Interaction of Glutathione with Hydrogen Peroxide: A Kinetic Model

Article abstract of DOI:10.1134/S0023158419030169

Abstract: The kinetics of the interaction of glutathione (GSH) with hydrogen peroxide (H₂O₂) was studied. It was shown that the rate of GSH consumption nonlinearly depended on reactant concentrations and the process was accompanied by the appearance of radicals with a relatively low rate, which was a fraction of a percent of the rate of GSH consumption. Based on the experimental results and literature data on the reactions of GSH with H₂O₂ and thiyl radicals, a kinetic model of the complex interaction of GSH and H₂O₂ in an aqueous solution at 37°C was proposed. The model includes 15 quasi-elementary reactions with corresponding rate constants, including the formation of the intermediate complex GSH–H₂O₂ and its subsequent reactions with the formation of final products. Computer simulation based on the model developed satisfactorily described the reaction kinetics in a wide range of reactant concentrations.

Full text of DOI:10.1134/S0023158419030169

ISSN 0023-1584, Kinetics and Catalysis, 2019, Vol. 60, No. 3, pp. 266–272. © Pleiades Publishing, Ltd., 2019.
Russian Text © The Author(s), 2019, published in Kinetika i Kataliz, 2019, Vol. 60, No. 3, pp. 281–288.
Interaction of Glutathione with Hydrogen Peroxide: A Kinetic Model
K. M. Zinatullinaa, b, *, O. T. Kasaikinaa, V. A. Kuz’minb, and N. P. Khrameevab
aSemenov Institute of Chemical Physics, Russian Academy of Sciences, Moscow, 119991 Russia
bEmanuel Institute of Biochemical Physics, Russian Academy of Sciences, Moscow, 119991 Russia
*e-mail: karinazinat11@gmail.com
Received October 4, 2018; revised December 7, 2018; accepted January 22, 2019
Abstract—The kinetics of the interaction of glutathione (GSH) with hydrogen peroxide (H2O2) was studied.
It was shown that the rate of GSH consumption nonlinearly depended on reactant concentrations and the
process was accompanied by the appearance of radicals with a relatively low rate, which was a fraction of a
percent of the rate of GSH consumption. Based on the experimental results and literature data on the reac-
tions of GSH with H2O2 and thiyl radicals, a kinetic model of the complex interaction of GSH and H2O2 in
an aqueous solution at 37°C was proposed. The model includes 15 quasi-elementary reactions with corre-
sponding rate constants, including the formation of the intermediate complex GSH–H2O2 and its subse-
quent reactions with the formation of final products. Computer simulation based on the model developed sat-
isfactorily described the reaction kinetics in a wide range of reactant concentrations.
Keywords: kinetics, glutathione, hydrogen peroxide, thiyl radicals, kinetic model
DOI: 10.1134/S0023158419030169
INTRODUCTION
tionship of GSH with various diseases including can-
cer, neurodegenerative diseases, acquired immunode-
ficiency syndrome, aging, heart attack, and stroke has
been studied [19–24].
Thiol-containing compounds play an important
role in protecting biological systems from oxidative
damage [1, 2]. Glutathione (GSH), which is the most
common cytosolic thiol, belongs to endogenous biologi-
cal antioxidants synthesized directly in living organisms.
GSH interacts with hydroxyl radicals, reduces hydrogen
peroxide, hydroperoxides, and –S–S– disulfide bonds,
and prevents the oxidation of proteins [3–9]. The con-
centration of GSH in biological tissues is 0.1–
10 mmol/L, which is significantly higher than the
concentrations of other potential bioantioxidants. In
cells, GSH is present predominantly in a reduced form
(GSH). Reactive oxygen species (ROS) oxidize GSH
to disulfide (GSSG). The ratio between reduced and
oxidized forms of glutathione ([GSH]/[GSSG]) in
cell is one of the most important parameters indicating
the level of oxidative stress [10–12]. Oxidative stress is
characterized by an increased ROS content, and it
reflects an imbalance between the rates of ROS for-
mation and utilization [13–15].
