Download Sam P. de Visser,* Jan-Uwe Rohde,* Yong

Coordination Chemistry Reviews 257 (2013) 381–393
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Coordination Chemistry Reviews
journal homepage: www.elsevier.com/locate/ccr
Review
Intrinsic properties and reactivities of mononuclear nonheme iron–oxygen
complexes bearing the tetramethylcyclam ligand
Sam P. de Visser a,∗ , Jan-Uwe Rohde b,∗ , Yong-Min Lee c,d , Jaeheung Cho c,d , Wonwoo Nam c,d,∗∗
a
Manchester Interdisciplinary Biocenter and School of Chemical Engineering and Analytical Science, University of Manchester, 131 Princess Street, Manchester M1 7DN,
United Kingdom
b
Department of Chemistry, The University of Iowa, Iowa City, IA 52242, United States
c
Department of Bioinspired Chemistry, Ewha Womans University, Seoul 120-750, South Korea
d
Department of Chemistry and Nano Science, Ewha Womans University, Seoul 120-750, South Korea
Contents
1.
2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Iron(IV)-oxo complexes of TMC and related macrocyclic ligands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.
Synthesis and characterization of mononuclear nonheme iron(IV)-oxo complexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.
Trans-Influences in [FeIV (O)(TMC)(X)]n+ complexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3.
Reactivities of [FeIV (O)(TMC)(X)]n+ complexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.4.
DFT calculations on iron(IV)-oxo complexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.4.1.
[FeIV (O)(TMC)(X)]n+ complexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.4.2.
A complex of a thiolate-appended TMC ligand, [FeIV (O)(TMCS)]+ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Iron(III)-superoxo species, [FeIII (O2 )(TMC)]2+ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Iron(III)-peroxo and -hydroperoxo complexes, [FeIII (O2 )(TMC)]+ and [FeIII (O2 H)(TMC)]2+ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.
Synthesis, characterization, and interconversion of iron–oxygen intermediates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.
Reactivity comparison . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
a r t i c l e
i n f o
Article history:
Received 17 April 2012
Received in revised form 5 June 2012
Accepted 8 June 2012
Available online 7 July 2012
Dedicated to Prof. Edward I. Solomon on
the occasion of his 65th birthday.
Keywords:
Metalloenzymes
Biomimetics
Oxygen activation
Iron-oxo
Intermediates
Macrocyclic ligands
382
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a b s t r a c t
Iron–oxygen species, such as iron(IV)-oxo, iron(III)-superoxo, iron(III)-peroxo, and iron(III)-hydroperoxo
complexes, are key intermediates often detected in the catalytic cycles of dioxygen activation by
heme and nonheme iron enzymes. Our understanding of the chemistry of these key intermediates
has improved greatly by studies of the structural and spectroscopic properties and reactivities of
their synthetic analogues. One class of biomimetic coordination complexes that has proven to be particularly versatile in studying dioxygen activation by metal complexes is comprised of FeIV O and
FeIII O2 (H) complexes of the macrocyclic tetramethylcyclam ligand (TMC, 1,4,8,11-tetramethyl-1,4,8,11tetraazacyclotetradecane). Several recent advances have been made in the synthesis and isolation of new
iron–oxygen complexes of this ligand, their structural and spectroscopic characterization, and elucidation of their reactivities in various oxidation reactions. In this review, we summarize the chemistry of
the first structurally characterized mononuclear nonheme iron(IV)-oxo complex, in which the FeIV O
group was stabilized by the TMC ligand. Complexes with different axial ligands, [FeIV (O)(TMC)(X)]n+ ,
and complexes of other cyclam ligands are discussed as well. Very recently, significant progress has also
been reported in the area of other iron–oxygen intermediates, such as iron(III)-superoxo, iron(III)-peroxo,
and iron(III)-hydroperoxo complexes bearing the TMC ligand. The present results demonstrate how synthetic and mechanistic developments in biomimetic research can advance our understanding of dioxygen
activation occurring in mononuclear nonheme iron enzymes.
© 2012 Elsevier B.V. All rights reserved.
∗ Corresponding authors.
∗∗ Corresponding author at: Ewha Womans University. Tel.: +82 2 3277 2392; Fax: +82 2 3277 4441.
E-mail addresses: [email protected] (S.P. de Visser), [email protected] (J.-U. Rohde), [email protected] (W. Nam).
0010-8545/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.ccr.2012.06.002
382
S.P. de Visser et al. / Coordination Chemistry Reviews 257 (2013) 381–393
1. Introduction
The cytochromes P450 (CYP 450) are a versatile group of hemebased monooxygenases with vital functions for human health,
including the biodegradation and metabolism of toxic compounds
in the body as well as the biosynthesis of hormones [1–7]. They utilize molecular oxygen at a heme center and react via oxygen atom
transfer to substrates, leading to C H hydroxylation, C C epoxidation, aromatic hydroxylation, and heteroatom oxidation [8,9].
The CYP 450s contain a central heme active site that is linked to
the protein via a thiolate bridge from a cysteinate residue [10,11].
The catalytic cycle of the CYP 450s starts from the resting state
(Fig. 1A) [12–14], where a water molecule fills the sixth binding
position of the metal. Upon substrate binding into the active site,
the water molecule is released and a five-coordinate high-spin ferric species with a vacant coordination site for dioxygen binding is
formed (Fig. 1B). After the reduction of the ferric heme by reduced
putidaredoxin to a five-coordinate high-spin ferrous heme (Fig. 1C),
dioxygen binds to the heme in a ferric-superoxo form (Fig. 1D) and
picks up another electron and proton to form a ferric-hydroperoxo
species (Fig. 1E) that is protonated to give an iron(IV)-oxo heme
␲-cation radical oxidant (Fig. 1F), which is the active species of the
enzyme and also known as Compound I (Cpd I). Due to the high
reactivity and short lifetime of Cpd I, it has been difficult to trap
and characterize it with spectroscopic methods, but recently Rittle
and Green collected the first pieces of evidence from Mössbauer
and UV–vis spectroscopic experiments [15]. However, its participation as active oxidant in the catalytic cycle was inferred from
indirect evidence [16,17] and high-level computational studies
[18–22] for a long time. Until recently, therefore, there was considerable discussion in the literature regarding the active oxidant
in CYP 450 enzymes, where some site-directed mutation studies
seemed to implicate the ferric-hydroperoxo species as active oxidant [23]. A series of computational and experimental biomimetic
studies, however, contradicted this conclusion and reasoned that
Cpd I is a superior oxidant over the ferric-hydroperoxo species at
least in heme enzymes and iron porphyrin models [24–27]. In CYP
450 enzymes, the second reduction step is rate-determining and
dioxygen-bound intermediates are short-lived (see Fig. 1). As a consequence, biochemical studies into the mechanism and reactivity
of Cpd I have been hampered by its short lifetime, and research has
been redirected to biomimetic model complexes instead.
A mononuclear FeIV O species is also believed to be the
key oxidant of nonheme iron enzymes that activate dioxygen
at a mononuclear FeII site. These enzymes carry out substrate
R-H
e–
R-H
FeIII
R-H
H2 O
H2O
hydroxylation, halogenation, and other reactions involving C H
bond activation for a variety of purposes, including biosynthetic functions, DNA repair, and cellular oxygen sensing. Many
of these enzymes, including several ˛-ketoglutarate- (˛KG)
and pterin-dependent oxygenases for which such a high-valent
Fe intermediate has been trapped in recent years, contain a
2His/1carboxylate ligand motif that links the metal to the protein.
The catalytic cycle of one representative enzyme, taurine:˛ketoglutarate dioxygenase (TauD) [7,28–34], is shown in Fig. 2 and
starts from a resting state where the three remaining Fe coordination sites are occupied by water molecules, and upon co-substrate
binding, namely ␣KG, two water molecules are replaced and the
third water molecule is released when substrate (taurine) enters
the binding site (Fig. 2A ). Subsequently, molecular oxygen binds
the metal in the ferric-superoxo form (Fig. 2B ), which is an elusive
intermediate that has been proposed by computational modeling to
attack the ␣-keto position of ␣KG to form a bicyclic ring-structure
(Fig. 2C ) [35,36]. Decarboxylation then leads to a high-valent
iron(IV)-oxo species with succinate bound (Fig. 2D ), which reacts
with substrate via hydrogen atom (H-atom) abstraction from the
substrate to give a ferric-hydroxo complex (Fig. 2E ). Rebound of the
hydroxyl group finally leads to the alcohol product (Fig. 2F ). The
iron(IV)-oxo species, in contrast to Cpd I of the CYP 450s, appears
to have a lifetime that is long enough to enable spectroscopic characterization, and work by Hausinger, Krebs, and Bollinger provided
compelling evidence of its spectroscopic and catalytic properties
[37–39]. In particular, D was characterized by spectroscopic techniques as a high-spin FeIV O species, and its kinetics were followed
spectroscopically. Further studies with deuterated substrate gave
evidence of an elevated kinetic isotope effect for the reaction and
implicated a rate determining H-atom abstraction reaction in the
process. To gain further insights into nonheme iron(IV)-oxo species,
a range of biomimetic model complexes was studied and characterized, which revealed considerable differences in activity between
nonheme iron and heme complexes.
