Mutagenesis, Vol. 15, No. 2, 121-125,
March 2000
© 2000 UK Environmental Mutagen Society/Oxford University Press
Spontaneous and osmium tetroxide-induced mutagenesis in an Escherichia coli strain deficient in both endonuclease III and endonuclease VIII
Biological Institute, Graduate School of Science, Tohoku University, Sendai 980-8578 and 1 Department of Radiology, School of Veterinary Medicine, University of Osaka Prefecture, Sakai 599-8531, Japan
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Abstract |
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Thymine glycol, uracil glycol, 5-hydroxycytosine and 5-hydroxyuracil are common base lesions produced by cellular metabolism as well as ionizing radiation and environmental carcinogens. Escherichia coli DNA glycosylase, endonuclease III and endonuclease VIII recognize and remove these lesions from DNA. In this study, we assessed the mutagenic potential of these lesions in the supF gene as a forward mutation target in double-stranded plasmid DNA using an E.coli strain deficient in both endonuclease III and endonuclease VIII. These lesions were introduced into pTN89 DNA by the chemical oxidant osmium tetroxide. Spontaneous supF mutations occurred at a frequency of 3.03x10–7 and osmium tetroxide-induced at a frequency of 8.25x10–7. Sequence analysis of supF mutants revealed that mutations occurred at cytosine sites rather than thymine sites, suggesting that thymine glycol is not the principal premutagenic lesion. In contrast, G:C
A:T transitions were dominantly detected in the spontaneous and osmium tetroxide-induced mutations in the endonuclease III and endonuclease VIII double defective host. In this case, products of cytosine oxidation such as 5-hydroxycytosine, which are the substrate for endonuclease III and endonuclease VIII, were the principal mutagenic lesions. |
Introduction |
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Reactive oxygen species (ROS) and the oxidative DNA damage produced by ROS are involved in cellular processes such as mutagenesis, carcinogenesis and aging (Ames, 1983
; Ames et al., 1993; Yamamoto et al., 1997). ROS are generated in cells by ionizing radiation, a variety of chemical agents and normal metabolism, and thus oxidative DNA damage contributes to both spontaneous and induced mutations. Of the many types of oxidative DNA damage known, 8-hydroxyguanine is a well-investigated purine lesion which mispairs with adenine during DNA replication to induce G:CT:A transversion mutations (Kasai and Nishimura, 1984; Wood et al., 1990; Shibutani et al., 1991; Cheng et al., 1992; Moriya, 1993). 8-Hydroxyguanine residues in DNA can be removed by an enzyme encoded by the mutM gene of Escherichia coli to prevent G:CT:A transversion mutations (Chung et al., 1991; Michaels et al., 1991; Bessho et al., 1992).
ROS can also attack pyrimidines and generate various pyrimidine modifications (Gajewski et al., 1990; Boiteux et al., 1992). The 5,6 double bonds of pyrimidines are vulnerable to ROS attack, and for thymine, 5,6-dihydroxy-5,6-dihydrothymine (thymine glycol) is formed. A major product of ROS attack on cytosine is 5,6-dihydroxy-5,6-dihydrocytosine (cytosine glycol), which is unstable and hydrates to form 5-hydroxycytosine (5-OHC) or deaminates to form uracil glycol, which can further dehydrate to form 5-hydroxyuracil (5-OHU).
Oxidized base lesions are repaired by a process called base excision repair (Demple and Harrison, 1994). Principal activities in E.coli that recognize oxidative pyrimidines are endonuclease III (endoIII) and endonulcease VIII (endoVIII) (Demple and Harrison, 1994; Jiang et al., 1997a,b; Saito et al., 1997). If the lesion is not repaired prior to DNA replication, it can either block DNA polymerase and thus be potentially lethal or it can be bypassed by DNA polymerase and be potentially mutagenic. Of the pyrimidine base modifications mentioned above, thymine glycol has been shown to be a potent blocker of DNA synthesis in vitro (Ide et al., 1985; Clark and Beardsley, 1989) and thus to be a potentially lethal lesion. Other pyrimidine products such as uracil glycol, 5-OHC and 5-OHU do not block DNA synthesis in vitro (Ide et al., 1991; Purmal et al., 1994) or in vivo (Feig et al., 1994) and are easily bypassed. 5-OHC and 5-OHU have been shown to be mutagenic in E.coli (Feig et al., 1994; Purmal et al., 1994).
