Fe(III) Protoporphyrin IX Encapsulated in a Zinc Metal-Organic Framework Shows Dramatically Enhanced Peroxidatic Activity

Article abstract of DOI:10.1021/acs.inorgchem.7b02612

Two MOFs, [H₂N(CH₃)₂][Zn₃(TATB)₂(HCOO)]·HN(CH₃)₂·DMF·6H₂O (1) and Zn-HKUST-1 (2), were investigated as potential hosts to encapsulate Fe(III) heme (Fe(III) protoporphyrin IX = Fe(III)PPIX). Methyl orange (MO) adsorption was used as an initial model for substrate uptake. MOF 1 showed good adsorption of MO (10.3 ± 0.8 mg g^-1) which could undergo in situ protonation upon exposure to aqueous HCl vapor. By contrast, MO uptake by 2 was much lower (2 ± 1 mg g^-1), and PXRD indicated that structural instability on exposure to water was the likely cause. Two methods for Fe(III)PPIX-1 preparation were investigated: soaking and encapsulation. Encapsulation was verified by SEM-EDS and showed comparable concentrations of Fe(III)PPIX on exposed interior surfaces and on the original surface of fractured crystals. SEM-EDS results were consistent with ICP-OES data on bulk material (1.2 ± 0.1 mass % Fe). PXRD data showed that the framework in 1 was unchanged after encapsulation of Fe(III)PPIX. MO adsorption (5.8 ± 1.2 mg g^-1) by Fe(III)PPIX-1 confirmed there is space for substrate diffusion into the framework, while the UV-vis spectrum of solubilized crystals confirmed that Fe(III)PPIX retained its integrity. A solid-state UV-vis spectrum of Fe(III)PPIX-1 indicated that Fe(III)PPIX was not in a μ-oxo dimeric form. Although single-crystal XRD data did not allow for full refinement of the encapsulated Fe(III)PPIX molecule owing to disorder of the metalloporphyrin, the Fe atom and pyrrole N atoms were located, enabling rigid-body modeling of the porphine core. Reaction of 2,2′-azino-bis(3-ethylbenzothiazoline)-6-sulfonic acid (ABTS) with H₂O₂, catalyzed by Fe(III)PPIX-1 and -2, showed that Fe(III)PPIX-1 is significantly more efficient than Fe(III)PPIX-2 and is superior to solid Fe(III)PPIX-Cl. Fe(III)PPIX-1 was used to catalyze the oxidation of hydroquinone, thymol, benzyl alcohol, and phenyl ethanol by tert-butyl-hydroperoxide with t_1/2 values that increase with increasing substrate molecular volume.

Full text of DOI:10.1021/acs.inorgchem.7b02612

Article
pubs.acs.org/IC
Cite This: Inorg. Chem. XXXX, XXX, XXX−XXX
Fe(III) Protoporphyrin IX Encapsulated in a Zinc Metal−Organic
Framework Shows Dramatically Enhanced Peroxidatic Activity
Nicola A. Dare,† Lee Brammer,‡ Susan A. Bourne,† and Timothy J. Egan*,†
†Department of Chemistry, University of Cape Town, Private Bag, Rondebosch 7701, South Africa
‡Department of Chemistry, University of Sheffield, Brook Hill, Sheffield S3 7HF, United Kingdom
S
* Supporting Information
ABSTRACT: Two MOFs, [H2N(CH3)2][Zn3(TATB)2-
(HCOO)]·HN(CH3)2·DMF·6H2O (1) and Zn-HKUST-1
(2), were investigated as potential hosts to encapsulate Fe(III)
heme (Fe(III) protoporphyrin IX = Fe(III)PPIX). Methyl
orange (MO) adsorption was used as an initial model for
substrate uptake. MOF 1 showed good adsorption of MO
(10.3 0.8 mg g−1) which could undergo in situ protonation
upon exposure to aqueous HCl vapor. By contrast, MO uptake
by 2 was much lower (2 1 mg g−1), and PXRD indicated
that structural instability on exposure to water was the likely
cause. Two methods for Fe(III)PPIX-1 preparation were
investigated: soaking and encapsulation. Encapsulation was
verified by SEM-EDS and showed comparable concentrations of Fe(III)PPIX on exposed interior surfaces and on the original
surface of fractured crystals. SEM-EDS results were consistent with ICP-OES data on bulk material (1.2 0.1 mass % Fe).
PXRD data showed that the framework in 1 was unchanged after encapsulation of Fe(III)PPIX. MO adsorption (5.8 1.2 mg
g−1) by Fe(III)PPIX-1 confirmed there is space for substrate diffusion into the framework, while the UV−vis spectrum of
solubilized crystals confirmed that Fe(III)PPIX retained its integrity. A solid-state UV−vis spectrum of Fe(III)PPIX-1 indicated
that Fe(III)PPIX was not in a μ-oxo dimeric form. Although single-crystal XRD data did not allow for full refinement of the
encapsulated Fe(III)PPIX molecule owing to disorder of the metalloporphyrin, the Fe atom and pyrrole N atoms were located,
enabling rigid-body modeling of the porphine core. Reaction of 2,2′-azino-bis(3-ethylbenzothiazoline)-6-sulfonic acid (ABTS)
with H2O2, catalyzed by Fe(III)PPIX-1 and -2, showed that Fe(III)PPIX-1 is significantly more efficient than Fe(III)PPIX-2 and
is superior to solid Fe(III)PPIX-Cl. Fe(III)PPIX-1 was used to catalyze the oxidation of hydroquinone, thymol, benzyl alcohol,
and phenyl ethanol by tert-butyl-hydroperoxide with t1/2 values that increase with increasing substrate molecular volume.
entrapped in sol−gels,7 hydrogels,8 zeolites,9−12 intercalated
INTRODUCTION
■
clays,13,14 detergent micelles,15 polymer films,16,17 gra-
Hemoproteins are a prominent subclass of metalloproteins
phene,18−22 carbon nanotubes,23,24 nanosheets,25 nanopar-
employing iron protoporphyrin IX (FePPIX) as a cofactor and
ticles,26 hybrid materials,27−29 and metal−organic frameworks
are responsible for a variety of essential metabolic functions
(MOFs).30
including gas binding, electron transport, and redox catalysis.1,2
Their versatility and ability to function with high stereo-,
chemo-, and regioselectivity render them extremely effective
catalysts.3,4 The efficiency of these systems is due, in part, to the
versatility of FePPIX, and consequently, there has been much
interest in harnessing the catalytic power of this prosthetic
group outside of its protein environment. This approach is
challenging, as FePPIX loses its catalytic potency when
removed from a protein binding pocket. A number of factors
including low solubility, aggregation, and irreversible oxidation
in aqueous solution account for this loss of catalytic activity.5,6
In an attempt to circumvent these complications, one can
envisage immobilizing FePPIX on a solid support in order to
prevent aggregation and irreversible oxidation while still
allowing substrate access to the catalytic center. Several
approaches have been investigated in this regard in an attempt
to develop efficient heterogeneous catalysts: FePPIX has been
To date, limited success has been achieved probably because,
in contrast to the original protein hosts, few of the materials
produce well-defined active sites.30,31 MOFs consist of metal-
containing building blocks which serve as nodes that are
connected into a two- or three-dimensional network by
multitopic organic ligands.32−35 These permanently porous
materials afford a large degree of structural versatility, and by
altering the ligand and metal combination, it is possible to tune
the dimensions and chemical composition of the pores.36,37
Thus, MOFs have the potential to overcome the problems
identified with other solid supports by providing a well-defined
environment for catalyst confinement in isolated active sites in
Received: October 10, 2017
© XXXX American Chemical Society
A
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
which substrate access to the catalytic sites is also controlled,
thereby creating robust and efficient catalysts.31,38−40
material.36 This is a problem that is yet to be addressed in the
field of metalloporphyrin@MOF catalysis. When designing a
metalloporphyrin@MOF catalyst, this, together with other
factors, needs to be taken into account. Thus, an ideal MOF for
FePPIX encapsulation requires the following features: (i)
cavities large enough to encapsulate the metalloporphyrin, (ii)
enough space for diffusion of small molecules (reactants and
products) through the framework, (iii) ability to withstand
catalyst leaching, and (iv) a framework that maintains its
structural and chemical integrity under catalytic conditions.69
An additional criterion for investigation of redox catalysis is that
the MOF itself should not be redox active.
Herein we report the preparation and characterization of a
Fe(III)PPIX-containing MOF constructed using redox inactive
Zn(II) ions, namely, [H2N(CH3)2][Zn3(TATB)2(HCOO)]
HN(CH3)2·DMF·6H2O (1). This MOF has wide helical
channels of 43 crystallographic symmetry and a very large
calculated solvent-accessible surface area.70 We demonstrate the
following: there is no change in the structure of the framework
upon encapsulation of the metalloporphyrin; Fe(III)PPIX is
distributed throughout the crystal and not merely confined to
the surface; it occupies well-defined positions in the framework;
it is not present as a μ-oxo dimer; the Fe(III)PPIX-loaded
framework retains efficient substrate diffusion through the
framework; this system is substantially more peroxidatically
active than the corresponding Zn(II)-HKUST-1 system (2)
encapsulating Fe(III)PPIX; and finally Fe(III)PPIX-1 is able to
catalyze oxidation of various substrates showing a dramatic
improvement compared to native solid hemin.
Two approaches can be adopted in the synthesis of
metalloporphyrin-containing MOFs: (i) the metalloporphyrin
can be incorporated into the framework of the MOF itself by
acting as a linker between metal nodes;41−44 or (ii) metal-
loporphyrins can be included as guests in pores within the
MOF.30,36,45 The first approach relies on the use of a
metalloporphyrin with peripheral functional groups in a suitable
geometric arrangement to serve as a multidentate ligand in the
formation of a MOF. Thus, only symmetric synthetic
metalloporphyrins such as iron(III) tetrakis(4-carboxyphenyl)
porphyrin can be used in this approach. On the other hand,
asymmetric metalloporphyrins, including the natural prosthetic
group FePPIX, can only be included in a MOF using the
second approach. This method is thus much more versatile and
can be used to address questions surrounding the reactivity of
specific metalloporphyrins. For example, it has been established
that the vinyl groups on FePPIX play an important role in its
catalytic activity in enzymes, but direct comparison with
synthetic analogues that lack these groups is difficult. As noted
above, in aqueous solution such a comparison is prevented by
aggregation and irreversible oxidation,46,47 but incorporation of
synthetic porphyrin analogues into enzymes is not generally
feasible. Including FePPIX and other synthetic iron porphyrins
as guests in a suitable MOF may be a viable strategy to make
such direct comparisons.
