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Feb 6, 2017 - ABSTRACT: We investigate the correlations between the redox potentials of nonalkylated cobalt corrinoids and the Co−C bond dissociatio...
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Redox Potentials of Cobalt Corrinoids with Axial Ligands Correlate with Heterolytic Co−C Bond Dissociation Energies Yoshitsugu Morita,†,‡ Koji Oohora,†,§,⊥ Akiyoshi Sawada,‡ Takashi Kamachi,‡,# Kazunari Yoshizawa,‡,# and Takashi Hayashi*,† †

Department of Applied Chemistry, Graduate School of Engineering, Osaka University, Suita 565-0871, Japan Institute for Materials Chemistry and Engineering and IRCCS, Kyushu University, Nishi-ku, Fukuoka 819-0395, Japan § PRESTO, JST, Kawaguchi 332-0012, Japan ⊥ Frontier Research Base for Global Young Researchers, Graduate School of Engineering, Osaka University, Suita 565-0871, Japan # Elements Strategy Initiative for Catalysts and Batteries (ESICB), Kyoto University, Nishikyo-ku, Kyoto 615-8520, Japan ‡

S Supporting Information *

ABSTRACT: We investigate the correlations between the redox potentials of nonalkylated cobalt corrinoids and the Co−C bond dissociation energies (BDEs) of the methylated species with an aqua or histidine axial ligand. A set of cobalt corrinoids, cobalamin, and its model systems, which include new version of myoglobin reconstituted with cobalt didehydrocorrin, are investigated. The Co(III)/Co(II) and Co(II)/Co(I) redox potentials of myoglobin reconstituted with cobalt tetradehydrocorrin and didehydrocorrin and the bare cofactors were determined. Density functional theory (DFT) calculations were performed to estimate the Co−C BDEs of the methylated species. It is found that the redox potentials correlate well with the heterolytic BDEs, which are dependent on the electronegativity of the corrinoid frameworks. The present study offers two important insights into our understanding of how enzymes promote the reactions: (i) homolysis is promoted by strong axial ligation and (ii) heterolysis is controlled by the redox potentials, which are regulated by the saturated framework and axial ligation in the enzyme.

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INTRODUCTION

cobalamin-dependent enzymes, cobalamin is generally coordinated by a histidine residue or a peripherally attached 6,7dimethylbenzimidazole (DMB) moiety as an axial ligand. One important aspect of the cofactor is its ability to generate an organometallic alkylcobalamin species whose Co−C bond dissociates via homolytic or heterolytic process in the enzymatic reactions.1,2 To better understand the mechanism of the unique reactions, the Co−C bonds of cobalt corrinoids have been investigated.3−5 Although the electrochemical properties of the alkylated cobalt corrinoid derivatives would give us important insights into the thermodynamic stabilities and reactivities of the Co−C bonds, examples of relevant redox potentials are quite limited because of the large negative reduction potentials and irreversible cyclic voltammograms of the cobalt complexes.6 In contrast, redox potentials of nonalkylated cobalt corrinoids in several solvents and cobalamin bound in the cobalamin-dependent enzymes have been determined.5,7,8 In this context, we hypothesized that the redox potentials of nonalkylated and alkylated cobalt corrinoids would be reflected in the chemical properties of the corrinoid frameworks and axial ligands. Furthermore, these potentials

Cobalamin, a metallocofactor, is a cobalt complex with a highly saturated corrinoid framework (Figure 1).1 In a series of

Figure 1. Chemical structures of Co(TDHC), Co(DDHC) and cobalamin with axial ligands. X = CH3−, H2O, or OH−; Lax = His, Im, H2O, or DMB; R = DMB-linked side chain. © XXXX American Chemical Society

