Plant Physiology 132:1149-1152 (2003)
© 2003 American Society of Plant Biologists
SCIENTIFIC CORRESPONDENCE
Redox Control of Protein Tyrosine Phosphatases and Mitogen-Activated Protein Kinases in Plants
Rajeev Gupta and
Sheng Luan*
Plant and Microbial Biology, University of California, Berkeley,
California 94720 (R.G., S.L.)
Environmental conditions, including light, temperature, water status, and
soil salinity, all modify the redox state of plant cells
(Allen et al., 1995 ). A number
of studies have shown that oxidative stress is a common factor that affects
plant growth and development under extreme environmental conditions (for
review, see Mittler, 2002).
Most recently, oxidative stress agent H2O2 has been
shown to serve as a critical messenger molecule in many signal transduction
pathways, including plant responses to pathogen, plant hormone abscisic acid,
and abiotic stress factors (Wojtaszek,
1997; Pei et al.,
2000; Bolwell et al.,
2001; Mittler,
2002). At least one of the mechanisms underlying
H2O2 function is the activation of calcium channels
(Pei et al., 2000;
Chico et al., 2002). Here, we
report that plant Tyr phosphatases such as AtPTP1
(Xu et al., 1998) serve as
targets for H2O2 and this may be associated with the
regulation of mitogen-activated protein (MAP) kinase activity in plants.
Although Ser/Thr and Tyr kinases/phosphatases play a critical role in cell
growth and development in animals, none of the typical Tyr kinases has been
characterized from higher plants. The existence of Tyr phosphatases in plants
has also been controversial until recently when several members of protein Tyr
phosphatase (PTP) family were characterized from Arabidopsis
(Gupta et al., 1998;
Xu et al., 1998;
Fordham-Skelton et al., 1999,
2002; Ulm et al.,
2001,
2002;
Gupta et al., 2002). These
studies suggest that protein Tyr (de) phosphorylation performs critical
functions in plants. In support of this hypothesis, biochemical and genetic
analyses confirm that Tyr phosphorylation, like that in animals and fungi, is
involved in the regulation of MAP kinase activities in plant cells (for
review, see Tena et al., 2001;
Zhang and Klessig, 2001;
Luan, 2002;
Ulm et al., 2002).
PTPs from all organisms contain an active site signature motif, (I/V)
HCXAGXXR(S/T) G, which harbors the catalytic cysteinyl residue involved
in formation of a phosphoenzyme reaction intermediate
(Guan, 1994). The PTPs are
categorized into three groups based on the studies in animals: receptor-like
PTP, intracellular PTP, and dual-specificity PTP (DsPTP;
Stone and Dixon, 1994). The
receptor-like PTPs appear to be found in animals, but not in fungi and plants.
The other two categories exist in all eukaryotes, including plants (Gupta et
al., 1998,
2002;
Xu et al., 1998;
Fordham-Skelton et al., 1999,
2002; Ulm et al.,
2001,
2002). Cys residue in the
catalytic domain is essential for the catalytic activity of PTPs from plants
as well as animals (Gupta et al.,
1998,
2002;
Xu et al., 1998) In animals,
it has been shown that oxidative stress inactivates the PTPs
(Caselli et al., 1998;
Denu and Tanner, 1998;
Lee and Esselman, 2002). In
one of the receptor-like PTPs, H2O2 induces a rapid and
reversible catalytic Cys-dependent conformation change in vivo
(Blanchetot et al., 2002).
These studies indicate that the catalytic Cys must be in the reduced form for
a PTP to be active. Because redox regulation is critically important in plant
cell regulation, we hypothesized that plant PTPs may also be regulated by
redox state of the Cys and thereby serving as a molecular target for oxidative
stress.