One of the first biomimetic model systems where an iron(IV)oxo species was trapped and characterized structurally was a
mononuclear nonheme iron(IV)-oxo complex of the tetraazamacrocyclic TMC ligand (TMC, 1,4,8,11-tetramethyl-1,4,8,11tetraazacyclotetradecane) [40]. This iron complex has since been
intensely studied, and valuable insights into its physical properties,
axial ligand influences, and reactivities with substrates have been
gained from this work. Furthermore, reactivity studies of several
[FeIV (O)(TMC)(X)]n+ complexes (X = a neutral or anionic ligand),
[FeIII (O2 )(TMC)]+ , and [FeIII (O2 H)(TMC)]2+ have unveiled consid-
S
Cys
O2
FeII
S
B
C
Cys
–
R-H O2
FeIII
S
Cys
FeIII
S
A
Cys
H2O
O H
R-H O
R-OH
FeIV
S
Cys
H+ R-H O
+.
F
e–, H+
FeIII
H2O
S
Cys
E
Fig. 1. Proposed catalytic cycle of cytochrome P450 enzymes.
D
S.P. de Visser et al. / Coordination Chemistry Reviews 257 (2013) 381–393
NH3+
NH3+
-
-
O3S
Asp
His
A'
O
O
FeII
R
O
+O2
O
Asp
His
FeIII
His
α-KG
taurine
B'
O3S
Asp
His
F'
-
O
O
R
O
His
O3S
O
O
Asp
His
FeIV
O
O
C'
CO2
FeII
His
NH3+
NH3+
-
-
OH
O3S
O
R
R
O
His
products
NH3+
-
NH3+
O
O3S
383
Asp
His
O
E'
OH
O3S
O
FeIII
Asp
His
FeIV
His
O
R
O
D'
His
O
R
O
Fig. 2. Proposed catalytic cycle of taurine:˛-ketoglutarate dioxygenase.
erable differences with respect to analogous intermediates in the
catalytic cycle of CYP 450 enzymes. In this review, we will give an
up-to-date overview of experimental and computational studies
of [FeIV (O)(TMC)(X)]n+ , [FeIII (O2 )(TMC)]+ , and [FeIII (O2 H)(TMC)]2+
complexes and their comparison to CYP 450 intermediates.
2. Iron(IV)-oxo complexes of TMC and related macrocyclic
ligands
Among the Fe Ox intermediates supported by the TMC ligand,
the iron(IV)-oxo complex [FeIV (O)(TMC)(NCCH3 )]2+ was the first
to be identified and isolated. Extensive spectroscopic and structural studies of this complex provided detailed insights into its
electronic structure and the intrinsic properties of the FeIV O unit.
Also described in this section are iron(IV)-oxo complexes of other
macrocyclic ligands that are closely related to TMC and complexes
resulting from axial ligand substitution.
The complex was further characterized by peaks in its
electrospray ionization mass spectrum (ESI MS) attributable
to
[FeIV (O)(TMC)(NCCH3 )]2+
and
[FeIV (O)(TMC)(OTf)]+
(OTf− = CF3 SO3 − ), by a 57 Fe Mössbauer quadrupole doublet
having a low isomer shift (ı) of 0.17 mm s−1 , and by an FeO stretching vibration (FeO ) at 835 cm−1 . The value for FeO represents the
average of data obtained by three different vibrational techniques
(i.e., 834 cm−1 by IR, 839 cm−1 by resonance Raman (rRaman), and
831 cm−1 by nuclear resonance vibrational spectroscopy (NRVS)),
which exhibit 18 O-isotope shifts of ca. 35 cm−1 as expected for
a diatomic FeO mode. In addition, NRVS-active FeNeq and FeNax
stretching and OFeNax bending modes were identified in the range
of ca. 300–650 cm−1 [44].
To shed some light on the origin of the unique near-IR
absorption band of [FeIV (O)(TMC)(NCCH3 )]2+ , Decker and Solomon
[45–47] carried out detailed variable-temperature magnetic circular dichroism (VT MCD) spectroscopic studies. From group theory,
five d–d ligand-field transitions are expected for an axially distorted
S = 1 FeIV O complex (C4v , d4 ; Fig. 4). Three bands were observed
2.1. Synthesis and characterization of mononuclear nonheme
iron(IV)-oxo complexes
The [FeIV (O)(TMC)(NCCH3 )]2+ complex was first prepared in
acetonitrile solution by oxygen atom transfer from iodosylbenzene
(PhIO) to the corresponding iron(II) complex, [FeII (TMC)(NCCH3 )]2+
(Eq. (1)). It was readily identified as a new intermediate by a band
in the near-IR region of its absorption spectrum (max = 824 nm).
[FeII (TMC)(NCCH3 )]
2+
+ PhIO −→ [FeIV (O)(TMC)(NCCH3 )]
CH3 CN
2+
+ PhI
(1)
Single crystals of the triflate salt of this highly oxidized complex
were obtained at −40 ◦ C, and its structure was established by Xray crystallography (Fig. 3a), which revealed an Fe O distance of
1.646(3) Å [40]. This very short distance is consistent with strong ␴
and ␲ bonding between the Fe center and the O atom and a formal
bond order of 2 (Fig. 3b). Notably, it is significantly shorter than the
Fe O distances in diiron(III) complexes with bridging oxo ligands
[41,42]. The crystal structure also showed that the FeIV O group
is sterically shielded by the macrocyclic TMC ligand, providing a
rationale for the remarkable stability of this compound (t1/2 ≈ 10 h
at 25 ◦ C) [43].
Fig. 3. Molecular structures of iron(IV)-oxo complexes of the TMC ligand.
(a) Crystallographically determined structure and (b) schematic drawing of
[FeIV (O)(TMC)(NCCH3 )]2+ and (c) crystallographically determined structure of a
Sc3+ -bound FeIV (O)(TMC) complex, [(TMC)FeIV (-O)Sc(OH)(OTf)4 ]. Hydrogen atoms
have been omitted. Carbon, gray; nitrogen, blue; oxygen, red; iron, scarlet; scandium, orange; sulfur, yellow; fluorine, green.
S.P. de Visser et al. / Coordination Chemistry Reviews 257 (2013) 381–393
Energy
384
dz2
Band V
Band IV
dx2–y2
Band I
Band III
dxz/dyz
R
N
R
N
R
N
R
R
N
R
Fig. 4. Ligand-field splitting diagram and spin- and electric-dipole-allowed d–d
transitions for an S = 1 FeIV O complex (C4v ) with assignments of the spectroscopically observed bands.
Extinction Coefficient
–1
–1
(M cm )
in the low-energy region of the MCD spectra (<16 000 cm−1 ) and
assigned to the following three transitions: 3dxy → 3dx2 −y2 (band
I), 3dxy → 3dxz/yz (band II), and 3dxz/yz → 3dx2 −y2 (band III), where
the z axis is defined by the Fe O bond. In support of this assignment,
band II displays a fine structure that could be attributed to a vibronic
progression in the FeO stretching mode, because the excitation of
an electron from a nonbonding orbital (3dxy ) into Fe O ␲* orbitals
(3dxz/yz ) causes a weakening of the Fe O ␲ bond. Two additional
bands associated with 3dxz/yz → 3dz2 (band IV) and 3dxy → 3dz2
transitions (band V) were found at higher energies. By correlating the energies of the bands observed in the MCD and absorption
spectra, the broad feature in the near-IR region of the absorption
spectrum was revealed to be a composite of the three low-energy
d–d transitions (bands I, II, and III), with band III being the most
intense (Fig. 5). On the basis of this analysis, the near-IR absorption band can be viewed as a fingerprint signature of S = 1 FeIV O
complexes.
