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Journal of Bacteriology, May 1999, p. 2958-2962, Vol. 181, No. 9
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Expression of Two Glutathione S-Transferase Genes in
the Yeast Issatchenkia orientalis Is Induced by
o-Dinitrobenzene during Cell Growth Arrest
Hisanori
Tamaki,*
Kenji
Yamamoto, and
Hidehiko
Kumagai
Division of Applied Life Sciences, Graduate
School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
Received 28 December 1998/Accepted 20 February 1999
 |
ABSTRACT |
Glutathione S-transferases (GSTs) Y-1 and Y-2 from the
yeast Issatchenkia orientalis were purified by passage
through a glutathione-agarose column, and the cDNA for GST Y-1 was
cloned and sequenced. The deduced amino acid sequence consisted of 188 residues with a total calculated molecular mass of 21,001 Da and showed
36.7% identity to that of GST Y-2, another GST isoenzyme expressed in
this strain. Escherichia coli DH5
transformed with
pUC119 harboring the GST Y-1 gene under the control of the
lac promoter exhibited 29-fold-higher GST activity than the
same strain with pUC119. Northern blot analysis revealed that both
genes were highly expressed in cells cultured in the presence of 200 µM o-dinitrobenzene (DNB), one of the substrates of GST,
while only the GST Y-1 gene was expressed, and only slightly, under
normal (DNB-free) culture conditions. The DNB in the medium arrested
cell growth until it was reduced by conjugation with reduced
glutathione. Kinetic analysis of GST gene expression during detoxification of DNB revealed that the levels of expression of both
genes were elevated within 3 h after the addition of DNB and that
they further increased until 12 h postaddition. The levels of
expression of both genes were decreased markedly when the DNB concentration in the culture medium was lowered. These results suggest
that I. orientalis cells sense xenobiotics and arrest cell
growth as a mechanism for preventing the induction of mutations by
these compounds, while the levels of expression of the GST genes are
up-regulated for detoxification.
| |
TEXT |
Glutathione S-transferase
(GST; EC 2.5.1.18) catalyzes the conjugation of reduced glutathione
(GSH) to a wide variety of electrophilic xenobiotics. Based on sequence
similarity and substrate specificity, the cytosolic GSTs comprise a
gene superfamily that includes six subclasses: alpha, mu, pi, theta,
kappa, and zeta (2, 6, 9, 10, 16). GST-alpha, -mu, and -pi
are abundant in human, rat, and mouse tissues and are thought to play a
major role in the detoxification of electrophilic xenobiotics,
including carcinogens. Some GST species were shown to be highly induced in tumor cells. High levels of GST-pi gene expression were frequently found in cell lines which became resistant to anticancer drugs, although high levels of GST-alpha and -mu expression were also often
observed. The mechanism of induction of GST has also been studied in
mammalian cell lines, and several cis-acting elements have
been detected in the 5'-flanking regions of various GST genes, including the antioxidant-responsive element (ARE) (19), the 12-O-tetradecanoyl phorbol-13-acetate-responsive element
(14), the xenobiotic-responsive element (XRE)
(18), and the GST-P enhancer element (20). Thus,
the relationship of GSTs to drug resistance in tumor cells has been
extensively studied in mammals.
GSTs have also been found in plants (11, 21) and insects
(27), and these enzymes were shown to be related to
resistance to herbicides and pesticides, respectively. GST genes have
been isolated from the prokaryotes Proteus mirabilis
(17), Methylophilus sp. strain DM11
(1), and Escherichia coli (13). In the
yeast Saccharomyces cerevisiae, the gene encoding the
regulatory protein Ure2p was shown to have sequence similarity to the
theta-class GSTs of maize and Drosophila melanogaster
(15); however, no GST activity was detected in Ure2p.
Recently, genes encoding two novel membrane-bound GSTs, GTT1
and GTT2, were identified in S. cerevisiae
(4). However, it is still not clear whether soluble GST
plays a major role in drug resistance in yeasts.
We have found GST activity in various yeast strains (8) and
have purified and characterized two GST isoenzymes, GST Y-1 and Y-2,
from the yeast Issatchenkia orientalis (26).
