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Journal of Bacteriology, August 2001, p. 4562-4570, Vol. 183, No. 15
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.15.4562-4570.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
DNA Microarray-Mediated Transcriptional Profiling
of the Escherichia coli Response to Hydrogen
Peroxide
Ming
Zheng,1,2
Xunde
Wang,1
Lori J.
Templeton,2
Dana R.
Smulski,2
Robert A.
LaRossa,2 and
Gisela
Storz1,*
Cell Biology and Metabolism Branch, National
Institute of Child Health and Human Development, National Institutes of
Health, Bethesda, Maryland 20892,1 and
Biochemical Science and Engineering, Central Research and
Development, E. I. DuPont de Nemours and Company, Wilmington,
Delaware 19880-03282
Received 15 March 2001/Accepted 15 May 2001
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ABSTRACT |
The genome-wide transcription profile of Escherichia
coli cells treated with hydrogen peroxide was examined with a
DNA microarray composed of 4,169 E. coli open reading
frames. By measuring gene expression in isogenic wild-type and
oxyR deletion strains, we confirmed that the peroxide
response regulator OxyR activates most of the highly hydrogen
peroxide-inducible genes. The DNA microarray measurements allowed the
identification of several new OxyR-activated genes, including the
hemH heme biosynthetic gene; the six-gene
suf operon, which may participate in Fe-S cluster assembly or repair; and four genes of unknown function. We also identified several genes, including uxuA, encoding
mannonate hydrolase, whose expression might be repressed by OxyR, since
their expression was elevated in the 
oxyR mutant
strain. In addition, the induction of some genes was found to be OxyR
independent, indicating the existence of other peroxide sensors and
regulators in E. coli. For example, the
isc operon, which specifies Fe-S cluster formation and
repair activities, was induced by hydrogen peroxide in strains lacking
either OxyR or the superoxide response regulators SoxRS. These results
expand our understanding of the oxidative stress response and raise
interesting questions regarding the nature of other regulators that
modulate gene expression in response to hydrogen peroxide.
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INTRODUCTION |
The Salmonella
enterica serovar Typhimurium and Escherichia coli
responses to hydrogen peroxide initially were analyzed 15 years
ago using two-dimensional gel separation of proteins (10, 20,
33). These studies showed that the expression of approximately 30 proteins is induced by hydrogen peroxide treatment: 12 proteins are
maximally induced within 10 min and 18 proteins are maximally induced
between 10 and 30 min after the addition of hydrogen peroxide (10). Mutational studies led to discovery of the OxyR
regulatory protein, which was shown to regulate the expression of 9 of
the 12 rapidly induced proteins (10). A variety of
approaches have led to the identification of some of the OxyR-activated
genes, including katG (encoding hydroperoxidase I),
ahpCF (encoding an alkyl hydroperoxide reductase),
oxyS (encoding a small regulatory RNA), dps
(encoding a nonspecific DNA binding protein), gorA (encoding glutathione reductase), grxA (encoding glutaredoxin 1),
trxC (encoding thioredoxin 2), fur (encoding the
Fur repressor of ferric ion uptake), and dsbG (encoding a
disulfide chaperone-isomerase) (41; also reviewed
in reference 30). OxyR also has been shown to be a
repressor of its own expression as well as that of fhuF
(encoding a ferric ion reductase) and flu (encoding the
antigen 43 outer membrane protein). Nevertheless, the identity of many
of the hydrogen peroxide-inducible proteins has remained unknown.
The recently developed microarray technology has allowed the parallel
study of the expression of every gene in an organism. This approach has
already been successfully used in studying E. coli gene
expression under a number of different growth conditions (13, 26,
31, 35, 36). Here, we report a survey of gene expression in
response to hydrogen peroxide. In addition to confirming the hydrogen
peroxide induction of most known OxyR-regulated genes, we have
identified several new members of the OxyR regulon. We also have found
that many genes are induced by hydrogen peroxide in an OxyR-independent
fashion, revealing complex regulation of the cellular response to
oxidative stress.
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MATERIALS AND METHODS |
Plasmids and strains.
