Department of Molecular and Cellular Biology,
College of Medicine, Chang Gung University, Kwei-San, Tao-Yuan,
Taiwan
 |
INTRODUCTION |
Mutagenesis by UV irradiation is not
a passive process but rather requires the active participation of
cellular proteins other than those in the replication complex. In
Escherichia coli, mutagenesis by UV irradiation and many
carcinogens requires the induction of SOS regulons (18, 43).
This category of mutagenesis has been frequently referred to as SOS
mutagenesis.
SOS mutagenesis in E. coli has been shown to be dependent on
four genes, lexA, umuD, umuC, and
recA (reviewed in reference 10). The LexA
protein, encoded by lexA, is the repressor for SOS regulons
(17, 18). It inhibits transcription by binding to operator
sequences, called SOS boxes, located upstream of SOS genes
(18). The UmuD and UmuC proteins are encoded by the
umuD and umuC genes, which are organized in an
operon under the regulation of lexA (35). In
wild-type cells, UmuDC proteins are expressed at a low basal
concentration. Among the many SOS-regulated genes, only the
umuDC operon must be induced for SOS mutagenesis
(36). While induction of the umuDC operon is an
essential process in SOS mutagenesis, SOS mutagenesis also requires
that UmuD be cleaved to the active UmuD' form (1, 29, 34).
Two UmuD' molecules combine with one UmuC molecule to form a complex
named UmuD'C, which is required for SOS mutagenesis (3, 50).
RecA appears to play at least two roles in SOS mutagenesis; one is its
regulatory role. In response to an SOS-inducing treatment, such as UV
irradiation, RecA becomes activated and mediates or facilitates the
proteolytic cleavage of LexA at an Ala-Gly bond, thus inducing the
expression of umuDC and other SOS-regulated genes
(17). A second role of activated RecA in SOS mutagenesis is
promoting the proteolytic cleavage of UmuD at an Ala-Gly bond,
producing two protein fragments of which the larger, COOH-terminal
fragment (UmuD') is required for SOS mutagenesis (29, 34).
RecA has a third essential role in SOS mutagenesis (1, 7,
37): allowing translesion DNA replication, possibly by complexing
with UmuD'C (9). The mechanism by which RecA performs its
third function in SOS mutagenesis is presently unknown.
The recF (14), recO (16),
and recR (27, 28) genes were originally
identified as those affecting the RecF pathway of recombination in
E. coli. Mutations in recF, recO, or
recR conferred recombination-deficient and extremely
UV-sensitive phenotypes in both recB recC sbcA and
recB recC sbcB sbcC genetic backgrounds (14, 16, 27,
28). In the recBC+ sbcBC+
genetic background, mutations in recF, recO, or
recR produced deficiencies in plasmid recombination and in
the repair of DNA daughter-strand gaps and increased the cells'
sensitivity to UV irradiation, but the mutations did not appear to
reduce conjugational or transductional recombination (6, 16, 19,
20, 24, 39). The deficiency caused by recF,
recO, and recR mutations can be partially
suppressed by a common suppressor mutation for recF,
recA(Srf) (4, 42, 46). Accumulating genetic
evidence suggests that the recF, recO, and
recR gene products function at the same step of
recombination and postreplication repair (4, 19, 33, 39,
46). The biochemical properties of purified RecF, RecO, and RecR
have been studied. RecF binds to single-stranded DNA (ssDNA) and, in
the presence of ATP or ATP-
S, double-stranded DNA (dsDNA) (11,
25, 26) but does not appear to have any positive effect on
RecA-catalyzed reactions in vitro (25, 41). RecR has not
been shown to exhibit any biochemical activity by itself. An
interaction of RecR with RecO in the absence of any DNA or nucleotide
cofactor (40) and an ATP- and dsDNA-dependent interaction of
RecF and RecR (47) have been reported. RecO binds to both
ssDNA and dsDNA and can promote renaturation of complementary ssDNA
(23) and homologous pairing of ssDNA and superhelical dsDNA
(22). RecO interacts with RecR and Ssb (40). This
interaction is thought to help RecA adhere to Ssb-coated ssDNA,
overcoming the Ssb inhibition of joint molecule formation in vitro
(40, 41). More recently, RecF has been shown to interact
with RecO, and the existence of a RecF-RecO-RecR complex in vitro has
been demonstrated (13). The biochemical roles of the
RecF-RecO-RecR complex in DNA repair and recombination, however, remain
an open question.
