Kinetics of β-Carotene Oxidation in the Presence of Highly Active Forms of μ-Carbido Diiron(IV) Tetraphenylporphyrinate

Article abstract of DOI:10.1134/S0036024418110390

Abstract: The oxidative destruction of β-carotene in the presence of highly oxidized forms of μ-carbido-bis[(5,10,15,20-tetraphenyl-21H,23H-porphyrinato)iron(IV)] (1 → 3) or its analog with axially coordinated imidazole (2 → 4) obtained under the action of tert-butyl hydroperoxide ^tBuOOH was studied by spectrophotometry. It was found that compound 3 is the oxo form of compound 1 singly oxidized at the macrocyclic ligand (π radical cation) under the action of which β-carotene is oxidized with a rate constant k = 3.3 L² mol^–2 s^–1. A?conclusion is drawn that short-lived compound 4 has unique EAS and is capable of oxidizing ^tBuOOH to form O₂, which makes it possible to consider it the model of peroxidase. The value of k for the reaction with the participation of β-carotene and compound 4 (k = 10.3 L² mol^–2 s^–1) is three times higher than that with the participation of compound 3. If a new portion of β-carotene is added, the process of its oxidative destruction in the presence of compounds 3 or 4 occurs without additives of the dimeric complex and peroxide. A?possible nature of compound 4 is discussed, as well as the influence of N-base in the coordination sphere of the complex on the nature of active intermediates and the rate of β-carotene decomposition.

Full text of DOI:10.1134/S0036024418110390

ISSN 0036-0244, Russian Journal of Physical Chemistry A, 2018, Vol. 92, No. 11, pp. 2128–2134. © Pleiades Publishing, Ltd., 2018.
Original Russian Text © O.R. Simonova, S.V. Zaitseva, E.Yu. Tyulyaeva, S.A. Zdanovich, O.I. Koifman, 2018, published in Zhurnal Fizicheskoi Khimii, 2018, Vol. 92, No. 11,
pp. 1692–1699.
CHEMICAL KINETICS
AND CATALYSIS
Kinetics of β-Carotene Oxidation in the Presence of Highly Active
Forms of μ-Carbido Diiron(IV) Tetraphenylporphyrinate
O. R. Simonovaa, S. V. Zaitsevaa, E. Yu. Tyulyaevaa,*, S. A. Zdanovicha, and O. I. Koifmana,b
a Krestov Institute of Solution Chemistry, Russian Academy of Sciences, Ivanovo, 153045 Russia
b Ivanovo State University of Chemistry and Technology, Ivanovo, 153000 Russia
*е-mail teu@isc-ras.ru
Received December 28, 2017
Abstract—The oxidative destruction of β-carotene in the presence of highly oxidized forms of μ-carbido-
bis[(5,10,15,20-tetraphenyl-21H,23H-porphyrinato)iron(IV)] (1 → 3) or its analog with axially coordinated
imidazole (2 → 4) obtained under the action of tert-butyl hydroperoxide tBuOOH was studied by spectropho-
tometry. It was found that compound 3 is the oxo form of compound 1 singly oxidized at the macrocyclic ligand
(π radical cation) under the action of which β-carotene is oxidized with a rate constant k = 3.3 L2 mol–2 s–1.
A conclusion is drawn that short-lived compound 4 has unique EAS and is capable of oxidizing tBuOOH to
form O2, which makes it possible to consider it the model of peroxidase. The value of k for the reaction with
the participation of β-carotene and compound 4 (k = 10.3 L2 mol–2 s–1) is three times higher than that with
the participation of compound 3. If a new portion of β-carotene is added, the process of its oxidative destruc-
tion in the presence of compounds 3 or 4 occurs without additives of the dimeric complex and peroxide.
A possible nature of compound 4 is discussed, as well as the influence of N-base in the coordination sphere
of the complex on the nature of active intermediates and the rate of β-carotene decomposition.
