Factors affecting the iron-oxygen vibrations of ferrous oxy and ferryl oxo heme proteins and model compounds

Oertling, W. A.; Kean, Robert T.; Wever, Ron; Babcock, Gerald T.

doi:10.1021/ic00339a021

Cited by 95 publications

(111 citation statements)

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“…From the relative enhancements of the 2 ferryl modes via excitation into the porphyrin soret band, we believe that the strongly enhanced 756 cm Ϫ1 mode corresponds to the heme ferryl species, whereas the weakly enhanced 808-cm Ϫ1 mode corresponds to the nonheme ferryl species. The Fe-O vibration for the heme ferryl species is on the lower side of the range reported for heme ferryl species (51). These values are very similar to those reported for lactoperoxidase (745 cm Ϫ1 ) and cytochrome c peroxidases (753 cm Ϫ1 ) (52) and may indicate weakening of the Fe IV AO bond by hydrogen bonding or a strong trans effect of the covalently attached proximal imidazole tail (52).…”

Section: Discussionsupporting

confidence: 80%

“…One band is observed at 808 cm Ϫ1 , and the other is observed at 756 cm Ϫ1 ; the bands shift by 32 cm Ϫ1 and 25 cm Ϫ1 , respectively. Fe-O vibrations for Fe IV AO porphyrin species have been observed between 745 cm Ϫ1 and 850 cm Ϫ1 (51,52), and those for nonheme ferryl species are observed between 800 and 840 cm Ϫ1 depending on spin state and different trans ligands (53)(54)(55)(56). The presence of only these 2 oxygen isotope-sensitive bands at 756 cm Ϫ1 and 808 cm Ϫ1 indicate that there are 2 distinct ferryl species in this intermediate.…”

Section: Resultsmentioning

confidence: 96%

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O ₂ reduction by a functional heme/nonheme bis-iron NOR model complex

Collman

Dey

Yang

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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O2 reactivity of a functional NOR model is investigated by using electrochemistry and spectroscopy. The electrochemical measurements using interdigitated electrodes show very high selectivity for 4e O2 reduction with minimal production of partially reduced oxygen species (PROS) under both fast and slow electron flux. Intermediates trapped at cryogenic temperatures and characterized by using resonance Raman spectroscopy under single-turnover conditions indicate that an initial bridging peroxide intermediate undergoes homolytic OOO bond cleavage generating a trans heme/nonheme bis-ferryl intermediate. This bis ferryl species can oxygenate 2 equivalents of a reactive substrate.C ytochrome c oxidase (CcO) and nitric oxide reductase (NOR) belong to the heme copper oxidase superfamily of enzymes (1, 2). CcO is the terminal enzyme in the respiratory chain of higher organisms, located in their mitochondrial membrane, that reduces O 2 to H 2 O as source of energy. The O 2 reduction process in CcO generates a pH gradient across the bilayer membrane, which provides the driving force for ATP synthesis. The bimetallic active site of CcO has a heme ligated to the protein by a proximal histidine ligand and a distal Cu B site coordinated by 3 histidine ligands ( Fig. 1) (3). In addition to the bimetallic site, there is a conserved tyrosine ligand covalently attached to one of the histidines coordinated to Cu B (4, 5). The NORs are the older member of the family and are found in bacteria using NO 3 Ϫ as source of energy instead of O 2 (2, 6, 7). Although there are no high-resolution crystal structures of NOR, biochemical studies and computer modeling indicate that these enzymes have a histidine-ligated heme, quite like the CcOs, and a distal Fe B , unlike Cu B in CcO, coordinated by 3 histidines ( Fig. 1) (8-10). NORs do not have the conserved tyrosine residue of CcO but have a few conserved key glutamate residues (11,12). Although the NOR enzymes are proposed to have specific proton channels, they are probably not involved in generating proton gradients (13-16).These 2 enzymes exhibit complementary reactivity toward 2 very significant diatomic molecules in nature; O 2 and NO. In eukaryotes CcO (aa 3 type) reduces O 2 to H 2 O and is reversibly but strongly inhibited by [17][18][19][20]. Several other CcOs (ba 3 , caa 3 , cbb 3 ) are reported to exhibit limited (Ͻ1%) NOR activity, i.e., reduce NO to N 2 O (7, 21). On the other hand, NORs that reduce NO to N 2 O are reversibly but strongly inhibited by O 2 , and some of them show modest (Ϸ10%) O 2 reduction activity (12). The parallels in their reactivities toward O 2 and NO and similarities in their secondary structures have led to a hypotheses regarding NOR's and CcO's similar evolutionary origins (6,22).Electrochemistry is a very powerful technique that can provide fundamental insights into reaction mechanisms of redox catalysts (23-27). Conventionally, a catalyst is deposited on a conducting electrode material (e.g., graphite); however, this approach does not allow site isola...

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Section: Discussionsupporting

confidence: 80%

Section: Resultsmentioning

confidence: 96%

O ₂ reduction by a functional heme/nonheme bis-iron NOR model complex

Collman

Dey

Yang

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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“…Three major factors can account for the high dissociation rate in LPO-Fe(II)-O 2 including the positive trans effect contributed by the proximal ligand, the heme pocket environment, and the geometry of Fe-O 2 linkage. Indeed, previous resonance Raman spectroscopy studies demonstrated that the (Fe-O 2 ) frequency for LPO was considerably lower than those reported for related and relevant hemoprotein model compounds (37,61,62). Collapse or narrowing in the heme pocket geometry and/or the orientation of the O 2 bond may increase the interaction between the OϭO and the positively charged L-arginine that is localized above the heme iron on the distal side of LPO.…”