Several other macrocyclic ligands related to TMC were
successfully used for the generation of mononuclear FeIV O
complexes, including tetradentate ligands with different
substituents and ring sizes (e.g., 14-membered TBC (1,4,8,1115-membered
tetrabenzyl-1,4,8,11-tetraazacyclotetradecane),
TAPM (1,4,8,12-tetramethyl-1,4,8,12-tetraazacyclopentadecane),
and 15-membered TAPH (1,4,8,12-tetraazacyclopentadecane)
[48,49]) as well as pentadentate ligands with neutral and
anionic donor groups (Chart 1; Table 1). One early example,
which actually pre-dates all of the other complexes reviewed
here, is the [FeIV (O)(cyclam-ac)]+ (cyclam-acH = 1,4,8,11tetraazacyclotetradecane-1-acetic acid) complex from Wieghardt’s
group [50] having a carboxylate group appended to the
cyclam scaffold. Noteworthy are also [FeIV (O)(TMC-py)]2+
(TMC-py = 4,8,11-trimethyl-1-(2-pyridylmethyl)-1,4,8,11tetraazacyclotetradecane) reported by Banse and coworkers
[51], which represents another crystallographically characterized
example, and [FeIV (O)(TMCS)]+ (TMCSH = 4,8,11-trimethyl1,4,8,11-tetraazacyclotetradecane-1-ethanethiol) with a pendant
thiolate donor (see Section 2.4.2) [52,53].
Bands I, II & III
0
400
N
N
Band V
Band IV
600
800
1000
Wavelength (nm)
Fig. 5. Electronic absorption spectra of [FeIV (O)(TMC)(NCCH3 )]2+ (black) and
[FeIV (O)(TMC){OC(O)CF3 }]+ (red) in CH3 CN.
R
TAPH, R = H
TAPM, R = Me
TMC, R = Me
TBC, R = Bn
H
200
N
Band II
dxy
400
R
N
H
N
N
N
N
H
cyclam-acH
CO2H
N
N
N
N
R
TMCSH, R = CH2SH
TMC-py, R = C5H4N
Chart 1. Structures of TMC and related macrocyclic ligands.
While PhIO has often been the oxidant of choice for the preparation of iron(IV)-oxo complexes, H2 O2 [40,54], O3 [50], and
peroxycarboxylic acids [53,55] have also been employed. However, H2 O2 may have limited utility, because it also can function
as a reductant toward nonheme iron(IV)-oxo complexes as was
shown very recently [56]. The biologically relevant oxidant (i.e.,
O2 ) has now increasingly been used to access iron(IV)-oxo complexes. In one case, [FeII (TMC)(NCCH3 )]2+ was found to react with
O2 in the presence of alcohols or ethers, where the FeII complex has lower redox potentials than in acetonitrile only [57].
The complex-to-dioxygen stoichiometry of 2:1 was suggestive of
a dinuclear O2 activation pathway proceeding through a (-1,2peroxo)diiron(III) species and subsequent homolytic O–O bond
cleavage to afford two equivalents of the iron(IV)-oxo complex.
Alternatively, [FeII (TMC)(NCCH3 )]2+ could react with O2 in acetonitrile to give [FeIV (O)(TMC)(NCCH3 )]2+ when both a reductant, such
as BPh4 − [51] and NADH (dihydronicotinamide adenine dinucleotide) analogues (e.g., BNAH (1-benzyl-1,4-dihydronicotinamide)
and AcrH2 (10-methyl-9,10-dihydroacridine) derivatives) [58], and
an acid, such as HClO4 , were present. These results indicated that
both an electron and a proton were required for O2 activation (Section 3). Interestingly, [FeIV (O)(TMC)(NCCH3 )]2+ was also generated
from [FeII (TMC)(NCCH3 )]2+ and O2 in the presence of substrates
with weak C H bonds, suggestive of the involvement of hydrogen
atom transfer from the substrate to an iron–oxygen species (Section
3) [59].
Relevant properties of the iron(IV)-oxo complexes reviewed
here, including the [FeIV (O)(TMC)(X)]+ complexes (Section 2.2),
are summarized in Table 1. They generally exhibit (i) characteristic low-intensity bands in the near-IR region with absorption maximum wavelengths ranging from 750 to 900 nm (ε,
100–400 M−1 cm−1 ), (ii) FeO stretching vibrations in the range
of 810–860 cm−1 , and (iii) low 57 Fe Mössbauer isomer shifts (ı)
[60,61]. The large and positive zero-field splittings (D, 20–35 cm−1 )
are consistent with an S = 1 ground state [62,63]. Because the lifetimes of many of these complexes are too short to allow the
growth of single crystals, their metal–ligand distances have been
determined by Fe K-edge EXAFS (extended X-ray absorption fine
structure) analysis, with Fe O distances falling in the range of
1.64(2)–1.70(2) Å. In the pre-edge region of the Fe K-edge X-ray
absorption spectra, the iron(IV)-oxo complexes display relatively
intense peaks associated with 1s → 3d transitions, whose energies
and intensities are sensitive to the oxidation state and coordination geometry, respectively, of the Fe center. The peak energies
(ca. 7114–7115 eV) usually are about 0.5–1 eV higher than those of
related FeIII complexes and about 1–1.5 eV higher than those of the
Table 1
Properties of iron(IV)-oxo complexes of TMC and related macrocyclic ligands.a
Fe O (Å)b
Fe N/O (Å)b , c
Epre-edge (eV)d
XAS pre-edge aread
FeO (cm−1 )e
FeO (cm−1 )e
ı (mm s−1 )
Neutral donor set, [Fe OL5 ]
[FeO(TAPH)(NCCH3 )]2+
[FeO(TMC)(NCCH3 )]2+
1.646
7114.1
26
841
835f
35
35f
0.17
1.24
26.95g
[FeO(TMC)(NCCH3 )]2+ h
[FeO(TMC-py)]2+
1.64
1.667
2.091cis
2.058trans
2.08
2.083cis
2.118trans
826
34
0.14
0.18
0.78
1.08
27.5
29
Complex
IV
b
c
d
e
f
g
h
i
j
D (cm−1 )
max (nm)
Refs.
1.754
2.175cis
1.64
1.67
1.65
2.08
2.07
2.07
7114.2
7114.7
7114.3
31
26
24
854
822
820
37
30
34
1.66
1.66
1.68
2.08
2.08
2.10
7114.4
7114.1
7115.1
24
21
20
814
823
34
34
1.70
1.64
2.09
2.06
7114.3
7114.1
18
25
750
824
[49]
[40]
806, 1026
834
[70]
[51]
[66]
831
0.20
0.16
0.16
0.14
0.17
0.15
0.15
0.01
0.19
0.19
1.39
0.42
0.60
0.61
0.70
0.25
0.16
1.37
–0.22
1.28
31
31
30
31
29
31
31
23
35
Structures of ligands are shown in Chart 1.
Distances from EXAFS are given with three significant figures and distances from X-ray crystallography with four significant figures.
For crystallographically determined Fe N distances, the position of the N atom with respect to the oxo ligand is indicated (cis or trans); average values are given for equatorial Fe N distances.
Fe K-edge XAS pre-edge peak energies, Epre-edge (referenced to an Fe foil calibration point of 7112.0 eV), and intensities (observed peak areas).
From resonance Raman spectroscopy, unless noted otherwise; 18 O-isotope shifts, FeO = (Fe16 O) − (Fe18 O).
Average from IR, resonance Raman, and NRV spectroscopy [40,44,73].
From EPR spectroscopy [63].
Isomer where oxo ligand is oriented syn with the four TMC N-methyl substituents.
Fe OH = 1.94 Å.
Fe S = 2.33 Å.