Keywords: β-carotene, oxidation, iron(IV) μ-carbido-tetraphenylporphyrinate, kinetics, active intermedi-
ates, peroxidase model
DOI: 10.1134/S0036024418110390
INTRODUCTION
the question of the nature of oxidizing active species
remains open [14–17]. In its turn, β-carotene, which
is a natural dye with various biological functions hav-
ing a highly conjugated system of double bonds is a
perfect subject of free radical attack in oxidation with
complex reaction products [18–22].
X-bridging (X = O, N, C) dimeric macrocyclic iron
complexes are currently the subject of active studies as
catalysts of redox reactions [1–8]. They are also bio-
mimetics that model the composition and active cen-
ters of natural enzymes [9, 10] acting via oxygen atom
transfer. These model complexes, by analogy with
their monomeric analogs make it possible to study the
reactivity of iron porphyrins and their chemical prop-
erties to understand complex structural and electron
features of the active site. The peroxidase activity of
iron-containing enzymes, which determines their
ability to initiate metabolism and detoxication of per-
oxides by oxidation with the formation of O2, is
important for the antioxidant system of a human
organism. The studies of mechanisms of such reac-
tions, especially the nature of active intermediates, is
complicated by their high reactivity and short life-
times, which restricts the choice of experimental tech-
niques applicable to the identification of intermediate
oxidized forms. The key intermediates in chemical
transformations of substrates under the action of
enzymes are the highly oxidized form of porphyrinoid
complexes O=Fe(IV) and the π radical cation form
oxidized at the macrocyclic ligand [11–13]. However,
The goal of this work was to study the reactivity and
fundamental features of oxidants in heme-containing
enzymes using μ-carbido diiron(IV) complex with
5,10,15,20-tetraphenyl-21H,23H-porphyrin as
a
model compound when its forms participate in the
oxidative decomposition of β-carotene.
EXPERIMENTAL
μ-Carbido-bis[(5,10,15,20-tetraphenyl-21H,23H-
porphyrinato)iron(IV)] [FeTPP]2C (1) was synthesized
according to the technique described in [23] from
ClFeTPP obtained and isolated according to reference
data [24]. 100 mg (0.14 mmol) of ClFeTPP were dis-
solved in 20 mL of isopropanol. KOH (1 g,
0.018 mmol) was added, and the mixture was boiled at
120°C for 20 min with stirring. The reaction was
accompanied by changes in the color of the solution
from red wine to magenta. CHCl3 (5 mL) was added to
2128

KINETICS OF β-CAROTENE OXIDATION IN THE PRESENCE
2129
0
the reaction mixture dropwise, and then the reaction
mixture was cooled to 40°C and diluted with water.
The organic layer containing [FeTPP]2C was sepa-
rated and chromatographed on Al2O3 (Brockmann
activity II) using CH2Cl2 as an eluent. EAS in C6H6
(A0, Aτ, and A∞ are absorbances at a working
logCCar
wavelength at the initial, current and final moment of
time, respectively).
(λmax, nm): 400, 522. IR spectrum: (C6H6, ν, cm–1),
960 (νas Fe=C=Fe), 423 (νs Fe=C=Fe), 461 (Fe–
DISCUSSION
The structural diversity of carotenoids belonging to
one of the most important groups of natural dyes
enables their diverse functions. To be specific, the
antioxidant properties of β-carotene, which has a
polyene structure are stipulated by its ability to enter
oxidation reactions under the action of free radicals.
Reactions of this type in the aqueous medium and
N
TPP). ESI–MS: m/z [FeTPP]2C]+ 1349.3. For
C89H56N8Fe2 calculated 1349.17.
μ-Carbido-bis[(imidazole)(5,10,15,20-tetraphenyl-
21H,23H-porphyrinato)iron(IV)](Im)2[FeTPP]2C (2).