There are a number of reports of the inclusion of synthetic
iron porphyrins in MOFs.45,48−58 Most have made use of an
HKUST-1 framework ([M3(BTC)2]) constructed using various
metal ions including Zn(II), Cu(II), Co(II), Ni(II), Mg(II),
and Cd(II). There are several reports of FePPIX-containing
MOFs used in composite materials for the construction of
electrochemical sensors.59−63 For example Chai and co-workers
used FePPIX encapsulated in Fe-MIL-88 functionalized with
gold nanoparticles to construct an electrochemical aptasensor
for thrombin detection.59 All of these composite materials using
hemin employed redox active MOFs such as Fe-MIL-88 and
Cu-HKUST-1 for hemin encapsulation. Recently, Cheng et al.
used nonredox active ZIF-8 with hemin and glucose oxidase
guests as an integrated nanozyme or INZyme to measure
glucose via oxidation of a synthetic substrate to form a
chromophoric product.64 No loading was reported for hemin in
this system. Luo et al. made use of the Cu-HKUST-1
framework to encapsulate Fe(III)PPIX which was applied
with limited success as a glucose sensor by coupling the
peroxidase reaction with a glucose oxidase enzyme.65 The Cu-
HKUST-1 system is, however, poorly suited for investigating
the redox activity of metalloporphyrins because Cu(II) is itself
redox active, and thus, the MOF exhibits inherent peroxidatic
activity.66,67 Qin et al. used the MIL-101-NH2(Al) framework.
Although this framework is not redox active, it undergoes a
structural and compositional change upon inclusion of hemin as
seen by PXRD.68 Finally, a drawback of both MOF CuHKUST-
1 and MIL-101-NH2(Al) was that they could encapsulate only a
small quantity of Fe(III)PPIX.
RESULTS AND DISCUSSION
■
Synthesis of Two Potential MOF Host Systems for
Fe(III)PPIX Encapsulation. The two MOFs 1 and 2 were
selected as potential Fe(III)PPIX hosts based on their large
pore sizes, solvent-accessible surface areas, and redox inactive
metal centers. Their key properties are given in Table 1.
Table 1. Properties of Frameworks 1 and 2 Pertinent to
Substrate Accessibility
[H2N(CH3)2]
[Zn3(TATB)2(HCOO)]
(1)
Zn-HKUST-1 (2)
a
a
a
pore diameter (Å)
pore topology
21.9
9.1, 5.9
c
b
43 infinite helical channels
square channels
d
d
% solvent accessible
50.7
64.2
d
d
solvent-accessible volume
4245
3002
per channel (Å3)
a
Calculated with the Mercury software package, excluding van der
Waals radii.71,72 Data from previously reported crystal structure.73
b
c
d
Data from previously reported crystal structure.70 Calculated using
the Mercury software package with a probe radius of 1.2 Å.71,72
Framework 1, which has previously been shown to be highly
porous, contains infinite 43 helical channels with permanent
porosity and has good gas adsorption properties.70 It also has
very large diameter solvent-accessible pores indicating that it
has the necessary room for Fe(III)PPIX encapsulation with
substrate accessibility. Cu-HKUST-1 has previously been used
as a host for metalloporphyrins but, although highly porous, is a
poor choice for studying the role of the FePPIX guest in redox
catalysis since the Cu(II) ions in the framework are redox active
and have been shown to exert peroxidatic activity them-
selves.66,67 Replacing Cu with redox inactive Zn affords Zn-
Despite the versatility in choice of metalloporphyrin afforded
by its inclusion as a guest in a MOF framework, a serious
drawback of this approach has been identified: namely, poor
access of substrates to the active site.30 In order to be
catalytically active, substrates require rapid access to the
metalloporphyrin to allow for efficient interaction and for
catalysis not to be limited to sites at the surface of the
B
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
Scheme 1. Synthesis of (a) [H2N(CH3)2][Zn3(TATB)2(HCOO)]·HN(CH3)2·DMF·6H2O (1) and (b) ZnHKUST-1 (2) from
a
Zn(NO3)·6H2O and Their Respective Ligands in DMF
a
Crystal structures of 1 and 2 are shown viewed along the a-axis.70,73
.
Figure 1. Adsorption of methyl orange by MOF crystals. (a) Methyl orange adsorption by 1 (black) and 2 (purple) shown as adsorption quotient
(qt) of MO adsorbed from a 40 μM MO solution in the presence of 2.5 mg of the MOF; (b) crystals of 1, (c) exposed to methyl orange and then (d)
HCl vapors; (e) crystals of 2 exposed to methyl orange.
HKUST-1 (2), an isostructural analogue with the same (3,4)-
connected tbo net topology and similar properties (Table 1).
Frameworks 1 and 2 without Fe(III)PPIX were synthesized
according to previously reported methods (Scheme 1) and
confirmed as phase-pure materials by Pawley fitting of powder
X-ray diffraction patterns (Figure S1).70,73 Single crystals of 1
were obtained and it was confirmed that they had the same
asymmetric unit as reported by Sun et al. (Figure S2).70
Location of solvent molecules in the channels was not possible
due to extensive disorder. It is important to note that the
addition of HNO3 in the synthesis of 1 was essential for the in
situ hydrolysis of solvent dimethylformamide molecules to form
both the formate ions that terminally coordinate to the zinc
oxygen clusters in the MOF and the dimethylammonium
counterions. Formate coordination causes increased stability
and results in the formation of infinite helical channels,
producing chiral crystals that crystallize as a racemic mixture.
Omission of HNO3 results in the formation of a thermally
unstable MOF which loses its crystallinity rapidly after removal
from solvent.70 The presence of the formate ion was observed
in the single-crystal structure of synthesized 1, and the high
thermal stability was confirmed by TG analysis (Figure S3).
The composition of the product was confirmed by combustion
analysis.
The ability of substrate to diffuse into the two structures,
essential for efficient MOF-assisted heterogeneous catalysis,
was investigated by monitoring the uptake of methyl orange
(MO) into the crystals. MO was chosen as a model substrate as
it is of a similar size to typical organic substrates and it is stable
under the conditions used to probe peroxidatic catalysis by
FePPIX. Framework 1 showed a substantial uptake of MO
(10.3 0.8 mg g−1 in 3 h, Figure 1a). MO uptake follows a
two-step process: an initial rapid step that is attributed to the
adsorption of the dye onto the crystal surface, followed by the
slower step of MO diffusion into the framework until
equilibrium is reached, a process similar to that previously
C
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
observed with the adsorption of MO into a Fe-HKUST-1
system.31 This diffusion of MO into 1 is clearly evidenced by
the dramatic color change from colorless to orange (Figure
1b,c) which shifts to red when the MO is protonated by
exposing crystals to vapor emanating from aqueous HCl
(Figure 1d). This latter chromism indicates that the substrate
can readily undergo chemical changes while contained within
the pores of the framework. By contrast, crystals of 2 show very
little orange color after exposure to MO for the same length of
time, indicating that minimal penetration occurs through this
framework. This was supported by the observed MO uptake
(Figure 1a) which displays only an initial fast step
representative of surface adsorption and a correspondingly
low adsorption quotient (2 1 mg g−1). It has been reported
that a densified layer forms on the surface of 2 which limits
porosity and has been shown to result in very poor gas sorption
properties.73,74 This may account for the observed low
adsorption of MO.
A further consideration was whether the framework
maintained its crystallinity after being exposed to aqueous
solution during MO adsorption. In the case of 1, crystallinity
was retained and Pawley fitting of the PXRD pattern
demonstrated that the material did not undergo any phase
changes upon exposure to water (Figure S4). Crystals of 2
immediately went opaque when exposed to water (Figure 1e).
PXRD analysis revealed that a phase change occurred upon
exposure to water (Figure S5), but the new phase could not be
identified because the pattern could not be indexed. An
extensive search of the literature did not yield a match for this
new phase. This change of phase upon exposure to aqueous
solution which may account for the poor MO adsorption data
indicated that 1 was more suitable for Fe(III)PPIX
encapsulation, and therefore, this framework was prioritized
for further investigation.
Synthesis and Characterization of Fe(III)PPIX-1. There
are two main synthetic methodologies for noncovalent
encapsulation of guests in MOFs: (i) diffusion by soaking the
MOF in a solution of the guest,75 and (ii) encapsulation by
including the guest in the MOF reaction mixture and allowing
the framework to form around it.48 The latter method has been
used with great success in the field of porphyrin MOF catalysis.
Both strategies were investigated to determine the optimal
method of Fe(III)PPIX inclusion into our chosen MOF (1).
Energy dispersive X-ray spectroscopy (EDS) analysis of the
original surface and exposed interior surface of fractured
crystals prepared by both methods was used to determine the
iron distribution in the crystals. Preparation of Fe(III)PPIX-1
via soaking was found to be unsuitable as there was no
detectable Fe on the newly exposed interior surface of crystals
broken open after completion of the preparation (Figure 2).
Instead Fe was localized at the original surface of the crystals,
indicating that only surface adsorption of Fe(III)PPIX had
occurred. The observation that very little, if any, Fe was present
within the crystal core suggests that Fe(III)PPIX is likely too
large to diffuse through the framework channels. By contrast,
Fe(III)PPIX-1 synthesized through encapsulation displayed a
uniform distribution of Fe throughout the crystal as there was
no statistically significant difference in the iron content between
the original surface and a newly exposed interior surface formed
by crystal cleavage (Figure 2). The loading of Fe(III)PPIX into
framework 1 prepared by encapsulation was determined by
ICP-OES on digested crystals (1.2 0.1 mass % Fe) and was
Figure 2. (a) Loading of Fe in crystals prepared via soaking and
encapsulation. Representative SEM images of fractured crystals
prepared via (b) soaking and (c) encapsulation. Red boxes indicate
interior surfaces of the crystal exposed upon cleavage, and black boxes
indicate unbroken original surface areas that were analyzed with EDS
as presented in part a. ICP-OES refers to the ICP-OES measurement
of bulk material prepared via the encapsulation method.
not significantly different from that determined using EDS
analysis.
The observation that Fe(III)PPIX uptake into 1 occurs
through encapsulation but not diffusion suggests that, once
included, catalyst leaching is not a concern. This was confirmed
by UV−vis spectroscopy, which showed an absence of the
characteristically intense Soret band of Fe(III)PPIX for an
aqueous solution in which Fe(III)PPIX-1 crystals were soaked
for over 3 h (Figure S6).
Pawley fitting of the powder X-ray diffraction pattern of
framework 1 following encapsulation of Fe(III)PPIX indicates
that the framework retained its integrity (Figure 3a and Figure
S7), with only a slight decrease in the length of the c-axis upon
formation of Fe(III)PPIX-1. The crystals showed no change in
morphology, although a dramatic color change due to the
presence of Fe(III)PPIX was observed (Figure 3b). This dark
color persisted throughout the crystal as observed upon
cleaving crystals. Furthermore, an experiment with differing
concentrations of Fe(III)PPIX in the reaction mixture revealed
using ICP-OES that a loading in the MOF of approximately 1.2
mass % Fe was the maximum that could be achieved (Figure
3c).
