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Journal of Bacteriology, August 1998, p. 3750-3756, Vol. 180, No. 15
School of Biological Sciences, University of
Wales Swansea, Swansea SA2 8PP, United Kingdom
Received 13 June 1997/Accepted 15 May 1998
hupA and hupB encode the HU is one of the most abundant
DNA-binding proteins in Escherichia coli, and it contributes
to the compaction of the genome into tight nucleosome-like structures
(40). E. coli HU is a small, basic, heat-stable
dimeric protein composed of two highly homologous subunits, HU E. coli hup mutants are sensitive to To determine in which pathway of DNA repair or damage tolerance the
hup gene is involved, we examined the interactions between hup and other genes whose functions in DNA repair and/or
damage tolerance have been well documented. It appears that a
deficiency in homologous recombination renders hup mutants
UV sensitive.
Bacterial strains, plasmids, and media.
The bacterial
strains and plasmids used are listed in Table
1. Standard phage P1 transduction,
performed as described by Sternberg and Maurer (47), was
used for the construction of different hup mutants. Plasmid
transformation was performed by the cold CaCl2 method as
described by Sambrook et al. (42). Bacteria were grown in
Luria broth (LB) medium and on LB agar. Tetracycline and
chloramphenicol were used at 10 µg/ml. Kanamycin, erythromycin, and
ampicillin were used at 50 µg/ml.
Isopropyl-
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Escherichia coli Strains Lacking Protein
HU Are UV Sensitive due to a Role for HU in Homologous
Recombination
ABSTRACT
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Abstract
Introduction
Materials & Methods
Results & Discussion
References
and 
subunits of the Escherichia coli histone-like protein HU.
Here we show that E. coli hup mutants are sensitive to UV
in the rec+ sbc+, recBC
sbcA, recBC sbcBC, umuDC,
recF, and recD backgrounds. However,
hupAB mutations do not enhance the UV sensitivity of resolvase-deficient recG ruvA strains. hupAB
uvrA and hupAB recG strains are supersensitive to UV.
hup mutations enhance the UV sensitivity of
ruvA strains to a much lesser extent but enhance that of
rus-1 ruvA strains to the same extent as for
rus+ ruv+ strains. Our results
suggest that HU plays a role in recombinational DNA repair that is not
specifically limited to double-strand break repair or daughter strand
gap repair; the lack of HU affects the RecG RusA and RuvABC pathways
for Holliday junction processing equally if the two pathways are
equally active in recombinational repair; the function of HU is not in
the substrate processing step or in the RecFOR-directed synapsis action
during recombinational repair. Furthermore, the UV sensitivity of
hup mutants cannot be suppressed by overexpression of
wild-type or mutant gyrB, which confers novobiocin
resistance, or by different concentrations of a gyrase inhibitor that
can increase or decrease the supercoiling of chromosomal DNA.
INTRODUCTION
Top
Abstract
Introduction
Materials & Methods
Results & Discussion
References
and
HU, encoded by the hupA and hupB genes located
at 90 and 10 min, respectively, on the E. coli chromosome (21, 22). Strains mutated in both hupA and
hupB have reduced viability, perturbed cell division, and a
number of other deficiencies (18, 50). The HU protein also
participates in a number of cellular mechanisms such as modulating the
expression of specific genes (36, 55), DNA melting at the
initiation of replication (20, 45), DNA breaking/rejoining
in transposition and inversion reactions (13, 25), and
homologous recombination (7, 19). In addition, although HU
does not recognize a particular DNA sequence, it can act at very
precise locations on the chromosomal DNA through specific binding to
particular DNA structures such as bulged DNA, four-way DNA junctions
(2, 37), and single-strand breaks or gaps (5).
irradiation, and in
vitro studies show that HU protects DNA against cleavage by rays (3). This finding suggests that HU may play a role in DNA
repair or in a mechanism of tolerance to DNA damage. There are several pathways for DNA repair or DNA damage tolerance in E. coli.
The pathway(s) in which a specific gene is involved can be inferred by
studying the phenotypic consequences of the interactions of the
specific mutant gene with other mutant genes whose functions in DNA
repair or damage tolerance have been well documented (4).
