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J Bacteriol, February 1998, p. 989-993, Vol. 180, No. 4
Department of Biological Sciences, University
of Alberta, Edmonton, Alberta T6G 2E9,1 and
Department of Biochemistry, University of Alberta, Edmonton,
Alberta T6G 2H7,2 Canada, and
Department
of Molecular and Human Genetics, Baylor College of Medicine,
Houston, Texas 770303
Received 25 June 1997/Accepted 14 December 1997
In vitro, the methyl-directed mismatch repair system of
Escherichia coli requires the single-strand exonuclease
activity of either ExoI, ExoVII, or RecJ and possibly a fourth, unknown
single-strand exonuclease. We have created the first precise null
mutations in genes encoding ExoI and ExoVII and find that cells lacking these nucleases and RecJ perform mismatch repair in vivo normally such
that triple-null mutants display normal mutation rates. ExoI, ExoVII,
and RecJ are either redundant with another function(s) or are
unnecessary for mismatch repair in vivo.
The methyl-directed mismatch repair
(MMR) system of Escherichia coli is a key enforcer of
genetic stability. The MMR system corrects DNA polymerase errors
(reviewed in reference 22) and prevents the
recombination of partially diverged DNA sequences (18, 19, 26,
39). E. coli strains lacking any essential component
of this system display a mutator phenotype in which mutation rates are
100- to 1,000-fold above normal (22, 30) and are better able
to recombine partially diverged DNA sequences (18, 26,
39). Both the elevated mutation rate and the relaxed sequence stringency of recombination of mutator strains may contribute to the pathogenicity of E. coli (14, 17).
Homologs of the E. coli MutS and MutL MMR proteins have been
identified in yeasts, mice, and humans and, as predicted from studies
with E. coli, their absence results in increased mutation,
genome instability, and, in mammals, cancer (reviewed in references
12, 23, and 24).
The molecular mechanism of methyl-directed MMR in E. coli,
as defined biochemically, includes the following steps (reviewed in
references 15, 22, 23, and 28).
Repair is initiated by the binding of MutS to the mismatch, of MutL to
MutS, and of MutH to a nearby d(GATC) sequence. An incision is made by
MutH 5' to the d(GATC) sequence on an unmethylated DNA strand. The nicked DNA strand is displaced by the coordinated activities of MutS,
MutL, and MutU (helicase II) and is degraded by exonucleases specific
for single-strand DNA. The exonuclease required depends on the position
of the incision relative to the mismatch: if the incision is located 3'
of the mismatch, repair requires the 3' to 5' exonucleolytic activity
of exonuclease I (ExoI) in a purified system and/or that of an
unidentified component in crude extracts (7); if the
incision is located 5' of the mismatch, repair requires the 5' to 3'
exonucleolytic activity of either RecJ or exonuclease VII
(ExoVII). The final steps in MMR require the activities of a
single-strand DNA-binding protein, DNA polymerase III, and DNA ligase
for filling the single-strand gap left by excision.
Of the components required biochemically, it is clear that MutS, MutL,
MutH, and MutU are also needed to perform their respective functions in
MMR in vivo. Null mutations in the genes encoding any one of these
disable MMR, resulting in cells displaying a mutator phenotype
(30-32) and decreased recombination sequence stringency
(18, 26, 39). For the single-strand exonucleases, their
roles in vivo have been less obvious, in part because of the absence of
precise null alleles of the genes encoding them. Razavy et al.
(27) constructed the first known precise null allele of the
gene encoding ExoI in E. coli, a deletion-insertion allele
called
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Mismatch Repair in Escherichia coli
Cells Lacking Single-Strand Exonucleases ExoI, ExoVII, and
RecJ
ABSTRACT
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xonA300::cat. Previous
E. coli alleles either are altered-function and dominant
alleles (e.g., sbcB15) (27), have not been
demonstrated to be null alleles (e.g., xonA2 and
xonA6) (25), or remove a large segment of the
E. coli chromosome such that phenotypes cannot be attributed
unambiguously to the lack of the ExoI-encoding gene
[(sbcB-his); cited in reference 7]. Similarly, for
ExoVII, the only previously known null alleles remove not only the
xseA gene encoding the enzyme's large subunit but also a
neighboring guanosine biosynthesis gene causing a guanosine requirement
(37). This could alter normal DNA metabolism, which could be
relevant to DNA MMR. A useful recJ-null allele has been described (16). Here we report the construction of the first precise null allele of ExoVII,
xseA18::amp (Table
1), and the first strains carrying
precise null mutations in genes encoding all three known E. coli single-strand-dependent exonucleases. These strains are
described and used to examine the role of the exonucleases in MMR in
vivo.
