Electron Transfer and Geometric Conversion of Co–NO Moiety in

Article pubs.acs.org/IC

Cite This: Inorg. Chem. XXXX, XXX, XXX−XXX

Electron Transfer and Geometric Conversion of Co−NO Moiety in Saddled Porphyrins: Implications for Trigger Role of Tetrapyrrole Distortion Min Tang,† Yan Yang,† Shaowei Zhang,† Jiafu Chen,‡ Jian Zhang,§ Zaichun Zhou,*,† and Qiuhua Liu*,† †

Key Laboratory of Theoretical Organic Chemistry and Functional Molecules, Ministry of Education, and School of Chemistry and Chemical Engineering, Hunan University of Science and Technology, Xiangtan 411201, China ‡ Hefei National Laboratory for Physical Sciences at Microscale, University of Science and Technology of China, Hefei 230026, China § Department of Chemistry, University of NebraskaLincoln, Lincoln, Nebraska 68588-0304, United States S Supporting Information *

ABSTRACT: The electrons of NO and Co are strongly delocalized in normal {Co-NO}8 species. In this work, {CoNO}8 complexes are induced to convert from (CoII)+•−NO• to CoIII−NO− by a core contraction of 0.06 Å in saddled cobalt(II) porphyrins. This intramolecular electron transfer mechanism indicates that nonplanarity of porphyrin is involved in driving conversion of the NO units from electrophilic NO• as a bent geometry to nucleophilic NO− as a linear geometry. This implies that distortion acts as a trigger in enzymes containing tetrapyrrole. The electronic behaviors of the CoII ions and Co−NO moieties were confirmed by Xray crystallography, EPR spectroscopy, theoretical calculation, UV−vis and IR spectroscopy, and electrochemistry. structural conversions of coordinated FeIII,17−19 CoII,20,21 CuII,22 and ZnII.23 For materials containing FeIII and CoII ions with unpaired electron(s), such a size contraction also increases the spin density in the dz2 orbital and excites the dz2 electron to generate π-cation radicals, without the need for any environmental changes. Binding to small molecules, e.g., NO, is universal to all proteins containing heme or corrin.24 In this work, we investigated whether an intramolecular electron transfer (ET), not the general electron delocalization, in {Co-NO}8 complex can occur in the presence of NO as noninnocent ligands.25 This will provide a novel avenue for better understanding how the heme or corrin conformation affects the electronic structures of metal ions and the resulting intramolecular ET.26 The conversion of cobalt ions and NO units in {Co-NO}8 complex can be proven or supported by the macrocycle core size, the bond parameters of the Co−NO moiety, the binding geometry of the axial NO, and orbital energy levels. Here, four 5,1015,20-distrapped cobalt(II) porphyrins, 1-Co to 4-Co (Scheme 1), with successive saddled distortions, were synthesized and characterized to determine the conformational driving effect of this macrocyclic deformation on the axial NO.

1. INTRODUCTION Nitric oxide (NO)1,2 is responsible for transmitting important signals and regulating cellular functions in the human body. Nitric oxide and nitroxyl anion (NO−) are physiologically important heart modulators.3,4 However, the biological effects of NO and NO− can differ significantly from each other. Pharmacological studies have shown that the effects of NO− are distinct from those of NO.5 Moreover, the signaling pathway of NO− is different from those of NO.6 Bioassay discrimination between NO and NO− is still problematic, and definitively resolving this issue is extremely difficult.3,4,7 The macrocyclic distortion is a conserved feature of particular proteins containing heme,8,9 vitamin B12,10 or chlorophylls,11,12 and nonplanarity is crucial in tetrapyrrole chemistry. The capture, generation, or conversion of NO and NO− can hardly work without nitric oxide synthase13 or nitric oxide reductase14 under normal physiological conditions. Most of two types of enzymes contain natural tetrapyrroles, e.g., heme cofactors, participating in each of these processes,12,14 which indicates that distortion greatly influences functions of these enzymes and redox properties of nitrosyl ligands. Distorted tetrapyrroles needed for a variety of biological functions can both stabilize the low-valent oxidation state of metal species and generate relevant high-valent complexes such as the iron(II)− and iron(IV,V)−oxo species in heme,15 or the cobalt(I) and cobalt(III) complexes in vitamin B12.16 Recently, we showed that the core contraction derived from the ruffling or saddling deformations of porphyrin rings can induce © XXXX American Chemical Society

Received: September 25, 2017

A

DOI: 10.1021/acs.inorgchem.7b02455 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry Scheme 1. Synthesis of Distrapped Cobalt(II) Porphyrinsa

2.2. Crystal Structure Determination. The crystal structures were determined by X-ray diffraction using a Bruker SMART 1000 charge-coupled device diffractometer equipped with a normal focus, 2.4 kW sealed-tube X-ray source, with monochromatic Mo Kα (λ = 0.71073 Å) or Cu Kα (λ = 1.54184 Å) radiation. A suitable single crystal of each compound was glued to a thin glass fiber with cyanoacrylate glue. The SMART program package was used to determine the unit cell parameters and to collect data. All structures were solved by direct methods and were refined on F2 by the fullmatrix least-squares method using the SHELXT-97 program. The positional parameters for the metal, nitrogen, and oxygen atoms were obtained by direct methods for all compounds. The remaining nonhydrogen atoms were routinely located from Fourier difference maps during the course of the refinement. All hydrogen atoms were placed geometrically and were refined by riding on their appropriate oxygen and carbon atoms. The final positions of all non-hydrogen atoms were refined anisotropically. Crystals of 1-Co to 4-Co were obtained by solvent diffusion in chloroform and methanol. 2.3. Electronic Structure Calculation. Several theoretical techniques used in this study were based on the density functional theory (DFT) of Kohn and Sham.28 The DFT calculations of single point energy were performed using the hybrid exchange-correlation functional B3LYP, as implemented in Gaussian 09,29 and the X-ray crystal structures were used as the starting point for the calculations. Single-point energy was obtained on the ground-state spin multiplicity.30 The 6-31G(d) basis set was used for all atoms.31 The information on d (Co) and p (N) orbital energies, d−π* backbonding, and partial atomic charge assignments were obtained using the pop=NBO key word, where NBO represent natural bond orbital procedure.29 All calculations were performed under Cs symmetry constraints. 2.4. General Spectroscopic Methods. Mass spectrometry was performed using a Waters Xevo Q-TOF instrument and a Varian IonSPEC QFT-9.4 instrument for ESI and MALDI measurements, respectively. Electron paramagnetic resonance (EPR) spectroscopy was performed at 130 K (9.0408 GHz, X band) using a JEOL JESFA200 EPR spectrometer. UV−vis spectra of the neutral compounds were obtained using a PerkinElmer Lambda 35 spectrophotometer. IR spectroscopies were performed on a Nicolet 6700 FTIR spectrometer. The cyclic voltammogram results were obtained on a CHI760E electrochemical workstation (Autolab) with a glass carbon electrode as the working electrode, a platinum wire as counter electrode, and Ag/ Ag+ as reference electrode.

