Nitric oxide dioxygenation reaction by oxy-coboglobin models: In-situ low-temperature FTIR characterization of coordinated peroxynitrite

Article abstract of DOI:10.1021/ja305774v

The oxy-cobolglobin models of the general formula (NH₃)Co(Por) (O₂) (Por = meso-tetra-phenyl and meso-tetra-p-tolylporphyrinato dianions) were constructed by sequential low temperature interaction of NH ₃ and dioxygen with microporous layers of Co-porphyrins. At cryogenic temperatures small increments of NO were introduced into the cryostat and the following reactions were monitored by the FTIR and UV-visible spectroscopy during slow warming. Upon warming the layers from 80 to 120 K a set of new IR bands grows with correlating intensities along with the consumption of the ν(O₂) band. Isotope labeling experiments with ¹⁸O ₂, ¹⁵NO and N¹⁸O along with DFT calculations provides a basis for assigning them to the six-coordinate peroxynitrite complexes (NH₃)Co(Por)(OONO). Over the course of warming the layers from 140 to 170 K these complexes decompose and there are spectral features suggesting the formation of nitrogen dioxide NO₂. Upon keeping the layers at 180-210 K the bands of NO₂ gradually decrease in intensity and the set of new bands grows in the range of 1480, 1270, and 980 cm ^-1. These bands have their isotopic counterparts when ¹⁵NO, ¹⁸O₂ and N¹⁸O are used in the experiments and certainly belong to the 6-coordinate nitrato complexes (NH ₃)Co(Por)(η¹-ONO₂) demonstrating the ability of oxy coboglobin models to promote the nitric oxide dioxygenation (NOD) reaction similar to oxy-hemes. As in the case of Hb, Mb and model iron-porphyrins, the six-coordinate nitrato complexes are not stable at room temperature and dissociate to give nitrate anion and oxidized cationic complex Co(III)(Por)(NH₃)_1,2.

Full text of DOI:10.1021/ja305774v

Article
pubs.acs.org/JACS
Nitric Oxide Dioxygenation Reaction by Oxy-Coboglobin Models: In-
situ Low-Temperature FTIR Characterization of Coordinated
Peroxynitrite
Tigran S. Kurtikyan,*,†,‡ Shahane R. Eksuzyan,† Vardan A. Hayrapetyan,† Garik G. Martirosyan,†
Gohar S. Hovhannisyan,† and John A. Goodwin§
†Molecule Structure Research Centre (MSRC) of the Scientific and Technological Centre of Organic and Pharmaceutical Chemistry
NAS, 0014, Yerevan, Armenia
§Department of Chemistry and Physics, Coastal Carolina University, South Carolina 29526-6054, United States
S
* Supporting Information
ABSTRACT: The oxy-cobolglobin models of the general
formula (NH3)Co(Por)(O2) (Por = meso-tetra-phenyl and
meso-tetra-p-tolylporphyrinato dianions) were constructed by
sequential low temperature interaction of NH3 and dioxygen
with microporous layers of Co−porphyrins. At cryogenic
temperatures small increments of NO were introduced into
the cryostat and the following reactions were monitored by the
FTIR and UV−visible spectroscopy during slow warming.
Upon warming the layers from 80 to 120 K a set of new IR bands grows with correlating intensities along with the consumption
of the ν(O2) band. Isotope labeling experiments with 18O2, 15NO and N18O along with DFT calculations provides a basis for
assigning them to the six-coordinate peroxynitrite complexes (NH3)Co(Por)(OONO). Over the course of warming the layers
from 140 to 170 K these complexes decompose and there are spectral features suggesting the formation of nitrogen dioxide NO2.
Upon keeping the layers at 180−210 K the bands of NO2 gradually decrease in intensity and the set of new bands grows in the
range of 1480, 1270, and 980 cm−1. These bands have their isotopic counterparts when 15NO, 18O2 and N18O are used in the
experiments and certainly belong to the 6-coordinate nitrato complexes (NH3)Co(Por)(η1−ONO2) demonstrating the ability of
oxy coboglobin models to promote the nitric oxide dioxygenation (NOD) reaction similar to oxy-hemes. As in the case of Hb,
Mb and model iron-porphyrins, the six-coordinate nitrato complexes are not stable at room temperature and dissociate to give
nitrate anion and oxidized cationic complex Co(III)(Por)(NH3)1,2.
Subsequent attack of the ferryl O-atom by NO2 through its
nitrogen atom produces O-bound nitrate, decay of which
results in metHb and nitrate anion.4
INTRODUCTION
■
Nitric oxide (NO) has been well characterized as an important
regulatory molecule in mammalian biology.1 The interaction of
NO with ferro- and ferri-heme proteins plays central roles in
cardiovascular regulation and neurotransmission.2 While
submicromolar NO concentrations are sufficient to perform
these functions, overproduction of nitric oxide can result in
harmful consequences mainly due to formation of the
peroxynitrite anion with further decomposition to aggressive
free radicals.3
It is commonly accepted that heme proteins are the principal
agents responsible for the NO scavenging.2−4 Under anaerobic
conditions, NO detoxification occurs via a 2-electron reduction
of two NO molecules to N2O by NO reductases (NORs). In
many bacteria and archaea, this NO-reductase reaction is
catalyzed by diiron proteins.4e,f Under aerobic conditions, the
main part for NO scavenging by red cells involves its direct
reaction with HbO2 leading to formation of nitrate anion and
the ferric form of the protein, metHb. It is suggested that this
process proceeds through the formation of coordinated
peroxynitrite that undergoes homolytic O−O bond cleavage
forming ferryl species and free radical nitrogen dioxide NO2.
Although all researchers are prone to think that the first stage
of the reaction is the formation of coordinated peroxynitrite, at
this moment there is no strong experimental evidence of its
observation. Kinetics studies by Herold et al. using rapid
scanning UV−vis spectroscopy at 20 °C followed the reactions
of NO with HbO2 and with oxy-myoglobin (MbO2) and
demonstrated the formation of transients with ms lifetimes.5
Subsequently, Olson et al.,6 using EPR to probe rapid-freeze
quenched (RFQ) samples from the NO reaction with HbO2,
reported formation of a high-spin Fe(III) species on this same
time scale. These intermediates were assigned as high-spin ferri-
heme peroxynitrite complexes on the basis of their electronic
spectra;5 however, Goldstein et al.7 reported an intermediate
with analogous spectral properties from the reaction of ferryl
myoglobin with NO2 and concluded that it was the nitrato
analog Fe(III)(ONO2). Notably, resonance Raman spectral
Received: June 19, 2012
Published: August 10, 2012
© 2012 American Chemical Society
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(RRS) studies of the ms intermediate formed by reaction of
NO with MbO2 in 3 °C alkaline solution and trapped by RFQ
identified this as the nitrato, not the peroxynitrito, complex.8
A spectroscopic study was recently carried out in our
laboratory to probe the viability of a FeIII(OONO)
intermediate in the reaction of the six-coordinate oxy-heme
model complex (NH3)Fe(Por)(O2) with NO in low-temper-
ature sublimed solids.9 Surprisingly at temperatures as low as
80−100 K the six-coordinate nitrato complexes (NH3)Fe-
(Por)(η1-ONO2) were formed without spectral detection of
any intermediates. In particular, peroxynitrite complexes were
not observed, and this result implied that, if formed,
isomerization of this putative intermediate to the nitrato
product was quite facile even under these conditions.