Imidazole (CIm = 10–3 mol/L) was added to a solution
of [FeTPP]2C (C1 = 10–6 mol/L) in benzene. The organic solvents are actively studied. Depending on
the nature of oxidant and reactivity, the time required
for β-carotene oxidative destruction reaction differs
[18, 20, 25, 26]. The catalytic role of metalloporphy-
rins in β-carotene oxidation was considered in very
few publications: (tetrakis(dichlorophenyl)porphyrin)
reaction of formation of bis-axial complex was con-
trolled by changes in EAS of the reaction mixture.
EAS in C6H6 (λmax, nm): 403, 526, 562, 605. IR spec-
trum (C6H6, ν, cm–1): 936 (νas Fe=C=Fe), 419 (νs
Fe=C=Fe), 435 (Fe–NTPP), 478 (Fe–NIm). ESI-MS:
m/z [(Im)2[FeTPP]2C]+ 1485.1. For C95H64N12Fe2
calculated 1485.33.
ruthenium(II)
and
(5,10,15,20-tetrakis(2,4,6-
trimethylphenyl)porhyrin)ruthenium(II)
carbonyl
were chosen as co-oxidants in carotene oxidative
t
Oxidized [FeTPP]2C (3) and (Im)2[FeTPP]2C (4)
destruction with BuOOH in hexane [27] and meta-
were obtained by the reaction of compounds 1 and 2,
chloroperoxybenzoic acid in benzene [19], respec-
tively. It was noted in the cited works that ruthenium
porphyrin complexes enter the reaction in the active
oxo form O=Ru(IV), but the mechanism of activation
for these species has not been proposed. In connection
with the above-mentioned catalytic activity of μ-
dimeric iron porphyrinoid complexes, the reaction
between β-carotene and oxidized derivatives of com-
pound 1 or its analog 2 with axially coordinated imid-
azole was carried out.
t
respectively, with BuOOH (
= 2.3 × 10–4–
CtBuOOH
2.3 × 10–3 mol/L) in benzene. The reactions of forma-
tion of oxidized forms of complexes were controlled by
changes in EAS of the reaction mixture.
EAS (3) in C6H6 (λmax, nm): 413, 572, 627.
IR spectrum (C6H6, ν, cm–1): 1295 (Cα–Cβ, Cα–
N), 914 (νas Fe=C=Fe), 422 (νs Fe=C=Fe), 435 (Fe–
NTPP).
The initial EAS (Fig. 1, line 1) of compound 1 in
benzene (C1 = 10–6 mol/L) changed upon adding
EAS (4) in C6H6 (λmax, nm): 414, 569, 609.
EAS spectra were recorded using a Cary 50 instru- tBuOOH (
ment. IR spectra were obtained by the attenuated total
= 2.3 × 10–3 mol/L) and trans-
formed to the spectrum of compound 3, which is sin-
gly oxidized π radical cation of the oxo form of the ini-
CtBuOOH
reflection method using Bruker Vertex V80 spectrom-
eter in the range of frequencies 4000–400 cm–1 (on the
average 64 scans) with a resolution of 2 cm–1 at a stan-
dard temperature. IR spectra were recorded using an
MVP 2 SeriesTM (Harrick) attachment with a dia-
mond crystal. The products of oxidative destruction
were analyzed by electrospray ionization mass spec-
trometry using a Bruker microTOF spectrometer.
tial complex O=FeTPP+•=C=FeTPP. The mecha-
nism of formation of highly oxidized forms of μ-
dimeric tetrapyrrole iron complexes, which were reli-
ably identified by various physicochemical methods,
under the action of H2O2 and organic peroxides is well
known [1–8, 28, 29]. Therefore, the bathochromic
shift of the В band from 400 to 413 nm and the growth
of Q bands at 570–630 nm in the EAS were attributed
to the formation of π radical cation 3 (Fig. 1, line 2). A
change in the electron structure of the dimeric iron
complex is reflected in the appearance of the absorp-
tion band in the IR spectrum at 1290 cm–1, which is
related to the vibrations of the Cα–Cβ and Cα–N
t
We used tert-butyl hydroperoxide BuOOH (98%)
and carotene (97%) from Sigma-Aldrich and dried
benzene.
