Copper(I) nitro complex with an anionic [HB(3,5-Me2Pz) 3]- ligand: A synthetic model for the copper nitrite reductase active site

Article abstract of DOI:10.1021/ic300932a

The new copper(I) nitro complex [(Ph₃P)₂N][Cu(HB(3,5- Me₂Pz)₃)(NO₂)] (2), containing the anionic hydrotris(3,5-dimethylpyrazolyl)borate ligand, was synthesized, and its structural features were probed using X-ray crystallography. Complex 2 was found to cocrystallize with a water molecule, and X-ray crystallographic analysis showed that the resulting molecule had the structure [(Ph₃P) ₂N][Cu(HB(3,5-Me₂Pz)₃)(NO₂)] ·H₂O (3), containing a water hydrogen bonded to an oxygen of the nitrite moiety. This complex represents the first example in the solid state of an analogue of the nitrous acid intermediate (CuNO₂H). A comparison of the nitrite reduction reactivity of the electron-rich ligand containing the CuNO₂ complex 2 with that of the known neutral ligand containing the CuNO₂ complex [Cu(HC(3,5-Me₂Pz) ₃)(NO₂)] (1) shows that reactivity is significantly influenced by the electron density around the copper and nitrite centers. The detailed mechanisms of nitrite reduction reactions of 1 and 2 with acetic acid were explored by using density functional theory calculations. Overall, the results of this effort show that synthetic models, based on neutral HC(3,5-Me₂Pz)₃ and anionic [HB(3,5-Me₂Pz) ₃]^- ligands, mimic the electronic influence of (His) ₃ ligands in the environment of the type II copper center of copper nitrite reductases (Cu-NIRs).

Full text of DOI:10.1021/ic300932a

Article
pubs.acs.org/IC
Copper(I) Nitro Complex with an Anionic [HB(3,5-Me2Pz)3]− Ligand: A
Synthetic Model for the Copper Nitrite Reductase Active Site
Sodio C. N. Hsu,*,† Yu-Lun Chang,†,‡ Wan-Jung Chuang,† Hsing-Yin Chen,*,† I-Jung Lin,†
Michael Y. Chiang,‡ Chai-Lin Kao,† and Hsuan-Ying Chen†
†Department of Medicinal and Applied Chemistry, Kaohsiung Medical University, Kaohsiung 807, Taiwan
‡Department of Chemistry, National Sun Yat-Sen University, Kaohsiung 804, Taiwan
S
* Supporting Information
ABSTRACT: The new copper(I) nitro complex [(Ph3P)2N][Cu(HB(3,5-Me2Pz)3)-
(NO2)] (2), containing the anionic hydrotris(3,5-dimethylpyrazolyl)borate ligand, was
synthesized, and its structural features were probed using X-ray crystallography. Complex 2
was found to cocrystallize with a water molecule, and X-ray crystallographic analysis
showed that the resulting molecule had the structure [(Ph3P)2N][Cu(HB(3,5-Me2Pz)3)-
(NO2)]·H2O (3), containing a water hydrogen bonded to an oxygen of the nitrite moiety.
This complex represents the first example in the solid state of an analogue of the nitrous
acid intermediate (CuNO2H). A comparison of the nitrite reduction reactivity of the electron-rich ligand containing the CuNO2
complex 2 with that of the known neutral ligand containing the CuNO2 complex [Cu(HC(3,5-Me2Pz)3)(NO2)] (1) shows that
reactivity is significantly influenced by the electron density around the copper and nitrite centers. The detailed mechanisms of
nitrite reduction reactions of 1 and 2 with acetic acid were explored by using density functional theory calculations. Overall, the
results of this effort show that synthetic models, based on neutral HC(3,5-Me2Pz)3 and anionic [HB(3,5-Me2Pz)3]− ligands,
mimic the electronic influence of (His)3 ligands in the environment of the type II copper center of copper nitrite reductases (Cu-
NIRs).
titration of the copper(I) nitro complex reduction process, have
led to the proposal that a nitrous acid intermediate (CuNO2H)
exists in the process. Observations made in recent studies28
show that sterically hindered tris(1-pyrazolyl)methane (TPM)
and tris(4-imidazolyl)carbinol (TIC) tridentate ligands in
model copper(I) nitro complexes exert steric and weak
electronic effects. Independently, we and others have described
rare copper(I) nitrito phosphine complexes, which also react to
form nitric oxide gas when treated with acetic acid under
anaerobic conditions.30,31 Therefore, these complexes serve as
functional but not structural models for Cu-NIRs. Recently, the
first example of a monomeric copper(I) nitrito complex,
containing two bidentate nitrogen ligands, was described,32 but
its catalytic activity was not evaluated.
Another important bioinorganic mimicking ligand, hydrotris-
(pyrazolyl)borate anion (RRTp), has been used to construct a
copper(II) nitrito complex (RRTpCuNO2)33−35 and structurally
models of the copper nitrosyl intermediate (RRTpCuNO).36−39
Hydrotris(triazolyl)borate, a RRTp analogue, has recently been
used as a ligand in CuNO2 complexes that have been probed as
structural and functional models of Cu-NIRs.40 Although a
comparison of the properties of the copper(I) nitro of RRTp
with known copper(I) nitro complexes28 containing TPM
would provide important information about the ligand effects
on the catalytic activities of Cu-NIRs, the RRTp complex
remains an unknown entity.25
INTRODUCTION
■
The active sites of copper-containing nitrite reductases (Cu-
NIRs), which transform NO2− to NO, contain a type I electron-
transfer center that is coupled via a His-Cys bridge to a type II
catalytic center.1−10 The results of numerous spectroscopic and
crystallographic studies have led to proposed mechanisms
(Scheme 1) for catalysis by the Cu-NIRs,11−22 which involve
the formation of copper(I) nitro or nitrito core species by
either the reduction of oxidized Cu-NIRs followed by nitrite
anion binding or the binding of nitrite to oxidized Cu-NIRs first
followed by reduction. In the next step of the catalytic pathway,
the copper(I) nitro or nitrito species is protonated by an
adjacent aspartate residue (Asp98), forming a copper nitrosyl
intermediate. Finally, NO is displaced from the copper by
water, regenerating the active enzyme.
