Subpicosecond oxygen trapping in the heme pocket of the oxygen sensor FixL observed by time-resolved resonance Raman spectroscopy

Kruglik, Sergei G.; Jasaitis, Audrius; Holá, Klára; Yamashita, Takahiro; Liebl, Ursula; Martin, Jean−Louis; Vos, Marten H.

doi:10.1073/pnas.0700445104

Cited by 32 publications

(46 citation statements)

References 45 publications

(88 reference statements)

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“…The tight distal heme pocket also precludes the activation of CooA by potential bulky ligands, such as imidazole (43). The formation of a tight trap for the functional ligand, which guarantees its fast geminate recombination with very high efficiency, is also seen in other heme-based sensor proteins, such as FixL (42). NP4 (21,44), a nitric oxide carrier protein, also forms a hydrophobic trap around NO in the low pH environment of the saliva in the blood feeding insect Rhodnius prolixus.…”

Section: Dna Binding Reduces Structural Heterogeneity In Hemebinding mentioning

confidence: 98%

“…In heme proteins, where O 2 is the functional ligand, the distal pocket is more polar, and the oxy complex is stabilized by hydrogen bonding of O 2 to nearby polar residues. For example, O 2 forms a stable complex by hydrogen bonding to His-64 in myoglobin (41) and to Arg-220 in FixL (42). The tight distal heme pocket also precludes the activation of CooA by potential bulky ligands, such as imidazole (43).…”

Section: Dna Binding Reduces Structural Heterogeneity In Hemebinding mentioning

confidence: 99%

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Effect of DNA Binding on Geminate CO Recombination Kinetics in CO-sensing Transcription Factor CooA

Benabbas

Karunakaran

Youn

et al. 2012

Journal of Biological Chemistry

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Background: CooA proteins are CO-sensing transcription factors. Results: DNA binding to CooA-CO speeds up geminate rebinding of CO. Conclusion: DNA binding reduces heme heterogeneity and CO rebinding barrier. This along with distal pocket trapping maintains the "on" state long enough for transcription to take place. Significance: This work provides a deeper understanding of the allosteric transition in CooA proteins.

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Section: Dna Binding Reduces Structural Heterogeneity In Hemebinding mentioning

confidence: 98%

Section: Dna Binding Reduces Structural Heterogeneity In Hemebinding mentioning

confidence: 99%

Effect of DNA Binding on Geminate CO Recombination Kinetics in CO-sensing Transcription Factor CooA

Benabbas

Karunakaran

Youn

et al. 2012

Journal of Biological Chemistry

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“…3 spectroscopy has been successfully used to characterize photodissociated heme-CO complexes in various heme proteins (19,(25)(26)(27)(28). It provides information about dynamic structures in the heme and its pocket.…”

Section: Time-resolved Resonance Raman Investigations Of Wt Ec Dosh-trmentioning

confidence: 99%

Roles of Arg-97 and Phe-113 in Regulation of Distal Ligand Binding to Heme in the Sensor Domain of Ec DOS Protein