Received: October 19, 2016

A

DOI: 10.1021/acs.inorgchem.6b02482 Inorg. Chem. XXXX, XXX, XXX−XXX

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Inorganic Chemistry

Electrochemical Measurements. Reconstituted Proteins. Spectroelectrochemical measurements were carried out at 25 °C using an optically transparent thin-layer electrode cell (optical path length of 1 mm) under an argon atmosphere. A Pt wire counter electrode and a Pt mesh working electrode were used, along with an Ag|AgCl reference electrode. The potentials of these electrodes were controlled and measured with CompactStat potentiostat (Ivium Technologies). The redox potential of the Ag|AgCl electrode was determined by a cyclic ′ voltammetry (CV) measurement of 0.1 M K3[Fe(CN)6] (EFe(III)/Fe(II) = 0.436 V vs NHE at pH 7)11 in 0.1 M potassium phosphate buffer solution at pH 7.0 prior to the experiment. A solution of rMb(CoII(TDHC)) (0.1 mM) was prepared in 0.1 M potassium phosphate buffer solution at pH 7.0 containing 1,1′-ferrocenedimethanol (1 mM) as an electron mediator. At each applied potential, the electronic absorption spectra were monitored until no further spectral changes were detected. The Nernst plots were obtained from the absorption changes at 510 nm of [rMb(CoIII(TDHC))]/[rMb(CoII(TDHC))] and the data were fitted to the Nernst equation. The resulting midpoint of the redox potential was determined with reference to the normal hydrogen electrode (NHE). In the case of rMb(CoIII(DDHC)), the protein solution (0.4 mM) in 0.1 M potassium phosphate buffer solution at pH 7.0 containing 2,3,5,6-tetramethylphenylene-14-diamine (0.45 mM) as an electron mediator was used. The redox potential was determined using the above method. Cofactors. The cyclic voltammogram measurements were performed at 25 °C under an argon atmosphere using a three-electrode cell equipped with a 1.6 mm diameter platinum electrode, a 0.5 mm diameter platinum wire electrode, and an Ag|AgCl electrode with a 3 M NaCl aqueous solution as working, counter and reference electrodes, respectively. A solution of CoII(TDHC) or CoII(DDHC) (2 mM) was prepared in 0.1 M potassium phosphate buffer solution at pH 7.0. To estimate the Co(II)/Co(I)-redox potential of Co(DDHC), the differential pulse voltammogram measurement was performed at 25 °C under an argon atmosphere using a three-electrode cell equipped with a 1.6-mm-diameter glassy carbon electrode, a 0.5-mm-diameter platinum wire electrode, and an Ag|AgCl electrode with a 3 M NaCl aqueous solution as working, counter, and reference electrodes, respectively. A solution of CoII(DDHC) (1.1 mM) in 0.1 M potassium phosphate buffer solution at pH 7.0 was used. The potentials of these electrodes were controlled and measured with CompactStat potentiostat (Ivium Technologies) using following parameters: pulse time, 10 ms; pulse amplitude, 10 mV; E step, 5 mV; scan rate, 0.1 V s−1; and equilibration time, 20 s. Computational Chemistry. We used the Becke−Perdew (BP86)12a,b method implemented in the Gaussian 09 program. For all atoms, the 6-31G(d) basis set was used. This level of theory BP86/ 6-31G(d) serves as an appropriate platform for addressing the structural, electronic, and spectroscopic properties of cobalamin cofactors.13,14 All calculations were carried out in the gas phase. As truncated models of cobalamin, Co(DDHC) and Co(TDHC), we used Co(corrin), Co(DDHC′) and Co(TDHC′), respectively, where all of the peripheral side chains are replaced with hydrogen atoms for the DFT calculations. Imidazole (Im) was used as a simplified model of the axial histidine residue (His93). The BDEs of the Co−C bonds of the Im- and H2O-coordinated cobalt corrinoid complexes are defined by the following equations:

may correlate with the physicochemical properties of the Co−C bonds of methylated species. This information would be useful in efforts to elucidate the mechanism of the enzymatic reactions. However, the quantitative correlation has not yet been demonstrated.5 Here, we investigate the correlations between the redox potentials of nonalkylated cobalt corrinoids and the Co−C bond dissociation energies (BDEs) of the methylated species with an aqua or histidine axial ligand (Figure 1).