MO uptake experiments confirmed that porosity was
retained in the Fe(III)PPIX-1 crystals, albeit to a lesser extent
than the empty framework itself (Figure 3d) with an adsorption
quotient for MO of 5.8 1.2 mg g−1 (56% of that observed for
the empty framework). This reduced capacity for MO uptake is
still nearly 3 times greater than the uptake for empty framework
2. Retention of porosity of 1 after encapsulation of Fe(III)PPIX
was verified using N2 adsorption isotherms. This experiment
also further confirmed encapsulation with a reduction of the
Langmuir surface area from 1398 to 1015 m2 g−1 (Figure S8).
The reported Langmuir surface area of 1 is close to that
reported previously,70 and the reduction after encapsulation
corresponds to a 30% reduction in Langmuir surface area. It
was also found that the material was able to adsorb and desorb
water vapor without loss of porosity (Figure S9), therefore
indicating that the material retains its stability in the presence of
water.
Evidence that Fe(III)PPIX had not degraded under the harsh
crystallization conditions employed was obtained by solubiliz-
ing crystals in basic DMF and recording the resulting UV−vis
D
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
Figure 3. (a) PXRD of 1 (black) and Fe(III)PPIX-1 (red) showing no significant change after encapsulation. (b) Images of 1 (top left) and
Fe(III)PPIX-1 (top right) showing the dramatic color change as well as the dark color present (bottom) within cleaved crystals. (c) Dependence of
loading of Fe(III)PPIX into 1 on concentration of Fe(III)PPIX in the reaction mixture. (d) Adsorption of MO into 1 (black) and Fe(III)PPIX-1
(red). (e) UV−vis spectra of solubilized 1 (black) and Fe(III)PPIX-1 (red) showing the presence of the Soret band at 403 nm in the latter. (f)
Solution-state UV−vis spectra of μ-[Fe(III)PPIX]2O (green) and H2O−Fe(III)PPIX (blue) compared to the solid-state UV−vis spectrum of
Fe(III)PPIX-1 (red).
spectrum. This revealed the characteristic Soret band of
Fe(III)PPIX at 400 nm (Figure 3e). Further information
regarding Fe(III)PPIX speciation in the framework was
obtained from solid-state optical absorption spectroscopy.
The absorption spectrum of Fe(III)PPIX in Fe(III)PPIX-1
clearly shows that it does not exhibit the spectroscopic features
of the μ-oxo dimer, since it lacks the characteristic feature near
600 nm. Instead, the broad envelope observed around 650 nm
more closely resembles the predominantly charge-transfer band
of H2O−Fe(III)PPIX (Figure 3f).76,77 The fact that Fe(III)-
PPIX remains intact after encapsulation and does not form a μ-
oxo dimer within the framework highlights the potential for
catalytic activity of Fe(III)PPIX when encapsulated in 1.
Crystal Structure of Fe(III)PPIX-1. Further insight into the
structure of Fe(III)PPIX-1 was obtained through single-crystal
X-ray diffraction analysis. The crystal studied was found to be a
three-component twin with approximately equal contributions
from each component. The framework was found to be
isostructural with empty framework 1. Interestingly, the
bridging formate group present in the empty framework
could not be located in the crystal structure of Fe(III)PPIX-1,
and only a bridging oxygen atom probably attributable to a
hydroxide ion between the secondary building units (SBUs)
was located. The crystals form as a racemic mixture and
therefore belong either to the space group P43 or P41. It should
be noted that previous studies of the host framework (1)
reported crystals of higher symmetry (P4322 or P4122).70
However, the presence of the asymmetric guest lowers the
symmetry of the system.70
The asymmetric unit contains an hourglass-shaped SBU, or
pinwheel SBU, which consists of two tetrahedral terminal zinc
ions and a central octahedral zinc ion (Figure 4a). The central
zinc is coordinated to six carboxylate oxygen atoms of the
TATB3− ligand while both tetrahedral zinc ions are coordinated
to three carboxylate oxygen atoms and a bridging oxygen atom,
linking the SBUs. The TATB3− ligands π-stack with each other
at a distance of 3.36 Å between the triazine rings and form a D3
Piedfort unit (θ ≈ 30°).70,78 The framework is a non-
interpenetrated (10,3)-a network with chiral 41 (or 43) helical
channels, creating a chiral environment within the channels.
These channels are the hypothesized pathways through which
substrates diffuse into the framework.
Despite exhaustive attempts to fully model the Fe(III)PPIX
guest within the framework, this was not possible, probably on
account of its extensive disorder within the channels,
exacerbated by the fact that the crystal was twinned and the
E
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
either the use of very low concentrations of both MO and
H2O2, resulting in slow reaction, or requiring an inconvenient
out of cell reaction. For this reason, the chemically and
structurally similar 2,2′-azino-bis(3-ethylbenzothiazoline)-6-sul-
fonic acid (ABTS) was chosen as a substrate for further
investigation. This substrate shows an increased absorption of a
band at 660 nm, which results from oxidation to the radical
cation (ABTS•+).80
To compare the activity of the two porphyrin@MOF
systems, Fe(III)PPIX-2 was synthesized in a similar manner
to Fe(III)PPIX-1 using the encapsulation method. Retention of
the framework structure of 2 on forming Fe(III)PPIX-2 was
confirmed by PXRD and Pawley fitting (Figure S11), and the
Fe content was determined by ICP-OES as 1.039
0.0004
mass % Fe (compared to 1.2 0.1 mass % Fe in Fe(III)PPIX-
1).
The MO adsorption quotient of Fe(III)PPIX-2 was found to
be 0.99 0.28 mg g−1, 50% of the adsorption quotient for 2 (2
1 mg.g−1). This decrease in adsorption quotient was
proportionate to that observed upon encapsulation of Fe(III)-
PPIX into 1. The much larger adsorption quotient in
Fe(III)PPIX-1 suggests that substrates would have better
access to catalytic sites in this material, being able to access
sites both on the surface and in the interior of the crystal. On
the other hand, for Fe(III)PPIX-2 it is likely that only surface
sites can be accessed. This suggests that Fe(III)PPIX-1 is likely
to be more suitable for MOF-encapsulated Fe(III)PPIX
catalysis.
Figure 4. Crystal structure of Fe(III)PPIX-1. (a) Coordination
environment and Piedfort unit of the framework as seen in the
asymmetric unit of Fe(III)PPIX-1 showing the located Fe and N
atoms of Fe(III)PPIX in 1 and (b) packing of Fe(III)PPIX-1 viewed
along the b-axis with a rigid-body model of the porphine core of
Fe(III)PPIX in the channels of the framework (shown as space-fill;
orange = Fe, blue = nitrogen).
loading low. Nonetheless, the central Fe(III) ion of Fe(III)-
PPIX could be located on the basis of residual electron density.
This was refined isotropically, and the site occupancy of the Fe
ions was refined using a combination of the ICP-OES loading
data and the magnitude of the observed electron density. The
nitrogen atoms coordinated to the central iron ion could be
located and were also refined isotropically using distance
restraints (Figure 4a). The occupancy of these nitrogen atoms
was lower than that of the iron, as they represent one
orientation of the disordered porphyrin center. Further residual
electron density in the vicinity of the iron center could not be
satisfactorily modeled. Location of the first coordination sphere
of Fe(III)PPIX, however, did allow its position in the
framework channels to be determined. It was not found to π-
stack with the TATB3− ligands along the walls of the channels,
but rather was present nearer the center of the channels. This
channel-center location of the heme could contribute to the
orientational disorder observed, as the interactions between
Fe(III)PPIX and the framework are likely to be weak.
The catalytic activity of Fe(III)PPIX-1 and Fe(III)PPIX-2
was also further compared to solid hemin, Fe(III)PPIX-Cl
(Figure 5). All reactions were conducted with [ABTS] ≫
Rigid-body modeling of the porphine core confirmed that
there is sufficient space for this substructure of Fe(III)PPIX in
the located position (Figure 4b). The solvent-accessible volume
after encapsulation is 3520 Å3 (calculated using the Mercury
software package with a probe radius of 1.2 Å),72 which is
approximately 40% of the unit cell volume. This confirms that
typical organic substrates, such as MO,71,72 have sufficient space
to diffuse into the channels.
Catalytic Activity of Fe(III)PPIX-1. To investigate whether
the Fe(III)PPIX-1 system is suitable as an efficient heteroge-
neous catalyst and whether it shows improved catalytic activity
over solid-state Fe(III)PPIX itself, its peroxidatic activity was
investigated. MO can undergo oxidation in the presence of
peroxides and a suitable catalyst,79 and it was indeed found to
react with H2O2 in the presence of Fe(III)PPIX-1 with 86.6%
conversion to its oxidized product (Figure S10). It is not,
however, a convenient substrate for kinetic studies owing to its
intense color which bleaches in this reaction. This necessitates
Figure 5. Initial rates of ABTS oxidation by H2O2 catalyzed by
Fe(III)PPIX-1 (red), Fe(III)PPIX-2 (orange), and solid Fe(III)PPIX-
Cl (blue). Inset: Initial rate with Fe(III)PPIX-1 (red) and solution
state Fe(III)PPIX (pink). Reaction conditions are given in Table 2.
[H2O2] ≫ [Fe(III)PPIX]. Under these reaction conditions one
H2O2 molecule will oxidize two ABTS molecules to ABTS•+
through the formation of a high valent iron-oxo intermedi-
ate.81,82 It was found that, in the presence of 1, no catalytic
activity was observed (Figure S12), confirming that 1 is not
itself catalytically active. The initial rates as well as the
percentage conversion of ABTS in each system are presented in
Table 2. It is important to note that the yield observed
experimentally is not a true reflection of the number of ABTS
molecules oxidized owing to disproportionation of ABTS•+.83
The ABTS•+ cation exists in equilibrium with unreacted ABTS
and an azodication. This reaction is slow and will therefore not
affect initial rates; however, it will affect the experimentally
F
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
Table 2. Summary of Kinetic Results for Oxidation of ABTS by H2O2
a
b
c
Fe(III)PPIX-1
Fe(III)PPIX-2
Fe(III)PPIX-Cl
12.24 mol %
d
catalyst loading
1.36 mol %
0.2380 0.0009
0.22 0.02
10.9 1.2
1.28 mol %
initial rate (mM ABTS•+ h−1
max [ABTS•+] (mM)
)
0.0826 0.0003
0.075 0.003
1.86 0.06
0.0062 0.0006
0.011 0.001
0.55 0.09
e
conversion %
f
TON
3.4 0.3
1.2 0.1
0.0202 0.0001
a
b
c
≈0.17 μmol of Fe(III)PPIX in 2.5 mL of TRIS reaction buffer. ≈0.16 μmol of Fe(III)PPIX in 2.5 mL of TRIS reaction buffer. ≈1.59 μmol of
d
e
Fe(III)PPIX. Mol of Fe(III)PPIX per mol of H2O2. Calculated using H2O2 as the limiting reagent with a maximum ABTS•+ yield of 2 mM:
f
conversion % = [ABTS•+] (mM)/2 × 100. TON = [ABTS•+] (M)/[Fe(III)PPIX] (M). All reactions were conducted under the following
conditions: 5 mM ABTS, 1 mM H2O2 in 0.01 M TRIS (pH 7.4), 37.00 °C, 2 h.