Because of the proposed key role they play in catalysis by the
Cu-NIRs, copper(I) nitro or nitrito complexes have been
important targets of structural and chemical studies. However,
the preparation of these substances has remained challenging,
and only a few copper(I) nitro complexes have been
characterized thus far by using single-crystal X-ray meth-
ods.23−28 In one effort, Tolman and co-workers synthesized the
first functional, mononuclear biomimetic model of the copper
centers in Cu-NIRs. The nitro-binding copper(I) complex
[(iPr-TACN)Cu(NO2)] (iPr-TACN = 1,4,7-triisopropyl-1,4,7-
triazacyclononane) prepared in this study was observed to
evolve nitric oxide gas through reaction with 2 equiv of acetic
acid.23 The results of related investigations,29 aimed at
examining the protonation reaction by using spectroscopic
Received: May 7, 2012
Published: August 20, 2012
© 2012 American Chemical Society
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evaluation of how the electronic properties of the two
differently charged ligands affect the electronic properties of
the complexes. Significantly, as discussed below, the results of
this effort demonstrate that the nitrite reductase reactivity of
neutral and anionic copper(I) nitro complexes is significantly
influenced by the electron density at the copper nitrite center.
Scheme 1. Revised Mechanism for Catalysis by Cu-NIRs
Based on the Results of Averill, Suzuki, and Hasnain3,10,17,19
RESULTS AND DISCUSSION
■
Synthesis and Spectroscopic Characterization of
Complexes 1 and 2. The neutral copper(I) nitro complex
[Cu(HC(3,5-Me2Pz)3)(NO2)] (1) was prepared through the
reaction of [Cu(HC(3,5-Me2Pz)3)(NCMe)](BF4)41 with
NaNO2 in methanol under N2 and isolated as a pale-yellow
solid (Scheme 2). An alternative method for the synthesis of
Scheme 2. Method for the Synthesis of Copper(I) Nitro
Complexes 1 and 2
complex 1 was reported in a publication28 that appeared during
the preparation of the current manuscript. Treatment of the
42
dimeric complex [HB(3,5-Me2Pz)3Cu]2 with an equimolar
amount of [(Ph3P)2N](NO2) [(Ph3P)2N = bis-
(triphenylphosphine)iminium] in tetrahydrofuran (THF)
leads to formation of the novel mononuclear copper(I) nitro
complex [(Ph3P)2N][Cu(HB(3,5-Me2Pz)3)(NO2)] (2), con-
taining a negatively charged [HB(3,5-Me2Pz)3]− ligand.
Crystallization of this substance from THF yields 2 as yellow
crystals. When wet THF is employed in the crystallization
process, an adventitious water molecule cocrystallizes with 2 to
generate the pale-yellow complex [(Ph3P)2N][Cu(HB(3,5-
Me2Pz)3)(NO2)]·H2O (3). For comparison purposes, an
attempt was made to crystallize the copper(I) nitro complex
1 from wet THF. However, in this case, a crystalline complex
containing water was not produced.
Below, we describe the results of an investigation that has led
to the synthesis and structural characterization of a copper(I)
nitro complex stabilized by the anionic tripodal scorpionate
ligand hydrotris(3,5-dimethylpyrazolyl)borate ([HB(3,5-
Me2Pz)3]−) and a comparison of its properties with that of
the known28 copper(I) nitro complex stabilized by the neutral
tris(3,5-dimethylpyrazolyl)methane [HC(3,5-Me2Pz)3] ligand
(Chart 1). Both complexes contain facially coordinating
pyrazole groups that closely mimic the pyramidal array of
histidine imidazoles that is present around copper in the type II
active site of Cu-NIRs. Moreover, this study enabled an
The structures of copper(I) nitro complexes 1 and 2 were
1
initially assigned using H NMR spectroscopy and elemental
analysis. The electrospray ionization mass spectrometry (ESI-
MS) data of 1 and 2 contain characteristic molecular ion peaks
and corresponding fragment ion peaks corresponding to the
loss of coordinated NO2. Also, UV−vis spectra of complexes 1
and 2 also contain diagnostic metal-to-ligand charge-transfer
(MLCT) bands at 293 and 336 nm, respectively (Figure 1).
The difference seen in the positions of the MLCT absorption
bands could be a consequence of the dissimilar electronic
structures of 1 and 2. The IR spectra of 1 and 2, measured
using KBr pellets, contain NO2 stretching bands for the anion 2
at 1302 and 1267 cm−1, which are shifted to lower frequencies
than those (1312 and 1285 cm−1) for the same stretching
modes in the neutral complex 1. This observation suggests that
the neutral [Cu(HB(3,5-Me2Pz)3)] moiety present in 2 causes
Chart 1. Structures of the Tris(3,5-
dimethylpyrazolyl)methane HC(3,5-Me2Pz)3 and
Hydrotris(3,5-dimethylpyrazolyl)borate Anionic [HB(3,5-
Me2Pz)3]− Ligands
−
a stronger CuI → NO2 π-back-bonding interaction than does
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and 3, respectively. Inspection of the plots show that N-nitro
coordination to the copper(I) center exists in each structure.
Figure 1. Absorption spectra of 1 (dashed line) and 2 (solid line) in
CH2Cl2 at room temperature.
the positive [Cu(HC(3,5-Me2Pz)3)] moiety in 1. The same
trend has been observed earlier in studies of copper(I)
acetonitrile and carbonyl complexes containing similar methane
and borate ligands.43
Figure 3. ORTEP representation of an anion of the X-ray structure of
3 (50% ellipsoids; some hydrogen atoms not shown for clarity).
To explore the electronic effects exerted by the negatively
charged borate ligand versus the corresponding neutral
methane ligand, cyclic voltammetric measurements with 2
(Figure S4 in the Supporting Information) in CH2Cl2
containing 0.1 M [n-Bu4N](PF6) were made and compared
with those of the known complex 1. Complex 1 exhibits a
quasi-reversible one-electron peak (E1/2 = 0.25 V; Epa = 0.39
V), assigned to the CuI/CuII redox process.28 In contrast, the
cyclic voltamagram of 2 contains an irreversible band
corresponding to an Epa value of 0.08 V, which is significantly
lower than that of 1. The results of the electrochemistry study
show that oxidation of complex 2 with the negative HB(3,5-
Selected bond lengths and angles of the complexes are listed in
Table 1 along with those of known complex 1 for
comparison.28 The coordination geometry around the copper
atom of 2 and 3, both of which contain chelated facial anionic
tridentate [HB(3,5-Me2Pz)3]− ligands, is best described as a
distorted tetrahedron. This feature is similar to that of 1, which
contains a chelated facial neutral HC(3,5-Me2Pz)3 auxiliary
ligand. It is noteworthy that a moderate hydrogen-bond
interaction, associated with an O(w)−O(NO2) distance of
2.898 Å,44 occurs between one of the oxygen atoms of the
copper(I) nitro unit and the cocrystallized water molecule in 3.
