Free radical scavenging activity of novel thiazolidine-2,4-dione derivatives

Article abstract of DOI:10.1002/bio.2454

Free radical activity towards superoxide anion radical (O2?), hydroxyl radical (HO^?) and 2,2-diphenyl-1-picrylhydrazyl (DPPH^?) of a series of novel thiazolidine-2,4-dione derivatives (TSs) was examined using chemiluminescence, electron paramagnetic resonance (EPR) and EPR spin trapping techniques. 5,5-Dimethyl-1-pyrroline-N-oxide (DMPO) was applied as the spin trap. Superoxide radical was produced in the potassium superoxide/18-crown-6 ether dissolved in dimethyl sulfoxide. Hydroxyl radical was generated in the Fenton reaction (Fe(II) + H₂O₂. It was found that TSs showed a slight scavenging effect (15-38% reduction at 2.5 mmol/L concentration) of the DPPH radical and a high scavenging effect of O2? (41-88%). The tested compounds showed inhibition of HO ^? -dependent DMPO-OH spin adduct formation (the amplitude of EPR signal decrease ranged from 20 to 76% at 2.5 mmol/L concentration. Our findings present new group compounds of relatively high reactivity towards free radicals. Copyright 2012 John Wiley & Sons, Ltd. Copyright

Full text of DOI:10.1002/bio.2454

Research article
Received: 22 August 2012,
Accepted: 18 October 2012
Published online in Wiley Online Library: 17 December 2012
(wileyonlinelibrary.com) DOI 10.1002/bio.2454
Free radical scavenging activity of novel
thiazolidine-2,4-dione derivatives†
Paweł Berczyński,a Irena Kruk,a Teresa Piechowska,a
Meltem Ceylan-Unlusoy,b Oya Bozdağ-Dündarb and
Hassan Y. Aboul-Eneinc*
ꢀꢀ
•
ABSTRACT: Free radical activity towards superoxide anion radical (O2), hydroxyl radical (HO ) and 2,2-diphenyl-1-picrylhydrazyl
•
(DPPH) of a series of novel thiazolidine-2,4-dione derivatives (TSs) was examined using chemiluminescence, electron
paramagnetic resonance (EPR) and EPR spin trapping techniques. 5,5-Dimethyl-1-pyrroline-N-oxide (DMPO) was applied as the
spin trap. Superoxide radical was produced in the potassium superoxide/18-crown-6 ether dissolved in dimethyl sulfoxide.
Hydroxyl radical was generated in the Fenton reaction (Fe(II) + H2O2. It was found that TSs showed a slight scavenging effect
(15–38% reduction at 2.5 mmol/L concentration) of the DPPH radical and a high scavenging effect of Oꢀ2ꢀ (41–88%). The tested
•
compounds showed inhibition of HO -dependent DMPO-OH spin adduct formation (the amplitude of EPR signal decrease ranged
from 20 to 76% at 2.5 mmol/L concentration. Our findings present new group compounds of relatively high reactivity towards
free radicals. Copyright © 2012 John Wiley & Sons, Ltd.
Keywords: 1,1-diphenyl-2-picrylhydoxyl radical; chemiluminescence; EPR; hydroxyl radical; spin trapping; superoxide radical;
thiazolidine 2,4-dione derivatives
triazol-3-ylsulfanyl)-thiazole-5-carbaldehyde using an acetic
Introduction
acid/sodium acetate mixture (11). All reagents for synthesis were
A considerable amount of evidence indicates that reactive oxygen
purchased from E. Merck (Darmstadt, Germany) and Aldrich
•
species (ROS) such as hydroxyl radical (HO) and superoxide anion
radical (Oꢀ2ꢀ) may play a dual function depending on their concen-
(Milwaukee, MI, USA).
4,5-Dihydroxy-1,3-benzene-disulfonic acid (Tiron), 5,5-dimethyl-
tration. ROS are produced in cells under normal physiological
1-pyrroline-1-oxide (DMPO), 6-hydroxy-2,5,7,8-tetramethyl-2
conditions during redox reactions and have useful physiological
carboxylic acid (Trolox), 18-crown-6 (1,4,7,10,13,16) hexaoxacy
functions, e.g. as in cellular signaling systems (1,2), but generated
clooctadecane and ascorbic acid were from Merck (Darmstadt,
in excess participate in several physiopathologies. They can
Germany); potassium superoxide (KO2) and ammonium ferrous
damage biomolecules and are involved in the etiology of several
sulfate hexahydrate were from Fluka (Buchs, Switzerland); and
human chronic diseases and aging (3,4). Growing experimental
p-nitroblue-tetrazolium chloride was from Sigma (St Louis, MO,
data suggest that cancer cells are under increased oxidative stress
USA). Anhydrous dimethyl sulfoxide (DMSO) was purchased
and contain increased concentrations of ROS compared to normal
from Aldrich (Milwaukee, WI, USA).
cells (5). In addition, studies provide evidence that during inflam-
matory processes, endogenous overgeneration of ROS occurs,
and that tumorigenesis is associated with inflammation (6).
