Spectroscopic characterization of a phenolate bound FeII-O 2 adduct: Gauging the relative "push" effect of a phenolate axial ligand

Article abstract of DOI:10.1039/c3cc47528j

Dioxygen adducts of solvent, imidazole and phenolate bound iron porphyrin complexes are reported. The data show that the Fe-O vibration of the Fe-O ₂ species shifts from 584 cm^-1 to 570 cm^-1 as neutral axial ligands are re

Full text of DOI:10.1039/c3cc47528j

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Spectroscopic characterization of a phenolate
bound FeII–O2 adduct: gauging the relative
‘‘push’’ effect of a phenolate axial ligand†
Cite this: Chem. Commun., 2014,
50, 5218
Received 1st October 2013,
Accepted 31st October 2013
Pradip Kumar Das, Kaustuv Mittra and Abhishek Dey*
DOI: 10.1039/c3cc47528j
www.rsc.org/chemcomm
Dioxygen adducts of solvent, imidazole and phenolate bound iron
porphyrin complexes are reported. The data show that the Fe–O
vibration of the Fe–O2 species shifts from 584 cmÀ1 to 570 cmÀ1 as
neutral axial ligands are replaced by the anionic phenolate ligand.
The iron–oxygen adduct is a well known intermediate in the catalytic
cycles of heme-containing enzymes involved in oxygen transport
and storage (e.g. in hemoglobin and myoglobin),1,2 O2 activation
(e.g. cytochrome P450, heme dioxygenase, etc.),3,4 and O2 reduction
(cytochrome c oxidase).5 The ‘‘push-effect’’ of the anionic thiolate ligand
in Cyt P450 has been proposed to lower the FeIII/II reduction potential,
weaken axial ligand binding and affect the heterolytic O–O bond
cleavage of a FeIII–OOH species (compound 0) to form a highly reactive
intermediate which is known as compound I.6–9 Apart from the more
common thiolate and imidazole axial ligands, phenolate (the coordi-
nating functional group of tyrosine) is also known to bind heme in
catalases, which is a key enzyme involved in disproportionation of the
reactive oxygen species, H2O2.10,11 However, very few experimental
studies have investigated the ‘push-effect’ of an anionic phenolate
ligand present in the active site of heme catalases.12
Fig. 1 The schematic representation of the complexes.
complex has not been reported to date. Herein, we describe the
formation of a diamagnetic oxygen adduct that possesses covalently
bound trans axial phenolate (1) and imidazole (3) ligands (Fig. 1), and
their characterization using resonance Raman spectroscopy (rR). The
comparison of the nFe–O vibration of the Fe–O2 adducts provides a
measure of the trans effect of a phenolate axial ligand.
The model compound (PIM) was synthesized according to
previous reports.29 A synthetic model of the phenolate bound
FeIII porphyrin complex, mimicking the phenolate co-ordination
of catalases, is prepared and the phenolate bearing arm is
covalently attached to the porphyrin macrocycle (Scheme 1).
The method utilizes the benign and very high yielding
Cu(I) catalyzed 1,3 cycloaddition of terminal alkylazides with
Due to the importance of these Fe–O2 species in nature, they have
generated significant research interest over the last three decades.13–15
Several synthetic Fe–O2 adducts have been reported wherein reso-
nance Raman (rR) spectroscopy has been used as a primary tool for
their characterization.16–19 In most synthetic systems, the Fe–O (nFe–O
vibration of a Fe–O2 adduct is observed between 550 and 585 cmÀ1
The O–O vibration is observed between 1140 and 1190 cmÀ1 20–23
)
.
.
Numerous oxy-heme synthetic models with a nitrogen axial ligand,
mimicking the histidine ligation of Mb and Hb, are reported where
the nFe–O vibrations are in the range 567–582 cmÀ1 22,24,25
.
A few
dioxygen adducts of thiolate-coordinated hemes have been reported
and they show the nFe–O vibration at around 530–545 cmÀ1 26–28
.
However the Fe–O2 adduct of the phenolate ligated iron porphyrin
Department of Inorganic Chemistry, Indian Association for the Cultivation of Science,
India. E-mail: icad@iacs.res.in; Fax: +91-33-2473-2805; Tel: +91-33-2473-4971
† Electronic supplementary information (ESI) available: Synthetic details, char-
acterization, resonance Raman (rR) and EPR. See DOI: 10.1039/c3cc47528j
Scheme 1 The synthetic scheme of the desired complexes.
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Fig. 2 EPR data for the oxidized, reduced and oxygenated samples of the
FeIII(OPhP) complex, at 77 K, 10 mW, gain 1 Â 104.
3-hydroxyphenylacetylene.30 In the final step, the coordination of
phenol to Fe is achieved by treatment of the precursor phenol
complex with activated K2CO3 in methanol to yield the desired
phenolate bound iron porphyrin complex FeIII(OPhP).
The X-band EPR data of the oxidized complex, FeIII(OPhP) in THF,
shows an axial high spin (HS) signal at g B 6 (Fig. 2, pink), indicative
of an S = 5/2 ground state (GS) at 77 K. This is consistent with the
S = 5/2 GS observed in the active sites of heme catalases.31 Upon