836, 940, 990
350, 845, 1010
387, 850, 1010
415, 812, 1015
407, 850, 1050
858
830, 1060
676
460, 570, 860
330, 830, 990
[43,73]
[73]
[72,73]
[70]
[72,73]
[73]
[73]
[50]
[52,53]
[53]
S.P. de Visser et al. / Coordination Chemistry Reviews 257 (2013) 381–393
Metal-ion bound, [L4 FeIV (-O)MIII X5 ]
[(TMC)Fe(-O)Sc(OH)(OTf)4 ]h
Monoanionic donor set, trans-[FeIV OL4 X]+
[FeO(TMC){OC(O)CF3 }]+
[FeO(TMC)(NCO)]+
[FeO(TMC)(NCS)]+
[FeO(TMC)(NCS)]+ h
[FeO(TMC)(N3 )]+
[FeO(TMC)(CN)]+
[FeO(TMC)(OH)]+ i
[FeO(cyclam-ac)]+
[FeO(TMCS)]+ j
[FeO(TMCSO2 )]+
a
EQ (mm s−1 )
2+
385
386
S.P. de Visser et al. / Coordination Chemistry Reviews 257 (2013) 381–393
corresponding FeII complexes [64,65]. The increased peak intensities (ca. 20–30 area units) are a consequence of the strong and
covalent Fe O bonding interaction, which results in axial distortion
of the Fe coordination geometry and 3dz2 –4pz mixing.
The structure and reactivity of one FeIV O complex was substantially altered by coordination to a strong Lewis acid. Reaction
of [FeIV (O)(TMC)(NCCH3 )]2+ with Sc(OTf)3 led to the isolation
of the metal-ion bound iron(IV)-oxo complex [(TMC)FeIV (O)Sc(OH)(OTf)4 ] [66]. The crystal structure revealed that the Fe
center is five-coordinate and the oxo ligand occupies the coordination site syn with the four N-methyl substituents of the TMC ligand
(Fig. 3c). The Fe O distance is with 1.754 Å significantly longer than
for the other two crystallographically characterized complexes,
which was attributed to a weakening of the Fe O bond due to
the coordination of the Lewis-acidic ScIII center. Although this distance would also be consistent with an oxo-bridged FeIII complex
[41,42], it is still shorter than the 1.82 Å distance of the FeIV OH
group reported for the protonated compounds II of chloroperoxidase [67,68] and cytochrome P450 119 [69]. Another example of a
syn isomer was characterized spectroscopically [70].
2.2. Trans-Influences in [FeIV (O)(TMC)(X)]n+ complexes
Systematic investigations of the influence of anionic ligands on
the spectroscopic properties of FeIV O complexes were reported
for two series of complexes, [FeIV (O)(TPA)(X)]+ (TPA = tris(2pyridylmethyl)amine) [71] and [FeIV (O)(TMC)(X)]+ [43,72,73],
where the X ligand is coordinated to the FeIV center in cis or trans
position relative to the oxo ligand. These complexes were accessed
by exchange of the neutral solvent ligands in the parent complexes,
[FeIV (O)(TPA)(NCCH3 )]2+ and [FeIV (O)(TMC)(NCCH3 )]2+ .
For the [FeIV (O)(TPA)(X)]n+ complexes with different equatorial ligands, the ligand-field band in the near-IR region shifts to
lower energies (max = 724–800 nm) with decreasing ligand-field
strength of the X ligand according to the spectrochemical series
[71]. On the other hand, the spectral changes caused by axial ligand
substitution in [FeIV (O)(TMC)(NCCH3 )]2+ are more complex as they
involve not only an energy shift but also a redistribution of absorption intensities (Fig. 5). Thus, [FeIV (O)(TMC)(X)]+ complexes with
various carboxylate (X− = CF3 CO2 − and CH3 CO2 − [43,74]) and pseudohalide ligands (X− = NCO− , NCS− , N3 − , CN− , and OH− [70,72,73])
trans to the oxo ligand exhibit max values of 800–860 nm and
broader absorption envelopes with additional peaks that extend
beyond 1000 cm−1 (Table 1). For [FeIV (O)(TMC)(NCCH3 )]2+ and
[FeIV (O)(TMC){OC(O)CF3 }]+ , the perturbations were analyzed by
MCD spectroscopy and attributed to variations in energies and
intensities of two of the five d–d transitions, i.e., 3dxy → 3dxz/yz
(band II) and 3dxz/yz → 3dx2 −y2 (band III), which in turn suggest that the 3dxz/yz orbitals are destabilized by Fe OC(O)CF3 ␲
interactions [46]. Aside from the pronounced modulation of the
FeIV O near-IR signature, some of the [FeIV (O)(TMC)(X)]+ complexes (X− = NCO− , NCS− and N3 − ) as well as [FeIV (O)(TMCS)]+
and [FeIV (O)(TMCSO2 )]+ (TMCSO2 H = 4,8,11-trimethyl-1,4,8,11tetraazacyclotetradecane-1-ethanesulfinic acid) possess distinct
absorption peaks in the UV–vis region that are associated with
charge transfer transitions [53,72,73].
In contrast to the electronic modulation, the Fe O distance was rather insensitive to the identity of the trans ligand
[d(Fe O) = 1.64–1.68 Å for [FeIV (O)(TMC)(X)]n+ ]. The FeO stretching mode proved to be a more sensitive reporter. The values of
FeO span a range of 40 cm−1 and decrease with increasing basicity
of the axial ligand (CF3 CO2 − < CH3 CN < CN− ≈ NCO− ≈ NCS− < N3 − ),
indicating that a stronger trans donor weakens the Fe O bond. A
similar relationship between FeO and donor strength of axial ligand
was reported for iron(IV)-oxo porphyrin complexes [75–77]. The
Aliphatic hydroxylation
Aromatic hydroxylation
OH
Alkylaromatic oxidation
C OH
C H
R
R
S
O
S
N
N
Fe
N
S-oxidation
N
C OH
X
P
C O
H
H3C
Alcohol oxidation
N
H
N + HCHO
P-O
O
P-oxidation
N-dealkylation
Alkene epoxidation
Fig. 6. Oxidation reactions mediated by [FeIV (O)(TMC)(X)]n+ and related nonheme
iron(IV)-oxo complexes.
changes in the FeO value could also be used to estimate changes
in the Fe O distance. Green [78] had previously demonstrated that
Badger’s rule, an empirical relationship between bond length (re )
and stretching frequency (e ), can be applied to the Fe O bonds of
heme and nonheme iron complexes (Eq. (2), where Cij and dij refer
to theoretically derived constants). Based on this relationship, the
40 cm−1 range found for FeO in [FeIV (O)(TMC)(X)]n+ complexes is
correlated with a distance range of 0.02 Å, which is in agreement
with the distances experimentally observed by X-ray crystallography and EXAFS analysis [73].
re =
Cij
(e )2/3
+ dij
(2)
The 57 Fe Mössbauer isomer shifts and XAS (X-ray absorption
spectroscopy) pre-edge peak energies of the [FeIV (O)(TMC)(X)]n+
complexes remain fairly constant and substantiate the FeIV oxidation state assignment. But the quadrupole splittings (EQ ) and
XAS pre-edge peak areas vary with the X ligand, presumably due
to varying extent of axial distortion [73].
2.3. Reactivities of [FeIV (O)(TMC)(X)]n+ complexes
Since [FeIV (O)(TMC)(NCCH3 )]2+ was the first synthetic iron(IV)oxo species to be stabilized and characterized, it led to a variety of
reactivity studies with different substrates. Summarized in Fig. 6
are chemical reactions investigated with [FeIV (O)(TMC)(X)]n+ complexes. Initially, the oxidation of PPh3 by [FeIV (O)(TMC)(NCCH3 )]2+
was studied [40], because it is a facile reaction requiring a small
activation energy. Subsequent studies utilized thioanisole, and its
sulfoxidation by the iron(IV)-oxo complex [26,72,79,80] was investigated giving evidence of a direct oxygen atom transfer mechanism
in line with what was proposed for CYP 450 enzymes [81,82].
Using a selection of para-substituted sulfides, reactivity trends
were determined and the measured rate constants were plotted
as a function of the Hammett parameters, which gave Hammett values between −1.4 and −2.5 [26,80]. These highly negative Hammett values implicate electrophilic character of the Fe O group,
as concluded before for sulfoxidation reactions by other metal-oxo
species [83–85].
Many studies addressed the enzymatically relevant and
mechanistically important reaction of aliphatic C H abstraction by nonheme iron(IV)-oxo complexes. Typical substrates
used in the reactions include alkylaromatic compounds with
weak C H bonds, such as xanthene (BDEC H = 75.5 kcal mol−1 ),
S.P. de Visser et al. / Coordination Chemistry Reviews 257 (2013) 381–393
387
H218O H216O
16
18
O
O
N
N
Fe
N
N
N
Fe
N
N
N
X
X
[FeIV(16O)(TMC)(X)]n+
[FeIV(18O)(TMC)(X)]n+
Scheme 1.
