Nitric oxide monooxygenation (NOM) reaction of cobalt-nitrosyl {Co(NO)}⁸ to Co^II-nitrito {Co^II(NO₂⁻)}: base induced hydrogen gas (H₂) evolution

Abstract

Here, we report the nitric oxide monooxygenation (NOM) reactions of a Co^III-nitrosyl complex (1, {Co-NO}⁸) in the presence of mono-oxygen reactive species, i.e., a base (OH⁻, tetrabutylammonium hydroxide (TBAOH) or NaOH/15-crown-5), an oxide (O²⁻ or Na₂O/15-crown-5) and water (H₂O). The reaction of 1 with OH⁻ produces a Co^II-nitrito complex {3, (Co^II-NO₂⁻)} and hydrogen gas (H₂), via the formation of a putative N-bound Co-nitrous acid intermediate (2, {Co-NOOH}⁺). The homolytic cleavage of the O–H bond of proposed [Co-NOOH]⁺ releases H₂via a presumed Co^III-H intermediate. In another reaction, 1 generates Co^II-NO₂⁻ when reacted with O²⁻via an expected Co^I-nitro (4) intermediate. However, complex 1 is found to be unreactive towards H₂O. Mechanistic investigations using ¹⁵N-labeled-¹⁵NO and ²H-labeled-NaO²H (NaOD) evidently revealed that the N-atom in Co^II-NO₂⁻ and the H-atom in H₂ gas are derived from the nitrosyl ligand and OH⁻ moiety, respectively.

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As a radical species, nitric oxide (NO) has attracted great interest from the scientific community due to its major role in various physiological processes such as neurotransmission, vascular regulation, platelet disaggregation and immune responses to multiple infections.¹ Nitric oxide synthase (NOS),² and nitrite reductase (NiR)³ enzymes are involved in the biosynthesis of NO. NOSs produce NO by the oxidation of the guanidine nitrogen in L-arginine.⁴ However, in mammals and bacteria, NO₂⁻ is reduced to NO by NiRs in the presence of protons, i.e., NO₂⁻ + e⁻ + 2H⁺ → NO + H₂O.⁵ Biological dysfunctions may cause overproduction of NO, and being radical it leads to the generation of reactive nitrogen species (RNS), i.e., peroxynitrite (PN, OONO⁻)⁶ and nitrogen dioxide (˙NO₂),⁷ upon reaction with reactive oxygen species (ROS) such as superoxide (O₂˙⁻),⁸ peroxide (H₂O₂),⁹ and dioxygen (O₂).¹⁰ Hence, it is essential to maintain an optimal level of NO. In this regard, nitric oxide dioxygenases (NODs)¹¹ are available in bio-systems to convert excess NO to biologically benign nitrate (NO₃⁻).¹²

NO₂⁻ + Fe^II + H⁺ ↔ NO + Fe^III + OH⁻ (1)

[M–NO]ⁿ + 2OH⁻ → [M–NO₂]⁽ⁿ⁻²⁾ + H₂O (2)

NOD enzymes generate NO₃⁻ from NO;^11b,12−13 however, the formation of NO₂⁻ from NO is still under investigation. Clarkson and Bosolo reported NO₂⁻ formation in the reaction of Co^III-NO and O₂.¹⁴ Nam and co-workers showed the generation of Co^II-NO₂⁻ from Co^III-NO upon reaction with O₂˙⁻.¹⁵ Recently, Mondal and co-workers reported NO₂⁻ formation in the reaction of Co^II-NO with O₂.¹⁶ Apart from cobalt, the formation of Cu^II-NO₂⁻ was also observed in the reaction of Cu^I-NO and O₂.¹⁷ For metal-dioxygen adducts, i.e., Cr^III-O₂˙⁻ and Mn^IV-O₂²⁻, NOD reactions led to the generation of Cr^III-NO₂⁻ (ref. 18) and Mn^V=O + NO₂⁻,¹⁹ respectively. However, the NOD reaction of Fe^III-O₂˙⁻ and Fe^III-O₂²⁻ with NO and NO⁺, respectively, generated Fe^III-NO₃⁻via Fe^IV=O and ˙NO₂.²⁰ Ford suggested that the reaction of ferric-heme nitrosyl with hydroxide leads to the formation of NO₂⁻ and H⁺.¹² Lehnert and co-workers reported heme-based Fe-nitrosyl complexes²¹ showing different chemistries due to the Fe^II-NO⁺ type electronic structures. On the other hand, Bryan proposed that the one-electron reduction of NO₂⁻ to NO in ferrous heme protein is reversible (eqn (1)).²² Also, it is proposed that excess NO in biological systems is converted to NO₂⁻ and produces one equivalent of H⁺ upon reaction with ˙OH.²³ Previously reported reactivity of M–NOs of Fe²⁴ with OH⁻ suggested the formation of NO₂⁻ and one equivalent of H⁺, where H⁺ further reacts with one equivalent of OH⁻ and produces H₂O (eqn (2)).²⁵