The involvement of the recF, recO, and
recR genes in SOS induction and in UV-radiation mutagenesis
(UVM) has been investigated. Mutations in the recF,
recO, and recR genes delay the induction of
several SOS-regulated genes (12, 38, 48). Mutations in recF decrease UVM of ssDNA phages but have no effect on
reversion of chromosomal hisG4 mutations (5, 15).
The recR mutants are normal with regard to UV-induced
reversion of hisG4 and argE3 mutations
(27). To the best of our knowledge, there has been no report
on the involvement of the recO gene in UVM. We initiated a
study to investigate the effect of a recO mutation on
UV-induced reversion of trpE65, and much to our surprise, we
observed that recO mutants are grossly deficient in UVM. In
view of the fact that recF, recO, and
recR mutants have common phenotypes and that the
recF, recO, and recR gene products
function at the same step of recombination and postreplication repair,
this observation raises the question of whether recF and
recR mutants are deficient in the UV-induced reversion of
trpE65. In this work, the possible involvement of
recF, recO, recR, and other RecF
pathway recombination genes in UVM was investigated.
| |
MATERIALS AND METHODS |
Bacterial strains and media.
The bacterial strains used are
listed in Table 1. The construction of
these strains by transduction has been described (39). All
of the strains used in this study are isogenic; i.e., they differ only
in the genes being investigated. The plasmid pGW2122, which produces
truncated UmuD' (29), was kindly provided by G. Walker. The
supplemented minimal medium (SMM) and DTM buffer have been described
(45). The complex media used were Luria broth (1% tryptone,
0.5% yeast extract, and 1% NaCl) and YENB (0.75% yeast extract and
0.8% nutrient broth). Reversion of from the Trp
phenotype to the Trp+ phenotype was assayed in SMM
containing 200 µg of nutrient broth per ml. Media were solidified by
adding Difco Bacto Agar at 1.5%. Phosphate buffer contained
Na2HPO4 at 5.83 g/liter and
KH2PO4 at 3.53 g/liter and had a pH of 7.0.
UV irradiation.
The source (254 nm) and measurement of the
fluence rate of UV irradiation have been described (44).
Survival curves were determined and assays for mutagenesis were carried
out as previously described (31).
Quantitation of mutagenesis.
The UV radiation-induced mutant
frequency was calculated per average mutant selection plate according
to a rearranged version of the formula of Bridges (2):
MF = (Mx × 108)/(Sc × volume plated).
Mx is defined as Mt 
Mpo + M0 (1-SF), where
Mt is the number of mutant colonies arising from
irradiated cells on mutant selection plates, Mpo
is the number of mutant colonies arising from nonirradiated cells on
mutant-selection plates, M0 is the number of
mutant colonies arising from nonirradiated cells on plates lacking the
growth-limiting nutrient, SF is the surviving fraction of
irradiated cells, Mx is the number of
radiation-induced mutants per mutant selection plate, and
Sc is the number of CFU per milliliter in the
cell suspension. Data were generally compiled from three experiments
per UV radiation fluence, with four mutant selection plates and three
viability plates per fluence.
| |
RESULTS |
Effects of recF, recG, recJ,
recO, recQ, and recR mutations on
UV-induced reversion from the Trp phenotype to the
Trp+ phenotype.
The involvement of the
recF, recO, and recR genes in UVM was
examined by an assay for reversion from the Trp phenotype
(trpE65) to the Trp+ phenotype. For comparison,
we included three other RecF pathway genes, recG,
recJ, and recQ, in the study. Similar levels of
UV induction of Trp+ reversion were detected in
recJ, recG, and recQ mutants and the rec+ control, indicating that mutations in
recJ, recG, or recQ have no effect on
UVM (Fig. 1 and data not shown). On the
other hand, the recF, recO, and recR
mutants exhibited altered levels of UVM. As shown in Fig. 1, the levels
of UV-induced Trp+ reversion in these three mutants are
comparable to those of rec+ organisms at low
fluences of UV radiation, e.g., 0.4 J/m2 or lower. At
higher fluences of UV radiation, however, the number of UV-induced
revertants is greatly reduced.