MATERIALS AND METHODS
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Abstract
Introduction
Materials & Methods
Results & Discussion
References
-D-thiogalactopyranoside (IPTG) was used at 1 mM.
TABLE 1.
E. coli strains and plasmids used
UV survival.
Strains were grown in LB to mid-log phase
(optical density at 600 nm [OD600] 
0.5) and serially
10-fold diluted in 1% NaCl; 50 µl of the diluted cell suspension was
spread onto each of three LB agar plates per UV dose. To induce
overexpression of wild-type or mutated plasmid-borne gyrB, 1 mM IPTG was included in the plates. To test the effect of the gyrase
inhibitor novobiocin on UV sensitivity, 0 to 60 µg of novobiocin per
ml was included in the plates. Under dimmed yellow light, the plates
were irradiated with various doses of 254-nm UV and incubated in the
dark for 24 or 48 h before the colonies were counted. The survival
values given are the means of two to four independent experiments.
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RESULTS AND DISCUSSION |
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Top
Abstract
Introduction
Materials & Methods
Results & Discussion
References
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UV sensitivity of hup strains.
Although HU is not
essential to E. coli, cells lacking HU have multiple
deficiencies (18, 50). Moreover, it has been shown that
hup mutants are sensitive to irradiation (3).
As the types of damages induced by and UV irradiations are
different, and mechanisms for repair of these damages are also
different, we tested if hup mutations render cells UV
sensitive. As shown in Fig. 1,
hup mutations render the cells UV sensitive in
rec+ sbc+, recBC
sbcA, and recBC sbcBC backgrounds.
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0.5), diluted in 1% NaCl, and irradiated on the
surface of LB agar plates. Surviving colonies were scored after 24 h of incubation in the dark. The strains identified by genotype were
JR1669, JR1670, JR1671, JR1672, and JR1672 transformed with plasmid
pYK20 (a), JC7623, SL1012, SL1013, and SL1014 (b), and JC8679, SL1015,
SL1016, and SL1017 (c).
(21). It has been shown
that plasmids bearing the hupA or hupB gene can
restore the -ray resistance of hupAB strains to nearly the wild-type level (3). The production of 2 homodimers
by plasmid pYK20 also increased the resistance of the hupAB
mutants to UV to nearly the level of wild-type cells (Fig. 1a). The
introduction of the same plasmid into wild-type cells caused no change
in UV sensitivity (data not shown). This result suggests that the UV sensitivity of the hup mutants is directly caused by the
absence of HU.
hup and uvrA interact synergistically. HU is involved in the compaction of genomic DNA (40); the lack of HU can cause a topological change of DNA (1, 16, 17, 33, 41, 48). Therefore, it is possible that lack of HU can change the DNA UV photochemistry and the excision repair of UV photoproducts. We analyzed the induction and repair patterns of cyclobutane pyrimidine dimers (CPDs) at the nucleotide level in the replication origin oriC, in the mRNA genes lacI and lacZ, and in the tRNA gene tyrT. Almost identical patterns of CPD induction and removal were observed in wild-type and hupAB strains (references 26 and 27 and data not shown). Using a CPD-specific monoclonal antibody, we measured the induction and removal of CPDs in bulk genomic DNA. Again, no apparent difference was seen between wild-type and hupAB cells (data not shown). These results suggest that the UV sensitivity of hup mutants is not caused by the change of UV photoproduct induction or a deficiency in nucleotide excision repair.
To further test if hup genes are involved in nucleotide excision repair, we examined the interaction between hup and uvrA, one of the genes essential for nucleotide excision repair in E. coli (for a review, see reference 43). As shown in Fig. 2d, the hupAB uvrA triple mutant is supersensitive to UV. It should be noted here that due to the high UV sensitivity of uvrA mutants, the applied UV doses are lower than those for the strains described in the adjacent graphs. The killing associated with the doses given to the triple mutant is much greater than the sum of the killing achieved by uvrA mutation plus the incremental killing by hupAB double mutations; i.e., hup and uvrA interact synergistically. Specifically, after a 3-J/m2 dose of UV, the surviving fraction for uvrA is 0.0021, whereas for the uvrA hupAB strain it is 0.00017. Based on this result and those obtained from the direct measurement of CPD removal, we conclude that HU is not involved in nucleotide excision repair.