The presence of this hydrogen-bonded (H-bonded) water
molecule suggests that the borate complex 2 might display a
higher reactivity toward protic solvents or acids. Indeed,
complex 2 is observed to decompose in a methanol solution,
while 1 is moderately stable under similar conditions. Recently,
Kujime et al. was able to detect the nitrous acid intermediate
(CuNO2H) in nitrite reduction brought about by the rapid
mixing of [(iPr-TACN)Cu(NO2)] with trifluoroacetic acid at
low temperature in a stopped-flow apparatus.29 Consequently,
complex 3, with hydrogen-bond interaction between a water
molecule and an oxygen atom of the copper(I) nitro unit,
represents the first solid-state example of an analogue of the
nitrous acid intermediate (CuNO2H).
−
Me2Pz)3 ligand is more favorable than that of the neutral
HC(3,5-Me2Pz)3 ligand containing complex 1. This finding
indicates that the redox potentials of copper(I) nitro complexes
are governed by the electronic nature of the tridentate ligands
−
[negative HB(3,5-Me2Pz)3 ligand versus neutral HC(3,5-
Me2Pz)3 ligand].
Structural Studies of Copper(I) Nitro Complexes 2
and 3. The ORTEP representations of the X-ray crystallo-
graphic structures of complexes 2 and 3 are shown in Figures 2
The structures of the copper(I) nitro complexes are
governed by the nature of their tridentate neutral HC(3,5-
Me2Pz)3 and negatively charged [HB(3,5-Me2Pz)3]− ligands.
The intraligand NL−Cu−NL angles are restrained by the
chelate rings to 87.1° for 1, 90.0° for 2, and 90.3° for 3, and the
averages of the angles from nitrogen atoms of the nitrite donors
to the pyrazolyl nitrogen atoms are 127.20° for 1, 125.22° for 2,
and 124.98° for 3. The nitrite O−N−O angle [122.8(3)°] of 3
is larger than the corresponding value for 1 [117.4(5)°], 2
[116.7(7)°], and a free nitrite anion [114.9(5)°],45 possibly as a
result of hydrogen-bond perturbation caused by the cocrystal-
lized water molecule in 3. The Cu−NL distances in the
tridentate ligands of 1−3, ranging from of 2.046 to 2.113 Å, are
similar. Importantly, the Cu−Nnitro distance in 2 [1.927(5) Å]
is relatively larger than that in 1 [1.883(6) Å], indicating the
role played by the charge of the borate versus the methane
ligands containing identical pyrazolyl substituents. Thus, the
cationic [Cu(HC(3,5-Me2Pz)3)]+ moiety interacts more
Figure 2. ORTEP representation of an anion of the X-ray structure of
2 (50% ellipsoids; hydrogen atoms not shown for clarity).
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Table 1. Selected Bond Lengths (Å) and Angles (deg) for 2 and 3 and Other Relevant Copper(I) Nitro Complexes
Cu−Nnitro
N−O
Cu−NL
O−N−O
NL−Cu−Nnitro
NL−Cu−NL
ref
1
2
1.883(6)
1.176(7)
1.278(7)
2.051(3)
2.051(3)
2.124(5)
2.070(3)
2.078(5)
2.103(4)
117.4(5)
126.7(1)
126.7(1)
128.4(2)
121.07(19)
126.38(19)
128.2(2)
86.2(2)
28
87.6(1)
87.6(2)
1.927(5)
1.903(3)
1.212(9)
1.290(12)
1.161(10)
1.332(13)
1.224(4)
1.224(4)
116.7(7)
89.17(16)
90.19(14)
90.51(17)
this work
a
116.8(8)
a
a
3
2.046(4)
2.089(3)
2.113(2)
122.8(3)
114.9(5)
121.14(11)
123.75(10)
130.06(11)
88.82(9)
90.45(10)
91.65(9)
this work
45
NaNO2
1.240(3)
a
Oxygen atoms in the copper-bound nitro were found to be disordered.
strongly with a nitrite anion than does the neutral [Cu(HB(3,5-
Me2Pz)3)] moiety. The average of the two N−O distances
(1.251 Å) of 2 is slightly larger than the corresponding values of
1 (1.227 Å) and a free nitrite [1.240(3) Å],45 a finding that is
consistent with the IR results. Again, these features may be a
consequence of different electronic interactions of a nitrite ion
with the positive [Cu(HC(3,5-Me2Pz)3)]+ and neutral [Cu-
(HB(3,5-Me2Pz)3)] moieties. A similar effect of the positive
[Cu(HC(3,5-Me2Pz)3)]+ and neutral [Cu(HB(3,5-Me2Pz)3)]
moieties on π acceptors and σ donors has been discussed by
Fujisawa et al.43,46 The water-containing complex 3 has a
smaller Cu−NO2 distance [1.903(3) Å] than 2 [1.927(5) Å],
showing that the hydrogen-bond interaction affects the
properties of the copper(I) nitro bond.
Figure 4. Spectral changes observed during the anaerobic reaction of 2
with acetic acid in CH2Cl2 at 233 K.
Reactivity with Acid. In order to gain information about
how the electronic effects govern the nitrite reductase activity
of the copper(I) nitro complexes, containing neutral or anionic
tridentate nitrogen-donor ligands, the reactivity of the anionic
ligand containing complex 2 with proton sources was
determined and compares with that of 1, containing a neutral
ligand. The results show that complex 2 is highly reactive
toward acids, as shown by the immediate color change that
occurs when the complex is subjected to acidic conditions. In
contrast, 1 reacts more slowly with acid. In studies probing the
reactivity toward oxygen, we observed that complex 2 is an
extremely air-sensitive compound and that 1 is air- and
moisture-stable in the solid state but air-sensitive in solution.