View larger version (19K):
[in this window]
[in a new window]
|
FIG. 1.
UVM of E. coli uvrA155 strains to a
Trp+ phenotype. The reversion from a Trp
phenotype to a Trp+ phenotype was assayed as described in
Materials and Methods. At 1.2 J/m2, UVM was not detected
for strain VW32, VW40, or VW48. A value of 50 Trp+ mutants
per 108 survivors is indicated with an arrow. Symbols:  ,
EWRP-1A (rec+ uvrA155);  , VW32
(uvrA155 recR252);  , VW40 (uvrA155 recO1504);
 , VW48 (uvrA155 recF332); ×, VW101 (uvrA155
recG258). The data for strains VW75 (uvrA155 recJ284)
and VW150 (uvrA155 recQ63) (not shown) are essentially
congruent with those for strains EWRP-1A and VW101.
|
|
Effects of the lexA51(Def) mutation and UmuD' on UV
mutagenesis of recF, recO, and recR
mutants.
From what is known about SOS mutagenesis, a deficiency in
UVM may be caused by a deficiency in the induction of SOS regulons, in
the cleavage of UmuD to active UmuD', or in RecA's third function in
UVM. To determine if the observed deficiency in UVM of recF, recO, and recR mutants may be caused by a
deficiency in the induction of SOS regulons, we examined the effect of
lexA51(Def) (the lexA51 mutation which produces
defective LexA and allows cells to express SOS regulons constitutively)
on UVM of recF, recO, and recR
mutants. The presence of the lexA51 mutation has no effect
on UVM of recA+ cells (compare
rec+ in Fig. 1 with lexA51 in Fig.
2) and fails to restore normal UVM in
recF, recO, and recR mutants (Fig. 2),
indicating that the deficiency in UVM of recF,
recO, and recR mutants is not due to a failure to
express SOS regulons. To examine if the observed deficiency in UVM of
recF, recO, and recR mutants may be
caused by a deficiency in the proteolytic cleavage of UmuD, we
transformed a recombinant plasmid, pGW2122, into recF,
recO, recR, lexA51 recF, lexA51
recO, and lexA51 recR strains. The presence of pGW2122 failed to restore normal UVM in recF, recO, and
recR strains (data not shown) and in lexA51 recF,
lexA51 recO, and lexA51 recR strains (Fig.
3). Therefore, deregulation of SOS
regulons and supply of UmuD' are insufficient to restore normal UVM in
recF, recO, and recR mutants.
View larger version (17K):
[in this window]
[in a new window]
|
FIG. 2.
UVM of E. coli uvrA155 lexA51 strains to a
Trp+ phenotype. Experimental details were as described in
Materials and Methods. UVM was not detected for strain VW174 or VW175
at 1.2 J/m2. A value of 50 Trp+ mutants per
108 survivors is indicated with an arrow. Symbols: ,
EWRP-1 (uvrA155 lexA51); , VW174 (uvrA155 lexA51
recR252); , VW175 (uvrA155 lexA51 recO1504); ,
VW16 (uvrA155 lexA51 recF332).
|
|
View larger version (17K):
[in this window]
[in a new window]
|
FIG. 3.
Effect of UmuD' on UVM of E. coli uvrA155
lexA51 strains to a Trp+ phenotype. The plasmid
pGW2122 was transformed into strains EWRP-1, VW16, VW174, and VW175,
and the reversion from a Trp phenotype to a
Trp+ phenotype was assayed as described in Materials and
Methods. UVM was not detected for strain VW16/pGW2122, VW174/pGW2122,
or VW175/pGW2122 at 1.2 J/m2. A value of 50 Trp+ mutants per 108 survivors is indicated
with an arrow. Symbols: , EWRP-1/pGW2122; , VW174/pGW2122; ,
VW175/pGW2122; , VW16/pGW2122.
|
|
Effects of recA(Srf) mutations on UVM of
recF, recO, and recR mutants.