The DNA sequences and coordinates
throughout the study are for E. coli from GenBank accession
no. U00096 (5). The plasmids used in the study were
constructed using fragments PCR amplified from chromosomal DNA. The
sequences of all oligonucleotides are listed in Table
1. To generate the hemH
promoter plasmids (pGSO131 and pGSO132), a 280-bp fragment produced
using primers 819 and 821 was cloned into pCR2.1 (Invitrogen) in both
orientations. To generate a sufA promoter plasmid (pGSO133),
a 378-bp fragment produced using primers 820 and 825 was cloned into
pCR2.1. To generate the isc promoter plasmid (pGSO135), a
500-bp fragment produced using primers 699 and 700 was cloned into the
EcoRI and BamHI sites of pUC18. The
oxyR::kan (GSO9 [32])
mutant allele was moved into MG1655 (2) by P1 transduction
(27) to generate GSO77. MC4100 (wild type), GSO47 (MC4100
oxyR::kan), GSO71 (MC4100 soxRS), and GSO72 (MC4100
fur::kan) were described previously (40).
RNA isolation.
Cultures were grown under aeration at 37°C
in Luria-Bertani (LB) rich medium (27). Exponential-phase
cultures (optical density at 600 nm = 0.2 to 0.5) were split into
aliquots; one aliquot was left untreated, and the other aliquots were
treated with the indicated amounts of hydrogen peroxide or paraquat.
After 10 min, the cells from 5, 10, or 25 ml of culture were harvested
and resuspended in 1 ml of Trizol equilibrated at 4°C (Gibco BRL).
All subsequent purification steps were carried out according to the
Trizol reagent manual (based on reference 9).
DNA microarray experiments.
Fabrication of the E. coli DNA microarray and procedures for cDNA labeling,
hybridization, and array quantification were described previously
(28, 35).
Primer extension assays.
Total RNA samples were subjected to
primer extension assays as described previously (37),
using primer 819 specific to hemH, primer 820 specific to
sufA, primer 188 specific to oxyS, primer 823 specific to soxS, and primer 686 specific to the
yfhP gene in the isc operon.
DNase I footprinting.
DNase I footprinting assays of
purified OxyR binding to the hemH and sufA
promoters were carried out as described previously (32).
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RESULTS |
DNA microarray measurements.
Wild-type (MG1655) cells and
isogenic oxyR (GSO77) mutant cells were grown to
exponential phase in LB rich medium. The cultures were split, and half
of each culture was treated with 1 mM hydrogen peroxide. After 10 min,
total RNA was isolated from the untreated and treated cultures. To
check whether the RNA samples showed a well-characterized peroxide
stress response, we examined the expression of the oxyS, ahpC,
katG, and fhuF genes using primer extension assays. As
observed previously, oxyS, ahpC, and katG showed
OxyR-dependent induction by hydrogen peroxide, and fhuF showed repression in the wild-type strain and slight induction in the
oxyR deletion strain (data not shown).
Each of the RNA samples was used as a template for cDNA synthesis with
attendant incorporation of either of two fluorescent
dyes, Cy3 and Cy5.
Pairs of differentially labeled untreated and
treated cDNA samples from
each strain then were hybridized to
a glass slide on which two sets of
the 4,169
E. coli open reading
frames (ORFs) were printed.
For each strain, two slides were used
for hybridization: for one slide,
the untreated sample was labeled
with Cy3 and the treated sample was
labeled with Cy5, and for
the second slide, the dye-sample pairings
were reversed. Thus,
the expression for each gene was measured four
times. The average
of the four data points is reported here. Overall,
the mRNA levels
of 140 genes in the wild-type strain showed
>4-fold induction
after treatment with hydrogen peroxide, and the mRNA
levels of
167 genes in the
oxyR strain showed >4-fold
induction. The 30
genes whose expression was induced most strongly in
the wild-type
strain are listed in Table
2, and the 30 genes whose expression
was
induced most strongly in the
oxyR strain are listed in
Table
3. All of these genes have
induction ratios of >10-fold.
OxyR-dependent response.
A hallmark of the E. coli
response to hydrogen peroxide is the rapid and strong induction of a
set of OxyR-regulated genes, including dps, katG, grxA,
ahpCF, and trxC. The observed >20-fold induction of
all of these genes in the wild-type strain (Table 2) but not the
oxyR strain (Table 3) provided an internal validation of
the microarray experiment. Of the other known OxyR-activated genes,
fur and gorA were slightly induced and
dsbG was unchanged in the wild-type strain treated with
hydrogen peroxide. Of the known OxyR-repressed genes, flu
was unchanged and fhuF was slightly repressed. A comparison
of the induction ratios between the wild-type strain and the
oxyR strain indicated that, among the 30 most highly
induced genes, 8 additional genes (hemH, sufABC,
yaiA, yaaA, yljA, and ybjM
[Table 4]) might be regulated by OxyR.