These properties may also be a consequence of the different
electronic nature of the CuNO2 cores of 1 and 2.
The results of this investigation show that the reaction of 1
with acetic acid is first-order with respect to 1. The plots of
pseudo-first-order rate constants for this process versus acetic
acid concentration are curved rather than linear (Figure S5 in
the Supporting Information), indicating the occurrence of a
stepwise proton-transfer mechanism in agreement with the
results of a previous study.28 As mentioned above, in contrast to
1, 2 is more reactive with acetic acid. The rate of reaction of 2
with acetic acid at 233 K was monitored by using UV−vis
absorption spectroscopy. In the spectra, a decrease in the
absorbance at 336 nm and a slight increase at 750 nm is
observed as reaction occurs (Figure 4). The reaction of 2 with
acid was found to be first-order in 2, and the rate constant is
linearly dependent on the concentration of acetic acid (Figure
S6 in the Supporting Information). The difference in the rate
expressions for reactions of 1 and 2 with acetic acid suggests
that these processes have different rate-limiting steps associated
with the electron-rich CuNO2 moiety in 2, which causes the
nitrite reduction step to be more rapid than it is in the reaction
of complex 1, containing the neutral ligand. The results of
titration experiments using 1 and acetic acid show that 2 equiv
of acetic acid is consumed in the reaction.28 On the other hand,
the same experiments with 2 clearly show that only 1 equiv of
acetic acid is consumed in the reaction (see Figure S7 in the
Supporting Information). This difference demonstrates that
different mechanisms operate in the nitrite reduction reaction
of 1 and 2.
The products generated in reactions of 1 and 2 with both
acetic and trifluoroacetic acid were isolated and shown using
ESI-MS, elemental, and X-ray crystallographic analysis to be the
respective complexes [Cu(HC(3,5-Me2Pz)3)(CH3COO)2] (4),
[Cu(HB(3,5-Me2Pz)3)(CH3COO)] (5), and [Cu(HC(3,5-
Me2Pz)3)(CF3COO)2] (6) (see below), in which an acetate
(trifluoroacetate) anion is bound to the copper(II) ion.
The temperature dependencies of the rates of the nitrite
reduction reactions of 1 and 2 were examined at four
temperatures in the range of 223−273 K (Tables 2 and S1 in
the Supporting Information). Analysis of the results using the
typical Eyring approach (Figures S8 and S9 in the Supporting
Information) gave the ΔH⧧ and ΔS⧧ values listed in Table 2.
Comparisons of the activation parameters with those of the
known copper(I) nitro complex [Cu(Me2bpa)(NO2)]26
[Me2bpa = bis(6-methyl-2-pyridylmethyl)amine] (ΔH⧧ = 25
1 kJ mol−1 and ΔS⧧ = −51 3 J K−1 mol−1) reveals that
reactions of 1 and 2 have significantly larger ΔH⧧ (32.96 2.40
kJ mol−1 for 1; 36.57 2.25 kJ mol−1 for 2) and more negative
ΔS⧧ (−170.27 9.68 J K−1 mol−1 for 1; −115.40 9.49 J K−1
mol−1 for 2) values. Because a large negative ΔS⧧ value
generally corresponds to reactions having rate-determining
transition states involving the loss of translational degrees of
freedom, the very large negative ΔS⧧ values for reactions of 1
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Table 2. Rate Constants for the Nitrite Reduction of
Copper(I) Nitro Complexes (0.25 mM) with Excess Acetic
Acid (25 mM)
kobs (s−1
)
temperature (K)
1
2
223
233
243
253
273
(1.21 0.09) × 10−2
(2.64 0.25) × 10−2
(7.30 0.45) × 10−2
(1.33 0.11) × 10−1
(2.80 1.30) × 10−4
(5.00 1.00) × 10−4
(9.33 1.15) × 10−4
(3.90 0.60) × 10−3
1
2
ΔH⧧ (kJ mol−1
)
32.96 2.40
36.57 2.25
ΔS⧧ (J K−1 mol−1
)
−170.27 9.68
−115.40 9.49
and 2 suggest that nearly complete associative proton transfer
takes place in the transition state.
In order to further investigate the proton-transfer step in the
nitrite reduction process, kinetic isotopic effect (KIE) experi-
ments were carried out. The observed KIEs (kH/kD) for the
protonation reactions of 1 and 2 were found to be ca. 1.73 and
0.93, respectively. Although little KIE data for reactions of the
type have been accumulated thus far, studies have shown that
the protonation reaction of the neutral [(iPr-TACN)Cu(NO2)]
complex has a kH/kD value of ca. 1.4 at 203 K.29 The similarity
of this KIE with that of the protonation reaction of 1 suggests
theat they have similar rate-determining transition states. kH/kD
= 0.93 for the reaction of 2 with acid, representing a small
inverse KIE, suggests that the protonation step in the nitrite
reduction reaction of this substance is not rate-determining and
that further reaction of the deuterated intermediate derived
from 2 is more stable relative to its protonated analogue.
Importantly, these findings also indicate that protonation
occurs through a late transition state involving hydrogen
bonding between the acid and CuNO2 core of 2, prior to
transfer of the proton to nitrite. The suggestion that this
hydrogen-bond interaction leads to an inverse KIE is supported
by the results of studies of the protonation reactions of metal
hydride complexes.47
Figure 5. ORTEP representation of the X-ray structure of 6 (50%
ellipsoids; hydrogen atoms not shown for clarity).
play an important role in nitrite reduction by the Cu-NIRs.
Previously, the best models devised for Cu-NIR active sites
were nitro-bonding copper(I) complexes containing neutral
i
tridentate ligands, with the copper unit bearing Pr-TACN,
bis(6-methyl-2-pyridylmethyl)amine (Me2bpa), or sterically
hindered TIC and TPM ligands.25,26,28 In contrast, 2 contains
an electron-rich copper(I) nitro moiety, which might cause it to
react efficiently with acid to yield nitric oxide in a process that
mimics nitrite reduction by the Cu-NIRs.