In addition to participating in the regulation of lexA
regulons and in the cleavage of UmuD, RecA has a third essential role in SOS mutagenesis (1, 7, 37). It is possible that the deficiency in UVM observed in recF, recO, and
recR mutants may be related to the third essential role of
RecA in SOS mutagenesis. The postreplication repair deficiency in
recF, recO, and recR mutants has been
previously shown to be partially suppressed by recA(Srf)
mutations, such as recA2020 (39, 45). To
determine if the recA(Srf) mutations may suppress the
deficiency of recF, recO, and recR
mutants in UVM, we examined the effect of the recA2020 mutation on UVM of these mutants. Interestingly, we observed that the
presence of the recA2020 mutation restored normal UVM in
these mutants (Fig. 4).
View larger version (16K):
[in this window]
[in a new window]
|
FIG. 4.
UVM of E. coli uvrA155 recA2020 strains to a
Trp+ phenotype. Experimental details were as described in
Materials and Methods. Symbols: , VW56 (uvrA155
recA2020); , VW55 (uvrA155 recA2020 recR252); ,
VW54 (uvrA155 recA2020 recO1504); , VW57 (uvrA155
recA2020 recF332).
|
|
| |
DISCUSSION |
In this work, we show that among the several RecF pathway genes
investigated in this study, only mutations in the recF,
recO, or recR gene produced a deficiency in
UV-induced reversion of tryE65. The deficiency in UVM caused
by recF, recO, and recR mutations appears to occur at higher fluences of UV radiation (Fig. 1). Derepression of the SOS regulon by lexA51(Def) and supply of
UmuD' failed to restore normal UVM in recF, recO,
and recR mutants (Fig. 2 and 3). Interestingly, the presence
of the recA2020 mutation restored normal UVM in
recF, recO, and recR mutants (Fig. 4). These results suggest that the recF, recO, and
recR genes do not act by affecting RecA's functions in the
induction of SOS regulons or in the cleavage of UmuD but may affect the
third role of RecA in UVM. Several speculations have been made on the
activities of RecA involved in its third role in UVM. These activities
include inhibition of the 3'-to-5' proofreading exonuclease of DNA
polymerase III (21), binding to small, single-stranded
regions of DNA (37), and directing the UmuD' and UmuC
proteins to the site of the lesion in DNA (1, 37, 49).
Recent studies on the biochemical functions of the RecF, RecO, and RecR
proteins suggest that RecF-RecO-RecR may help RecA displace Ssb at a
DNA daughter-strand gap, which was produced after replication of a
UV-damaged DNA template and, presumably, a DNA lesion for
postreplication repair and SOS repair (13, 40). The
multiprotein RecA-RecF-RecO-RecR-Ssb bound at the gapped DNA (13,
40) may form a presynaptic filament which initiates recombination
repair. Alternatively, the multiproteins bound at the gapped DNA may
help RecA complex with UmuD'C and allow translesion DNA synthesis to
take place. According to this postulate, the role of RecF-RecO-RecR in
UVM may be (i) to chaperone RecA to gapped DNA bound by Ssb so that
RecA can perform its third function in UVM or (ii) to moderate the
interaction of RecA with UmuD'C. Recent findings of a major role of
RecA in stabilizing Umu proteins in vivo (8) suggest the
alternative possibility that RecF-RecO-RecR may affect RecA's ability
to stabilize Umu proteins.
Our results indicating an involvement of the recF,
recO, and recR genes in UVM are inconsistent with
the previous observations that recF and recR
mutants are normal in regard to UVM (15, 27). This
discrepancy may be attributed to the differences in the reversion
assays and/or the genetic backgrounds of parent strains used. The
hisG4 and argE3 mutations in K-12 strain
AB1157's genetic background were employed in the previous reversion
studies, while the trpE65 mutation in the EWRP-1A (a K-12
and B hybrid) genetic background was used in the present study. All of
the hisG4, argE3, and trpE65 mutations
are known to be ochre nonsense mutations (32), yet the
precise molecular base change in each of these mutations is not known,
to the best of our knowledge. We have transduced the trpE65
mutation into a uvrA recF143 strain of AB1157 and have
observed that the recF143 mutation reduced UV-induced reversion of trpE65 (data not shown). This result suggests
that it is the different mutations used in the reversion assay which account for the observed difference. However, systematic studies on the
effect of recF, recO, and recR
mutations on the UV-induced reversions of hisG4 in the
EWRP-1A genetic background and trpE65 in the AB1157 genetic
background are needed to provide a definite answer.