To study the effect of H2O2 on plant PTPs, we
analyzed the phosphatase activity of the purified AtPTP1 using pyronitrophenyl
phosphate as a substrate (Xu et al.,
1998). Results from one representative experiment are shown in
Figure 1. The phosphatase
activity of AtPTP1 was linear with time until H2O2 (1
mM) was added to the assay mixture. The activity of AtPTP1 was
arrested within 1 min after addition of H2O2
(Fig. 1A). The AtPTP1 remains
inactive until 200 units of catalase and DTT (10 mM) was added to
decompose H2O2 and reduce Cys residues in the AtPTP1
protein. The activity of AtPTP1 was rapidly restored within 4 min
(Fig. 1A). To examine whether
H2O2 affects the AtPTP1 stability, we treated purified
AtPTP1 with H2O2 and/or DTT and/or catalase for 60 min,
and samples were analyzed by SDS-PAGE. The data indicated that none of these
treatments changed the AtPTP1 stability
(Fig. 1B), suggesting that
inactivation of AtPTP1 by H2O2 may follow the
conformational change shown in animal PTPs
(Blanchetot et al., 2002).
Based on these experiments, we concluded that AtPTP1 and possibly other plant
PTPs (containing the catalytic cysteines) are reversibly inactivated by
oxidative stress, as shown in animal PTPs
(Caselli et al., 1998;
Denu and Tanner, 1998;
Lee and Esselman, 2002).
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Figure 1. Effect of redox conditions on AtPTP1 protein and its phosphatase activity.
A, Phosphatase activity of AtPTP1 (100 ng) was assayed at room temperature
using pyronitrophenyl phosphate (20 mM) as a substrate in a
phosphatase buffer (50 mM Tris-HCl, pH 7.0, and 2 mM
dithiothreitol [DTT]) by measuring A405 as described
previously (Xu et al., 1998).
To change the redox state, H2O2 (1 mM) and
DTT (10 mM and 200 units of catalase to decompose
H2O2) were added 10 and 20 min after initiation of the
phosphatase reaction. The data from one of three experiments are shown.
Phosphatase activity calculated at different times is shown in arbitrary
units. B, AtPTP1 is stable under different redox states. Purified AtPTP1 (5
µg) was incubated in 1 mM H2O2 and/or 10
mM DTT and/or catalase (200 units) for 60 min and was separated in
a 12% (w/v) SDS-PAGE gel. The gel was stained with Coomassie Blue to detect
AtPTP1.
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In all organisms studied thus far, PTPs play a role in MAP kinase
regulation. The activation of MAP kinases requires phosphorylation of Thr and
Tyr residues in an activation loop of MAP kinases
(Anderson et al., 1990).
Dephosphorylation of Thr or Tyr or both causes inactivation of a MAP kinase
(for review, see Camps et al.,
2000; Keyse,
2000). In animals, dual-specificity PTPs (DsPTPs) have been shown
to play a major role in the inactivation of different MAP kinases (for review,
see Camps et al., 2000;
Keyse, 2000). However, in
yeast, DsPTP and Tyr-specific PTPs are involved in regulation of MAP kinases
(Wurgler-Murphy et al., 1997;
van Drogen and Peter, 2001).
Recent studies have shown that PTPs function in the regulation of MAP kinases
in plants as well (Luan et al.,
2001; Luan, 2002;
Ulm et al., 2002).
Interestingly, oxidative stress such as H2O2 treatment
activates MAP kinases in plant cells, consistent with the finding that
H2O2 inactivates PTPs, negative regulators of MAP
kinases. Although it is difficult to determine whether MAP kinase activation
is a result of PTP inactivation by H2O2, we decided to
make a correlation analysis.
To examine the MAP kinase activation pattern in Arabidopsis, we treated
3-week-old wild-type (Colgl11) seedlings with H2O2 and
measured MAP kinase activity in the total protein extract in an in-gel kinase
assay (Zhang and Klessig,
1997). The H2O2 treatment activated a major
MAP kinase at 47 kD within 5 min of treatment
(Fig. 2A). Although earlier
studies have shown that H2O2 activates a 47-kD MAP
kinase (Desikan et al., 2001;
Yuasa et al., 2001), the
kinetics of activation appeared to differ. H2O2 also
activates ANP1, an MAP kinase kinase kinase. In Arabidopsis that initiates a
phosphorylation cascade involving two stress MAP kinases, AtMPK3 and AtMPK6
(Kovtun et al., 2000). We also
examined the level and stability of AtPTP1 protein in the total extracts by
western-blot analysis. AtPTP1 antibodies were raised in a rabbit and were
purified using affinity methods (Lin et
al., 1996). Purified AtPTP1 antibodies recognized a single protein
species at the predicted size of AtPTP1 protein. Consistent with the in vitro
results, H2O2 treatment did not change the AtPTP1
protein level and stability in vivo (Fig.