To assess this issue, 2 and the known complex 1 were
investigated for their NO-generating ability. The addition of 6
equiv of trifluoroacetic acid to independent oxygen-free CH2Cl2
solutions of 1 and 2 at room temperature promotes a color
change from pale yellow to blue-green and stoichiometric
evolution of NO gas (52.3 3.72% for 1; 83.3 2.3% for 2;
Table 3), identified by using the known gas chromatography
Table 3. Yields of NO Generation from Reactions of 1 and 2
with Trifluoroacetic Acid in CH2Cl2
Structural Study of the Copper(II) Complex 6. As
mentioned above, the reaction of complex 1 with trifluoroacetic
acid produces 6. Single crystals of 6 were grown by the slow
diffusion of Et2O into a mixture of 1 and trifluoroacetic acid.
Inspection of the ORTEP plot of the crystallographic data
(Figure 5) shows that the coordination sphere around the
copper(II) ion in 6 has essentially a distorted square-pyramidal
geometry, with the basal plane comprised of two nitrogen
atoms, N2 and N4, from the tris(pyrazolyl)methane ligand and
two oxygen atoms, O1 and O3, from two monodentate
trifluoroacetate anions. The axial site in this geometry is
occupied by the nitrogen N6 from the tris(pyrazolyl)methane
ligand. This coordination geometry is supported by the
observed structural parameter τ value of 0.21.48 In contrast to
related tris(pyrazolyl)methane- and tris(pyrazolyl)-
boratecopper(II) complexes, the coordination geometry of 6
also contains a N3O2 coordination sphere, which has smaller τ
value (<0.1).33,49,50 These structural differences are presumably
caused by unfavorable steric interactions between the
trifluoromethyl and methyl groups on the tripodal scorpionate
tris(pyrazolyl)methane ligand.
yield (%)
entry
1
2
1
2
3
55.1
53.8
48.1
81.2
85.8
82.8
average standard deviation
52.3 3.72
83.3 2.3
with a thermal conductivity detector (GC-TCD) method
(Figure S10 in the Supporting Information).25,26,30 Compar-
isons of the NO evolution results with those arising from
studies of the known copper(I) nitro nitrogen ligand
environment complexes [(iPr-TACN)Cu(NO2)] (ca.
100%),25 [Cu(Me2bpa)(NO2)] (ca. 95%),26 and [(iPr-TIC)-
Cu(NO2)] [iPr-TIC = tris(3,5-diisopropyl-1-pyrazoyl)-
methane] (ca. 70%)28 demonstrate that the copper(I) nitro
complex 2 is also a good functional Cu-NIR model that
produces NO in reaction with trifluoroacetic acid under
anaerobic conditions. Importantly, no N2O gas is produced,
and the green-blue copper(II) products 6 and [Cu(HB(3,5-
Me2Pz)3)(CF3COO)] (7) (characterized by ESI-MS or
crystallographic methods) are generated as products in the
respective reactions of CuNO2 complexes 1 and 2.
NO Generation. The fact that the anionic ligand containing
complex 2 is more reactive toward protonation steps than its
neutral analogue 1 suggests that the electronic effects could
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Figure 6. M06/6-31G* free-energy profile for nitrite reduction of 1.
Figure 7. M06/6-31G* free-energy profile for nitrite reduction of 2.
Computational Results. Computational methods were
employed to gain additional information about the detailed
reaction mechanisms of nitrite reduction reactions of complexes
1 and 2. To economize on computing resources, the molecular
structures of 1 and 2 were simplified by eliminating three
methyl groups distant from the CuNO2 moiety because they
are expected to have minor influences on the reactivity. The
reaction pathways and the corresponding free-energy changes
derived from density functional theory (DFT) M06/6-31G*
calculations are summarized in Figures 6 and 7, and the
optimized structures for the relevant transition states and
intermediates are shown in Figures 8 and 9.
The first step in the reaction of complex 1 (Figures 6 and 8)
involves its association with acetic acid to form the H-bonded
complex. Two H-bonded conformations, B and B′, were found
to be energy minima (Figure 10). While the two conformations
are nearly isoenergetic (B is only 0.3 kcal mol−1 higher in
energy than B′), they display very different behaviors in the
subsequent proton-transfer step. While proton transfer from
−
acetic acid to NO2 in both conformations is barrierless, the
energy change occurring is considerably lower for B than it is
for B′ (5.8 vs 19.7 kcal mol−1; Figure 10). In conformation B,
acetic acid is located in close proximity to copper and,
therefore, during proton transfer the negative charge
accumulated on the conjugate base of the acid can be stabilized
by a CH3COO−···CuI interaction. This stabilizing interaction is
reflected in a significant decrease of the CH3COO−···CuI
distance from 3.018 to 2.172 Å in the course of proton transfer
(Figure 10). In contrast, this stabilizing interaction is not
available in the reaction of conformation B′ because acetic acid
−
is separated from copper by intervening NO2 .
The computational results suggest that the first protonation
−
of NO2 is taking place via the H-bonded conformation B
rather than B′, and it results in the formation of the protonated
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Figure 8. M06/6-31G*-optimized geometries of the transition states
and selected intermediates in the course of nitrite reduction of 1. For
clarity, the ligand moieties are represented by wireframes.
Figure 10. Relaxed potential energy surface scan of proton transfer
−
from acetic acid to NO2 for the complex of 1 and acid in H-bonded
conformations (a) B and (b) B′.
association step is thermodynamically less favorable, with an
association free energy of 3.1 kcal mol−1 (D → E).
Subsequently, the H-bonded complex E undergoes the second
proton-transfer reaction, leading to cleavage of the N−O bond
and the release of a water molecule (E → TSE/F → F). This
step is found to be rate-determining with an activation free
energy of 18.6 kcal mol−1 and a reaction free energy of −6.1
kcal mol−1. The stabilizing interaction between acetate and the
copper atom once again plays a role in the second protonation
step, as evidenced by a decrease of the O(acetate)···Cu distance
from 3.185 Å in E to 2.035 Å in TSE/F to 1.932 Å in F (Figure
8).
The results of wave-function stability tests indicate that the
most stable electronic states for TSE/F and F are singlet
biradical rather than closed-shell singlet or triplet. Analysis of
the natural population data reveals that the two spins are
mainly distributed on copper (the spin densities are 0.4708 in
TSE/F and 0.5843 in F) and NO (the spin densities are −0.5868
in TSE/F and −0.7418 in F). These results suggest that the
second protonation step is a proton-coupled electron-transfer
process in which the proton transfer from acetic acid to NO2H
simultaneously triggers an electron transfer from CuI to NO2H.
