Retinal conformation and dynamics in activation of rhodopsin illuminated by solid-state 2H NMR spectroscopy

Michael F Brown, Karina Martínez-Mayorga, Koji Nakanishi, Gilmar F J Salgado, Andrey V. Struts

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

Solid-state NMR spectroscopy gives a powerful avenue for investigating G protein-coupled receptors and other integral membrane proteins in a native-like environment. This article reviews the use of solid-state 2H NMR to study the retinal cofactor of rhodopsin in the dark state as well as the meta I and meta II photointermediates. Site-specific 2H NMR labels have been introduced into three regions (methyl groups) of retinal that are crucially important for the photochemical function of rhodopsin. Despite its phenomenal stability 2H NMR spectroscopy indicates retinal undergoes rapid fluctuations within the protein binding cavity. The spectral lineshapes reveal the methyl groups spin rapidly about their three-fold (C3) axes with an order parameter for the off-axial motion of For the dark state, the 2H NMR structure of 11-cis-retinal manifests torsional twisting of both the polyene chain and the β-ionone ring due to steric interactions of the ligand and the protein. Retinal is accommodated within the rhodopsin binding pocket with a negative pretwist about the C11=C12 double bond. Conformational distortion explains its rapid photochemistry and reveals the trajectory of the 11-cis to trans isomerization. In addition, 2H NMR has been applied to study the retinylidene dynamics in the dark and light-activated states. Upon isomerization there are drastic changes in the mobility of all three methyl groups. The relaxation data support an activation mechanism whereby the β-ionone ring of retinal stays in nearly the same environment, without a large displacement of the ligand. Interactions of the β-ionone ring and the retinylidene Schiff base with the protein transmit the force of the retinal isomerization. Solid-state 2H NMR thus provides information about the flow of energy that triggers changes in hydrogen-bonding networks and helix movements in the activation mechanism of the photoreceptor.

Original languageEnglish (US)
Pages (from-to)442-453
Number of pages12
JournalPhotochemistry and Photobiology
Volume85
Issue number2
DOIs
StatePublished - Mar 2009

Fingerprint

Norisoprenoids
Rhodopsin
Retinaldehyde
Nuclear magnetic resonance spectroscopy
Conformations
Magnetic Resonance Spectroscopy
Chemical activation
Nuclear magnetic resonance
activation
solid state
Isomerization
nuclear magnetic resonance
proteins
spectroscopy
Ligands
Polyenes
Photochemistry
isomerization
Schiff Bases
Hydrogen Bonding

ASJC Scopus subject areas

  • Physical and Theoretical Chemistry
  • Biochemistry
  • Medicine(all)

Cite this

Retinal conformation and dynamics in activation of rhodopsin illuminated by solid-state 2H NMR spectroscopy. / Brown, Michael F; Martínez-Mayorga, Karina; Nakanishi, Koji; Salgado, Gilmar F J; Struts, Andrey V.

In: Photochemistry and Photobiology, Vol. 85, No. 2, 03.2009, p. 442-453.