Section: Initial Rapid Spectroscopic Characterization Of O 2 Bindingmentioning

confidence: 87%

“…Collapse or narrowing in the heme pocket geometry and/or the orientation of the O 2 bond may increase the interaction between the OϭO and the positively charged L-arginine that is localized above the heme iron on the distal side of LPO. Therefore, the electron density on the antibonding * orbital of the OϭO bond is pulled up by the influence of a positively charged residue localized on the distal side above the heme moiety (62,63). Weakening the Fe-O 2 linkage might allow the ligand trans to O 2 to pull the iron out of the plane away from the O 2 .…”

Section: Initial Rapid Spectroscopic Characterization Of O 2 Bindingmentioning

confidence: 99%

High Dissociation Rate Constant of Ferrous-Dioxy Complex Linked to the Catalase-like Activity in Lactoperoxidase

Galijašević¹,

Saed²,

Diamond³

et al. 2004

Journal of Biological Chemistry

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“…17,18 It is also noted that these lowered frequencies, relative to corresponding values observed near 570 cm -1 for hemoglobin and myoglobin, are also consistent with expectations based on consideration of the trans-axial ligand effects, as has been carefully considered by Babcock and coworkers. 20 These frozen oxygenated samples were then irradiated with a 60 Co γ-source to produce the reduced hydroperoxo forms; the EPR spectra confirmed the conversion with approximately 60% yield ( Figure S2). The RR spectra were acquired using the 442 nm excitation line, a wavelength in closer resonance with the Soret band of the hydroperoxo form.…”

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confidence: 90%

Resonance Raman Detection of the Hydroperoxo Intermediate in the Cytochrome P450 Enzymatic Cycle

et al. 2007

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The resonance Raman spectra of the hydroperoxo complex of camphor-bound CYP101 have been obtained by cryoradiolytic reduction of the oxygenated ferrous form that had been rapidly frozen in water/glycerol frozen solution; EPR spectroscopy was employed to confirm the identity of the trapped intermediate. The ν(O−O) mode, appearing at 799 cm -1 , is observed for the first time in a peroxo-heme adduct. It is assigned unambiguously by employing isotopomeric mixtures of oxygen gas containing 50% 16 O 18 O, confirming the presence of an intact O−O fragment. The ν(Fe−O) mode is observed at 559 cm -1 (H2O). Furthermore, both modes shift down by 3 cm -1 , documenting the formulation as a hydroperoxo complex, in agreement with EPR data.NOT THE PUBLISHED VERSION; this is the author's final, peer-reviewed manuscript. The published version may be accessed by following the link in the citation at the bottom of the page. Society, Vol 129, No. 20 (2007): pg. 6382-6383. DOI. This article is © American Chemical Society and permission has been granted for this version to appear in e-Publications@Marquette. American Chemical Society does not grant permission for this article to be further copied/distributed or hosted elsewhere without the express permission from American Chemical Society. Journal of the American Chemical 3The cytochromes P450 heme-thiolate enzymes facilitate quite difficult chemical transformations through a multistep reaction cycle that culminates in the generation of a remarkably potent oxidizing species capable of hydroxylating even inert substrates. [1][2][3] Following substrate binding to the resting state ferric enzyme, two sequential one-electron reductions bracketing the binding of molecular oxygen and a subsequent proton delivery step lead to heterolytic O−O bond cleavage and formation of a highly reactive ferryl heme species comparable to the so-called Compound I intermediate of peroxidases. [4][5][6] Thus, key precursors to this critical cleavage reaction are activated heme-bound peroxo and hydroperoxo fragments; that is, (protoporphyrin)Fe(III)(O2 2-) or Fe(III)(O−OH -). A useful approach to access and study these species is to generate and trap the relatively stable oxy-ferrous P450 complex and then to subject the cryotrapped (77 K) sample to radiolytic reduction using radiation from synchrotron, 60 Co γ-ray, or 32 P sources. 7,8 Enzymatic intermediates produced by cryoradiolytic reduction of the oxygenated complex of cytochrome P450cam (CYP101) have been detected by both electronic absorption and EPR spectroscopic methods. 7,9,10 However, critical mechanistic information has been missing, and it is now important to attempt to provide more detailed structural characterization of the active sites of these species.Resonance Raman (RR) spectroscopy is an especially attractive probe of such species, effectively interrogating both the heme macrocycle structure and various iron−ligand fragments. [11][12][13][14][15] In fact, the feasibility of coupling this powerful spectroscopic probe with cryogenic ...

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Factors affecting the iron-oxygen vibrations of ferrous oxy and ferryl oxo heme proteins and model compounds

Cited by 95 publications

References 6 publications

O ₂ reduction by a functional heme/nonheme bis-iron NOR model complex

O ₂ reduction by a functional heme/nonheme bis-iron NOR model complex

High Dissociation Rate Constant of Ferrous-Dioxy Complex Linked to the Catalase-like Activity in Lactoperoxidase

Resonance Raman Detection of the Hydroperoxo Intermediate in the Cytochrome P450 Enzymatic Cycle

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Factors affecting the iron-oxygen vibrations of ferrous oxy and ferryl oxo heme proteins and model compounds

Cited by 95 publications

References 6 publications

O 2 reduction by a functional heme/nonheme bis-iron NOR model complex

O 2 reduction by a functional heme/nonheme bis-iron NOR model complex

High Dissociation Rate Constant of Ferrous-Dioxy Complex Linked to the Catalase-like Activity in Lactoperoxidase

Resonance Raman Detection of the Hydroperoxo Intermediate in the Cytochrome P450 Enzymatic Cycle

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O ₂ reduction by a functional heme/nonheme bis-iron NOR model complex

O ₂ reduction by a functional heme/nonheme bis-iron NOR model complex