Figure 6. (a) Yield of ABTS•+ (relative to cycle 1) and (b) initial rate of ABTS oxidation represented as mM ABTS•+ h−1 μmol−1 of Fe(III)PPIX
catalyzed by Fe(III)PPIX-1 through five successive cycles of catalyst recovery and reuse.
observed yield of ABTS•+ and therefore the experimentally
observed TON.83
reaches the efficiency of catalysts in which the metalloporphyrin
forms part of a highly ordered framework.
Both Fe(III)PPIX-1 and Fe(III)PPIX-2 showed a dramatic
increase in yield and conversion of ABTS relative to solid
Fe(III)PPIX-Cl in spite of the fact that the quantity of
Fe(III)PPIX was more than 10-fold higher in the Fe(III)PPIX-
Cl experiments. This is a clear indication that the Fe(III)PPIX
centers are more accessible in the metalloporphyrin@MOF
materials compared to Fe(III)PPIX-Cl. Fe(III)PPIX-1, how-
ever, exhibited an approximately 3-fold faster rate and 6-fold
higher conversion than Fe(III)PPIX-2 confirming that the
former is a more efficient catalyst than the latter. This is
consistent with the ability of substrates to access the
Fe(III)PPIX sites in the interior of 1 by diffusion and not
only surface sites as seems to be the case for framework 2 as
well as the fact that Fe(III)PPIX-1 is structurally stable in water,
while Fe(III)PPIX-2 is not.
It is noteworthy that, at the same substrate concentration, the
initial rate of reaction catalyzed by dissolved Fe(III)PPIX-OH
(0.125 μmol Fe(III)PPIX; 1 mol %) in aqueous solution was
only about 6 times faster (1.34 0.06 mM ABTS.hr−1) than
that for Fe(III)PPIX-1 (Figure 5, inset). On the other hand,
this fast reaction in solution quickly dropped off so that the
conversion of ABTS was only 5.67% compared to 10.91% for
Fe(III)PPIX-1 after reaction completion. This suggests the rate
of the reaction is limited by the diffusion of ABTS into the
frameworks. The increased yield can probably be attributed to
the framework preventing catalyst aggregation and protecting
the metalloporphyrin from oxidative degradation, both of which
contribute to limited FePPIX catalyst lifetime in solution.
Interestingly, when comparing the oxidation of ABTS
catalyzed by Fe(III)PPIX-1 and a metalloporphyrin@MOF
with porphyrin linkers (MMPF-6) reported by Chen et al., the
initial rates are comparable (0.2380 0.0009 mM ABTS•+ h−1
mM−1 H2O2 for Fe(III)PPIX-1 and 0.2945 mM ABTS•+ h−1
mM−1 H2O2 for MMPF-6).41 This indicates that Fe(III)PPIX-1
The reusability of Fe(III)PPIX-1 was investigated by
conducting recycling experiments. The catalyst maintained its
structural integrity through several cycles. PXRD analysis
showed only changes in intensity of the peaks (Figure S13)
and can be attributed to differing solvent content in the
material as residual DMF leaves the pores and is replaced by
water. Pawley fitting confirmed that the unit cell remained the
same after three successive cycles of ABTS oxidation with a
slight expansion along the a- and b-axes from 18.0993 to
18.15374 Å (Figure S13). Fe(III)PPIX-1 showed no loss of
catalytic activity through five successive cycles, demonstrating
that this catalyst has excellent recyclability (Figure 6). Thus, by
encapsulating Fe(III)PPIX into the MOF, the catalytic center
becomes stable in an aqueous medium and, being heteroge-
neous, can be recovered and reused. This is different from
previously reported recyclability for a synthetic tetraphenyl
porphyrin in Cu-HKUST-148 and for Fe(III)PPIX encapsulated
in MIL-101-NH2(Al)68 which both showed a decrease in
activity after each successive cycle.
The versatility of Fe(III)PPIX-1 as an oxidation catalyst was
investigated by studying oxidation of hydroquinone (HQ) to its
corresponding benzoquinone (BQ). The reaction was initially
carried out in water with H2O2 as the oxidant; however,
formation of side products was observed. Changing to
acetonitrile (AcN) solvent with t-butyl-hydroperoxide
(tBuOOH) as oxidant resulted in a clean reaction which was
also faster. Indeed, it was found that the oxidation of ABTS by
tBuOOH in water was also faster than that by H2O2, with the
initial rate going from to 0.2380 0.0009 mM ABTS•+ h−1 to
0.44 0.07 mM ABTS•+ h−1 (Figure S14).
t
The oxidation of HQ by BuOOH in AcN was readily
monitored by UV−vis spectroscopy. The decrease in λmax of
HQ (280 nm) as well as an increase in the λmax of BQ (240
nm) showed complete conversion of HQ to BQ within 20 h
G
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
Figure 7. Oxidation of HQ by tBuOOH catalyzed by Fe(III)PPIX-1: (a) UV−vis spectra of the reaction mixture at different time points (* denotes
an isosbestic point); (b) increasing concentration of BQ (green) and decreasing concentration of HQ (blue) as a function of time; and (c) 1H NMR
spectra of the reaction mixture at 0, 2, and 24 h.
t
Table 3. Conversion, Half-Lives, and Molar Volumes of Substrates Oxidized by BuOOH in the Presence of Fe(III)PPIX-1
a
Relative concentrations of substrate and product were determined by NMR at each time point by integrating each peak relative to an internal
standard (tBuOOH + in situ formed tert-butanol [tBuOH]). All reactions were carried out with 15 mg of substrate in 1 mL of d3-AcN and initiated
by addition of 50 μL of 70% (w/w) tBuOOH in water at 25 °C. Characterization of products is presented in Supporting Information (Figures S18−
b
S27). Half-lives were determined from UV−vis spectroscopy data obtained at 37.00 °C, fitted with a nonlinear regression model in GraphPad Prism
(Figure S16).84 Molecular volume was calculated using Chemicalize.85
c
(Figure 7a). The presence of an isosbestic point confirmed
there were only two chromophoric components present in
solution. The half-life of the reaction was determined by
monitoring either the increase in concentration of BQ or the
decrease in concentration of HQ (Figure 7b, Table 3). The
reaction was further monitored by 1H NMR spectroscopy at 0,
2, and 24 h. The disappearance of the peak corresponding to
the CH protons (δ 6.63 ppm) of HQ and the appearance of the
peak corresponding to the CH protons of BQ (δ 6.77 ppm)
further confirmed 100% conversion of HQ to BQ (Figure 7c).
H
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
In light of the instability of framework 2 in aqueous media,
the oxidation of HQ by Fe(III)PPIX-2 in AcN by tBuOOH was
investigated and compared to that by Fe(III)PPIX-1. It was
found that there was incomplete conversion (41.5%) compared
to Fe(III)PPIX-1 (100%) and a longer half-life (2.56 h
compared to 2.07 h) indicating that even in an organic solvent
this material is considerably less efficient as an oxidation
catalyst (Figure S15).
CONCLUSION
■
In this study, we reported that encapsulation of Fe(III)PPIX in
a MOF affords an effective and long-lived oxidation catalyst for
a variety of substrates. We have directly shown access of
substrates into the framework of [H2N(CH3)2][Zn3(TATB)2-
(HCOO)]·HN(CH3)2·DMF·6H2O (1) and the corresponding
catalytically active material Fe(III)PPIX-1, which most
probably occurs by diffusion through the infinite 43 helical
channels. The distribution and accessibility of catalytic sites in
Fe(III)PPIX-1 have been confirmed by synchrotron single-
crystal X-ray diffraction, and this is the first report of single-
crystal X-ray data for encapsulation of Fe(III)PPIX into a
MOF. By contrast, Zn-HKUST-1 (2) shows poor substrate
uptake, and Fe(III)PPIX-2 shows correspondingly poorer
catalytic performance than Fe(III)PPIX-1. Furthermore, the
observed aqueous instability of 2 reinforces its unsuitability as a
peroxidation catalyst in this system. Inclusion of Fe(III)PPIX
into 1 drastically increases both the initial rate of peroxidatic
oxidation of ABTS compared to solid Fe(III)PPIX-Cl and
dramatically increases the yield compared to both solid-state
Fe(III)PPIX-Cl and solution-state Fe(III)PPIX. What is more,
Fe(III)PPIX-1 was shown to catalyze ABTS oxidation by H2O2
at an initial rate less than an order of magnitude slower than
Fe(III)PPIX in solution. The catalyst can be readily recovered
and recycled without loss in catalytic activity. Furthermore, the
ability of Fe(III)PPIX-1 to oxidize both H2O2 as well as a
variety of other substrates further demonstrates its efficacy as a
heterogeneous oxidation catalyst. This emphasizes the success
of the Fe(III)PPIX-1 system in harnessing the power of
Fe(III)PPIX in a synthetic heterogeneous MOF host. This
MOF system therefore provides a suitable support for
comparing the reactivity of Fe(III)PPIX with synthetic
porphyrins. Detailed mechanistic studies on this system are
currently underway with both Fe(III)PPIX and Fe(III)
tetraphenylporphine.
In view of the 100% conversion of HQ in the presence of
Fe(III)PPIX-1, the oxidation of other substrates, thymol (TH),
benzyl alcohol (BN), and phenyl ethanol (PH), was
investigated in the presence of this catalyst (Table 3, Figure
S16). All reactions were monitored in the same manner as HQ,
1
with an added H NMR spectrum at 48 h. These reactions did
not achieve full conversion, and it was found that as the
molecular volume of the substrate increased, the half-life of the
reaction increased, suggesting that the larger molecules diffuse
through the pores more slowly and this therefore affects the
reaction rate. This hypothesis was supported by the fact that
the same oxidation reactions catalyzed by Fe(III)PPIX in
solution did not show a similar trend (Table S1, Figure S17).
Rather, it was found that the half-lives for the oxidation of TH,
BN, and PH were approximately equal. This points toward the
possible use of Fe(III)PPIX-1 as a size-selective oxidation
catalyst and emphasizes the importance of the catalytic sites in
the interior of the MOF.
