Spectroscopic characterization of a hydroperoxo-heme intermediate: Conversion of a side-on peroxo to an end-on hydroperoxo complex

Article abstract of DOI:10.1002/anie.200904572

Chemical Equitation Presentation Modeling job: Protonation of a closed seven-coordinate side-on heme peroxide can switch its spin state from high- to low-spin and convert the η² binding fashion into a monodentate configuration to afford the cor

Full text of DOI:10.1002/anie.200904572

Communications
DOI: 10.1002/anie.200904572
Enzyme Models
Spectroscopic Characterization of a Hydroperoxo–Heme
Intermediate: Conversion of a Side-On Peroxo to an
End-On Hydroperoxo Complex**
Jin-Gang Liu, Takehiro Ohta, Satoru Yamaguchi, Takashi Ogura,
Satoshi Sakamoto, Yonezo Maeda, and Yoshinori Naruta*
Angewandte
Chemie
9262
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The ferric hydroperoxo–heme species [Fe–OOH] (com-
pound 0) is well known as a common key intermediate in
the catalytic cycles of heme-containing monooxygenase and
peroxidase enzymes.[1–4] The catalytic cycles of nitric oxide
synthase,[1] cytochrome P450,[2] and heme oxygenase (HO)[3]
generally involve single-electron reduction of an oxy–ferrous
intermediate to form a ferric peroxo species. This process is
often coupled with proton transfer to the distal oxygen atom
of the peroxo intermediate to afford the ferric hydroperoxo
species. The ferric hydroperoxo–heme species has also been
suggested to be a plausible intermediate in the catalytic cycle
of cytochrome c oxidase (CcO).[5] Although the crucial role of
ferric (hydro)peroxo hemes has been widely recognized, the
transient character of these intermediates has hampered
efforts to characterize them during catalytic turnover under
physiological conditions. The generation of ferric (hydro)-
peroxo intermediates in heme enzymes is typically achieved
by radiolytic reduction of the corresponding ferrous–oxy
À
[FeIII(O2 )] precursor at cryogenic temperature (77 K).[6–9]
Owing to their relevance to enzymatic transformations,
(hydro)peroxo porphyrin model complexes have been
actively investigated.[5,10–14] The frequently observed inter-
mediates are high-spin side-on peroxo species,[11,12] and the
infrequently reported low-spin hydroperoxo models, which
are mainly observed by UV/Vis and EPR spectroscopy, are
ligated by an exogenous axial ligand.[13] Characterization of
such low-spin (hydro)peroxo–heme complexes by resonance
Raman spectroscopy (rR) has not yet been reported. In our
previous synthetic model studies of CcO, we reported a series
of copper-ion-bridged heme peroxides.[14] Herein, we describe
efficient methods for the preparation of a low-spin end-on
Scheme 1. Selective preparation of hydroperoxo–heme species 2 by
different routes.
state and binding-mode switch of heme peroxide that is
triggered by protonation.
The model compound [(tmpIm)FeII] was prepared accord-
ing to a procedure similar to the multistep method described
in our previous report[14a] starting from 5,10,15-trismesityl-20-
(2-nitrophenyl)porphyrin. In the next step, a solution of
[(tmpIm)FeII] in MeCN/THF (20:80) at À308C reacted
rapidly with KO2, which was solubilized with [2,2,2]cryptand
in MeCN, to afford a brownish-green complex 1. This
complex has a UV/Vis spectrum ((lmax (e/mÀ1 cmÀ1) = 440
(1.1 ꢁ 105), 574 (1.1 ꢁ 104), 615 nm (7.0 ꢁ 103); Figure 1) that is
similar to that of a side-on peroxo species [(tmp)FeIII(O22À)]
(tmp = 5,10,15,20-tetrakis(2,4,6-trimethylphenyl)porphyrin;
lmax(e/mÀ1 cmÀ1) = 439 (1.3 ꢁ 105), 569 (1.2 ꢁ 104), 614 nm (6.5 ꢁ
ferric hydroperoxo heme species [(tmpIm)FeIII OOH] (2,
À
Scheme 1) that possesses a covalently linked axial imidazole
(Im) ligand, as confirmed by UV/Vis, EPR, rR, and Mꢀssba-
uer spectroscopy. Our experimental results demonstrate that
protonation of a side-on high-spin heme peroxide leads to the
formation of the corresponding end-on low-spin hydroper-
oxide. This reaction represents the first example of a spin-
[*] Dr. J.-G. Liu, Dr. T. Ohta, Prof. Dr. Y. Naruta
Institute for Materials Chemistry and Engineering
Kyushu University
Higashi-ku, Fukuoka, 812-8581 (Japan)
Fax: (+81)92-642-2715
E-mail: naruta@ms.ifoc.kyushu-u.ac.jp
Homepage: http//narutalab.ifoc.kyushu-u.ac.jp
S. Sakamoto, Prof. Dr. Y. Maeda
Graduate School of Sciences, Kyushu University
Higashi-ku, Fukuoka 812-8581 (Japan)
Dr. S. Yamaguchi, Prof. Dr. T. Ogura
Graduate School of Life Sciences, University of Hyogo
Hyogo, 678-1297 (Japan)
[**] This work was financially supported by Grants-in-Aid for Scientific
Research (S) (no. 17105003, YN), for Young Scientists (B) (no.