TABLE 1.
E. coli K-12 strains and plasmids
The viabilities of strains of two different genetic backgrounds carrying the null alleles of xonA, xseA, and recJ (Table 1) are normal (Table 2), and their growth curves are not markedly different from those of their Exo+ parents (Fig. 1). It was shown previously that strains defective for all three exonucleases display decreased homologous recombination and Chi activity when Chi stimulates recombination opposite heterologous DNA (27). The latter phenotype was observed only in the triple mutant and not in any of the double-exonuclease mutants. As predicted on the basis of their recombination-depressed phenotypes, our strains carrying the null alleles of xonA, xseA, and recJ also display elevated UV light sensitivity. In both genetic backgrounds, their sensitivities are greater than that of any of the single mutants and less than those of recA recombination-deficient strains (data not shown).
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Studies of MMR in vitro were inconclusive as to whether the absence of the three exonucleases should be sufficient to block MMR in cells. On the one hand, in a purified system, the presence of ExoVII or RecJ was required for MMR with a d(GATC) sequence 5' to the mismatch and ExoI was required for repair with the d(GATC) sequence 3' to the mismatch (7). ExoVII could not substitute for ExoI on 3' substrates in the purified system (7), despite the fact that ExoVII has been found to possess both 3' and 5' single-strand nuclease activity in other in vitro assays (5). On the other hand, in a crude system, MMR of 3' substrates occurred in extracts of cells lacking ExoI, leading the authors to suggest the possible existence of a fourth single-strand exonuclease in E. coli which substitutes for ExoI in their crude system (7). However, ExoVII was present in the crude extract lacking ExoI. Because the ability of ExoVII to digest 3' ends in the crude system is unknown, it remains possible that ExoVII was supporting the repair of 3' substrates.
In vivo studies in which recombination was assayed suggested links between the single-strand exonucleases and MMR (8, 9). The authors described MMR protein-dependent recombination of UV-irradiated DNA. They found that single- and double-exonuclease mutants display small decreases in the frequency of such recombination, indicating roles for these nucleases in either MMR, recombination, or both (8). Because single- and double-exonuclease mutants have since been shown to have similarly small decreases in their frequencies of normal (MMR-independent) recombination (20, 27), it now seems likely that recombination rather than MMR was inhibited by exonuclease deficiency in the previous study (8). The observation of single-strand DNA formation in nuclease-proficient cells, but not in cells deficient for one of the single-strand exonucleases (8), similarly cannot distinguish whether such single-strand DNA was an intermediate in MMR or recombination or in both processes or neither process.
To test whether single-strand exonucleases are required for MMR in vivo, we asked whether cells lacking ExoI, ExoVII, and RecJ display the mutator phenotype characteristic of MMR-deficient cells. For two separate E. coli K-12 strain backgrounds, we found that cells lacking ExoI, ExoVII, and RecJ displayed mutation rates similar to those of their xonA+ xseA+ recJ+ parents (Table 3). In contrast, isogenic strains lacking MutL, an essential component of MMR in vivo, showed greatly elevated mutation rates. Thus, the activities of ExoI, ExoVII, and RecJ appear not to be essential for MMR in vivo.
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Could the triple-exonuclease mutants be MMR deficient but fail to display the mutator phenotype? For example, it might be that ExoI, ExoVII, and RecJ are necessary and sufficient exonuclease activities for MMR in vivo but that triple-mutant cells initiating MMR die from accumulation of the nicked but not displaced DNA intermediate. This would kill those cells that experienced polymerase errors and so prevent a mutator phenotype. This possibility seems unlikely for two reasons. First, the viabilities of strains lacking ExoI, ExoVII, and RecJ are normal (Table 2), providing no evidence that those attempting MMR die. Second, mutU helicase mutants would be expected to accumulate a similar DNA intermediate (a nicked but not displaced strand) but these are viable and display a mutator phenotype (31, 32). This argues that failure to complete MMR after nicking is not a lethal event.
We will discuss three possible explanations for the results presented. First, another as yet uncharacterized exonuclease(s) may be sufficient for MMR. Cooper et al. (7) postulated that another exonuclease must contribute after they found repair of 3' but not 5' substrates in cells lacking ExoI and RecJ. If such an activity catalyzes MMR in vivo in our assay, then it is interesting that apparently normal levels of MMR can be accomplished with only this 3' nuclease.