Here in this report, we explore the mechanistic aspects of nitric oxide monooxygenation (NOM) reactions of the Co^III-nitrosyl complex, [(12TMC)Co^III(NO⁻)]²⁺/{Co(NO)}⁸ (1),^15,26 bearing the 12TMC ligand (12TMC = 1,4,7,10-tetramethyl-1,4,7,10-tetraazacyclododecane) with mono-oxygen reactive species (O²⁻, OH⁻ and H₂O) (Scheme 1). Complex 1 reacts with the base (OH⁻, tetrabutylammonium hydroxide (TBAOH)/or NaOH in the presence of 15-crown-5 as the OH⁻ source) and generates the corresponding Co^II-nitrito complex, [(12TMC)Co^II(NO₂⁻)]⁺ (3), with the evolution of hydrogen gas (H₂) via the formation of a plausible N-bound Co-nitrous acid intermediate ([Co-NOOH]⁺, 2) in CH₃CN at 273 K (Scheme 1, reaction (I)). Also, when 1 reacts with the oxide (O²⁻ or Na₂O in the presence of 15-crown-5), it generates the Co^II-nitrito complex (3) via a probable Co^I-nitro, [(12TMC)Co^I(NO₂⁻)] (4), intermediate (Scheme 1, reaction (II)); however, 1 does not react with water (Scheme 1, reaction (III)). Mechanistic investigations using ¹⁵N-labeled-¹⁵NO, D-labeled-NaOD and ¹⁸O-labelled-¹⁸OH⁻ demonstrated, unambiguously, that the N and O-atoms in the NO₂⁻ ligand of 3 resulted from NO and OH⁻ moieties; however, the H-atoms of H₂ are derived from OH⁻. To the extent of our knowledge, the present work reports the very first systematic study of Co^III-nitrosyl complex reactions with H₂O, OH⁻ and O²⁻. This new finding presents an alternative route for NO₂⁻ generation in biosystems, and also illustrates a new pathway of H₂ evolution, in addition to the reported literature.^12,27

Scheme 1 Nitric oxide monooxygenation (NOM) reactions of cobalt-nitrosyl complex (1) in the presence of a base (OH⁻), sodium oxide (Na₂O) and water (H₂O).

To further explore the chemistry of [(12TMC)Co^III(NO⁻)]²⁺ (1),^15,26 and the mechanistic insights of NOM reactions, we have reacted it with a base (OH⁻), an oxide (O²⁻), and water (H₂O). When complex 1 was reacted with TBAOH in CH₃CN, the color of complex 1 changed to light pink from dark pink. In this reaction, the characteristic absorption band of 1 (370 nm) disappears within 2 minutes (Fig. 1a; ESI, Experimental section (ES) and Fig. S1a†), producing a Co^II-nitrito complex, [(12TMC)Co^II(NO₂⁻)]⁺ (3), with H₂ (Scheme 1, reaction (Ib)), in contrast to the previous reports on base induced NOM reactions (eqn (2)).^12,25,28 The spectral titration data confirmed that the ratio-metric equivalent of OH⁻ to 1 was 1 : 1 (ESI, Fig. S1b†). 3 was determined to be [(12TMC)Co^II(NO₂⁻)](BF₄) based on various spectroscopic and structural characterization experiments (vide infra).^15,26b