2B). Studies have shown that the 47-kD MAP kinase activated by
H2O2 is AtMPK6
(Desikan et al., 2001;
Yuasa et al., 2001). To
support the notion that AtPTP1 inactivation may be related to the activation
of MAP kinase by H2O2, we expressed and purified
glutathione S-transferase (GST)-AtPTP1, GST-AtMEK1, and GST-AtMPK6
from Escherichia coli as described previously
(Gupta et al., 1998), and
studied whether AtPTP1 can dephosphorylate and inactivate AtMPK6. As shown in
Figure 3B, AtMEK1 (a MAP kinase
kinase) activated AtMPK6 in a kinase assay using MBP as a substrate
(Gupta et al., 1998). When the
activated AtMPK6 was treated with AtPTP1, its activity was drastically reduced
(Fig. 3B). It is clear from the
data that AtPTP1 could inactivate AtMPK6 in vitro
(Fig. 3B). Moreover, the
inactivation of AtMPK6 is proportional to the extent of Tyr dephosphorylation
in AtMPK6 (Fig. 3D).
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Figure 2. Oxidative stress activates a 47-kD (AtMPK6) MAP kinase without any change
in AtPTP1 protein level. Three-week-old Arabidopsis (Col-gl11) seedlings grown
on plates containing Murashige and Skoog medium (one-half strength Murashige
and Skoog salt and 1x Gamborg's vitamins) were treated with 1
mM H2O2 (30 mL for each 90-mm plate) by
submerging seedlings for different periods of time. Samples were frozen in
liquid nitrogen and stored at –80°C before use. Total protein was
extracted and used for further experiments. A, In-gel kinase assay using
myelin basic protein (MBP) as a substrate. In-gel kinase assay was performed
as described by Zhang and Klessig
(1997). Briefly, the tissue
was ground to fine powder in extraction buffer (100 mM HEPES, pH
7.5, 5 mM EDTA, 5 mM EGTA, 10 mM DTT, 10
mM sodium vanadate, 10 mM NaF, 50
mM -glycerolphosphate, 1 mM phenylmethylsulfonyl
fluoride, 1 mM benzamidine, 5 µg
mL–1 leupeptin, 5 µg
mL–1 pepstatin A, 5 µg
mL–1 aprotinin, and 10% [v/v] glycerol). The
supernatant was collected after centrifugation at 16,000g at 4°C
for 30 min. Total protein (15 µg) from each sample was separated in a 12%
(w/v) SDS-PAGE containing MBP (0.25 mg mL–1).
After electrophoresis, the gel was washed four times for 20 min each at room
temperature in the wash buffer (25 mM Tris-HCl, pH 7.5, 1
mM DTT, 0.1 mM sodium vanadate, 5 mM NaF, 0.5
mg mL–1 bovine serum albumin, and 0.1% [v/v]
Triton X-100). To renature the kinases, the gel was incubated in renaturing
buffer (25 mM Tris-HCl, pH 7.5, 1 mM DTT, 0.1
mM sodium vanadate, and 5 mM NaF) at 4°C overnight.
The kinase reaction was performed by incubating the gel in 50 mL of kinase
buffer (25 mM HEPES, pH 7.5, 2 mM EGTA, 12 mM
MgCl2,1mM DTT, 0.1 mM sodium vanadate, 200
nM ATP, and 50 µCi of  -32P-ATP; 3,000 Ci
mmol–1) for 1 h at room temperature. The gel was
washed with several changes of 5% (w/v) trichloroacetic acid and 1% (w/v)
NaPPi to remove the unincorporated -32P-ATP. Autoradiography
was performed using x-ray film (Kodak Biomax; Eastman-Kodak, Rochester, NY).
