Biomimetic catalysis of a porous iron-based metal-metalloporphyrin framework

Article abstract of DOI:10.1021/ic301923x

A porous metal-metalloporphyrin framework, MMPF-6, based upon an iron(III)-metalated porphyrin ligand and a secondary binding unit of a zirconium oxide cluster was constructed; MMPF-6 demonstrated interesting peroxidase activity comparable to that of the heme protein myoglobin as well as exhibited solvent adaptability of retaining the peroxidase activity in an organic solvent.

Full text of DOI:10.1021/ic301923x

Communication
pubs.acs.org/IC
Biomimetic Catalysis of a Porous Iron-Based Metal−
Metalloporphyrin Framework
Yao Chen, Tran Hoang, and Shengqian Ma*
Department of Chemistry, University of South Florida, 4202 East Fowler Avenue, Tampa, Florida 33620, United States
S
* Supporting Information
ABSTRACT: A porous metal−metalloporphyrin frame-
work, MMPF-6, based upon an iron(III)-metalated
porphyrin ligand and a secondary binding unit of a
zirconium oxide cluster was constructed; MMPF-6
demonstrated interesting peroxidase activity comparable
to that of the heme protein myoglobin as well as exhibited
solvent adaptability of retaining the peroxidase activity in
an organic solvent.
s new types of functional materials, porous metal−organic
Aframeworks (MOFs) have experienced rapid development
over the past decade.1 Their amenability to be designed with
specific functionality makes them stand out from traditional
porous materials2 and affords them great potential for various
applications, such as gas storage/separation,3 CO2 capture,4
sensors,5 and catalysis.6 Their tunable pore spaces and
functional pore walls7 also provide a new opportunity for
biomimetic catalysis, which, however, has rarely been explored.8
To develop porous MOFs as platforms for biomimetic catalysis,
one can utilize their pore systems to directly immobilize
enzymes/proteins9 or selectively encapsulate the active centers
of enzymes into the cavities of MOFs8 or one can regularly
arrange the active centers of enzymes into MOF frameworks
using the derivatives of active center molecules as struts.10 The
later strategy is particularly appealing to mimic heme proteins
because iron porphyrin that is the active center (iron
protoporphyrin IX) of heme proteins can be readily function-
alized as struts for the construction of MOFs.11 In a
continuation of our work on the development of porous
metal−metalloporphyrin frameworks (MMPFs),12 herein we
report an iron-based MMPF, MMPF-6, which demonstrates
interesting peroxidase activity comparable to that of the heme
protein myoglobin (Mb).
Figure 1. (a) Iron(III) meso-tetrakis(4-carboxyphenyl)porphyrin
chloride ligand. (b) Zr6O8(CO2)8(H2O)8 SBU. (c) Hexagonal and
triangular 1D channels of MMPF-6. Color scheme: C, gray; O, red; Cl,
green; Zr, turquoise.
Supporting Information, SI). The permanent porosity of
MMPF-6 was assessed by N2 sorption at 77 K (Figure 2),
which revealed a typical type IV isotherm14 and a Brunauer−
Emmett−Teller surface area of 2100 m2/g comparable to that
Dark-red block crystals of MMPF-6 were obtained by
reacting iron(III) meso-tetrakis(4-carboxyphenyl)porphyrin
chloride (Fe-TCPP-Cl; Figure 1a) with zirconyl chloride
under solvothermal conditions. Single-crystal X-ray studies
revealed that MMPF-6 has the same structure as the recently
reported MOF-545-Fe,13 in which the Fe-TCPP-Cl ligands
connect with the in situ generated secondary building units
(SBUs) of Zr6O8(CO2)8(H2O)8 (Figure 1b) to form a three-
dimensional structure consisting of hexagonal and triangular
one-dimensional (1D) channels that have diameters of ∼36 and
∼12 Å (atom-to-atom distance), respectively (Figure 1c). The
phase purity of the bulk sample MMPF-6 was confirmed by
powder X-ray diffraction (PXRD) studies (Figure S1 in the
Figure 2. N2 sorption isotherms of MMPF-6 at 77 K (inset: pore-size
distribution based upon the DFT model).
Received: September 3, 2012
Published: November 20, 2012
© 2012 American Chemical Society
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dx.doi.org/10.1021/ic301923x | Inorg. Chem. 2012, 51, 12600−12602