The apparent rate constants kapp and the rate con-
stants k of carotene oxidation at 298 K were deter-
mined by changes in absorbance (A) of the reaction
mixture at a working wavelength that corresponded to bonds in pyrrole rings (Fig. 2а) [30]. When changes in
the maximum of carotene absorption band λmax
=
the EAS ceased, β-carotene (CCar = (4.33–8.54) ×
10‒4 mol/L) was added to the solution, and changes in
463 nm at constant concentrations of initial com-
t
pounds 1, 2, and BuOOH and different concentra- the absorbance were recorded at a wavelength equal to
tions of carotene by least-squares optimization of the the maximum of the carotene absorption band λmax
=
dependence log(A0 – A∞)/(Aτ – A∞)–τ and logkapp
–
463 nm (Fig. 1, lines 3, 4) until its complete disappear-
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SIMONOVA et al.
A
1
3
A
3
4
2
500
600
λ, nm
1
2
4
350
400
450
500
550
600
650 λ, nm
–6
Fig. 1. Electron absorption spectra of compounds in benzene: (1) compound 1 (C = 10 mol/L); (2) compound 3 (
=
CtBuOOH
1
–3
–4
2.3 × 10 mol/L); (3) compound 3 after adding β-carotene (C = 4.3 × 10 mol/L); (4) the same as 3 upon reaction com-
Car
pletion.
ance. Note that EAS of β-carotene remains tra of the initial compound 1 or its π radical cation
unchanged in pure benzene, and in the presence of form 3. This intermediate (compound 5) is likely the
tBuOOH for 6 h the intensity of absorption bands only
result of hemolytic O–O bond cleavage in the perox-
slightly decreases. If compound 3 participates, the ide –O• coordinated to the iron cation, which then
decomposition of β-carotene occurs for several min- transforms into the radical cation on the macrocycle,
utes. The apparent rate constants of the reaction are of and the product of further reduction in the process of
the formal first order (log kapp) in the 3–β-carotene– β-carotene oxidation (Scheme 1).
benzene system at a constant concentration of metal-
Moreover, Criegee biradicals can be intermediates
in the reaction [20], which are capable of participating
in further oxidation both in the free form and coordi-
loporphyrin linearly correlate with log CCar (the cor-
relation equation is log kapp = 0.501 + 0.931log CCar
,
R2 = 0.994). The value of tan α ≈ 1 corresponds to the nated on iron cation in the dimeric complex. The pres-
first order with respect to substrate and, therefore, to ence of active species in the solution is supported by
the second-order rate equation (1) with a reaction rate further reaction of carotene decomposition without
constant k = 3.3 L2 mol–2 s–1.
−dCCar /dτ = kC3CCar
tBuOOH additives. When adding a new portion of the
substrate to the final mixture, the β-carotene band,
which appeared at 463 nm, disappears again, while the
bands of oxidized form 5 are retained. Their intensity
does not change upon ten cycles. The rate constant of
the process remains almost unchanged during these
ten cycles. Figure 3a shows the kinetic curves of the
oxidative decomposition of β-carotene in the presence
of compound 3 if the substrate is periodically added to
the reaction mixture. Table 1 shows the reaction prod-
ucts identified by the ESI–MS method using refer-
ence data.
(1)
.
The oxidative decomposition of β-carotene is a
complex multiple-step process that occurs via the for-
mation of intermediate mono- and biradical forms,
apocarotenals, epoxides and other species and that
leads to the formation of many products (>15) [18–20,
25–27]. The reactions of this sort were studied earlier
in the mixture of organic solvents. Under the action of
variousoxidants,thezerothorderwithrespecttoβ-car-
otene (see [20] and references therein) was found. It
can be explained by the participation of the products
of primary oxidation of the initial compound rather
than the initial compound itself in the rate-limiting
step. However, when studying analogous reactions in
food products, like in our case, the order with respect
to β-carotene was the first [20].