27150173, JGL) from JSPS, on Priority Areas (no. 19027044, YN),
Innovative Areas (no. 20200050, JGL) from MEXT; and by the
Elemental Science and Technology Project from MEXT. The 430 nm
laser was set up by Dr. Ken’ichi Nakagawa, The University of Electro-
Communications (Japan).
Figure 1. UV/Vis spectra of [(tmpIm)FeII] (black trace), and its reaction
with KO2 to afford complex 1 (red trace) in MeCN/THF (20:80) at
À308C. Protonation of complex 1 by methanol yields complex 2 (blue
trace) at À658C. The inset shows the magnified Q-band region.
Supporting information for this article is available on the WWW
under http://dx.doi.org/10.1002/anie.200904572.
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À1
103)) prepared under similar experimental conditions (Fig-
pound 1, the n(O O) stretching is 2 cm lower and n(Fe O)
is 5 cmÀ1 higher than that of the imidazole-free side-on peroxo
[(tmp)FeIII(O22À)]. This result may be an indication that
À
À
ure S1 in the Supporting Information). The EPR spectrum of
complex 1 (Figure 3a) has a typical rhombic marker signal at
g ꢀ 4.2, which is similar to that of [(tmp)FeIII(O22À)] and is
consistent with a h2-peroxo–heme species. Complex 1 was
then further characterized by rR spectroscopy. The rR spectra
of complex 1 show two groups of isotope shifts (Figure 2).
À
binding of the axial imidazole ligand to iron weakens the O
O bond by increasing the p*-orbital electron density. The Fe
À
O bond is strengthened by back-donation from the oxygen to
the iron atom and by electron donation of the imidazole
ligand to the oxygen p* orbital through the trans effect. The
implication of association of the imidazole with the iron
porphyrin is further supported by the following observation:
in the presence of the coordinating solvent DMSO, the side-
on peroxo compound [(dmso)(tmp)FeIII(O22À)] exhibited
dramatically increased nucleophilicity relative to the parent
compound [(tmp)FeIII(O22À)], as a result of the axial associ-
One band appears at 807 cmÀ1 and shifts to 758 cmÀ1 upon 18
O
À
substitution. This band is assignable to the n(O O) stretching
vibration of a peroxo species. The other band at 475 cmÀ1
18
(16O) and 455 cmÀ1 ( O) is assigned to the n(Fe O) stretching
À
À
vibration. The relatively lower frequency of n(Fe O) is
similar to that of the nonheme h2-peroxo complexes.[15] For
À
À
comparison, the n(O O) and n(Fe O) stretching vibrations
of the side-on compound [(tmp)FeIII(O22À)] appear at
809 cmÀ1 and 470 cmÀ1, respectively (Figure S2 in the Sup-
porting Information). These results suggest that, for com-
ation of DMSO to the iron porphyrin.[12c–d] The rR spectrum
of [(dmso)(tmp)FeIII(O2 )] has n(O O) and n(Fe O) bands
at 807 cmÀ1 and 476 cmÀ1, respectively (Figure S3 in the
Supporting Information). These bands are essentially the
2À
À
À
À
same as those of complex 1. The observed n(O O) value is
comparable to that of similar side-on heme peroxide obtained
by IR spectroscopy.[12f] These results may suggest that
complex 1 is a seven-coordinate (7c) side-on peroxide species.