9,10-dihydroanthracene
(DHA,
BDEC H = 77 kcal mol−1 ),
1,4-cyclohexadiene
(BDEC H = 78 kcal mol−1 ),
and
fluorene
(BDEC H = 80 kcal mol−1 ) [86–88]. Due to the relatively low
oxidizing power of many biomimetic nonheme iron(IV)-oxo
complexes, these alkylaromatic compounds turned out to be
excellent substrates for mechanistic studies on C H bond activation reactions [83,89–91]. Studies on the axial ligand effect of
[FeIV (O)(TMC)(X)]n+ in C H abstraction and oxygen atom transfer
reactions highlighted the fact that electron-donating anionic
ligands enhance the H-atom abstraction ability of the iron-oxo
species [92]. A plot of the second-order rate constants against the
BDEC H values of the substrates gave a linear correlation. Moreover,
the reactions proceeded with a high kinetic isotope effect (KIE) of
>10 for hydrogen atom abstraction from xanthene and DHA. The
identity of the axial ligand in [FeIV (O)(TMC)(X)]n+ also affected
reduction potentials and reorganization energies in electron
transfer processes, as different reduction potentials were determined for [FeIV (O)(TMC)(NCCH3 )]2+ (Ered = 0.39 V and = 2.37 eV),
[FeIV (O)(TMC){OC(O)CF3 }]+ (Ered = 0.13 V and = 2.12 eV), and
[FeIV (O)(TMC)(N3 )]+ (Ered = –0.05 V and = 1.97 eV) [93].
As shown in Fig. 6, nonheme iron(IV)-oxo complexes, including
[FeIV (O)(TMC)(X)]n+ , mediate alcohol oxidation, N-dealkylation,
olefin oxidation, and aromatic hydroxylation reactions. The
iron(IV)-oxo complexes activate alcohols exclusively by H-atom
abstraction from the ␣-CH bonds of the alcohols, and the C H
bond cleavage is the rate-determining step [94,95]. The oxidative
N-dealkylation reaction was proposed to occur via an electron
transfer-proton transfer (ET-PT) mechanism [96,97] that proceeds with an initial electron transfer followed by a proton
transfer to give an overall hydrogen atom abstraction. Although
it has been shown that the nonheme iron(IV)-oxo complexes,
[FeIV (O)(TPA)(NCCH3 )]2+ and [FeIV (O)(Bn-TPEN)]2+ (Bn-TPEN = Nbenzyl-N,N ,N -tris(2-pyridylmethyl)ethane-1,2-diamine),
react
with olefins to give the corresponding epoxide products (e.g., the
formation of cyclooctene oxide in the oxidation of cyclooctene)
[49,55,98], the mechanism of the reaction remains elusive. In
aromatic hydroxylation reactions, Nam and co-workers have proposed that the aromatic ring oxidation by [FeIV (O)(TPA)(NCCH3 )]2+
and [FeIV (O)(Bn-TPEN)]2+ does not occur via a H-atom abstraction
mechanism but involves an initial electrophilic attack on the
␲-system of the aromatic ring to produce a tetrahedral radical or
a cationic ␴-complex [99,100].
The [FeIV (O)(TMC)(NCCH3 )]2+ complex was also used in elucidating the mechanism of oxygen exchange between high-valent
metal-oxo species and labeled water (Scheme 1) [101], because
18 O-labeled water experiments have frequently been carried out
to obtain indirect insight into the nature of the reactive intermediates involved in catalytic oxygenation reactions [102–105]. In
this study, direct evidence that nonheme iron(IV)-oxo complexes
exchange their oxygen atom with H2 18 O was obtained for the
first time by monitoring changes of the iron(IV)-oxo species by
electrospray ionization mass spectrometry. The degree of the oxygen exchange depended markedly on the concentration of H2 18 O
and the reaction temperature but not on the presence of a trans
axial ligand. Thus, a mechanism for the oxygen-atom exchange in
Fig. 7. Molecular orbitals of [FeIV (O)(TMC)(Cl)]+ .
nonheme iron(IV)-oxo models was proposed that does not proceed via the trans oxo-hydroxo tautomerism pathway proposed for
high-valent metal-oxo porphyrins [106] but by a variant involving
a cis-dihydroxoiron(IV) transition state.
2.4. DFT calculations on iron(IV)-oxo complexes
2.4.1. [FeIV (O)(TMC)(X)]n+ complexes
To understand the reactivity patterns of the [FeIV (O)(TMC)(X)]n+
complexes and in particular the effect of the axial ligand on the reaction rates and mechanisms, a series of detailed density functional
theory (DFT) calculations were done and established two-statereactivity type mechanisms [107–109]. High-lying occupied and
low-lying virtual orbitals of [FeIV (O)(TMC)(Cl)]+ are shown in Fig. 7.
The lowest metal 3d orbital is the ␲*xy orbital that is located in the
plane of the nitrogen atoms of the TMC ring and is nonbonding and
doubly occupied. Slightly higher in energy are a pair of degenerate ␲*FeO orbitals for the antibonding interactions of 3dxz/yz on iron
with 2px/y on the oxygen atom. With a halide as an axial ligand,
these two orbitals also mix with 3px/y atomic orbitals on the halide,
which is absent with neutral ligands such as acetonitrile. Higher
lying and virtual are the ␴∗2 orbital for the antibonding interactions
z
along the Fe O bond and the ␴∗2 2 orbital for the antibonding
x −y
interaction of the metal with the nitrogen atoms of the TMC group.
Experimental studies characterized all [FeIV (O)(TMC)(X)]n+ intermediates irrespective of the axial ligand as triplet spin states with
2
1
1
␲∗xy ␲∗xz ␲∗yz orbital occupation. Higher in energy is a quintet spin
2
1
1
1
state with ␲∗xy ␲∗xz ␲∗yz ␴∗2
x −y2
configuration, which is the ground
state in enzymatic nonheme iron(IV)-oxo complexes [110]. DFT calculations generally give the triplet and quintet spin state close in
energy and environmental perturbations and/or solvent effect can
change their ordering and relative energies slightly.
Subsequently, the H-atom abstraction ability of the
[FeIV (O)(TMC)(X)]n+ complexes was calculated with DFT methods
using a range of model substrates [107–109], and Fig. 8 displays
the aliphatic hydroxylation mechanism of the benzyl position of
ethylbenzene by [FeIV (O)(TMC)(X)]n+ (X = NCCH3 or Cl− ) with data
taken from ref 109. The reaction starts from a reactant complex
(R) between iron(IV)-oxo species and substrate and proceeds
with a H-atom abstraction via a transition state (TSHA ) leading
to an iron(III)-hydroxo with a nearby radical (A). Rebound of the
hydroxo group to the ethylbenzene radical restgroup is barrierless
and leads to alcohol products (PA ). The overall exothermicity
388
S.P. de Visser et al. / Coordination Chemistry Reviews 257 (2013) 381–393
Fig. 8. Free energy profile for aliphatic hydroxylation of the benzyl position in ethylbenzene by [FeIV (O)(TMC)(NCCH3 )]2+ and [FeIV (O)(TMC)(Cl)]+ . Free energies are in
kcal mol−1 relative to a reactant complex in the quintet spin state, whereas bond lengths are in angstroms, angles in degrees and the imaginary mode in the transition state
in wavenumbers.
is large for the oxidant with X = NCCH3 but considerably less
than that for X = Cl− . This affects the complete reaction pathway,
whereby all barriers and intermediates are lower in energy for
the reaction starting with [FeIV (O)(TMC)(NCCH3 )]2+ as compared
to those starting with [FeIV (O)(TMC)(Cl)]+ . Note that although the
triplet spin reactants are the ground state, actually the mechanism
takes place on the quintet spin state, which implies a spin state
crossing from triplet to quintet prior to the H-atom abstraction.
Thus, in the triplet spin state the electron transfer fills a ␲*
orbital with a second electron, whereas in the quintet spin state
a complete exchange stabilized metal 3d-system is formed that
results in favorable high-spin over intermediate-spin reactivity.
Nevertheless, the DFT calculations confirm the conclusions derived
from experiment that [FeIV (O)(TMC)(NCCH3 )]2+ is a better oxidant
than [FeIV (O)(TMC)(Cl)]+ in H-atom abstraction reactions.