In this work we returned to this problem by using Co-
porphyrins as the model compounds. In studies of
hemoproteins, the technique of replacement of the neutral
iron porphyrin prosthetic group with different metalloporphyr-
ins has been very useful,10 especially with Co-porphyrins that
possess dioxygen binding ability, but contrary to EPR silent
Fe(II)-porphyrins (d6) these can be studied by EPR due to
single odd-electron configuration (d7). The EPR studies of Co
hemoproteins provided many important insights for under-
standing the electronic and geometric structures, which were
not possible for the diamagnetic deoxy and oxy iron
hemoproteins. With regard to the observation of peroxynitrite
complexes, the results obtained for the Co-containing systems
were more promising.11 Koppenol and co-workers reported12
the synthesis of the tris(tetraethyl-ammonium)-
pentacyanoperoxy nitritocobaltate(III) complex by the reaction
of NO with pentacyanodioxygencobaltate(II). They explained
its stability with the presence of cyano groups diminishing the
Lewis acid character of the metal. Theopold and co-workers
attempted to isolate a peroxynitrito complex from the reaction
of the dioxygen complex of tris(pyrazolyl)borate-cobalt(II)
with NO in tetrahydrofuran or toluene solution.13 At
temperatures below −61 °C an intermediate was observed,
which may have been the desired peroxynitrito complex.
Eventually the nitrito and nitrato complexes were obtained in
this study.
Although Co-substituted hemoproteins and Co-porphyrin
models reversibly bind O2, to the best of our knowledge there
are not studies devoted to their potential ability to promote
nitric oxide dioxygenation (NOD) reaction. In this paper we
addressed this problem by application of the sublimed layers
methodology14 that is based on the preparation of the porous
layered solids by the vacuum sublimation of metal meso-
tetraarylporphyrinato complexes onto a substrate cooled by
liquid nitrogen (LN2). The facile reactions of these heme
models with volatile reactants can be studied in detail using
FTIR and optical spectroscopy. The power of this technique
draws from the ability to investigate such processes under
carefully controlled and tunable conditions, especially temper-
ature.
In this study, the reaction of nitric oxide (NO) with specially
constructed porous layered solids of the oxy-coboglobin models
(NH3)Co(Por)(O2) was monitored by FT-IR and UV−visible
spectroscopy from 80 K to room temperature. It was found for
the first time that the NOD reaction proceeds also with
coboglobin models. For this system, fortunately, the formation
of the six-coordinate nitrato complexes (L)Co(Por)(η1-ONO2)
proceeds at much higher temperatures (beginning at 180 K),
and at lower temperatures it was possible to detect the
intermediates that were characterized by FT-IR spectroscopy
with the use of experiments with isotopically labeled 18O2,
15NO and N18O species. These data are supported by the
predictions of DFT calculations that give support to the belief
that we were able to register the FTIR spectra of coordinated
peroxynitrite for the first time.
It should be mentioned here that as valuable as model
compounds Co-porphyrins are, they cannot be considered
equal with heme systems. For example, Co promotes/stabilizes
superoxo character of corresponding dioxygen adducts to a
much higher extent than Fe, Co(III) has a higher preference
toward six-coordination than Fe(III), Co(III) is more kineti-
cally inert than Fe(III), etc.10b All this can lead to different
mechanisms and characteristics of intermediate species along
reaction pathways. However, despite the observed intermedi-
ates being more related to the chemistry of cobalamins and
their interactions with nitrogen oxides species, the spectral
information obtained here will be very useful for analogous
studies performed with iron−porphyrins and related systems.
EXPERIMENTAL SECTION
■
Co(TPP) and Co(TTP) were synthesized using the literature
methods.15 Before the experiment they were additionally purified by
column chromatography with dry alumina using reagent grade
chloroform as the eluent. NO (15NO, N18O) was purified by passing
it through KOH pellets and a cold trap (dry ice/acetone) to remove
the higher nitrogen oxides and trace quantities of water. The purity
was checked by IR measurements of the layer obtained by slow
deposition of NO onto the cold substrate of the optical cryostat (77
K). The IR spectrum did not show the presence of N2O, N2O3 or
H2O. 15NO with 98.5% enrichment was purchased from the Institute
of Isotopes, Republic of Georgia, and was purified by the same
procedures. N18O was obtained by the reduction of N18O2 over
metallic Hg in an evacuated flask. N18O2 was synthesized according to
the following procedure. The 1:2 mixture of N2 and 18O2 gases
(Cambridge isotopic laboratories) was introduced into an evacuated
glass balloon provided with inserted electrodes. Upon continuous
electric discharge, the colorless gas mixture turned to reddish-brown,
indicating the formation of N18O2.
Sublimed layers of Co(TPP) (Co(TTP)) were obtained on the cold
(77 K) KBr support of an optical cryostat according to the published
procedure.14 Then about 0.3 Torr equivalent NH3 was added at LN2
and the layer was annealed at 120−130 K temperatures, at which the
formation of Co(Por)(NH3) was completed. A few tenths of a torr of
O2 was then introduced into the cryostat at LN2 and annealed to assist
the formation of desired mixed dioxygen complexes (NH3)Co(Por)-
(O2). Both of these processes can be controlled while monitoring by
FTIR spectroscopy according to the shifts of some of the porphyrin
bands. After obtaining the desired six-coordinate dioxygen complexes,
the cryostat was pumped out at maximally high temperatures until the
mixed complex was intact, then the layer was cooled by LN2 and small
increments (∼0.1 Torr equivalent) of NO were stepwise introduced
into the cryostat. The layer was then slowly warmed to room
temperature and the FTIR or UV−visible spectra were obtained at
various controlled temperatures measured by a thermocouple. The
UV−visible spectra were taken after the FTIR measurements of the
same samples confirmed the identity of each species. The FTIR and
UV−visible spectra were acquired on a Nexus (Thermo Nicolet
Corporation) in the spectral range 400−4000 cm−1 with a resolution 2
cm−1 and Specord M-40 (Carl Zeiss, Jena) or Helios γ (Thermo
Nicolet Corporation) spectrometers in the range of 350−900 nm,
respectively.
Computational analysis was carried out with Spartan '06 software
running under a Windows operating system. Equilibrium geometries
for the low-spin, ground state derivatives of (NH3)Co(P)(OONO) (P
= porphinato dianion) were first determined by DFT (BP/6-31G*)
methods and IR frequencies calculated from the resulting structures. In
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the case of the cis forms of (NH3)Co(P)(OONO) and (NH3)Co-
(TPP)(OONO), the OONO dihedral angle was locked at 0.0° in the
determination of the equilibrium geometry and IR spectrum. The
relative energies of the cis and trans isomers were determined from the
Spartan '06 thermodynamics program based upon geometries
determined by DFT methods and IR frequencies determined by
DFT methods for the (NH3)Co(P)(OONO) models. Likewise, DFT
methods were used with Spartan '10 for determining equilibrium
geometries, IR frequencies and thermodynamics parameters for the cis
and trans (OONO) isomers of (NH3)Co(TPP)(OONO).
coordinated O2 was still intact in vacuo. This procedure was
applied to eliminate the traces of O2 adsorbed in the layer.
Figure 1 demonstrates the spectral changes upon the reaction
of O2(18O2) with Co(TTP)(NH3). The intense ν(O2) band of
RESULTS AND DISCUSSION
■
Construction of Six-coordinate Oxy-coboglobin Mod-
els. To construct the six-coordinate dioxygen complexes of
porphyrins with trans ammonia ligand (NH3)Co(Por)(O2) the
strategy demonstrated in Scheme 1 was applied. In contrast to
Scheme 1
Figure 1. FTIR spectra in the range of ν(O2) stretching for Co(TTP)
(solid line), (NH3)Co(TTP)(O2) (dashed line) and (NH3)Co(TTP)-
(18O2) (dotted line) at 80 K.
iron−porphyrins, the first axial ligand binding constant K1 in
Co−porphyrins is much greater than that of the second ligand
K2.16 This allows for obtaining the five-coordinate complexes
by the reaction of small quantities of NH3 with amorphous
layers of Co-porphyrins.