(a) An equivalent of pyrrole and Co(AcO)2·2H2O, propionic/butyric (2:1, v/v) acid mixed, refluxing for 15 min. (b) Another equivalent of pyrrole, refluxing for another 45 min in air. a

2. EXPERIMENTAL SECTION 2.1. General Synthetic Method. Four alkyl-distrapped cobalt porphyrins were prepared according to the published Alder−Longo condensation method,27 using a metal-mediated template strategy.22,23 2,2′-[Ethane-1,2-diylbis(oxy)]di(5-tert-butyl)benzaldehyde (5; 3.82 g, 10 mmol), pyrrole (0.67 g, 10 mmol), and Co(OAc)2·2H2O (∼2.2 g, 11 mmol) were added to a boiling propionic/butyric (2:1, v/v) acid mixture (200 mL) within 5 min. Another equivalent of pyrrole (0.67 g, 10 mmol) was added to the solution after 15 min under reflux; the mixture was further stirred for 45 min, and then the solvent was removed under reduced pressure. The solid residue was extracted three times with dichloromethane (80 mL × 3). The dichloromethane solution was washed five times with water and dried with sodium sulfate. After removal of the solvent, the residue was separated by silica gel column chromatography with dichloromethane/petroleum ether (1:2, v/v) to give the purple solid 1-Co. In the synthesis, the CoII ion acts as both a template and a cobalt source. The other three samples, i.e., 2-Co to 4-Co, were synthesized using the same method. All reagent-grade reactants and solvents were used as received from chemical suppliers. 1-Co: 146.7 mg, yield 2.9%. UV−vis (chloroform, 293 K): λmax = 439.2, 559.9, 611.8 nm. HR MS (MALDI): found for C64H64CoN4O4 [M]+ 1011.4284; calcd 1011.4254. 2-Co: 816.0 mg, yield 15.7%. UV−vis (chloroform, 293 K): λmax = 429.4, 549.6, 598.0 nm. HR MS (MALDI): found for C66H68CoN4O4 [M]+ 1039.4568; calcd 1039.4567. 3-Co: 859.3 mg, yield 16.1%. UV−vis (chloroform, 293 K): λmax = 420.0, 537.6, 574.2 nm. HR MS (MALDI): found for C68H72CoN4O4 [M]+ 1067.4863; calcd 1067.4880. 4-Co: 695.6 mg, yield 12.7%. UV−vis (chloroform, 293 K): λmax = 416.8, 538.8, 555.6 nm. HR MS (MALDI): found for C70H76CoN4O4 [M]+ 1095.5212; calcd 1095.5193. The four corresponding Co−NO complexes, 1-Co-NO to 4-CoNO, were obtained by directly adding freshly made dry NO gas to solutions of the cobalt(II) porphyrins. The cobalt porphyrin 1-Co (50 mg, 0.05 mmol) was dissolved in dry dichloromethane (20 mL). The solution was degassed five times, and then dry NO gas was slowly bubbled through the solution until the 1-Co had completely disappeared, i.e., after about 35 min. The target complex was carefully purified by recrystallization based on solvent volatilization to give the dark violet solid 1-Co-NO. The other three complexes, 2-Co-NO to 4Co-NO, were obtained using the same treatment. Note that all the complex samples needed protection from air and water during the entire reaction, purification, and storage processes, and all reactants, solvents, and containers, including the gas-guide tubes, were rigorously dried and degassed before these complexations.

3. RESULTS AND DISCUSSION 3.1. Synthesis. Four distrapped samples, i.e., 1-Co to 4-Co, are obtained by condensation of a dialdehyde with pyrrole at a molar ratio of 1:2 with the yields of 2.5−16.0% (Scheme 1). The formation of these highly deformed macrocycles involves tandem reactions, namely, condensation, oxidation, and aromatization.23 In the condensation step, symbiotic isomers, two for x = 2, 3 and three for x = 4, 5, are formed because of the different attachment sites of the straps that run over the macrocycles (see Supporting Information, p S2). Therefore, the yields of the target structures are low and they are separated by column chromatography. The four cobalt(II) porphyrin complexes containing axial NO groups are obtained by bubbling NO into the corresponding solutions of the cobalt(II) porphyrins. Formation of the Co−NO moiety is strongly suppressed by oxygen and water. The resulting complexes are purified by recrystallization through solvent volatilization in dry dichloromethane under a NO atmosphere. All target materials are characterized using X-ray diffraction, UV−vis spectroscopy, high-resolution mass spectrometry, and IR spectroscopy. The cobalt(II) porphyrins and their NO complexes are collectively denoted by P-Cos and P-Co-NOs, respectively. B

DOI: 10.1021/acs.inorgchem.7b02455 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry

Figure 1. Crystal structures of P-Cos and corresponding P-Co-NOs. LN1N3 and LN2N4 shown at the bottom of each structure are the diagonal N−N distances of the core. The bond lengths of each Co−NO moiety are also indicated.

Table 1. Selected Structural Parameters of Model Complexes material

LN1N3 (Å)a

LN2N4 (Å)a

LNN (Å)a

LCoN (Å)b

LNO (Å)b

ACoNO (deg)c

1-Co 1-Co-NO 2-Co

3.788(15) 3.819(4) 3.834(5)d 3.836(5) 3.842(2)

3.905(15) 3.843(4) 3.913(5) 3.939(5) 3.931(2)

3.847 3.831 3.881

1.941(6)

1.392(9)

180.0(1)

3.887

1.841(2)

1.173(6)d 1.180(9)

127.3(5) 120.6(5)

3.851(5)d 3.847(5) 3.877(3) 3.879(4) 3.937(3)

3.903(5) 3.901(5) 3.940(3) 3.889(4) 3.966(3)

3.877 1.836(3)

1.199(12)

131.2(9)

1.834(3)

1.202(5)

2-Co-NO 3-Co 3-Co-NO 4-Co 4-Co-NO

3.909 3.884 3.952

a

122.1(3) b

LN1N3 and LN2N4 are the diagonal N−N distances; LNN is averaged from respective LN1N3 and LN2N4 and is defined as core diameter. LCoN and LNO are the bond lengths of Co−N and N−O in Co−NO moieties, respectively. cACoNO is the bond angle of Co−N−O. dThe parallel bond values are extracted from the twin structures.

3.2. Structural Analysis. Single crystals of P-Cos and PCo-NOs are obtained by solvent diffusion using chloroform/ methanol and by solvent volatilization with dichloromethane in

dry NO atmosphere, respectively. The crystal structures and selected structural parameters are shown in Figure 1 and Table 1. In all structures, the central macrocycle adopts the typical C

DOI: 10.1021/acs.inorgchem.7b02455 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry saddle-type deformation that is similar to one of the dominant conformations in heme.9 It is known that the out-of-plane deformation of the macrocycle induces an in-plane deformation (i.e., the core diameter changes),19 which significantly affects the electronic structures, including the spin states and orbital energy levels, of the porphyrin metal center. Such structural information can be obtained from a comparison of the crystallographic data of the two series of materials. Core contraction induced by macrocyclic deformation acts as a switch to tune the electronic structure of a range of metallic species including iron,17 cobalt,20 copper,22 and zinc.23 Due to the distrapped feature of P-Co-NOs, the structural changes in the cores are not pure contractions like those previously observed in deformed porphyrins.17,22 Indeed, the core geometry is deformed from an approximate square in a normal system to a rhombus, and the rhomboid character increases as the ring distortion increases, as shown by plots of LN1N3 and LN2N4 against the number of carbon atoms in the strap (nC) (see Supporting Information, p S5). Here, we use the plot of the core diameter (LNN), defined as the average value of LN1N3 and LN2N4, against nC to visualize the core contraction (Figure 2).

Scheme 2. Schematic Diagram of Changes on Co−NO Moiety under Core Contractiona

a

The solid point (•) denotes the unpaired electron, and the asterisk (*) is the excited cobalt ion from the π-cation radical (e.g., 1-Co+•). The blue ellipse represents the distorted porphyrin.