B, Anti-AtPTP1 western-blot analysis. For raising anti-AtPTP1 antibodies,
AtPTP1 protein (Xu et al.,
1998) was used as an antigen to inject a rabbit at Cocalico
Biological (Reamstown, PA). For western-blot analysis, total protein (30
µg) from each sample was separated in 12% (w/v) SDS-PAGE and transferred
onto a nitrocellulose membrane (Bio-Rad, Hercules, CA). The membrane was
incubated in 5% (w/v) nonfat dry milk in Tris-buffered saline/Tween 20 (TBST;
20 mM Tris-HCl, pH 7.5, 137 mM NaCl, and 0.1% [v/v]
Tween 20) for 1 h at room temperature. Purified anti-AtPTP1 antibodies were
used at a 1:500 dilution in TBST in the presence of 1% (w/v) nonfat dry milk.
The bound antibody was detected by horseradish peroxide-conjugated anti-rabbit
secondary antibodies (1:5,000 dilution in TBST + 1% [w/v] nonfat dry milk;
Santa Cruz Biotechnology, Santa Cruz, CA) using an enhanced chemiluminescence
kit (Amersham Pharmacia Biotech, Piscataway, NJ).
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Figure 3. In vitro dephosphorylation and inactivation of AtMPK6 by AtPTP1. The coding
sequences of AtMEK1 (an MAP kinase kinase; GenBank accession no. AAB97145),
AtMPK6 (GenBank accession no. BAA04869), and AtPTP1
(Xu et al., 1998) were
amplified by PCR using pfu polymerase and were cloned in frame with
GST in pGEX-KG vector (Amersham Pharmacia). Fusion proteins (GST-AtMEK1,
GST-AtMPK6, and GST-AtPTP1) were expressed and purified from E. coli
as described previously (Gupta et al.,
1998). The activation/inactivation of AtMPK6 and MBP kinase assay
was performed as in earlier studies (Gupta
et al., 1998; Huang et al.,
2000). Briefly, GST-AtMEK1 and GST-AtMPK6 were mixed and incubated
at 30°C for 30 min in the presence of 50 µM ATP in kinase
buffer (50 mM Tris-HCl, pH 7.5, 10 mM MgCl2,
and 10 mM MnCl2) to phosphorylate/activate the AtMPK6.
The activated AtMPK6 was treated with AtPTP1 in the presence of 2
mM DTT for 30 min at 30°C followed by inactivation of AtPTP1 by
treatment with 10 mM sodium vanadate for 15 min. AtMPK6 treated
with buffer (lane buffer) and AtPTP1 (lane AtPTP1) was used for kinase assay
at 30°C for 30 min with MBP (3 µg) and 10 µCi of
-32P-ATP (3,000 Ci mmol–1) in
the kinase buffer. Samples were resolved by SDS-PAGE, and autoradiography was
performed using x-ray film (Kodak Biomax; Eastman-Kodak). A, Coomassie-stained
gel showing the amount of GST-AtMPK6, GST-AtMEK1, and AtPTP1 used in the
experiment. B, MBP-kinase activity of activated GST-AtMPK6 treated with buffer
or AtPTP1. C, Amido-black stained membrane showing GST-AtMPK6 treated with
buffer or AtPTP1 after transfer from the gel in A. D, Tyr-phosphorylation
state of the activated GST-AtMPK6 treated with buffer or AtPTP1. Western blot
was performed as described for Figure
2B. The membrane from C was probed with anti P-Tyr antibodies
(PY99; Santa Cruz Biotechnology) at a dilution of 1:2,000. The bound antibody
was detected by horseradish peroxide-conjugated anti-mouse (1:2,000 dilution)
secondary antibodies (Santa Cruz Biotechnology) using an enhanced
chemiluminescence kit (Amersham Pharmacia).
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In summary, these experiments show that AtPTP1 is reversibly inactivated by
H2O2 without affecting the stability of AtPTP1 protein.
AtPTP1 inactivation was strongly correlative to MAP kinase (AtMPK6) activation
by H2O2, suggesting that AtPTP1 may represent a primary
target for oxidative stress in plants.
Received January 22, 2003;
returned for revision February 10, 2003;
accepted March 5, 2003.
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FOOTNOTES
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Article, publication date, and citation information can be found at
www.plantphysiol.org/cgi/doi/10.1104/pp.103.020792.
*
Corresponding author; e-mail
sluan{at}nature.berkeley.edu;
fax 510–642–4995.
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