Therefore, the electronic state of F is better characterized as
CuII−NO• rather than CuI−NO+. The final step involving
liberation of NO (F → G) has a transition state that is located
on the electronic potential energy surface only 0.3 kcal mol−1
Figure 9. M06/6-31G*-optimized geometries of the transition states
and selected intermediates in the course of nitrite reduction of 2. For
clarity, the ligand moieties are represented by wireframes.
structure C in which the Cu−NO2H moiety exists in a syn
conformation defined by the H−O−N−Cu relation (Figure 6).
To facilitate the second protonation step, a syn−anti
transformation is formed through O−H rotation around the
N−O bond (C → TSC/D → D). The activation and reaction
free-energy changes for this transformation are +7.2 and −5.8
kcal mol−1, respectively. Once the anti conformation D is
formed, the second acetic acid can approach and bind in a
manner that is similar to formation of the H-bonded
conformation in the first association step. However, the second
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above F (further correction for the Gibbs free energy would
make it lower than F). As a consequence, NO release from F
should be a barrierless process with a free-energy change of
−6.1 kcal mol−1. These results indicate that F is not a stable
intermediate on the free-energy surface and, thus, NO and H2O
dissociate rapidly following (or in concert with) the second
protonation process (i.e., the reaction proceeds through E →
TSE/F → G).
The first two steps in the reaction of complex 2 (Figures 7
and 9) involve the association of 2 with acetic acid and
subsequent protonation of nitrite. As is the case with complex
1, two H-bonded conformations, I and I′, are found in the
pathway for 2 (Figure 11). The free-energy difference between
coordination (J → TSJ/K → K). The side-on η2-N,O-bonding
structure, K, lies only 1.5 kcal mol−1 above the η1-N-bonding
structure, J, and the activation free energy for J → K
transformation is only 6.2 kcal mol−1. The side-on bound
NO2H moiety in the intermediate K then cleaves to form OH
and NO, which then individually coordinate to the copper atom
to form intermediate L. It should be noted that a
hydroxonitrosyl intermediate of this type has been observed
in the previous computational studies on Cu-NIRs.51,52 The
results of relative DFT calculations on the CuINO system also
show an side-on-bound intermediate owing to steric
interactions with amino acid residues.53
The activation and reaction free-energy changes for K → L
were estimated to be 6.7 and 0.8 kcal mol−1, respectively.
Intermediate L was found to be a singlet biradical with a spin
density of 0.5095 on copper and a spin density of −0.6955 on
NO, which means that an electron has been transferred from
CuI to NO at this stage. To locate the transition state for the
final step of the process, involving NO release from the
intermediate L, a relaxed potential energy surface scan was
performed by stretching along the Cu···NO axis. The
computational results indicate that the total electronic energy
monotonically increases with the Cu···NO distance (Table S3
in the Supporting Information). In other words, the release of
NO is an endergonic process and it does not have an energetic
barrier. However, as NO leaves, the entropic contribution
becomes larger, which, in turn, creates a transition state on the
free-energy surface at a Cu···NO distance of ca. 3.1 Å (Table S3
in the Supporting Information). The activation and reaction
free energies for the NO release step, L → TSL/M → M, were
estimated to be 7.1 and 3.1 kcal mol−1, respectively.
In summary, the reaction of complex 1 with acetic acid
proceeds through two protonation steps followed by the
immediate release of H2O and NO, and the second protonation
step is rate-determining with an activation energy of 18.6 kcal
mol−1. Importantly, the DFT results provide a theoretical basis
for the experimentally observed curved-line plot of kobs versus
[H+] and the deuterium KIE in the reaction of 1. On the other
hand, the reaction of complex 2 with acetic acid requires only
the first protonation step to rupture the N−O bond of nitrite
and form a hydroxonitrosyl intermediate. This conclusion
explains why the rate of nitrite reduction involving complex 2 is
first-order in H+. Furthermore, the protonation of complex 2 is
not rate-determining because other steps in the mechanistic
pathway have comparable activation energies. This fact could
explain why a deuterium KIE was not observed in the reaction
of complex 2. Finally, the calculated energy barrier for the
reaction of 2 (6.2−7.1 kcal mol−1) is considerably lower than
that of 1 (18.6 kcal mol−1), an observation that is consistent
with the finding that the former complex displays higher
reactivity.
Above we described the interesting crystal structure of 3 in
which a water molecule acts as hydrogen-bond donor to a
nitrite oxygen atom. In addition, evidence exists to support the
proposal that several water molecules are present in the active
sites of Cu-NIRs.16 Consequently, it is interesting and
important to know how hydrogen bonding affects the catalytic
reactivity of these enzymes. The results of our preliminary
calculations show that when H2O is H-bonded to oxygen atoms
of nitrite in complexes 1 and 2, the first protonation step in the
overall process leading to NO production is impeded.
Specifically, the energy of the protonation step increases from
5.8 to 9.1 kcal mol−1 and from 6.9 to 11.5 kcal mol−1 for the
Figure 11. Relaxed potential energy surface scan of proton transfer
from acetic acid to NO2 for the complex of 2 and acid in H-bonded
conformations (a) I and (b) I′.
−
I and I′ is only 0.6 kcal mol−1, with the former being less stable.
However, proton transfer from acetic acid to nitrite is calculated
to be endergonic by 6.9 kcal mol−1 in I, more favorable than the
endergonicity of 12.4 kcal mol−1 in I′, due to the
CH3COO−···CuI-stabilizing interaction.
Interestingly, the following steps in the reaction of complex 2
were found to be distinct from those of complex 1. Rotation of
O−H around the N−O bond in the syn-CuI−NO2H moiety
does not result in formation of the anti conformation of CuI−
NO2H. Instead, in the course of rotation, the bonding mode
between Cu and NO2H gradually changes and eventually
reaches a novel intermediate state with side-on NO
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Scheme 3. Proposed Mechanism for Nitrite Reduction of 1
Scheme 4. Proposed Mechanism for Nitrite Reduction of 2
reactions of 1 and 2, respectively. This result leads to a tentative
conclusion that the nitrite reduction reactivity is reduced when
the oxygen atom of nitrite is H-bonded to a water molecule.
Further computational studies that consider the hydrogen-
bonding effects on other steps of the reaction mechanism, the
influence of different hydrogen-bonding conformations, and the
number of water molecules are needed to fully understand this
issue.
