Heme Photolysis Occurs by Ultrafast Excited State Metal-to-Ring Charge Transfer

Franzen, Stefan; Kiger, Laurent; Poyart, Claire; Martin, Jean−Louis

doi:10.1016/s0006-3495(01)76207-8

Cited by 120 publications

(197 citation statements)

References 77 publications

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“…In the sixcoordinate bound state with heme iron the spin states are S ϭ 0, S ϭ 1͞2, and S ϭ 0, for Im-FeP-CO, Im-FeP-NO, and Im-FeP-O 2 , respectively. After photolysis, the diatomic ligands move away from the iron along the coordinate Q D and the spin state of the iron changes from S ϭ 0 to S ϭ 2 as the d-electrons populate the d z 2 and d x 2 -y 2 orbitals of the five-coordinate adduct (2). Experimental evidence suggests that iron out-of-plane motion is extremely rapid along coordinate Q P (46,47).…”

Section: Discussionmentioning

confidence: 99%

“…The calculations of Im-FeP-XO (X ϭ C, N, and O) models consider geometries at Q P ϭ 0.2 and 0.4 Å to include two possible out-of-plane geometries. Given the rapidity of photolysis, it is reasonable to assume that the spin state of the iron is randomized relative to that of the photolyzed ligand (2,50). The assumption that the spin states of the free ligands and the iron are uncorrelated implies that possible spin states are S Fe ϩ S ligand , S Fe ϩ S ligand Ϫ 1, .…”

Section: Discussionmentioning

confidence: 99%

“…The dissociation of carbon monoxide (CO), nitric oxide (NO), and oxygen (O 2 ) from the iron of heme occurs by both a thermal and photolytic process (2)(3)(4). In the case of flash photolysis, the fate of the ligand depends on the competition between the intrinsic (or geminate) recombination rate constant and protein relaxation in a docking site roughly 3.5 Å from the iron as well as ligand escape from the protein (5)(6)(7)(8).…”

mentioning

confidence: 99%

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Spin-dependent mechanism for diatomic ligand binding to heme

Franzen

2002

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

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105

134

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The nature of diatomic ligand recombination in heme proteins is elucidated by using a Landau-Zener model for the electronic coupling in the recombination rate constant. The model is developed by means of explicit potential energy surfaces calculated by using density functional theory (DFT). The interaction of all possible spin states of the three common diatomic ligands, CO, NO, and O2, and high-spin heme iron is compared. The electronic coupling, rebinding barrier, and Landau-Zener force terms can be obtained and used to demonstrate significant differences among the ligands. In particular the intermediate spin states of NO (S ‫؍‬ 3͞2) and O2 (S ‫؍‬ 1) are shown to be bound states. Rapid recombination occurs from these bound states in agreement with experimental data. The slower phases of O2 recombination can be explained by the presence of two higher spin states, S ‫؍‬ 2 and S ‫؍‬ 3, which have a small and relatively large barrier to ligand recombination, respectively. By contrast, the intermediate spin state for CO is not a bound state, and the only recombination pathway for CO involves direct recombination from the S ‫؍‬ 2 state. This process is significantly slower according to the Landau-Zener model. Quantitative estimates of the parameters used in the rate constants provide a complete description that explains rebinding rates that range from femtoseconds to milliseconds at ambient temperature.T he binding of diatomic ligands to heme has been studied for over 100 years (1). The dissociation of carbon monoxide (CO), nitric oxide (NO), and oxygen (O 2 ) from the iron of heme occurs by both a thermal and photolytic process (2-4). In the case of flash photolysis, the fate of the ligand depends on the competition between the intrinsic (or geminate) recombination rate constant and protein relaxation in a docking site roughly 3.5 Å from the iron as well as ligand escape from the protein (5-8). Recombination of these ligands occurs by the reverse of the thermal process. The time dependence of recombination serves as a probe of the intrinsic properties of the diatomic ligand-iron bond formation and dynamic processes that occur in the protein that surrounds the heme cofactor (9-11). The startlingly different recombination dynamics of CO, NO, and O 2 have been attributed to spin states in earlier work (3,12). In the present study, the ground state potential energy surfaces for the potential energy surfaces of all possible spin states are calculated by using density functional theory (DFT) and compared within the context of a Landau-Zener (L-Z) model for the intrinsic recombination process of each of the ligands. The observed recombination kinetics of CO, NO, and O 2 can be influenced by protein dynamics if the intrinsic recombination rate constant is slower than these dynamics (10,(13)(14)(15)(16). When a combination of temperature and viscosity dependence is used, the general time scale for the intrinsic rate constants can be extracted, and it is these rate constants that are compared in the present work.The rebindin...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Spin-dependent mechanism for diatomic ligand binding to heme