The remaining 16 most highly induced genes showed approximately equal levels of hydrogen peroxide induction in the wild-type strain and the
oxyR strain.
(i) hemH.
One gene, hemH
(b0475), whose expression was induced 11-fold by hydrogen
peroxide in the wild-type strain and <2-fold in the oxyR
strain, encodes a ferrochelatase that catalyzes the incorporation of
ferrous ion into protoporphyrin IX in the final step in protoheme biosynthesis (3). The hemH locus also was named
visA since some ferrochelatase mutants of E. coli
were identified by virtue of having a photosensitive phenotype
(19). It was determined previously that the
photosensitivity was caused by the increased levels of protoporphyrin
IX which accumulate in the mutants lacking ferrochelatase
(21). To confirm OxyR regulation of hemH, we carried out primer extension assays. As shown in Fig.
1B, hemH induction by hydrogen
peroxide in vivo was clearly dependent on OxyR. The
start of the transcript corresponds to an A residue at position 497255, 24 bp upstream of the hemH start codon. An in vitro DNase I
footprinting experiment showed that oxidized OxyR binds to the
hemH promoter centered at 497211, overlapping and just
upstream of the 
35 region (Fig. 1C).
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FIG. 1.
OxyR-dependent induction of hemH. (A)
Sequence of the hemH promoter. The hemH
transcription start is marked by the black arrow, and the start of the corresponding ORF is denoted by
the white arrow. The DNase I footprints for OxyR binding are indicated
by the dark boxes. (B) Primer extension assays of hemH
expression in wild-type (MC4100) and oxyR (GSO47)
strains grown in LB medium. Exponential-phase cultures were split into
two aliquots: one aliquot was left untreated, and the other was treated
with 1 mM hydrogen peroxide. The cells were harvested after 10 min,
total RNA was isolated, and primer extension assays were carried out
with primer 819 specific to hemH. The neighboring
sequencing reactions were carried out with the same primer. (C) DNase I
footprinting assays of oxidized OxyR binding to the top and bottom
strands relative to the hemH promoter. The regions
protected by OxyR on both strands are indicated by the brackets. The
plasmids carrying the hemH promoter fragment in both
orientations were digested with NotI, labeled with
32P, and then digested with BamHI to give
the labeled top and bottom strands. The samples were run in parallel
with Maxam-Gilbert G/A sequencing ladders.
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(ii) suf operon.
Three genes,
sufA/ydiC (b1684), sufB/ynhE (b1683), and
sufC/ynhD (b1682), whose expression was strongly
induced in the wild-type strain but not the oxyR
strain, are members of a six-gene cluster (b1679 to b1684). These genes
are transcribed in the same direction and show potential for
translational coupling. Patzer and Hantke (24) suggested
that the gene cluster forms an operon and, because of possible
involvement in sulfur mobilization, named the genes sufA, sufB,
sufC, sufD, sufS, and sufE. Of the six ORFs, the
sufS gene and its product are the best characterized. This
gene encodes one of three NifS homologs in E. coli and also
has been named csdB (18). All three E. coli NifS homologs, IscS, CSD, and SufS/CsdB, catalyze the
elimination of sulfur from L-cysteine and
selenium from L-selenocysteine (18).
However, the SufS/CsdB protein was shown to be 290 times more active on
L-selenocysteine than on L-cysteine and was thus considered the E. coli counterpart of the mammalian selenocysteine lyase
(18). The gene products of the remaining five
suf genes are less well studied, but some show interesting
homologies to other characterized proteins. sufA encodes a
homolog of IscA which, together with the products of the
iscS and iscU genes, is involved in Fe-S cluster
formation and repair. The sufB, sufC, and sufD
genes encode components of an ATP binding cassette (ABC)
transporter. No biochemical data can be found with regard to these
three genes. However, genetic studies have shown that E. coli
sufC mutants have delayed soxR-dependent induction of a
soxS-lacZ gene fusion (22), and the stability
of the [2Fe-2S] ferric ion reductase protein encoded by
fhuF is decreased in sufD mutants
(24). The final gene in the operon, sufE,
encodes a conserved oxidoreductase, a homolog of which is present
downstream of the csd gene.
Although only
sufA,
sufB, and
sufC are
among the most highly induced genes,
sufD (b1681),
sufS (b1680), and
sufE (b1679) also
are induced
with higher ratios in the wild-type strain than in
the
oxyR strain (Table
4 and Fig.
2A). To confirm OxyR
regulation
of this operon and to map the start of the
suf
transcript, we
carried out primer extension assays (Fig.