As monitored by the vacuum gauge, low pressures of NH3
(∼0.3 Torr equivalent) were supplied into the cryostat at low
temperatures and the layers were allowed to be warmed until
certain temperatures, at which the formation of five-coordinate
complexes was completed. FTIR spectra served as a reliable
tool for monitoring this process, since some porphyrin bands
underwent noticeable shifts upon the Co(Por) + NH3 →
Co(Por)(NH3) transition.
The spectral changes observed upon the formation of
Co(Por)(NH3) complexes are reproduced in the Figure S1a,b
(Supporting Information). Intense porphyrin bands of Co-
(TPP) in the vicinity of 1000 cm−1 shift to lower frequencies
and change their relative intensities. The same occurs with the
single porphyrin band of Co(TTP) in this spectral range.
Notably, when six-coordinated dioxygen complexes (NH3)Co-
(Por)(O2) were formed upon exposition of this species under
O2 at low temperatures, these bands shifted back to their initial
positions. It is reasonable to suggest that these spectral changes
upon NH3 binding are connected with the out-of-plane motion
of the Co center in the five-coordinate complex, followed by a
shift back of the Co center into the plane of the porphyrin
when O2 binds. Such out-of-plane motion perturbs the
overlapping between metal dπ- and porphyrin eg*-orbitals
resulting in changes of energy of some porphyrin vibrations.
After formation of the five-coordinate ammonia complexes,
Co(Por)(NH3), a few tenths Torr of O2 (18O2) was supplied
into the cryostat at LN2 and the layer was allowed to warm
under O2 atmosphere to a certain temperature at which the
intensity of ν(O2) band, which characterizes the dioxygen
complex (NH3)Co(Por)(O2), reached maximum intensity. The
layer was then cooled to LN2 and the O2 excess was pumped
out. Spectrally controlled pumping was continued upon layer
warming until the temperature (∼120 K), at which the
coordinated dioxygen at 1141 cm−1 appeared in spectra and
shifts to 1073 cm−1 upon use of 18O2 in perfect agreement with
that expected for a perturbed diatomic molecule.
The same bands for (NH3)Co(TPP)(O2) appear at 1139
and 1072 cm−1 (Supporting Information, Figure S2). This
result indicates the formation of six-coordinate dioxygen
complexes, since the ν(O2) in the five-coordinate complex
with Co(TPP) appears at 1278 cm−1 in an Ar matrix17 and
1251 cm−1 in sublimed layers.18 The absence of the O2 band in
the 1250 cm−1 range also indicates that there are no unligated
Co-porphyrin molecules in the layer. The disposition of ν(O2)
in the six-coordinate mixed complexes are indicative for an end-
on bound superoxo ligand.19a Upon formation of the 5-
coordinate ammonia complexes Co(Por)(NH3) both Soret and
Q bands in the UV−visible spectra undergo red shifts and new
weak band emerges as a shoulder at about 590 nm (Supporting
Information, Figure S3, dashed). Further bathochromic shifts
are observed upon formation of the six-coordinate dioxygen
complexes with well separated two bands in the Q-band region
(Figure S3, dotted) that manifest the formation of six-
coordinate dioxygen complexes with the trans electron donor
ligand.19b
Reaction of NO with Six-coordinate Dioxygen
Complexes. FTIR Characterization of an Intermediate.
After constructing the six-coordinate dioxygen complexes,
(NH3)Co(Por)(O2), their low-temperature interaction with
NO was spectrally monitored upon slow warming of the layers.
The introduction of NO into the cryostat was carried out
stepwise by small increments (∼0.1 Torr) of preliminary
cooled NO, and new portions were introduced only after
spectral changes indicated the consumption of the previous
one.
It is necessary to note that the FTIR spectrum of Co(TTP)
is more convenient for the spectral study performed in this
investigation. Particularly, the band connected with the ring
stretching vibration of tolyl groups in the vicinity of 1600 cm−1
has a very low intensity and the interval between 700 and 800
cm−1 is relatively free of the bands compared to TPP-derivative.
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As will be shown below, both of these ranges give important
information about intermediates formed in the course of the
NO reaction with the six-coordinate dioxygen complexes. For
this reason, the spectral data are listed for Co(TTP) derivative
and those for Co(TPP) are represented in the Supporting
Information (Table S1).
and therefore should be assigned to the moiety containing both
these atoms. The position of this band lies in the range
characteristic for the double bond and the values of isotopical
shifts are close to the values predicted by DFT calculations for
ν(NO) of coordinated peroxynitrite within a few cm−1 (see
Table 1). In the peroxynitrite anion obtained by photolysis of
KNO3 in an Ar matrix, this mode is observed at 1444 cm−1 for
the cis isomer and at 1528 cm−1 for trans K(OONO).20 In the
IR spectrum of peroxynitrite anion as tetramethylammonium
salt this vibration is disposed presumably at 1496 cm−1 (nujol
mull).21 The uncertainty here is connected with the obscuring
by the bands of the tetramethylammonium cation. Noteworthy,
in the peroxynitrous acid, HOONO, this band is disposed at
1703 cm−1,22 so the covalent bonding of peroxynitrite’s
terminal oxygen increases the ν(NO) band by about 200
cm−1 as a result of the greater energy separation in the two
modes associated with the nitrogen−oxygen stretches. In our
system, this band occupies an intermediate position between
those of peroxynitrite anion and peroxynitrous acid, the
behavior that should actually be anticipated upon coordination
with transition metal, in which the bonding exhibits partially
ionic character. It is noteworthy that the value of 1621 cm−1
was reported by Koppenol and coauthors for the frequency of
this mode in the sodium pentacyanoperoxynitritocobaltate(III)
Na3[Co(CN)5(OONO)].12
The spectral changes observed upon the reaction of NO with
layered (NH3)Co(TTP)(O2) are demonstrated in Figure 2.
Figure 2. FTIR spectral changes accompanying the reaction of small
NO increments with the layered (NH3)Co(TTP)(O2) upon its
warming from 80 to 120 K.
The band in the 950 cm−1 region is sensitive to the oxygen
labeling in the dioxygen moiety (Table 1) and upon 18O
substitution it undergoes more than 30 cm−1 low-frequency
shift. Upon 15N substitution this band was shifted by only 8
cm−1, indicating relatively little involvement of the N atom in
this mode (Figure 3). Disposition of this band is typical for
peroxo compounds and the magnitudes of the isotopic shifts
indicate that this band involves O−O stretching to a great
extent. Analogous vibrational modes were observed at 952, 932,
and 915 cm−1 in the K(OONO),20 N(CH3)4(OONO)21 and
Na3[Co(CN)5(OONO)],12 respectively. For peroxynitrous
acid in an Ar matrix this vibration was found at 952 and 957
cm−1 in different matrix sites and reveals 4−5 cm−1 downshifts
in the 15N-containing species.22a The 5 cm−1 downshift of this
band was also observed for N(CH3)4(OO15NO)21 relative to
the natural abundance compound. The same pattern is
observed in our case. The analysis above provides reason
The band of coordinated dioxygen at 1141 cm−1 decreases in
intensity and a set of new bands grow with correlating
intensities in the vicinity of 1600, 950, 740, and 540 cm−1 that
belong to an intermediate that is fairly stable until 140 K, but
after further warming begins to decompose.
The aforementioned bands had their analogs when 18O2,
15NO and N18O isotopomers were used in the experiments.
These data are summarized in Table 1 together with calculated
values of stretching frequencies assuming formation of the O-
coordinated peroxynitrite as a most plausible scenario for the
interaction of NO with (NH3)Co(Por)(O2) at very low
temperatures. In calculations that were performed for all
isotopic species, the relative values were given more credence
than the absolute frequencies. The new bands in aforemen-
tioned spectral ranges were assigned as follows.