Fe(III)PPIX-1 has been shown to be both effective as a
heterogeneous oxidation catalyst and very much more efficient
than solid hemin. Owing to the focus of previous studies on
applications as functional materials, it is not possible to directly
compare the catalytic activity of Fe(III)PPIX-1 to the
previously synthesized FePPIX@MOFs. Luo et al. synthesized
FePPIX@Cu-HKUST-1 and studied the oxidation of luminol
by H2O2 using chemiluminescence. Unfortunately, no kinetics
data were reported since the study focused on detection of
H2O2 and glucose by coupling the FePPIX@MOF with glucose
oxidase.65 Furthermore, since copper is redox active,66,67 it is
not certain whether the activity can be directly ascribed to the
metalloporphyrin. In the study by Qin et al., FePPIX was
encapsulated in MIL−101(Al)−NH2 which converted to MIL−
53(Al)−NH2 after encapsulation, and a loading of FePPIX into
the MOF of 1.02% was found using the Al:Fe ratio.68 This
loading was similar to that of Fe(III)PPIX in 1 found in this
study. The catalytic oxidation of 3,3,5,5-tetramethylbenzidine
(TMB) by H2O2 was investigated, and the material was found
to be catalytically active, but no initial rates were reported, so
direct comparison to Fe(III)PPIX-1 again could not be made.
Cheng et al. also encapsulated FePPIX in a redox inactive
MOF, ZIF-8.64 In this study no initial rates or loading of
FePPIX in ZIF-8 were reported. The focus was on utilizing the
MOF with the enzyme glucose oxidase and FePPIX guests for
the purpose of glucose detection. This system was quite robust
in that it maintained activity through four cycles, but it was
apparently less stable than Fe(III)PPIX-1 in that there was
about a 20% reduction in activity by the fourth cycle. In
addition, in all reports to date, no single-crystal X-ray data of
Fe(III)PPIX encapsulated within the framework were reported,
and there is no confirmation that Fe(III)PPIX was distributed
throughout the MOF crystal and not confined to the surface
except in the case of the ZIF-8 system.
EXPERIMENTAL SECTION
■
General. With the exception of 4,4′,4″-s-triazine-2,4,6-triyl-
tribenzoic acid (CGene Tech. Inc.), all chemicals were purchased
from Sigma-Aldrich and used without further purification. Double-
distilled deionized water was provided by a Millipore Direct-Q3 water
purification system. The solvent used for synthesis was anhydrous
N,N-dimethylformamide (DMF, 99.8% purity) which was stored over
activated molecular sieves (3 Å). All glassware was washed
scrupulously as reported previously in order to prevent build-up of
Fe(III)PPIX.86 TGA was performed on a TA-Q500 TA, and data were
analyzed using the Universal Analysis 2000 program.
Synthesis of [H2N(CH3)2][Zn3(TATB)2(HCOO)]·HN(CH3)2·DMF·
6H2O (1). Single crystals of 1 were prepared by dissolving 4,4′,4″-s-
triazine-2,4,6-triyl-tribenzoic acid (H3TATB) (5 mg, 0.0113 mmol)
and Zn(NO3)2.6H2O (27 mg, 0.0907 mmol) in DMF (2 mL) with 30
μL of 0.5 M HNO3 in a glass vial. The vial was sealed with a lid and
covered with Parafilm to ensure a tighter seal, sonicated to ensure the
dissolution of all material, and placed in an oven at 105 2 °C for 16
h. The oven was then allowed to cool to room temperature over 4 h;
the crystals were collected and washed extensively with fresh DMF.
The product was identified and phase purity confirmed by Pawley
fitting of the PXRD pattern, elemental combustion analysis, and TGA.
The dimethylammonium ([H2N(CH3)2]+) counterion and formate
ions present in the structure are produced by acid hydrolysis of DMF.
Combustion analysis provided evidence for further uncoordinated
dimethylamine, DMF, and H2O in the channels of the MOF. These
solvent molecules were identified using a combination of TGA (Figure
S28) and elemental analysis and were in good agreement with
previously reported results.70 Anal. Calcd for C56H59N9O21Zn3: C,
I
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
48.38%; H, 4.28%; N, 9.07%. Found: C, 48.65%; H, 4.12%; O, 9.10%.
Solvent mass % from TGA: 20.9 1.1%.
Inductively Coupled Plasma Optical Emission Spectrometry
(ICP-OES). Samples were ashed in a furnace at 600 °C overnight
before digestion with 4 mL of 4:1 conc HF and HNO3 at 130 °C for
48 h (Warning: HF is extremely dangerous and should be handled with
caution.) These samples were then dried and washed twice with 2 mL
of conc HNO3 with drying between washes. The solid material
remaining was diluted in a 5% HNO3 solution before analysis by ICP-
OES using a Varian 730-ES spectrometer. The mass % of Fe was
calculated from the data obtained. All ICP-OES measurements of each
sample were done on three preparations of the same material which
were then combined in order to obtain an accurate mass % across
differing preparations.
Gas Sorption. Both N2 and water vapor sorption experiments were
conducted using a Micromeritics 3Flex surface area analyzer.
Approximately 100 mg of oven-dried 1 and Fe(III)PPIX-1 were
further dried under dynamic vacuum for 24 h at 80 °C prior to being
treated in a Micromeritics Flowprep with a constant flow of nitrogen
gas over the sample at 60 °C for 24 h. The samples were further
heated at 60 °C under vacuum in situ on the Micromeritics 3Flex
surface area analyzer in order to ensure all solvent was evacuated from
the pores of the MOF. Adsorption isotherms for N2 were measured at
−196 °C and water vapor at 25 °C. Data were analyzed using 3Flex
Version 3.01 to obtain the calculated Langmuir surface area.
X-ray Diffraction. Single-Crystal X-ray Diffraction. Single crystals
of Fe(III)PPIX-1 were removed from the mother liquor and
immediately placed under Paratone oil in order to prevent solvent
loss and crystal degradation. Due to the dark color of the crystals, light
polarization could not be used to select a sample of suitable quality for
data collection. Instead, crystals were screened on a Bruker KAPPA
APEX II Duo diffractometer using Mo Kα radiation (λ = 0.71073 Å)
to find suitable crystals.
Synthesis of Zn-HKUST-1 (2). Single crystals of 2 were prepared by
dissolving benzene-1,3,5-tricarboxylic acid (28 mg, 0.133 mmol) and
Zn(NO3)2·6H2O (62 mg, 0.208 mmol) in DMF (2 mL) in a glass vial.
The vial was sealed with a lid and covered with Parafilm, sonicated to
ensure all material was dissolved, and placed in an oven at 85 2 °C
for 20 h. The oven was then allowed to cool to room temperature over
3 h, and the crystals were collected and washed extensively with fresh
DMF. The product was identified and phase purity confirmed by
Pawley fitting of the PXRD. TGA was used to determine the solvent
content (Figure S28). Solvent mass % from TGA: 32.58 0.60%.
Synthesis of Fe(III)PPIX-1 and Fe(III)PPIX-2. The same
procedures used for synthesis of 1 and 2 were used for the synthesis
of Fe(III)PPIX-1 and Fe(III)PPIX-2, respectively, with the exception
that 5 mg (0.0079 mmol) of hematin (Fe(III)PPIX-OH) was included
in each reaction mixture. The crystals obtained from each mixture were
washed extensively with fresh DMF in order to remove excess surface-
adsorbed Fe(III)PPIX-OH. The products were identified, and phase
purity was confirmed by Pawley fitting of PXRD patterns of the bulk
materials. TGA was used to determine the solvent content (Figure
S28). The amount of Fe(III)PPIX encapsulated within the framework
was determined using ICP-OES. Solvent mass % from TGA:
Fe(III)PPIX-1, 18.17 0.28%; Fe(III)PPIX-2, 27.22 0.73%.
Ultraviolet−Visible (UV−vis) Spectroscopy. Solution-state
UV−vis spectra were recorded on a Shimadzu UV-1800 spectropho-
tometer over the range 200−800 nm. Quartz cuvettes (Hellma,
Suprasil, 1 cm path length) were maintained at a constant temperature
of 25.00
0.02 °C by a TCC-100 thermoelectrically temperature-
controlled cell holder accessory. Solid-state spectra were recorded at
room temperature on a Cary 5000 UV−vis spectrophotometer with a
Harrick Praying Mantis diffuse reflectance accessory.
Full data collection using synchrotron radiation was conducted at
the I19 small-molecule single-crystal diffraction beamline at Diamond
Light Source (λ = 0.6889(3) Å), which is equipped with a Pilatus 2 M
detector.88 An Oxford Cryosystems Cryostream device was used to
cool the crystal to −173.15(2) °C using dry N2 gas. Data were
collected as a series of four sequences of frames with 0.1 s exposure
time per frame with no beam attenuation. The best data were obtained
for a crystal determined to be a three-component twin. Three-
component twin data integration and reduction were performed using
ChrysAlisPro, and data were corrected for absorption using multiscan
empirical absorption correction.89 Unit cell and space group were
determined using ChrysAlisPro. Structure solution was conducted
using direct methods with SHELXS-97 which located all non-
hydrogen atoms of the MOF, while SHELXL-97 was used in a
refinement by full matrix least-squares on F2, with anisotropic
displacement parameters.90 Hydrogen atoms were placed with
geometric constraints and were refined with isotropic displacement
parameters. All structure determination was completed using the
Olex2 interface.91
The iron center of the porphyrin core was located using residual
electron density and refined isotropically with a fixed site occupancy
based on the calculated loading from the ICP-OES data. The nitrogen
atoms forming the first coordination sphere of the porphyrin were also
located and their positions refined using distance and angle restraints.
These atoms were modeled with a lower site occupancy than the iron
as a consequence of orientational disorder of the porphine core.90
Crystal structure data are presented in Table S2.