To the best of our knowledge, this is the first reliable rR
evidence for this type of side-on heme peroxides.[12f]
The most striking difference between complex 1 and
[(tmp)FeIII(O22À)], (7c versus 6c side-on peroxo), comes from
their reactivity toward protonation. Addition of methanol
(400 equivalents) to a solution of complex 1 in MeCN/THF
(20:80) at À658C afforded a new species, complex 2. The
electronic absorption spectrum of complex 1 underwent
distinct spectral changes upon addition of methanol, with a
shift in the Soret band from 440 nm to 428 nm and a split in
the Q bands to 535, 562, and 609 nm (Figure 1). The UV/Vis
features are similar to those of the previously reported
hydroperoxo–heme model compounds such as [(tmp)FeIII-
( OH)( OOH)] (lmax = 428, 563, 601 nm).[13a] The EPR
experiments further confirmed this transformation. Protona-
tion of complex 1 caused the disappearance of the signal at
g ꢀ 4.2 and a new set of signals appeared at g = 2.31, 2.19, and
1.95 (Figure 3b). This result clearly indicates the signature of
a low-spin ferric heme species in a strong field with small
g dispersion. This set of g values corresponds very well with
those of the previously reported hydroperoxo–heme model
À
À
Figure 2. Resonance Raman spectra of complex 1 containing a) 16
O
and b) 18O. c) Difference spectrum of (a)À(b). lex =441.6 nm, 77 K.
III
[13a]
À
compound [(Im)(tmp)Fe ( OOH)] (g = 2.32, 2.19, 1.94),
and is similar to the g values of the end-on ferric hydro-
peroxo–heme intermediate generated in enzymes using
cryoradiolytic methods. For example, the g values of the
ferric hydroperoxo–heme intermediate of hemoglobin are
2.31, 2.18, and 1.94.[6] The formation of MeOH/MeOÀ-bound
low-spin ferric species is ruled out by these observed g values,
as can be seen from the EPR spectrum of the room-
temperature decomposed product, which shows a wide span
of g values (Figure 3c). On the other hand, for the six-
coordinate (6c) side-on peroxide [(tmp)FeIII(O22À)], protona-
tion under similar experimental conditions produces no new
intermediates and leads directly to decomposition of the
peroxide (Figure S4 in the Supporting Information). Thus,
protonation of a 7c side-on peroxide switches the closed form
to an end-on hydroperoxide. These results indicate that axial
Figure 3. EPR spectra of a) complex 1, b) 2, and c) the room-temper-
ature decomposition product of 2, 77 K. The signal labeled with an
asterisk originates from residual O2 in the solution.
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imidazole ligation to the heme iron is crucial for the
generation of the hydroperoxo species.
Preparation of the hydroperoxo species could also be
achieved by reaction of [FeII(tmpIm)] with KO2 in the
presence of methanol at À758C. Upon addition of KO2 to a
EtCN/THF (20:80) solution of [FeII(tmpIm)] containing
methanol (400 equiv), the Soret band immediately shifted
from 423 nm (e = 1.1 ꢁ 105) to 427 nm (9.9 ꢁ 104) and the
Q bands shifted from 532 (1.6 ꢁ 104), 564 (8.6 ꢁ 103) to 533
(1.2 ꢁ 104), 564 (1.0 ꢁ 104), and 609 nm (7.3 ꢁ 103; Figure 4).
Figure 4. UV/Vis spectra of complex 2 (c) prepared from reaction
of KO2 with [(tmpIm)FeII] (g) in the presence of methanol
(400 equiv) in EtCN/THF (20:80) at À758C. The inset shows the EPR
spectrum of complex 2 prepared as described above.
Figure 5. A) Resonance Raman spectra of complex 2 containing a) 16
O
These UV/Vis spectral features are similar to those of
complex 2. The EPR spectrum of this species has the same
set of g values (g = 2.32, 2.19, 1.95) as complex 2 (Figure 4,
inset). Thus, these results indicate that the same compound
was prepared by the two different routes. Complex 2 was
further characterized by rR spectroscopy. The rR spectra
reveal isotope shifts of 810(16O)/763(18O) cmÀ1 in the region
near 800 cmÀ1 and of 570(16O)/544(18O) cmÀ1 in the low-
frequency region (Figure 5A). Deuterium substitution of
and b) 18O. c) Difference spectrum of (a)À(b); B) Resonance Raman
spectra of [(tmpIm)FeIII OOD] containing a) 16O and b) 18O. c) Differ-
À
ence spectrum of (a)À(b). lex =429.6 nm, 77 K.