The high frequency band in the vicinity of 1600 cm−1 is
sensitive to both isotopomers of nitrogen oxide (15NO, N18O)
Table 1. Infrared Frequencies and Their Assignment for the Co-OONO Group of the Intermediate Proposed to be
a
(NH3)Co(TTP)(OONO)
νs(O−O−N), δ(O−NO), νa(O−O−N), δ(O−NO),
[Δν] = ν − νisotope [Δν] = ν − νisotope
ν (Co−O), [Δν] = ν −
νisotope
ν (NO), [Δν] = ν − νisotope
exp. comp.
1596 1678
adduct
exp. comp. exp. comp.
954 967 740
exp.
544
comp.
560
(NH3)Co(TTP)(OONO)
711
(NH3)Co(TTP)(18O18ONO)
(NH3)Co(TTP)(OO15NO)
(NH3)Co(TTP)(18O18O15NO)
(NH3)Co(TTP)(18O18ON18O)
cis-(NH3)Co(P)(OONO)
1594 [2]
1677 [1]
1647 [31]
1646 [32]
1635 [42]
1702
924 [30]
946 [8]
930 [37]
960 [7]
922 [45]
925 [42]
910
∼710 [30]
737 [3]
686 [25]
708 [3]
683 [27]
681 [30]
796
522 [22]
542 [2]
536 [24]
559 [1]
536 [24]
536 [24]
575
1564 [32]
1564 [32]
1555 [41]
914 [40]
916 [38]
∼710 [30]
∼707 [33]
523 [21]
522 [22]
trans-(NH3)Co(TPP)(OONO)
cis-(NH3)Co(TPP)(OONO)
1665
967
704
565
1673
798
573
a
Calculations are performed for the (NH3)Co(P)(OONO), (P = porphynato dianion) that has an equilibrium geometry with the OONO ligand in
the trans orientation (dihedral angle = 174.44°), except where noted for this cis OONO isomer in which the dihedral angle was fixed at 0.0°.
Calculations were also performed for (NH3)Co(TPP)(OONO) for both the cis and trans isomers. For the cis isomer the dihedral angle was fixed at
0.0°, and for the trans isomer it was calculated as 175.48°.
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isotopically sensitive band at frequencies close to those
mentioned above together with DFT predictions gives the
basis to suggest that addition of NO to coordinated O2 leading
to the formation of single O−O peroxo bond intensifies the
Co−O vibration allowing its observation in the FTIR spectra.
In the spectral range of this study (400−4000 cm−1), we did
not observe any isotopically sensitive bands that could be
assigned to the uncoupled ν(N−O) of coordinated peroxyni-
trite. According to DFT calculations, this vibration should lay at
436 cm−1. Taking that into account and also the fact that most
of the calculated frequencies were increased compared with the
experimentally observed ones, it is likely that it may be disposed
near the spectral limit of our measurement. This low value
indicates that the bond between NO and O−O groups is
rather weak. Such weak bonding was also predicted for
peroxynitrous acid, for which, according to the ab initio
calculation at the RMP2/6-31G* level, the ν(N−O) stretching
is disposed at 439 cm−1,24 which was out of the spectral range
of measurements performed by Lee and coauthors.22
Dioxygen binding with Co-porphyrins is weak and O2
releasing could not be completely excluded. This may lead to
NO autoxidation that in turn should result in formation of
different NxOy species. Therefore the thorough literature
analysis of the IR spectra of such compounds has been
performed. Due to low temperature conditions of this
experiment special attention was attracted to the thermally
unstable adducts that were mainly studied by matrix isolation
spectroscopy. This analysis shows that the set of bands
observed in this work for the intermediate does not match to
the spectra of any NxOy species, IR spectra of which are
described in literature.24,25 We believe, therefore, that the
intermediate formed at the initial stage of the reaction between
NO and (NH3)Co(Por)(O2) is the six-coordinate peroxynitrite
complex (NH3)Co(Por)(OONO) as is demonstrated on the
Scheme 2.
Figure 3. FTIR spectra in the range of predominantly ν(O−O)
vibrations of intermediate proposed to be (NH3)Co(TTP)(OONO)
species for the experiments with O2/NO (solid), O2/15NO (dotted),
18O2/N18O (dashed).
enough to assign the 954 cm−1 band to preferentially O−O
stretching of O−O−NO group.
DFT computations were used to determine frequencies of
the O−O−NO ligand with isotopic substitution. The
equilibrium geometries of the ligand were first determined for
the porphine model system as (NH3)Co(P)(OONO). In this
case, the cis isomer was 12 kJ/mol more stable than the trans
isomer at 77 K. With the actual (NH3)Co(TPP)(OONO),
steric factors played an important role in the ligand geometry
since the cis isomer was found to be 56 kJ/mol less stable than
the trans isomer. Further computations to determine the
relative isotopic shifts were carried out using the simpler
porphine model system. These computational studies show that
O−O stretching band just mentioned could better be described
as a symmetrical O−O−N stretch mixed with the O−NO
bending mode.
In the spectra of Co(TTP) derivatives, a band appears at
about 740 cm−1, the growth of which correlates with intensities
of the aforementioned bands and is similar to the band at about
950 cm−1 revealing weak and strong sensitivity to 15NO- and
18O2-labeling isotopomers, respectively. For the Co(TPP)
complexes, this band is masked by the intense TPP bands
and can be registered only in difference spectra. DFT
calculations predict that in this spectral range the asymmetric
O−O−N stretch mixed with O−NO bending mode should
be disposed. Experimental observations are in accordance with
this prediction.
The next band in the set of bands that grow with correlating
intensities upon consumption of dioxygen in the six-coordinate
complexes (NH3)Co(Por)(O2) is disposed in the low-
frequency range in the vicinity of 540 cm−1. It displays
noticeable sensitivity to 18O2 substitution and is almost
insensitive to 15N labeling (Table 1). Computations predict
the existence of the Co−O stretching mode in this spectral
region. For characterization of the metal−oxygen bond in the
oxy-globins and related model compounds the IR spectroscopy
is rarely used most likely because of the low intensity of the
corresponding bands. In this study we also were not able to
detect in the FTIR spectra the ν (Co−O2) band in
(NH3)Co(Por)(O2) complexes. In contrast the Resonance
Raman spectroscopy gives valuable information about
vibrations of metal−oxygen moiety.23 It reveals the band of
ν(Co−O2) at 527 cm−1 for the Co(II)(TpivPP)(1,2-Me2Im)-
(O2), 516 cm−1 for the Co(II)(TpivPP)(N-MeIm)(O2) and
540 cm−1 for oxy meso CoMb. The observation of an
Scheme 2
Its equilibrium geometry determined by DFT (BP/6-31G*)
is shown in Figure S7 (Supporting Information) and has a trans
OONO dihedral angle of 174.44°. It is necessary to stress that
formation of a peroxynitritometal complex via the reaction of a
dioxygenmetal ion with nitrogen monoxide is in most cases
inferred and not directly observed.11
For completeness, it should be added here that according to
the indirect experimental evidence and computational work the
peroxynitrite can be not only O-bound,but also be N-
coordinated11b−h or an O,O′ chelating11i,j ligand. For ruling
out these possibilities, the following experimental and
computational works were carried out. By sequential reactions
of NO and NH3 vapors on the sublimed layers of Co-
porphyrins, the thermally unstable six-coordinate complexes
(NH3)Co(Por)(NO) were obtained.19c Introduction into the
cryostat a few tenths of a torr of O2 at 80 K and slow warming
of the substrate to 120 K did not lead to the appearance of new
bands in the FTIR spectra manifesting that no intermediate is
formed. Hence the hypothesis of an N-coordinated peroxyni-
trite should be ruled out, at least in our experimental
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conditions. On the other hand, the DFT calculations for the
chelating peroxynitrite gives a set of IR bands completely
different from those observed in our study. Particularly, for such
a mode of binding, the nitrosyl ν(NO) is predicted to be
disposed at about 1300 cm−1 which is incompatible with the
experimental observations.