Superoxide radical was prepared according to the procedure
given by Valentine et al. (12). A 60-mg aliquot of 18-crown-6
The investigation of biological and antioxidant activities of
natural substances and natural derivatives having different substi-
tuents or even synthetic analogues capable of quenching toxic
free radicals, generated under oxidative stress conditions, are the
topic of much research (7–10).
* Correspondence to: Hassan Y. Aboul-Enein, Pharmaceutical and Medicinal
Chemistry Department, The Pharmaceutical and Drug Industries Research
Division, National Research Centre, Dokki, Cairo 12311, Egypt. E-mail:
haboulenein@yahoo.com
Based on our promising studies on thiazolyl thiazolidinedione
derivatives, concerning their antioxidant capacities, we have
undertaken evaluation of the scavenging property of some
1†
This article was published online on December 7, 2012. An error was subse-
quently identified. This notice is included in the online and print versions to
indicate that both have been corrected April 30, 2013.
ꢀꢀ
•
novel thiazolidine-2,4-dione derivatives (TSs) (Fig. 1) for O2, HO
a
Institute of Physics, Faculty of Mechanical Engineering and Mechatronics,
West Pomeranian University of Technology in Szczecin, Al. Piastów 48/49,
70-311 Szczecin, Poland
•
and 2,2-diphenyl-1-picrylhydrazyl radical (DPPH).
b
Ankara University, Faculty of Pharmacy, Department of Pharmaceutical
Materials and methods
Chemistry, 06100 Tandoğan, Ankara, Turkey
The compounds tested were synthesized by the Knoevenagel
reaction of 3-substituted benzyl-2,4-thiazolidinediones and
phenacyl-2,4-thiazolidinediones with 4-chloro-2-(5-methyl[1,2,4]
c
Pharmaceutical and Medicinal Chemistry Department, The Pharmaceutical
and Drug Industries Research Division, National Research Centre, Dokki,
Cairo 12311, Egypt
Luminescence 2013; 28: 900–904
Copyright © 2012 John Wiley & Sons, Ltd.

Free radical scavenging activity of thiazolidine-2,4-dione derivatives
O
R1
R ¼ ½ðIo ꢂ IÞ=Ioꢃ ꢄ 100%
where Io and I represent the CL intensities measured in the
absence of an inhibitor (TS) (the control reaction) and I is that
in the presence of a tested compound.
The hydroxyl radical scavenging activity of TDs was measured
using the Fenton reaction in a sodium trifluoroacetate solution
and ferrous ions as a catalyst (13,14)
H
S
S
N
A
C
B
N
D
CH3
S
N
N
N
Cl
R2
O
Substituents
R2
Compound
1a - 1f
Feð IIÞ þ H2O2 ! HOꢀ þ Feð IIÞ þ HOꢂ
(1)
R1
a
b
c
d
e
f
H
H
H
H
H
Cl
H
and DMPO as a spin trap. The final concentrations of reagents were:
10 mmol/L sodium trifluoroacetate, 0.625 mmol/L ammonium
ferrous sulfate, 0.5 mmol/L H2O2, sodium trifluoroacetate buffer
(0.02 mol/L, pH 6.15) and 25 mmol/L DMPO dissolved in water.
Hydroxyl radical reacts with the DMPO trap giving a stable, easy
measurable with electron paramagnetic resonance (EPR) the
DMPO ꢂ OHꢀ spin adduct (15):
F
Cl
Br
Cl
NO2
ꢀ
HOꢀ þ DMPO ! DMPO ꢂ OH
(2)
The reaction mixture was placed in the EPR cavity using a
quartz flat cell within an optical path length of 0.25 mm. The EPR
signal was analyzed approximately 1 min after the introduction
of ammonium ferrous sulfate.