Powder X-ray Diffraction. Powder X-ray diffraction (PXRD) was
used to confirm the structure of the bulk material. All patterns were
collected at 25 °C on a Bruker D8 Advance diffractometer with a
Lynxeye detector using Cu Kα radiation (λ = 1.5406 Å) and operating
at 40 mA and 30 kV. A receiving slit of 0.6 mm and primary and
secondary slits of 2.5 mm were used. All samples were measured using
a zero-background sample holder and were lightly ground to a fine
powder before collection of data. The samples were scanned over a 2θ
range of 4° to 40° using a step size of 0.02° (1760 steps) with 2 s
exposure time. Pawley fitting92 was conducted using TOPAS (v 4.2) in
order to determine unit cells from the PXRD patterns.93
Methyl Orange (MO) Adsorption. Prior to the MO adsorption
experiments, single crystals of 1, 2, Fe(III)PPIX-1, and Fe(III)PPIX-2
were kept in an oven at 50 °C for 14 h. The remaining DMF mass was
determined by TGA and accounted for to obtain an accurate mass of
material used for MO adsorption experiments in order to calculate the
adsorption quotient. All TGA experiments were performed with a dry
N2 gas flow rate of 50 cm3 min−1 and were monitored from room
temperature to 400 °C at a heating rate of 10 °C min−1. A 40 μM
aqueous methyl orange (MO) solution was prepared by diluting a 1
mM aqueous stock solution of MO (sodium 4-{[4-(dimethylamino)-
phenyl]diazenyl}benzene-1-sulfonate) in 0.01 M TRIS buffer (pH
7.4). Approximately 2.5 mg of the appropriate dried MOF material was
added, and the decrease in concentration of MO was monitored at 465
nm using UV−vis spectroscopy over 3 h. (A Beer’s law plot was used
to determine the extinction coefficient of the MO.) All experiments
were conducted with constant magnetic stirring until equilibrium was
reached. The TG data were used to calculate an accurate mass of
crystals used in the experiments without framework-associated solvent
for the adsorption quotient calculation. Data were analyzed using
nonlinear regression analysis in GraphPad Prism v6.05.84 The
adsorption quotient was calculated from eq 1:
(ci − ct)V
qt =
(1)
m
where qt is the mass of dye adsorbed at time t (mg·g−1), ci and ct are
the initial and time t solution concentrations respectively (mg·L−1), V
is the volume of the aqueous dye solution added (L) and m is the mass
of material studied (g).87
Scanning Electron Microscopy (SEM). A Leo 1450 LaB6
scanning electron microscope with a Bruker XFlash EDS Si Drift
Detector was used to obtain micrographs of crystals. Quantification of
the zinc and iron content on the exterior and exposed interior surfaces
of Fe(III)PPIX-1 crystals prepared by soaking and encapsulation
methods was performed using energy dispersive X-ray spectroscopy
(EDS). Prior to visualization, samples were sputter-coated with
carbon. Statistical significance was determined using an unpaired two-
tailed t test.
J
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
Kinetics Measurements. The chromophoric substrate 2,2′-azino-
bis(3-ethylbenzothiazoline)-6-sulfonic acid (ABTS) was used to
monitor the progress of the peroxidatic reaction catalyzed by
Fe(III)PPIX-Cl or the Fe(III)PPIX-MOF systems. In a typical
reaction, 1 mg of catalyst was added to 2.375 mL of 5 mM aqueous
ABTS solution (0.01 M TRIS, pH 7.4). The reaction was initiated by
adding 125 μL of 20 mM H2O2 (final concentration of 1 mM H2O2
and total volume of 2.5 mL), and the rate of ABTS•+ formation was
monitored by the intensity of its absorption band at 660 nm on a
Shimadzu UV-1800 spectrometer at 37.00 0.02 °C with constant
magnetic stirring. Data were analyzed using the one-phase exponential
Research Foundation for financial support via a PhD student-
ship. We are grateful to the Diamond Light Source (beamline
I19) for beamtime and to Dr. Sarah Barnett for conducting the
experiments at Diamond Light Source. We thank Dr. Scott
Bohle (McGill University, Canada) for use of the solid-state
UV−vis spectrometer. We would also like to thank Dr. Rebecca
Smith (University of Sheffield) for her contribution to early
efforts in crystallographic characterization of Fe(III)PPIX-1.
REFERENCES
■
function in GraphPad Prism in order to obtain maximal yield (Ymax
)
and a straight-line function to obtain initial rates.84
(1) Groves, J. T. Models and Mechanisms of Cytochrome P450
Action. In Cytochrome P450; Springer US: Boston, MA, 2007; pp 1−
43.
The recycling experiments were conducted in the same manner as
the previous kinetics measurements in triplicate (cycles four and five
were single measurements). Crystals were collected and dried after
each successive cycle. The solvent content was determined using TGA
analysis before each cycle, and PXRD was conducted to ensure that
crystallinity was retained.
(2) Poulos, T. L. Heme Enzyme Structure and Function. Chem. Rev.
2014, 114, 3919−3962.
(3) Schmid, A.; Dordick, J. S.; Hauer, B.; Kiener, A.; Wubbolts, M.;
Witholt, B. Industrial biocatalysis today and tomorrow. Nature 2001,
409, 258−268.
Oxidation of Additional Substrates. Hydroquinone (15 mg,
0.1362 mmol), benzyl alcohol (15 μL, 0.1443 mmol), thymol (15 mg,
0.0995 mmol), or phenyl ethanol (15 μL, 0.1226 mmol) was each
added to 1 mL of acetonitrile (AcN) containing either Fe(III)PPIX-1
(5 mg, 0.89 μmol Fe(III)PPIX), Fe(III)PPIX-2 (5 mg, 0.64 μmol), or
178 μL of 5 mM hemin solution (0.89 μmol in 1 mL). The reaction
was started by adding 50 μL of tert-butyl hydroperoxide. The reaction
was monitored spectrophotometrically on a Shimadzu UV-1800 by
reading aliquots of the reaction mixture at time intervals. All spectra
were recorded over a range 200−800 nm. Nuclear magnetic resonance
(NMR) spectra of in situ reactions under the same conditions were
obtained in acetonitrile-d3 to confirm the reaction product. NMR
spectra were recorded on a Bruker 400 MHz Ultrashield 400 Plus
NMR spectrometer, and chemical shifts (δ) were recorded relative to
acetonitrile-d3 (δ 1.94 ppm in 1H NMR, δ 118.26 ppm in 13C NMR).
All chemical shift values are reported in ppm.
(4) Reedy, C. J.; Gibney, B. R. Heme Protein Assemblies. Chem. Rev.
2004, 104, 617−649.
(5) Bruice, T. C. Reactions of hydroperoxides with metal-
lotetraphenylporphyrins in aqueous solutions. Acc. Chem. Res. 1991,
24, 243−249.
(6) Guo, C.-C.; Song, J.-X.; Chen, X.-B.; Jiang, G.-F. A new evidence
of the high-valent oxo−metal radical cation intermediate and hydrogen
radical abstract mechanism in hydrocarbon hydroxylation catalyzed by
metalloporphyrins. J. Mol. Catal. A: Chem. 2000, 157, 31−40.
(7) Battioni, P.; Cardin, E.; Louloudi, M.; Schollhorn, B.; Spyroulias,
G. a.; Mansuy, D.; Traylor, T. G. Metalloporphyrinosilicas: a new class
of hybrid organic-inorganic materials acting as selective biomimetic
oxidation catalysts. Chem. Commun. 1996, 2037−2038.
(8) Wang, Q.; Yang, Z.; Ma, M.; Chang, C. K.; Xu, B. High Catalytic
Activities of Artificial Peroxidases Based on Supramolecular Hydrogels
That Contain Heme Models. Chem. - Eur. J. 2008, 14, 5073−5078.
(9) Liu, C.-J.; Li, S.-G.; Pang, W.-Q.; Che, C.-M. Ruthenium
porphyrin encapsulated in modified mesoporous molecular sieve
MCM-41 for alkene oxidation. Chem. Commun. 1997, 65−66.
(10) Holland, B. T.; Walkup, C.; Stein, A. Encapsulation,
Stabilization, and Catalytic Properties of Flexible Metal Porphyrin
Complexes in MCM-41 with Minimal Electronic Perturbation by the
Environment. J. Phys. Chem. B 1998, 102, 4301−4309.
(11) Cady, S. S.; Pinnavaia, T. Porphyrin intercalation in mica-type
silicates. Inorg. Chem. 1978, 17, 1501−1507.
ASSOCIATED CONTENT
* Supporting Information
The Supporting Information is available free of charge on the
ACS Publications website at DOI: 10.1021/acs.inorg-
chem.7b02612.
■
S
Pawley fitting of PXRDs, additional data, and character-
ization of catalytic products (PDF)
Accession Codes
(12) Kosal, M. E.; Chou, J.-H.; Wilson, S. R.; Suslick, K. S. A
functional zeolite analogue assembled from metalloporphyrins. Nat.
Mater. 2002, 1, 118−121.
(13) Schick, G. A.; Schreiman, I. C.; Wagner, R. W.; Lindsey, J. S.;
Bocian, D. F. Spectroscopic characterization of porphyrin monolayer
assemblies. J. Am. Chem. Soc. 1989, 111, 1344−1350.
(14) Barloy, L.; Battioni, P.; Mansuy, D. Manganese porphyrins
supported on montmorillonite as hydrocarbon mono-oxygenation
catalysts: particular efficacy for linear alkane hydroxylation. J. Chem.
Soc., Chem. Commun. 1990, 1365−1367.
(15) van den Broeke, L. J. P.; de Bruijn, V. G.; Heijnen, J. H. M.;
Keurentjes, J. T. F. Micellar Catalysis for Epoxidation Reactions. Ind.
Eng. Chem. Res. 2001, 40, 5240−5245.
(16) Nestler, O.; Severin, K. A Ruthenium Porphyrin Catalyst
Immobilized in a Highly Cross-linked Polymer. Org. Lett. 2001, 3,
3907−3909.
(17) Yu, X.-Q.; Huang, J.-S.; Yu, W.-Y.; Che, C.-M. Polymer-
Supported Ruthenium Porphyrins: Versatile and Robust Epoxidation
Catalysts with Unusual Selectivity. J. Am. Chem. Soc. 2000, 122, 5337−
5342.
(18) Xue, T.; Jiang, S.; Qu, Y.; Su, Q.; Cheng, R.; Dubin, S.; Chiu, C.-
Y.; Kaner, R.; Huang, Y.; Duan, X. Graphene-Supported Hemin as a
Highly Active Biomimetic Oxidation Catalyst. Angew. Chem. 2012,
124, 3888−3891.
CCDC 1577957−1577958 contain the supplementary crystal-
lographic data for this paper. These data can be obtained free of
charge via www.ccdc.cam.ac.uk/data_request/cif, or by email-
ing data_request@ccdc.cam.ac.uk, or by contacting The
Cambridge Crystallographic Data Centre, 12 Union Road,
Cambridge CB2 1EZ, UK; fax: +44 1223 336033.
AUTHOR INFORMATION
Corresponding Author
*E-mail: Timothy.Egan@uct.ac.za.
■
ORCID
Lee Brammer: 0000-0001-6435-7197
Susan A. Bourne: 0000-0002-2491-2843
Timothy J. Egan: 0000-0001-7720-8473
Notes
The authors declare no competing financial interest.
ACKNOWLEDGMENTS
■
This research was supported by the National Research
Foundation of South Africa (Grant Number
CPRR13082330465). N.A.D. acknowledges the National
K
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
(19) Lv, X.; Weng, J. Ternary Composite of Hemin, Gold
Nanoparticles and Graphene for Highly Efficient Decomposition of
Hydrogen Peroxide. Sci. Rep. 2013, 3, 3285−3295.
