland FA (1983) Formation of DNA adducts in vitro and in Salmonella typhimurium upon metabolic reduction of the environmental mutagen 1-nitropyrene. Cancer Res 43:2052–2058

    CAS  PubMed  Google Scholar 

  • Isono K, Yourno J (1974) Chemical carcinogens as frameshift mutagens: Salmonella DNA sequence sensitive to mutagenesis by polycyclic carcinogens. Proc Natl Acad Sci USA 71:1612–1617

    Article  CAS  Google Scholar 

  • Kado CI, Liu ST (1981) Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 145:1365–1375

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kato T, Shinoura Y (1977) Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light. Mol Gen Genet 156:121–131

    CAS  PubMed  Google Scholar 

  • Kitagawa Y, Akaboshi E, Shinagawa H, Horii T, Ogawa H, Kato T (1985) Structural analysis of the umu operon required for inducible mutagenesis in Escherichia coli. Proc Natl Acad Sci USA 82:4336–4340

    Article  CAS  Google Scholar 

  • Koch WH, Cebula TA, Foster PL, Eisenstadt E (1992) UV mutagenesis in Salmonella typhimurium is umuDCdependent despite the presence of samAB. J Bacteriol 174:2809–2815

    Article  CAS  Google Scholar 

  • Koffel-Schwartz N, Fuchs RPP (1989) Genetic control of AAF-induced mutagenesis at alternating GC sequences: an additional role for RecA. Mol Gen Genet 215:306–311

    Article  CAS  Google Scholar 

  • Lambert IB, Napolitano RL, Fuchs RPP (1992) DNA adduct-induced stabilization of slipped frameshift intermediates within repetitive sequences: implications for mutagenesis. Proc Natl Acad Sci USA 90:5989–5993

    Google Scholar 

  • Lefevre JF, Fuchs RPP, Daune MP (1978) Comparative studies on the 7-iodo and 7-fluoro derivatives of N-acetoxy-N-2-acetylaminofluorene: binding sites on DNA and conformational change of modified deoxytrinucleotides. Biochemistry 17:2561–2567

    Article  CAS  Google Scholar 

  • Levin DE, Ames BN (1986) Classifying mutagens as to their specificity in causing the six possible transitions and transversions: a simple analysis using the Salmonella mutagenicity assay. Environ Mol Mutagen 8:9–28

    Article  CAS  Google Scholar 

  • Levin DE, Marnett LJ, Ames BN (1984) Spontaneous and mutagen-induced deletions: mechanistic studies in Salmonella tester strain TA 102. Proc Natl Acad Sci USA 81:4457–4461

    Article  CAS  Google Scholar 

  • Lindsley JE, Fuchs RPP (1994) Use of single-turnover kinetics to study bulky adduct bypass by T7 DNA polymerase. Biochemistry 33:764–772

    Article  CAS  Google Scholar 

  • Little JW (1984) Autodigestion of LexA and phage repressors. Proc Natl Acad Sci USA 81:1375–1379

    Article  CAS  Google Scholar 

  • Little JW, Edmiston SH, Pacelli LZ, Mount DW (1980) Cleavage of the Escherichia coli lexA protein by the recA protease. Proc Natl Acad Sci USA 77:3225–3229

    Article  CAS  Google Scholar 

  • Lodwick D, Strike P (1991) Distribution of sequences homologous to the impCAB operon of TP110 among bacterial plasmids of different incompatibility groups. Mol Gen Genet 229:27–30

    Article  CAS  Google Scholar 

  • Lodwick D, Owen D, Strike P (1990) DNA sequence analysis of the imp UV protection and mutation operon of the plasmid TP110: identification of a third gene. Nucleic Acids Res 18:5045–5050

    Article  CAS  Google Scholar 

  • Maenhaut-Michel G, Janel-Bintz R, Fuchs RPP (1992) A umuDC-independent SOS pathway for frameshift mutagenesis. Mol Gen Genet 235:373–380