Also, cloning of the GST Y-2 gene and its expression in E. coli were carried out (24, 25). Conjugation of
o-dinitrobenzene (DNB) to glutathione and metabolism of
glutathione conjugate in the yeast I. orientalis were
studied, and the mechanism of detoxification of this xenobiotic in
I. orientalis was determined (23). Other investigators reported that overexpression of the GST Y-2 gene in
S. cerevisiae led to an increase in resistance to DNB, and GST Y-2 was shown to be involved in detoxification of DNB
(31). Here, we report the isolation and nucleotide sequence
of the GST Y-1 gene from the yeast I. orientalis. Also, the
expression levels of the GST Y-1 and Y-2 genes in response to the
addition of DNB, an electrophilic xenobiotic, were examined.
Purification of GSTs Y-1 and Y-2 by affinity chromatography.
Previously, we reported the purification and properties of GSTs Y-1 and
Y-2 (26) and the cloning and sequencing of GST Y-2. However,
the GST Y-1 gene has not yet been cloned because of the low yield of
this protein. Since GST Y-1 showed 10-fold-higher specific activity
than Y-2 and has been suggested to play a major role in detoxification
in cells, it was deemed important to clone this gene. We have developed
methods for the purification of GSTs Y-1 and Y-2. Purification of GSTs
Y-1 and Y-2 from I. orientalis was performed by two-step
column chromatography, using DEAE-cellulose and glutathione-agarose
(Table 1). Cell growth conditions, cell extract preparation, protamine treatment, DEAE-cellulose column chromatography, and GST and protein assays were done as previously described (26). The active fractions from the DEAE-cellulose column were applied to a glutathione-agarose (Sigma Chemical Co., catalog no. G4510) column (2 by 10 cm) which was equilibrated with 50 mM potassium phosphate buffer, pH 7.0, containing 1 mM EDTA, 10 mM
sodium sulfite, and 20% glycerol (stabilizing buffer). The column was
washed with 4 volumes of the same buffer after sample application. GST
activity was eluted with four volumes of the same buffer supplemented
with 5 mM GSH and 0.5 M NaCl. There are two different types of
glutathione-agarose available from commercial sources; in one type
(Sigma Chemical Co.; catalog no. G4510), GSH is attached to the agarose
by a sulfur moiety, while in the other (Sigma Chemical Co.; catalog no.
G9761) it is attached via the -amino group of the glutamyl residue.
GST activity bound only to the former type of glutathione-agarose (Sigma catalog no. G4510) (data not shown), indicating that the -amino group of the glutamyl residue is necessary for recognition of
glutathione as a substrate by GSTs Y-1 and Y-2.
The active fraction from the GSH-agarose column showed two bands on
sodium dodecyl sulfate-polyacrylamide gel electrophoresis
(SDS-PAGE)
gels, with molecular masses of 23 and 21 kDa (data
not shown), which
corresponded with the sizes of GST Y-2 and GST
Y-1, respectively. Both
proteins were subjected to protein sequencing
without further
purification.
Protein sequence analysis and synthesis of an oligonucleotide
probe.
Proteins in the eluted fractions from the GSH-agarose
column were separated by SDS-PAGE and then electroblotted onto
Immobilon-PSQ polyvinylidene difluoride membranes (Millipore Co.). Two
protein bands that stained with Ponceau S were cut out and applied to an automated protein sequencer. The protein with a mass of 23 kDa gave
the sequence N-Thr-Phe-Ala-Thr-Val-Tyr-Ile-Lys-C, which was identical
to the N-terminal sequence of GST Y-2 (25). The other
protein, with a mass of 21 kDa, gave the sequence
N-Thr-Phe-Gly-Thr-Leu-Tyr-Ile-Leu-Pro-Pro-C and was thought to be GST
Y-1. To determine more of the sequence of the 21-kDa protein, the
active fraction was subjected to SDS-PAGE and the 21-kDa protein band,
which stained with Coomassie blue, was cut out and electroeluted. The
isolated 21-kDa protein was subjected to treatment with lysyl
endopeptidase and then purified by high-performance liquid
chromatography. Two purified lysyl endopeptidase-produced fragments
gave
the sequences N-Trp-Leu-Ser-Phe-Ala-Asn-Ser-Asp-Leu-Cys-Gly-Ala-Met-Val-Gly-Val-Trp-Phe-Cys-Lys-C and N-Tyr-Leu-Gly-Leu-Glu-Ile-Asn-Val-Lys-C. From the partial amino
acid sequence underlined in the former peptide sequence, a 17-mer
degenerate oligonucleotide probe was synthesized
[5'-TG(T/C)GG(G/A/T/C)GC(G/A/T/C)ATGGT(G/A/T/C)GG-3'].
