Probing the electronic and geometric structure of ferric and ferrous myoglobins in physiological solutions by Fe K-edge absorption spectroscopy

Lima, Frederico A.; Penfold, Thomas J.; Veen, Renske M. van der; Reinhard, Marco; Tavernelli, Ivano; Röthlisberger, Ursula; Benfatto, M.; Milne, Christopher J.; Chergui, Majed

doi:10.1039/c3cp53683a

Cited by 41 publications

(61 citation statements)

References 129 publications

(209 reference statements)

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“…Adopting such an approach, X-ray scattering studies of MbCO in solution with a 100-ps resolution were recently reported (38)(39)(40), but the spatial resolution is such that tertiary and global structural changes can be probed but not atomic-scale changes. In addition, this approach does not deliver information about the electronic structure of the active site, which plays a central role in the biochemistry and reactivity of heme proteins (41,42). The valence 3d electrons of the iron atom are significantly delocalized over the porphyrin ligand π*-orbitals, and the ability of the heme to redistribute charge and spin density plays an important role in the formation and stabilization of a variety of intermediates important for biological function (42)(43)(44).…”

Section: Significancementioning

confidence: 99%

“…In addition, this approach does not deliver information about the electronic structure of the active site, which plays a central role in the biochemistry and reactivity of heme proteins (41,42). The valence 3d electrons of the iron atom are significantly delocalized over the porphyrin ligand π*-orbitals, and the ability of the heme to redistribute charge and spin density plays an important role in the formation and stabilization of a variety of intermediates important for biological function (42)(43)(44). Time-resolved X-ray absorption spectroscopy (XAS) (45) offers the advantage of interrogating the electronic and geometric structure of the biochemically active center of the system with elemental selectivity (i.e., the Fe atom).…”

Section: Significancementioning

confidence: 99%

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NO binding kinetics in myoglobin investigated by picosecond Fe K-edge absorption spectroscopy

Silatani

Lima

Penfold

et al. 2015

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

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Diatomic ligands in hemoproteins and the way they bind to the active center are central to the protein's function. Using picosecond Fe K-edge X-ray absorption spectroscopy, we probe the NO-heme recombination kinetics with direct sensitivity to the Fe-NO binding after 532-nm photoexcitation of nitrosylmyoglobin (MbNO) in physiological solutions. The transients at 70 and 300 ps are identical, but they deviate from the difference between the static spectra of deoxymyoglobin and MbNO, showing the formation of an intermediate species. We propose the latter to be a six-coordinated domed species that is populated on a timescale of ∼200 ps by recombination with NO ligands. This work shows the feasibility of ultrafast pump-probe X-ray spectroscopic studies of proteins in physiological media, delivering insight into the electronic and geometric structure of the active center.nitrosylmyoglobin | ligand binding | X-ray absorption | picosecond | pump-probe D iatomic molecules, such as CO, NO, and O 2 , are the receptors that bind to and activate heme proteins. Among them, NO has been highlighted as a key biological messenger (1) and its level controls various physiological responses, such as NO synthases, message transduction (soluble guanylyl cyclases) (2, 3), NO transport and oxidation [hemoglobin, myoglobin (Mb), and nitrophorin] (4-6), and regulation of the NO/O 2 balance (neuroglobin) (7,8). In all of these cases, the heme group that binds the NO ligand is chemically identical, and therefore, variations in the reactivity and function are thought to be closely related to the spin, electronic configuration, and geometric structure on binding (9) and/or suggestive of different steric and electronic interactions of the bound NO with neighboring protein residues (10). Consequently, there is great interest in understanding the nature of NO binding to heme proteins and its biochemical role.The binding kinetics of NO in Mb have been studied by a variety of time-resolved spectroscopic techniques. Ligand dissociation from the heme iron was triggered by excitation into either the Soret or the Q bands, whereas the ensuing dynamics were probed using transient absorption (TA) in the UV visible (UVVis) (11)(12)(13)(14)(15)(16)(17)(18)(19)(20), the near IR (21-23), and the mid-IR (10, 23, 24) or by resonance Raman spectroscopy (20). For UV-Vis and near-IR TA spectroscopy, the signals are dominated by the π-orbitals of the porphyrin, whereas mid-IR TA of the NO stretch mode is sensitive to the orientation of the NO dipole. Resonance Raman spectroscopy maps several vibrational modes of the porphyrin, but most studies have focused on the important Fe-N stretch vibration (at 220 cm −1 ) with the proximal histidine (20,(25)(26)(27), which is sensitive to the position of the iron atom out of the heme plane and to the strain that the protein exerts on the heme through movements of the helices (28, 29).All of the TA studies report multiexponential recombination kinetics with time constants spanning from subpicoseconds to several hundreds of pi...