Optimized geometries are typical for structures calculated for
H-abstraction barriers for a range of substrates and iron(IV)oxo oxidants [111–119] and show that the substrate attacks the
iron(IV)-oxo group from the top. This follows from the electron
transfer processes, whereby an electron is shuttled from substrate
into the ␴∗2 orbital along the Fe O bond [120]. The imaginary
frequencies in the transition state are large (>i900 cm−1 ), which
implicates that the reaction will proceed with a considerable
kinetic isotope effect and tunneling [114,115,121]. Despite the
fact that both rate determining transition states 5 TSHA,NCCH3 and
5 TS
HA,Cl refer to a H-atom abstraction barrier with significant radical character on the substrate, the intermediates show considerable
differences in electron occupation. Thus, 5 ACl is a radical intermedi∗1 1
∗1 ∗1 ∗1 ∗1
ate with xy
xz yz
2
2 2 sub configuration with an S = 2 on the
x −y
z
metal antiferromagnetically coupled to a substrate radical. On the
other hand, 5 ANCCH3 represents a cationic intermediate that is the
result of a formal hydride transfer from substrate to oxo group with
∗1 0
∗2 ∗1 ∗1 ∗1
xy
xz yz
2
2 2 sub configuration. Note that the second elecx −y
z
tron transfer that is part of the hydride transfer is only transferred
after the transition state and en route to the intermediate.
Another process studied in detail relates to the aromatic hydroxylation of arenes by [FeIV (O)(TMC)(X)]n+ complexes. An example
of two calculated energy profiles of ethylbenzene hydroxylation
by [FeIV (O)(TMC)(NCCH3 )]2+ and [FeIV (O)(TMC)(Cl)]+ are shown in
Fig. 9. The mechanisms are the same irrespective of the axial ligand and follow a mechanism devised for Cpd I of CYP 450 [100,122]
z
Fig. 9. Free energy profile for aromatic hydroxylation of the para-position of ethylbenzene by [FeIV (O)(TMC)(NCCH3 )]2+ and [FeIV (O)(TMC)(Cl)]+ . Free energies are in kcal mol−1
relative to a reactant complex in the quintet spin state, whereas bond lengths are in angstroms, angles in degrees and the imaginary mode in the transition state in
wavenumbers.
S.P. de Visser et al. / Coordination Chemistry Reviews 257 (2013) 381–393
with an electrophilic addition leading to a ␴-complex (B) via a transition state TSarom . Thereafter, the ipso-proton is reshuttled to one
of the nitrogen atoms of the TMC ring to form a phenolate bound
to iron(III) with a protonated TMC ligand. Rebound of the proton to
phenolate gives phenol products (PB ). The latter steps proceed fast
and with virtually no barrier heights, so that the initial barrier via
TSarom is rate determining. The imaginary frequencies in the transition states are considerably lower than those found for hydrogen
atom abstraction reactions and lead to almost no or slightly inverse
kinetic isotope effects.
Although the mechanistic features of the reactions starting with
[FeIV (O)(TMC)(NCCH3 )]2+ and [FeIV (O)(TMC)(Cl)]+ are the same,
there are considerable differences in electronic properties along the
reaction mechanism. Thus, in analogy to the H-abstraction barriers
discussed above, the initial electrophilic addition leads to a single
electron transfer from the arene to the metal and gives partial radical character of the arene in the transition state. With Cl− as axial
ligand, this state relaxes to a radical intermediate (5 BCl ), whereas a
second electron transfer takes place en route from 5 TSarom,NCCH3 to
form a cationic intermediate 5 BNCCH3 . These differences in radical
versus cationic pathways were allocated to differences in orbital
energy level of the ␲*xy orbital, which is higher in energy for RCl
and thereby affects the electron affinity of the oxidant and consequently the electron transfer processes. Therefore, the axial ligand
has a profound effect on the orbital energy levels and in particular the one involving metal 3d-interactions. It affects the spin state
ordering and energies as well as the electron abstraction ability of
the oxidant. As such, it has a dominant effect on reactivity patterns.
studies
on
the
relative
reactivities
of
Further
[FeIV (O)(TMC)(X)]n+ complexes in H-atom abstraction and oxygen
atom transfer reactions found computational trends according
to the electrophilicity of the oxidant [123]. At first glance, these
studies seemed to contradict experiment; however, when blending of rate constants for triplet and quintet states was taken into
account, the correct trends were observed. This implies that full
spin equilibration occurs and that the spin orbit coupling between
the triplet and quintet spin states may affect rate constants and
reactivity patterns.
2.4.2. A complex of a thiolate-appended TMC ligand,
[FeIV (O)(TMCS)]+
Comparative studies by Dawson and co-workers [124] on peroxidase and CYP 450 enzymes highlighted differences in the axial
ligand bound to the heme, whereby the axial thiolate ligand in the
CYP 450 s was proposed to induce a ‘push-effect’, but the axial
histidine ligand in peroxidases gives a ‘pull-effect’ of electrons.
Since then many studies on iron porphyrins have tried to quantify the axial ligand effect [66,125–127]. In particular, Gross and
Nimri [125] found a trans-influence of the axial ligand that affected
spectroscopic parameters including FeO stretching frequencies as
well as a trans-effect on the rate constants of styrene epoxidation. Subsequently, Nam and co-workers have demonstrated
that iron(IV)-oxo porphyrin ␲-cation radicals, [FeIV (O)(Porp+• )(Cl)]
and [FeIV (O)(Porp+• )(NCCH3 )]+ , exhibit different reactivity patterns
depending on the identity of the axial ligand, as shown, for example,
in the selectivity for cis- versus trans-olefins in olefin epoxidation,
the oxidizing power in alkane C H bond activation, and the regioselectivity of aromatic ring versus aliphatic C H hydroxylation in the
oxidation of ethylbenzene [128–131]. These results demonstrate
unambiguously that iron(IV)-oxo porphyrin ␲-cation radicals can
exhibit diverse reactivity patterns under different circumstances.
To understand the ligand binding in CYP 450 enzymes and
to mimic this in synthetic analogs, many attempts have been
made to create biomimetic model complexes with axial thiolate
ligation. One of the first successfully characterized iron(IV)-oxo
species with axially ligated thiolate was the [FeIV (O)(TMCS)]+
389
[FeII(TMC)(NCCH3)]2+ + O2
e–, H+
[FeIII(O2)(TMC)]2+
A
B
[FeIII(O2H)(TMC)]2+
iron(III)-hydroperoxo
iron(III)-superoxo
R-H R
C
[FeIV(O)(TMC)(NCCH3)]2+ + HO
Scheme 2.
complex [52]. Subsequently, this led to a series of experimental and computational studies into the reactivities of
[FeIV (O)(TMCS)]+ .
Computational modeling established the electronic properties
of [FeIV (O)(TMCS)]+ and studied C H abstraction and double bond
epoxidation with propene as a model substrate [120]. In contrast
to the [FeIV (O)(TMC)(X)]n+ models described above, calculations
on [FeIV (O)(TMCS)]+ identified it as a high-spin (quintet) ground
state slightly below the experimentally assigned triplet spin ground
state. Thus, the triplet-quintet energy gap is determined by the
relative energies of the ␲*xy and ␴∗2 2 molecular orbitals and
x −y
when the energy gap narrows the quintet spin state drops below
the triplet in energy [123]. In particular, in five-coordinate complexes including the enzymatic nonheme iron(IV)-oxo species, the
␲∗xy /␴∗2 2 energy gap is small and a high-spin state is found as the
x −y
ground state. Another facet of this spin state ordering is the fact that
[FeIV (O)(TMCS)]+ reacts via single-state-reactivity on a quintet spin
state surface only.
Thereafter, a comparative study on the regioselectivity of
aliphatic hydroxylation versus epoxidation by [FeIV (O)(TMCS)]+
and [FeIV (O)(Porp+• )(SH)] was performed. Gas-phase epoxidation
barriers were a few kcal mol−1 lower in energy than H-atom
abstraction barriers from propene by [FeIV (O)(Porp+• )(SH)]. On the
other hand, reactivity of propene with [FeIV (O)(TMCS)]+ gave dominant H-atom abstraction reaction instead. This was explained from
stereochemical interactions of hydrogen atoms of the TMCS ring
with the approaching substrate, whereby the substrate is closer in
the epoxidation transition states than in the H-atom abstraction
transition states.