With regard to thymine glycol mutagenicity, Hayes et al. (1988) demonstrated that osmium tetroxide (OsO4)-treated single-stranded M13 DNA transfected into wild-type E.coli showed a bias for mutation at cytosine sites rather than thymine sites, indicating that thymine glycol is not responsible for OsO4 mutagenesis. OsO4 is a well-known chemical oxidant that induces thymine glycols (Dizdaroglu et al., 1986). On the other hand, Basu et al. (1989) observed that single-stranded M13 DNA containing one thymine glycol at a unique site showed TC transitions, implying that thymine glycol is mutagenic. These authors, however, observed that thymine glycol was not detectably mutagenic in double-stranded DNA.
Thymine glycol is repaired by the E.coli endoIII and endoVIII enzymes, which are encoded by the nth and nei genes, respectively. An E.coli nth nei double mutant is hypersensitive to X-rays and exhibits a spontaneous mutator phenotype with 20-fold higher mutation frequency as measured by rifampin sensitivity (Jiang et al., 1997a; Saito et al., 1997). This double mutant is also extremely sensitive to H2O2 and shows an 8.4-fold higher spontaneous mutation frequency in Arg+ His+ revertants (Saito et al., 1997). X-rays and H2O2 are both exogenous sources of ROS generation and introduce thymine glycol in DNA molecules with other types of damage (Boiteux et al., 1992). Thus, thymine glycol may be involved in the increase in mutation frequency in nth nei double mutants. We investigated the mutagenic potential of thymine glycol using an E.coli nth nei double mutant as the host strain. We evaluated the mutation frequency and analyzed the mutation spectrum of the E.coli supF gene in the plasmid pTN89 (Obata et al., 1998) for spontaneous and OsO4-induced events. We also observed the LacZ+ reversion mutation spectrum using the CC101–CC106 F' system (Cupples and Miller, 1989). We found that G:CA:T transitions occurred predominantly in the three assay systems. Our observations therefore suggested that thymine glycol is not a mutagenic lesion and that the nth nei double mutant is a G:CA:T transition mutator, probably because of a repair defect of uracil glycol, 5-OHC and 5-OHU.
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Materials and methods |
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Bacterial strains and plasmids
Escherichia coli NKJ1004 (Saito et al., 1997
) and NKJ2004 (Shimamura et al., 1997) were used for mutagenesis experiments. NKJ1004 is a derivative of AB1157 (Howard-Flanders et al., 1966) and has the alleles 
nth::Cm and nei::Km. SY5 is an F'-negative derivative of JM107 (Yanisch-Perron et al., 1985). NKJ2002, NKJ2003 and NKJ2004 are derivatives of SY5 and have the alleles nth::Cm, nei::Km and nth::Cm nei::Km, respectively. The F episome from strains CC101–CC106, derived from P90C (Cupples and Miller, 1989), was transferred to SY5, NKJ2002, NKJ2003 and NKJ2004. Each strain carries a different lacZ– mutation at codon 461, which reverts to GAC (specifying glutamic acid) via a specific base substitution in each case (see also Figure 1). Only glutamic acid at position 461 results in the Lac+ phenotype. Escherichia coli KS40 (lacZam gyrA rpsL) (Akasaka et al., 1992), derived from MBM7070 (Seidman et al., 1985), harbors pOF105 (Obata et al., 1998) which carries the gyrAam and rpsLam genes in the pACYC plasmid and is designated KS40/pOF105. Escherichia coli XL1-BlueMRF' (Stratagene) was used as the host for M13KO7, which was used to prepare single-stranded DNA for DNA sequencing. Plasmid pTN89 carries the E.coli supF and ampicillin resistance genes, f1 replication origin and SV40 T antigen (Obata et al., 1998).
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Media and reagents
Luria-Bertani (LB) broth, LB plates, minimal glucose plates, minimal lactose plates, M9 medium and phosphate buffer were used as described previously (Kobayashi et al., 1998
; Obata et al., 1998). The amino acids proline, threonine, leucine, histidine and arginine (each at 100 µg/ml) were included if necessary in M9 medium, minimal glucose plates and minimal lactose plates. Nalidixic acid (Nal), streptomycin (Sm), ampicillin (Ap) and chloramphenicol (Cm) were included if necessary in medium at concentrations of 50, 100, 150 and 30 µg/ml, respectively. Enzymes and reagents used for DNA manipulation and DNA sequencing were purchased from TaKaRa Biomedicals Co. (Kyoto, Japan) and Applied Biosystems Inc. (Foster City, CA). Osmium tetroxide (OsO4) was purchased from Nakalai Tesque Co. (Kyoto, Japan). The oligonucleotide 5'-GTACACGAGGCCCTT-3' used as the primer for DNA sequencing was purchased from Sawady Technology Co. Ltd (Tokyo, Japan).