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EXPERIMENTALS

Instruments. Ultraviolet−visible light (UV-vis) spectral measurements were carried out with a Shimadzu Model UV-3150 or Model UV-2550 double-beam spectrophotometer, or a Shimadzu BioSpecnano spectrometer. Electrospray ionization−time-of-flight mass spectroscopy (ESI-TOF MS) analyses were performed with a Bruker Daltonics micrOTOF II mass spectrometer. ICP-OES (inductively coupled plasma−optical emission spectroscopy) was performed on a Shimadzu Model ICPS-7510 emission spectrometer. The pH measurements were made with a Horiba Model F-52 pH meter. Materials. All reagents of the highest guaranteed grade available were obtained from commercial sources and were used as received, unless otherwise indicated. Distilled water was demineralized using a Barnstead NANOpure DIamond or Millipore Integral3 apparatus. Synthesis of tetradehydrocorrin cobalt complex, CoII(TDHC), and preparation of myoglobin reconstituted with CoII(TDHC), rMb(CoII(TDHC)), were reported in our previous paper.9 Didehydrocorrin cobalt complex was prepared according to procedures in the literature.5a,b Native horse heart myoglobin (Sigma−Aldrich) was purified with a cation exchange CM-52 cellulose column. The apoprotein was prepared according to Teale’s method.10 A cobalt standard solution for ICP-OES was purchased from Wako Pure Chemical Industries. Preparation of Didehydrocorrin Cobalt(II) Complex, CoII(DDHC). In an autoclave, 10% palladium on carbon (7 mg) was added into a solution of CoII(TDHC)9 (5.0 mg, 7.5 μmol) in methanol (2 mL) containing acetic acid (0.02 mL) and hydrogenation was performed under 1.2 MPa of H2 atmosphere at 85 °C for 2 h (Scheme 1). The palladium on carbon was removed by filtration and

Scheme 1. Synthesis of Co(DDHC)

then the filtrate was concentrated under reduced pressure. The residue was dissolved into a minimum amount of CH2Cl2 and reprecipitated with hexane to yield didehydrocorrin cobalt complex, CoII(DDHC), as brown powder. (2.9 mg, 4.5 μmol, 58%). HR-MS (ESI, positive mode): m/z = 616.245, [M−Cl]+; calcd. C33H41N4O4Co, 616.246. Incorporation of Co(DDHC) into Apomyoglobin. A Co(DDHC) solution (1 mM, 0.4 mL, 0.4 μmol) in 0.1 M potassium phosphate buffer at pH 7.0 was added dropwise into 1 mL of apomyoglobin solution (0.1 mM, 0.1 μmol) with gently shaking on an ice bath. After equilibrating at 4 °C under an aerobic condition overnight, the mixture was concentrated by ultrafiltration. The protein containing Co(DDHC) was purified by passing it through a HiTrap Desalting column (5 mL, GE Healthcare) with 0.1 M potassium phosphate buffer at pH 7.0. The eluted fractions were concentrated and stored in darkness at −80 °C. The molar coefficient at 507 nm was determined to be 8.22 mM−1 cm−1 by an ICP-OES measurement. ESITOF MS (ESI, negative mode): m/z = 2508.30; calculated m/z (z) for rMb(CoIII(DDHC)) (C802H1251N214O222S2Co) = 2508.31 (7−).

for homolytic cleavage: BDE = E(CoII(Leq)(Lax)) + E(•CH3) − E(CoIII(CH3)(Leq)(Lax))

for heterolytic cleavage:

BDE = E(CoI(Leq)) + E(CH3+) + E(Lax) − E(CoIII(CH3)(Leq)(Lax)) where E(X) is the energy of the optimized structure of X; Leq is an equatorial ligand; and Lax is an axial ligand (Im or H2O). The dielectric B

DOI: 10.1021/acs.inorgchem.6b02482 Inorg. Chem. XXXX, XXX, XXX−XXX

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Inorganic Chemistry effects of protein environment and aqueous media on the BDEs were estimated at the BP86/SV(P) level of theory by using the conductorlike screening model 13g (COSMO) implemented in the TURBOMOLE program. For protein environment, the dielectric constant was chosen to be 4, which is a standard value that has been used in previous studies.15 For aqueous media, the dielectric constant was chosen to be 74.8, which is a standard value of the aqueous solution. To estimate the electronegativity of the free base of the corrinoids, we used the Becke−Perdew method,12b,c as implemented in the Turbomole package (version 7.0, Turbomole GmbH, Germany), according to the literature.16