2B).
Consistent with
the microarray data, we detected OxyR-dependent
induction of
sufA.
A strong primer extension product ending
in a T residue at position
1762442, 32 bp upstream of the
sufA start codon at position 1762410,
was observed when RNA
isolated from the wild-type strain was used
as the template. We also
carried out DNase I footprinting experiments
to test for OxyR binding
to the
sufA promoter. In a computational
scan of the
E. coli genome, we predicted a putative OxyR site
centered
at 1762663, 253 bp upstream of the
sufA start codon
(
41).
The DNase I footprinting carried out using a 378-bp
fragment from
the
sufA-
ydiH intragenic region
showed that oxidized OxyR exclusively
bound to the predicted site (Fig.
2C). However, this single OxyR
binding site was far upstream from the
end of the primer extension
product, and at all other known
OxyR-activated promoters, the
transcription factor binds at a position
overlapping or directly
upstream of the
35 sequence of the promoter.
Possibly, the initial
sufA transcript is longer and is
either processed or folded into
a complex secondary structure
impervious to reverse transcriptase.
Given the unusually high
conservation of the
sufA-ydiH intragenic
region
(
34), it is likely that the regulation of
sufA
expression
is complex. We did not observe strong Fur regulation of
sufA expression
under conditions used in our experiments
(data not shown). However,
two putative Fur binding sites, centered at
positions 1762460
and 1762466, have been predicted in the
suf promoter (K. Lewis,
B. Doan, M. Zheng, G. Storz, and
T. D. Schneider, unpublished
data), and Fur-dependent
expression of
sufD-lacZ and
sufS-lacZ fusions has
been observed previously (
24). More experiments
are needed
to fully understand the regulation of the
suf operon.
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FIG. 2.
OxyR-dependent induction of the suf
operon. (A) Structure of the suf operon and sequence of
the sufA promoter. The induction ratios observed for the
wild-type and oxyR mutant strains in the microarray
experiment are given below each gene. The sufA
transcription start is marked by the black arrow, and the start of the
corresponding ORF is denoted by a white arrow. The DNase I footprints
for OxyR binding are indicated by the dark boxes. Our computational
search (41) predicted an OxyR binding site of 9.6 bits
centered at position 922026. (B) Primer extension assays of
sufA expression in wild-type (MC4100) and
oxyR (GSO47) strains grown in LB medium.
Exponential-phase cultures were split into two aliquots: one aliquot
was left untreated, and the other was treated with 1 mM hydrogen
peroxide. The cells were harvested after 10 min, total RNA was
isolated, and primer extension assays were carried out with primer 820 specific to sufA. The neighboring sequencing reactions
were carried out with the same primer. (C) DNase I footprinting assays
of oxidized OxyR binding to the top and bottom strands relative to the
sufA promoter. The regions protected by OxyR on both
strands are indicated by the brackets. For OxyR binding to the top
strand, the 32P-labeled primer 828 and unlabeled primer 825 were used to PCR amplify a 187-bp fragment. For OxyR binding to the
bottom strand, the 378-bp NotI-BamHI
fragment of pGSO133 was labeled with 32P at the
BamHI site. The samples were run in parallel with
Maxam-Gilbert G/A sequencing ladders.
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(iii) Genes of unknown function.
Four ORFs of unknown
function, yaiA, yaaA, yljA, and
ybjM, showed much stronger peroxide induction in the
wild-type strain than in the oxyR deletion strain.
yaaA and yljA are conserved ORFs, but
experimental data about the function of the corresponding proteins
cannot be found in the literature. Primer extension assays confirmed
that transcripts initiating directly upstream of the predicted first
codon of the yaiA, yaaA, and yljA ORFs
are induced by hydrogen peroxide in an OxyR-dependent manner (data not
shown). The computational search for OxyR binding sites
(41) predicted a putative OxyR binding site centered at
position 922026 in the yljA promoter. Interestingly, we were
not able to detect a transcript that would encode the predicted
125-amino-acid (aa) YbjM ORF. Instead, Northern blots and primer
extension analysis showed that the OxyR-regulated grxA
transcript is approximately 600 nucleotides in length and extends into
the strand opposite ybjM. Inspection of the ybjM
antisense sequence revealed that this opposite strand also encodes an
81-aa ORF. The arrays used in our experiments do not distinguish
between strands. Thus, we suggest that the signal detected for
ybjM actually corresponds to OxyR activation of a gene which
is encoded on the opposite strand and is likely to be in an operon with
grxA.