Nitrite Reduction Mechanisms. On the basis of
information found in the literature and the results of our
computational calculations,26,28 we suggest that the mechanism
concisely presented in Scheme 3 is operable in the nitrite
reduction process of the neutral ligand containing complex 1.
The existence of the protonated intermediate D in this process
is supported by studies by Kujime et al., in which a nitrous acid
intermediate (CuNO2H) was detected in a stopped-flow
experiment involving the rapid mixing of [(iPr-TACN)Cu-
(NO2)] with trifluoroacetic acid at low temperature.28,29
Intermediate D, subsequently, reacts with acid followed by
the release of NO to give the copper(II) acetate product 4. This
mechanism was proposed earlier by Fujii and co-workers based
on the results of kinetic measurements.28 In the current effort,
we isolated the final product of this process in the form of
complexes 4 and 6 containing carboxylate anions bound to
copper.
reduction process is best thought about as proton transfer
triggering an electron-transfer reaction.21 Therefore, the
formation of intermediate J might trigger rearrangement and
electron transfer to form intermediate L, which then releases
NO to give intermediate M. Several CuIIOH complexes
stabilized by tris(pyrazolyl)borate ligands have been described,
and these serve as precedents for intermediate M.54−56 Finally,
protonation of M leads to the elimination water and acetate
anion binding to generate 5.
CONCLUSION
■
In summary, copper(I) nitrite complexes 1 and 2, containing
the respective neutral HC(3,5-Me2Pz)3 or anionic [HB(3,5-
Me2Pz)3]− tripodal scorpionate ligands, have been prepared as
models of the active site of dissimilatory Cu-NIRs. X-ray crystal
structural analysis of 2 reveals that the geometry of the copper
center is a distorted tetrahedral and nitrite is N-coordinated to
copper. The results of a mechanism study show that in
reactions of these complexes with acetic acid the protonation
steps are not rate-determining. The nitrite reduction reactivity
of neutral and anionic copper(I) nitro complexes are
significantly influenced by the electron density around copper
and nitrite. The highly reactive, anionic ligand containing
complex 2 forms a new copper(I) nitro complex, 3, with a
cocrystallized water molecule that is H-bonded to an oxygen
atom of the copper(I) nitro moiety. Complex 3 represents the
first example of a solid-state nitrous acid intermediate
(CuNO2H) analogue. The results of DFT calculations show
that nitrite reduction reactions of 1 and 2 proceed through
different mechanistic pathways.
The nitrite reduction mechanism for the reaction of complex
2 with acetic acid is displayed in Scheme 4. Importantly,
titration experiments of 2 with acetic acid, consuming 1 equiv
of acetic acid, support this proposed mechanism. The
protonated intermediate J in this pathway is similar to the
nitrous acid intermediate (CuNO2H) D. The novel complex 3,
containing an anionic copper(I) nitro unit with an H-bonded
water molecule, isolated in this effort represents the first
example of an analogue of the nitrous acid intermediate
(CuNO2H). Recently, Solomon et al. suggested that the nitrite
A survey of the literature shows that most copper(I) nitro
bonding mode complexes possessing trinitrogen-donor auxil-
iary ligands release NO gas upon treatment with acid.25,26,28
However, no examples exist of copper(I) nitrito complexes with
trinitrogen donors as auxiliary ligands undergoing this process.
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immersion quartz probe of 1 cm path length (Hellma) and fitted to a
Schlenk flask containing 50 mL of a CH2Cl2 solution of 1 or 2 (both
0.25 mM) under a N2 atmosphere. The reaction was started with the
addition of 360 μL of acetic acid, which was degassed with N2 before
use.
Measurement of NO Generation. A solution of 2 (56.7 mg,
0.059 mmol) in CH2Cl2 (0.9 mL) was prepared in a small vial capped
with a rubber septum. A solution of trifluoroacetic acid (30 μL) in
CH2Cl2 (0.1 mL) was then introduced with a syringe at room
temperature. The solution changed immediately from colorless to
blue. Analysis of the headspace gas by a TCD indicated that NO had
Only two copper(I) nitrito complexes containing phosphine
ligands have been observed to release NO gas under acidic
conditions.30,31 Because phosphine ligands are unsuitable
models of the imidazole ligand, the copper(I) nitrito phosphine
complexes are not good structural models for Cu-NIRs. On the
basis of the results accumulated thus far, we believe that
copper(I) nitro complexes containing neutral HC(3,5-Me2Pz)3
or anionic [HB(3,5-Me2Pz)3]− ligands serve as the best
synthetic models of the type II copper centers in enzymes
that promote nitrite reduction.
been generated (83.3
2.3 for 2). The NO generation data are
obtained by using three different experiments (see Table 3 and Figure
S10 in the Supporting Information). NO concentrations were
determined by using a calibration curve correlating responses to
known concentrations of NO gas mixed with N2 (120, 100, 80, 60, and
40 ppm of NO in N2); molar quantities were calculated using the ideal
gas equation.
EXPERIMENTAL SECTION
■
All manipulations involving copper(I) complexes were carried out
under an atmosphere of purified N2 in a drybox or using standard
Schlenk techniques. Chemical reagents were purchased from Aldrich
Chemical Co. Ltd., Lancaster Chemicals Ltd., or Fluka Ltd. All of the
reagents were used without further purification, apart from all solvents,
which were dried over Na (Et2O and THF) or CaH2 (CH2Cl2, and
CH3CN) and then thoroughly degassed before use. The copper(I)
complexes [Cu(HC(3,5-Me2Pz)3)(NCMe)](BF4)41 and [HB(3,5-
X-ray Crystal Structure Determinations. All single-crystal X-ray
diffraction data were accumulated using a Bruker Nonius Kappa CCD
diffractometer using Mo Kα radiation (λ = 0.71073 Å). The data
collection was executed using the SMART program.57 Cell refinement
and data reduction were made with the SAINT program.58 The
structure was determined using the SHELXTL/PC program59 and
refined using full-matrix least squares. All non-hydrogen atoms were
refined anisotropically, whereas hydrogen atoms were placed at
calculated positions and included in the final stage of refinement with
fixed parameters. The disordered THF solvent molecules in complex 2
were removed from the diffraction data using the SQUEEZE program.
Further details are given in Table S4 in the Supporting Information.