cDNA cloning and sequencing of the GST Y-1 gene.
A 
gt10
cDNA library, constructed from poly(A)+ RNA purified from
I. orientalis cultured with DNB, was screened with the
degenerate oligonucleotide probe described above. Several positive
clones were obtained from the 50,000 plaques screened. One of the
positive clones, containing a 0.7-kb cDNA fragment, was isolated, and
the cDNA fragment was subcloned into the EcoRI site of
pUC119 to construct pGS148. E. coli DH5 transformed with
pGS148 showed 29-fold-higher GST activity (94 mU/mg) than the same
strain transformed with pUC119 (3.2 mU/mg) when cultured with
isopropyl-
-D-thiogalactopyranoside (IPTG), and this
suggested that the cDNA contained the GST Y-1 gene. A 0.7-kb cDNA
fragment sufficient to cover the GST Y-1 gene was sequenced in both
directions. A single open reading frame, consisting of 188 amino acid
residues with a calculated total molecular mass of 21,001 Da, was
found, which agreed with the results obtained by SDS-PAGE. This open
reading frame contained amino acid sequences showing complete identity
with those of the N-terminal and lysyl endopeptidase-produced fragments
from the purified 21-kDa protein (Fig.
1).
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FIG. 1.
Alignment of amino acid sequences of several theta-class
GSTs. Each amino acid sequence was deduced from the cloned-DNA sequence
(GST Y-2 [25], maize GST I [21],
maize GST III [11], P. mirabilis GST
[17], and E. coli GST
[13]). Amino acid positions are indicated on the
right. The amino acid residues conserved with those of GST Y-1 are
shaded. Asterisks indicate the amino acids completely conserved in the
six GSTs. The double dagger indicates conserved serine residues in
theta-class GSTs.
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|
The deduced amino acid sequence of GST Y-1 was compared with those of
GSTs from other species. GST Y-1 showed the highest
degree of homology
(36.7% over 188 amino acid residues) to GST
Y-2, another GST isoenzyme
in
I. orientalis.
The major cytosolic GSTs were grouped into four classes, designated
alpha, mu, pi (
9), and theta (
10), according to
their
primary structures and other properties. GST Y-1 did not show
any
significant homology to mammalian GSTs of the alpha, mu, or
pi classes
(data not shown) but showed a slight sequence similarity
to theta-class
enzymes, such as bacterial GSTs from
E. coli (20.5%
over
166 amino acids) (
13) and
P. mirabilis (26.4%
over 159
amino acids) (
17) as well as GSTs I (
21)
and III (
11) from
maize (25.9% over 143 amino acids and
24.0% over 104 amino acids,
respectively) (Fig.
1).
X-ray crystallographic studies have shown that the alpha-, mu-, and
pi-class GSTs exhibit similar topological patterns despite
their low
degree of identity at the primary-structure level (
30).