The FT-IR spectrum of 3 showed a characteristic peak for nitrite stretching at 1271 cm⁻¹ (Co^II-14NO₂⁻) and shifted to 1245 cm⁻¹ (Co^II-15NO₂⁻) when 3 was prepared by reacting ¹⁵N-labeled NO (Co^III-15NO) with OH⁻ (Inset, Fig. 1a and Fig. S2†). The shifting of NO₂⁻ stretching (Δ = 30 cm⁻¹) indicates that the N-atom in the NO₂⁻ ligand is derived from Co^III-15NO. The ESI-MS spectrum of 3 showed a prominent peak at m/z 333.2, [(12TMC)Co^II(¹⁴NO₂⁻)]⁺ (calcd m/z 333.2), which shifted to 334.2, [(12TMC)Co^II(¹⁵NO₂⁻)]⁺ (calcd m/z 334.2), when the reaction was performed with Co^III-15NO (Inset, Fig. 1b; ESI, Fig. S3a†); indicating clearly that NO₂⁻ in 3 was derived from the NO moiety of 1. In addition, we have reacted 1 with Na¹⁸OH (ES and ESI†), in order to follow the source of the second O-atom in 3-NO₂⁻. The ESI-MS spectrum of the reaction mixture, obtained by reacting 1 with Na¹⁸OH, showed a prominent peak at m/z 335.2, [(12TMC)Co^II(¹⁸ONO⁻)]⁺ (calcd m/z 335.2), (SI, Fig. S3b†) indicating clearly that NO₂⁻ in 3 was derived from ¹⁸OH⁻. The ¹H NMR spectrum of 3 did not show any signal for aliphatic protons of the 12TMC ligand, suggesting a bivalent cobalt center (Fig. S4†).^26b Furthermore, we have determined the magnetic moment of 3, using Evans' method, and it was found to be 4.62 BM, suggesting a high spin Co(II) metal center with three unpaired electrons (ESI† and ES).²⁹ The exact conformation of 3 was provided by single-crystal X-ray crystallographic analysis (Fig. 2b, ESI, ES, Fig. S5, and Tables T1 and T2†) and similar to that of previously reported Co^II-NO₂⁻/M^II-NO₂⁻.^15,26b Also, we have quantified the amount of nitrite (90 ± 5%), formed in the above reaction, using the Griess reagent (ESI, ES, and Fig. S6†).

Fig. 1 (a) UV-vis spectral changes of 1 (0.50 mM, black line) upon addition of OH⁻ (1 equiv.) in CH₃CN under Ar at 273 K. Black line (1) changed to red line (3) upon addition of OH⁻. Inset: IR spectra of 3-¹⁴NO₂⁻ (blue line) and 3-¹⁵NO₂⁻ (red line) in KBr. (b) ESI-MS spectra of 3. The peak at 333.2 is assigned to [(12TMC)Co^II(NO₂)]⁺ (calcd m/z 333.1). Inset: isotopic distribution pattern for 3-¹⁴NO₂⁻ (red line) and 3-¹⁵NO₂⁻ (blue line).

Fig. 2 Displacement ellipsoid plot (20% probability) of 3 at 100 K. Disordered C-atoms of the TMC ring, anion and H-atoms have been removed for clarity.