    Article  CAS  Google Scholar 

  • Maron DM, Ames BN (1983) Revised methods for the Salmonella mutagenicity test. Mutat Res 113:173–215

    Article  CAS  Google Scholar 

  • McCann J, Spingarn NE, Kobori J, Ames BN (1975) Detection of carcinogens as mutagens: bacterial tester strains with R-factor plasmids. Proc Natl Acad Sci USA 72:979–983

    Article  CAS  Google Scholar 

  • Miller JH (1992) A short course in bacterial genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Murli S, Walker GC (1993) SOS mutagenesis. Curr Opinion Genet Dev 3:719–725

    Article  CAS  Google Scholar 

  • Nohmi T, Battista JR, Dodson LA, Walker GC (1988) RecA-mediated cleavage activates UmuD for mutagenesis: mechanistic relationship between transcriptional derepression and posttranslational activation. Proc Natl Acad Sci USA 85:1816–1820

    Article  CAS  Google Scholar 

  • Nohmi T, Hakura A, Nakai Y, Watanabe M, Murayama SY, Sofuni T (1991) Salmonella typhimurium has two homologous but different umuDC operons: cloning of a new umuDC-like operon (samAB) present in a 60-megadalton cryptic plasmid of S. typhimurium. J Bacteriol 173:1051–1063

    Article  CAS  Google Scholar 

  • Nohmi T, Yamada M, Watanabe M, Murayama SY, Sofuni T (1992) Roles of Salmonella typhimurium umuDC and samAB in UV mutagenesis and UV sensitivity. J Bacteriol 174:6948–6955

    Article  CAS  Google Scholar 

  • Perry KL, Elledge SJ, Mitchell BB, Marsh L, Walker GC (1985) umuDC and mucAB operons whose products are required for UV light- and chemical-induced mutagenesis: UmuD, MucA, and LexA proteins share homology. Proc Natl Acad Sci USA 82:4331–4335

    Article  CAS  Google Scholar 

  • Rajagopalan M, Lu C, Woodgate R, O'Donnell M, Goodman MF, Echols H (1992) Activity of the purified mutagenesis proteins UmuC, UmuD′, and RecA in replicative bypass of an abasic DNA lesion by DNA polymerase III. Proc Natl Acad Sci USA 89:10777–10781

    Article  CAS  Google Scholar 

  • Sedgwick SG, Lodwick D, Doyle N, Crowne H, Strike P (1991) Functional complementation between chromosomal and plasmid mutagenic DNA repair genes in bacteria. Mol Gen Genet 229:428–436

    Article  CAS  Google Scholar 

  • Shinagawa H, Kato T, Ise T, Makino K, Nakata A (1983) Cloning and characterization of the umu operon responsible for inducible mutagenesis in Escherichia coli. Gene 23:167–174

    Article  CAS  Google Scholar 

  • Shinagawa H, Iwasaki H, Kato T, Nakata A (1988) RecA proteindependent cleavage of UmuD protein and SOS mutagenesis. Proc Natl Acad Sci USA 85:1806–1810

    Article  CAS  Google Scholar 

  • Slilaty SN, Little JW (1987) Lysine-156 and serine-119 are required for LexA repressor cleavage: a possible mechanism. Proc Natl Acad Sci USA 84:3987–3991

    Article  CAS  Google Scholar 

  • Smith CM, Eisenstadt E (1989) Identification of a unmDClocus in Salmonella typhimuriumLT2. J Bacteriol 171:3860–3865

    Article  CAS  Google Scholar 

  • Smith CM, Koch WM, Franklin SB, Foster PL, Cebula TA, Eisenstadt E (1990) Sequence analysis and mapping of the Salmonella typhimurium LT2 umuDC operon. J Bacteriol 172:4964–4978

    Article  CAS  Google Scholar 

  • Steinborn G (1978a) Uvm mutants of Escherichia coli K12 deficient in UV mutagenesis. I. Isolation of uvm mutants and their phenotypical characterization in DNA repair and mutagenesis. Mol Gen Genet 165:87–93