El-Mashtoly

Nakashima²,

Tanaka

et al. 2008

Journal of Biological Chemistry

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The direct oxygen sensor protein isolated from Escherichia coli (Ec DOS) is a heme-based signal transducer protein responsible for phosphodiesterase (PDE) activity. Binding of O 2 , CO, or NO to a reduced heme significantly enhances the PDE activity toward 3,5-cyclic diguanylic acid. We report stationary and time-resolved resonance Raman spectra of the wild-type and several mutants (Glu-93 3 Ile, Met-95 3 Ala, Arg-97 3 Ile, Arg-97 3 Ala, Arg-97 3 Glu, Phe-113 3 Leu, and Phe-113 3 Thr) of the heme-containing PAS domain of Ec DOS. For the CO-and NO-bound forms, both the hydrogen-bonded and nonhydrogen-bonded conformations were found, and in the former Heme-based sensors are a class of enzymes that regulates the enzymatic activities and DNA binding in response to the presence of diatomic gas molecules CO, NO, or O 2 (1-6). The direct oxygen sensor from Escherichia coli (Ec DOS) 4 is a hemebased signal transducer protein responsible for phosphodiesterase (PDE) activity (7,8). The Ec DOS is composed of a C-terminal PDE catalytic domain and the N-terminal hemecontaining domain. The latter is a prototypical PAS domain, which is a ubiquitous protein sensory domain found in all kingdoms (9), and has a conserved ␣/␤ folds consisting of ϳ147 residues (10, 11). The Ec DOS protein has a PDE activity specific to 3Ј,5Ј-cyclic diguanylic acid (12, 13), and the binding of O 2 , CO, or NO to the reduced heme significantly enhances the PDE activity (14, 15). Thus, Ec DOS is a novel gas-sensor enzyme that has unprecedented ability to be activated by different gas molecules. Because the CO and NO concentrations in the cells are very low (nanomolar), it is likely that Ec DOS is predominantly an oxygen sensor enzyme whereby catalysis is regulated in response to the micromolar O 2 level (16). It is believed that the structural changes in the heme vicinity caused by ligand binding to the heme provide the initial event in the gas sensing, followed by intramolecular signal transduction from the heme to the functional domain, and thus regulating the PDE activity. Fig. 1 illustrates the crystal structure of the truncated heme sensor domain (Ec DOSH) of Ec DOS protein (10). In the reduced form (Fig. 1A), Met-95 and His-77 are the heme axial ligands in the distal and proximal sides, respectively, and Met-95 forms a hydrogen bond with heme 7-propionate. Upon O 2 binding to the reduced heme, Met-95 is replaced by O 2 and heme 7-propionate forms a hydrogen bond with Arg-97 instead of Met-95. This stabilizes the heme-coordinated O 2 (Fig. 1B). Thus, the replacement of a distal axial ligand from Met-95 to O 2 perturbs the heme 7-propionate hydrogen bonding network, resulting in large conformational changes in the FG loop (10). On the other hand, the role of other distal residues (Fig. 1) and the heme 7-propionate hydrogen bonding network are not clear in the CO-or NO-sensing mechanism.To understand the gas-sensing mechanism of Ec DOS, it is essential to determine the changes in the heme and surrounding structures caused by distal ligand binding/di...

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“…At the same time, the binding of a diatomic and subsequent T → R transition have not yet been studied by a time-resolved technique sensitive to heme structural changes. The first event following gaseous ligand binding, namely, the transition from domed-to-planar heme, is believed to occur in less than 0.6 ps, by analogy with the well-studied heme response to ligand release (11,12,24,25), although the structural constraints and energy barriers for these two opposite processes are not necessarily the same. We investigated the primary event related to the T → R transition by subpicosecond TR 3 and report the observation of the in-plane movement of the ferrous heme iron induced by NO geminate rebinding, following a femtosecond photodissociating laser pulse.…”

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confidence: 99%

“…Our approach is based on the findings that (i) the transition from planar to domed heme structure induces a change in Raman intensity of the low-frequency ν Fe-His stretching band (19,26) located within the range 200-240 cm −1 ; (ii) the intensity of ν Fe-His resonantly excited within the Soret absorption band depends on the out-of-plane position of the iron with respect to the heme macrocycle plane (27) and is zero for the in-plane iron position. For this study, we have employed a specially designed home-built subpicosecond TR 3 spectrometer having ∼0.7-ps temporal and ∼25-cm −1 spectral resolution (24,28,29), probing structural changes in the time range not yet accessible to TRXD.…”

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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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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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Subpicosecond oxygen trapping in the heme pocket of the oxygen sensor FixL observed by time-resolved resonance Raman spectroscopy

Cited by 32 publications

References 45 publications

Effect of DNA Binding on Geminate CO Recombination Kinetics in CO-sensing Transcription Factor CooA

Effect of DNA Binding on Geminate CO Recombination Kinetics in CO-sensing Transcription Factor CooA

Roles of Arg-97 and Phe-113 in Regulation of Distal Ligand Binding to Heme in the Sensor Domain of Ec DOS Protein

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

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