3. Iron(III)-superoxo species, [FeIII (O2 )(TMC)]2+
Dioxygen activation by a high-spin iron(II) complex in the presence of electron and proton sources in CH3 CN was reported by Nam
and co-workers [58]. In this reaction, [FeIV (O)(TMC)(NCCH3 )]2+
was generated from [FeII (TMC)(NCCH3 )]2+ and O2 in the presence
of NADH analogues, such as BNAH and AcrH2 derivatives, as an
electron source and HClO4 as a proton source in CH3 CN. The mechanism proposed for O2 activation is as follows: The reaction is
initiated by binding of O2 to the high-spin iron(II) complex, producing an iron(III)-superoxo species. Subsequently, iron(III)-peroxo
and iron(III)-hydroperoxo species are generated by consecutive
electron- and proton-transfer reactions (Scheme 2, pathway A).
Finally, homolytic O O bond cleavage affords the iron(IV)-oxo
species (Scheme 2, pathway C) [91]. It was also reported by Nam
and co-workers that [FeIV (O)(TMC)(NCCH3 )]2+ could be generated
in the reaction of [FeII (TMC)(NCCH3 )]2+ and O2 in the presence
of substrates with weak C H bonds (e.g., olefins, such as cyclohexene and cyclooctene, and alkylaromatic compounds, such as
xanthene and 9,10-dihydroanthracene) [59]. In this reaction, an
iron(III)-superoxo intermediate was proposed as an active oxidant
that abstracts a H-atom from the substrate (Scheme 2, pathway
B). Especially, when the substrates were olefins (e.g., cyclohexene
390
S.P. de Visser et al. / Coordination Chemistry Reviews 257 (2013) 381–393
and cyclooctene), [FeIV (O)(TMC)(NCCH3 )]2+ was formed in a high
yield because of its low reactivity toward these olefins. In
these reactions, the formation of [FeIV (O)(TMC)(NCCH3 )]2+ was
faster with olefins having lower C H bond dissociation energies [132]; the second-order rate constants for cyclohexene
(BDE = 81 kcal mol−1 ) and cyclooctene (BDE = 85 kcal mol−1 ) were
1.2 M−1 s−1 and 2.9 × 10−1 M−1 s−1 , respectively. Furthermore, a
kinetic isotope effect (KIE) value of 6.3(3) in the formation of
[FeIV (O)(TMC)(NCCH3 )]2+ was obtained using cyclohexene and
cyclohexene-d10 as substrates. These results indicated that the
C H bond activation of the olefin by an iron(III)-superoxo species,
[FeIII (O2 )(TMC)]2+ , is the rate-determining step in the formation of
[FeIV (O)(TMC)(NCCH3 )]2+ (Scheme 2, pathway B) [59].
DFT calculations were performed on the H-atom abstraction from cyclohexadiene by [FeIV (O)(TMC)(NCCH3 )]2+ and
[FeIII (O2 )(TMC)]2+ [133]. For [FeIV (O)(TMC)(NCCH3 )]2+ , Habstraction barriers of 19.7 and 10.6 kcal mol−1 were found for the
triplet and quintet spin states, respectively. In contrast to experimental results, however, the barrier heights for H-abstraction from
cyclohexadiene by [FeIII (O2 )(TMC)]2+ are well higher in energy.
This was explained by differences in spin-inversion-probability,
whereby the iron(IV)-oxo intermediate stays on the more
endothermic triplet spin state, whereas the iron(III)-superoxo
intermediate can relax to a more reactive spin state surface.
Apart from studies on iron(III)-superoxo intermediates, calculations also were performed on iron(II)-superoxo, [FeII (O2 )(TMC)]+ ,
and nickel(II)-superoxo, [NiII (O2 )(TMC)]+ , intermediates and their
reactivities with substrates [134,135]. The iron(II)-superoxo complex was found to be a sluggish oxidant in aromatic hydroxylation
reactions but capable of reacting with aliphatic C H substrates on
a sextet spin state surface with low barriers [135]. Barrier heights
for analogous processes catalyzed by [NiII (O2 )(TMC)]+ were even
higher and it was only found to be a suitable oxidant for substrates
with weak C H bonds (e.g., xanthene or cyclohexadiene) and PPh3
[134].
4. Iron(III)-peroxo and -hydroperoxo complexes,
[FeIII (O2 )(TMC)]+ and [FeIII (O2 H)(TMC)]2+
4.1. Synthesis, characterization, and interconversion of
iron–oxygen intermediates
An iron(III)-peroxo complex, [FeIII (O2 )(TMC)]+ , was prepared
by reacting the corresponding iron(II) complex with H2 O2 in
the presence of base [91,136]. The blue intermediate persisted
for several hours at 0 ◦ C, and the greater thermal stability of
[FeIII (O2 )(TMC)]+ allowed for the isolation of crystals, which were
used for a structure determination and spectroscopic and reactivity studies. The electronic absorption spectrum of [FeIII (O2 )(TMC)]+
shows a distinct absorption band at 750 nm (ε = 600 M−1 cm−1 ).
The rRaman spectrum of the iron(III)-peroxo complex, obtained
upon 778-nm excitation in acetone-d6 at 77 K, exhibits two 18 Oisotope-sensitive bands at 825 and 487 cm−1 . The X-ray crystal
structure of [FeIII (O2 )(TMC)]ClO4 revealed a mononuclear iron
complex with a side-on bound O2 2− ligand. The iron center is
coordinated in a distorted octahedral geometry arising from the triangular FeOO moiety with a small bite angle of 45.03(17)◦ (Fig. 10a).
The FeOO geometry is similar to that of the crystallographically
characterized 1:1 Fe/O2 adduct of naphthalene dioxygenase (NDO),
where dioxygen binds side-on to the iron center in the active
site (1.75 Å resolution, rO O ≈ 1.45 Å) [137]. Furthermore, the structurally determined O O distance of 1.463(6) Å and the rRaman data
are indicative of peroxo character of the OO group [138–140]. It
is worth noting that all four N-methyl groups point to the same
side of the FeN4 plane as the peroxo moiety, as observed in other
Fig. 10. Molecular structures of iron–oxygen complexes of the TMC ligand. (a)
Crystallographically determined structure of the ‘side-on’ iron(III)-peroxo complex,
[FeIII (O2 )(TMC)]+ , and (b) DFT optimized structure of the ‘end-on’ iron(III)hydroperoxo complex, [FeIII (O2 H)(TMC)]2+ . Hydrogen atoms have been omitted
except for that of the hydroperoxo group. Carbon, gray; nitrogen, blue; oxygen, red;
hydrogen, cyan; iron, scarlet.
metal(III)-peroxo complexes [141–143]. In the case of the Sc3+ bound iron(IV)-oxo complex, [(TMC)FeIV (-O)Sc(OH)(OTf)4 ], the
N-methyl groups are also syn with the oxo ligand (Fig. 3c) [66],
whereas those in [FeIV (O)(TMC)(NCCH3 )]2+ are anti to the oxo ligand (Fig. 3a) [40]. In addition, no axial ligand binds to the Fe
ion trans to the peroxo ligand in [FeIII (O2 )(TMC)]+ , which is similar to other metal(III)-peroxo complexes [141–143] as well as
the Sc3+ -bound FeIV (O)(TMC) complex [66], but different from the
[FeIV (O)(TMC)(NCCH3 )]2+ complex [40].
Addition of a slight excess amount of HClO4 to a solution of
[FeIII (O2 )(TMC)]+ in acetone/CF3 CH2 OH (3:1) at −40 ◦ C immediately produced a violet intermediate, [FeIII (O2 H)(TMC)]2+
(Fig. 10b). Subsequently, this iron(III)-hydroperoxo species
was converted to the corresponding iron(IV)-oxo complex,
[FeIV (O)(TMC)]2+ (Scheme 3). The iron(III)-hydroperoxide complex,
[FeIII (O2 H)(TMC)]2+ , was characterized using a variety of spectroscopic methods; the EPR spectrum of a frozen acetone/CF3 CH2 OH
(3:1) solution of the complex measured at 10 K shows signals
at g = 6.8, 5.2, and 1.96, which is consistent with a high-spin
(S = 5/2) FeIII species [144,145]. The rRaman spectrum of the
[FeIII (O2 H)(TMC)]2+ complex exhibits two 18 O-isotope-sensitive
bands at 658 and 868 cm−1 for the FeO and OO stretching vibrations, respectively [91]. The structural information obtained by
XAS/EXAFS and DFT calculations indicates that an end-on, highspin [FeIII (O2 H)(TMC)]2+ complex with syn orientation of OOH−
and N-methyl groups does not bind a solvent ligand trans to the
OOH− ligand [91].