There are several questions that need to be addressed even when the
above discrepancy is resolved. First, why do mutations in
recF, recO, and recR produce a
deficiency in UV-induced reversion of trpE65 but not in that
of hisG4 or argE3? Second, why can
recA2020, which only partially suppresses both the UV
sensitivity and the postreplication repair deficiency of
recF, recO, and recR mutants (39,
45), fully restore the normal UVM of recF,
recO, and recR mutants (Fig. 4)? We offer the
following speculations based on the known defects caused by
recF, recO, and recR mutations. The
fact that mutations in the recF, recO, and
recR genes are known to produce a 50% deficiency in the
repair of DNA daughter-strand gaps (30, 39, 44) suggests
that half of the repair of DNA daughter-strand gaps does not require
the participation of the recF, recO, and
recR genes. Assuming that UV-induced reversion of a given
mutation requires that errors be made during the processing of a
specific DNA daughter-strand gap, it is possible that the processing of
such a gap requires the participation of the recF, recO, and recR genes. A provocative speculation,
for example, is that the recF, recO, and
recR genes are involved in the processing of DNA
daughter-strand gaps produced in leading-strand synthesis but not for
those produced in lagging-strand synthesis. According to such a
postulate, reversion of a mutation requiring errors to be made during
the processing of leading-strand DNA daughter-strand gaps would show a
dependency on the recF, recO, and recR
genes. On the other hand, reversion of a mutation requiring errors to be made during the processing of lagging-strand DNA daughter-strand gaps would be independent of the recF, recO, and
recR genes. This may explain why there are different
requirements for the recF, recO, and
recR genes in different reversion assays. To account for the
differential effects of recA2020 on the suppression of deficiencies both in postreplication repair and in UVM in
recF, recO, and recR mutants, we
suggest that among the DNA daughter-strand gaps that require the
participation of the recF, recO, and
recR genes for repair, some are processed through an
error-free process and some are processed through an error-prone
process. Restoration by recA2020 of the portion of
postreplication repair which is error prone can explain why a partial
restoration of postreplication repair proficiency can lead to a full
restoration of UVM in recF, recO, and
recR mutants. According to this postulate, the portion of
postreplication repair restored by recA2020 is error prone. Future experiments shall test the validity of this hypothesis.
In conclusion, we have presented evidence for an involvement of the
recF, recO, and recR genes in UVM. Our
results indicate that these genes do not act by affecting RecA's
functions in the induction of SOS regulons or in the cleavage of UmuD.
We suggest that the recF, recO, and
recR gene products act by affecting the third role of RecA
in UVM.
This work was supported by Chang Gung Medical research grant CMRP 378 and National Science Council of Taiwan research grant NSC
85-2331-B182-107.
| 1.
|
Bailone, A.,
S. Sommer,
J. Knezevic,
M. Dutreix, and R. Devoret.
1991.
A RecA protein mutant deficient in its interaction with the UmuDC complex.
Biochimie
73:479-484[Medline].
|
| 2.
|
Bridges, B. A.
1972.
Simple bacterial systems for detecting mutagenic agents.
Lab. Pract.
21:413-419[Medline].
|
| 3.
|
Bruck, I.,
R. Woodgate,
K. McEntee, and M. F. Goodman.
1996.
Purification of a soluble UmuD'C complex from Escherichia coli: cooperative binding of UmuD'C to single-stranded DNA.
J. Biol. Chem.
271:10767-10774[Abstract/Free Full Text].
|
| 4.
|
Clark, A. J.
1991.
rec genes and homologous recombination on Escherichia coli.
Biochimie
73:523-532[Medline].
|
| 5.
|
Clark, A. J.,
M. R. Volkert, and L. J. Margossian.
1979.
A role for recF in repair of UV damage to DNA.