(iv) Possible OxyR-repressed genes.
In comparing genes induced
by hydrogen peroxide in the wild type (Table 2) and the
oxyR mutant (Table 3), we noted a number of genes,
uxuA, ygaQ, ytfK, ydcH,
ydeN, and yaeH, that were induced more strongly
in the oxyR background. OxyR is both an activator and a
repressor. Thus, it is possible that OxyR represses these genes in
response to oxidative stress. Our computational search predicted an
OxyR binding site at position 4549044 between uxuAB (encoding mannonate hydrolase and mannonate oxidoreductase) and the
divergent gntP gene (encoding a possible gluconate permease) (Fig. 3). Since uxuB and
gntP also showed higher induction ratios in the absence of
OxyR, it is intriguing to speculate that the two divergent promoters
are repressed by oxidized OxyR. Similarly, there are two predicted OxyR
binding sites at positions 2784053 and 2784276 between ygaQ
and a putative divergent gene designated b2653, and both
ygaQ and b2653 showed a higher induction ratio in the
oxyR mutant strain. In this context, it also is
noteworthy that three genes, ybjC, nfsA/mdaA
(encoding nitrofuran reductase I activity B), and rimK
(encoding a ribosomal modification protein), divergent to
grxA were induced in the oxyR mutant but not
the wild-type strain. No OxyR binding sites were predicted upstream of
ytfK, ydcH, ydeN, and yaeH,
so these genes may or may not be repressed directly by OxyR. OxyR
binding to these promoters and the predicted sites will need to be
tested experimentally.
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FIG. 3.
Possible OxyR-dependent repression of
gntP and uxuAB; b2653,
ygaQ, ygaR, and b2656; and
ybjC, nfsA/mdaA, and
rimK. The gene organization of the corresponding operons
is shown. Predicted OxyR binding sites (41) of 7.0 bits
centered at position 4549044, 8.8 bits centered at position 2784053, and 5.4 bits centered at position 2784276 are underlined. The confirmed
OxyR binding site upstream of the grxA promoter
(39) is indicated by the black boxes. The transcription
starts documented for grxA and predicted for
ybjC are denoted by solid and dotted arrows,
respectively. The induction ratios observed for the wild-type and
oxyR mutant strains in the microarray experiment are
given below each gene.
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OxyR-independent responses.
Below, we describe the expression
of genes that are induced similarly by hydrogen peroxide in the
wild-type strain and the oxyR mutant strain. It is
interesting that among genes induced moderately in both the wild-type
strain and the oxyR deletion strain were a number of heat
shock genes (groEL, groES, grpE, dnaK, and htpG) including those encoding
proteolytic activities (clpA, clpB, clpX, and
clpP). SOS genes (recA, recN,
lexA, and dinD); sulfate and cysteine metabolism
genes (cysKAUPNDHJ and sbp); genes specifying
tricarboxylic acid cycle enzymes (acnA and fumA);
the nrdHIEF operon, which directs synthesis of a second ribonucleotide reductase system; and the universal stress gene uspA also were induced to some extent in both the wild-type
strain and the mutant strain. In contrast, the expression of many
ribosomal protein genes, cold shock genes, ATP synthase genes, and
transporter genes was repressed.
(i) SoxRS regulon.
The SoxRS regulon was reported previously
to be induced primarily by superoxide-generating compounds and not by
hydrogen peroxide (23). Thus, we were surprised to find
that several members of this regulon such as fpr (encoding
ferredoxin-flavodoxin reductase) and sodA (with an induction
ratio of 8 and encoding manganese superoxide dismutase), as well as
soxS itself, were among the genes most strongly induced by 1 mM hydrogen peroxide in both the wild-type background and the
oxyR mutant strain background. To directly compare the
induction of OxyR and SoxR target genes by both hydrogen peroxide and
superoxide-generating compounds, we treated wild-type cells with either
0, 0.01, 0.03, 0.1, 0.3, and 1 mM hydrogen peroxide or the same
concentrations of paraquat (methyl viologen), a standard inducer of the
soxRS regulon. We then carried out primer extension assays
to examine the expression of oxyS, a primary OxyR target,
and soxS, the only known SoxR target (Fig.
4). As expected, oxyS was
strongly induced by all concentrations of hydrogen peroxide and
soxS was induced by all concentrations of paraquat,
consistent with the notion that OxyR primarily senses hydrogen peroxide
while SoxR primarily responds to superoxide-generating compounds.