As is known from the literature, a metal-nitrous acid intermediate may form either by the reaction of a metal-nitrosyl with a base²⁷ or by the metal-nitrite reaction with an acid (nitrite reduction chemistry);^26b however, the products of both the reactions are different. Here, for the first time, we have explored the reaction of Co^III-nitrosyl (1) with a base. In this reaction, it is clear that the formation of Co^II-nitrito would be accomplished by the release of H₂ gas via the generation of a transient N-bound [Co-(NOOH)]⁺ intermediate (Scheme 2, reaction (II)). The formation of Co^II-NO₂⁻ (3) from the [Co-(NOOH)]⁺ intermediate is likely to proceed by either (i) homolytic cleavage of the O–H bond and release of H₂via the proposed Co^III-H transient species (Co^III-H = Co^II + 1/2H₂)³⁰ (Scheme 2, reaction (III)), as reported in previous literature where the reduced cobalt, in a number of different ligand environments, is a good H⁺ reduction catalyst and generates H₂ gas via a Co^III-H intermediate³¹ or (ii) heterolytic cleavage of the O–H bond and the formation of Co^I-NO₂⁻ + H⁺.²⁷ In the present study, we observed the formation of 3 and H₂via the plausible homolytic cleavage of the NOO–H moiety of 2 as shown in Scheme 2, in contrast to the previous reports on base-induced reactions on metal-nitrosyls (eqn (3)).²⁷ Taking together both possibilities, (i) is the most reasonable pathway for the NOM reaction of complex 1 in the presence of a base (as shown in Scheme 2, reaction (III)). And the reaction is believed to go through a Co^III-H intermediate as reported previously in Co^I-induced H⁺ reduction in different ligand frameworks and based on literature precedence, we believe that complex 1 acts in a similar manner.³¹

Scheme 2 NOM reaction of complex 1 in the presence of OH⁻, showing the generation of Co^II-nitrito (3) and H₂via a Co(III)-hydrido intermediate.

In contrast to an O-bound Co^II-ONOH intermediate, where N–O bond homolysis of the ON-OH moiety generates H₂O₂ (Scheme 2, reaction (IV)),^26b the N-bound [Co-(NOOH)]⁺ intermediate decomposes to form NO₂⁻ and a Co(III)-H transient species, arising from β-hydrogen transfer from the NOO–H moiety to the cobalt-center (Scheme 2, reaction (II)).^30a,c,32 The Co(III)-hydrido species may generate H₂ gas either (a) by its transformation to the Co(II)-nitrito complex (2) and H₂ gas as observed in the case of Co^III-H intermediate chemistry^30a,c,e−g as proposed in the chemistry of the Co^I complex with H⁺ reduction³¹ and other metal-hydrido intermediates³² and also explained in O₂ formation in PN chemistry^17,33 or (b) by the reacting with another [Co-(NOOH)]⁺ intermediate (Scheme 2, reaction (III)).

Furthermore, we have confirmed the H₂ formation in the NOM reaction of 1 with OH⁻ by headspace gas mass spectrometry (Fig. 3a). Also, carrying out the reaction of 1 with NaOD leads to the formation of the [Co-(NOOD)]⁺ intermediate, which then transforms to a Co^III-D transient species. Further, as described above, the Co^III-D species releases D₂ gas, detected by headspace gas mass spectrometry (Fig. 3b), which evidently established that H₂ gas formed in the reaction of 1 with OH⁻. In this regard, we have proposed that in the first step of this reaction, the nucleophilic addition of OH⁻ to {Co-NO}⁸ generates a transient N-bound [Co-(NOOH)]⁺ intermediate that is generated by an internal electron transfer to Co^III (Scheme 2, reaction (I)). By following the mechanism proposed in the case of Co^III-H,^30a−c O₂,¹⁵ and H₂O₂(ref. 26b) formation, we have proposed the sequences of the NOM reaction of 1, which leads to the generation of Co^II-nitrito and H₂ (Scheme 2, reaction (I)–(III) and Scheme 3). In the second step, O–H bond homolytic cleavage generates a Co^III-H transient species + NO₂⁻via a β-hydrogen elimination reaction of the [Co-(NOOH)]⁺ intermediate.³² The Co^III-H intermediate may undergo the following reactions to generate H₂ gas and Co^II-nitrito either (a) by the natural decomposition of the Co^III-H transient species to generate H₂,^30a,c,e−g or (b) by the H-atom abstraction from another [Co-(NOOH)]⁺ intermediate (Scheme 3). Also, to validate our assumption that the reaction goes through a plausible N-bound [Co-(NOOH)]⁺ intermediate followed by its transformation to the Co^III-H species (vide supra), we have performed the reaction of 1 with NaOH/NaOD (in 1 : 1 ratio). In this reaction, we have observed the formation of a mixture of H₂, D₂, and HD gases, which indicates clearly that the reaction goes through the formation of Co^III-H and Co^III-D transient species via the aforementioned mechanism (Fig. 3c). This is the only example where tracking of the H atoms has confirmed the H₂ generation from an N-bound NOO–H moiety as proposed for H₂ formation from Co^III-H.³⁰