Scheme 3
Decomposition of the Peroxynitrite Intermediate.
After the bands of intermediate reach their maxima and all
coordinated dioxygen in (NH3)Co(Por)(O2) is spent the
cryostat was pumped out at temperatures (about 150 K), at
which the intermediate still intact. This allows pumping out the
unreacted NO and some part of the NH3 excess. Upon further
warming of the layer to 170 K the bands at 953, 740, and 540
cm−1 disappear. During this process the band in the vicinity of
1600 cm−1 undergoes a small high frequency shift but only
slightly decreases in intensity. Simultaneously, a weak band
grows at about 775 cm−1 as a low-frequency shoulder of the
intense porphyrin band at about 800 cm−1 and is seen more
clearly in the 15N-labeled experiments (Figure 4a,b).
not find an isotopically sensitive band in this spectral range. It
probably has a very low intensity and is obscured by the bands
of porphyrin itself. What can be reliably confirmed for this stage
of reaction is the breaking of the O−O peroxide bond that is
weak and readily undergoes homolysis for cobalt alkylper-
oxides.27
It is worth noting that the decomposition of the intermediate
assigned to coordinated peroxynitrite does not lead to
immediate formation of six-coordinate nitrato complexes (see
below) but proceeds through the formation of the second
intermediate with disrupted peroxide bond, that supports the
idea about the formation of the caged (NH3)(Por)Co−
O•/•NO2 pair.
Formation of the Six-coordinate Nitrato Complexes
(NH3)Co(Por)(η1-ONO2). Further slow warming of the layer
from 180 to 210 K leads to the gradual disappearance of the
species characterized by the bands at about 1600 and 778 cm−1
(1565 and 769 cm−1 in the experiments with 15NO), with
concomitant growth of three new bands in the vicinity of 1485,
1270, and 985 cm−1 (Figure 5a,b). These bands have their
Figure 4. FTIR spectra demonstrating decomposition of peroxynitrite
intermediate upon warming the layers of (a) (NH3)Co(TTP)-
(OONO) and (b) (NH3)Co(TTP)(OO15NO) from 150 to 170 K.
These bands with the isotopic counterparts in the experi-
ments with 15N- and 18O-labeled compounds most likely
belong to the νa(NO2) and δ(ONO) of nitrogen dioxide NO2
monomer. The frequency of the first band is somewhat lower,
and the frequency of the second one is somewhat higher than
reported for the NO2 monomer in the matrices.25a We think
that these deviations are connected with the H-bonding of
nitrogen dioxide with coordinated or free NH3 that is still
present in the layer. As a general rule, hydrogen bonding lowers
the frequency of stretching vibrations, since it lowers the
restoring force, but increases the frequency of bending
vibrations since it produces additional restoring force.26 It
should be added that the frequency of the nitrogen dioxide
monomer reveal considerable dependence on the environment.
The νa(NO2), for example, appears at 1611 cm−1 in Ar and at
1624 cm−1 in a carbon dioxide matrix.
Figure 5. FTIR spectral changes upon warming of (a) (NH3)Co-
(TTP)(O2)+NO and (b) (NH3)Co(TTP)(O2)+15NO systems from
180 to 210 K.
isotopic counterparts at about 1450, 1245, and 970 cm−1 when
15NO was used in the experiments. The frequencies of the new
species formed in the 180−210 K temperature interval in the
experiments with the natural abundance O2 and NO and
different 18O- and 15N-containing isotopomers with their
various combinations are summarized in Table 2. The spectra
of three such systems are demonstrated in Figure 6.
The results obtained can be interpreted in terms of
homolytic disruption of O−O bond, that should lead to the
formation of NO2 and Co oxo species (NH3)(Por)CoO ↔
(NH3)(Por)Co−O• as is shown on the Scheme 3. According to
DFT calculations the ν(CoO) vibration should appear at 691
cm−1 and at 660 cm−1 for 18O-labeled analog. However, we did
The positions of these bands, their relative intensities and
isotopic shifts are close to those observed in the six-coordinate
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Table 2. Infrared Frequencies (cm−1) of Nitrato Group in the Six-coordinate Nitrato Complexes of Co- and Fe-TPP (Data in
Parentheses Are Given for TTP Derivatives)
compounds
νa(NO2) (m)
νs(NO2) (s)
ν(O−N) (w)
ref.
(NH3)Co(TPP) (η1-ONO2)
(NH3)Co(TPP) (η1-O15NO2)
(NH3)Co(TPP) (η1-18ON18O2)
(NH3)Co(TPP) (η1-18ON(18O)O)
(NH3)Co(TPP) (η1-18O15N(18O)O)
(NH3)Fe(TPP) (η1-ONO2)
(NH3)Fe(TPP) (η1- 18ON(18O)O)
(NH3)Fe(TPP) (η1-O15NO2)
(NO)Fe(TPP) (η1-ONO2)
1484 (1485)
1459 (1460)
1456 (1460)
1465 (1470)
1437 (1438)
1499 (1496)
1481 (1482)
1472 (1469)
1505
1270 (1269)
1248 (1247)
1244 (1243)
1252 (1254)
1228 (1229)
1268 (1268)
1252 (1253)
1249 (1249)
1265
∼983 (983)
∼970 (970)
942 (935)
953 (955)
946 (946)
938 (936)
913 (914)
925 (925)
969
this work
this work
this work
this work
this work
9
9
9
28a
(NO)Fe(TPP) (η1-O15NO2)
(THF)Fe(TPP) (η1-ONO2)
(THF)Fe(TPP) (η1-O15NO2)
1472
1246
954
28a
1491 (1486)
1457 (1454)
1280 (1277)
1258 (1258)
∼997 (∼995)
986 (984)
28b
28b
form,32 while in Mn(TPP)(η1-ONO2) monodentate coordina-
tion is realized.33 Vibrational spectroscopy can be useful for
differentiation of these modes of binding in nitrato complexes
of transition metals. In the bidentate form, two high frequency
stretching bands {ν(NO) and νa(NO2)} of comparable
intensities are more separated than νa(NO2) and νs(NO2)
vibrations upon monodentate coordination.34
This pattern is also operational in the nitrato complexes of
metalloporphyrins. It has been shown that coordination of the
sixth ligand to Fe(TPP)(η2-O2NO) forming the thermally
unstable six-coordinate complexes (L)Fe(TPP)(η1-ONO2) (L
= NO, THF)28a,b is accompanied with bidentate−monodentate
isomerization. This process leads to the low frequency shift of
the high frequency band at about 1530 cm−1 for 30−40 cm−1
and noticeable decreasing in its intensity, while the second high
frequency band in the vicinity of 1270 cm−1 increases in
intensity with very slight frequency shifting.