Franzen

2002

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

Self Cite

105

134

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“…13) While low energy UV-visible or infra-red spectroscopy can also probe d-d transitions, the optical spectra are dominated by intense %-% Ã absorption bands from the porphyrin ring, the so-called Q-or B-(Soret) bands. 14,15) This makes it difficult to separate out the ligand character states from the pure Fe character d-d transitions in myoglobins, although resonance Raman spectroscopy study 16) have discussed iron to porphyrin ring charge transfer as a key element of photolysis of diatomic ligands. As will be shown in the following, using RXES and model cluster calculations, we quantify the electronic structure of four different aqueous myoglobin …”

Section: Introductionmentioning

confidence: 99%

Ligand Energy Controls the Heme-Fe Valence in Aqueous Myoglobins

et al. 2009

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We use resonant X-ray emission spectroscopy and model calculations to quantify the ligand: heme-Fe energy structure of aqueous myoglobins. For reduced (Fe 2þ ) and oxidized (Fe 3þ ) states, the removal or addition of an electron primarily involves charge changes on the ligand-site, and not the Fe-site. The results indicate a finite positive/negative charge-transfer energy Á between the heme-Fe 3d and ligand valence electronic states for Fe 2þ /Fe 3þ . Thus, the energy difference between the ligand and Fe 3d states (þÁ or ÀÁ) determines the charge properties of myoglobins. The study provides a reliable method for characterizing ligand-metal binding of biological systems in solution.

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“…Light absorption within the Soret band at 400 nm induces a sub-100-fs photodissociation process in MbO 2 , whereas metMb undergoes ultrafast internal conversion without dissociation of water. [68][69][70][71] The present 2DRR experiments are dominated by vibrational motions on the ground state potentials because of the short excited state lifetimes and one-color experimental conditions. 2DRR spectra acquired for both metMb and MbO 2 are presented in Figures 7(b) and 7(c), respectively.…”

Section: B Resolution Of Line Broadening Mechanisms In Water-and Oxymentioning

confidence: 98%

Perspective: Two-dimensional resonance Raman spectroscopy

Molesky

Guo

Cheshire

et al. 2016

The Journal of Chemical Physics

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Two-dimensional resonance Raman (2DRR) spectroscopy has been developed for studies of photochemical reaction mechanisms and structural heterogeneity in complex systems. The 2DRR method can leverage electronic resonance enhancement to selectively probe chromophores embedded in complex environments (e.g., a cofactor in a protein). In addition, correlations between the two dimensions of the 2DRR spectrum reveal information that is not available in traditional Raman techniques. For example, distributions of reactant and product geometries can be correlated in systems that undergo chemical reactions on the femtosecond time scale. Structural heterogeneity in an ensemble may also be reflected in the 2D spectroscopic line shapes of both reactive and non-reactive systems. In this perspective article, these capabilities of 2DRR spectroscopy are discussed in the context of recent applications to the photodissociation reactions of triiodide and myoglobin. We also address key differences between the signal generation mechanisms for 2DRR and off-resonant 2D Raman spectroscopies. Most notably, it has been shown that these two techniques are subject to a tradeoff between sensitivity to anharmonicity and susceptibility to artifacts. Overall, recent experimental developments and applications of the 2DRR method suggest great potential for the future of the technique. Published by AIP Publishing. [http://dx

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Heme Photolysis Occurs by Ultrafast Excited State Metal-to-Ring Charge Transfer

Cited by 120 publications

References 77 publications

Spin-dependent mechanism for diatomic ligand binding to heme

Spin-dependent mechanism for diatomic ligand binding to heme

Ligand Energy Controls the Heme-Fe Valence in Aqueous Myoglobins

Perspective: Two-dimensional resonance Raman spectroscopy

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