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hup mutations markedly enhance the UV sensitivity of umuDC strains. Reduced tolerance to DNA damage renders cells sensitive to the damaging agents. One of the known DNA damage tolerance mechanisms is via translesion synthesis, in which the umuDC operon has an indispensable role (reviewed in reference 11). We tested the interaction between mutations of hup and umuDC. As shown in Fig. 2c, the UV killing of the hupAB umuDC strain is roughly the sum of the killing in the umuDC mutant plus the increased killing by hupAB mutations over the level for wild-type strains. This finding suggests that hup and umuDC genes are involved in independent pathways for DNA damage tolerance or repair. In other words, the UV sensitivity caused by hup mutations is not due to the deficiency in translesion synthesis.
hup mutations do not enhance the UV sensitivity of
resolvase-deficient recG ruvA strains.
hupAB
mutations do not curtail the rapid SOS response (3). The
-ray sensitivity of hup mutants may result from the lack of sufficient protection of the chromosomal DNA from radiation, as
shown by in vitro experiments (3). Alternatively, this
sensitivity may be due to the deficiency in the repair of
-ray-induced double-strand breaks, which is achieved by homologous
recombination (24). It has been shown that hupAB
mutants are deficient in homologous recombination (7, 19).
Our results, which are similar to those of Dri et al. (7),
showed that hupAB caused a two- to fivefold reduction in P1
transduction and conjugational recombination in the
rec+ sbc+, recBC sbcA,
and recBC sbcBC backgrounds (data not shown). As shown
above, hupAB interact with uvrA synergistically,
as is typical for a mutation that blocks recombinational repair
(15, 29, 30). The fact that hupAB mutations do
not enhance the -ray sensitivity of recA strains
(3) also supports the idea that HU is involved in
recombinational repair.
hup mutations confer different phenotypes on
recG and ruvA strains.
RuvAB with RuvC and
RecG with RusA provide two overlapping pathways for processing Holliday
junctions (28, 32, 34, 44). To test the role of HU in the
two pathways, we analyzed the interaction of hup with
recG and ruvA. hupAB recG strains are
far more sensitive to UV than hupAB or recG
strains (Fig. 2f), while hupAB ruvA strains are slightly
more sensitive than ruvA strains (Fig. 2g). This finding
indicates that hup mutations mainly hinder the
recombinational pathway in which Holliday junctions are processed by
RuvABC. To exclude the possibility that the interrupted genes were
inserted into the recipient genomes rather than substituted for the
normal genes during phage P1 transduction, we constructed the hup
ruvA strains by introducing
ruvA60::Tn10 into the hup
strains and by introducing hupA::Cm and
hupB::Km into the ruvA strains.
Substitutions of the wild-type genes with the interrupted genes were
confirmed by Southern blot analysis (data not shown). The strains
constructed showed the same interactions between hup and
ruvA. Moreover, the hupAB ruvA strains were just
as sensitive to UV as hupA ruvA strains (Fig. 2g).
Additional hupB mutations in the hupA ruvA
strains did not render the cells more UV sensitive. Presumably the 2 homodimers cannot compensate for the function of the
heterodimers in hupA ruvA strains.