Inorganic Chemistry
Communication
reported in the literature.13 The pore-size distribution analysis
based upon N2 adsorption data at 77 K by the use of a density
functional theory (DFT) model revealed that the pore sizes of
MMPF-6 are predominantly around 11 and 33 Å (Figure 2,
inset), which are close to the channel sizes observed
crystallographically.
It is well-known that heme is the catalytic center for heme
proteins, including cytochromes, peroxidases, myoglobins, and
hemoglobins, and is capable of performing peroxidation of
organic substrates by the use of hydrogen peroxide.15 The
peroxidase activity of heme proteins can be assessed with some
standard assays of selected substrates by monitoring the rate of
increase in absorbance at feature wavelengths of the oxidation
products subsequent to the addition of peroxide, such as
oxidation of 1,2,3-trihydroxybenzene (THB) to purpurogallin
(420 nm) involving oxygen transfer16a and oxidation of 2,2′-
azinodi(3-ethylbenzothiazoline)-6-sulfonate (ABTS) to
ABTS•+ (660 nm) involving electron transfer16b (Scheme 1).
Scheme 1. Reaction Schemes for Oxidation of THB (Top)
and ABTS (Bottom) by Hydrogen Peroxide Catalyzed by a
Heme-Based Catalyst
Figure 3. Kinetic traces for oxidation of THB in (a) HEPES buffer and
(b) an ethanol solution and oxidation ABTS in (c) HEPES buffer and
(d) an ethanol solution.
mM/s for ABTS•+ formation, which is about one-fourth that for
free Mb in HEPES buffer (Figure 3c and Table 1). We
reasoned that the slower initial rate for MMPF-6 compared to
free Mb should originate from diffusion of the substrates from
solution into the channels of MMPF-6. MMPF-6(Fr)
demonstrated much lower activities for both reactions
compared to MMPF-6 (Figure 3a,c and Table 1), indicating
insignificant contributions from the framework and zirconium
oxide cluster. MMPF-6 can be reused for four cycles without a
significant drop in its peroxidase activity (Table 1) and can also
retain its framework integrity, as confirmed by PXRD studies
(Figure S1 in the SI), highlighting its heterogeneous feature.
We also assessed the peroxidase activity of MMPF-6 in
organic solvents, in which heme proteins are known to easily
lose their activities.17 Catalytic assays performed in ethanol
solutions indicated that MMPF-6 demonstrated an initial rate
of 4.34 × 10−4 mM/s for purpurogallin formation and 7.56 ×
10−5 mM/s for ABTS•+ formation (Figure 3b,d), meaning an
enhancement of ∼107 and ∼215 times, respectively, for the
reactions without catalyst (Table 1). In comparison, free Mb
exhibited a much slower initial rate (Table1 and Figure 3b,d)
because of the agglomeration of Mb molecules in ethanol.17
Slow initial rates were observed for MMPF-6(Fr), furthering
supporting the essential role of heme centers in MMPF-6 for
the peroxidase activities.
In summary, a porous iron-based MMPF, MMPF-6, was
constructed by self-assembly of the iron(III) meso-tetrakis(4-
carboxyphenyl)porphyrin chloride ligand with the in situ
generated Zr6O8(CO2)8(H2O)8 SBU under solvothermal
conditions. MMPF-6 demonstrated interesting peroxidase
activity comparable to that of the heme protein Mb in terms
of the initial reaction rates in buffer solutions. MMPF-6
retained the peroxidase activity in an ethanol solution,
highlighting its adaptability for organic solvents. This work
paves a way to develop MOFs as a new type of biomimetic
