Sub‐picosecond Raman spectrometer for time‐resolved studies of structural dynamics in heme proteins

Kruglik, Sergei G.; Lambry, Jean−Christophe; Martin, Jean−Louis; Vos, Marten H.; Négrerie, Michel

doi:10.1002/jrs.2685

Cited by 25 publications

(34 citation statements)

References 62 publications

(58 reference statements)

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“…The TR 3 apparatus has 0.7-ps temporal resolution and 25-cm −1 spectral resolution (28,46,47). The broad band photolysis pulse (560-570 nm; 2 μJ; 100 fs) is delayed and collinearly superimposed to the probe beam (435 nm; 25 cm −1 ; 25 nJ).…”

Section: Methodsmentioning

confidence: 99%

Picosecond primary structural transition of the heme is retarded after nitric oxide binding to heme proteins

Kruglik

Yoo

Franzen

et al. 2010

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

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121

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We investigated the ultrafast structural transitions of the heme induced by nitric oxide (NO) binding for several heme proteins by subpicosecond time-resolved resonance Raman and femtosecond transient absorption spectroscopy. We probed the heme iron motion by the evolution of the iron-histidine Raman band intensity after NO photolysis. Unexpectedly, we found that the heme response and iron motion do not follow the kinetics of NO rebinding. Whereas NO dissociation induces quasi-instantaneous iron motion and heme doming (<0.6 ps), the reverse process results in a much slower picosecond movement of the iron toward the planar heme configuration after NO binding. The time constant for this primary domed-to-planar heme transition varies among proteins (∼30 ps for myoglobin and its H64V mutant, ∼15 ps for hemoglobin, ∼7 ps for dehaloperoxidase, and ∼6 ps for cytochrome c) and depends upon constraints exerted by the protein structure on the heme cofactor. This observed phenomenon constitutes the primary structural transition in heme proteins induced by NO binding.time-resolved Raman spectroscopy | allostery | structural dynamics T he role of diatomics endogenously generated in cells as messengers in various signaling pathways has been demonstrated for nitric oxide (NO) (1, 2) and carbon monoxide (CO) (3, 4) and various gas-sensors heme proteins have been discovered in the last two decades (5). In these signaling pathways, the binding of diatomics to their respective heme sensor domain triggers a response of the associated enzymatic domain by modulating the catalytic or the gene regulating activity (5). Recently, myoglobin (Mb) was proposed to be involved in the regulation of NO level (6), and neuroglobin was proposed as a sensor regulating the NO∕O 2 balance (7). Similarly to Hb (8-10), the signaling mechanisms are based at the molecular level on an allosteric structural change of the receptor/sensor protein coupled to a change of activity or affinity and are induced by diatomic ligation to the heme iron cofactor. The signal of diatomic binding/release can be transmitted to the overall protein structure either by in-plane/out-of-plane motion of the iron through the bound proximal histidine or by the cleavage of the iron-histidine (Fe-His) bond. In particular, for Hb and its monomeric counterpart Mb, the out-of-plane iron motion occurs in less than 1 ps after gaseous ligand release (11,12) and represents the first event of the allosteric R → T transition (9). This primary heme iron motion is followed by overall tertiary changes, notably motion of α-helices (13). Upon gaseous ligand binding, the reverse T → R allosteric transition is coupled to the iron motion toward the heme plane, and this primary motion is also considered quasi-instantaneous since the stereochemical description of Hb allostery by Perutz (9, 10) although up to now it has never been observed.The ultrafast events in the interaction of heme proteins with various gaseous ligands were studied extensively at molecular level in the last two decades by femtosec...

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Section: Methodsmentioning

confidence: 99%

Picosecond primary structural transition of the heme is retarded after nitric oxide binding to heme proteins

Kruglik

Yoo

Franzen

et al. 2010

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

Self Cite

121

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“…The corresponding energy relaxation processes have been extensively studied with a variety of ultrafast techniques, such as time-resolved infrared 7 and visible [8][9][10] absorption, as well as by Impulsive Raman 11 and Coherent Emission Interferometry 12 . Using Time-Resolved Resonance Raman (TR 3 ) and Transient Raman Resonance Spectroscopy (TRRS), heme cooling has been observed on the timescales of a few picoseconds by looking at either vibrational shift [13][14][15] or the Stokes/Antistokes ratio 2,16,17 of the totally symmetric in-plane breathing modes with large cross section (ν 4 and ν 7 )…”

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confidence: 99%

Direct observation of subpicosecond vibrational dynamics in photoexcited myoglobin

et al. 2016

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“…The position of the GS bands was set to the values determined by the fit of the static spectrum. The width was allowed to be broader to account for some excess of vibrational energy on the haem, which is expected to dissipate on timescales >1 ps, 26,27 but the ratio between the respective areas was kept unchanged. The fits are shown in Figure 6 of the supplementary material.…”

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A cascade through spin states in the ultrafast haem relaxation of met-myoglobin

Consani

Auböck

Bräm

et al. 2014

The Journal of Chemical Physics

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We report on a study of the early relaxation processes of met-Myoglobin in aqueous solution, using a combination of ultrafast broadband fluorescence detection and transient absorption with a broad UV-visible continuum probe at different pump energies. Reconstruction of the spectra of the transient species unravels the details of the haem photocycle in the absence of photolysis. Besides identifying a branching in the ultrafast relaxation of the haem, we show clear evidence for an electronic character of the intermediates, contrary to the commonly accepted idea that the early time relaxation of the haem is only due to cooling. The decay back to the ground state proceeds partially as a cascade through iron spin states, which seems to be a general characteristic of haem systems.

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Sub‐picosecond Raman spectrometer for time‐resolved studies of structural dynamics in heme proteins

Cited by 25 publications

References 62 publications

Picosecond primary structural transition of the heme is retarded after nitric oxide binding to heme proteins

Picosecond primary structural transition of the heme is retarded after nitric oxide binding to heme proteins

Direct observation of subpicosecond vibrational dynamics in photoexcited myoglobin

A cascade through spin states in the ultrafast haem relaxation of met-myoglobin

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