Mutational specificity test using strains CC101–CC106
Five or more independent cultures of SY5, NKJ2002, NKJ2003 and NKJ2004 carrying F' derived from CC101–CC106 were grown overnight in M9 medium. The cells were washed by centrifugation, then serial dilutions were made. Appropriate dilutions were plated on minimal lactose plates for Lac+ reversion assay and minimal glucose plates to count the number of viable cells. The viable cells were counted after 2 days incubation at 37°C, and Lac+ revertants were counted after 3 days.
Treatment of plasmid pTN89 with OsO4
pTN89 (5.52 µg in TE buffer consisting of 10 mM Tris–HCl, pH 7.6, 1 mM EDTA, pH 8.0) was treated with 0.5 and 1.0% OsO4 at 65°C for 10 min (Kow and Wallace, 1987). The reaction was terminated by keeping on ice for 1 min and the plasmid was collected by chromatography on DE-52 (Whatman, Fairfield, NJ) eluted with 2 M NaCl. Following ethanol precipitation, oxidized DNA was resuspended in TE buffer. To determine whether plasmids contained thymine glycol, DNA was incubated with E.coli endoIII, which had been purified as described (Asahara et al., 1989), in 20 µl reaction mixtures containing 10 mM Tris–HCl, pH 7.5, 1 mM EDTA, pH 8.0, 100 mM NaCl for 30 min at 37°C, and conversion of form I pTN89 to open circular form II was determined by electrophoresis on 0.7% agarose gels.
Transfection and supF mutant analysis
pTN89 treated or untreated with OsO4 was introduced into NKJ1004 (nth nei) by electroporation and the cells were grown at 37°C overnight in 2.5 ml of LB broth supplemented with Ap to allow processing and replication of the plasmids and the progeny plasmids were extracted from the cells. Progeny plasmids derived from individual transfectants were assayed separately for mutant supF genes to distinguish mutations that occurred from normal siblings. KS40/pOF105 cells were transformed with the plasmid extracted from NKJ1004 by electroporation and transformants with mutant supF were plated on minimal glucose plates containing Nal, Sm, Ap and Cm (Obata et al., 1998). The total number of transformants was determined by plating a portion of the cells on LB plates containing Ap and Cm after overnight incubation at 37°C. Strain KS40/pOF105 is resistant to Sm and Nal if it contains a mutant supF, whereas cells carrying an active supF do not produce colonies on such plates. The minimal glucose plates were incubated at 37°C for 24 h. Sm- and Nal-resistant colonies were restreaked on LB plates containing X-gal and IPTG, and one of the white colonies was picked for further analysis. Mutation frequency was calculated according to Akasaka et al. (1992).
DNA sequencing
Plasmid DNA was extracted from a putative supF mutant transformant and transfected into XL1-BlueMRF' where single-stranded DNA was prepared by infection with M13KO7 helper phage. DNA was sequenced by the dideoxy chain termination method using an automated sequencer model 373A (Applied Biosytems Inc., Foster City, CA). The polymerization reaction was primed with the appropriate primer.
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Results |
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Characterization of lacZ reversion mutations in an nth nei double mutant strain
We recently reported the weak mutator phenotype of the nth nei double mutant of E.coli, which has almost no thymine glycol glycosylase activity, using simultaneous reversion from argE his-6 to Arg+ His+ (Saito et al., 1997
). This mutation has been shown to arise only from G:CA:T transitions (Ruiz-Rubio et al., 1988). In other words, reversion from argE his-6 to Arg+ His+ can never detect A:T site mutagenesis. Therefore, it has not been determined whether thymine glycol is a mutagenic lesion in vivo. In this study, the mutator phenotype of an nth nei double mutant was investigated using the CC101–CC106 F' lacZ reversion system (Cupples and Miller, 1989). As shown in Figure 1
, a strain that lacks both endoIII and endoVIII specifically stimulated the G:CA:T transition. This stimulation was also seen in the nth allele, suggesting involvement of endoIII in the G:CA:T transition. This result is consistent with the observations reported previously by ourselves (Saito et al., 1997) and others (Cunningham and Weiss, 1985) demonstrating that nth or nth nei mutants showed a weak mutator phenotype of G:CA:T transitions. On the other hand, the results presented in Figure 1 show that the nth, nei and nth nei strains did not stimulate A:T site reversions at coding position 461 in the lacZ gene. In the following experiments, we examined whether A:T site mutations occurred in the forward mutation system in NKJ1004 (nth nei) cells.