Fig. 3 Mass spectra of formation of (a) H₂ in the reaction of 1 (5.0 mM) with NaOH (5.0 mM), (b) D₂ in the reaction of 1 (5.0 mM) with NaOD (5.0 mM), (c) D₂, HD, and H₂ in the reaction of 1 (5.0 mM) with NaOD/NaOH (1 : 1), and (d) H₂ in the reaction of 1 (5.0 mM) with NaOH in the presence of 2,4 DTBP (50 mM).

Scheme 3 NOM reaction of complex 1 in the presence of OH⁻, showing the different steps of the reaction.

While, we do not have direct spectral evidence to support the formation of the transient N-bound [Co-(NOOH)]⁺ intermediate and its decomposition to the Co^III-H transient species via β-hydrogen transfer from the NOOH moiety to the cobalt center, support for its formation comes from our finding that the reactive hydrogen species can be trapped by using 2,4-di-tert-butyl-phenol (2,4-DTBP).³⁴ In this reaction, we observed the formation of 2,4-DTBP-dimer (2,4-DTBP-D, ∼67%) as a single product (ESI, ES, and Fig. S7†). This result can readily be explained by the H-atom abstraction reaction of 2,4-DTBP either by [Co-(NOOH)]⁺ or Co^III-H, hence generating a phenoxyl-radical and 3 with H₂ (Fig. 3d and Scheme 2, reaction (a)). Also, we have detected H₂ gas formation in this reaction (ESI,† ES, and Fig. 3d). In the next step, two phenoxyl radicals dimerized to give 2,4-DTBP-dimer (Scheme 2c, reaction (II)). Thus, the observation of 2,4-DTBP-dimer in good yield supports the proposed reaction mechanism (Scheme 2, reaction (a) and (b)). Further, the formation of 2,4 DTBP as a single product also rules out the formation of the hydroxyl radical as observed in the case of an O-bound nitrous acid intermediate.^26b

Furthermore, we have explored the NOM reactivity of 1 with Na₂O/15-crown-5 (as the O²⁻ source) and observed the formation of the Co^II-nitrito complex (3) via a plausible Co^I-nitro (4) intermediate (Scheme 1, reaction (IIa); also see the ESI† and ES); however, 1 was found to be inert towards H₂O (Scheme 1, reaction (III); also see the ESI, ES and Fig. S8†). The product obtained in the reaction of 1 with O²⁻ was characterized by various spectroscopic measurements.^15,26b The UV-vis absorption band of 1 (λ_max = 370 nm) disappears upon the addition of 1 equiv. of Na₂O and a new band (λ_max = 535 nm) forms, which corresponds to 3 (ESI, Fig. S9†). The FT-IR spectrum of the isolated product of the above reaction shows a characteristic peak for Co^II-bound nitrite at 1271 cm⁻¹, which shifts to 1245 cm⁻¹ when exchanged with ¹⁵N-labeled-NO (¹⁵N¹⁶O) (ESI, ES, and Fig. S10†), clearly indicating the generation of nitrite from the NO ligand of complex 1.^26b The ESI-MS spectrum recorded for the isolated product (vide supra) shows a prominent ion peak at m/z 333.1, and its mass and isotope distribution pattern matches with [(12-TMC)Co^II(NO₂)]⁺ (calc. m/z 333.1) (ESI, Fig. S11†). Also, we quantified the amount of 3 (85 ± 5%) by quantifying the amount of nitrite (85 ± 5%) using the Griess reagent test (ESI, ES, and Fig. S6†).