R1
O
N
H
S
S
A
N
D
N
The testing of the dependence of the relative height of the
second line in the four-line EPR spectrum of the DMPO ꢂ OHꢀ
spin adduct, formed in the absence (Ho) and the presence of
C
B
CH3
S
N
N
Cl
R2
O
•
O
the HO scavenger (H), allows calculation of the EPR ratios (Q):
Qð%Þ ¼ ½ðHo ꢂ HÞ=Hoꢃ ꢄ 100%
Substituents
R2
Compound
2a - 2f
To evaluate the antioxidative property (i.e. the interaction of a
potential antioxidant; a TS) we applied the DPPH radical reduction
from a method given by Nanjo et al. (16). The DMSO solution of
each tested compound or DMSO itself as a control was added to
DPPH dissolved in ethanol. After mixing for 10 s the solution was
introduced into a flat quartz cell with an optical path length of
R1
a
b
c
d
e
f
H
H
H
H
H
Cl
H
F
Cl
Br
Cl
•
0.25 mm, and the EPR signal was detected as a function of time.
•
The reduction of DPPH by a tested compound was followed by
the decrease in its EPR signal. Scavenging activity of TSs was calcu-
lated after 5 min according to the following equation:
R ¼ ½ðHo ꢂ HÞ=Hoꢃ ꢄ 100%
NO2
where Ho is the relative height of the third peak in the EPR
spectrum in the absence of an inhibitor (considered as a control
reaction) and H- is the relative peak hight that is measured in
the presence of an inhibitor. EPR spectra were recorded at room
temperature with an X-band standard spectrometer operating
at 9.3 GH, using a modulation frequency of 100 kHz.
Figure 1. Chemical structure of thiazolidine-2,4-dione derivatives.
was dissolved in 10 mL of dry DMSO and then KO2 (7 mg) was
quickly introduced into the flask using a syringe to avoid contact
with air humidity. The mixture was stirred for 1 h to give a pale
yellow solution of 10 mmol/L Oꢀ2ꢀ, which was stable at room tem-
perature for at least 1 h. The Oꢀ2ꢀ concentration was determined
using ultraviolet spectra (lmax = 251 nm, e = 2686 ꢁ 29 mol/cm).
Chemiluminescence (CL) intensity was recorded using an
EMI9553Q photomultiplier with a S20 cathode sensitive in the
range 200–800 nm, connected to a Zeiss K-200 recorder.
Reagents were introduced to a thermostated glass cuvette
placed in a light tight chamber using polyethylene pipes with
aid of semiautomatic syringes. A personal computer equipped
with a home-made software program was used to monitor and
analyze the output signal. The effects of inhibitors and scaven-
gers were expressed as the percentage inhibition of original
measurements of the CL intensity:
Results and discussion
Within the framework of this study, the primary characterization
of the free radical scavenging activity of 12 novel synthesized
compounds was performed employing the DPPH radical. The
radical has a proton, for which an EPR spectrum is shown in
Fig. 2. The spectrum exhibits five splitting lines and decreases
significantly on exposure to proton radical scavengers. The
capacity of antioxidants to scavenge the DPPH radical has been
exemplified by their action as hydrogen atom donors (17). The
method was successfully applied for the primary characteriza-
tion of free radical scavenging and antioxidant activities of
several natural and synthetic substances (18–20). All tested TSs
Luminescence 2013; 28: 900–904
Copyright © 2012 John Wiley & Sons, Ltd.
wileyonlinelibrary.com/journal/luminescence

P. Berczyński et al.
curve of the CL shows an initial rapid approximately first-order
decay followed by a very small decrease lasting at least 3 min
(Fig. 4). This reaction has become very useful for detecting anti-
oxidative effects of biologically important substances and selec-
tion of natural compounds inhibiting the Oꢀ2ꢀ radical (9,10,22,23).
Reactions responsible for generation of the CL emitter (pairs of
singlet oxygen) from the O2ꢀꢀ/DMSO system have been reported
in previous papers (21,24–26), and the main reaction responsible
100
90
80
70
60
50
1a
2b
1d
2a
2c
2d
1c
1
for the O2 production is removal of a proton from DMSO (21).
2e
1b
1e
1
2Oꢀ2ꢀ þ 2ð CH3Þ2 SO ! O2 þ ð CH3Þ2 SO2 þ CH3 SOCH2 þ OHꢂ
2f
1f
(4)
0
2
4
6
8
10
All examined TSs (dissolved in DMSO) added to the Oꢀ2ꢀ= DMSO
system exerted a short-lasting ‘“flash’ followed by a decrease in
light emission. Figure 4 (curves 3 and 4) shows the representa-
tive kinetic curves for compounds 1f and 2f, respectively. Curve
2 presents an effect of DMSO at the same concentration as in the
TS compound/DMSO sample; this reaction was considered as a
control. The examined compounds showed a high quenching
ratio ranging from 49% to 88% at a concentration of 1 mmol/L
(Fig. 5). Only one compound, 1e showed a scavenging effect lower
than that of an inhibitor specific to Oꢀ2ꢀ, such as p-nitroblue-
tetrazolium chloride at the same concentration.