The most important evidence that supports this conversion is the binding geometries of the axial NO ligand (Figure 1). Upon coordination to metalloporphyrins with the N atom, NO can form two binding geometries, linear or bent, denoted by NOlinear or NObent, respectively.33,34 An exclusive NOlinear geometry was found in 1-Co-NO, distinctly different from the previously reported bent cobalt(II)−nitrosyl (CoII−NO−) form.35 The bent NO conformations in 2-Co-NObent to 4-CoNObent are converted to a linear form in 1-Co-NOlinear with increasing deformation. For LS CoII ion in regular porphyrins, in which the 3dπ orbitals are completely filled, only the nonbonded 3dz2 orbital remains as a singly occupied molecular orbital (SOMO). The pπ* orbital of NO therefore creates inphase σ-type bonding with the 3dz2 SOMO, resulting in bent Co−NObent bonds in P-Co-NOs,33 like those in 2-Co-NO to 4Co-NO, with bond angles varying in the range 120−131°. The current complexes, 2-Co-NO to 4-Co-NO, hold a radical unit (NO•) with some electrophilic property. The ring deformation, however, may allow contributions from the inner 3dπ orbitals, especially dxy, which significantly alter the spin interactions.36 In the case of 1-Co-NO, apparently, the formation of axial NO− anion is derived from a direct transfer of the excited 3dz2 electron to NO. In reality, however, the original 3dz2 electron will be paired with a dxy electron in advance, and a new 3dxy SOMO will consequently form because of a potent horizontal contraction. In this way, the pπ* orbitals of the NO unit will overlap with the new 3dxy SOMO and an electron transfer (ET) process completes between the two orbitals, and such a d−π couple is considerably weaker than the σ-type bonding with 3dz2 orbital taking place in 2-Co-NO to 4-Co-NO. The filled pπ* orbitals of NO further rehybridize with the empty 3dxy orbitals of a CoIII ion. A linear Co−NO geometry (ACoNO = 180.0°) is therefore observed in this case because of the involvement of both 3dπ orbital of Co and pπ* ones of NO. The formation of the linear Co−NO bond in 1-Co-NO is in agreement with that of linear FeIII complexes recently published crystallographic data and theoretical predictions.37,38 The case is however different from that for the Fe−containing systems, which have flexible bond angles because of the different overlapping degrees between pπ* of NO and dxy of metals.32,33 In brief, all these observations indicate that the axial NO is converted from the σ-coordination in three more-planar porphyrins to the unique π-coordination in the highly distorted structure. 1-Co-NO forms an integral anion (NO−) with nucleophilic property after an intramolecular ET. The extra contributions of axial NO in highly distorted porphyrin complex 1-Co-NO possibly include increasing of

Figure 2. Deviations of core diameters (LNN) in P-Cos and P-CoNOs. ΔL1 and ΔL2, calculated from gaps, are the deviations in P-Cos and P-Cos-NOs, respectively. Asterisks (*) denotes excited cobalt ions.

For P-Cos, the LNN values of 2-Co to 4-Co vary slightly around 3.89 Å, which is almost the same as that in a regular porphyrin;32 whereas the value of 3.85 Å for 1-Co is significantly smaller. The gap (ΔL1) between these two values is 0.04 Å, reflecting a structural conversion of LS CoII ions and an excitation of the dz2 electron, as discussed in our previous report.20 After complexation with NO, a similar deviation of LNN was observed, with a gap between 1-Co-NO and 2-Co-NO of 0.06 Å, larger than that of 0.04 Å described above. Note that, for all structures, the estimated standard deviation (ESD) of the Co−N bonds in the cores is within the range of 0.002−0.015 Å, which is much smaller than the gaps of 0.04 or 0.06 Å. NO binding results in pairing the excited dz2 electron of 1Co-NO and stabilizes a unique CoIII−NO− moiety, which is different from the dominant (CoII)+•−NO• forms in the other three complexes (Scheme 2). Tracking the binding geometries and the bond length of the Co−NO moiety should be effective to confirm the electronic structure and determine the direction of electron transfer caused by the change of ligand conformation. D

DOI: 10.1021/acs.inorgchem.7b02455 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry

the bond order of axial NO in 1-Co-NO. One is the electron transfer from Co to NO, as described above; the other is the charge feedback from the same direction, as displayed in Scheme 2 (labeled by feedback π bond). Two effects collectively decrease the N−O bond order, leading to an elongated N−O distance. This is confirmed by the N−O bond length (LNO) of 1.39 Å in 1-Co-NO, which is 0.21 Å longer than that for the other three analogues.39 Third, formation of CoIII−NO− takes advantage of mutual charge delocalization between Co−porphyrin and Co−NO in rival π systems, which will improve the symmetry of the N4 core, and the core will preferentially contract in the longer N2−N4 direction, rather than the shorter N1−N3 direction, as manifested by the convergence of LN1N3 (3.82 Å) and LN2N4 (3.84 Å) in 1-Co-NO (Table 1). 3.3. EPR Analysis. EPR spectroscopy is a powerful technique to monitor the structural change of many species containing unpaired electrons,37,40−43 including metalloporphyrins.44,45 Thus, EPR was employed to further confirm the proposed conversions depicted in Scheme 2. The EPR responses of 2-Co to 4-Co (Figure 4) are in line with those reported for LS CoII ions.20,46 Each curve consists of the g∥ branch, with two peaks at g values of ∼2.01 and ∼1.97, and the g⊥ branch with much weaker intensity at a g value of ∼2.06. These EPR features indicate that the energy level of the 3dz2 orbital is too low to interact with the porphyrin π1u system.21 The EPR response of 1-Co, however, is clearly simpler, and the g value of the dominant signal is 2.0011,47 indicating a nature of

charge density to the central metal due to coordination and that of electronegativity attraction to dxy electron in inner layer. The intramolecular CT or ET process that produces either (CoII)+•−NO• or CoIII−NO− units will inevitably change the bond parameters.6,37 A plot of the bond lengths (LNX, X = Co or O) of Co−N and N−O against nC is shown in Figure 3.

Figure 3. Changes in Co−N (LCoN) and N−O (LNO) bond lengths in Co−NO moiety.

First, two types of binding modes give two different values for LCoN: 1.94 Å for 1-Co-NO and 1.84 Å for the other three complexes. Such change is completely consistent with the πand σ-coordination, respectively. Second, two factors weaken

Figure 4. EPR spectra of 1-Co to 4-Co (top left) and after axial ligation with NO (top right) and 1,4-diazobicyclo[2,2,2]octane (Da) (bottom). All measurements were performed in toluene solution (∼3.0 × 10−3 M) at 130 K. The arrows (↓ and ↑) and solid point (•) indicate signals from dz2 electrons in two perpendicular directions, and the asterisk (*) indicates signal from excited cobalt ions as the π-cation radical (1-Co+•). The numbers are the corresponding Lande g factor. E

DOI: 10.1021/acs.inorgchem.7b02455 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry

Figure 5. Relative energy level (Ed) of d orbital in Co atoms of P-Co-NO (left) and P-Co (right).