However, we also observed that soxS was partially induced by
high concentrations of hydrogen peroxide and that oxyS was
slightly induced by high concentrations of paraquat.
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FIG. 4.
oxyS and soxS induction by
hydrogen peroxide and paraquat. The figure shows the results of primer
extension assays of oxyS and soxS
transcript levels in wild-type (MC4100) cells grown in LB medium. An
exponential-phase culture was split into aliquots: one aliquot was left
untreated, and the other aliquots were exposed to the indicated
concentrations of hydrogen peroxide and paraquat. The cells were
harvested after 5 min, total RNA was isolated, and primer extension
assays were carried out with primer 188 specific to oxyS
and primer 823 specific to soxS.
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(ii) isc operon.
The isc gene
cluster, yfhP (b2531), iscS/yfhO (b2530),
iscU/yfhN (b2529), iscA/yfhF (b2528),
hscB (b2527), hscA (b2526), fdx (b2525), and yfhJ (b2524), has received attention due to its
role in Fe-S cluster formation and cysteine-related metabolism
(12, 25, 38). The fact that Fe-S cluster damage is a major
consequence of oxidative stress prompted us to examine the regulation
of this cluster. The expression profiles indicated that the first four genes (yfhP, iscS, iscU, and iscA) in
the cluster were modestly induced in both the wild-type strain and the
oxyR deletion strain (Fig.
5A). The induction ratios for the last
four genes (hscB, hscA, fdx, and
yfhJ) were within the error of the experiment, suggesting
that these four genes were not induced and that they are regulated
differently. This result is consistent with a report that the
hscBA genes are transcribed independently of the
isc genes (15). Primer extension assays showed
that isc operon induction by hydrogen peroxide (Fig. 5B) and
paraquat (data not shown) was independent of both OxyR and SoxRS. These
assays also allowed the transcription start to be mapped to a G residue
(on the strand opposite the one shown in Fig. 5A) at position 2660219, 68 bp upstream of the yfhP start codon.
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FIG. 5.
OxyR- and SoxRS-independent induction of the
isc operon. (A) Structure of the isc
operon and sequence of the yfhP promoter. The induction
ratios observed for the wild-type and oxyR mutant
strains in the microarray experiment are given below each gene. The
yfhP transcription start is marked by the black arrow,
and the start of the corresponding ORF is denoted by a white arrow. (B)
Primer extension assays of yfhP expression in wild-type
(MC4100), oxyR (GSO47), soxRS
(GSO71), and fur (GSO72) strains grown in LB medium.
Exponential-phase cultures were split into two aliquots: one aliquot
was left untreated, and the other was treated with 1 mM hydrogen
peroxide. The cells were harvested after 10 min, total RNA was
isolated, and primer extension assays were carried out with primer 686 specific to yfhP. The neighboring sequencing reactions
were carried out with the same primer.
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(iii) Induction of other genes.
Among the other genes whose
expression was strongly induced in an OxyR-independent manner were
cysK, encoding cysteine synthase, which catalyzes the last
step in cysteine synthesis; sbp and cysP, encoding periplasmic sulfate binding proteins; and dsdA,
encoding a D-serine deaminase. We also observed
modest induction of other genes in the cysteine biosynthesis pathway.
The induction of these genes suggested a concerted effort to accumulate
more cysteine in response to hydrogen peroxide treatment. Two other
genes, tnaA and tnaL, that were highly induced in
an OxyR-independent manner are involved in amino acid catabolism. The
ibpA and ibpB genes encoding heat shock proteins
also were strongly induced in both the wild-type and oxyR
strains (Tables 1 and 2). The observed induction of the genes encoding
the HSP20 chaperones in response to oxidative stress was consistent
with a recent report that ibpA-, ibpB-, and
ibpAB-overexpressing strains are resistant not only to heat
but also to paraquat treatment (14).
There are 10 genes of unknown function among the most highly induced
genes whose expression is independent of OxyR.
yfiA was
strongly induced (36-fold) in the wild-type strain and became
the most
strongly induced (109-fold) gene in the
oxyR mutant
strain. The function of YfiA is not clear. Recent reports have
shown
that the YfiA protein is associated with 70S ribosomes and
stabilizes
ribosomes against dissociation (
1,
16). Nine other
strongly induced genes encode relatively small ORFs:
yjiD
(133
aa),
ymgB (88 aa),
yeeD (75 aa),
ycfR (85 aa, induced 9-fold in
the
oxyR
strain),
ycgZ (78 aa, induced 9-fold in the
oxyR strain),
ymgA (90 aa, induced 3-fold in
the wild type),
yceP (84 aa, induced
10-fold in the wild
type),
ynaF (144 aa, induced 8-fold in the
wild type), and
ycgK (133 aa, induced 9-fold in the wild type).