As mentioned above, the six-coordinate nitrato complexes of
metalloporphyrins with biologically important Fe, Co and Mn
metals are not stable at ambient conditions and were spectrally
characterized only for the iron−porphyrins at low temper-
atures.9,28,35 In the complexes obtained by low-temperature
interaction of electron donor ligands with the Fe(TPP)(η2-
O2NO), the following bands were reported for the nitrato
group in (L)Fe(TPP)(η1-ONO2): 1505 m, 1266 s and 978 w
and 1490 m, 1278 s and ∼997 w cm−1 for the NO28a and
THF28b trans ligands correspondingly. These data together with
that of the six-coordinate nitrato complexes of iron-porphyrins
with trans ammonia ligand (NH3)Fe(Por)(η2-O2NO) obtained
by the NOD-reaction9 show the bands of coordinated nitrate
lie in the same spectral range with the same relative intensities
and closely related values of isotopical shifts (see Table 2) as
was observed in this work for the Co-derivatives. Additional
evidence for the formation of six-coordinate nitrato complexes
with the trans ammonia ligand (NH3)Co(TPP)(η1-ONO2) is
the presence in spectra of the stretching bands of coordinated
NH3 in the high frequency range 3450−3250 cm−1 that is free
of other spectral features. They undergo low-frequency shifts
from the values of νa(NH3) and νs(NH3) of free NH3 (Figure
S5, Supporting Information) as usually occurs upon ammonia
coordination.34 In the 1270 cm−1 spectral range a band appears
(Figure 6) as a high frequency shoulder of the intense νs(NO2)
band in the spectra of natural abundance nitrato complex, but is
well separated in the spectra of isotopical species (Figure 6,
dashed and dotted lines). This band represents the deformation
δs(NH3) mode of coordinated ammonia34 and was seen also in
Figure 6. FTIR spectra of 3 different (NH3)Co(TTP)(O2) + NO
systems after warming to 210 K and high vacuum pumping:
(NH3)Co(TTP)(O2) + NO (solid line), (NH3)Co(TTP)(O2) +
15NO (dashed line), (NH3)Co(TTP)(18O2) + 15NO (dotted line).
nitrato complexes of iron-porphyrins with trans electron-donor
ligands9,28 and can be unambiguously assigned to the six-
coordinate nitrato complexes (NH3)Co(Por)(η1−ONO2) (see
discussion below). In these compounds the nitrate group is
coordinated through the one of oxygen atoms in monodentate
fashion. The three IR-active stretching modes expected for this
structure would be a low-frequency ν(O−N) band for the
coordinated oxygen and two(symmetric and asymmetric)
modes for the uncoordinated NO2 fragment. Therefore, the
bands in the vicinity of 1485, 1270, and 985 cm−1 should be
assigned to the vibrations that predominantly belong to
νa(NO2), νs(NO2) and ν(O−N) stretching of coordinated
nitrato group.
The stable nitrato complexes of metalloporphyrins charac-
terized until now are the complexes where the nitrate is a sole
axial ligand.29 In mononuclear complexes, the nitrate ligand can
be bound with metal by one or two oxygen atoms forming
mono- or bidentate complexes. In metalloporphyrins the mode
of coordination depends both on the nature of metal and
porphyrin substituents. For example, in Fe(TPP)(η2-O2NO)
the symmetric bidentate coordination is realized,30 while in
Fe(OEP)(η1-ONO2) coordination occurs in monodentate
fashion.31 In Co(OEP′)(η2-O2NO) (OEP′-modified octaethyl-
porhyrinato ligand) the nitrate is bound in symmetric bidentate
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the spectra of Fe-derivatives.9 The electronic absorption spectra
of Co-porphyrins also undergo noticeable changes upon
formation of both the six-coordinate dioxygen and nitrato
complexes as can be seen in Figure 7.
cm−1. This band has its isotopic analogs in the experiments with
15N (Figure 9) and 18O containing species and unambiguously
Figure 7. UV−visible spectra of thin layers containing Co(TTP) (solid
line) (NH3)Co(TTP)(O2) (dashed line) and (NH3)Co(TTP)(η1-
ONO2) (dotted line). The spectra were taken after FTIR measure-
ments of the same samples confirming the identity of each species.
Figure 9. FTIR spectra of the products of NOD reaction at room
−
temperature CoIII(TTP)(NH3)1,2•NO3 (solid line), CoIII(TTP)-
(NH3)1,2•15NO3 (dashed line).
The Soret band of Co(TTP) at 409 nm undergoes a red shift
to 434 and 439 nm upon formation of (NH3)Co(TTP)(O2)
and (NH3)Co(TTP)(η1-ONO2) indicating an increasing metal
oxidation state. In its turn the single band of Co(TTP) at 535
nm splits into two components disposing at 558 and 597 nm
for (NH3)Co(TTP)(O2) and 556 and 596 nm for (NH3)Co-
(TTP)(η1-ONO2). Absorption spectra of nitrato-complexes
obtained in this paper are very close to those available in
literature for tervalent cobalt complexes of porphyrins.36
The discussion above clearly indicates that Co-porphyrins
similar to heme-analogues also promote the NOD-reaction but
at much higher temperatures, allowing the observation of
transient species formed in the course of this biologically
important transformation.
Further Transformations of Six-coordinate Nitrato
Complexes upon Warming. The six-coordinate nitrato-
complexes (NH3)Co(Por)(η1-ONO2) are not thermally stable
and decompose after warming the systems to room temper-
ature. Spectral changes accompanying this process are
demonstrated in the Figure 8. The bands of coordinated
nitrato group disappear and new broad band overlapping with
the porphyrin band at 1350 cm−1 grows in the vicinity of 1370
should be assigned to the degenerate asymmetric stretching
mode ν3 of the nitrate anion.34 Sustaining this interpretation a
weak isotopically sensitive band also grows in the vicinity of
830 cm−1 where the out-of-plane deformation mode ν2 of NO3¯
anion is disposed.34
The doubly degenerate in the bare ion ν3 band is not a single
band but has complex shape that is certainly connected with the
H-bonding of NO3¯ with NH3 (coordinated or solvated) that
lowers the D3 h symmetry of nitrate-anion and removes the
degeneracy of ν3 mode. Such splitting was described in the
literature for the NO3¯/H2O system. Depending on the
quantity of the H2O molecule per an NO3¯ ion and the
symmetry of H-bonding, the different characteristics of ν3
splitting into two components was observed with separation
of the bands as much as 43 cm−1 in some cases.37 Obviously the
same pattern should be observed for the NO3¯/NH3 system.
The results obtained clearly indicate that six-coordinate
nitrato-complexes of Co-porphyrins decompose at room
temperature to nitrate-anion and amino-complexes of Co-
(III)-porphyrins. In contrast to the Co(II) species the six-
coordinate amino-complexes of Co(III)-porphyrins much more
stable36 and there is uncertainty in our experiments if the
cationic complex formed is mono- or bis-ligated {Co(III)-
(Por)(NH3) or Co(III)(Por)(NH3)2}. The NH3 stretching
vibrations in the 3250−3450 cm−1 range are disposed at higher
wavenumbers for uncoordinated NH3 compared to those of
coordinated ammonia and the spectral features indicate that
there is some quantity of uncoordinated NH3 in the layer in the
course of decomposition of nitrato-complexes. Since UV−
visible spectra undergo very minor changes upon transition
from six-coordinate nitrato complexes to ammonia complexes
of Co(III)-porphyrins (Figure S6, Supporting Information), we
think that the coordination number of Co(III)-ion did not
change and so favor the formation of six-coordinate ammonia
complex (Scheme 4). The species eventually formed in the
course of NOD reaction is fairly stable and high-vacuum
pumping upon warming the system to 350 K does not reveal
noticeable spectral changes. The result obtained in this work is
similar to that for heme-containing globins4 and modeling iron-
porphyrin systems,9 in which the NOD-reaction results in the
formation of nitrate anion and oxidized hemes.
Figure 8. FTIR spectra demonstrating decomposition of six-
coordinate nitrato complex (NH3)Co(TTP)(η1-ONO2) with elimi-
−
nation of NO3 upon warming the layered solid from 210 K to RT.
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Scheme 4
AUTHOR INFORMATION
■
Corresponding Author
kurto@netsys.am
Present Address
‡Molecule Structure Research Centre (MSRC) of the Scientific
and Technological Centre of Organic and Pharmaceutical
Chemistry NAS, 0014, Yerevan, Armenia.
Notes
The authors declare no competing financial interest.