Cold Spring Harbor Symp. Quant. Biol.
43:887-892.
|
| 6.
|
Clark, A. J.,
S. J. Sandler,
K. D. Willis,
C. C. Chu,
A. A. Blanar, and S. T. Lovett.
1984.
Genes of the RecE and RecF pathways of conjugational recombination in E. coli.
Cold Spring Harbor Symp. Quant. Biol.
49:453-462[Medline].
|
| 7.
|
Dutreix, M.,
P. L. Moreau,
A. Bailone,
F. Galibert,
J. R. Battista,
G. C. Walker, and R. Devoret.
1989.
New recA mutations that dissociate the various RecA protein activities in Escherichia coli provide evidence for an additional role for RecA protein in UV mutagenesis.
J. Bacteriol.
171:2415-2423[Abstract/Free Full Text].
|
| 8.
|
Frank, E. G.,
M. Gonzalez,
D. G. Ennis,
A. S. Levine, and R. Woodgate.
1996.
In vivo stability of the Umu mutagenesis proteins: a major role for RecA.
J. Bacteriol.
178:3550-3556[Abstract/Free Full Text].
|
| 9.
|
Frank, E. G.,
J. Hauser,
A. S. Levine, and R. Woodgate.
1993.
Targeting of the UmuD, UmuD', and MucA' mutagenesis proteins to DNA by RecA protein.
Proc. Natl. Acad. Sci. USA
90:8169-8173[Abstract/Free Full Text].
|
| 10.
|
Friedberg, E. C.,
G. C. Walker, and W. Siede.
1995.
.
DNA repair and mutagenesis.
ASM Press, Washington, D.C.
|
| 11.
|
Griffin, T. J., IV, and R. D. Kolodner.
1990.
Purification and preliminary characterization of the Escherichia coli K-12 RecF protein.
J. Bacteriol.
172:6291-6299[Abstract/Free Full Text].
|
| 12.
|
Hegde, S.,
S. J. Sandler,
A. J. Clark, and M. V. V. S. Madiraju.
1995.
recO and recR mutations delay induction of SOS response in Escherichia coli.
Mol. Gen. Genet.
246:254-258[Medline].
|
| 13.
|
Hegde, S. P.,
M.-H. Qin,
X.-H. Li,
M. A. L. Atkinson,
A. J. Clark,
M. Rajagopalan, and M. V. V. S. Madiraju.
1996.
Interactions of RecF protein with RecO, RecR, and single-stranded DNA binding proteins reveal roles for the RecF-RecO-RecR complex in DNA repair and recombination.
Proc. Natl. Acad. Sci. USA
93:14468-14473[Abstract/Free Full Text].
|
| 14.
|
Horii, Z., and A. J. Clark.
1973.
Genetic analysis of the RecF pathway of genetic recombination in Escherichia coli K-12: isolation and characterization of mutants.
J. Mol. Biol.
80:327-344[Medline].
|
| 15.
|
Kato, T.,
R. H. Rothman, and A. J. Clark.
1977.
Analysis of the role of recombination and repair in mutagenesis of Escherichia coli K-12.
Genetics
87:1-18[Abstract/Free Full Text].
|
| 16.
|
Kolodner, R.,
R. A. Fishel, and M. Howard.
1985.
Genetic recombination of bacterial plasmid DNA: effect of RecF pathway mutations on plasmid recombination in Escherichia coli.
J. Bacteriol.
163:1060-1066[Abstract/Free Full Text].
|
| 17.
|
Little, J. W.
1983.
The SOS regulatory system: control of its state by the level of RecA protease.
J. Mol. Biol.
167:791-808[Medline].
|
| 18.
|
Little, J. W., and D. W. Mount.
1982.
The SOS regulatory system of E. coli.
Cell
29:11-22[Medline].
|
| 19.
|
Lloyd, R. G., and C. Buckman.
1991.
Overlapping functions of recD, recJ, and recN provide evidence of three epistatic groups of genes in Escherichia coli recombination and DNA repair.
Biochimie
73:313-320[Medline].
|
| 20.
|
Lloyd, R. G., and A. Thomas.
1983.
On the nature of the RecBC and RecF pathways of conjugational recombination in Escherichia coli.