catalyst and also opens up new perspectives for mimicking
heme-based proteins. Ongoing work in our laboratory includes
the design and synthesis of new iron-based MMPFs for
biomimetic catalysis.
The regular arrangement of hemes [iron(III) porphyrin
macrocycles] with the five-coordinate iron(III) centers oriented
toward the channels in MMPF-6 prompted us to evaluate the
potential peroxidase activity of MMPF-6. Catalytic assays were
conducted for MMPF-6 and compared with the heme protein
Mb. Mb is an oxygen storage protein,17 and its peroxidase
activity has also been widely studied,18 although the activity is
lower than that of native peroxidase.19
Before catalytic assays, the content of the heme centers in
MMPF-6 was measured to be 6.18 × 10−4 mol/g by inductively
coupled plasma mass spectrometry experiments on the
activated MMPF-6 sample. The relatively lower measured
content of the heme centers compared to that estimated from
the single-crystal X-ray crystallography derived formula (7.98 ×
10−4 mol/g) should be attributed to the incomplete removal of
the high-boiling-point guest N,N-dimethylformamide molecules
during the activation process. Free-base MMPF-6, MMPF-
6(Fr), was also synthesized (Figure S1 in the SI) for control
experiments.
As shown in Figure 3, without catalyst, the blank reaction is
going very slowly with rates of only 3.47 × 10−5 mM/s for THB
oxidation and 2.87 × 10−6 mM/s for ABTS oxidation (Table 1)
in 4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid
(HEPES) buffer. MMPF-6 indicates a very fast initial rate of
1.39 × 10−3 mM/s for purpurogallin formation,20 which is
about one-third as fast as free Mb in HEPES buffer (Figure 3a
and Table 1). Notably, MMPF-6 demonstrates impressive
activity not only for oxidation involving oxygen transfer but also
for oxidation involving electron transfer. In the context of
ABTS oxidation, it exhibits a fast initial rate of 8.18 × 10−4
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Inorganic Chemistry
Communication
Table 1. Summary of Catalysis Results of Oxidation of THB and ABTS in the Presence of 10 mM H2O2
initial rate for purpurogallin formation
initial rate for purpurogallin
formation in ethanol (mM/s)
initial rate for ABTS•+ formation in initial rate for ABTS•+ formation
in HEPES buffer (mM/s)
HEPES buffer (mM/s)
in ethanol (mM/s)
blank
3.47 × 10−5
3.37 × 10−3
1.39 × 10−3
9.89 × 10−5
4.29 × 10−6
4.59 × 10−5
4.34 × 10−4
6.62 × 10−5
2.87 × 10−6
3.54 × 10−3
8.18 × 10−4
2.82 × 10−5
3.51 × 10−7
1.87 × 10−5
7.56 × 10−5
1.65 × 10−5
a
free Mb
MMPF-6
MMPF-
6(Fr)
MMPF-
9.06 × 10−4
6.96 × 10−5
6.26 × 10−4
6.96 × 10−5
b
6
a
b
Diluted to 5 μM. The fourth cycle.
(9) (a) Lykourinou, V.; Chen, Y.; Wang, X.-S.; Meng, L.; Hoang, T.;
ASSOCIATED CONTENT
■
Ming, L.-J.; Musselman, R. L.; Ma, S. J. Am. Chem. Soc. 2011, 133,
10382. (b) Chen, Y.; Lykourinou, V.; Vetromile, C.; Hoang, T.; Ming,
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Y.; Lykourinou, V.; Hoang, T.; Ming, L.-J.; Ma, S. Inorg. Chem. 2012,
51, 9156−9158.
S
* Supporting Information
Experimental procedures and PXRD patterns. This material is
available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
■
Corresponding Author
*E-mail: sqma@usf.edu.
Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS
■
S.M. acknowledges the University of South Florida for financial
support of this work.
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