In living organisms, hydroperoxides are reduced by
glutathione peroxidases, enzymes specific for organs
and tissues that use GSH as a substrate and efficiently
reduce not only H2O2 but also organic hydroperox-
ides, including the hydroperoxides of membrane poly-
unsaturated fatty acids. GSH is involved in many
physiological processes. In living organisms, it regu- generation of radicals, the rate of which is a fraction of
lates protein conformations and gene expression using a percent of the rate of GSH consumption, but it was
thiol–disulfide exchange reactions and affects lym- sufficient to initiate the chain reaction of GSH with
phocytes and immune reactions [16–19]. The rela- the unsaturated phenols resveratrol and caffeic acid
In recent decades, the role of GSH in the biochem-
istry of cancer cells has been actively investigated. It
was assumed that GSH is a key element in their pro-
tection against free radicals and electrophiles, and it
determines the sensitivity of cells to radiation and drug
cytotoxicity. Multiple drug and radiation resistance of
tumor cells, as compared with that of normal tissues,
was associated with an increased level of GSH in them
[22–25]. In the literature, the redox pair GSH/GSSG
and H2O2 occupy a central place in the determination
of redox homeostasis and redox signaling [26–31].
According to published data [2, 6, 32–35], the
interaction of GSH and H2O2 proceeds stoichiometri-
cally in accordance with the following equation:
2GSH + H2O2 → GSSG + 2H2O.
However, in a number of works, it was noted that,
despite the general stoichiometry corresponding to the
above equation, the process rate is of the first order
with respect to GSH concentration [2, 31, 36], and it
depends on a ratio between the concentrations of GSH
and H2O2 [36]. Recently [37, 38], we found that the
interaction of GSH and H2O2 was accompanied by the
266

INTERACTION OF GLUTATHIONE WITH HYDROGEN PEROXIDE
267
[39, 40]. The rates of radical formation (Wi) were mea- (1 cm) of an Ultraspec1100Pro spectrophotometer
(Amersham plc, the United States).
Errors in the determination of the concentrations of
reagents and the rates of reactions did not exceed 15%.
The analysis of the kinetics of the interaction of
GSH with H2O2 and the computer simulation of the
kinetic curves of reagent consumption were performed
using a published program [43].
sured by an inhibitor method using an anionic poly-
methine dye A (the pyridine salt of 3,3'-di-γ-sulfopro-
pyl-9-methylthiacarbocyaninebetaine) as an acceptor.
This water-soluble dye is inert with respect to thiols
and hydrogen peroxide, but it actively and stoichio-
metrically reacts with free radicals [41]. With the use of
the method of competing reactions, it is possible to
evaluate the antiradical activity of antioxidants based
on the consumption of A. In particular, the value of
krO2 = 0.84 × 105 M–1 s–1 was obtained for the rate
constant of a reaction of GSH with the peroxyl radical
from 2,2'-azobis(2-amidinopropane) hydrochloride
(AAPH) in an aqueous solution at 37°C [38, 40].
In this work, we experimentally studied the con-
centration dependences of the rate of GSH consump-
tion and the rate of formation of radicals in a reaction
of GSH with H2O2. Using computer simulation and
taking into account the experimental results and avail-
able published data on the reactions of GSH, H2O2,
and thiyl radicals, we carried out an analysis of possi-
ble ways of the nonenzymatic conversion of GSH into
GSSG. We constructed a kinetic model of the complex
interaction of GSH and H2O2 (in an aqueous solution at
37°C) to adequately describe the kinetics of the reaction
in a wide range of reactant concentrations.
RESULTS AND DISCUSSION
Figure 1 shows the dependences of the initial rate
of GSH consumption (WGSH) on the concentrations of
GSH and H2O2 at different ratios between their con-
centrations (0.1 < [GSH]0/[H2O2]0 < 2.5). Linear ana-
morphoses of these dependences in logarithmic coor-
dinates (Fig. 1b) indicate fractional orders of the rate
of GSH consumption with respect to reactant concen-
trations:
0.3
1.2
0
[
]
0
(1)
WGSH ≅ const GSH
H O
,
[
]
2
2
where сonst = (1.7 0.2) × 10–3 M–0.5 s–1.
The rate of initiation of radicals was measured by
an inhibitor method based on the consumption of the
radical acceptor (A). Figure 2a shows changes in the
absorption spectra of A recorded at regular intervals of
1 min after the introduction of the acceptor into the
reaction mixture. From Fig. 2b, it follows that the
acceptor A does not react with GSH and H2O2 taken
separately, and it is consumed only in the reaction with
radicals generated upon their interaction (curve 3).