In which step(s) of recombinational repair is HU involved? The recombinational repair of UV-induced DNA damages is thought to occur by a mechanism termed postreplication repair. Two major types of postreplication repair processes exist; one repairs daughter strand DNA gaps, and the other repairs double-strand breaks generated from the unrepaired daughter strand gaps (51-53). Daughter strand gap repair depends on RecF (51, 52). Double-strand break repair depends mainly on RecB but to a minor extent on RecF (51-53). The RecBCD enzyme initiates DNA unwinding at double-strand DNA ends, and its nuclease activity is controlled by Chi sites in such a way that the enzyme produces a potent single-stranded DNA substrate for homologous pairing (for a review, see reference 46). However, the repair deficiency of recB recC mutants can be suppressed by secondary mutations in either the sbcA or sbcB locus, and in each case the suppression can be rationalized in terms of an effect on the generation of 3' ends (for reviews, see references 23 and 54). sbcA mutations activate exonuclease VIII, which digests double-stranded DNA ends to produce long 3' tails, and this could provide an alternative means of producing the invasive 3' ends. sbcBC mutations inactivate exonuclease I, which digests single-stranded DNA from the 3' end, so that its inactivation might leave 3' ends available to initiate recombinational repair. The hupAB mutants do not degrade their DNA after UV irradiation any more extensively than wild-type strains (data not shown), although it has been proposed that the specific binding of HU to the DNA single-strand breaks or gaps may have a role in protecting these region from further degradation by endonucleases (5). The findings that hupAB mutations render rec+ sbc+, recBC sbcA, and recBC sbcBC (in which the recombinational substrates are generated by different mechanisms) strains sensitive to UV (Fig. 1) and that the UV sensitivity of the recD strain is also enhanced by the hup mutations (Fig. 2a) suggest that HU is unlikely to be involved in the substrate processing step of recombinational repair.
The products of recF, recO, and recR function together to facilitate synapsis during recombinational repair (49). Our results show that hupAB mutations greatly enhance the UV sensitivity of recF strains (Fig. 2b), indicating that HU is not involved in the synapsis action directed by RecFOR. Interestingly, in a recF background, hupA or hupB single mutations caused a considerable increase in UV sensitivity (Fig. 1 and 2), while hupA hupB double mutations led to no significant increase (Fig. 2b). Presumably, as in the ruvA background (see above),2 or 2 homodimers cannot substitute for the function of
the heterodimers in the recF background. Experiments
in vitro (38) showed that HU actually inhibits RecA-promoted
pairing of homologous DNA molecules. Whether HU has a role in the
synapsis actions that are not directed by RecFOR needs to be
elucidated.
Our results concerning the interaction in terms of UV sensitivity
between hup and the genes involved in homologous
recombination, together with the fact that hup mutants are
also sensitive to irradiation (3), suggest that the
function of HU in recombinational repair lies in the common step(s) for
double-strand break repair and daughter strand gap repair. It is quite
likely that the common step is that of Holliday junction processing,
since hup mutations do not cause an increase in the UV
sensitivity of resolvase-deficient recG ruvA strains. If
this is the case, the interaction between HU and the resolvases is
unlikely to be a direct protein-protein contact, since hup
mutations affect both RecG RusA and RuvABC pathways. Further work is
needed to determine exactly in which step(s) or action(s) during
recombinational repair HU is involved.
The UV sensitivity of hup mutants cannot be suppressed by overexpression of wild-type gyrB or gyrB mutations that confer novobiocin resistance. In prokaryotes, the degree of supercoiling is determined by the relative activities of at least two enzymes, DNA gyrase and topoisomerase I. DNA gyrase activity leads to increased negative supercoiling of the DNA, while topoisomerase I activity relaxes the DNA (for reviews, see references 8 and 31). Although lacking topoisomerase activity, HU may contribute to DNA topology. In vitro, HU bends DNA and wraps it into nucleosome-like structures (40). A small amount of relaxation was seen in DNA extracted from HU-deficient cells (41). hupAB mutants show a growth deficiency (18, 33, 50) and are hypersensitive to the gyrase inhibitor novobiocin. These phenotypes of hupAB strains may result from the relaxation of chromosomal DNA, as they can be suppressed by overexpression of the wild-type gyrB gene or by gyrB mutations that confer novobiocin resistance (33). This notion is supported by the observation that DNA supercoiling increased toward wild-type levels in the presence of gyrB suppressors (33). We wondered whether the UV sensitivity of hup mutants can also be suppressed by overexpression of the wild-type gyrB gene or by the gyrB mutations that confer novobiocin resistance. To test this, plasmid pAG111, which bears the tac promoter-controlled wild-type gyrB gene (12), was used to transform the wild-type and hupAB strains. The hupAB strains transformed with pAG111 formed large, uniform colonies if the cells were cultured on agar plates containing 1 mM IPTG. Variable sizes of colonies formed if the same cells were cultured on plates that did not contain IPTG (data not shown). These results indicate that the heterogeneous colony phenotype of hupAB strains is indeed suppressed by overexpression of the gyrB gene. However, UV sensitivity was virtually unchanged for both the wild-type and hupAB strains by inducing the overexpression of the wild-type gyrB gene borne on plasmid pAG111 (data not shown).