The
N-terminal domain of each class of GST has been considered
to be very
important for GSH binding, and site-directed mutagenesis
studies have
suggested that the highly conserved Tyr residue near
the N terminus is
essential for catalytic activity which may activate
GSH by promoting
thiolate anion formation (
7,
22). Recently,
the crystal
structure of a theta-class enzyme from
Lucilia cuprina was
reported (
29). Although its structure was similar to those
of the other GSTs, and the Tyr residue near the N terminus was
conserved, the hydroxyl group of the Ser residue in the N-terminal
domain was found to be close to the position of the conserved
Tyr
residue of the mammalian GSTs (alpha, mu, and pi) on superposition
of
the GST crystal structures. Site-directed mutagenesis experiments
also
revealed that the Ser residue in the N-terminal region of
theta-class
GSTs plays the same important role in catalysis as
the Tyr residue in
alpha-, mu-, and pi-class GSTs (
3).
Although the Ser residue was conserved in GST Y-1, it was replaced by a
Thr residue in GST Y-2. Since the replacement of a
Ser residue with Thr
in theta-class enzymes reduced activity (
3),
the difference
in the specific activities of GSTs Y-1 and Y-2
(GST Y-1 showed
10-fold-higher specific activity with 1-chloro-2,4-dinitrobenzene
[CDNB] than did GST Y-2) might have been due to this amino acid
residue.
Effects of DNB on GST gene expression.
We previously reported
that cells cultured with DNB showed increased GST activity
(8). To determine whether DNB affects GST Y-1 or Y-2 gene
expression, Northern blot analysis was performed. Total RNA was
prepared from exponential-phase cells cultured with or without 200 µM
DNB, and 20 µg of each RNA sample was subjected to Northern blot
analysis with GST Y-1 or Y-2 cDNA as a probe (Fig.
2). The expression level of GST Y-1 in
cells cultured with DNB was 7.7-fold higher than that in cells cultured
without DNB. High levels of GST Y-2 gene expression were also observed
in cells cultured with DNB, while no expression of GST Y-2 was detected under normal (DNB-free) culture conditions. These results indicate that
expression of both GST genes is strongly induced by DNB.
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FIG. 2.
Northern blot analysis. Twenty-microgram portions of
total RNA extracted from I. orientalis cultured with
(induced [I]) or without (control [C]) 200 µM DNB were loaded
onto 1% agarose gels and, after electrophoresis, stained with ethidium
bromide (bottom). After proteins were blotted onto Hybond
N+ nylon membranes, hybridization was performed with
32P-labeled GST Y-1 (top left) or Y-2 (top right) cDNA
probe (2 × 106 cpm/ml). The positions of 25S and 18S
rRNAs are indicated on the right.
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|
We also reported previously that when DNB was added to the culture
medium, cell growth was repressed for about 48 h and then
cells
began to grow with highly induced GST activity (
23). To
examine the responses of the GST Y-1 and Y-2 genes to DNB, two
sets of
time course experiments were performed. First, the early
response to
addition of DNB was analyzed. Cells were grown in
20 liters of yeast
extract-peptone-dextrose (YEPD) medium containing
200 µM DNB, and
every 3 h after DNB addition 2 liters of culture
was removed and
cell growth was monitored by determining the optical
density at 600 nm.
Cells in each sample were precipitated by centrifugation
and flash
frozen in liquid nitrogen prior to RNA extraction, and
each supernatant
was subjected to high-performance liquid chromatography
as described
previously (
23). Once DNB was added to the culture
medium,
cell growth was repressed immediately, and this growth
arrest lasted
for at least 48 h (Fig.
3C and D).
The DNB concentration
in the culture medium did not change for 48 h (Fig.
3D), while
the levels of expression of both the GST Y-1 and Y-2
genes were
already increased at 3 h after DNB addition (Fig.
3A).
The levels
of expression of both genes increased and reached a plateau
at
12 h after addition of DNB. After a lag phase caused by DNB
addition,
I. orientalis started to grow again, detoxifying
DNB (as a glutathione
conjugate), which was enzymatically digested to
S-2-nitrophenyl
cysteine and secreted into the culture
medium (
23). We next
monitored the genetic responses when
cells again started to grow
with a high detoxifying capability. Cells
started to grow exponentially
after a 48-h lag phase, and the DNB
concentration in the culture
medium decreased in inverse proportion to
cell population growth
(Fig.