Table 1 summarizes the experimental values of the
rates of radical formation (WA) at various concentra-
tions of H2O2 and GSH. It can be seen that the rates of
formation of radicals are lower than WGSH by two
orders of magnitude. Like WGSH, the dependences of
EXPERIMENTAL
Glutathione (GSH), Ellman’s reagent (5,5'-dith-
iobis(2-nitrobenzoic acid) (DTNB), Sigma-Aldrich),
and hydrogen peroxide (Usol’khimprom) were used
without preliminary purification. An anionic poly-
methine dye (the pyridine salt of 3,3'-di-γ-sulfopro-
pyl-9-methylthiacarbocyaninebetaine, Gosniikhim-
fotoproekt) served as a radical acceptor (A) [39]. Dou-
ble-distilled and deionized water (Direct-Q UV
Millipore, 18 MΩ cm) was used as a reaction medium. WA on GSH and H2O2 concentrations are also nonlin-
ear, and they have fractional orders with respect to
Reactions were carried out at 37°C in a thermostat-
reactant concentrations different from the orders in
ted glass cell equipped with a magnetic stirrer. In the
course of the reaction, aliquot portions (15 μL) were
taken from the reaction vessel in order to determine
the concentration of GSH by the Ellman method [42].
For this purpose, an aliquot portion was added to
3 mL of a sodium phosphate buffer solution (PBS,
pH 7.4) containing 0.1 mM DTNB, and the concen-
tration of 2-nitro-5-thiobenzoic acid, which is formed
by the interaction of GSH with DTNB, was deter-
mined spectrophotometrically (λmax = 412 nm, ε =
Eq. (1) for WGSH
:
0.75
0.75
(2)
W ≅ const GSH
H O
2
,
[
]
[
]
A
2
where const = (1.3 0.2) × 10–5 M–0.5 s–1.
As a rule, fractional orders with respect to the con-
centrations of basic reagents are indicative of a com-
plex multistage mechanism of the process.
To analyze the kinetics of the interaction of GSH
and H2O2, we used computer simulation in accor-
dance with a published program [43]. The kinetic
reaction scheme—a set of quasi-elementary reactions
(Table 2)—was constructed step-by-step taking into
account the following features of the process: (1) a rel-
0.14 × 105 M–1 cm–1). The concentration of basic
H2O2 solutions in the absence of GSH was monitored
by an iodometric method.
The rate of generation of radicals (WA) was measured
by an inhibitor method based on the consumption of the ative increase in WGSH at [H2O2]0 > [GSH]0 and a rel-
acceptor A, whose concentration changes were measured
ative decrease in WGSH at [GSH]0 > [H2O2] ( Fig. 1);
(2) the formation of radicals and nonlinear depen-
dences of the initial rate of consumption of A on the
by spectrophotometry (ε = 0.77 × 105 M–1 cm–1 at
λ
max = 546 nm) directly in thermostatted quartz cells
KINETICS AND CATALYSIS Vol. 60 No. 3 2019

268
ZINATULLINA et al.
(а)
(b)
WGSH × 107, М s–1
7 + log(WGSH)
12
1.2
2
10
8
1.0
0.8
0.6
0.4
0.2
3
6
1
4
4
2
0
2
4
6
8
10
12
0
0.5
1.0
1.5
[GSH]; [H2O2], mМ
3 + log(GSH); 3 + log(H2O2)
Fig. 1. (a) Dependence of the rate of GSH consumption (W
) on the concentration of GSH in the presence of (1) 4 mM H O
2 2
GSH
and on the concentration of H O in the presence of (2) 4.5 mM GSH; (b) dependence of the rate of GSH consumption on the
2
2
concentrations of (3) GSH and (4) H O in logarithmic coordinates. (r, s) Experimental and (-) calculated data; aqueous solu-
2
2
tion, 37°С.
(а)
(b)
D
D543
0.6
0.6
1
2
0.5
0.4
0.3
0.2
0.1
0
0.5
0.4
0.3
0.2
0.1
3
440 460 480 500 520 540 560 580 600
0
2
4
6
8
10
12
14
t, min
λ, nm
Fig. 2. (a) Changes in the absorption spectra of a 7 μM solution of acceptor A in a mixture of 5 mM GSH and 5.3 mM H O ;
2
2
aqueous solution, 37°С. The spectra were recorded at regular intervals of 1 min. (b) Kinetic curves of consumption of 7 μM accep-
tor A in the presence of (1) 10 mM GSH, (2) 10 mM H O , and (3) a mixture of 5 mM GSH with 5.3 mM H O .