Mꢀssbauer spectrum of complex 2 exhibits a quadrupole
doublet characterized by an isomer shift dFe of 0.25 mmsÀ1
and a quadrupole splitting DEq of 2.16 mmsÀ1. These param-
eters are typical for a low-spin ferric species and are in
agreement with those of the hydroperoxo–heme species
(dFe = 0.29 mmsÀ1, DEq = 2.03 mmsÀ1) from heme oxygen-
ase.[7d]
complex 2 with MeOD produced a 4 cmÀ1 upshift of the n(O
À
O) band and a 4 cmÀ1 downshift of the n(Fe O) band
À
(Figure 5B). These H/D substitution shifts are in good
agreement with previously reported rR data for metallo–
hydroperoxo species and are consistent with the existence of
hydrogen-bonding between the hydroperoxo and methanol
molecules.[16] Thus, the modes at 810 and 570 cmÀ1 can be
It is worth noting that complex 2 may also be generated
through
a
one-electron reduction of the oxy form
[(tmpIm)FeIII(O2 )] in the presence of a proton source. This
reaction occurs in a similar manner to that of the catalytic
processes of heme enzyme systems. Oxygenation of a solution
of [(tmpIm)FeII] in EtCN/THF (20:80) in the presence of
methanol (400 equiv) at À758C produced the corresponding
dioxygen adduct, which represents a superoxide species
À
À
À
assigned to the hydroperoxide n(O O) and n(Fe O) stretch-
À
À
ing vibrations, respectively. The observed n(O O) and n(Fe
O) values are comparable to those of the hydroperoxo
intermediate isolated by the cryoreduction method with
À
À
À
cytochrome P450 whose n(O O) and n(Fe O) modes
[(tmpIm)FeIII(O2 )] and has UV/Vis absorption maxima at
appear at 774 and 564 cmÀ1, respectively.[16a]
426, 535, and 589 nm. After removal of the excess dioxygen,
addition of one equivalent of cobaltocene ([CoCp2]) imme-
diately produces a new species with UV/Vis absorption
maxima at lmax = 427, 534, 564 and 610 nm. These features
The characterization of complex 2 was further corrobo-
rated by Mꢀssbauer data. The zero-field Mꢀssbauer spectra of
57Fe-enriched complexes 2 was measured at 80 K. The
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are similar to those of complex 2 obtained in the reaction of
[(tmpIm)FeII] with KO2 in the presence of methanol in the
same solvents (Figure 6). The EPR spectrum of this species
shows signals at g = 2.32, 2.19, and 1.95, which confirm its
identification as complex 2 (Figure 6, inset). As expected, the
[1] D. J. Stuehr, Biochim. Biophys. Acta Bioenerg. 1999, 1411, 217 –
230.
[2] a) I. G. Denisov, T. M. Makris, S. G. Sligar, I. Schlichting, Chem.
Rev. 2005, 105, 2253; b) S. Jin, A. Bryson, J. H. Dawson, J. Biol.
Inorg. Chem. 2004, 9, 644 – 653.
[3] M. Unno, T. Mastui, M. Ikeda-Saito, Nat. Prod. Rep. 2007, 24,
553 – 570.
[4] a) K. Kuhnel, E. Derat, J. Terner, S. Shaik, I. Schlichting, Proc.
Natl. Acad. Sci. USA 2007, 104, 99 – 104; b) I. G. Denisov, J. H.
Dawson, L. P. Hager, S. G. Sligar, Biochem. Biophys. Res.
Commun. 2007, 363, 954 – 958; c) I. G. Denisov, T. M. Makris,
S. G. Sligar, J. Biol. Chem. 2002, 277, 42706 – 42710.
[5] E. Kim, E. E. Chufan, K. Kamaraj, K. D. Karlin, Chem. Rev.
2004, 104, 561 – 588.
[6] a) M. C. R. Symons, R. L. Petersen, Biochim. Biophys. Acta
Protein Struct. 1978, 537, 70 – 76; b) R. Kappl, M. Hoehn-
Berlage, J. Huettermann, N. Bartlett, M. C. R. Symons, Biochim.
Biophys. Acta Protein Struct. Mol. Enzymol. 1985, 827, 327 – 343.
[7] a) W. Leibl, W. Nitschke, J. Huttermann, Biochim. Biophys. Acta
Protein Struct. Mol. Enzymol. 1986, 870, 20 – 30; b) R. Davydov,
J. D. Satterlee, H. Fujii, A. Sauer-Masarwa, D. H. Busch, B. M.
Hoffman, J. Am. Chem. Soc. 2003, 125, 16340 – 16346; c) M.
Ibrahim, I. G. Denisov, T. M. Makris, J. R. Kincaid, S. G. Sligar, J.