In summary, we have demonstrated the reaction of Co^III-nitrosyl, [(12-TMC)Co^III(NO⁻)]²⁺/{CoNO}⁸ (1), with mono-oxygen reactive species (O²⁻, OH⁻ and H₂O) (Scheme 1). For the first time, we have established the clear formation of a Co^II-nitrito complex, [(12TMC)Co^II(NO₂⁻)]⁺ (3), and H₂ in the reaction of 1 with one equivalent of OH⁻via a transient N-bound [Co-(NOOH)]⁺ (2) intermediate. This [Co-(NOOH)]⁺ intermediate undergoes the O–H bond homolytic cleavage and generates a Co^III-H transient species with NO₂⁻, via a β-hydrogen elimination reaction of the [Co-(NOOH)]⁺ intermediate, which upon decomposition produces H₂ gas. This is in contrast to our previous report, where acid-induced nitrite reduction of 3 generated 1 and H₂O₂via an O-bound Co^II-ONOH intermediate.^26b Complex 1 was found to be inert towards H₂O; however, we have observed the formation of 3 when reacted with O²⁻. It is important to note that H₂ formation involves a distinctive pathway of O–H bond homolytic cleavage in the [Co-(NOOH)]⁺ intermediate, followed by the generation of the proposed Co^III-H transient species (Co^II + 1/2H₂)³⁰ prior to H₂ evolution as described in Co^I chemistry with H⁺ in many different ligand frameworks.³¹ The present study is the first-ever report where the base induced NOM reaction of Co^III-nitrosyl (1) leads to Co^II-nitrito (3) with H₂ evolution via an N-bound [Co-(NOOH)]⁺ intermediate, in contrast to the chemistry of O-bound Co^II-ONOH^26b, hence adding an entirely new mechanistic insight of base induced H₂ gas evolution and an additional pathway for NOM reactions.

Conflicts of interest

There are no conflicts to declare.

Acknowledgements

This work was supported by Grants-in-Aid (Grant No. EEQ/2016/000466) from SERB-DST. We acknowledge Prof. Wonwoo Nam and co-workers for the stabilization of initial complexes and providing a ground to develop new chemistry. We acknowledge Prof. K. N. Ganesh (Director, IISER Tirupati) for continuous guidance and support, special thanks to Dr Sayam Sen Gupta (IISER Kolkata), Dr E. Balaraman (IISER Tirupati) and Dr R. O. Ramabhadran (IISER Tirupati) for fruitful discussion and support. SCS thanks DST-FIST for the single crystal facility at PU.