reduction, the complex becomes EPR silent (Fig. 2, blue), indicating
the formation of a Fe(II) species. Upon exposing the reduced sample
to O2 at À80 1C no new EPR signal is observed (Fig. 2, green),
consistent with the formation of an S = 0 diamagnetic Fe–O2 adduct.
The rR spectra, in the low frequency region of the oxidized
complex FeIII(OPhP), show peaks at 573 and 589 cmÀ1, corres-
Fig. 3 rR data for the oxidized, reduced and oxygenated samples of the
FeIII(OPhP) complex, at 77 K (A) (500 cmÀ1–700 cmÀ1) and (B) 1250 cmÀ1
1350 cmÀ1 region showing the C–O vibration.
–
ponding to Fe–OPh vibrations (Fe–O stretch and n10) (Fig. 3A), substitution (Fig. 4A), i.e., binding of the anionic phenolate ligand to
consistent with the values reported for the active sites of bovine the Fe center lowers the nFe–O vibration by 14 cmÀ1. A similar nFe–O
liver catalases.10 The nFe–O frequency of the oxygen adduct 1 was reported for a MeOH bound Fe–O2 adduct.18
appears at 570 cmÀ1 and shifts to 548 cmÀ1 upon 18O2 substitution
The oxidized PIM complex shows an axial HS EPR signal at g B 6
(Fig. 3A). A very weak feature has potentially been identified at which mimics the coordination and spin state properties of histidine
1147 cmÀ1 that might correspond to the O–O stretch which shifts coordinated heme active sites.32 The reduced and oxy adducts are EPR
to 1088 cmÀ1 upon 18O2 substitution (Fig. S1, ESI†).
silent (Fig. S5, ESI†). The rR spectra of imidazole bound dioxygen
In the high frequency region, the rR data show a band at adduct 3 display an isotope-sensitive band at 578 (16O2)/552 (18O2) cmÀ1
1320 cmÀ1 in the oxidized complex (Fig. 3B, pink) which is absent in the low-frequency region (Fig. 4B), which is assigned to the Fe–O
in the precursor phenol complex or the PIM complex (Fig. S2, ESI†) stretching vibration of the Fe–O2 species. The observed nFe–O frequency
and can be tentatively assigned to the C–O stretching vibration of the is in the range of those reported for the histidine/imidazole bound
bound phenolate.10 This band shifts to 1294 cmÀ1 in the reduced hemoproteins and synthetic models (nFe–O = 568–582 cmÀ1).16,33 Thus
state (Fig. 3B, green) and further shifts to 1310 cmÀ1 in the dioxygen binding of an anionic phenolate ligand lowers the nFe–O vibration
adduct (Fig. 3B, blue and violet). These data suggest that the relative to a neutral imidazole ligand by 8 cmÀ1
.
phenolate ligand stays bound to the iron center in the oxidized,
The rR spectra of the complex FeIII(OPhP) shows the oxidation and
reduced and oxygen bound forms. Note that definitive assignment spin state markers, n4 and n2 bands, at 1364 and 1555 cmÀ1 respectively
of the phenolate vibrations will entail the synthesis of an O18 labeled (Fig. S6, ESI,† pink), which is typical of S = 5/2 Fe(III) porphyrins and is
phenol linker which is not easily accessible.
consistent with the EPR data. Upon reduction of this complex, the
The corresponding phenol precursor FeIII(HOPhP) shows similar marker bands shift to 1347 cmÀ1 and 1541 cmÀ1 (Fig. S6, ESI,† green),
changes in the EPR spectra as the oxygen adduct is formed (Fig. S3, indicating the formation of a HS S = 2 Fe(II) species. The O2 adduct
ESI†). The absence of nFe–O and nC–O vibrations in the low and high (both 16O2 and 18O2), in addition to some residual HS Fe(II) and Fe(III)
frequency regions of the rR spectra of the oxidized phenol complex signals, shows a new set of bands at 1368 and 1567 cmÀ1 (Fig. S6, ESI,†
FeIII(HOPhP) is indicative of the fact that the phenol may not be violet and blue). These n4 and n2 vibrations are characteristic of Fe–O2
bound to the iron centre as in the phenolate complex FeIII(OPhP) adducts where the Fe center is in a low-spin S = 1/2 Fe(III) state
(Fig. S4, ESI†). A solvent molecule (THF or MeOH) may be bound antiferromagnetically coupled to the oxygen, resulting in the formation
instead to the Fe center.19 The oxygen adduct of complex 2 shows a of a diamagnetic iron-oxy adduct. The rR data of the precursor phenol
nFe–O vibration at 584 cmÀ1 which shifts to 557 cmÀ1 upon 18O2 complex and the PIM complex show a similar trend of n4 and n2 bands
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This work is funded by CSIR [Grant 01(2412)10/EMr-II] and DST
(Grant SR/IC-35/2009). P.K.D. and K.M. acknowledge a CSIR SRF
fellowship.
Notes and references
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Complex
n(Fe–O2)/cmÀ1
Ref.
À
FeII(OPhP)(O2 ꢀ)(1)
570
584
578
567–576
537–545
568–582
530–540
This work
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2, 34
26, 28, 35
16, 33
FeII(HOÀPhP)(THF)(O2 ꢀ)(2)
À
PIM(O2 ꢀ)(3)
(HbA/Mb)Fe–O2
(P450cam)Fe–O2
(Imd)(TPpivP)Fe–O2
(C6H5SÀ)(TPpivP)Fe–O2
26, 36
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5220 | Chem. Commun., 2014, 50, 5218--5220
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