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Section: Significancementioning

confidence: 99%

Section: Significancementioning

confidence: 99%

NO binding kinetics in myoglobin investigated by picosecond Fe K-edge absorption spectroscopy

Silatani

Lima

Penfold

et al. 2015

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

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“…[1,3] Another alternative is the presence of a strongly binding ligand, e.g., the metal-oxo groups proposed to be the reactive species in many enzymatic and synthetic systems. [4][5][6][7] Oxo groups also appear as bridging ligands in many bi-and multinuclear transition metal complexes.…”

Section: Introductionmentioning

confidence: 99%

Applications to metal K pre-edges of transition metal dimers illustrate the approximate origin independence for the intensities in the length representation

et al. 2016

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PostprintThis is the accepted version of a paper published in Molecular Physics. This paper has been peer-reviewed but does not include the final publisher proof-corrections or journal pagination. Citation for the original published paper (version of record):Sørensen, L K., Guo, M., Lindh, R., Lundberg, M. (2017) Applications to metal K pre-edges of transitionmetal dimers illustrate the approximate origin independence for the intensities in the length representation Molecular Physics, 115(1-2): 174-189

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“…[2][3][4][5] The K preedge directly probes the unoccupied and partially occupied valence orbitals involved in catalysis and can play a key role in the identification and characterization of reactive sites, e.g., site symmetry, oxidation state and ligand-field splitting. [6][7][8][9][10] Westre and co-workers analyzed the iron K pre-edges for a large series of systems, both experimentally and theoretically. They showed how energy and intensity depend on oxidation state and coordination number, and provided a general method for their interpretation.…”

Section: Introductionmentioning

confidence: 99%

“…They showed how energy and intensity depend on oxidation state and coordination number, and provided a general method for their interpretation. 7 The K pre-edge has already been very useful in geometry and electronic structure analysis, such as determining the protonation state of a ferryl intermediate 9 and the coordination number of a non-heme iron active site. 10 For centrosymmetric complexes, the K pre-edges are asso- ciated with electron transitions from the 1s to the 3d orbitals.…”

Section: Introductionmentioning

confidence: 99%

Simulations of iron K pre-edge X-ray absorption spectra using the restricted active space method

Guo

Sørensen

Delcey

et al. 2016

Phys. Chem. Chem. Phys.

106

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Simulations of iron K pre-edge X-ray absorption spectra using the core restricted active space method.Physical Chemistry, http://dx.doi.org/10.1039/c5cp07487hAccess to the published version may require subscription. N.B. When citing this work, cite the original published paper. Permanent link to this version:http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-243571Simulations of iron K pre-edge X-ray absorption spectra using the restricted active space method † Meiyuan Guo, a Lasse Kragh Sørensen, a Mickaël G. Delcey, a,b Rahul V. Pinjari, a,c and Marcus Lundberg * aThe intensities and relative energies of metal K pre-edge features are sensitive to both geometric and electronic structure. With the possibility to collect high-resolution spectral data it important to find theoretical methods that include all important spectral effects: ligand-field splitting, multiplet structures, 3d-4p orbital hybridization, and charge-transfer excitations. Here the restricted active space (RAS) method is used for the first time to calculate metal K pre-edge spectra of open-shell systems, and its performance is tested against six iron complexes: [FeCl 6 ] n-, [FeCl 4 ] n-, and [Fe(CN) 6 ] n-in ferrous and ferric oxidation states. The method gives good descriptions of the spectral shapes for all six systems. The mean absolute deviation for the relative energies of different peaks is only 0.1 eV. For the two systems that lack centrosymmetry [FeCl 4 ] 2-/1-, the ratios between dipole and quadrupole intensity contributions are reproduced with an error of 10%, which leads to good descriptions of the integrated pre-edge intensities. To gain further chemical insight, the origins of the pre-edge features have been analyzed with a chemically intuitive molecular orbital picture that serves as a bridge between the spectra and the electronic structures. The RAS method can thus be used to predict and rationalize the effects of changes in both oxidation state and ligand environment in a number of hard X-ray studies of small and medium-sized molecular systems.

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Probing the electronic and geometric structure of ferric and ferrous myoglobins in physiological solutions by Fe K-edge absorption spectroscopy

Cited by 41 publications

References 129 publications

NO binding kinetics in myoglobin investigated by picosecond Fe K-edge absorption spectroscopy

NO binding kinetics in myoglobin investigated by picosecond Fe K-edge absorption spectroscopy

Applications to metal K pre-edges of transition metal dimers illustrate the approximate origin independence for the intensities in the length representation

Simulations of iron K pre-edge X-ray absorption spectra using the restricted active space method

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