imidazole (10 mM) (see Figure 2b, as well as Figure S1 in the Supporting Information). These results indicate that Co(DDHC) is coordinated by the His93 residue in the heme pocket of myoglobin.5b Redox Potentials of the Cobalamin Models. The Co(III)/Co(II)-redox potentials of rMb(Co(DDHC)) and rMb(Co(TDHC))9 were determined by spectroelectrochemical measurements to be 0.30 and 0.51 V, respectively (see Figure S2 in the Supporting Information). All redox potentials in this work are represented vs NHE. The value of rMb(Co(DDHC)) is closer to that of cobalamin bound to methionine synthase (MetH, 0.27 V)8 than that of rMb(Co(TDHC)). As base-off models, the Co(II)/Co(I)- and Co(III)/Co(II)-redox potentials of the bare cofactors were also determined by cyclic voltammetry or differential pulse voltammetry in 0.1 M potassium phosphate buffer at pH 7.0 (Figure S3 in the Supporting Information) and the values are

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RESULTS AND DISCUSSION Preparation of Didehydrocorrin Cobalt(II) Complex, CoII(DDHC). Previously, we reported on our efforts to reconstitute myoglobin with cobalt tetradehydrocorrin (Co(TDHC)), rMb(Co(TDHC)), as a His-on model of cobalamin-dependent enzymes.9,17 The Co(II) and Co(III) species have penta- and hexa-coordinated structures with histidine-ligation, respectively, while the Co(I) species has a tetra-coordinated structure without histidine-ligation.9,17 As another model, cobalt didehydrocorrin with two propionate groups, Co(DDHC), was prepared for the present study (Figure 1). The corrinoid framework of Co(TDHC) was hydrogenated with 10% Pd on carbon in methanol containing 1% acetic acid under 1.2 MPa H2 to yield Co(DDHC) (Scheme 1).5b The product was identified by ESI-TOF MS (m/ z = 616.245; calculated m/z for [M−Cl]+ = 616.246). Myoglobin reconstituted with Co(DDHC), rMb(Co(DDHC)), was obtained by the conventional method (Figure 2a).10 The ESI-TOF MS spectrum shows that the cobalt cofactor is incorporated into apomyoglobin (apoMb) in a 1:1 ratio (found m/z = 2508.30; calculated m/z (z) for rMb(CoIII(DDHC)) = 2508.31 (7−)). The UV-vis spectrum of rMb(CoIII(DDHC)) is clearly consistent with that of CoIII(DDHC) in 0.1 M potassium phosphate buffer containing

Table 1. Redox Potentials of the Reconstituted Proteins and Cofactors in Aqueous Solutions Redox Potentials (V vs NHE) complex

Co(II)/Co(I)

Co(III)/Co(II)

rMb(Co(TDHC)) Co(TDHC)b rMb(Co(DDHC))b Co(DDHC)b cobalamin in MetHd cobinamidee

−0.13 −0.07 n.d.c −0.49 −0.53 −0.50

0.51b 0.59 0.30 0.45 0.27 0.51

a

a Data taken from ref 9. bData taken from this work. cAlthough the potential was not determined, rMb(CoII(DDHC)) can be reduced by sodium tetrahydroborate. dData taken from ref 8. Cobalamin is bound in MetH as a His-on/base-off form. eData taken from ref 18. Base-off form.

summarized in Table 1. The redox potentials decrease as follows: Co(TDHC) > Co(DDHC) > cobalamin

and the axial ligand exchange from H2O to the histidine residue decreases the redox potentials (Figure S4 in the Supporting Information).9,18 The redox potential trend was investigated in theoretical studies. We used Co(TDHC′), Co(DDHC′), and Co(corrin) as truncated models of Co(TDHC), Co(DDHC), and cobalamin, respectively, where all of the peripheral side chains are replaced with hydrogen atoms (Figure S5 in the Supporting Information).17 Imidazole (Im) was used as an axial ligand in a His-on model. In contrast, H2O was used as an axial ligand for a His-off model, because base-off cobalamin is coordinated by a water molecule in aqueous solution.1 The redox potentials are in good agreement with corresponding computed values for the cobalt corrinoid models with an Im or aqua axial ligand (Figure S6 in the Supporting Information). Furthermore, DFT calculations support the negative shift of the redox potential upon Im-coordination, indicating that the histidine ligation efficiently stabilizes the high valent cobalt species, relative to H2O ligation (Figure S7 in the Supporting Information). Correlation between the Redox Potentials and the Bond Dissociation Energies (BDEs). To investigate the correlation between the redox potentials of nonalkylated cobalt corrinoids and the properties of the Co−C bond, we estimated