Table 2. Orbital Energy Level (Ed/au) of Co Atoms orbital

1-Co-NO

2-Co-NO

3-Co-NO

4-Co-NO

1-Co

2-Co

3-Co

4-Co

3dx2−y2 3dz2 3dxz 3dyz 3dxy

−0.142 −0.229 −0.220 −0.168 −0.267

−0.110 −0.152 −0.230 −0.222 −0.247

−0.106 −0.149 −0.210 −0.209 −0.229

−0.113 −0.158 −0.226 −0.228 −0.250

−0.116 −0.201 −0.263 −0.212 −0.246

−0.122 −0.209 −0.218 −0.272 −0.253

−0.118 −0.208 −0.217 −0.267 −0.251

−0.133 −0.201 −0.252 −0.230 −0.236

organic radical.48 The drastic difference between 1-Co and the other three compounds suggests that the unpaired electron in the 3dz2 orbital of 1-Co is present in the π-cation radical, labeled by 1-Co+•,49,50 and is delocalized over the entire π ring upon the core contraction. Similar phenomena have been observed in our previous reports on nonplanar porphyrins containing iron,17,18 cobalt,20 and copper.22 The EPR spectra of cobalt(II) porphyrins are extremely sensitive to axial ligations.51,52 This sensitivity arises from the dz2 spin along the axial direction, and an activated dz2 electron shows higher sensitivity to noninnocent ligands, NO.53,54 On the basis of the dz2 excitation discussed above, alteration of the dz2 spin can be readily deduced from the differences caused by axial ligation.55 The EPR spectra of P-Co-NOs are depicted in Figure 5a. For 2-Co-NO to 4-Co-NO, with more-planar rings, the (CoII)+•−NO• structure behaves as the typical three hyperfine splitting features at g values of 2.0259, 2.0157, and 2.0051,56 similar to that reported by Scholes53 and Pietrzyk.55 For 1-Co-NO, electron transfer effectively occurs as the core strongly contracts and two radicals are paired up with each other (Scheme 2, right), where the unpaired electron of NO couples with the unpaired dxy electron of the d7 cobalt making the complex EPR silent.57 This EPR presentation also allows the electronic structure of 1-Co-NO to be assigned as ionic form of CoIII−NO−, which is ascribed to the change in the coordination geometry. These observations prove that the diradical (CoII)+•−NO• moieties in 2-Co-NO to 4-Co-NO with more-planar rings was formally converted to the ionic CoIII−NO− in the highly distorted 1-Co-NO without any odd electron. The entire process can be defined as an intramolecular redox reaction driven by the change of conformation, and the only driving force is the core contraction resulting from the saddled deformation. A set of control experiments were performed to further clarify the difference among the dz2 spin states by adding a diagnostic ligand, 1,4-diazobicyclo[2,2,2]octane (Da), to P-Cos (Figure 5c). Note that the diagnostic ligand Da can adjust both the energy level and spin density of that unpaired electron, but avoid the pairing to this odd electron. For the three more-

planar samples, the EPR responses show larger shifts and higher intensities, indicated by 2.2 and 2.4 values of the g⊥ branch, and 2.0 value of the g∥ one after ligation. These changes are derived from axial activation by Da, which only increases the dz2 orbital spin density after ligation.58 This activation creates the condition for d−π orbital interactions between the metal dz2 and porphyrin π1u,21 which broadens the signals of the g∥ branch, and splitting of the g⊥ branch disappears. For the highly distorted 1-Co, the dz2 electron is in completely different state(s) after ligation; the g⊥ branch signals combine to give a broad peak at ∼2.42, and the g∥ signal becomes weaker and the radical feature almost disappears. The origin of these EPR changes can be attributed to the substituent effect of Da on the dz2 electron at the axial position. The dz2 electron in 1-Co is repelled to higher position(s), and the initial signal based on d−π interaction disappears accordingly because of mismatching in the energy level after ligation. The initial radical feature therefore also falls off.59 3.4. Computational Analysis. Since the crystal structures of four P-Cos and their P-Co-NOs have been obtained, so the energy level (Ed) of each Co d orbital can be directly calculated using DFT method without structural optimization. The electronic structures and the structural conversion of the Co−NO moiety should be fully reflected in the changes of d electrons in energy level (Ed).60 All calculations are performed using the B3LYP/6-31G(d) method,61 as implemented in Gaussian 09. The computation results of orbital energy level (Ed) of Co atoms are shown in Table 2 and Figure 5, and the other computation information is presented in the Supporting Information, p S7. DFT calculations show that the binding of d orbitals and coupling of d electrons in Co atoms are responsible for the change of energy levels of d orbitals, which agrees fairly well with those from parameter changes of their crystal and EPR results above. According to the conversions proposed in Scheme 2, dz2, dxy, and dx2−y2 orbitals are closely related to ET or CT processes because of the favorable orbital directions, and the Ed changes in these orbitals should be dominant and F

DOI: 10.1021/acs.inorgchem.7b02455 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry initiative (Figure 5). So the Ed of only the three d orbitals is deliberately linked by lines, respectively, for discussion below. The Ed values of the dz2 orbital significantly change after complexation with NO. In P-Cos, the Ed values appear at a fairly narrow range of −0.20 to −0.21 au; while in P-Co-NOs, the Ed values diverge into −0.15 to −0.16 au for 2-Co-NO to 4Co-NO and −0.23 au for 1-Co-NO. This dissimilation can be interpreted as different binding or coupling of dz2 orbitals, as discussed in sections 3.2 and 3.3. The increase of 0.05 au for the former is derived from the delocalization of dz2 electron and σcoordination of dz2 orbital with a higher pz orbital (−0.14 au) in the N atom of NO, while the decreasing of 0.03 au for the latter is due to the coupling and rehybridization of dz2 electron with a low dxy one (−0.25 au) in Co. For dxy orbitals, their Ed values should remain largely unchanged because it is difficult for NO binding to affect the energy level of inner dxy orbitals. For four P-Cos and 2-Co-NO to 4-Co-NO, this prediction is true, as manifested by slight fluctuation of Ed between −0.23 and −0.25 au, while for 1-Co-NO, the Ed (dxy) value of −0.27 au deviates from that range, which should originate from the coupling and rehybridization of new dxy SOMO with pπ* orbitals of NO, as discussed in section 3.2. As for the dx2−y2 orbitals, the NO binding cannot effectively change their Ed value through axial direction if N4 core size was not small enough, but the binding can enhance the whole electron density of central Co atom and improve the efficiency of core contraction when the core is small enough, and the Ed (dx2−y2) value will accordingly decrease, as shown by the 0.14 au of 1-Co-NO, which is 0.02 au lower than that of 1-Co. 3.5. Spectroscopic Analysis. A saddled deformation results in in-plane core contraction, which affects the ring spectra62 and magnetic properties of the metal center.63 The conversion of the P-Co-NO species is further clarified by UV− vis spectroscopy (Figure 6). For P-Cos from 4-Co to 1-Co, the

with NO, even larger red shifts are observed from 4-Co-NO to 1-Co-NO (Figure 6, top). The differences in the spectra compared with those of the pure P-Cos lie in larger peak widths and irregular spectral shifts. The differences need further analysis through differential spectral treatment. The plot of the differences (Δλmax) at the maxima against nC shows a noncontinuous trend (Figure 6, insert). Here, Δλmax values are calculated as the differences between the magnitudes of the shift at the maximum for each Co−NO complex and its counterpart. This difference spectral treatment can be used to track the energy levels of these cobalt porphyrins upon NO binding. A ∼10 nm gap can be clearly observed between the two curves in this plot; this is equal to an increase of 6 kJ/mol in the molecular energy level. This deviation is thought to originate from the different coordination modes and the more complicated electron delocalization caused by axial binding of NO, which is different from those previously reported for pure orbital exchange of metal species for monostrapped iron17,18 and cobalt20 porphyrins, and indicates the conversion of the Co−NO moieties. For 4-Co-NO to 2-Co-NO, with moreplanar rings, the Co−NO moieties maintain a σ-coordination mode, and the Δλmax values continuously alter from −2.4 to 11.8 nm, reflecting a regular red-shift trend. The contribution to the spectral shift has three main components: charge transfer from NO to the metalloporphyrin,39 electron delocalization from the metal to the NO ligand,66,67 and the normal coupling between the porphyrin and ligand.68,69 The red shift from 4Co-NO to 2-Co-NO arises for all three components because of the increasing sensitivity of the CoII dz2 electron and the NO radical during the core contraction, as proven by the EPR spectra and computational data shown above. For 1-Co-NO, with a highly distorted ring, Δλmax appears at 7.2 nm, reflecting the weak d−π coupling between the metalloporphyrin and the NO ligand, which is consistent with the conclusion that the Co−NO moiety is converted to the CoIII−NO− based on a π-coordination after an intramolecular ET. The spectral difference indicates that there is a considerable deformation effect, which changes the ground state of the total complex. The Q-band of these materials also includes some unique splitting phenomena after complexation, which can give much information in changes of energy level (see Supporting Information, p S7). Additional evidence for the formation of the nitrosyl anion rather than the neutral NO ligand in 1-Co-NO comes from IR spectroscopy (Figure 7). The positions and relative intensities of the NO bands (νNO) depend on the oxidation state of NO and reflect the changes in electron density in metallic complexes.70 For instance, νNO of NO+, NO, and NO− as ligands appear in the range of >1840, 1760−1600, and 1700− 1530 cm−1, respectively.71,72 Inspection of IR spectra of all 8 materials shows that the NO binding to Co centers accounts for a strong band (νNO) at 1685−1676 cm−1. For complexes 2Co-NO to 4-Co-NO behaving as bent Co−N−O geometry, the νNO values appear at 1685 cm−1 as strong sharp peak, while the νNO of 1-Co-NO as linear Co−N−O geometry shifts to 1676 cm−1 as a broader peak, which is fully consistent with that in previous reports related to Co−NO species, 1689 cm−1 for NO and 1679 cm−1 for NO− in KBr pellets.38,71 Theoretically, the ∼10 cm−1 difference is too “small” to warrant a speculative NO to NO− formulation change. A strong electron delocalization between Co and NO in normal {Co-NO}8 complexes,32,33 however, makes the vNO of the NO form similar to that of the NO− one. That is, the vNO in 2-Co-NO to 4-Co-NO appearing