To test if gyrB mutations that confer resistance to novobiocin can suppress the UV sensitivity of hupAB strains, we isolated a number of novobiocin-resistant clones from hupAB strains by picking up large colonies from LB plates containing 150 µg of novobiocin per ml. The clones formed large, uniform colonies, but none showed increased resistance to UV (data not shown). We also transformed wild-type and hupAB strains with pAG111 derivatives pCC205 and pCC206 that bear mutant gyrB genes conferring novobiocin resistance (6). pCC205 bears the gyrB gene with a CG-TA transition at position 407, and pCC206 bears the gyrB gene with a GC-AT transition at position 406 (6). Again, no increased UV resistance was seen in the hupAB strains by inducing the overexpression of the mutant gyrB genes with IPTG (data not shown).The UV sensitivity of hup mutants cannot be suppressed by different concentrations of gyrase inhibitor that can increase or decrease the supercoiling of the chromosomal DNA. Bensaid et al. (1) showed that a decrease in the intracellular concentration of HU is accompanied by an increase in the relaxing activity of topoisomerase I; the ability to increase relaxing activity, or to decrease an excess of supercoiling, is important for cells to survive in the absence of HU. It is proposed that the absence of HU, like the removal of histones, results first in the excess of DNA supercoiling which must be removed by topoisomerase I activity for the cells to survive. Contrary to the scenario suggested by Malik et al. (33), the relaxation of the chromosomal DNA is proposed to be beneficial to the hupAB cells.
To determine whether the excess of unconstrained supercoiling due to the lack of HU is linked to UV sensitivity, we used the DNA gyrase inhibitor novobiocin. It has been shown that low levels (about 12.5 µg/ml for novobiocin) of gyrase inhibitors induce gyrase production, leading to a net increase in negative supercoiling of DNA, but higher levels reduce DNA supercoiling (10, 35). To measure the sensitivity of wild-type and hupAB strains to the gyrase inhibitor, cells were spread onto LB plates containing 0 to 60 µg of novobiocin per ml, and the plates were incubated for 48 h at 37°C before the colonies were counted. As shown in Fig. 3a, the hupAB strains were moderately sensitive to higher concentrations of novobiocin. To test the effect of DNA topological changes induced by novobiocin on UV sensitivity, the cells were also spread onto LB plates containing novobiocin (0 to 60 µg/ml), irradiated with UV (30 J/m
2), and incubated for 48 h at 37°C. To
determine the cell killing caused by novobiocin, the survival fractions
were expressed as those obtained from the UV-irradiated plates divided
by those obtained from the unirradiated plates containing the
corresponding concentrations of novobiocin. As shown in Fig. 3b, the
survival fraction for both wild-type and hupAB strains to
the fixed dose of UV slightly decreased as the concentration of
novobiocin increased. However, the curves of UV survival for the
wild-type and hupAB strains are almost parallel within the
range of novobiocin concentrations used (Fig. 3b), indicating that the
UV sensitivity of hupAB strains cannot be suppressed by
increasing or decreasing the supercoiling of the chromosomal DNA.
|
) and hupAB (JR1672;
*) strains. Strains were grown in LB to log phase (OD600 | |
ACKNOWLEDGMENTS |
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We are deeply in debt to the people who generously supplied E. coli strains and plasmids.
This work was supported by research funds from Dwr Cymru.
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FOOTNOTES |
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* Corresponding author. Mailing address: School of Biological Sciences, University of Wales Swansea, Singleton Park, Swansea SA2 8PP, United Kingdom. Phone: (44) 1792 295384. Fax: (44) 1792 295447. E-mail: r.waters{at}swansea.ac.uk.
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REFERENCES |
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Top
Abstract
Introduction
Materials & Methods
Results & Discussion
References
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Journal of Bacteriology, August 1998, p. 3750-3756, Vol. 180, No. 15
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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