Computational Method. All DFT calculations were carried out
using the Gaussian 09 program.60 The hybrid meta functional, M06,
combined with 6-31G* (5D, 7F) basis functions was used throughout
in this work. The M06 functional was chosen because it has been
shown to have good performance for many areas of chemical
problems, including main-group thermochemistry, kinetics, non-
covalent interactions, and, in particular, transition-metal thermochem-
istry.61,62 An ultrafine grid, specified by the “integral-
(grid=ultrafinegrid)” keyword, was used for numerical integrations.
Vibrational frequency analysis was performed for each optimized
structure to identify whether it is an equilibrium structure or a
transition state. The thermal correction to Gibbs free energy was made
under the conditions of 298.15 K and 1 atm. The “stable=opt”
keyword was used to test the wave-function stability as well as to
obtain a stable broken-symmetry solution (i.e., singlet biradical) if
instability exists. Once the broken-symmetry wave function was found,
the geometry was reoptimized in this electronic state. The spin
densities were evaluated using the natural population analysis method.
42
Me2Pz)3Cu]2 were prepared as described in the literature. IR
spectra were recorded on a Varian FT-IR 640 spectrometer. UV−vis
spectra were recorded on an Agilent 8453 spectrophotometer. 1H, 13C,
and 31P NMR spectra were acquired on a Varian Gemini-200 proton/
carbon FT-NMR spectrometer or a Varian Gemini-500 proton/carbon
FT-NMR spectrometer. ESI-MS spectra were collected on a Waters
ZQ 4000 mass spectrometer. Elemental analyses were performed on a
Heraeus CHN-OS rapid elemental analyzer. Cyclic voltammetry was
measured at a scan rate of 100 mV s−1 at around 10−4 M CH2Cl2
solutions using 0.1 M [n-Bu4N](PF6) as the supporting electrolyte and
referenced to Fc+/0. GC-TCD experiments were performed using a
Varian CP- 3800 gas chromatograph, a Porpak Q column (6 ft, 20 mL
min−1 flow rate, 30 °C, nitrogen carrier gas), and a TCD.
[Cu(HC(3,5-MePz)3)(NO2)] (1). A solution of [Cu(HC(3,5-
Me2Pz)3)(NCMe)](BF4) (0.205 g, 0.420 mmol) in 10 mL of
methanol was added to a solution of sodium nitrite (0.144 g, 2.095
mmol) in 5 mL of methanol. A yellow solid precipitate formed
immediately. The resulting precipitate was isolated by filtration,
washed with methanol (5 mL), and dried under vacuum at room
temperature to give a yellow product (0.12 g, 70%). Anal. Calcd for
C16H22O2N7Cu: C, 47.11; H, 5.44; N, 24.03. Found: C, 47.27; H,
5.51; N, 23.95. 1H NMR (acetone-d6): δ 7.85 (s, 1H, HC(3,5-
Me2Pz)3), 6.12 (s, 3H, 4-HPz), 2.54 (s, 9H, Me2Pz), 2.38 (s, 9H,
Me2Pz). IR (KBr, cm−1): ν(NO2) 3141, 2986, 2958, 2923, 1565, 1467,
−
−
1413, 1389, 1312 (1289, 15NO2 ), 1285 (1262, 15NO2 ), 1240, 1155,
−
1099, 1039, 980, 899, 849, 824 (814, 15NO2 ), 801, 705, 698, 631.
ESI-MS(+): m/z 361.29 ([Cu(HC(3,5-MePz)3)]+).
[(Ph3P)2N][Cu(HB(3,5-MePz)3)(NO2)] (2). In a glovebox, a
solution of [(Ph3P)2N](NO2) (0.162 g, 0.277 mmol) in 20 mL of
THF was added to a solution of [HB(3,5-Me2Pz)3Cu]2 (0.1 g, 0.138
mmol) in 5 mL of THF followed by stirring for 30 min. The solution
was kept at −20 °C for 3 days to yield yellow crystals (0.13 g, 0.138
mmol, 50%). Anal. Calcd for C51H52BCuN8O2P2: C, 64.80; H, 5.54;
ASSOCIATED CONTENT
* Supporting Information
Additional figures (Figure S1−S14) and tables (Table S1−S4)
and crystallographic data in CIF format for the structure
determinations of 2, 3, and 6. This material is available free of
charge via the Internet at http://pubs.acs.org.
■
S
1
N, 11.85. Found: C, 64.77; H, 5.81; N, 11.83. H NMR (acetone-d6):
δ 7.58−7.78 (m), 5.76 (s, 3H, 4-H(Pz)), 2.41 (s, 9H, CMe), 2.30 (s,
9H, CMe). IR (KBr, cm−1): 2922, 2470, 1542, 1438, 1302 (1284,
AUTHOR INFORMATION
Corresponding Author
*E-mail: sodiohsu@kmu.edu.tw (S.C.N.H.), hychen@kmu.edu.
tw (H.-Y.C.).
■
−
−
−
15NO2 ), 1267 (1265, 15NO2 ), 1186, 1115, 754 (746, 15NO2 ), 723,
694. ESI-MS(−): m/z 406.26 ([Cu(HB(3,5-Me2Pz)3)(NO2)]−).
[(Ph3P)2N][Cu(HB(3,5-MePz)3)(NO2)]·H2O (3). In a glovebox, 2
(0.1 g, 0.10 6 mmol) was dissolved in 2 mL of degassed wet THF and
kept at −20 °C for 7 days to yield yellow crystals (0.03 g, 30%). Anal.
Calcd for C51H54O3N8BCuP2: C, 63.59; H, 5.65; N, 11.63. Found: C,
63.37; H, 5.51; N, 11.68.
Notes
The authors declare no competing financial interest.
Kinetics. Kinetic studies of nitrite reduction of 1 or 2 in CH2Cl2
were carried out by monitoring decreases in the intensities of the 262
and 336 nm absorption bands, respectively. The absorbance was
detected by using an Agilent 8453 spectrophotometer equipped with
an UNISOKU USP-203A cryostat or a custom-designed fiber-optic
ACKNOWLEDGMENTS
■
Financial support for this study by a grant from the National
Science Council (Taiwan) is highly appreciated (NSC Grant
100-2113-M-037-006-MY2). We thank Ting-Shen Kuo, Na-
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