    Article  CAS  Google Scholar 

  • Steinborn G (1978b) Uvm mutants of Escherichia coliK12 deficient in UV mutagenesis. II. Further evidence for a novel function in error-prone repair. Mol Gen Genet 175:203–208

    Article  Google Scholar 

  • Streisinger G, Owen J (1985) Mechanisms of spontaneous and induced frameshift mutation in bacteriophage T4. Genetics 109:633–659

    CAS  PubMed  PubMed Central  Google Scholar 

  • Streisinger G, Okada Y, Emrich J, Newton J, Tsugita A, Terzaghi E, Inouye M (1966) Frameshift mutations and the genetic code. Cold Spring Harbor Symp Quant Biol 31:77–89

    Article  CAS  Google Scholar 

  • Takagi S, Kimura M, Katsuki M (1993) Direct sequencing of PCR products using unlabeled primers. BioTechniques 14:218–221

    CAS  PubMed  Google Scholar 

  • Thomas SM, Sedgwick SG (1989) Cloning of Salmonella typhimurium DNA encoding mutagenic DNA repair. J Bacteriol 171:5776–5782

    Article  CAS  Google Scholar 

  • Thomas SM, Crowne HM, Pidsley SC, Sedgwick SG (1990) Structural characterization of the Salmonella typhimurium LT2 umu operon. J Bacteriol 172:4979–4987

    Article  CAS  Google Scholar 

  • Urios A, Herrera G, Aleixandre V, Sommer S, Blanco M (1994) Mutability of Salmonella tester strains TA1538 (hisD3052) and TA1535 (hisG46) containing the UmuD' and UmuC proteins of Escherichia coli. Environ Mol Mutagen 23:281–285

    Article  CAS  Google Scholar 

  • Walker GC (1984) Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol Rev 48:60–93

    CAS  PubMed  PubMed Central  Google Scholar 

  • Watanabe M, Ishidate M Jr, Nohmi T (1989) A sensitive method for the detection of mutagenic nitroarenes: construction of nitroreductase-overproducing derivatives of Salmonella typhimurium strains TA98 and TA100. Mutat Res 216:211–220

    Article  CAS  Google Scholar 

  • Witkin EM (1976) Ultraviolet mutagenesis and inducible DNA repair in Escherichia coli. Bacteriol Rev 40:869–907

    CAS  PubMed  PubMed Central  Google Scholar 

  • Woodgate R, Rajagopalan M, Lu C, Echols H (1989) UmuC mutagenesis protein of Escherichia coli: purification and interaction with UmuD and UmuD'. Proc Natl Acad Sci USA 86:7301–7305

    Article  CAS  Google Scholar 

  • Woodgate R, Levine AS, Koch WK, Cebula TA, Eisenstadt E (1991) Induction and cleavage of Salmonella typhimurium UmuD protein. Mol Gen Genet 229:81–85

    CAS  PubMed  Google Scholar 

  • Yamada M, Hakura A, Sofuni T, Nohmi T (1993) New method for gene disruption in Salmonella typhimurium: construction and characterization of an ada-deletion derivative of Salmonella typhimurium TA1535. J Bacteriol 175:5539–5547

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Division of Genetics and Mutagenesis, National Institute of Health Sciences, 1-18-1 Kamiyoga, 158, Setagaya-ku, Tokyo, Japan

    Takehiko Nohmi, Masami Yamada, Michiko Matsui, Keiko Matsui, Masahiko Watanabe & Toshio Sofuni

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  1. Takehiko Nohmi
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  2. Masami Yamada
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  3. Michiko Matsui
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  4. Keiko Matsui
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  5. Masahiko Watanabe
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  6. Toshio Sofuni
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Communicated by R. Devorek

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Nohmi, T., Yamada, M., Matsui, M. et al. Involvement of umuDC ST genes in nitropyrene-induced -CG frameshift mutagenesis at the repetitive CG sequence in the hisD3052 allele of Salmonella typhimurium . Molec. Gen. Genet. 247, 7–16 (1995). https://doi.org/10.1007/BF00425816

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