References

1. (a) G. B. Richter-Addo, P. Legzdins and J. Burstyn, Chem. Rev., 2002, 102, 857–860; (b) C. Bogdan, Nat. Immunol., 2001, 2, 907–916; (c) L. Jia, C. Bonaventura, J. Bonaventura and J. S. Stamler, Nature, 1996, 380, 221–226; (d) R. F. Furchgott, Angew. Chem., Int. Ed., 1999, 38, 1870–1880; (e) L. J. Ignarro, Angew. Chem., Int. Ed., 1999, 38, 1882–1892; (f) L. J. Ignarro, Nitric oxide: biology and pathobiology, Academic press, 2000.
2. (a) L. Castillo, T. C. deRojas, T. E. Chapman, J. Vogt, J. F. Burke, S. R. Tannenbaum and V. R. Young, Proc. Natl. Acad. Sci. U. S. A., 1993, 90, 193–197; (b) R. M. Palmer, D. S. Ashton and S. Moncada, Nature, 1988, 333, 664–666.
3. (a) C. E. Sparacino-Watkins, J. Tejero, B. Sun, M. C. Gauthier, J. Thomas, V. Ragireddy, B. A. Merchant, J. Wang, I. Azarov, P. Basu and M. T. Gladwin, J. Biol. Chem., 2014, 289, 10345–10358; (b) C. Gherasim, P. K. Yadav, O. Kabil, W. N. Niu and R. Banerjee, PLoS One, 2014, 9, e85544; (c) J. L. Zweier, P. Wang, A. Samouilov and P. Kuppusamy, Nat. Med., 1995, 1, 804–809.
4. (a) Q. Liu and S. S. Gross, Methods Enzymol., 1996, 268, 311–324; (b) C. Nathan and Q. W. Xie, J. Biol. Chem., 1994, 269, 13725–13728.
5. (a) B. A. Averill, Chem. Rev., 1996, 96, 2951–2964; (b) J. O. Lundberg, E. Weitzberg and M. T. Gladwin, Nat. Rev. Drug Discovery, 2008, 7, 156–167.
6. R. Radi, Proc. Natl. Acad. Sci. U. S. A., 2004, 101, 4003–4008.
7. C. H. Lim, P. C. Dedon and W. M. Deen, Chem. Res. Toxicol., 2008, 21, 2134–2147.
8. (a) S. Goldstein, J. Lind and G. Merenyi, Chem. Rev., 2005, 105, 2457–2470; (b) P. C. Dedon and S. R. Tannenbaum, Arch. Biochem. Biophys., 2004, 423, 12–22; (c) P. Pacher, J. S. Beckman and L. Liaudet, Physiol. Rev., 2007, 87, 315–424.
9. B. Kalyanaraman, Proc. Natl. Acad. Sci. U. S. A., 2004, 101, 11527–11528.
10. R. S. Lewis and W. M. Deen, Chem. Res. Toxicol., 1994, 7, 568–574.
11. (a) P. R. Gardner, A. M. Gardner, L. A. Martin and A. L. Salzman, Proc. Natl. Acad. Sci. U. S. A., 1998, 95, 10378–10383; (b) M. P. Doyle and J. W. Hoekstra, J. Inorg. Biochem., 1981, 14, 351–358.
12. P. C. Ford and I. M. Lorkovic, Chem. Rev., 2002, 102, 993–1018.
13. M. P. Schopfer, B. Mondal, D. H. Lee, A. A. Sarjeant and K. D. Karlin, J. Am. Chem. Soc., 2009, 131, 11304–11305.
14. S. G. Clarkson and F. Basolo, Inorg. Chem., 1973, 12, 1528–1534.
15. P. Kumar, Y. M. Lee, Y. J. Park, M. A. Siegler, K. D. Karlin and W. Nam, J. Am. Chem. Soc., 2015, 137, 4284–4287.
16. K. Gogoi, S. Saha, B. Mondal, H. Deka, S. Ghosh and B. Mondal, Inorg. Chem., 2017, 56, 14438–14445.
17. G. Y. Park, S. Deepalatha, S. C. Puiu, D. H. Lee, B. Mondal, A. A. Narducci Sarjeant, D. del Rio, M. Y. Pau, E. I. Solomon and K. D. Karlin, J. Biol. Inorg Chem., 2009, 14, 1301–1311.
18. A. Yokoyama, K. B. Cho, K. D. Karlin and W. Nam, J. Am. Chem. Soc., 2013, 135, 14900–14903.
19. S. Hong, P. Kumar, K. B. Cho, Y. M. Lee, K. D. Karlin and W. Nam, Angew. Chem., Int. Ed. Engl., 2016, 55, 12403–12407.
20. A. Yokoyama, J. E. Han, K. D. Karlin and W. Nam, Chem. Commun., 2014, 50, 1742–1744.
21. (a) A. B. McQuarters, J. W. Kampf, E. E. Alp, M. Hu, J. Zhao and N. Lehnert, Inorg. Chem., 2017, 56, 10513–10528; (b) V. K. K. Praneeth, F. Paulat, T. C. Berto, S. D. George, C. Näther, C. D. Sulok and N. Lehnert, J. Am. Chem. Soc., 2008, 130, 15288–15303.