The action of compound 3 in the reaction studied
is analogous to the action of the π radical cation of nat-
ural enzymes (compound I) participating in oxidation
reactions in living organisms and various biomimetics
(Scheme 1).
It is well known that axial ligands on iron cations
The final spectrum of the reaction mixture after the that are in the trans position to the active site deter-
disappearance of the band corresponding to β-caro- mine the activity of these compounds when binding
tene does not coincide with the spectrum of any of the and transporting gases, in electron transfer, and in
initial compounds. Nor does it coincide with the spec- catalysis [23, 28, 31–35]. To elucidate the effect of
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KINETICS OF β-CAROTENE OXIDATION IN THE PRESENCE
OtBu
2131
O
а
FeIV
C
H+
FeIV
tBuO
tBuOOH
O
FeIV
FeIV
C
C
FeIV
FeIV
1
5
b
O
FeIV
k
Oxidation
products
β-Carotene
C
FeIV
3
Scheme 1.
pound 4) and is accompanied by changes in the EAS
shown in Fig. 4 (lines 1 and 2). However, the maxi-
mums of the spectral line 2, which corresponds to the
oxidized form 4 do not coincide with those of the π
radical cation form 3 (Fig. 1, line 2), and in the IR spec-
trum of the complex, the band corresponding to the
vibration of the form oxidized at the macrocycle is
absent (Fig. 2, c). Moreover, when detecting form 4 by
spectral methods, the solution starts to drill, which
points to the evolution of O2. When adding β-carotene to
c
1400
1350
1300
1250
1200
ν, сm−1
the solution, it decolorizes for 80 s (k ≈ 25 L2 mol–2 s–1).
The kinetics of β-carotene decomposition in the pres-
ence of compound 4 was studied in the range of mea-
Fig. 2. IR spectra of (a) compound 3, (b) 3–β-carotene
and (c) compound 4. The point marks vibrations of π rad-
ical cation form.
t
surable rates at a lower concentration of BuOOH
(
= 2.3 × 10–3 mol/L). The linear dependence
CtBuOOH
N-bases in the coordination sphere of the iron com-
plex studies on the rate of formation and the form of
the active species in the oxidative destruction of β-car-
otene, the reaction was studied with the participation
of compound 4, which is the oxidized form of the axial
complex 2.
of apparent rate constants of the reaction of formal
first order (log kapp) for 4–β-carotene–benzene sys-
tem (correlation equation log kapp = 1.019 +
0.992logCCar, R2 = 0.999) has tan α = 1. The second-
order rate constant k in the rate equation analogous to
Eq. (1) with C4 instead of C3 is 10.3 L2 mol–2 s–1, which
is three times higher than that of the reaction with
compound 3. β-Carotene added to the reaction mix-
ture upon the reaction completion is also decolorized,
similarly to the reaction with the participation of com-
pound 3. However, after several cycles, the rate of the
process gradually decreases, which is evident from a
decrease in the apparent constant kapp (Fig. 3b).
The introduction of imidazole molecules into the
coordination sphere of complex 1 leads to the forma-
tion of compound 2 (Fig. 4, line 1) [31], which is anal-
ogous to axial μ-carbido diiron(IV) macrocyclic com-
plexes studied earlier [28, 29]. The addition of
tBuOOH (
CtBuOOH
= 8.6 × 10–3 mol/L) to the solution
of compound 2 in benzene leads to its oxidation (com-
RUSSIAN JOURNAL OF PHYSICAL CHEMISTRY A Vol. 92 No. 11 2018

2132
SIMONOVA et al.
(a)
A
0.6
0.4
0.2
0
0
200
400
600
800
1000
(b)
1200
1400
1600
1800
τ, s
A
1.0
0.6
0.2
1000
2000
3000
4000
5000
τ, s
Fig. 3. Kinetic curves for the reaction of oxidative decomposition of β-carotene in the presence of (a) compound 3 and (b) com-
pound 4 when the substrate is periodically added to the reaction mixture.