2
2
2 2
initial concentrations of GSH and H2O2; (3) the main
products of the conversion of GSH and H2O2 are
GSSG and H2O; and (4) a kinetic reaction scheme
with optimized rate constants should describe the
experimental curves of the consumption of GSH and
the acceptor A introduced into the reaction mixture.
An analysis of published data on the kinetics of the
interaction of GSH and H2O2 showed the following: it
was hypothesized [2, 6, 31, 44] that the initial product
of a reaction between a thiol and H2O2 is a sulfenic
acid (–SOH), which then quickly reacts with the thiol
to form a disulfide:
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INTERACTION OF GLUTATHIONE WITH HYDROGEN PEROXIDE
269
Table 1. Rates of consumption of the acceptor A (7.2 μM) at different concentrations of H2O2 in the presence of 5 mM
GSH and at different concentrations of GSH in the presence of 8.6 mM H2O2 (aqueous solution, 37°C)
[H2O2] = 8.6 mM; [A] = 7.2 μM
WA × 109, M/s
[GSH] = 5 mM; [A] = 7.2 μM
WA × 109, M/s
[H2O2], mM
[GSH], mМ
experimental
0.1
calculated data
experimental
calculated data
0.45
0.9
1
1.75
2
3.5
4.4
8.8
1
0.88
1.62
1.8
1.0
2.5
5.0
6.9
8.0
1.3 0.15
3.8 0.4
6.2 0.6
7.3 0.7
9.85 1.0
10.0 1.0
2.4
3.5
5.5
7.8
9.6
1.7 0.2
2.0 0.2
2.5 0.25
2.8 0.3
4.5 0.45
4.9 0.5
5.6 0.6
2.52
2.8
4.25
4.95
5.25
10.0
10.3
Table 2. Kinetic model of the interaction of GSH with H O in the presence of the radical acceptor A in aqueous solution at 37°C
2
2
ki, M–1 s–1
Reaction
Reference*
Rate constant
1.2 × 10–1
**1 × 10–6
4 × 10–3
7 × 10–4
**2 × 10–3
8 × 10–1
1.3
**9 × 10–4
4 × 10–4
1 × 108
9 × 10–2
1 × 10–3
1 × 109
6 × 105
2 × 108
H2O2 + GSH → K
K → H2O2 + GSH
K + GSH → GSSG + 2H2O
K + GSH → GS• + GS• + 2H2O
K → GSOH + H2O
GSOH + GSH → GSSG + H2O
GSH + GSH → С
С → GSH + GSH
GSH + H2O2→ GS• + OH• + H2O
OH• + GSH → H2O + GS•
K + K → GSSG + 2H2O +H2O2
С + H2O2 → GSSG + 2H2O
GS• + GS• → GSSG
(I)
(II)
[36]
[36]
k1
k2
(III)
(IV)
(V)
[36]
k3
This work
This work
[2, 44]
[32]
k4
k5
(VI)
(VII)
(VIII)
(IX)
(X)
k6
k7
[32]
k8
This work
This work
[36]
k9
k10
k11
k12
k13
k15
k16
(XI)
(XII)
(XIII)
(XIV)
(XV)
This work
[45]
GS• + A → B•
B• + B• → products
This work
This work
K and C refer to the complexes GSH–H O and GSH–GSH, respectively.
2
2
* References to publications in which the corresponding reaction is mentioned. The rate constants were estimated by Abedinzadeh et al. [36]
only for the interaction of GSH with H O in a phosphate buffer solution.
2
2
.
–1
** The rate constant dimensionality is s
and H2O2 was obtained from the dependence of the
above constant on the concentration of GSH (~ mM).
Abedinzadeh et al. [36] carefully studied the kinetics
of consumption of GSH and H2O2 on their interaction
in a neutral aqueous solution at concentrations of the
order of mM and the ratios [GSH]0/[H2O2]0 in a range
from 0.2 to 2. Based on the differential absorption
spectra of the reaction mixture observed in specially
designed cells and on the experimentally observed
GSH + H2O2 → GSOH + H2O,
GSOH+ GSH → GSSG + H2O.