22. N. S. Bryan, Free Radical Biol. Med., 2006, 41, 691–701.
23. T. A. Heinrich, R. S. da Silva, K. M. Miranda, C. H. Switzer, D. A. Wink and J. M. Fukuto, Br. J. Pharmacol., 2013, 169, 1417–1429.
24. J. H. Swinehart, Coord. Chem. Rev., 1967, 2, 385–402.
25. F. Roncaroli, L. M. Baraldo, L. D. Slep and J. A. Olabe, Inorg. Chem., 2002, 41, 1930–1939.
26. (a) P. Kumar, Y. M. Lee, L. Hu, J. Chen, Y. J. Park, J. Yao, H. Chen, K. D. Karlin and W. Nam, J. Am. Chem. Soc., 2016, 138, 7753–7762; (b) M. A. Puthiyaveetil Yoosaf, S. Ghosh, Y. Narayan, M. Yadav, S. C. Sahoo and P. Kumar, Dalton Trans., 2019, 48, 13916–13920.
27. F. Roncaroli, M. E. Ruggiero, D. W. Franco, G. L. Estiu and J. A. Olabe, Inorg. Chem., 2002, 41, 5760–5769.
28. J. H. Swinehart and P. A. Rock, Inorg. Chem., 1966, 5, 573–576.
29. (a) S. Hong, K. D. Sutherlin, J. Park, E. Kwon, M. A. Siegler, E. I. Solomon and W. Nam, Nat. Commun., 2014, 5, 5440; (b) D. F. Evans, J. Chem. Soc., 1959, 2003–2005,  10.1039/jr9590002003; (c) D. F. Evans and D. A. Jakubovic, J. Chem. Soc., Dalton Trans., 1988, 2927–2933,  10.1039/DT9880002927.
30. (a) J. L. Dempsey, J. R. Winkler and H. B. Gray, J. Am. Chem. Soc., 2010, 132, 1060–1065; (b) V. Artero and M. Fontecave, Coord. Chem. Rev., 2005, 249, 1518–1535; (c) J. L. Dempsey, B. S. Brunschwig, J. R. Winkler and H. B. Gray, Acc. Chem. Res., 2009, 42, 1995–2004; (d) M. K. Sahoo, K. Saravanakumar, G. Jaiswal and E. Balaraman, ACS Catal., 2018, 8, 7727–7733; (e) S. C. Marinescu, J. R. Winkler and H. B. Gray, Proc. Natl. Acad. Sci. U. S. A., 2012, 109, 15127–15131; (f) X. Hu, B. S. Brunschwig and J. C. Peters, J. Am. Chem. Soc., 2007, 129, 8988–8998; (g) N. Queyriaux, D. Sun, J. Fize, J. Pécaut, M. J. Field, M. Chavarot-Kerlidou and V. Artero, J. Am. Chem. Soc., 2020, 142, 274–282.
31. (a) V. Artero, M. Chavarot-Kerlidou and M. Fontecave, Angew. Chem., Int. Ed., 2011, 50, 7238–7266; (b) E. S. Andreiadis, P. A. Jacques, P. D. Tran, A. Leyris, M. Chavarot-Kerlidou, B. Jousselme, M. Matheron, J. Pecaut, S. Palacin, M. Fontecave and V. Artero, Nat. Chem., 2013, 5, 48–53; (c) A. E. King, Y. Surendranath, N. A. Piro, J. P. Bigi, J. R. Long and C. J. Chang, Chem. Sci., 2013, 4, 1578–1587; (d) D. Basu, S. Mazumder, X. Shi, H. Baydoun, J. Niklas, O. Poluektov, H. B. Schlegel and C. N. Verani, Angew. Chem., Int. Ed., 2015, 54, 2105–2110; (e) S. Roy, Z. Huang, A. Bhunia, A. Castner, A. K. Gupta, X. Zou and S. Ott, J. Am. Chem. Soc., 2019, 141, 15942–15950.
32. (a) A. Boddien, D. Mellmann, F. Gartner, R. Jackstell, H. Junge, P. J. Dyson, G. Laurenczy, R. Ludwig and M. Beller, Science, 2011, 333, 1733–1736; (b) X. Yang, Dalton Trans., 2013, 42, 11987–11991.
33. (a) O. A. Babich and E. S. Gould, Res. Chem. Intermed., 2002, 28, 575–583; (b) J. W. Coddington, J. K. Hurst and S. V. Lymar, J. Am. Chem. Soc., 1999, 121, 2438–2443; (c) S. Pfeiffer, A. C. Gorren, K. Schmidt, E. R. Werner, B. Hansert, D. S. Bohle and B. Mayer, J. Biol. Chem., 1997, 272, 3465–3470.
34. M. F. R. Mulcahy, D. J. Williams and J. R. Wilmshurst, Aust. J. Chem., 1964, 17, 1329–1341.

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Footnote

† Electronic supplementary information (ESI) available. CCDC 1974616. For ESI and crystallographic data in CIF or other electronic format see DOI: 10.1039/d0sc01572e

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