Figure 6. UV−vis spectra of P-Cos before (bottom) and after (top) addition of NO in chloroform (2−4 × 10−5 M) at 293 K. Δλmax is defined as difference spectra of the maximum for Co−NO complex from its parent complex. ΔΔλmax represents the gap between the curve (Δλmax) of 1-Co and those of 2-Co to 4-Co.

maximum (λmax) of the Soret band shows a significant red shift from 416.8 to 439.2 nm with increasing deformation (Figure 6, bottom). The red-shift behaviors are attributed to the hybrid orbital deformation of the macrocycle64 if the effect of the metal center is neglected, and the shift continuously changes as the distortion degree increases. Although the shift also includes the impact of the central metal,23,37,65 it is swamped by the dominant hybrid orbital deformation effect. After complexation G

DOI: 10.1021/acs.inorgchem.7b02455 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry

responses of NO ligands from those of P−Co components. Ring nonplanarity can switch on metal (d)−porphyrin (π) orbital interactions in saddled75 and ruffled76 porphyrin systems. Typically, the ring-centered interactions will result in four redox reactions: a π-anion radical and a dianion on reduction and a π-cation radical and dication on oxidation. These reactions have been experimentally and theoretically proven.77 For 1-Co to 4-Co, four of the related redox responses can be identified clearly at a glass carbon electrode in the range of +1.60 to −1.90 V (Figure 8, left). Among these responses, dianion (P−Co)2−, π-cation radical (P−Co)−•, and dication (P−Co)2+ behave as reversible patterns in the range of −1.19 to −1.34, 0.66−0.74, and 0.97−1.05 V, respectively, while the response of π-anion radical (P−Co)−• (labeled as ●) includes an irreversible branch in the range of −0.40 to −0.57 V (Eap) besides a reversible one at ∼0.12 V (E).20 Under current measurement conditions, the electrochemical shift can reflect the structural conversion of central Co(II) species. The significant changes relevant to this metallic conversion are included in reactions related to π-anion radical (P−Co)−• and π-cation radical (P−Co)+•. For the reactions of (P−Co)−•, the reversible reduction observed at E = ∼0.12 V remains constant, while the other irreversible one at Eap = −0.40 to −0.57 V shows visible shift, which can be assigned to two reduction processes of porphyrin ring and central Co(II) ion, respectively. From the perspective of mechanism, the single-electron reduction of all porphyrin rings including those in complexes P-Co-NOs is similar, as supported by constant E values,73,78 while the Co(II) reduction differs; Eap values divided into two groups as the core contracts are closely related to changes of dz2 SOMO in Co(II) ion. For one group including 4-Co to 2-Co, the dz2 SOMO gradually rises because of the successive core contraction, as accompanied by visibly positive shift of Eap from −0.57 to −0.40 V, while for the other group containing only 1-Co, the intensive contraction turns the dz2 SOMO into a π-cation radical, which makes the reduction more difficult, as manifested by the markedly negative shift of >0.10 V compared to that of 2-Co (Eap = −0.40 V). As for the

Figure 7. IR spectra of P-Cos (black) and P-Co-NOs (red) at 293 K. The asterisk (*) represents the absorption of NO. All spectra were measured in KBr pellets.

at 1685 cm−1 comes from a resonant NO, not from a pure NO ligand. A more detailed analysis is provided in the Supporting Information (p S13). 3.6. Electrochemical Analysis. Porphyrin nonplanarity induced by protein is an effective strategy for the rational tuning of the redox potentials of metal centers,73 which gives rich information about the metallic structure before and after structural distortion.22,74 The conversion of the nitrosyl ligand depending on the porphyrin distortion has been clarified by the various ways described above which illustrate two distinct NO bonding modes.71,72 In this section, cyclic voltammograms of the Co−NO complexes were measured to follow the changes in the redox ability of NO ligands before and after this conversion (Figure 8). The electrochemistry in Figure 8 mainly includes the changes in the two aspects of P−Co and NO under core contraction. The cyclic voltammograms of the four P-Cos as references should be discussed in advance before considering those of NO in the parallel P-Co-NOs, which is helpful to discriminate the

Figure 8. Cyclic voltammograms of P-Cos (left) and P-Co-NOs (right). All samples are dissolved in benzonitrile containing 0.1 M TBAPF6 (tetra-nbutylammonium hexafluorophosphate) at room temperature under an inert gas. Scan rate = 0.1 V s−1. (P−Co)−• and (P−Co)+• represent π-anion radical and π-cation radical, respectively. (P−Co)2− and (P−Co−NO)2− represent dianions of P-Cos and P-Co-NOs, respectively. The reaction potential (E/V) of reversible redox processes and the reduction peak potential (Eap/V) of irreversible processes are inserted below each electrochemical reaction, where E = (Eap + Ecp)/2, and Ecp denotes oxidation peak potential. All Eap and Ecp values are shown in the Supporting Information, p S9. H

DOI: 10.1021/acs.inorgchem.7b02455 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry formation of (P−Co)+•, the reversible oxidation also depends on the change of dz2 SOMO. The redox voltage is observed at E = 0.74 V because of the existence of a dz2 single electron, and the value shifts to 0.66 V because of transfer of the dz2 electron to π system. The negative shift of 0.08 V is believed to be caused by saddling-induced d−π interactions. Next, the electrochemical response of NO depending on core contraction will be deliberately discussed. The cyclic voltammograms of four P-Co-NOs produces two new reversible responses (Figure 8, right, labeled by ■ and □, respectively). The two responses are distinct from those of P−Co counterparts, so that both responses appear to only involve changes of NO components, and the reactions may be described as formation of nitrosyl anion (NO−) and nitrosyl cation (NO+). In other words, the reduction of NO appears at E = −1.55 − −1.58 V (■), while its oxidation appears at E = 0.46−0.52 V (□), which is close to the reported values in MnNO−porphyrins.79 Similarly, formation of NO− and NO+ species is closely related to change of the dz2 SOMO under the electrochemical conditions. Redox potential (E) of NO will take on a similar trend to that of formation of (P−Co)−• and (P−Co)+•. The E values of NO− and NO+ reactions consist of two groups during the core contraction. For 4-Co to 2-Co, the E values of NO− and NO+ reaction lightly increase from −1.58 to −1.55 V and from 0.54 to 0.52 V, respectively, due to the increase of the dz2 SOMO level, while for 1-Co, the negative shift of 0.03 V for NO− and 0.06 V for NO+ takes place compared to −1.55 and 0.46 V of 2-Co, respectively. The negative shift behaviors can be readily explained by the occurrence of d−π interaction between metal (d) and porphyrin (π) after a potent core contraction.49 The NO component in highly saddled cobalt(II) porphyrin 1-Co-NO is easier to oxidize and more difficult to reduce than those in more planar Co−NO complexes because of its structural conversion affected by macrocycle distortion.