The results from the Oꢀ2ꢀ scavenging assay show, once again,
the important property of TSs, i.e. the antioxidant ability. For
Oꢀ2ꢀ activity, three types of reactions are proposed: action as an
oxidant; reducing agent; and powerful nucleophile in aprotic
solvents (27,28). The strongly decreased CL from the Oꢀ2ꢀ/DMSO
system in the presence of TSs shows that the compounds were
able to scavenge Oꢀ2ꢀ species directly by hydrogen transfer:
Time [min]
Figure 2. EPR time course of the reduction of the DPPH free radical by 2.5
mmol/L TSs (curves 1–12) in DMSO (25% v/v)/C2H5OH (75% v/v). Inset graph
shows the EPR spectrum of the DPPH radical detected in the absence of a scav-
enger. Denotation of the TSs are given in Fig. 1. The remaining conditions are
reported under the Materials and Methods section. [Correction made here after
initial online publication.]
were able to scavenge the DPPH radical. The reactions between
DPPH and TSs were biphasic, similar to the reference antioxi-
dants the vitamin E analog Trolox and ascorbic acid (data not
shown). The kinetic curves exhibit two features, first the rapid
decrease lasting about 1 min, and the second slower with hyper-
bolic curves, reaching a steady state in t > 10 min. Figure 3
summarises the DPPH scavenging ratio of the examined TSs,
ascorbic acid and Trolox.
Generally, the compounds presented only a slight effect in
the range 15–39% at the maximum tested concentration
(2.5 mmol/L). Our observations demonstrate that the TSs studied
show a DPPH reduction much lower than ascorbic acid and
Trolox at lower concentration (50%). However, the detected
positive DPPH test suggests that all examined compounds can
react with free radicals. To confirm the free radical scavenging
ability of TSs compounds we examined their activity towards
Oꢀ2ꢀ and HO radicals. Superoxide anion radical produced from
KO2 in (CH3)2SO in the presence of 18-crown-6 ether as a solubi-
lizing agent (21) exhibits a strong light emission. The kinetic
•
•
Oꢀ2ꢀ þ Hꢀ ! HOOꢂ
(5)
(6)
•
•
HOOꢂ þ ð CH3Þ2 SO ! ð CH3Þ2 SO2 þ OHꢂ
140
120
100
80
120
100
80
60
60
40
2
1
40
20
39
4
3
33
30
30
28
28
27
25
20
0
0
20
20
40
60
80
100
120
140
160
180
17
16
15
Time [s]
1a 1b 1c 1d 1e
1f
2a 2b 2c 2d 2e
2f Vit CTrolox
Figure 4. The effect of the TSs (2.5 mmol/L) on the chemiluminescence intensity
accompanying 1 mmol/L Oꢀ2ꢀ generated in DMSO. Curve 1 — the chemiluminescence
kinetic from Oꢀ2ꢀ alone; curve 2, CL recorded under the same condition as curve 1 but
after an addition of 0.5 mL DMSO (control); curve 3 and 4 are the same as the control
but in the presence of compounds 1 f, 2 f dissolved in 0.5 mL DMSO (1.76 mol/L),
respectively. An arrow indicates the moment of the compound or DMSO addition.
Temperature 296 K. [Correction made here after initial online publication.]
Figure 3. Scavenging effects of thiazolidine-2,4-dione derivatives (2.5 mmol/L),
ascorbic acid and Trolox (1.25 mmol/L) on DPPH radical. Analysis was performed
5 min after addition of scavenging compound. The electron paramagnetic resonance
settings were microwave power 20 mW; modulation amplitude 0.2 G; time constant
0.2 s; receiver gain 3.2 ꢄ 104. Temperature 295 K. Reagent concentrations are the same
as in Fig. 2.
wileyonlinelibrary.com/journal/luminescence
Copyright © 2012 John Wiley & Sons, Ltd.
Luminescence 2013; 28: 900–904

Free radical scavenging activity of thiazolidine-2,4-dione derivatives
100
90
90
80
70
60
50
40
30
20
10
0
B
A
88
80
82
70
60
50
40
30
20
10
0
76
75
71
68
68
63
59
56
55
54
50
49
1a 1b 1c 1d 1e
1f
2a 2b 2c 2d 2e
2f Tiron NBT
1a 1b 1c 1d 1e
1f
2a 2b 2c 2d 2e
2f
Figure 5. Scavenging effect of thiazolidine-2,4-dione derivatives, Tiron and
p-nitroblue-tetrazolium chloride (NBT; 1 mmol/L) on the chemiluminescence from
1 mmol/L Oꢀ2ꢀ radicals generated in dimethyl sulfoxide. The remaining conditions are
the same as in Fig. 4.
