Investigations of Low-Frequency Vibrational Dynamics and Ligand Binding Kinetics of Cystathionine β-Synthase

Karunakaran, Venugopal; Benabbas, Abdelkrim; Sun, Yuhan; Zhang, Zhenyu; Singh, Siddharth; Banerjee, Ruma; Champion, P. M.

doi:10.1021/jp909700r

Cited by 17 publications

(18 citation statements)

References 71 publications

(233 reference statements)

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“…The free energy released on protein/protein complex formation may be converted into vibrational energy of local modes, which could bring the system toward the transition state for ET. In particular, lower frequency modes are thermally accessible and have been shown to play key roles as reaction coordinates in enzyme-facilitated processes (30). In this work, the QCC-NCA analysis of the NRVS data of Cyt c has revealed that most heme-based and Fe-{axial ligand} vibrations have major contributions from pp modes (Table S2).…”

Section: Assignment Of the Nrvs Spectrum Of Ferric Cyt C Density Funmentioning

confidence: 76%

Heme-protein vibrational couplings in cytochrome c provide a dynamic link that connects the heme-iron and the protein surface

Galinato

Kleingardner

Bowman

et al. 2012

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

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The active site of cytochrome c (Cyt c ) consists of a heme covalently linked to a pentapeptide segment (Cys-X-X-Cys-His), which provides a link between the heme and the protein surface, where the redox partners of Cyt c bind. To elucidate the vibrational properties of heme c , nuclear resonance vibrational spectroscopy (NRVS) measurements were performed on 57 Fe-labeled ferric Hydrogenobacter thermophilus cytochrome c 552 , including 13 C 8 -heme–, 13 C 5 15 N-Met–, and 13 C 15 N-polypeptide (pp)–labeled samples, revealing heme-based vibrational modes in the 200- to 450-cm −1 spectral region. Simulations of the NRVS spectra of H. thermophilus cytochrome c 552 allowed for a complete assignment of the Fe vibrational spectrum of the protein-bound heme, as well as the quantitative determination of the amount of mixing between local heme vibrations and pp modes from the Cys-X-X-Cys-His motif. These results provide the basis to propose that heme-pp vibrational dynamic couplings play a role in electron transfer (ET) by coupling vibrations of the heme directly to vibrations of the pp at the protein–protein interface. This could allow for the direct transduction of the thermal (vibrational) energy from the protein surface to the heme that is released on protein/protein complex formation, or it could modulate the heme vibrations in the protein/protein complex to minimize reorganization energy. Both mechanisms lower energy barriers for ET. Notably, the conformation of the distal Met side chain is fine-tuned in the protein to localize heme-pp mixed vibrations within the 250- to 400-cm −1 spectral region. These findings point to a particular orientation of the distal Met that maximizes ET.

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Section: Assignment Of the Nrvs Spectrum Of Ferric Cyt C Density Funmentioning

confidence: 76%

Heme-protein vibrational couplings in cytochrome c provide a dynamic link that connects the heme-iron and the protein surface

Galinato

Kleingardner

Bowman

et al. 2012

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

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“…It is also noteworthy that a number of recent studies 6, 20–21, 33 demonstrate CO binding kinetics that are very different from Mb and Hb. In all of these studies, CO more typically binds to the heme with a prefactor of k 0 ~10 11 s −1 (Table 1), which is similar to that of NO binding 19 .…”

Section: Discussionmentioning

confidence: 99%

Ultrafast CO Kinetics in Heme Proteins: Adiabatic Ligand Binding and Heavy Atom Tunneling