Regardless of the polarity of a putative substituting nuclease(s), the existence of one or more is suggested by the discoveries of MMR-associated single-strand exonucleases in the yeasts Schizosaccharomyces pombe (34) and Saccharomyces cerevisiae (35). In these systems a single 5' single-strand-dependent exonuclease associates with (35) and/or is required for proper function of (34) the MMR apparatus.
There are two uncharacterized open reading frames in the E. coli genome sequence that contain conserved exonuclease motifs, although neither gene's product has been tested yet for nuclease function (13). Either of these or an as yet unidentified gene might supply a function that substitutes for that of ExoI, ExoVII, and RecJ exonucleases in MMR in vivo.
Second, it is formally possible that the three single-strand exonucleases are normally required for MMR in vivo and that cells lacking them do not show an in vivo mutator phenotype because their absence induces the expression of a new substituting activity. This idea could be tested by in vitro analysis of MMR in crude extracts of our triple-exonuclease-defective strains, as both the crude and purified in vitro MMR assays require exonuclease, at least when 5' substrates are used (7). If a new exonuclease-bypassing (or substituting) activity were expressed only in the triple mutant, one might expect 5' substrates to be repaired in crude extracts of the triple-exonuclease mutants, but not in double-mutant extracts, as was reported previously for 5' substrates (7). Also, any 3' substrate repair detected would be unambiguously independent of ExoVII.
One specific version of this general idea is addressed by data shown in Table 4. If the triple-nuclease-defective strain grew slowly or were inviable, then cells already harboring a secondary (suppressor) mutation might usually be selected when constructing triple-exonuclease mutants. When this kind of problem occurs, most cells receiving the deleterious mutation during the strain construction (the third nuclease allele in our constructions) are lost, and the rare suppressor-carrying mutants predominate among progeny that carry the deleterious mutation. This possibility was tested by determining the efficiency of recovering the third nuclease mutation in P1 transduction experiments in which the third nuclease mutation is introduced by selection for a nearby, linked marker rather than by direct selection. We find that there is no bias against recovering the third exonuclease mutation in double-exonuclease mutants, as compared with exonuclease-proficient strains (Table 4). This argues strongly against the presence of secondary suppressor mutations in triple-exonuclease-deficient strains.
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Finally, it could be that single-strand exonuclease activity is not required for MMR in vivo, even though it is required in vitro. Complete displacement of the unmethylated DNA strand by MutU helicase may be unfavorable in vitro, perhaps because the displaced single-strand DNA can reanneal. Exonuclease activity would then be required to degrade the displaced DNA strand. This requirement might be bypassed in vivo if MutU, MutS, and MutL could remove the unmethylated DNA strand completely. This might occur in vivo but not in vitro for any of several possible reasons including the following.
(i) In vivo, the displaced strand might not reanneal because it competes for reannealing with the (perfectly complementary) parental strand at the replication fork. A competitor strand is not provided in vitro.
(ii) A single nick was provided to direct MutU helicase in the experiments demonstrating nuclease requirements in vitro. Perhaps the normal in vivo substrate is a mismatch flanked by two nicks, making complete removal of the displaced strand possible without exonucleolytic digestion.
(iii) The displaced strand might be stabilized and prevented from reannealing in vivo by single-strand binding proteins or other activities or conditions that might not have been optimized in the in vitro systems.
With any of these possibilities, the single-strand exonucleases might still degrade the displaced single strand, but this would not be an obligate step in MMR.
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ACKNOWLEDGMENTS |
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We thank D. Berg for Kohara phage; H. J. Bull, S. Gottesman, P. J. Hastings, P. Modrich, H. Razavy, R. Sidhu, and an anonymous reviewer for comments on the manuscript; H. Razavy and S. Szigety for strain construction; C. Thulin for excellent technical assistance; and the E. coli Genetic Stock Center for strains.
This work was supported by grants from the National Cancer Institute of Canada, funded by the Canadian Cancer Society, from the Medical Research Council of Canada (MRC), and grant GM53158 from the National Institute of General Medical Sciences (United States). A graduate studentship (R.S.H.) and a postdoctoral fellowship (M.-J.L.) were provided by the Alberta Heritage Foundation for Medical Research, and R.S.H. held an Honorary Izaak Walton Killam Memorial Scholarship. S.M.R. was supported by MRC Scientist and Alberta Heritage Senior Medical Scholar awards.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030. Phone: (713) 798-6924. Fax: (713) 798-5386. E-mail: smr{at}bcm.tmc.edu.
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J Bacteriol, February 1998, p. 989-993, Vol. 180, No. 4
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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