(20) Bi, S.; Zhao, T.; Jia, X.; He, P. Magnetic graphene oxide-
supported hemin as peroxidase probe for sensitive detection of thiols
in extracts of cancer cells. Biosens. Bioelectron. 2014, 57, 110−116.
(21) Li, Y.; Huang, X.; Li, Y.; Xu, Y.; Wang, Y.; Zhu, E.; Duan, X.;
Huang, Y. Graphene-hemin hybrid material as effective catalyst for
selective oxidation of primary C-H bond in toluene. Sci. Rep. 2013, 3,
1787−1792.
(22) Kumar, S.; Bhushan, P.; Bhattacharya, S. Facile synthesis of
Au@Ag−hemin decorated reduced graphene oxide sheets: a novel
peroxidase mimetic for ultrasensitive colorimetric detection of
hydrogen peroxide and glucose. RSC Adv. 2017, 7, 37568−37577.
(23) Rayati, S.; Sheybanifard, Z. Catalytic activity of Mn(III) and
Fe(III) porphyrins supported onto multi-walled carbon nanotubes in
the green oxidation of organic dyes with hydrogen peroxide: a
comparative study. J. Iran. Chem. Soc. 2016, 13, 541−546.
(24) Jia, H.; Sun, Z.; Jiang, D.; Yang, S.; Du, P. An iron porphyrin-
based conjugated network wrapped around carbon nanotubes as a
noble-metal-free electrocatalyst for efficient oxygen reduction reaction.
Inorg. Chem. Front. 2016, 3, 821−827.
(25) Li, B. L.; Luo, H. Q.; Lei, J. L.; Li, N. B. Hemin-functionalized
MoS2 nanosheets: enhanced peroxidase-like catalytic activity with a
steady state in aqueous solution. RSC Adv. 2014, 4, 24256−24262.
(26) Liu, Q.; Chen, P.; Xu, Z.; Chen, M.; Ding, Y.; Yue, K.; Xu, J. A
facile strategy to prepare porphyrin functionalized ZnS nanoparticles
and their peroxidase-like catalytic activity for colorimetric sensor of
hydrogen peroxide and glucose. Sens. Actuators, B 2017, 251, 339−348.
(27) Lin, Y.; Wu, L.; Huang, Y.; Ren, J.; Qu, X. Positional assembly of
hemin and gold nanoparticles in graphene−mesoporous silica
nanohybrids for tandem catalysis. Chem. Sci. 2015, 6, 1272−1276.
(28) Thirumalraj, B.; Rajkumar, C.; Chen, S.-M.; Barathi, P. Highly
stable biomolecule supported by gold nanoparticles/graphene nano-
composite as a sensing platform for H2O2 biosensor application. J.
Mater. Chem. B 2016, 4, 6335−6343.
(40) Dhakshinamoorthy, A.; Alvaro, M.; Garcia, H. Metal−organic
frameworks as heterogeneous catalysts for oxidation reactions. Catal.
Sci. Technol. 2011, 1, 856−867.
(41) Chen, Y.; Hoang, T.; Ma, S. Biomimetic Catalysis of a Porous
Iron-Based Metal−Metalloporphyrin Framework. Inorg. Chem. 2012,
51, 12600−12602.
(42) Feng, D.; Gu, Z.-Y.; Li, J.-R.; Jiang, H.-L.; Wei, Z.; Zhou, H.-C.
Zirconium-Metalloporphyrin PCN-222: Mesoporous Metal-Organic
Frameworks with Ultrahigh Stability as Biomimetic Catalysts. Angew.
Chem. 2012, 124, 10453−10456.
(43) Meng, L.; Cheng, Q.; Kim, C.; Gao, W.-Y.; Wojtas, L.; Chen, Y.-
S.; Zaworotko, M. J.; Zhang, X. P.; Ma, S. Crystal Engineering of a
Microporous, Catalytically Active fcu Topology MOF Using a
Custom-Designed Metalloporphyrin Linker. Angew. Chem., Int. Ed.
2012, 51, 10082−10085.
(44) Smithenry, D. W.; Wilson, S. R.; Suslick, K. S. A Robust
Microporous Zinc Porphyrin Framework Solid. Inorg. Chem. 2003, 42,
7719−7721.
(45) Zhang, Z.; Wojtas, L.; Zaworotko, M. J. Three Porphyrin-
Encapsulating Metal−Organic Materials with Ordered Metallopor-
phyrin Moieties. Cryst. Growth Des. 2014, 14, 1526−1530.
(46) Fernandez, M.; Frydman, R. B.; Hurst, J.; Buldain, G. Structure/
activity relationships in porphobilinogen oxygenase and horseradish
peroxidase. An analysis using synthetic hemins. Eur. J. Biochem. 1993,
218, 251−259.
(47) Sugita, Y.; Yoneyama, Y. Oxygen Equilibrium of Hemoglobins
Containing Unnatural Hemes: Effect Of Modification Of Heme
Carboxyl Groups And Side Chains At Positions 2 And 4. J. Biol. Chem.
1971, 246, 389−394.
(48) Larsen, R. W.; Wojtas, L.; Perman, J.; Musselman, R. L.;
Zaworotko, M. J.; Vetromile, C. M. Mimicking Heme Enzymes in the
Solid State: Metal−Organic Materials with Selectively Encapsulated
Heme. J. Am. Chem. Soc. 2011, 133, 10356−10359.
(49) Larsen, R. W.; Miksovska, J.; Musselman, R. L.; Wojtas, L.
Ground- and Excited-State Properties of Zn(II) Tetrakis(4-tetrame-
thylpyridyl) Pophyrin Specifically Encapsulated within a Zn(II)
HKUST Metal−Organic Framework. J. Phys. Chem. A 2011, 115,
11519−11524.
(50) Zhang, Z.; Zhang, L.; Wojtas, L.; Nugent, P.; Eddaoudi, M.;
Zaworotko, M. J. Templated Synthesis, Postsynthetic Metal Exchange,
and Properties of a Porphyrin-Encapsulating Metal−Organic Material.
J. Am. Chem. Soc. 2012, 134, 924−927.
(51) Alkordi, M. H.; Liu, Y.; Larsen, R. W.; Eubank, J. F.; Eddaoudi,
M. Zeolite-like Metal−Organic Frameworks as Platforms for
Applications: On Metalloporphyrin-Based Catalysts. J. Am. Chem.
Soc. 2008, 130, 12639−12641.
(52) Larsen, R. W.; Wojtas, L.; Sagun, E.; Shugla, A.; Bachilo, S.;
Vetromile, C. M.; Yaghi, O. M.; Ess, D. H.; McCafferty, D. G.; Meyer,
T. J. Fixed distance photoinduced electron transfer between Fe and Zn
porphyrins encapsulated within the Zn HKUST-1 metal organic
framework. Dalt. Trans. 2015, 44, 2959−2963.
(53) Ling, P.; Lei, J.; Zhang, L.; Ju, H. Porphyrin-Encapsulated
Metal−Organic Frameworks as Mimetic Catalysts for Electrochemical
DNA Sensing via Allosteric Switch of Hairpin DNA. Anal. Chem. 2015,
87, 3957−3963.
(54) Li, C.; Qiu, W.; Long, W.; Deng, F.; Bai, G.; Zhang, G.; Zi, X.;
He, H. Synthesis of porphyrin@MOFs type catalysts through “one-
pot” self-assembly. J. Mol. Catal. A: Chem. 2014, 393, 166−170.
(55) Zhang, Z.; Gao, W.-Y.; Wojtas, L.; Ma, S.; Eddaoudi, M.;
Zaworotko, M. J. Post-Synthetic Modification of Porphyrin-Encapsu-
lating Metal-Organic Materials by Cooperative Addition of Inorganic
Salts to Enhance CO2/CH4 Selectivity. Angew. Chem., Int. Ed. 2012,
51, 9330−9334.
(29) Zhao, Y.; Zhang, Y.; Liu, A.; Wei, Z.; Liu, S. Construction of
Three-Dimensional Hemin-Functionalized Graphene Hydrogel with
High Mechanical Stability and Adsorption Capacity for Enhancing
Photodegradation of Methylene Blue. ACS Appl. Mater. Interfaces
2017, 9, 4006−4014.
(30) Chakraborty, J.; Nath, I.; Verpoort, F. Snapshots of encapsulated
porphyrins and heme enzymes in metal-organic materials: A prevailing
paradigm of heme mimicry. Coord. Chem. Rev. 2016, 326, 135−163.
(31) García-García, P.; Muller, M.; Corma, A. MOF catalysis in
̈
relation to their homogeneous counterparts and conventional solid
catalysts. Chem. Sci. 2014, 5, 2979−3007.
(32) Qiu, S.; Zhu, G. Molecular engineering for synthesizing novel
structures of metal−organic frameworks with multifunctional proper-
ties. Coord. Chem. Rev. 2009, 253, 2891−2911.
(33) Janiak, C.; Vieth, J. K. MOFs, MILs and more: concepts,
properties and applications for porous coordination networks (PCNs).
New J. Chem. 2010, 34, 2366−2388.
(34) Zhou, H.-C.; Long, J. R.; Yaghi, O. M. Introduction to Metal-
Organic Frameworks. Chem. Rev. 2012, 112, 673−674.
(35) Zhou, H.-C.; Kitagawa, S. Metal-Organic Frameworks (MOFs).
Chem. Soc. Rev. 2014, 43, 5415−5418.
(36) Chen, Y.; Ma, S. Biomimetic catalysis of metal−organic
frameworks. Dalt. Trans. 2016, 45, 9744−9753.
(37) Rowsell, J. L. C.; Yaghi, O. M. Metal−organic frameworks: a
new class of porous materials. Microporous Mesoporous Mater. 2004,
73, 3−14.
́
(38) Corma, A.; García, H.; Llabres i Xamena, F. X. Engineering
(56) Chen, Y.; Wojtas, L.; Ma, S.; Zaworotko, M. J.; Zhang, Z. Post-
synthetic transformation of a Zn(II) polyhedral coordination network
into a new supramolecular isomer of HKUST-1. Chem. Commun.
2017, 53, 8866−8869.
(57) Park, J.; Lee, H.; Bae, Y. E.; Park, K. C.; Ji, H.; Jeong, N. C.; Lee,
M. H.; Kwon, O. J.; Lee, C. Y. Dual-Functional Electrocatalyst Derived
Metal Organic Frameworks for Heterogeneous Catalysis. Chem. Rev.
2010, 110, 4606−4655.
(39) Furukawa, H.; Cordova, K. E.; O’Keeffe, M.; Yaghi, O. M. The
Chemistry and Applications of Metal-Organic Frameworks. Science
2013, 341, 1230444.