Figure 6. (A) The electron paramagnetic resonance spectrum of the DMPO–OH
spin adduct arising from the Fenton reaction. (B) The inhibitory effect of thiazoli-
dine-2,4-dione derivatives compounds (2.5 mmol/L) on the DMPO–OH radical forma-
tion. The electron paramagnetic resonance settings were microwave power 20 mW;
modulation amplitude 0.5 G; time constant 0.3 s; receiver gain 4 ꢄ 104. Temperature
295 K.
The protective effect of TSs against Oꢀ2ꢀ, although observed in a
non-cellular system, is interesting from the antioxidant point
of view in cellular systems. The overproduction of ROS in a cell
is the main reason for changes caused by oxidative stress.
Superoxide radical is the first product of phagocytosis occurring
during inflammation as a result of respiratory burst (i.e. strongly
increased consumption of oxygen) (29,30).
effect. From group 2 only three compounds of six (i.e. 2c, 2d, 2f)
showed the scavenging activity ranging from 16% to 41%. This
finding implies that compounds from group 2 were less efficient
•
in the HO scavenging than from group 1.
The benzene ring, present in both groups of TSs plays an essen-
ꢀ
Although O2 is a short-lived species undergoing conversion to
•
tial role in the HO scavenging process. Findings for compounds
a rather unreactive molecule hydrogen peroxide (H 2 O 2) (31,32):
•
from group 1 effective in scavenging HO above 20% indicated
1
2O2ꢀꢀ þ 2Hþ ! H2O2 þ O2
(7)
that 4-Cl, 4-Br and 4-NO2 substitution in the benzene ring plays
an important role in radical scavenging activity. Compounds from
group 2, which differ from those in group 1 by the presence of a
carbonyl group and having 4-Cl, 4-Br or 4-NO2 substitution on
the benzene ring were able to scavenge HO radicals. This fact
points to a likely contribution of the Cl, Br and NO2 substituents
to the molecular stabilization, increasing TSs reactivity towards
the species is considered as a precursor of the strongest reactive
oxidizing agent HO radical, generated in a cell through the
Haber–Weiss/Fenton type reactions (equation 1).
Equation 7 also generates the excited states of molecular ox-
ygen, i.e. singlet oxygen (1O2), which is a strong oxidant in a cell.
To confirm further the free radical scavenging activity of the TSs
•
HO . The findings also suggest that presence of the second Cl atom
•
tested, we examined their reactivity towards HO , using the EPR
on the benzene ring suppresses reactivity of the tested compound
with this radical. The TS compounds from both groups with no
substituents in the benzene ring showed no activity.
spectroscopy and spin-trapping technique with DMPO as a trap.
Hydroxyl radical reacts with DMPO at a very high rate constant
(k = 4.3 ꢄ 109 mol/s), and arising spin adduct DMPO ꢂ OHꢀ
exhibits a four-line spectrum with 1:2:2:1 signal intensity and
nitrogen (aN) and b proton (aH) hyperfine coupling constants
aN = aH = 14.9 G [the spectrum was presented in a previous
paper (11)].
In conclusion, the scavenging properties for ROS and the
DPPH radical of TSs were examined for the first time. The results
showed that TSs examined were effective and efficient in
ꢀꢀ
•
scavenging O2 , and some of them were effective as HO
scavengers. Considering the structural similarity between the
•
ꢀ
To verify whether HO has been trapped by the DMPO spin trap
groups of compounds examined, it is very likely that the O2 scav-
we repeated the experiments in the presence of ethanol, which is
enging activity depends on the hydrogen donating ability of the
•
considered as a strong inhibitor of HO . Consistent with findings of
•
D ring, while the HO scavenging activity depends on the type of
Finkelstein et al. (15) we observed quenching of the DMPO ꢂ OHꢀ
spin adduct spectrum by approximately 30% in the presence of
ethanol (10% v/v) and the appearance of a new six-line spectrum
with aN = 15.8 G and aH = 2.8 G (data not shown). The spectrum is
due to spin trapping of the a-hydroxyethyl radical (33):
substituents on the benzene ring.
The examined compounds, therefore, are promising molecules
to prevent or control oxidative stress.
ꢀ
C2H5 OH þ HOꢀ ! C2H5 C HOH
(8)
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