Winterbourn and Metodiewa [2] presented the kinetic
characteristics of the reactions of GSH and several
other thiols with H2O2 in a phosphate buffer at 37°C
and pH 7.4. The effective rate constant was deter-
mined from the exponential kinetic curves of H2O2
consumption in an excess of GSH, and a rate constant
of 0.9 M–1 s–1 for the bimolecular reaction of GSH consumption of H2O2, Abedinzadeh et al. [36] sug-
KINETICS AND CATALYSIS Vol. 60 No. 3 2019

270
ZINATULLINA et al.
gested the formation of the intermediate complex of radicals in the reaction of GSH and H2O2 and pro-
GSH–H2O2, in which the thiol group –SH reacts with posed previously [37] the following relatively simple
Ellman’s reagent just as in free GSH, and H2O2 can- reaction scheme taking into account the assumption of
not be determined by the titanium sulfate method used Abedinzadeh et al. [36] on the formation of the GSH–
[36]. We failed to find published data on the formation H2O2 complex:
GSH
↓
GSH+ H O ꢀ GSH–H O → G–S–S–G + 2H O
[
]
2
2
2
2
2
↓
Radicals (GS•)
↓
GS• + А
↓
Products
Scheme 1.
In Table 2, reactions (I)–(IV) correspond to this duced with consideration for published data on the in-
termediate formation of sulfenic acid (GSOH). Reac-
tions (VII) and (VIII)—the formation of a glutathione
scheme (K is the GSH–H2O2 complex). Reaction
(XIII) (k13 = 109 M–1 s–1 [45]) characterizes the rapid
recombination of thiyl radicals, and reactions (XIV)
and (XV) correspond to the interaction of the acceptor
A with thiyl radicals. However, the simulation showed
that the linear dependences of WGSH on the initial re-
actant concentrations correspond to the sets of reac-
tions (I)–(IV) and (XIII)–(XV) even with the varia-
tion of the rate constants k1–k4 over a rather wide
dimer GSH + GSH
GSH–GSH (C), in which the
ꢀ
thiol groups are determined by the Ellman method,
were introduced into the model in order to relatively
decrease WGSH and WA in an excess of GSH. It should
be noted that Deutsch et al. [32], who studied GSH by
negative ion electrospray mass spectrometry, found
that dimer ions were detected along with GSH ions in
an aqueous solution, whereas the dimer was not de-
range of values. Reactions (V) and (VI) were intro- tected in a phosphate buffer solution (0.1 M, pH ~ 7).
(а)
(b)
[GSH]*, mМ
6
[A], μМ
7
6
5
4
3
2
1
5
4
3
2
1
1
2
3
0
20
40
60
80
100
120
t, min
0
2
4
6
8
10 12 14 16 18 20
t, min
Fig. 3. (a) Kinetic curves of consumption of thiyl groups in a solution of 4.5 mM GSH (1) in the absence of H O , (2) in a mixture
2
2
with 4 mM H O , and (3) in a mixture with 8.5 mM H O . (r, s, n) Experimental data (according to Ellman); lines illustrate
2
2
2 2
calculations based on the kinetic model (Table 2) [GSH]* = [GSH] + [K] + 2 [C]. (b) Kinetic curve of consumption of 6 μM
acceptor A in the presence of 10 mM GSH and 8.6 mM H O . The points refer to the experimental data, and the line illustrates
2
2
the calculation by the kinetic model (Table 2).
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INTERACTION OF GLUTATHIONE WITH HYDROGEN PEROXIDE
271
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Reaction (XII) was added in order to relatively in-
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and they simulate the kinetic curves of acceptor con-
sumption together with the other reactions.
The presented kinetic model with optimized rate
constants adequately describes the experimental con-
centration dependences of WA and WGSH (Fig. 1 and
Table 1) and the experimental kinetic curves of GSH
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Based on the experimentally obtained concentra-
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We found that the kinetic model satisfactorily
reflects not only the concentration dependences of the
rates WGSH and WA but also the experimental kinetic
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FUNDING
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Translated by Valentin Makhlyarchuk
Shapiro, B.I., and Kuzmin, V.A., Russ. Chem. Bull.,
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No. 3
2019