Figure 2. (a) Preparation of myoglobin reconstituted with Co(DDHC). (b) UV-vis spectra of apoMb (black dashed line) and rMb(CoIII(DDHC)) (red solid line) in 0.1 M potassium phosphate buffer at pH 7 at 25 °C. C

DOI: 10.1021/acs.inorgchem.6b02482 Inorg. Chem. XXXX, XXX, XXX−XXX

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Table 2. DFT-Computed Homolytic and Heterolytic Bond-Dissociation Energies (BDEs) of the Co−C Bonds in CoIII(CH3) (Cor)(Lax)a and Stabilization Energy Induced by the Axial Ligand Exchange in the Gas Phaseb Homolytic BDE (kcal mol−1) cobalt corrinoid III

c

Co (CH3) (TDHC′)(Lax) CoIII(CH3) (DDHC′)(Lax)d CoIII(CH3) (corrin)(Lax)c

Heterolytic BDEe (kcal mol−1)

Axial Ligand Exchange Energy, ΔELE)f (Lax: H2O → Im) (kcal mol−1)

Lax = Im

Lax = H2O

Lax = Im

Lax = H2O

CoIII(CH3) (Cor)(Lax)a

CoII(Cor)(Lax)a

32.5 34.9 36.4

37.1 38.5 39.7

151.0 164.5 169.6

144.2 158.0 162.2

−6.8 −6.5 −7.4

−11.4 −10.1 −10.7

a

Cor is the corrinoid ligand. bAt the BP86/6-31G(d) level of theory. cData taken from ref 17a. dData taken from this work. eThe value of the heterolytic BDE for the axial ligand-coordinated CH3−Co complex is affected by dissociation of both CH3−Co and Co−Lax bonds, which provide the three fragments. fThe ligand exchange energy (ΔELE) by axial ligand exchange from H2O to Im is defined by the following equations: ΔELE for the CoIII(CH3) (Cor)(Lax) = E(CoIII(CH3)(Cor)(Im)) + E(H2O) − {E(CoIII(CH3)(Cor)(H2O)) + E(Im)} and ΔELE for the CoII(Cor)(Lax) = E(CoII(Cor)(Im)) + E(H2O) − {E(CoII(Cor)(H2O)) + E(Im)}, where E(X) is the energy of the optimized structure of X.

of CH3+ as a heterolysis product is larger than that of •CH3 as a homolysis product (E(CH3+) − E(•CH3) = 226 kcal mol−1). Figure 3b shows the plots of the heterolytic BDEs against the observed redox potentials of the nonalkylated cobalt corrinoids. Compared to the homolytic BDEs, the heterolytic BDEs linearly correlate with the redox potentials of the cobalt corrinoids, regardless of the identity of the axial ligand. Furthermore, the axial ligand exchange from H2O to Im increases the heterolytic BDEs due to the greater stabilization of the Co(III) species by the Im-ligation than that by the H2Oligation. Electronegativity of the Corrinoid Frameworks. To elucidate the framework effect on the redox potentials and the BDEs, electronegativity values of the free-base corrinoids were estimated from DFT calculations (Table 3).19 The electro-

homolytic BDEs of the Co−C bond of the methylated cobalt corrinoids (Table 2).7b Plots of the homolytic BDEs against the observed redox potentials of the nonalkylated cobalt corrinoids are shown in Figure 3a. A weak negative correlation between

Table 3. Computed Energy Levels of HOMO and LUMO and Electronegativity (χHL)a for the Free-Base Corrinoidsb corrinoid

εHOMO (eV)

εLUMO (eV)

χHL (eV)

TDHC′ DDHC′ corrin

−4.74 −4.50 −4.45

−3.50 −2.44 −2.36

4.12 3.47 3.41

Electronegativity (χHL) is defined by the following equation: χHL = {−εHOMO − εLUMO}/2, where εHOMO and εLOMO are energy levels of the HOMO and LUMO of the free-base corrinoids, respectively.19 b Chemical structures of free-base corrinoids are shown in Figure 4. a

Figure 3. Plots of DFT-computed (a) homolytic and (b) heterolytic BDEs against the experimental Co(II)/Co(I)- and Co(III)/Co(II)redox potentials of nonalkylated cobalt corrinoids. The plots of Imand aqua-coordinated corrinoids are shown with solid red triangles (▲) and solid blue circles (●), respectively.