L
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
from Iron-Porphyrin- Encapsulated Metal−Organic Frameworks. ACS
Appl. Mater. Interfaces 2017, 9, 28758−28765.
Guest Access As Exemplified by Zn-HKUST-1. J. Am. Chem. Soc. 2011,
133, 18257−18263.
(74) Song, X.; Jeong, S.; Kim, D.; Lah, M. S. Transmetalations in two
metal−organic frameworks with different framework flexibilities:
Kinetics and core−shell heterostructure. CrystEngComm 2012, 14,
5753−5756.
(75) Inokuma, Y.; Yoshioka, S.; Ariyoshi, J.; Arai, T.; Hitora, Y.;
Takada, K.; Matsunaga, S.; Rissanen, K.; Fujita, M. X-ray analysis on
the nanogram to microgram scale using porous complexes. Nature
2013, 495, 461−466.
(76) Asher, C.; de Villiers, K. A.; Egan, T. J. Speciation of
Ferriprotoporphyrin IX in Aqueous and Mixed Aqueous Solution Is
Controlled by Solvent Identity, pH, and Salt Concentration. Inorg.
Chem. 2009, 48, 7994−8003.
(77) Kuter, D.; Venter, G. A.; Naidoo, K. J.; Egan, T. J. Experimental
and Time-Dependent Density Functional Theory Characterization of
the UV−Visible Spectra of Monomeric and μ-Oxo Dimeric
Ferriprotoporphyrin IX. Inorg. Chem. 2012, 51, 10233−10250.
(78) Jessiman, A. S.; MacNicol, D. D.; Mallinson, P. R.; Vallance, I.
Inclusion compound design: the piedfort concept. J. Chem. Soc., Chem.
Commun. 1990, 18, 1619−1621.
(79) Serra, A. C.; Docal, C.; Rocha Gonsalves, A. M. d’A. Efficient
azo dye degradation by hydrogen peroxide oxidation with metal-
loporphyrins as catalysts. J. Mol. Catal. A: Chem. 2005, 238, 192−198.
(80) Ortiz de Montellano, P. R.; De Voss, J. J. Substrate Oxidation by
Cytochrome P450 Enzymes. In Cytochrome P450; Springer US:
Boston, MA, 2005; pp 183−245.
(81) Adams, P. A. The Peroxidasic Activity of the Haem Octapeptide
Microperoxidase-8 (MP-8): The Kinetic Mechanism of the Catalytic
Reduction of H2O2 by MP-8 using 2,Z’- Azinobis-(3-ethylbenzothia-
zoline-6-sulphonate) (ABTS) as Reducing Substrate. J. Chem. Soc.,
Perkin Trans. 2 1990, 2, 1407−1414.
(82) Brausam, A.; Eigler, S.; Jux, N.; van Eldik, R. Mechanistic
Investigations of the Reaction of an Iron(III) Octa-Anionic Porphyrin
Complex with Hydrogen Peroxide and the Catalyzed Oxidation of
Diammonium-2,2′-azinobis(3-ethylbenzothiazoline-6-sulfonate). Inorg.
Chem. 2009, 48, 7667−7678.
(58) Zhang, Z.; Gao, W.-Y.; Wojtas, L.; Ma, S.; Eddaoudi, M.;
Zaworotko, M. J. Metal−Organic Frameworks Post-Synthetic
Modification of Porphyrin-Encapsulating Metal−Organic Materials
by Cooperative Addition of Inorganic Salts to Enhance CO2/CH4
Selectivity. Angew. Chem., Int. Ed. 2012, 51, 9330−9334.
(59) Xie, S.; Ye, J.; Yuan, Y.; Chai, Y.; Yuan, R. A multifunctional
hemin@metal−organic framework and its application to construct an
electrochemical aptasensor for thrombin detection. Nanoscale 2015, 7,
18232−18238.
(60) Wang, L.; Yang, H.; He, J.; Zhang, Y.; Yu, J.; song, Y. Cu-Hemin
Metal-Organic-Frameworks/Chitosan-Reduced Graphene Oxide
Nanocomposites with Peroxidase-Like Bioactivity for Electrochemical
Sensing. Electrochim. Acta 2016, 213, 691−697.
(61) Yuan, G.; Wang, L.; Mao, D.; Wang, F.; Zhang, J. Voltammetric
hybridization assay for the β1-adrenergic receptor gene (ADRB1), a
marker for hypertension, by using a metal organic framework (Fe-
MIL-88NH2) with immobilized copper(II) ions. Microchim. Acta
2017, 184, 3121−3130.
(62) He, J.; Yang, H.; Zhang, Y.; Yu, J.; Miao, L.; Song, Y.; Wang, L.
Smart Nanocomposites of Cu-Hemin Metal-Organic Frameworks for
Electrochemical Glucose Biosensing. Sci. Rep. 2016, 6, 36637.
(63) Zhou, X.; Guo, S.; Gao, J.; Zhao, J.; Xue, S.; Xu, W. Glucose
oxidase-initiated cascade catalysis for sensitive impedimetric aptasensor
based on metal-organic frameworks functionalized with Pt nano-
particles and hemin/G-quadruplex as mimicking peroxidases. Biosens.
Bioelectron. 2017, 98, 83−90.
(64) Cheng, H.; Zhang, L.; He, J.; Guo, W.; Zhou, Z.; Zhang, X.; Nie,
S.; Wei, H. Integrated Nanozymes with Nanoscale Proximity for in
Vivo Neurochemical Monitoring in Living Brains. Anal. Chem. 2016,
88, 5489−5497.
(65) Luo, F.; Lin, Y.; Zheng, L.; Lin, X.; Chi, Y. Encapsulation of
Hemin in Metal−Organic Frameworks for Catalyzing the Chem-
iluminescence Reaction of the H2O2−Luminol System and Detecting
Glucose in the Neutral Condition. ACS Appl. Mater. Interfaces 2015, 7,
11322−11329.
(66) Zhu, Q.; Chen, Y.; Wang, W.; Zhang, H.; Ren, C.; Chen, H.;
Chen, X. A sensitive biosensor for dopamine determination based on
the unique catalytic chemiluminescence of metal−organic framework
HKUST-1. Sens. Actuators, B 2015, 210, 500−507.
(67) Tan, H.; Li, Q.; Zhou, Z.; Ma, C.; Song, Y.; Xu, L.; Wang, L. A
sensitive fluorescent assay for thiamine based on metal-organic
frameworks with intrinsic peroxidase-like activity. Anal. Chim. Acta
2015, 856, 90−95.
(68) Qin, F.-X.; Jia, S.-Y.; Wang, F.-F.; Wu, S.-H.; Song, J.; Liu, Y.
Hemin@metal−organic framework with peroxidase-like activity and its
application to glucose detection. Catal. Sci. Technol. 2013, 3, 2761−
2768.
(83) Childs, R. E.; Bardsley, W. G. The steady-state kinetics of
peroxidase with 2,2’-azino-di-(3-ethyl-benzthiazoline-6-sulphonic acid)
as chromogen. Biochem. J. 1975, 145, 93−103.
(84) GraphPad Prism v6.05; GraphPad Software: San Diego, CA,
2014.
(85) ChemAxon. Chemicalize; 2017.
(86) de Villiers, K. A.; Kaschula, C. H.; Egan, T. J.; Marques, H. M.
Speciation and structure of ferriprotoporphyrin IX in aqueous
solution: spectroscopic and diffusion measurements demonstrate
dimerization, but not μ-oxo dimer formation. JBIC, J. Biol. Inorg.
Chem. 2007, 12, 101−117.
́ ́
(87) García, E.; Medina, R.; Lozano, M.; Hernandez Perez, I.; Valero,
M.; Franco, A. Adsorption of Azo-Dye Orange II from Aqueous
Solutions Using a Metal-Organic Framework Material: Iron-
Benzenetricarboxylate. Materials 2014, 7, 8037−8057.
(69) Yang, S.; Sun, J.; Ramirez-Cuesta, A. J.; Callear, S. K.; David, W.
I. F.; Anderson, D. P.; Newby, R.; Blake, A. J.; Parker, J. E.; Tang, C.
C.; Schroder, M. Selectivity and direct visualization of carbon dioxide
̈
(88) Nowell, H.; Barnett, S. A.; Christensen, K. E.; Teat, S. J.; Allan,
D. R. I19, the small-molecule single-crystal diffraction beamline at
Diamond Light Source. J. Synchrotron Radiat. 2012, 19, 435−441.
(89) Oxford Diffraction. CrysAlis Pro; Rigaku Corporation: Oxford,
UK, 2017.
and sulfur dioxide in a decorated porous host. Nat. Chem. 2012, 4,
887−894.
(70) Sun, D.; Ke, Y.; Collins, D. J.; Lorigan, G. A.; Zhou, H.-C.
Construction of Robust Open Metal−Organic Frameworks with
Chiral Channels and Permanent Porosity. Inorg. Chem. 2007, 46,
2725−2734.
(90) Wilson, K. S.; Dodson, E. J.; Di Marco, S.; Priestle, J. P.;
Gruttler, M. G.; Mittl, P. R. E.; De La Rose, M. A.; Sheldrick, G. M. A
̈
(71) Macrae, C. F.; Edgington, P. R.; McCabe, P.; Pidcock, E.;
Shields, G. P.; Taylor, R.; Towler, M.; Van De Streek, J. Mercury:
Visualization and analysis of crystal structures. J. Appl. Crystallogr.
2006, 39, 453−457.
short history of SHELX. Acta Crystallogr., Sect. A: Found. Crystallogr.
2008, 64, 112−122.
(91) Dolomanov, O. V.; Bourhis, L. J.; Gildea, R. J.; Howard, J. A. K.;
Puschmann, H. OLEX2: a complete structure solution, refinement and
analysis program. J. Appl. Crystallogr. 2009, 42, 339−341.
(92) Pawley, G. S. Unit-cell refinement from powder diffraction
scans. J. Appl. Crystallogr. 1981, 14, 357−361.
(72) Macrae, C. F.; Bruno, I. J.; Chisholm, J. A.; Edgington, P. R.;
McCabe, P.; Pidcock, E.; Rodriguez-Monge, L.; Taylor, R.; van de
Streek, J.; Wood, P. A. Mercury CSD 2.0 − new features for the
visualization and investigation of crystal structures. J. Appl. Crystallogr.
2008, 41, 466−470.
(93) Bruker AXS. DiffracPlus Topas v. 4.2; 2009.
(73) Feldblyum, J. I.; Liu, M.; Gidley, D. W.; Matzger, A. J.
Reconciling the Discrepancies between Crystallographic Porosity and
M
DOI: 10.1021/acs.inorgchem.7b02612
Inorg. Chem. XXXX, XXX, XXX−XXX