Molecular dynamics of the primary photochemical event in rhodopsin

Tallent, Jack R.; Hyde, Elaine W.; Findsen, Leonore A.; Fox, Geoffrey; Birge, Robert R.

doi:10.1021/ja00031a007

Cited by 71 publications

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“…Torsional strain along the ethylenic chain has been previously proposed as a mechanism for energy storage in the Batho chromophore (12)(13)(14). Since the first crystal structure of rhodopsin was published in 2000 (32), a number of molecular dynamics calculations have been performed to model the Batho structure (64-66).…”

Section: Discussionmentioning

confidence: 99%

“…The transduction of this torsional energy presumably drives the movements of E2 through the steric interactions at the 9-and 13-methyl groups, as well as the movement of H3 through the electrostatic interaction of Glu113 (on H3) with the PSB. The induced E2 and H3 movements coordinated by the functionally important disulfide bond (63) may further couple to the hydrogen-bond network in the binding pocking that conducts the counterion switch process (19).Torsional strain along the ethylenic chain has been previously proposed as a mechanism for energy storage in the Batho chromophore (12)(13)(14). Since the first crystal structure of rhodopsin was published in 2000 (32), a number of molecular dynamics calculations have been performed to model the Batho structure (64-66).…”

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confidence: 99%

“…However, the C 11 =C 12 HOOP modes of the Batho chromophore are unexpectedly decoupled producing a nearly isolated C 11 H wag at 920 cm -1 and C 12 H wag at 858 cm -1 . Since this assignment was achieved, the origin of this key structural observation about the structure of the Batho chromophore has remained unresolved despite a wide variety of theoretical models and experimental studies (1,13,(29)(30)(31).…”

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confidence: 99%

“…Rho is a paradigmatic G protein-coupled receptor, whose 7-transmembrane helical structure forms a binding pocket for 11-cis-retinal, which is covalently linked to Lys296 on helix 7. Within 200 fs after photoexcitation (8,9), the 11-cis-retinal protonated Schiff base (PSB) isomerizes to all-trans-retinal (ATR) with a quantum yield of 0.65 to form the primary photoproduct, Bathorhodopsin (10,11), which stores ∼30 kcal/mol or ∼60% of the incident photon energy (Figure 1) (12)(13)(14). Subsequently, the highly distorted chromophore relaxes, and the transduced energy is used to drive conformational changes in the opsin protein (15)(16)(17)(18).…”

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confidence: 99%

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Resonance Raman Analysis of the Mechanism of Energy Storage and Chromophore Distortion in the Primary Visual Photoproduct

et al. 2004

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The vibrational structure of the chromophore in the primary photoproduct of vision, bathorhodopsin, is examined to determine the cause of the anomalously decoupled and intense C 11 =C 12 hydrogenout-of-plane (HOOP) wagging modes and their relation to energy storage in the primary photoproduct. Low-temperature (77 K) resonance Raman spectra of Glu181 and Ser186 mutants of bovine rhodopsin reveal only mild mutagenic perturbations of the photoproduct spectrum suggesting that dipolar, electrostatic, or steric interactions with these residues do ded by NIHnot cause the HOOP mode frequencies and intensities. Density functional theory calculations are performed to investigate the effect of geometric distortion on the HOOP coupling. The decoupled HOOP modes can be simulated by imposing ∼40° twists in the same direction about the C 11 =C 12 and C 12 -C 13 bonds. Sequence comparison and examination of the binding site suggests that these distortions are caused by three constraints consisting of an electrostatic anchor between the protonated Schiff base and the Glu113 counterion, as well as steric interactions of the 9-and 13-methyl groups with surrounding residues. This distortion stores light energy that is used to drive the subsequent protein conformational changes that activate rhodopsin.Photoactive proteins play a vital role in a variety of light-energy and light-signaling processes that are characterized by pico-to femtosecond light-driven structural changes of a proteinbound chromophore followed by activated conformational changes of the protein. In systems such as rhodopsin (Rho) 1 (1), bacteriorhodopsin (2,3), halorhodopsin (4), photoactive yellow protein (5), and phytochrome (6,7), primary high-energy intermediates are produced with structurally perturbed chromophores. What is the nature of the protein-chromophore interactions that store the energy needed to drive subsequent protein conformational changes? To address this question, we have studied the photoactivation of rhodopsin, a dim-light photoreceptor, using a multidisciplinary approach that integrates Raman spectroscopy, mutagenesis, density functional theory (DFT) calculations, and bioinformatic analysis. † Funding was provided by NIH Grant EY02051 (to R.A.M. Rho is a paradigmatic G protein-coupled receptor, whose 7-transmembrane helical structure forms a binding pocket for 11-cis-retinal, which is covalently linked to Lys296 on helix 7. Within 200 fs after photoexcitation (8,9), the 11-cis-retinal protonated Schiff base (PSB) isomerizes to all-trans-retinal (ATR) with a quantum yield of 0.65 to form the primary photoproduct, Bathorhodopsin (10,11), which stores ∼30 kcal/mol or ∼60% of the incident photon energy (Figure 1) (12)(13)(14). Subsequently, the highly distorted chromophore relaxes, and the transduced energy is used to drive conformational changes in the opsin protein (15)(16)(17)(18). Recently, we found that this structural evolution includes a retinal counterion switch from Glu113 in the dark state to Glu181 in the metarhodopsin I (Met...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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confidence: 99%