negativity generally indicates the tendency of the framework to attract electrons. Thus, a lower electronegativity value indicates a greater extent of electron donation from the framework to the metal center. The data listed in Table 3 show the decrease in electronegativity as follows:

the homolytic BDEs and the redox potentials is found in cobalt corrinoids with each Im or aqua coordination form: negative shifts of the redox potentials of the cobalt complexes with the same axial ligand increase the homolytic BDEs. In addition, it is found that axial ligation has an influence on the homolytic BDEs. Indeed, the exchange of the axial ligand from H2O to Im clearly decreases the homolytic BDEs, because of the more effective stabilization of the Co(II) species by such axial ligand exchange than that of the methylated Co(III) species (see Table 2, as well as Figure S8 in the Supporting Information). Thus, the ligand exchange decreases both of the redox potentials and homolytic BDEs for each cobalt corrinoid (Figure 3a). The heterolytic BDEs were also determined by DFT calculations (Table 2). The calculated BDEs are significantly larger than the homolytic BDEs, because the computed energy

Co(TDHC′) ≫ Co(DDHC′) > cobalamin

This is mainly caused by destabilization of the energy level of the lowest unoccupied molecular orbital (LUMO) of the saturated framework due to contraction of the conjugation systems of the corrinoid frameworks (Figure 4). Consequently, a more highly saturated framework leads to lower electronegativity and greater electron donation, which provides a more-stable high-valency species in the corrinoids (see Figures S7 and S8).20 Thus, a more highly saturated framework induces a negative redox potential and an increased BDE21 to provide a negative linear correlation between BDE and the redox potential (Figure 3). Furthermore, it is found that the negative slopes of the plots of the heterolytic BDEs against the redox potentials are ∼7-fold greater than those of the homolytic BDEs. This is because the stabilization of the Co(I) species, as D

DOI: 10.1021/acs.inorgchem.6b02482 Inorg. Chem. XXXX, XXX, XXX−XXX

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for the homolytic and heterolytic Co−C bond cleavages of the methylated cobalt corrinoids and computed bond lengths (PDF)

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Takashi Hayashi: 0000-0002-2215-935X Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by Grants-in-Aid for Scientific Research provided by JSPS KAKENHI Grant Numbers JP15H05804, JP24655051, JP15H00944, JP22105013, JP16H00837, the JSPS Japanese−German Graduate Externship, and JST PRESTO. Y.M. appreciates support from the JSPS Research Fellowship for Young Scientists (JSPS KAKENHI Grant Number JP14J00790).

Figure 4. Frontier molecular orbitals and their energy levels of freebase corrinoids at the BP86/TZVP level of theory.19

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a heterolysis product, by the framework with low electronegativity is more effective than that of the Co(II) species as a homolysis product (Figure S8). Thus, a clear linear correlation is observed for the Im- and H2O-coordinated cobalt corrinoids, in the case of heterolytic BDEs.22 These findings indicate that the electronegativity modulates both of the redox potentials and BDEs, resulting in the correlation.

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CONCLUSION In conclusion, we have determined the redox potentials of Co(TDHC) and Co(DDHC) with the normal histidine ligand in the protein matrix, as well as those with an aqua ligand in the buffer solution. The electrochemical and theoretical data show the correlations between the redox potentials and Co−C bond dissociation energies (BDEs) for the Im- and H2O-coordinated cobalt corrinoids through the framework effect, which modulates the electronegativity. We also demonstrate that there is a stronger correlation in the heterolysis, which is due to stability of the Co(I) species, compared to the species generated after homolysis. Thus, the heterolytic Co−C bond cleavage would be effectively promoted by the positive redox potential of the cofactor, which is regulated by the protein matrix of the native enzyme.7,8,23 In contrast, homolytic cleavage is promoted by the strong axial coordination. The present study will contribute to the elucidation of the reaction mechanisms of cobalamin-dependent enzymes.