Homology
searches suggest that
ynaF encodes a filament protein.
YeeD
and YcfR show homology to other unknown ORFs, but all of
the other
genes encoding the small ORFs at best have very low
scores in BLAST
searches. We note that the small size of many
of these predicted
proteins may have precluded them from being
detected on the
two-dimensional gels initially used to characterize
the response to
hydrogen
peroxide.
| |
DISCUSSION |
Use of DNA microarrays to characterize the oxidative stress
response.
DNA microarray technology already has been shown to be a
useful tool in studying global expression patterns in response to a
number of different growth conditions; here, we examine the E. coli response to oxidative stress. In the experiment that we have
presented, we were able to confirm the induction of many oxidative
stress genes that were laboriously identified over a period of almost
20 years. In addition, we were able to identify several new hydrogen
peroxide-inducible genes: some new members of the OxyR regulon and
others induced by an OxyR-independent mechanism. We do note a few
limitations of our experiment. First, since the glass slides that we
used carry only DNA corresponding to ORFs, we did not detect expression
of the strongly induced OxyS RNA. Second, for reasons that are not
understood, the induction of some of the OxyR-regulated ORFs such as
dsbG was not detected. Thus, it has been an advantage to
simultaneously carry out a computational search for additional OxyR
binding sites (41). A third limitation is that the arrays
are not strand specific. From the array data, we assumed that the
annotated ybjM gene was induced by OxyR; however, primer
extension and Northern experiments showed that hydrogen peroxide
treatment actually leads to the induction of a transcript on the
opposite strand. Despite the limitations listed above, future
microarray experiments to examine the global gene response to hydrogen
peroxide and other oxidants over a range of concentrations and times
should give even further insight into the E. coli response to oxidative stress. Experiments to examine the gene expression profiles in specific mutants also should help to further delineate the
roles of specific regulators. For example, by examining the hydrogen
peroxide response in strains lacking the OxyS small RNA regulator, we
may be able to differentiate those genes regulated directly by OxyR and
those regulated indirectly through OxyS RNA.
Identification of OxyR-regulated genes.
We have identified
several new OxyR-regulated genes. One example is hemH
encoding the ferrochelatase that catalyzes the conversion of
protoporphyrin IX to protoheme, the final step of protoheme biosynthesis. Heme is an essential cofactor for both the
katG- and the katE-encoded hydroperoxidase
enzymes, and it has long been known that katG transcription
and hydroperoxidase I activity are strongly induced in response to
oxidative stress. If ferrochelatase is the limiting step in protoheme
biosynthesis, the induction of hemH may be needed to satisfy
the need for increased heme levels associated with increased
hydroperoxidase production. Protoporphyrin IX can generate reactive
oxygen species in the presence of light (21). Thus, the
induction of hemH may be important to reduce the
concentration of the potentially toxic protoporphyrin IX intermediate. Since hydrogen peroxide oxidizes the pool of intracellular ferrous iron, increased ferrochelatase production also may be required to allow
for the enzyme to compete for lowered levels of iron. Additional
experiments are needed to distinguish between these possible
explanations for the OxyR-dependent induction of hemH. It is
interesting that, in Bacillus subtilis, an operon
(hemAXCDBL) encoding enzymes for the early steps of heme
biosynthesis is induced by hydrogen peroxide (6, 8),
although our DNA microarray experiments did not provide evidence for
the induction of the corresponding genes in E. coli.
We also discovered that the
sufA, sufB, sufC, sufD, sufS,
and
sufE genes are part of the OxyR regulon. The observation
that
all of the genes were induced by hydrogen peroxide in an
OxyR-dependent
way is consistent with a previous proposal that these
genes form
an operon (
24). Although the exact in vivo
function of the
suf operon is not clear, limited biochemical
evidence suggests that
suf-encoded proteins are involved in
Fe-S cluster and/or S and/or
Se metabolism. Since Fe-S clusters are one
of the primary cellular
targets of oxidative stress (reviewed in
reference
29), there
is a clear need to induce proteins
that help to assemble or repair
these clusters. Patzer and Hantke
(
24) isolated
sufD and
sufS mutants
based on their requirement for the
fhuF-encoded ferric
ion
reductase activity. Given this observation, it seems contradictory
that
the
suf operon is induced by oxidized OxyR while
fhuF is
repressed by oxidized OxyR (
41). We
suggest that this opposing
regulation indicates that the
suf-encoded proteins are required
for cellular functions in
addition to FhuF. In general, since
hemH and the
suf operon, as well as some of the OxyR-regulated
genes of
unknown function, are highly conserved among prokaryotic
species,
future genetic and biochemical studies of these genes
and their gene
products will increase our understanding of cellular
defenses against
oxidative
stress.