Mol. Gen. Genet.
190:156-161[Medline].
|
| 21.
|
Lu, C.,
R. H. Scheuermann, and H. Echols.
1986.
Capacity of RecA protein to bind preferentially to UV lesions and inhibit the editing subunit ( ) of DNA polymerase III: a possible mechanism for SOS-induced targeted mutagenesis.
Proc. Natl. Acad. Sci. USA
83:619-623[Abstract/Free Full Text].
|
| 22.
|
Luisi-DeLuca, C.
1995.
Homologous pairing of single-stranded DNA and superhelical double-stranded DNA catalyzed by RecO protein from Escherichia coli.
J. Bacteriol.
177:566-572[Abstract/Free Full Text].
|
| 23.
|
Luisi-DeLuca, C., and R. D. Kolodner.
1994.
Purification and characterization of the Escherichia coli RecO protein: renaturation of complementary single-stranded DNA molecules catalyzed by the RecO protein.
J. Mol. Biol.
236:124-138[Medline].
|
| 24.
|
Luisi-DeLuca, C.,
S. T. Lovett, and R. D. Kolodner.
1989.
Genetic and physical analysis of plasmid recombination in recB recC sbcB and recB recC sbcA Escherichia coli K-12 mutants.
Genetics
122:269-278[Abstract/Free Full Text].
|
| 25.
|
Madiraju, M. V. V. S., and A. J. Clark.
1991.
Effect of RecF protein on reactions catalyzed by RecA protein.
Nucleic Acids Res.
19:6295-6300[Abstract/Free Full Text].
|
| 26.
|
Madiraju, M. V. V. S., and A. J. Clark.
1992.
Evidence for ATP binding and double-stranded DNA binding by Escherichia coli RecF protein.
J. Bacteriol.
174:7705-7710[Abstract/Free Full Text].
|
| 27.
|
Mahdi, A. A., and R. G. Lloyd.
1989.
Identification of the recR locus of Escherichia coli K-12 and analysis of its role in recombination and DNA repair.
Mol. Gen. Genet.
216:503-510[Medline].
|
| 28.
|
Mahdi, A. A., and R. G. Lloyd.
1989.
The recR locus of Escherichia coli K-12: molecular cloning, DNA sequencing and identification of the gene product.
Nucleic Acids Res.
17:6781-6794[Abstract/Free Full Text].
|
| 29.
|
Nohmi, T.,
R. R. Battista,
L. A. Dodson, and G. C. Walker.
1988.
RecA-medicated cleavage activates UmuD for mutagenesis: mechanistic relationship between transcriptional derepression and post-translational activation.
Proc. Natl. Acad. Sci. USA
85:1816-1820[Abstract/Free Full Text].
|
| 30.
|
Rothman, R. H., and A. J. Clark.
1977.
The dependence of postreplication repair on uvrB in a recF mutant of Escherichia coli K-12.
Mol. Gen. Genet.
155:279-286[Medline].
|
| 31.
|
Sargentini, N. J., and K. C. Smith.
1980.
Involvement of genes uvrD and recB in separate mutagenic deoxyribonucleic acid repair pathways in Escherichia coli K-12 uvrB5 and B/r uvrA155.
J. Bacteriol.
143:212-220[Abstract/Free Full Text].
|
| 32.
|
Sargentini, N. J., and K. C. Smith.
1985.
Spontaneous mutagenesis: the roles of DNA repair, replication, and recombination.
Mutat. Res.
154:1-27[Medline].
|
| 33.
|
Sawitzke, J. A., and F. W. Stahl.
1992.
Phage lambda has an analog of Escherichia coli recO, recR and recF gene.
Genetics
130:7-16[Abstract].
|
| 34.
|
Shinagawa, H.,
H. Iwasaki,
T. Kato, and A. Nakata.
1988.
RecA protein-dependent cleavage of UmuD protein and SOS mutagenesis.
Proc. Natl. Acad. Sci. USA
85:1806-1810[Abstract/Free Full Text].
|
| 35.
|
Shinagawa, H.,
T. Kato,
T. Ise,
K. Makino, and A. Nakata.
1983.