The role of N-bases coordinated by metal, which calculated by the DFT method for (FePc)2C in [40],
stabilize highly covalent forms of both monomeric and
dimeric macrocyclic and nonheme iron complexes in
increasing the reactivity and catalytic activity of these
compounds in oxidation reactions is described well in
the literature [23, 28, 31–36]. However, the reaction
features and spectral data shown in Figs. 1 and 4 point
to the participation of carotene in the oxidation of var-
ious active forms of complexes 1 and 2. If in the case of
compound 1, form 3 stable in the solution and oxi-
dized at a macrocyclic ligand (Fig. 2b) participates in
the reaction, the position of bands in the EAS for
compound 4 (414 and 609 nm) does not allow one to
identify it as a singly oxidized π radical cation form. It
is obvious that compound 4 is so active that it can oxi-
but there are no experimental data that support the
proposed structure. When studying the oxidation
reactions of monomeric iron complexes with corroles,
corrolazines, and porphyrins and their catalytic roles
in oxidation of various substrates, reaction schemes
were proposed that involve the participation of oxo
forms of iron(V) [41–45]. The method of laser photol-
ysis was used to oxidize iron(IV) 5,10,15-tri(pentaflu-
orophenyl)(chlorato)corrolate (O2ClO)FePFPC in
CH3CN with the formation of short-lived reactive
intermediate that was detected by spectrophotometry
[46]. Based on its unique EAS, which differed from
the spectrum of π radical cation, and the high reactiv-
ity, the authors denoted this species as an oxo complex
of iron(V). The latter is isoelectronic to singly oxidized
t
dize BuOOH to form O2 analogously to oxidized
forms of some monomeric and dimeric porphyrin
complexes of iron(IV) [37, 38].
According to the references data, μ-carbido
diiron(IV) complexes with tetraazaporphyrin, tetrap-
henylporphyrin, phthalocyanine, and tetra-(tert-
butyl)phthalocyanine (homo- and heteroleptic) can
be subjected to two one-electron oxidations electro-
chemically [7, 23, 33, 39]. The product of the first oxi-
dation in all cases is a radical cation with a positive
charge localized on one of the macrocyclic ligands,
and the product of the second oxidation was not iden-
tified. Only in the case of (FeTAP)2C two processes
with potentials in the positive range were assigned to
consecutive oxidations of two macrocycles in the com-
plex with the formation of π radical dication [7]. The
other highly covalent species can be the oxo form of
the Fe4+ complex with the localization of a positive
charge on one of the macrocyclic ligands and a radical
on the bridging carbon atom. The hypothetical geo-
metric and electronic structure of such a species was
Table 1. The products of β-carotene oxidation identified by
the ESI–MS method after the reaction in the presence of
compounds 3 and 4
[M+]
Compound
Ionone
174
166
208
180
208
377
392
152
192
184
8-Apo-β-carotenal
5,6-Epoxy-β-ionone
Dihydroactinidiolide*
10'-Apo-β-carotenal
β-Cyclocitral
β-Ionone
Criegee biradical
12'-Apo-β-carotenal biradical
7-Apo-β-carotenal biradical
* Present only after reaction with the participation of compound 4.
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KINETICS OF β-CAROTENE OXIDATION IN THE PRESENCE
2133
A
A
3
4
1
3
2
500
550
550
600
600
λ, nm
650
1
2
4
350
400
450
500
650 λ, nm
–3
Fig. 4. Electron absorption spectra of compounds in benzene: (1) compound 2 and (2) compound 4 ( tBuOOH = 2.3 × 10 mol/L);
C
–4
(3) compound 4 after adding β-carotene (C = 4.3 × 10 mol/L); (4) the same as 3 upon reaction completion.
Car
IV
+•, which is more reactive
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This work was supported by the Russian Founda-
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No. 11
2018