et al. 2017

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We report on the ultrafast kinetics of CO rebinding to carbon monoxide oxidation activator protein (ChCooA) over a wide temperature range and make comparisons with the kinetics of CO and NO binding to protoheme (Fe protoporphyrin IX) and myoglobin (Mb). The CO binding to ChCooA is non-exponential over many decades in time at all temperatures studied, including room temperature. To describe this kinetic response we use a linear coupling model with a distribution of enthalpic rebinding barriers that is attributed primarily to protein-induced heterogeneity in the heme doming conformation (distributed barrier model, DBM). Above the solvent glass transition (Tg ~180K), CO rebinding kinetics displays an anti-Arrhenius behavior (i.e., the rate decreases as temperature increases) and this is ascribed to an evolution of the distribution toward increased heme doming and larger enthalpic barriers. Between Tg and ~60K, the non-exponential rebinding slows down as the temperature is lowered and the survival fraction follows the predictions expected for a quenched barrier distribution. However, below ~60K the rebinding kinetics do not continue to slow as predicted by the thermally activated DBM. A possible explanation for this behavior is explored that involves quantum mechanical tunneling of the iron atom along the heme doming coordinate. When the ultrafast CO rebinding kinetics of CooA are compared to the much slower CO rebinding in myoglobin, a two order-of-magnitude increase in the Arrhenius prefactor, from ~109 s−1 to ~1011 s−1, is revealed. A similar prefactor is found for NO binding to CooA, which is typical for NO rebinding to ferrous heme systems. Because kinetic studies of CO rebinding to protoheme also reveal prefactors near ~1011 s−1, we revisit the commonly held view that the CO binding reaction is non-adiabatic due to spin-forbidden (ΔS=2) selection rules. A non-adiabatic sequential mechanism, involving first order (ΔS=1) transitions, is considered as a possible explanation for ultrafast CO rebinding; however, the relative crossing energies of the relevant spin states leads us to conclude that the CO ligand binding reaction is adiabatic rather than non-adiabatic and that entropic factors, rather than spin-selection rules, are the cause of the reduced Arrhenius prefactor for CO binding in Mb and Hb.

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“…Although difficult to detect in frequency-domain IR or Raman spectroscopy, saddling and ruffling frequencies have been reported to contribute to the time-domain vibrational coherences observed following femtosecond laser excitation. 47, 48 …”

Section: Discussionmentioning

confidence: 99%

Vibrational Probes and Determinants of the S = 0 ⇌ S = 2 Spin Crossover in Five-Coordinate [Fe(TPP)(CN)]⁻

Peng

Barabanschikov

et al. 2012

Inorg. Chem.

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The low-frequency vibrational characterization of the spin crossover complex, five-coordinate cyano(tetraphenylporpyrinato)iron(II), [Fe(TPP)(CN)]−, is reported. Nuclear resonance vibrational spectroscopy has been used to measure all low-frequency vibrations involving iron at several temperatures; this yields vibrational spectra of both the low- (S = 0) and high-spin (S = 2) states. Multi-temperature oriented single-crystal measurements facilitate assignments of the vibrational character of all modes and are consistent with the DFT-predicted spectra. The availability of the entire iron vibrational spectrum allows for the complete correlation of the modes between the two spin states. These data demonstrate that not only do the frequencies of the vibrations shift to lower values for the high-spin species as would be expected owing to the weaker bonds in the high-spin state but that the mixing of iron modes with ligand modes changes substantially. Diagrams illustrating the changing character of the modes and their correlation is given. The reduced iron-ligand frequencies are the primary factor in the entropic stabilization of the high-spin state responsible for the spin crossover.

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Investigations of Low-Frequency Vibrational Dynamics and Ligand Binding Kinetics of Cystathionine β-Synthase

Cited by 17 publications

References 71 publications

Heme-protein vibrational couplings in cytochrome c provide a dynamic link that connects the heme-iron and the protein surface

Heme-protein vibrational couplings in cytochrome c provide a dynamic link that connects the heme-iron and the protein surface

Ultrafast CO Kinetics in Heme Proteins: Adiabatic Ligand Binding and Heavy Atom Tunneling

Vibrational Probes and Determinants of the S = 0 ⇌ S = 2 Spin Crossover in Five-Coordinate [Fe(TPP)(CN)]⁻

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Investigations of Low-Frequency Vibrational Dynamics and Ligand Binding Kinetics of Cystathionine β-Synthase

Cited by 17 publications

References 71 publications

Heme-protein vibrational couplings in cytochrome c provide a dynamic link that connects the heme-iron and the protein surface

Heme-protein vibrational couplings in cytochrome c provide a dynamic link that connects the heme-iron and the protein surface

Ultrafast CO Kinetics in Heme Proteins: Adiabatic Ligand Binding and Heavy Atom Tunneling

Vibrational Probes and Determinants of the S = 0 ⇌ S = 2 Spin Crossover in Five-Coordinate [Fe(TPP)(CN)]−

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Vibrational Probes and Determinants of the S = 0 ⇌ S = 2 Spin Crossover in Five-Coordinate [Fe(TPP)(CN)]⁻