Inactivation of double-stranded plasmid DNA by OsO4
The double-stranded DNA of plasmid pTN89 was treated with 0, 0.5 or 1.0% OsO4 at 65°C for 10 min. OsO4 can react with thymine and thymine glycol constitutes 85% or more of the modified thymines (Dizdaroglu et al., 1986). To confirm the formation of endoIII-sensitive sites, including thymine glycol, in these treatments we digested plasmids with E.coli endoIII, separated the products on 0.7% agarose gels and observed the conversion of form I pTN89 to open circular form II (data not shown). Inactivation of OsO4-treated plasmid was tested in transfection assays, using competent AB1157 and NKJ1004 (nth nei) cells. Figure 2 shows that the dose-dependent inactivation of Ap-resistant transformants was increased in NKJ1004, indicating the lethal effects of thymine glycol.
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) or NKJ1004 nth nei (
). Points represent the means with standard errors from three to five independent experiments.OsO4-induced mutagenesis in NKJ1004 cells
supF mutations were monitored in NKJ1004 cells. The plasmid pTN89 carrying the supF gene was treated with 0, 0.5 and 1.0% OsO4 and transfected into NKJ1004 cells. The transformants were cultured in LB broth containing Ap overnight. The plasmids were extracted from individual overnight cultures and supF mutants were selected using the KS40/pOF105 system (Obata et al., 1998
). supF mutation frequencies for 0, 0.5 and 1.0% treatment were 3.03 ± 2.65x10–7, 5.85 ± 1.04x10–7 and 8.25 ± 3.06x10–7, respectively. Thus, 1% OsO4 can induce ~2.7-fold supF mutation in NKJ1004. supF mutation frequency in the nth+ nei+ strain KS40 was 3.06x 10–7 (Akasaka et al., 1992). Thus, as far as supF mutation is concerned, NKJ1004 is not even a weak mutator.
Sequence specificities of spontaneous and 1% OsO4-induced supF mutations in NKJ1004 cells
We collected 47 spontaneous and 65 OsO4-induced supF mutants and the specificity was determined by DNA sequencing. The sequence alterations detected are summarized in Tables I and II. In both cases, >90% of mutations were base substitutions.
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The spontaneous base substitutions in NKJ1004 were comprised of three types: G:C
A:T, G:CC:G and G:CT:A, in that order. No mutations at A:T sites were observed. OsO4-induced supF base substitutions in NKJ1004 were also comprised of G:CA:T, G:CC:G and G:CT:A. No mutations at A:T sites were observed. In both cases, G:CA:T transition was the most common base substitution, accounting for 45% of spontaneous and 61% of OsO4-induced supF mutations. Base substitutions in NKJ1004 constituted 94% of the spontaneous and 91% of the OsO4-induced supF mutations (Table I). The frequency of G:CA:T transition in NKJ1004 was, therefore, 3.03x10–7x0.94x0.45 = 1.28x10–7 for spontaneous cases and 8.25x10–7x0.91x0.61 = 4.58x10–7 for OsO4-induced cases. A predominance of mutations at G:C sites was also seen in spontaneous supF mutations in wild-type E.coli (Table II; ref. 31). However, in the wild-type strain, G:CT:A was predominant (46%), followed by G:CC:G (27%) and G:CA:T (12%). The frequency of G:CA:T transition was 3.06x10–7x0.64x0.12 = 0.24x10–7. Thus, nth nei stimulates G:CA:T transitions.
Figure 3 shows the site distribution of base substitution mutagenesis in NKJ1004 in the supF gene of pTN89. There were no marked differences in site distribution between spontaneous and OsO4-induced supF mutations in NKJ1004. In both cases, base substitutions occurred at four mutational hot spots (positions 133C, 156G, 159G and 160G).
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Discussion |
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OsO4 reacts with thymine bases in DNA and thymine glycol accounts for >85% of modified thymines (Dizdaroglu et al., 1986
). Several previous studies have shown that thymine glycol exhibits lethality in vitro (Ide et al., 1985; Clark and Beardsley, 1989). Thymine glycol is repaired by E.coli endoIII and endoVIII, which are encoded by the nth and nei genes, respectively. A strain defective in both nth and nei is hypersensitive to X-rays and hydrogen peroxide. Therefore, thymine glycol has been suggested to be lethal in vivo (Jiang et al., 1997a; Saito et al., 1997). We found that OsO4-treated plasmids showed lower transfection efficiency in NKJ1004 (nth nei) than the wild-type strain (Figure 2), indicating that inactivation of the plasmid DNA by OsO4 treatment is due to thymine glycol.