3D). Both the GST Y-1 and Y-2 genes were
highly expressed
at early exponential phase (48 and 54 h), but the
levels of expression
of both genes were markedly reduced 3 h
later, in the middle of
the exponential growth phase (57 h), at which
time most of the
DNB in the culture medium had been detoxified by
glutathione conjugation
(Fig.
3B). These results indicated that the
levels of expression
of both GST genes were regulated by the DNB
concentration in the
medium and that the response of these genes to DNB
was very rapid.
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FIG. 3.
Effects of DNB on cell growth and GST gene expression.
I. orientalis cells grown in YPD medium to late exponential
phase were inoculated into a jar fermentor containing 20 liters of YPD
medium, and the cells were further cultivated after DNB was added to
200 µM. (A and B) Before and after DNB addition, cell cultures were
sampled at the indicated times and samples were subjected to Northern
blot analysis. Levels of GST Y-1 (top) and GST Y-2 (middle) mRNAs are
shown. Total RNA was loaded onto agarose gels, electrophoresed, and
stained with ethidium bromide (bottom). (A) Cells cultured for 0 to
12 h; (B) cells cultured for 32 to 78 h. (C and D) Cell
growth and DNB concentration (conc.) in the culture medium were also
analyzed. (C) Cells cultured for 0 to 12 h; (D) cells cultured for
32 to 78 h. OD600nm, optical density at 600 nm.
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The mechanisms of induction of several GST isoenzymes from mammals have
been studied. Analysis of the 5'-flanking region of
the rat liver GST
Ya subunit gene revealed two
cis-acting regulatory
elements
(
12): an XRE (
18) and an ARE (
12). The
XRE is also
found in the 5'-flanking region of the cytochrome P-450IA1
gene
and has been shown to be responsible for activation by planar
aromatic compounds. The ARE is distinct from the XRE and mediates
induction by the metabolites of several planar aromatic compounds
as
well as reactive oxygen species. In this study, the activities
of both
GST Y-1 and GST Y-2 were induced markedly by the addition
of DNB, an
electrophilic compound. Since the induction of both
genes was dependent
on the presence of DNB in the medium, there
might be an upstream
regulatory element(s) such as an XRE or ARE
in these genes. Further
studies are necessary to elucidate the
mechanisms of induction of GSTs
in yeast
cells.
In this study, DNB was shown to induce the expression of two GST genes.
Some electrophiles are also known to cause DNA damage
which affects the
cell cycle. It has been reported that many types
of cells respond to
DNA damage by regulating progression through
subsequent mitotic cell
cycles (
28). Regulation of cell cycle
transitions in
response to damage is a result of signal transduction
pathways called
checkpoints (
5). In the yeast
S. cerevisiae,
checkpoints responding to DNA damage or to inhibition of DNA
replication
regulate entry into and progression through S phase and
mitosis.
Since DNB is an electrophilic compounds which is known to
react
with nucleophilic residues in nucleotides and proteins, it is
possible that DNB causes DNA damage or inhibits DNA replication,
resulting in G
1 or G
2 arrest. Our observation
that the addition
of DNB repressed cell growth is consistent with the
cell cycle
arrest mechanism of electrophiles. Thus, it is plausible
that
I. orientalis cells monitor toxic compounds in the
environment
and arrest the cell cycle as a means of preventing the
induction
of mutation by these compounds while inducing detoxifying
systems
such as GST to protect
themselves.
Nucleotide sequence accession number.
The nucleotide sequence
of the 711-bp cDNA encoding the GST Y-1 gene has been submitted to the
DDBJ/EMBL/GenBank databases under accession no. AB021655.
| |
ACKNOWLEDGMENTS |
This work was supported by a grant-in-aid for scientific research
(10306007) from the Ministry of Education, Science, and Culture of Japan.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Division of
Applied Life Sciences, Graduate School of Agriculture, Kyoto
University, Kyoto 606-8502, Japan. Phone: (81)-75-753-6278. Fax:
(81)-75-753-6275. E-mail:
noritama{at}kais.kyoto-u.ac.jp.
| |
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Journal of Bacteriology, May 1999, p. 2958-2962, Vol. 181, No. 9
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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