Overlap with other regulatory pathways.
We observed
soxS induction by 1 mM hydrogen peroxide in our DNA
microarray measurements and, by primer extension assays, confirmed that
soxS could be induced by 0.3 and 1 mM hydrogen peroxide. Recent assays of a SoxRS-regulated
micF::luxCDABE fusion (4) and measures of soxS transcript levels by multiplex reverse
transcription-PCR (17) also suggest that SoxR is activated
by high concentrations of hydrogen peroxide. These results expand the
overlap between the superoxide and peroxide responses in E. coli. The observed soxS induction may be due to some
SoxR oxidation by high peroxide concentrations. Alternatively, hydrogen
peroxide might lead to the generation of another signal that activates
SoxR or to inefficient SoxR reduction, by as yet uncharacterized
mechanisms. Two known members of the SoxRS regulon, fpr and
sodA, were among the most highly hydrogen peroxide-induced
genes in both the wild-type and the oxyR mutant cells. It
is possible that the expression of other transcripts that are induced
independently of OxyR is under the control of the SoxRS regulators.
Our DNA microarray results also show that there is overlap between the
oxidative stress and heat shock and SOS responses.
This overlap was
presaged by the initial two-dimensional gel experiments
(
20,
33) as well as by assays of small panels of stress-responsive
promoters fused to
luxCDABE (
4). A systematic
identification
of all the genes regulated by particular transcription
factors
should help to map out the complex genetic regulatory network
among the different stress responses. Two recent studies have
examined
the whole-genome expression pattern in
Saccharomyces cerevisiae cells exposed to a variety of stress conditions
including
oxidative stress and heat shock (
7,
11). One
difference between
the bacterial and yeast responses to hydrogen
peroxide is noteworthy;
while there is a predominant, clearly defined
OxyR-regulated response
in
E. coli, the
S. cerevisiae response involves a large set of
general stress
proteins. In the
oxyR mutant strain, the induction
of
other general stress transcripts becomes more pronounced, making
the
peroxide response in the
oxyR strain more akin to the
S. cerevisiae response. Possible parallels can be drawn
between the
response to oxidative stress and that to amino acid
starvation.
While wild-type
E. coli cells induce specific
operons in response
to deprivation of specific amino acids (for
example, Khodursky
et al. [
13] describe the specific
response to tryptophan starvation),
wild-type
S. cerevisiae
cells induce a generalized response upon
encountering a limited supply
of any one amino acid. Inactivation
of an
E. coli response
to a particular amino acid-mediated regulatory
circuit results in an
emphasis upon the second, more generalized
stringent
response.
Our study points out that the activities of transcription factors, in
addition to OxyR and SoxRS, may be modulated by oxidative
stress. An
example of such regulation is the
isc operon. Both
microarray and primer extension measurements showed that
isc
expression
is induced by peroxide. Given the role of the
isc
gene products
in Fe-S assembly, this induction is not surprising.
However, it
was unexpected to find that the induction is independent of
both
OxyR and SoxR, indicating the existence of an unidentified redox
regulatory pathway. We also were intrigued by the strong
OxyR-independent
induction of the
yfiA gene. Identification
of these alternate
pathways of hydrogen peroxide-dependent gene
induction and the
characterization of the redox sensing mechanisms
involved are
important directions for future
studies.
| |
ACKNOWLEDGMENTS |
We thank L. Heineman and E. DeRose of DuPont for assistance in
data processing and J. Imlay for useful comments on the manuscript.
The work in Bethesda was supported by the intramural programs of the
National Institute of Child Health and Human Development and the
National Cancer Institute and a fellowship from the American Cancer
Society (M.Z.).
| |
FOOTNOTES |
*
Corresponding author. Mailing address: NIH, Building
18T, Room 101, 18 Library Dr., MSC 5430, Bethesda, MD 20892-5430. Phone: (301) 402-0968. Fax: (301) 402-0078. E-mail:
storz{at}helix.nih.gov.
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Journal of Bacteriology, August 2001, p. 4562-4570, Vol. 183, No. 15
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.15.4562-4570.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