Cloning and characterization of the umu operon for inducible mutagenesis in E. coli.
Gene
23:167-174[Medline].
|
| 36.
|
Sommer, S.,
J. Knezevic,
A. Bailone, and R. Devoret.
1993.
Induction of only one SOS operon is required for SOS mutagenesis in Escherichia coli.
Mol. Gen. Genet.
239:137-144[Medline].
|
| 37.
|
Sweasy, J. B.,
E. M. Witkin,
N. Sinha, and V. Roegner-Maniscalco.
1990.
RecA protein of Escherichia coli has a third essential role in SOS mutator activity.
J. Bacteriol.
172:3030-3036[Abstract/Free Full Text].
|
| 38.
|
Thoms, B., and W. Wackernagel.
1987.
Regulatory role of recF in the SOS response of Escherichia coli: impaired induction of SOS genes by UV irradiation and nalidixic acid in a recF mutant.
J. Bacteriol.
169:1731-1736[Abstract/Free Full Text].
|
| 39.
|
Tseng, Y. C.,
J. L. Hung, and T. V. Wang.
1994.
Involvement of RecF pathway recombination genes in postreplication repair in UV-irradiated Escherichia coli cells.
Mutat. Res.
315:1-9[Medline].
|
| 40.
|
Umezu, K., and R. D. Kolodner.
1994.
Protein interactions in genetic recombination in Escherichia coli: interactions involving RecO and RecR overcome the inhibition of RecA by single-stranded DNA-binding protein.
J. Biol. Chem.
269:30005-30013[Abstract/Free Full Text].
|
| 41.
|
Umezu, K.,
N. W. Chi, and R. D. Kolodner.
1993.
Biochemical interaction of the Escherichia coli RecF, RecO, and RecR proteins with RecA protein and single-stranded DNA binding protein.
Proc. Natl. Acad. Sci. USA
90:3875-3879[Abstract/Free Full Text].
|
| 42.
|
Volkert, M. R., and M. A. Hartke.
1984.
Suppression of Escherichia coli recF mutations by recA-linked srfA mutations.
J. Bacteriol.
157:498-506[Abstract/Free Full Text].
|
| 43.
|
Walker, G. C.
1984.
Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli.
Microbiol. Rev.
48:60-93[Free Full Text].
|
| 44.
|
Wang, T.-C. V., and K. C. Smith.
1983.
Mechanisms for recF-dependent and recB-dependent pathways of postreplication repair in UV-irradiated Escherichia coli uvrB.
J. Bacteriol.
156:1093-1098[Abstract/Free Full Text].
|
| 45.
|
Wang, T.-C. V., and K. C. Smith.
1986.
recA (Srf) suppression of recF deficiency in the postreplication repair of UV-irradiated Escherichia coli K-12.
J. Bacteriol.
168:940-946[Abstract/Free Full Text].
|
| 46.
|
Wang, T. V.,
H. Y. Chang, and J. L. Hung.
1993.
Cosuppression of recF, recR and recO mutations by mutant recA alleles in Escherichia coli cells.
Mutat. Res.
294:157-166[Medline].
|
| 47.
|
Webb, B. L.,
M. M. Cox, and R. B. Inman.
1995.
An interaction between the Escherichia coli RecF and RecR proteins dependent on ATP and double-stranded DNA.
J. Biol. Chem.
270:31397-31404[Abstract/Free Full Text].
|
| 48.
|
Whitby, M. C., and R. G. Lloyd.
1995.
Altered SOS induction associated with mutations in recF, recO, and recR.
Mol. Gen. Genet.
246:174-179[Medline].
|
| 49.
|
Woodgate, R., and S. Sedgwick.
1992.
Mutagenesis induced by bacterial UmuDC proteins and their plasmid homologues.
Mol. Microbiol.
6:2213-2218[Medline].
|
| 50.
|
Woodgate, R.,
M. Rajagopalan,
C. Lu, and H. Echols.
1989.
UmuC mutagenesis protein of Escherichia coli: purification and interaction with UmuD and UmuD'.
Proc. Natl. Acad. Sci. USA
86:7301-7305[Abstract/Free Full Text].
|
![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
Top
Abstract
Introduction