Am. Chem. Soc. 2003, 125, 13714 – 13718; d) R. Garcia-Serres, R.
Davydov, T. Matsui, M. Ikeda-Saito, B. M. Hoffman, B. H.
Huynh, J. Am. Chem. Soc. 2007, 129, 1402 – 1412; e) M. Unno, H.
Chen, S. Kusama, S. Shaik, M. Ikeda-Saito, J. Am. Chem. Soc.
2007, 129, 13394 – 13395.
[8] a) R. Davydov, A. Ledbetter-Rogers, P. Martasek, M. Larukhin,
M. Sono, J. H. Dawson, B. S. S. Masters, B. M. Hoffman,
Biochemistry 2002, 41, 10375 – 10381; b) R. Davydov, R.
Perera, S. Jin, T.-C. Yang, T. A. Bryson, M. Sono, J. H.
Dawson, B. M. Hoffman, J. Am. Chem. Soc. 2005, 127, 1403 –
1413.
Figure 6. UV/Vis spectra of ferric superoxide [(tmpIm)FeIII(O2À)] (g)
and its [CoCp2] reduction products in the presence of 400 equiv of
methanol (complex 2, c) in EtCN/THF (20:80) at À758C. The inset
shows the EPR spectrum of complex 2 as prepared above.
hydroperoxo compound [(tmpIm)FeIII OOH] can therefore
[9] a) R. Davydov, T. Yoshida, M. Ikeda-Saito, B. M. Hoffman, J.
Am. Chem. Soc. 1999, 121, 10656 – 10657; b) R. Davydov, V.
Kofman, H. Fujii, T. Yoshida, M. Ikeda-Saito, B. M. Hoffman, J.
Am. Chem. Soc. 2002, 124, 1798 – 1808.
[10] a) J. D. Soper, S. V. Kryatov, E. V. Rybak-Akimova, D. G.
Nocera, J. Am. Chem. Soc. 2007, 129, 5069 – 5075; b) N.
Suzuki, T. Higuchi, T. Nagano, J. Am. Chem. Soc. 2002, 124,
9622 – 9628; c) Y. Watanabe, J. Biol. Inorg. Chem. 2001, 6, 846 –
856; d) E. Kim, K. Kamaraj, B. Galliker, N. D. Rubie, P.
Moenne-Loccoz, S. Kaderli, A. D. Zuberbuhler, K. D. Karlin,
Inorg. Chem. 2005, 44, 1238 – 1247.
À
be prepared by using the methods outlined above (Scheme 1).
In summary, efficient methods for preparation of low-spin
end-on ferric hydroperoxo heme species from an imidazole-
tailed porphyrin [(tmpIm)FeII] have been demonstrated. We
have shown for the first time that protonation of a 7c side-on
heme peroxide can switch its spin state from high- to low-spin
and convert the h2 binding mode to a monodentate config-
uration. Furthermore, we succeeded in mimicking the proton-
coupled electron-transfer (PCET) formation of a hydroper-
oxo heme species in a manner similar to that occurring in the
catalytic processes of enzyme systems. The experimental
results suggest that the axial imidazole ligation to the heme is
crucial for O2 activation, which occurs through the formation
of a metastable hydroperoxo species. This model complex will
provide a convenient system for exploring the nature of
unstable hydroperoxo reactive intermediates that are difficult
to observe under ambient catalytic turnover of the enzymes.
Results thus obtained will provide a benchmark for character-
ization and assignment of important hydroperoxo–heme
intermediates.
[11] a) K. Dꢂrr, B. P. Macpherson, R. Warratz, F. Hampel, T. Tuczek,
M. Helmreich, N. Jux, I. Ivanovic-Burmazovic, J. Am. Chem.
Soc. 2007, 129, 4217 – 4228; b) E. E. Chufꢃn, K. D. Karlin, J. Am.
Chem. Soc. 2003, 125, 16160 – 16161; c) D. Mandon, R. Weiss, M.
Franke, E. Bill, A. X. Trautwein, Angew. Chem. 1989, 101, 1747 –
1750; Angew. Chem. Int. Ed. Engl. 1989, 28, 1709 – 1711.
[12] a) J. Annaraj, J. Cho, Y.-M. Lee, S. Y. Kim, R. Latifi, S. P.
de Visser, W. Nam, Angew. Chem. 2009, 121, 4214 – 4217; Angew.
Chem. Int. Ed. 2009, 48, 4150 – 4153; b) W. Nam, Acc. Chem. Res.