Accession Codes

CCDC 1527309−1527316 contain the supplementary crystallographic data for this paper. These data can be obtained free of charge via www.ccdc.cam.ac.uk/data_request/cif, or by emailing [email protected], or by contacting The Cambridge Crystallographic Data Centre, 12 Union Road, Cambridge CB2 1EZ, UK; fax: +44 1223 336033.

■

*E-mail: [email protected]. *E-mail: [email protected]. ORCID

Jian Zhang: 0000-0003-0274-0814 Zaichun Zhou: 0000-0003-2075-8241 Funding

This study was supported by the National Natural Science Foundation of China (No. 21372069 and 21602054) and the Scientific Research Fund of Hunan Provincial Education Department (No. 15K042). Notes

The authors declare no competing financial interest.

■ ■

ACKNOWLEDGMENTS China Scholarship Council (201708430033) is acknowledged. REFERENCES

(1) Cherry, P. D.; Furchgott, R. F.; Zawadzki, J. V.; Jothianandan, D. Role of endothelial cells in relaxation of isolated arteries by bradykinin. Proc. Natl. Acad. Sci. U. S. A. 1982, 79, 2106−2110. (2) Ignarro, L. J.; Buga, G. M.; Wood, K. S.; Byrns, R. E.; Chaudhuri, G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U. S. A. 1987, 84, 9265−9269. (3) Jugdutt, B. I. The Role of Nitric Oxide in Heart Failure; Springer: 2004. (4) Carnicer, R.; Crabtree, M. J.; Sivakumaran, V.; Casadei, B.; Kass, D. A. Nitric oxide synthases in heart failure. Antioxid. Redox Signaling 2013, 18, 1078−1099. (5) Paolocci, N.; Saavedra, W. F.; Miranda, K. M.; Martignani, C.; Isoda, T.; Hare, J. M.; Espey, M. G.; Fukuto, J. M.; Feelisch, M.; Wink, D. A.; Kass, D. A. Nitroxyl anion exerts redox-sensitive positive cardiac inotropy in vivo by calcitonin gene-related peptide signaling. Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 10463−10468. (6) Doctorovich, F.; Bikiel, D.; Pellegrino, J.; Suárez, S. A.; Larsen, A.; Martí, M. A. Nitroxyl (azanone) trapping by metalloporphyrins. Coord. Chem. Rev. 2011, 255, 2764−2784. (7) Collman, J. P.; Farnham, P.; Dolcetti, G. Intramolecular redox equilibriums of cobalt-nitrosyl complexes. J. Am. Chem. Soc. 1971, 93, 1788−1790. (8) Shaik, S.; Cohen, S.; Wang, Y.; Chen, H.; Kumar, D.; Thiel, W. P450 enzymes: their structure, reactivity, and selectivity-modeled by QM/MM calculations. Chem. Rev. 2010, 110, 949−1017. (9) Al-Karadaghi, S.; Franco, R.; Hansson, M.; Shelnutt, J. A.; Isaya, G.; Ferreira, G. C. Chelatases: distort to select? Trends Biochem. Sci. 2006, 31, 135−142. (10) Bandarian, V.; Pattridge, K. A.; Lennon, B. W.; Huddler, D. P.; Matthews, R. G.; Ludwig, M. L. Domain alternation switches B12dependent methionine synthase to the activation conformation. Nat. Struct. Biol. 2002, 9, 53−56. (11) Saito, K.; Shen, J. R.; Ishida, T.; Ishikita, H. Short hydrogen bond between redox-active tyrosine Y(Z) and D1-His190 in the photosystem II crystal structure. Biochemistry 2011, 50, 9836−9844. (12) Marletta, M. A.; Hurshman, A. R.; Rusche, K. M. Catalysis by nitric oxide synthase. Curr. Opin. Chem. Biol. 1998, 2, 656−663.

4. CONCLUSIONS In conclusion, a unique intramolecular redox reaction of {CoNO}8 complex that converts from (CoII)+•−NO• diradical to the CoIII−NO− ionic form is definitively demonstrated. This reaction shows that the conversion of electrophilic NO• to nucleophilic NO− is feasible by virtue of the core contraction of saddled porphyrins. Such ET mechanism indicates that the nonplanar tuning of tetrapyrroles triggers conformational change in this conversion of NO units from pure coordination to a rare reduction, or vice versa. This implies that distortion makes a real contribution in enzymes containing heme cofactors. NO and the nitrosyl ion are responsible for transmitting important signals in the human body, and the results indicate the importance of macrocycle distortion for most nitric oxide synthases and nitric oxide reductases.

■

AUTHOR INFORMATION

Corresponding Authors

ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.inorgchem.7b02455. Additional results, analysis of synthetic structures and spectra, detailed mass, DFT calculation, UV−vis, NMR and IR spectra, and redox potential of CV (PDF) I

DOI: 10.1021/acs.inorgchem.7b02455 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry

Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian 09, Revision A.02; Gaussian, Inc.: Wallingford, CT, 2009. (30) Abe, M.; Ishihara, C.; Nojima, M. DFT prediction of groundstate spin multiplicity of cyclobutane-1,3-diyls: notable effects of two sets of through-bond interactions. J. Org. Chem. 2003, 68, 1618−1621. (31) Grande, L. M.; Noll, B. C.; Oliver, A. G.; Scheidt, W. R. Dynamics of NO motion in solid-state [Co(tetraphenylporphinato)(NO)]. Inorg. Chem. 2010, 49, 6552−6557. (32) Sparapany, J. W.; Crossley, M. J.; Baldwin, J. E.; Ibers, J. A. Structure of the cobalt(II)-″capped″ porphyrin, Co(C3-Cap)•3CHCl3. J. Am. Chem. Soc. 1988, 110, 4559−4564. (33) Scheidt, W. R.; Duval, H. F.; Neal, T. J.; Ellison, M. K. Intrinsic structural distortions in five-coordinate (nitrosyl)iron(II) porphyrinate derivatives. J. Am. Chem. Soc. 2000, 122, 4651−4659. (34) Hunt, A. P.; Lehnert, N. Heme-nitrosyls: electronic structure implications for function in biology. Acc. Chem. Res. 2015, 48, 2117− 2125. (35) Walter, M. R.; Dzul, S. P.; Rodrigues, A. V.; Stemmler, T. L.; Telser, J.; Conradie, J.; Ghosh, A.; Harrop, T. C. Synthesis of CoIINO− complexes and their reactivity as a source of nitroxyl. J. Am. Chem. Soc. 2016, 138, 12459−12471. (36) Walker, F. A.; Nasri, H.; Turowska-Tyrk, I.; Mohanrao, K.; Watson, C. T.; Shokhirev, N. V.; Debrunner, P. G.; Scheidt, W. R. πAcid Ligands in iron(III) porphyrinates. Characterization of low-spin bis(tert-butylisocyanide)(porphyrinato)iron(III) complexes having (dxz,dyz)4(dxy)1 ground states. J. Am. Chem. Soc. 1996, 118, 12109− 12118. (37) Pellegrino, J.; Bari, S. E.; Bikiel, D. E.; Doctorovich, F. Successful stabilization of the elusive species {FeNO}8 in a heme model. J. Am. Chem. Soc. 2010, 132, 989−995. (38) Lehnert, N.; Scheidt, W. R.; Wolf, M. W. In Nitrosyl Complexes in Inorganic Chemistry, Biochemistry and Medicine II; Mingos, D. M. P., Ed.; Springer Berlin Heidelberg: Berlin, Heidelberg, 2014; pp 155− 223. (39) Roncaroli, F.; Videla, M.; Slep, L. D.; Olabe, J. A. New features in the redox coordination chemistry of metal nitrosyls {M−NO+; M− NO•; M−NO−(HNO)}. Coord. Chem. Rev. 2007, 251, 1903−1930. (40) Luca, O. R.; Crabtree, R. H. Redox-active ligands in catalysis. Chem. Soc. Rev. 2013, 42, 1440−1459. (41) Singh, R.; Switala, J.; Loewen, P. C.; Ivancich, A. Two [Fe(IV)O Trp*] intermediates in M. tuberculosis catalase-peroxidase discriminated by multifrequency (9−285 GHz) EPR spectroscopy: reactivity toward isoniazid. J. Am. Chem. Soc. 2007, 129, 15954−15963. (42) Ghosh, S. K.; Patra, R.; Rath, S. P. Axial ligand coordination in sterically strained vanadyl porphyrins: synthesis, structure, and properties. Inorg. Chem. 2008, 47, 9848−9856. (43) Patra, R.; Chaudhary, A.; Ghosh, S. K.; Rath, S. P. Modulation of metal displacements in a saddle distorted macrocycle: synthesis, structure, and properties of high-spin Fe(III) porphyrins and implications for the hemoproteins. Inorg. Chem. 2008, 47, 8324−8335. (44) Walker, F. A. An electron spin resonance study of coordination to the fifth and sixth positions of α,β,γ,δ-tetra(p-methoxyphenyl)porphinatocobalt(II). J. Am. Chem. Soc. 1970, 92, 4235−4244. (45) Nellutla, S.; van Tol, J.; Dalal, N. S.; Bi, L. H.; Kortz, U.; Keita, B.; Nadjo, L.; Khitrov, G. A.; Marshall, A. G. Magnetism, electron paramagnetic resonance, electrochemistry, and mass spectrometry of the pentacopper(II)-substituted tungstosilicate [Cu5(OH)4(H2O)2(Aα-SiW9O33)2]10‑, a model five-spin frustrated cluster. Inorg. Chem. 2005, 44, 9795−9806. (46) Banci, L.; Bencini, A.; Benelli, C.; Gatteschi, D.; Zanchini, C. In Structures versus Special Properties; Springer Berlin Heidelberg: Berlin, Heidelberg, 1982; pp 37−86. (47) Aebischer, A.; Heer, S.; Biner, D.; Krämer, K.; Haase, M.; Güdel, H. U. Visible light emission upon near-infrared excitation in a transparent solution of nanocrystalline β-NaGdF4: Yb3+, Er3+. Chem. Phys. Lett. 2005, 407, 124−128. (48) Rajca, A. Organic diradicals and polyradicals: From spin coupling to magnetism? Chem. Rev. 1994, 94, 871−893.

(13) Saito, K.; Umena, Y.; Kawakami, K.; Shen, J. R.; Kamiya, N.; Ishikita, H. Deformation of chlorin rings in the Photosystem II crystal structure. Biochemistry 2012, 51, 4290−4299. (14) Moenne-Loccoz, P. Spectroscopic characterization of heme iron-nitrosyl species and their role in NO reductase mechanisms in diiron proteins. Nat. Prod. Rep. 2007, 24, 610−620. (15) Ortiz de Montellano, P. R.; De Voss, J. J. Oxidizing species in the mechanism of cytochrome P450. Nat. Prod. Rep. 2002, 19, 477− 493. (16) Li, D.; Stuehr, D. J.; Yeh, S. R.; Rousseau, D. L. Heme distortion modulated by ligand-protein interactions in inducible nitric-oxide synthase. J. Biol. Chem. 2004, 279, 26489−26499. (17) Zhou, Z.; Liu, Q.; Yan, Z.; Long, G.; Zhang, X.; Cao, C.; Jiang, R. Conversion of electron configuration of iron ion through core contraction of porphyrin: implications for heme distortion. Org. Lett. 2013, 15, 606−609. (18) Liu, Q.; Zhou, X.; Liu, H.; Zhang, X.; Zhou, Z. Fractional transfer of a free unpaired electron to overcome energy barriers in the formation of Fe4+ from Fe3+ during the core contraction of macrocycles: implication for heme distortion. Org. Biomol. Chem. 2015, 13, 2939−2946. (19) Liu, Q.; Tang, M.; Zeng, W.; Zhang, X.; Wang, J.; Zhou, Z. Optimal size matching and minimal distortion energy: implications for natural selection by the macrocycle of the iron species in heme. Eur. J. Inorg. Chem. 2016, 2016, 5222−5229. (20) Liu, Q.; Zhang, X.; Zeng, W.; Wang, J.; Zhou, Z. Fine-tuning of electronic structure of cobalt(II) ion in nonplanar porphyrins and tracking of a cross-hybrid stage: implications for the distortion of natural tetrapyrrole macrocycles. J. Phys. Chem. B 2015, 119, 14102− 14110. (21) Liu, Q.; Zhang, X.; Zeng, W.; Wang, J.; Zhou, Z. Origin of d-π Interaction in cobalt(II) porphyrins under synergistic effects of core contraction and axial ligation: implications for a ligand effect of natural distorted tetrapyrrole. Chin. J. Chem. 2016, 34, 910−918. (22) Zhou, Z.; Tang, M.; Liu, Q.; Zhang, X.; Zhou, X. Formation of π-cation radicals in highly deformed copper(II) porphyrins: implications for the distortion of natural tetrapyrrole macrocycles. Eur. J. Inorg. Chem. 2016, 2016, 3585−3591. (23) Zhou, Z.; Zhou, X.; Liu, Q.; Zhang, X.; Liu, H. Fixation of zinc(II) ion to dioxygen in a highly deformed porphyrin: implications for the oxygen carrier mechanism of distorted heme. Org. Lett. 2015, 17, 4078−4081. (24) Poulos, T. L. Heme enzyme structure and function. Chem. Rev. 2014, 114, 3919−3962. (25) Kaim, W. Manifestations of noninnocent ligand behavior. Inorg. Chem. 2011, 50, 9752−9765. (26) Saha, S.; Gogoi, K.; Mondal, B.; Ghosh, S.; Deka, H.; Mondal, B. Reaction of a nitrosyl complex of cobalt porphyrin with hydrogen peroxide: putative formation of peroxynitrite intermediate. Inorg. Chem. 2017, 56, 7781−7787. (27) Adler, A. D.; Longo, F. R.; Kampas, F.; Kim, J. On the preparation of metalloporphyrins. J. Inorg. Nucl. Chem. 1970, 32, 2443−2445. (28) Kohn, W.; Sham, L. J. Self-consistent equations including exchange and correlation effects. Phys. Rev. 1965, 140, A1133−A1138. (29) Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, J. A., Jr.; Peralta, J. E.; Ogliaro, F.; Bearpark, M.; Heyd, J. J.; Brothers, E.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, N. J.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas, Ö .; J