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Resonance Raman Analysis of the Mechanism of Energy Storage and Chromophore Distortion in the Primary Visual Photoproduct

et al. 2004

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“…Two-photon spectroscopy indicates that the binding site of rhodopsin is neutral (Birge, Murray, Zidovetzki and Knapp, 1987), and consequently there is a negatively charged counter ion in the vicinity of the chromophore. There is evidence that the primary counter ion of the Schiff base is Glu-113 (Zhukovski and Oprian, 1989) Also, one or more water molecules are present within the rhodopsin binding site, and the high C = N stretching frequency and large ND isotope shift indicate that the Schiff base is strongly hydrogen bonded (RodmanGilson, and Honig, 1988), possibly to water in the binding site (Cossette and Vocelle, 1987;Tallent, Hyde, Findsen, Fox et al, 1992). A possible model of the rhodopsin binding site that is consistent with available experimental data, and which we call the minimal 11-cis-retinal PSB complex, is shown in Fig.…”

Section: Simulation Of the 11-cis-retinal Chromophorementioning

confidence: 99%

A First-Principles Study of 11-Cis-Retinal: Modelling the Chromophore-Protein Interaction In Rhodopsin

Sugihara¹,

Entel²,

Buß

2002

Phase Transitions

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The 11-cis-retinal protonated Schiff base is the chromophore of rhodopsin, the photoreceptor in the vertebrate eye. The photochemical isomerization from 11-cis to the all-trans form triggers a series of enzymatic reactions known as the visual cascade which eventually leads to a neural signal. Experiments such as resonance Raman, NMR etc., have shown that 11-cis-retinal is probably highly twisted in the protein pocket. Because detailed knowledge about the kind of interaction with the protein is missing, a theoretical description of the chromophore conformation is difficult. In the simulations the results of which will be presented here, we assume that the retinal chromophore, as a consequence of the steric fit into the protein binding pocket, undergoes a specific kind of conformational change. The structure we obtain is in good agreement with the experimentally observed highly twisted conformation of the chromophore backbone.

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Interconversion pathways of the protonated ?-ionone Schiff base: An ab initio molecular dynamics study

Terstegen¹,

Carter

Buß³

1999

Int. J. Quant. Chem.

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Ab initio molecular dynamics at the RHFr3-21G level have been Ž . performed to study interconversion pathways bond rotation and ring inversion of the protonated ␤-ionone Schiff base. Starting with different stationary points on the Born᎐Oppenheimer potential energy surface, the trajectories are followed for 2100 fs. A perfunctory analysis of the reaction pathways reveals a dynamical behavior in agreement with classical expectations.

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Molecular dynamics of the primary photochemical event in rhodopsin

Cited by 71 publications

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Resonance Raman Analysis of the Mechanism of Energy Storage and Chromophore Distortion in the Primary Visual Photoproduct

Resonance Raman Analysis of the Mechanism of Energy Storage and Chromophore Distortion in the Primary Visual Photoproduct

A First-Principles Study of 11-Cis-Retinal: Modelling the Chromophore-Protein Interaction In Rhodopsin

Interconversion pathways of the protonated ?-ionone Schiff base: An ab initio molecular dynamics study

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