2007, 40, 522 – 531; c) D. L. Wertz, J. S. Valentine, Struct. Bond-
ing (Berlin) 2000, 97, 37 – 60, and references therein; d) M. Selke,
J. S. Valentine, J. Am. Chem. Soc. 1998, 120, 2652 – 2653; e) J. N.
Burstyn, J. A. Roe, A. R. Miksztal, B. A. Shaevitz, G. Lang, J. S.
Valentine, J. Am. Chem. Soc. 1988, 110, 1382 – 1388; f) E.
McCandlish, A. R. Miksztal, M. Nappa, A. Q. Sprenger, J. S.
Valentine, J. D. Stong, T. G. Spiro, J. Am. Chem. Soc. 1980, 102,
4268 – 4271. In this paper, preliminary rR characterization of the
side-on heme-peroxide [(dmso)(oep)Fe(O22À)] (oep = octae-
Received: August 17, 2009
Published online: October 30, 2009
thylporphyrin) was attempted, however, the band at 780 cmÀ1
,
Keywords: bioinorganic chemistry · enzyme models ·
À
which was tentatively assigned to n(O O), was significant lower
.
heme proteins · iron · O O activation
than that of the corresponding IR band (806 cmÀ1).
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[13] a) K. Tajima, S. Oka, T. Edo, S. Miyake, H. Mano, K. Mukai, H.
Sakurai, K. Ishizu, J. Chem. Soc. Chem. Commun. 1995, 1507 –
1508; b) K. Tajima, M. Shigematsu, J. Jinno, K. Ishizu, H. Ohya-
Nishihuchi, J. Chem. Soc. Chem. Commun. 1990, 144 – 145; c) K.
Tajima, J. Jinno, K. Ishizu, H. Sakurai, H. Ohya-Nishiguchi,
Inorg. Chem. 1989, 28, 709 – 715; d) M. Rivera, G. A. Caignan,
A. V. Astashkin, A. M. Raitsimring, T. K. Shokhireva, F. A.
Walker, J. Am. Chem. Soc. 2002, 124, 6077 – 6089.
[14] a) J.-G. Liu, Y. Naruta, F. Tani, Angew. Chem. 2005, 117, 1870 –
1874; Angew. Chem. Int. Ed. 2005, 44, 1836 – 1840; b) J.-G. Liu,
Y. Naruta, F. Tani, T. Chishiro, Y. Tachi, Chem. Commun. 2004,
120 – 121; c) J.-G. Liu, Y. Naruta, F. Tani, Chem. Eur. J. 2007, 13,
6365 – 6378; d) T. Chishiro, Y. Shimazaki, F. Tani, Y. Tachi, Y.
Naruta, S. Karasawa, S. Hayami, Y. Maeda, Angew. Chem. 2003,
115, 2894 – 2897; Angew. Chem. Int. Ed. 2003, 42, 2788 – 2791.
[15] a) A. J. Simaan, S. Dopner, F. Banse, S. Bourcier, G. Bouchoux,
A. Boussac, P. Hildebrandt, J.-J. Girerd, Eur. J. Inorg. Chem.
2000, 1627 – 1633; b) G. Roelfes, V. Vrajmasu, K. Chen, R. Y. N.
Ho, J.-U. Rohde, C. Zondervan, R. M. Crois, E. P. Schudde, M.
Lutz, A. L. Spek, R. Hage, B. L. Feringa, E. Mꢂnck, L. Que, Jr.,
Inorg. Chem. 2003, 42, 2639 – 2653; c) F. Neese, E. I. Solomon, J.
Am. Chem. Soc. 1998, 120, 12829 – 12848.
[16] a) I. G. Denisov, P. J. Mak, T. M. Makris, S. G. Sligar, J. R.
Kinkaid, J. Phys. Chem. A 2008, 112, 13172 – 13179; b) P. J. Mak,
I. G. Denisov, D. Victoria, T. M. Makris, T. Deng, S. G. Sligar,
J. R. Kincaid, J. Am. Chem. Soc. 2007, 129, 6382 – 6383; c) M.
Ibrahim, I. G. Denisov, T. M. Makris, J. R. Kincaid, S. G. Sligar, J.
Am. Chem. Soc. 2003, 125, 13714 – 13718; d) T. Kitagawa, M. R.
Ondrias, D. L. Rousseau, M. Ikeda-Saito, T. Yonetani, Nature
1982, 298, 869 – 871.
Angew. Chem. Int. Ed. 2009, 48, 9262 –9267
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