CONCLUSIONS
■
As shown by FTIR and UV−visible spectroscopy NO reacts
with layered oxy-coboglobin model compounds, (NH3)Co-
(Por)(O2), at low temperatures giving the six-coordinate
nitrato complexes (NH3)Co(Por)(η1-ONO2) thereby demon-
strating the ability of these systems to promote nitric oxide
dioxygenation (NOD) reaction. In contrast to the iron
porphyrin analog (NH3)Fe(Por)(O2), in which NOD-reaction
proceeds at temperatures lower than 100 K without spectral
observation of intermediates,9 the formation of nitrato
complexes by Co-derivatives occurs at much higher temper-
ature (180 K) giving the opportunity to follow the sequence of
reactions at lower temperatures. The first transient formed at
very low temperatures (80−120 K) and characterized by FTIR
spectroscopy is believed to be the putative six-coordinate
peroxynitrite complex (NH3)Co(Por)(η1-OONO). This con-
clusion was made based on the experiments with labeled 15NO,
N18O and 18O2 species and predictions provided by DFT
computations. In the temperature interval 140−170 K this
intermediate decomposes and there is spectral evidence of NO2
formation. This should be interpreted as homolytic O−O bond
cleavage and formation of a caged radical pair (NH3)Co(Por)-
ACKNOWLEDGMENTS
■
This work was supported by the State Committee of Science
RA (Grant #11-1d052) and Armenian National Science and
Education Fund (ANSEF) based in New York (Project PS-
Cheminorg −2520).
REFERENCES
■
(1) (a) Ignarro, L. Nitric Oxide: Biology and Pathobiology; Academic
Press, San Diego, 2000. (b) Tonzetich, Z. J.; McQuade, L. E.; Lippard,
S. J. Inorg. Chem. 2010, 49, 6338−6348.
(2) Ford, P. C.; Lorkovic, I. M. Chem. Rev. 2002, 102, 993−1017.
(3) (a) Groves, J. T. Curr. Opin. Chem. Biol. 1999, 3, 226−235.
(b) Pacher, P.; Beckman, J. S.; Liaudet, L. Physiol. Rev. 2007, 87, 315−
324. (c) Nathan, C.; Shiloh, M. U. Proc. Natl. Acad. Sci. U.S.A. 2000,
97, 8841−8848. (d) Gardner, P. R.; Martin, L. A.; Hall, D.; Gardner,
A. M. Free Radical Biol. Med. 2001, 31, 191−204.
(4) (a) Su, J.; Groves, J. T. Inorg. Chem. 2010, 49, 6317−6329.
(b) Schopfer, M. P.; Wang, J.; Karlin, K. D. Inorg. Chem. 2010, 49,
6267−6282. (c) Su, J.; Groves, J. T. J. Am. Chem. Soc. 2009, 131,
12979−12988. (d) Lee, J. B.; Hunt, J. A.; Groves, J. T. J. Am. Chem.
̂
Soc. 1998, 120, 7493−7501. (e) Moenne-Loccoz, P. Nat. Prod. Rep.
•
O• and NO2. Beginning at 180 K three new bands in the
2007, 24, 610−620. (f) Hino, T.; Matsumoto, Y.; Nagano, S.;
Sugimoto, H.; Fukumori, Y.; Murata, T.; Iwata, S.; Shiro, Y. Science
2010, 330, 1666−1670.
vicinity of 1480, 1270, and 980 cm−1 grow manifesting
formation of the six-coordinate nitrato complexes. These
complexes are not stable at room temperature and eliminate
nitrate anion to form cationic Co(III)-porphyrin complexes
ligated by ammonia.
(5) (a) Herold, S. FEBS Lett. 1998, 439, 85−88. (b) Herold, S.;
Exner, M.; Nauser, T. Biochemistry 2001, 40, 3385−3395.
(6) Olson, J. S.; Folley, E. W.; Rogge, C.; Tsai, A.-L.; Dohle, M. L.;
Lemon, D. D. Free Radical Biol. Med. 2004, 36, 685−697.
(7) Goldstein, S.; Merenyi, G.; Samuni, A. J. Am. Chem. Soc. 2004,
126, 15694−15701.
The overall NOD-reaction with oxy-cobalt models mimics
the reaction promoted by hemes and the results of this study
favor the mechanism of this transformation offered by
numerous researchers4 but never unambiguously demonstrated
by direct experimental observations.
(8) Yukl, E. T; de Vries, S.; Moenne-Loccoz, P. J. Am. Chem. Soc.
2009, 131, 7234−7235.
(9) Kurtikyan, T. S.; Ford, P. C. Chem. Commun. 2010, 46, 8570−
8572.
(10) (a) Hayashi, T. In Porphyrin Handbook; Kadish, K. M., Smith, K.
M., Guilard, R., Eds; World Publishing Company: Singapour, 2010;
Vol. 5, Ch. 23, 2−70. (b) Bioinorganic Chemistry: A Short Course; Roat-
Malone, R. M., Ed.; John Wiley & Sons Inc.: New York, 2007; p 501.
(c) Collman, J. P.; Berg, K. E.; Sunderland, C. J.; Aukauloo, A.; Vance,
M. A.; Solomon, E. I. Inorg. Chem. 2002, 41, 6583−6596.
(11) (a) Herold, S; Koppenol, W. H. Coord. Chem. Rev. 2005, 249,
499−506. (b) Clarkson, S. G.; Basolo, F. Inorg. Chem. 1973, 12, 1528−
1534. (c) Videla, M.; Roncaroli, F.; Slep, L. D.; Olabe, J. A. J. Am.
Chem. Soc. 2007, 129, 278−279. (d) Roncaroli, F.; Videla, M.; Slep, L.
D.; Olabe, J. A. Coord. Chem. Rev. 2007, 251, 1903−1930. (e) Frech,
C. M.; Blacque, O.; Schmalle, H. W.; Berke, H. Dalton Trans. 2006,
4590−4598. (f) Goodwin, J. A.; Coor, J. L.; Kavanagh, D. F.; Sabbagh,
M.; Howard, J. W.; Adamec, J. R.; Parmley, D. J.; Tarsis, E. M.;
Kurtikyan, T. S.; Hovhannisyan, A. A.; Desrochers, P. J.; Standard, J.
M. Inorg. Chem. 2008, 47, 7852−7862. (g) Goodwin, J. A.; Kurtikyan,
T. S. J. Porph. Phthaloc. 2011, 15, 99−105. (h) Silaghi-Dumitrescu, R.
J. Mol. Struct.: Theochem. 2005, 722, 233−237. (i) Park, G. Y.;
Deepalatha, S.; Puiu, S. C.; Lee, D.-H.; Mondal, B.; Sarjeant, A. A. N.;
del Rio, D.; Pau, M. Y. M.; Solomon, E. I.; Karlin, K. D. J. Biol. Inorg.
Chem. 2009, 14, 1301−1311. (j) Maiti, D.; Lee, D. H.; Sarjeant, A. A.
ASSOCIATED CONTENT
■
S
* Supporting Information
Figure S1. FTIR spectral changes accompanying the formation
of (NH3)Co(Por). Figure S2. FTIR spectra of Co(TPP),
(NH3)Co(TPP)(O2) and (NH3)Co(TPP)(18O2) in the range
of ν(O2) vibration. Figure S3. UV−visible spectra of layered
Co(TPP), Co(TPP)(NH3) and (NH3)Co(TPP)(O2). Figure
S4. UV−visible spectra of layered Co(TPP) and (NH3)Co-
(TPP)(OONO) and (NH3)Co(TPP)(ONO2). Figure S5.
FTIR spectra of (NH3)Co(TTP)(η1-ONO2) in the range of
NH3 stretching vibrations. Figure S6. Visible spectra of
(NH3)Co(TTP)(η1-ONO2) and Co(III)(TTP)(NH3)2·NO3 .