Concerning the conversion of [FeIII (O2 H)(TMC)]2+ into
IV
[Fe (O)(TMC)]2+ , two plausible mechanisms are considered
for hydroperoxide O O bond cleavage in [FeIII (O2 H)(TMC)]2+ :
One involves heterolytic O O bond cleavage to generate an
FeV O species, followed by one-electron reduction to give the
FeIV O complex (Scheme 4, pathways A and B). The second
possible mechanism involves homolytic O O bond cleavage in
[FeIII (O2 H)(TMC)]2+ to afford [FeIV (O)(TMC)]2+ and a hydroxyl
radical (Scheme 4, pathway C). Que and co-workers have proposed
the former mechanism based on the observation that the formation
rate of [FeIV (O)(TMC)]2+ from [FeIII (O2 H)(TMC)]2+ in CH3 CN solution was accelerated with increasing proton concentration [146]. In
contrast, Nam and co-workers have proposed the homolytic O O
bond cleavage mechanism based on the observation that the rate of
hydroperoxo O O bond cleavage in [FeIII (O2 H)(TMC)]2+ was independent of the proton concentration for the acetone/CF3 CH2 OH
solvent system [91]. Additional evidence in support of the O O
bond homolysis mechanism was obtained by carrying out reactions in the presence and absence of substrates; the yields of the
[FeIV (O)(TMC)]2+ product formed in the presence and absence
of substrates were the same (Scheme 4, pathways A and D),
S.P. de Visser et al. / Coordination Chemistry Reviews 257 (2013) 381–393
N
FeIII
N
OH
+
O O
N
2+
O
+H+
N
N
N
FeIII
N
2+
O
N
–HO•
N
391
N
FeIV
N
N
Iron(III)-peroxo
Iron(III)-hydroperoxo
Iron(IV)-oxo
nucleophilic
deformylation
• nucleophilic • electrophilic
deformylation oxidation
electrophilic
oxidation
Scheme 3.
suggesting that a highly reactive iron(V)-oxo species was not
generated in the O O bond cleavage of [FeIII (O2 H)(TMC)]2+ [91].
4.2. Reactivity comparison
The reactivities of the iron(III)-peroxo and iron(III)-hydroperoxo
complexes were examined in both nucleophilic and electrophilic
reactions and then compared to those of the iron(IV)-oxo
complex (Scheme 3). When the nucleophilic character of the
three intermediates, [FeIII (O2 )(TMC)]+ , [FeIII (O2 H)(TMC)]2+ , and
[FeIV (O)(TMC)(NCCH3 )]2+ , was tested in aldehyde deformylation reactions [147], the iron(III)-hydroperoxo species
showed the greatest reactivity in the deformylation of 2phenylpropionaldehyde (2-PPA), and the reactivity order of
[FeIII (O2 H)(TMC)]2+ > [FeIII (O2 )(TMC)]+ > [FeIV (O)(TMC)(NCCH3 )]2+
was
observed
[91].
Interestingly,
formation
of
[FeIV (O)(TMC)(NCCH3 )]2+ was observed in the reaction of
[FeIII (O2 H)(TMC)]2+ and 2-PPA, proposing that the reaction is
initiated via the nucleophilic attack of the iron(III)-hydroperoxo
species on the carbonyl carbon of 2-PPA, followed by O O bond
cleavage of the peroxohemiacetal leading to the formation of
the iron(IV)-oxo species [91]. The high reactivity of the iron(III)hydroperoxo species in nucleophilic reactions, compared to
the side-on iron(III)-peroxo species (i.e., [FeIII (O2 )(TMC)]+ ), was
ascribed to the end-on binding mode of the hydroperoxo ligand [147,148]. The reactivity of [FeIII (O2 H)(TMC)]2+ was further
investigated using primary (1◦ -CHO), secondary (2◦ -CHO), and
tertiary (3◦ -CHO) aldehydes, and the observed reactivity order of
1◦ -CHO > 2◦ -CHO > 3◦ -CHO supports the nucleophilic character of
the iron(III)-hydroperoxo species.
The electrophilic character of the iron(III)-peroxo, iron(III)hydroperoxo, and iron(IV)-oxo complexes was also investigated in
the oxidation of alkylaromatic compounds with weak C H bonds,
such as xanthene and 9,10-dihydroanthracene. While the iron(III)peroxo complex did not show any significant spectral changes
upon addition of the substrates, the iron(III)-hydroperoxo and
iron(IV)-oxo complexes reacted with DHA, showing that these
iron–oxygen intermediates are capable of abstracting an H-atom
3+
O
Š
OH
H
O
O
2+
III
Fe
[FeIII(O2H)(TMC)]2+
FeV
V
[Fe (O)(TMC)]3+
A
C
B
FeIII
2+
FeIV
IV
[Fe (O)(TMC)]2+
Scheme 4.
Prod-[O]
D
eŠ
O
OH
Sub
3+
from DHA with similar reactivity in this C H bond activation
reaction. Thus, as summarized in Scheme 3, the iron(III)-peroxo
and iron(IV)-oxo complexes show reactivities in nucleophilic and
electrophilic reactions, respectively. Interestingly, the high-spin
iron(III)-hydroperoxo complex is an active oxidant in both nucleophilic and electrophilic reactions.
Recent comparative studies on the reactivity of nonheme
iron(III)-hydroperoxo and iron(IV)-oxo with an N4Py (N,N-bis(2pyridylmethyl)-N-[bis(2-pyridyl)methyl]amine or Bn-TPEN ligand
system in substrate halogenation reactions showed higher activity
for the nonheme iron(III)-hydroperoxo than for the iron(IV)oxo complexes [149]. Thus, the reaction of tetrabutylammonium
bromide with iron(III)-hydroperoxo complexes resulted in the formation of OBr− with rate constants that were three orders of
magnitude higher than those for reactions with the corresponding iron(IV)-oxo complexes. DFT studies confirmed the reaction
processes and showed that the nonheme iron(III)-hydroperoxo
species is a potential oxidant. The origin of the reactivity differences
between heme and nonheme iron(III)-hydroperoxo was assigned
to differences in spin states, whereby the nonheme iron(III)hydroperoxo complex has a high-spin ground state, whereas it
is low-spin for the heme-based iron(III)-hydroperoxo complex,
thereby making the former species more reactive. These studies have thus highlighted critical differences between heme and
nonheme iron(III)-hydroperoxo versus iron(IV)-oxo intermediates,
where the heme iron(III)-hydroperoxo species was found to be a
sluggish oxidant [24–27].
5. Conclusion
In recent years, considerable new insights into the intrinsic properties of nonheme metal–oxygen complexes have been
gained through a combination of experimental and computational techniques. Thus, short-lived catalytic cycle intermediates,
such as the iron(IV)-oxo, iron(III)-superoxo, iron(III)-peroxo, and
iron(III)-hydroperoxo species, were synthesized and spectroscopically characterized using biomimetic nonheme ligand systems. The
most successful set of data to date has come from the nonheme
iron system with the TMC ligand [9,150–152]. A range of different
structures were stabilized and characterized and detailed reactivity patterns with a selection of substrate types were investigated.
A clear picture is now starting to emerge surrounding the activity
of enzymatic catalytic cycle intermediates and the potency of oxidants. The TMC ligand system with its tetradentate coordination
also enabled studies of the influences/effects of axial ligands on the
spectroscopic properties and reactivity of FeIV O intermediates.
Furthermore, comparisons between heme and nonheme iron
systems have been made and remarkable differences have been
discovered. In particular, studies of biomimetic porphyrin complexes, where Cpd I was found to be the only viable oxidant in
oxygen atom transfer reactions, have suggested the existence of
a single active oxidant in heme enzymes, such as the cytochromes
392
S.P. de Visser et al. / Coordination Chemistry Reviews 257 (2013) 381–393
P450. By contrast, recent evidence from nonheme iron based superoxo and hydroperoxo complexes revealed reactivity patterns that
are considerably different from those of their heme analogues with
occasionally higher reactivities for these intermediates than for the
corresponding iron(IV)-oxo complexes. Future studies into the differences and comparisons of heme and nonheme iron oxygenases
are expected to give further insights into the chemistry of these
important enzymes.
Acknowledgments
WN acknowledges the financial support from NRF/MEST of
Korea through the CRI (W.N.), GRL (2010-00353), and WCU (R312008-000-10010-0) programs.
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