DOI: 10.1021/acs.inorgchem.7b02455 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry (49) Fujii, H. Characterization and intramolecular spin coupling of a monomeric a1u copper(II) porphyrin π-cation radical. Inorg. Chem. 1993, 32, 875−879. (50) Liao, M.-S.; Scheiner, S. β-Substituted copper porphyrin cations: A2u or A1u radicals? Chem. Phys. Lett. 2003, 367, 199−206. (51) Nishida, Y.; Kida, S. Splitting of d-orbitals in square planar complexes of copper(II), nickel(II) and cobalt(II). Coord. Chem. Rev. 1979, 27, 275−298. (52) La Mar, G. N.; Walker, F. A. Proton nuclear magnetic resonance and electron spin resonance investigation of axial solvation in planar, low-spin cobalt(II) porphyrin complexes. J. Am. Chem. Soc. 1973, 95, 1790−1796. (53) Usov, O. M.; Choi, P. S.; Shapleigh, J. P.; Scholes, C. P. ENDOR of NO-ligated cytochrome c’. J. Am. Chem. Soc. 2006, 128, 5021−5032. (54) Usov, O. M.; Sun, Y.; Grigoryants, V. M.; Shapleigh, J. P.; Scholes, C. P. EPR-ENDOR of the Cu(I)NO complex of nitrite reductase. J. Am. Chem. Soc. 2006, 128, 13102−13111. (55) Pietrzyk, P.; Sojka, Z. Co2+/Co0 redox couple revealed by EPR spectroscopy triggers preferential coordination of reactants during SCR of NOx with propene over cobalt-exchanged zeolites. Chem. Commun. 2007, 1930−1932. (56) Abe, M. Diradicals. Chem. Rev. 2013, 113, 7011−7088. (57) Coulson, A. F. W.; Yonetani, T. Oxidation of cytochrome c peroxidase with hydrogen peroxide: Identification of the ‘Endogenous donor’. Biochem. Biophys. Res. Commun. 1972, 49, 391−398. (58) Little, R. G.; Hoffman, B. M.; Ibers, J. A. The coordination of sterically hindered bases to metalloporphyrins. Bioinorg. Chem. 1974, 3, 207−215. (59) Satoh; Ohba, Y.; Yamauchi, S.; Iwaizumi, M. Temperature- and axial-ligand-dependent EPR spectra of cobalt porphyrin cation radicals: effects of mixing of the A1u and A2u states and a locally excited triplet state. Inorg. Chem. 1992, 31, 298−303. (60) Zerner, M.; Gouterman, M. Porphyrins. Theor. Chim. Acta 1966, 4, 44−63. (61) Linder, D. P.; Rodgers, K. R. Fe-N-O structure and bonding in six-coordinate {FeNO}6 porphyrinates containing imidazole: implications for reactivity of coordinated NO. Inorg. Chem. 2005, 44, 1367− 1380. (62) Song, Y.; Haddad, R. E.; Jia, S. L.; Hok, S.; Olmstead, M. M.; Nurco, D. J.; Schore, N. E.; Zhang, J.; Ma, J. G.; Smith, K. M.; Gazeau, S.; Pecaut, J.; Marchon, J. C.; Medforth, C. J.; Shelnutt, J. A. Energetics and structural consequences of axial ligand coordination in nonplanar nickel porphyrins. J. Am. Chem. Soc. 2005, 127, 1179−1192. (63) Christoforidis, K. C.; Louloudi, M.; Milaeva, E. R.; Deligiannakis, Y. Mechanism of catalytic decomposition of pentachlorophenol by a highly recyclable heterogeneous SiO2−[Feporphyrin] catalyst. J. Catal. 2010, 270, 153−162. (64) Zhou, Z.; Cao, C.; Liu, Q.; Jiang, R. Hybrid orbital deformation (HOD) effect and spectral red-shift property of nonplanar porphyrin. Org. Lett. 2010, 12, 1780−1783. (65) Kulcsár, Á .; Saltiel, J.; Zimányi, L. Dissecting the photocycle of the bacteriorhodopsin E204Q mutant from kinetic multichannel difference spectra. extension of the method of singular value decomposition with self-modeling to five components. J. Am. Chem. Soc. 2001, 123, 3332−3340. (66) Van Doorslaer, S.; Schweiger, A. A continuous wave and pulse electron paramagnetic resonance study of Co(II) (tetraphenylporphyrin) in different matrices. Phys. Chem. Chem. Phys. 2001, 3, 159−166. (67) Van Doorslaer, S.; Vinck, E. The strength of EPR and ENDOR techniques in revealing structure-function relationships in metalloproteins. Phys. Chem. Chem. Phys. 2007, 9, 4620−4638. (68) Zimmermann, J.; Siggel, U.; Fuhrhop, J.-H.; Röder, B. Excitonic Coupling between B and Q Transitions in a Porphyrin Aggregate. J. Phys. Chem. B 2003, 107, 6019−6021. (69) Moroni, L.; Gellini, C.; Salvi, P. R.; Marcelli, A.; Foggi, P. Excited states of porphyrin macrocycles. J. Phys. Chem. A 2008, 112, 11044−11051.

(70) Enemark, J. H.; Feltham, R. D. Principles of structure, bonding, and reactivity for metal nitrosyl complexes. Coord. Chem. Rev. 1974, 13, 339−406. (71) Suarez, S. A.; Fonticelli, M. H.; Rubert, A. A.; de la Llave, E.; Scherlis, D.; Salvarezza, R. C.; Marti, M. A.; Doctorovich, F. A surface effect allows HNO/NO discrimination by a cobalt porphyrin bound to gold. Inorg. Chem. 2010, 49, 6955−6966. (72) Richter-Addo, G. B.; Hodge, S. J.; Yi, G.-B.; Khan, M. A.; Ma, T.; Van Caemelbecke, E.; Guo, N.; Kadish, K. M. Synthesis, characterization, and spectroelectrochemistry of cobalt porphyrins containing axially bound nitric oxide. Inorg. Chem. 1996, 35, 6530− 6538. (73) Olea, C., Jr.; Kuriyan, J.; Marletta, M. A. Modulating heme redox potential through protein-induced porphyrin distortion. J. Am. Chem. Soc. 2010, 132, 12794−12795. (74) Kadish, K. M. The Electrochemistry of Metalloporphyrins in Nonaqueous Media. In Progress in Inorganic Chemistry; Lippard, S. J., Ed.; John Wiley & Sons, Inc.: Hoboken, NJ, 2007; Vol. 34, pp 435− 605. (75) Ghosh, A.; Halvorsen, I.; Nilsen, H. J.; Steene, E.; Wondimagegn, T.; Lie, R.; van Caemelbecke, E.; Guo, N.; Ou, Z.; Kadish, K. M. Electrochemistry of nickel and copper β-octahalogenomeso-tetraarylporphyrins. Evidence for important role played by saddling-induced metal(dx2‑y2)−Porphyrin(“a2u”) orbital interactions. J. Phys. Chem. B 2001, 105, 8120−8124. (76) Simonneaux, G.; Schünemann, V.; Morice, C.; Carel, L.; Toupet, L.; Winkler, H.; Trautwein, A. X.; Walker, F. A. Structural, magnetic, and dynamic characterization of the (dxz,dyz)4(dxy)1 groundstate low-spin iron(III) tetraphenylporphyrinate complex [(p-TTP)Fe(2,6-XylylNC)2]CF3SO3. J. Am. Chem. Soc. 2000, 122, 4366−4377. (77) Kadish, K. M.; Royal, G.; Caemelbecke, E. V. In The Porphyrin Handbook; Kadish, K. M., Smith, K. M., Guilard, R., Eds.; Academic Press: San Diego; Vol. 8, pp 1−114. (78) Fang, Y.; Gorbunova, Y. G.; Chen, P.; Jiang, X.; Manowong, M.; Sinelshchikova, A. A.; Enakieva, Y. Y.; Martynov, A. G.; Tsivadze, A. Y.; Bessmertnykh-Lemeune, A.; Stern, C.; Guilard, R.; Kadish, K. M. Electrochemical and spectroelectrochemical studies of diphosphorylated metalloporphyrins. Generation of a phlorin anion product. Inorg. Chem. 2015, 54, 3501−3512. (79) Kelly, S.; Lancon, D.; Kadish, K. M. Electron-transfer and ligand-addition reactions of (TTP)Mn(NO) and (TTP)Co(NO) in a nonaqueous media. Inorg. Chem. 1984, 23, 1451−1458.

K

DOI: 10.1021/acs.inorgchem.7b02455 Inorg. Chem. XXXX, XXX, XXX−XXX