A “Push−Pull” Mechanism for Heterolytic O−O Bond Cleavage in Hydroperoxo Manganese Porphyrins

Abstract

A water-soluble manganese porphyrin, 5,10,15,20-tetrakis-(1,3-dimethylimidazolium-2-yl)porphyrinatomanganese(III) (Mn(III)TDMImP) is shown to react with H(2)O(2) to generate a relatively stable dioxomanganese(V) porphyrin complex (a compound I analog). Stopped-flow kinetic studies revealed Michaelis Menton-type saturation kinetics for H(2)O(2). The visible spectrum of a compound 0 type intermediate, assigned as Mn(III)(OH)(OOH)TDMImP, can be directly observed under saturating H(2)O(2) conditions (Soret band at 428 nm and Q bands at 545 and 578 nm). The rate-determining O-O heterolysis step was found to have a very small activation enthalpy (ΔH(≠) = 4.2 ± 0.2 kcal mol(-1)) and a large, negative activation entropy (ΔS(≠) = -36 ± 1 cal mol(-1) K(-1)). The O-O bond cleavage reaction was pH independent at 8.8 < pH < 10.4 with a first-order rate constant of 66 ± 12 s(-1). These observations indicate that the O-O bond in Mn(III)(OH)(OOH)TDMImP is cleaved via a concerted "push-pull" mechanism. In the transition state, the axial (proximal) (-)OH is partially deprotonated ("push"), while the terminal oxygen in (-)OOH is partially protonated ("pull") as a water molecule is released to the medium. This mechanism is reminiscent of O-O bond cleavage in heme enzymes, such as peroxidases and cytochrome P450, and similar to the fast, reversible O-Br bond breaking and forming reaction mediated by similar manganese porphyrins. The small enthalpy of activation suggests that this O-O bond cleavage could also be made reversible.

Efficient water oxidation catalyzed by homogeneous cationic cobalt porphyrins with critical roles for the buffer base

“…The nucleophilic addition of water to a doubly oxidized cobaltoxo intermediate is formally the microscopic reverse of the conversion of the manganese analog HOO-Mn III TDMImP to transdioxoMn V TDMImP that we have recently described (Scheme 3) (39,40). Here, both the hydroperoxo-manganese(III) complex and the oxo-manganese(V) complex were spectroscopically observed and the kinetics of the process could be analyzed in detail.…”

A mechanistic study on the disproportionation and oxidative degradation of phenothiazine derivatives by manganese(III) complexes in phosphate acidic media

“…Although recent progress in solar energy research has led to an increased interest in photosynthesis and artificial photosynthesis [4,5], the structure of this cluster is still unknown [6][7][8][9] and very few manganese-based homogeneous catalysts have been reported to evolve oxygen upon oxidation [10,11]an observation that, however, has recently been questioned [12]. The ability to catalyze the heterolytic cleavage of the O-O bond in hydrogen peroxide and molecular dioxygen by manganese has been recently intensively studied [13]. Despite the mechanism of these processes catalyzed by heme oxygenases, such as cytochrome P450, cytochrome c oxidase, peroxidases, and catalase being known [14][15][16][17][18][19], direct observation of the O-O bond cleavage has been difficult due to the complex catalytic cycles, short-lived iron intermediates, and required cryogenic conditions.…”

“…Despite the mechanism of these processes catalyzed by heme oxygenases, such as cytochrome P450, cytochrome c oxidase, peroxidases, and catalase being known [14][15][16][17][18][19], direct observation of the O-O bond cleavage has been difficult due to the complex catalytic cycles, short-lived iron intermediates, and required cryogenic conditions. High-valent manganese oxo intermediates are more stable and can be functional analogs of heme proteins appearing in many biological systems using hydrogen peroxide and molecular dioxygen [13]. Recently, a bridged manganese(V) porphyrin dimer was shown to oxidize water into dioxygen, [20] and reversible O-O bond cleavage was observed for a manganese corrole system [21,22], and the design of novel, long-lived manganese(III) complexes, which can be a model of the precursor of the endogenous high-valent peroxo and oxo intermediates, has been published recently [23].…”

SOD Therapeutics: Latest Insights into Their Structure-Activity Relationships and Impact on the Cellular Redox-Based Signaling Pathways

“…Further, the para compounds are planar and, thus, favor intercalation within groves of nucleic acids, which may prevent their action and/or cause toxicity to normal tissue (18,220). Also, it would undergo oxidative degradation faster then ortho analog (30,128). Rawal et al just reported the tumor suppression in sc nude mouse xenograft model of human pancreatic cell line (220).…”