−
Figure S7. Equilibrium geometry of the trans-(NH3)Co(TPP)-
(OONO) derivative as obtained from DFT (BP/6-31G*)
optimization. Table S1. Infrared frequencies and their assign-
ment for the Co-OONO group of the intermediate supposed to
be (NH3)Co(TPP)(OONO). This material is available free of
charge via the Internet at http://pubs.acs.org.
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N; Pau, M. Y. M.; Solomon, E. I.; Gaoutchenova, K.; Sandermeyer, J.;
Karlin, K. D. J. Am. Chem. Soc. 2008, 130, 6700−6701.
(12) Wick, P. K.; Kissner, R.; Koppenol, W. H. Helv. Chim. Acta
2000, 83, 748−754.
(η2-O2NO)29 and it seems likely that the species formed is Co(TPP)
(η2-O2NO). (b) Tovrog, B. J.; Diamond, S. E.; Mares, F.; Szalkiewicz,
A. J. Am. Chem. Soc. 1981, 103, 3522−3526.
(36) (a) Scheidt, W. R.; Cunningham, J. A.; Hoard, L. G. J. Am.
Chem. Soc. 1973, 95, 8289−8294. (b) Sugimoto, H.; Ueda, N.; Mori,
M. Bull. Chem. Soc. Jpn. 1981, 54, 3425−3432.
(37) Goebbert, D. J.; Garand, E.; Wende, T.; Bergman, R.; Meijer,
G.; Asmis, K. R.; Neumark, D. M. J. Phys. Chem. A 2009, 113, 7584−
7592.
(13) Thyagarajan, S.; Incarvito, C. D.; Rheingold, A. L.; Theopold, K.
H. Inorg. Chim. Acta 2003, 345, 333−339.
(14) (a) Kurtikyan, T. S.; Gasparyan, A. V.; Martirosyan, G. G.;
Zhamkochyan, G. A. J. Appl. Spectrosc. 1995, 62, 62−65. (b) Kurtikyan,
T. S.; Ford, P. C. Coord. Chem. Rev. 2008, 252, 1486−1496.
(15) (a) Epstein, L. M.; Straub, D. K.; Maricondi, C. Inorg. Chem.
1967, 6, 1720−1722. (b) Bhatti, W.; Bhatti, M.; Imbler, P.; Lee, A.;
Lorenzen, B. J. Pharm. Sci. 1972, 61, 307−309.
(16) (a) Walker, F. A. J. Am. Chem. Soc. 1973, 95, 1150−1153.
(b) Walker, F. A. J. Am. Chem. Soc. 1973, 95, 1154−1159.
(17) Kozuka, M.; Nakamoto, K. J. Am. Chem. Soc. 1981, 103, 2162−
2168.
(18) Kurtikyan, T. S.; Martirosyan, G. G.; Akopyan, M. E. Kinetics
Catal. 2001, 42, 281−288.
(19) (a) Collman, J. P.; Berg, K. E.; Sunderland, C. J.; Aukauloo, A.;
Vance, M. A.; Solomon, E. I. Inorg. Chem. 2002, 41, 6583−6596.
(b) Kurtikyan, T. S.; Martirosyan, G. G.; Gasparyan, A. V.; Akopyan,
M. E.; Zhamkochyan, G. A. J. Appl. Spectrosc. 1990, 53, 728−734.
(c) Kurtikyan, T. S.; Markaryan, E. R.; Mardyukov, A. N; Goodwin, J.
A. Inorg. Chem. 2007, 46, 1526−1528.
(20) Lo, W.-J.; Lee, Y.-P.; Tsai, J. H. M.; Hamilton, T. P.; Harrison, J.
G.; Beckman, J. S. J. Chem. Phys. 1995, 103, 4026−4034.
(21) Bohle, D. S.; Hansert, B.; Paulson, S. C.; Smith, B. D. J. Am.
Chem. Soc. 1994, 116, 7423−7424.
(22) (a) Cheng, B.-M.; Lee, J.-W.; Lee, Y.-P. J. Phys. Chem. 1991, 95,
2814−2817. (b) Lo, W.-J.; Lee, Y.-P. J. Phys. Chem. 1994, 101, 5494−
5499.
(23) (a) Mackin, H. C.; Tsubaki, M.; Yu, N.-T. Biophys. J. 1983, 41,
349−357. (b) Tsubaki, M.; Yu, N.-T. Proc. Natl. Acad. Sci. U.S.A. 1981,
78, 3581−3585. (c) Proniewicz, L. M.; Nakamoto, K.; Kincaid, J. R. J.
Am. Chem. Soc. 1988, 110, 4541−4545. (d) Proniewicz, L. M.;
Kulczicky, A.; Weselucha-Birczinska, A.; Maicherczyk, H.; Nakamoto,
K. New J. Chem. 1999, 71−76.
(24) (a) Beckers, H.; Zeng, X.; Willner, H. Chem.Eur. J. 2010, 16,
1506−1520. (b) Jacox, M.; Thompson, W. E. J. Chem. Phys. 2008, 129,
204306/1−15. (c) McGrath, M. P.; Francl, M. M.; Rowland, F. S.;
Hehre, W. J. J. Phys. Chem. 1988, 92, 5352−5357. (d) Lee, Ch.-I.; Lee,
Y.-P.; Wang, X.; Qin, Q.-Z. J. Chem. Phys. 1998, 109, 10446−10455.
(25) (a) Fateley, W. G.; Bent, H. A.; Crawford, B., Jr. J. Chem. Phys.
1959, 31, 204−217. (b) Varetti, E. D.; Pimentel, G. C. J. Chem. Phys.
1971, 55, 3813−3821. (c) Hisatsune, I. C.; Devlin, J. P; Wada, Y. J.
Chem. Phys. 1960, 33, 714−719.
(26) Colthup, N. B., Daly, L. H., Wiberley, S. E. Introduction to
Infrared and Raman Spectroscopy, 3rd ed.; Academic Press: Boston,
MA, 1990.
(27) Hikichi, S.; Komatsuzaki, H.; Akita, M.; Moro-Oka, Y. J. Am.
Chem. Soc. 1998, 120, 4699−47.
(28) (a) Gulyan, G. M.; Kurtikyan, T. S.; Ford, P. C. Inorg. Chem.
2008, 47, 787−789. (b) Kurtikyan, T. S.; Martirosyan, G. G.;
Hakobyan, M. E.; Ford, P. C. Chem. Commun. 2003, 1706−1707.
(29) Wyllie, G. R. A.; Scheidt, W. R. Chem. Rev. 2002, 102, 1067−
1089.
(30) Wyllie, G. R. A.; Munro, O. Q.; Schulz, Ch. E.; Scheidt, W. R.
Polyhedron 2007, 26, 4664−6472.
(31) Ellison, M. K.; Shang, M.; Kim, J.; Scheidt, W. R. Acta
Crystalogr., Sect.C 1996, C52, 3040−3050.
(32) Battenqq, P.; Hamilton, A. L.; Johnson, A. W.; Mahendran, M.;
Ward, D.; King, T. J. J. Chem. Soc., Perkin Trans. 1977, 1, 1623−1627.
(33) Suslick, K. S.; Watson, R. A. Inorg. Chem. 1991, 30, 912−919.
(34) Nakamoto, K. Infrared and Raman Spectra of Inorganic and
Coordination Compounds, 3rd ed.; Wiley: New York, 1978; p 244.
(35) (a) The formation of (Py)Co(TPP)(NO3) as a result of
disproportionation reaction 2(Py)Co(TPP)(NO2) = (Py)Co(TPP)
(NO) + (Py)Co(TPP)(NO3) was suggested based on the IR bands at
1530, 1265 and 990 cm−1.35b Very close frequencies show Fe(TPP)
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