We assessed the mutability of thymine glycol using a nth nei double mutant E.coli host totally deficient in thymine glycol glycosylases and a double-stranded plasmid carrying the supF gene as a target. As shown in Table II, base substitution mutations induced in OsO4-oxidized DNA showed G:CA:T, G:CC:G and G:CT:A, and no mutations were observed at thymine sites. The strong bias at cytosine sites was also seen in spontaneous base substitutions of supF in NKJ1004 cells (Table II). Hayes et al. (1988) previously demonstrated that OsO4-treated single-stranded M13 DNA transfected into wild-type E.coli showed a bias for occurrence at cytosine sites rather than thymine sites. Thus, in forward mutation assay systems, OsO4-induced base substitutions show a bias mainly toward cytosine sites but not thymine sites in the wild-type as well as nth nei strains. Essentially the same results that nth nei double mutation does not stimulate A:T site mutations but stimulates only G:CA:T transitions were obtained using the F episome of CC101–CC106 in NKJ2004 cells (Figure 1). These results indicate that lesions other than thymine glycol are responsible for the spontaneous and OsO4-induced mutagenesis in NKJ1004 and NKJ2004. We thus concluded that thymine glycol is not a major premutagenic lesion.
Although we found no evidence for mutagenesis at thymine glycols, we characterized the weak mutator phenotype of the nth nei double mutant. DNA sequence analysis of spontaneous forward mutations in the supF gene showed that the common base change in this strain was a G:CA:T transition (Table II). Essentially the same mutagenic specificity was observed for OsO4-induced forward mutation of the supF gene, which again gave G:CA:T transitions (Table II). Finally, reversion of the F episome mutant lacZ system in the nth nei strain stimulated only G:CA:T transition (Figure 1). In the F' experiment, we demonstrated that the nth defect alone showed a G:CA:T transition mutator effect but the nei defect alone did not (Figure 1). Similar results that nth nei is a G:CA:T transition mutator and OsO4 can induce G:CA:T transitions were reported previously (Jiang et al., 1997a; Saito et al., 1997; Hayes et al., 1988).
Cytosine glycol is a second major product of OsO4 (Dizdaroglu et al., 1986), which is unstable and dehydrates to form 5-OHC or deaminates to form uracil glycol, which can also dehydrate to form 5-OHU. 5-OHC is known to mispair with adenine in vitro (Purmal et al., 1994). Uracil glycol and 5-OHU pair with adenine (Purmal et al., 1994, 1998). As uracil glycol and 5-OHU are derived from cytosine, they are expected to be potent mutagenic lesions leading to G:CA:T transitions. 5-OHC, uracil glycol and 5-OHU are recognized and removed by endoIII and endoVIII (Jiang et al., 1997b; Hatahet et al., 1994). These biochemical characteristics of endoIII and endoVIII can be used to interpret the G:CA:T mutator phenotype of the nth mutant and the nth nei double mutant. As shown in Figure 1, the single nei mutant showed an increase in G:CA:T transitions. On the other hand, amplified amounts of endoVIII can suppress the G:CA:T mutator phenotype of the nth nei double mutant (Saito et al., 1997). Thus, in the nei mutant, endoIII is present at levels more than sufficient to repair the 5-OHC, uracil glycol and 5-OHU which lead to G:CA:T transitions. It was shown previously that most of the thymine glycol glycosylase activity in E.coli is due to expression of endoIII, and 10–40% to endoVIII (Cunningham and Weiss, 1985; Saito et al., 1997). Thus, the G:CA:T transitions observed in spontaneous and OsO4-induced mutants were due to oxidized cytosines such as 5-OHC, uracil glycol and 5-OHU.
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Acknowledgments |
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This research was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Culture, Japan.
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Notes |
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2 To whom correspondence should be addressed. Tel: +81 22 217 6706; Fax: +81 22 217 6706; Email: yamamot{at}mail.cc.tohoku.ac.jp
3 Present address: Department of Cell Biology, Graduate School of Medicine, Tohoku University, Sendai 980-8575, Japan
4 Present address: School of Environmental Science, Division of Science, Murdoch University, Murdoch, WA 6150, Australia
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Received on August 5, 1999; accepted on October 24, 1999.
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