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REFERENCES

(1) (a) Kräutler, B.; Puffer, B. Vitamin B12-Derivatives: Organometallic Catalysts, Cofactors and Ligands of Bio-Macromolecules. In Handbook of Porphyrin Science; Kadish, K. M., Smith, K. M., Guilard, R., Eds.; World Scientific: Singapore, 2012; Vol. 25, pp 131−263. (b) Kräutler, B. Organometallic Chemistry of B12 Coenzyme. In Metal Ions in Life Science; Sigel, A., Sigel, H., Sigel, R. K. O., Eds.; Royal Society of Chemistry: Cambridge, U.K., 2009; Vol. 6, pp 1−51. (c) Gruber, K.; Puffer, B.; Kräutler, B. Chem. Soc. Rev. 2011, 40, 4346− 4363. (d) Matthews, R. G. Cobalamin-Dependent Methyltransferases. Acc. Chem. Res. 2001, 34, 681−689. (2) (a) Drennan, C. L.; Huang, S.; Drummond, J. T.; Matthews, R. G.; Lidwig, M. L. Science 1994, 266, 1669−1674. (b) Froese, D. S.; Kochan, G.; Muniz, J. R. C.; Wu, X. C.; Gileadi, C.; Ugochukwu, E.; Krysztofinska, E.; Gravel, R. A.; Oppermann, U.; Yue, W. W. Structures of the Human GTPase MMAA and Vitamin B12-dependent Methylmalonyl-CoA Mutase and Insight into Their Complex Formation. J. Biol. Chem. 2010, 285, 38204−38213. (3) (a) Geno, M. K.; Halpern, J. Why Does Nature Not Use the Porphyrin Ligand in Vitamin B12? J. Am. Chem. Soc. 1987, 109, 1238− 1240. (b) Brown, K. L. Chemistry and Enzymology of Vitamin B12. Chem. Rev. 2005, 105, 2075−2150. (c) Brown, K. L. The Enzymatic Activation of Coenzyme B12. Dalton Trans. 2006, 1123−1133. (d) Kumar, M.; Kozlowski, P. M. Corrin Ring-induced Redox Tuning. Chem. Commun. 2012, 48, 4456−4458. (e) Jensen, K. P.; Ryde, E. Conversion of Homocysteine to Methionine by Methionine Synthase: A Density Functional Study. J. Am. Chem. Soc. 2003, 125, 13970− 13971. (4) (a) Govender, P. P.; Navizet, I.; Perry, C. B.; Marques, H. M. DFT Studies of Trans and Cis Influences in the Homolysis of the Co− C Bond in Models of the Alkylcobalamins. J. Phys. Chem. A 2013, 117, 3057−3068. (b) De March, M.; Demitri, N.; Geremia, S.; Hickey, N.; Randaccio, L. Trans and Cis Influences and Effects in Cobalamins and in Their Simple Models. J. Inorg. Biochem. 2012, 116, 215−227. (d) Zipp, C. F.; Michael, J. P.; Fernandes, M. A.; Mathura, S.; Perry, C. B.; Navizet, I.; Govender, P. P.; Marques, H. M. The Synthesis of a Corrole Analogue of Aquacobalamin (Vitamin B12a) and Its Ligand Substitution Reactions. Inorg. Chem. 2014, 53, 4418−4429. (5) (a) Murakami, Y.; Aoyama, K. Transition-metal Complexes of Pyrrole Pigments. XIII. Reduction and Coordination Behaviors of the Cobalt(II) Complexes of 1,19-Disubstituted Tetradehydrocorrins as Demonstrated by the Presence of Various Bases. Bull. Chem. Soc. Jpn. 1976, 49, 683−688. (b) Murakami, Y.; Aoyama, Y.; Tokunaga, K. Transition-metal Complexes of Pyrrole Pigments. 16. Cobalt Complexes of 1,19-dimethyldehydrocorrins as Vitamin B12 Models. J.

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.inorgchem.6b02482. UV-vis spectra of Co(DDHC) in the presence of Im and in the absence of Im, electrochemical measurements, redox potentials of base-off and His-on cobalt corrinoids, chemical structures of corrinoid models for the DFT calculations, plots of the experimental redox potentials and DFT-calculated ΔE of the corresponding reduction reactions, energy diagrams of the Co(III), Co(II) and Co(I) species of the cobalt corrinoids, energy diagrams E

DOI: 10.1021/acs.inorgchem.6b02482 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

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DOI: 10.1021/acs.inorgchem.6b02482 Inorg. Chem. XXXX, XXX, XXX−XXX