Research output: Contribution to journalArticle

Brown, Michael F ; Martínez-Mayorga, Karina ; Nakanishi, Koji ; Salgado, Gilmar F J ; Struts, Andrey V. / Retinal conformation and dynamics in activation of rhodopsin illuminated by solid-state 2H NMR spectroscopy. In: Photochemistry and Photobiology. 2009 ; Vol. 85, No. 2. pp. 442-453.
@article{3e0ebe1d4c8445299e6ba6e2d5ffb246,
title = "Retinal conformation and dynamics in activation of rhodopsin illuminated by solid-state 2H NMR spectroscopy",
abstract = "Solid-state NMR spectroscopy gives a powerful avenue for investigating G protein-coupled receptors and other integral membrane proteins in a native-like environment. This article reviews the use of solid-state 2H NMR to study the retinal cofactor of rhodopsin in the dark state as well as the meta I and meta II photointermediates. Site-specific 2H NMR labels have been introduced into three regions (methyl groups) of retinal that are crucially important for the photochemical function of rhodopsin. Despite its phenomenal stability 2H NMR spectroscopy indicates retinal undergoes rapid fluctuations within the protein binding cavity. The spectral lineshapes reveal the methyl groups spin rapidly about their three-fold (C3) axes with an order parameter for the off-axial motion of For the dark state, the 2H NMR structure of 11-cis-retinal manifests torsional twisting of both the polyene chain and the β-ionone ring due to steric interactions of the ligand and the protein. Retinal is accommodated within the rhodopsin binding pocket with a negative pretwist about the C11=C12 double bond. Conformational distortion explains its rapid photochemistry and reveals the trajectory of the 11-cis to trans isomerization. In addition, 2H NMR has been applied to study the retinylidene dynamics in the dark and light-activated states. Upon isomerization there are drastic changes in the mobility of all three methyl groups. The relaxation data support an activation mechanism whereby the β-ionone ring of retinal stays in nearly the same environment, without a large displacement of the ligand. Interactions of the β-ionone ring and the retinylidene Schiff base with the protein transmit the force of the retinal isomerization. Solid-state 2H NMR thus provides information about the flow of energy that triggers changes in hydrogen-bonding networks and helix movements in the activation mechanism of the photoreceptor.",
author = "Brown, {Michael F} and Karina Mart{\'i}nez-Mayorga and Koji Nakanishi and Salgado, {Gilmar F J} and Struts, {Andrey V.}",
year = "2009",
month = "3",
doi = "10.1111/j.1751-1097.2008.00510.x",
language = "English (US)",
volume = "85",
pages = "442--453",
journal = "Photochemistry and Photobiology",
issn = "0031-8655",
publisher = "Wiley-Blackwell",
number = "2",

}

TY - JOUR

T1 - Retinal conformation and dynamics in activation of rhodopsin illuminated by solid-state 2H NMR spectroscopy

AU - Brown, Michael F

AU - Martínez-Mayorga, Karina

AU - Nakanishi, Koji

AU - Salgado, Gilmar F J

AU - Struts, Andrey V.

PY - 2009/3

Y1 - 2009/3

N2 - Solid-state NMR spectroscopy gives a powerful avenue for investigating G protein-coupled receptors and other integral membrane proteins in a native-like environment. This article reviews the use of solid-state 2H NMR to study the retinal cofactor of rhodopsin in the dark state as well as the meta I and meta II photointermediates. Site-specific 2H NMR labels have been introduced into three regions (methyl groups) of retinal that are crucially important for the photochemical function of rhodopsin. Despite its phenomenal stability 2H NMR spectroscopy indicates retinal undergoes rapid fluctuations within the protein binding cavity. The spectral lineshapes reveal the methyl groups spin rapidly about their three-fold (C3) axes with an order parameter for the off-axial motion of For the dark state, the 2H NMR structure of 11-cis-retinal manifests torsional twisting of both the polyene chain and the β-ionone ring due to steric interactions of the ligand and the protein. Retinal is accommodated within the rhodopsin binding pocket with a negative pretwist about the C11=C12 double bond. Conformational distortion explains its rapid photochemistry and reveals the trajectory of the 11-cis to trans isomerization. In addition, 2H NMR has been applied to study the retinylidene dynamics in the dark and light-activated states. Upon isomerization there are drastic changes in the mobility of all three methyl groups. The relaxation data support an activation mechanism whereby the β-ionone ring of retinal stays in nearly the same environment, without a large displacement of the ligand. Interactions of the β-ionone ring and the retinylidene Schiff base with the protein transmit the force of the retinal isomerization. Solid-state 2H NMR thus provides information about the flow of energy that triggers changes in hydrogen-bonding networks and helix movements in the activation mechanism of the photoreceptor.

AB - Solid-state NMR spectroscopy gives a powerful avenue for investigating G protein-coupled receptors and other integral membrane proteins in a native-like environment. This article reviews the use of solid-state 2H NMR to study the retinal cofactor of rhodopsin in the dark state as well as the meta I and meta II photointermediates. Site-specific 2H NMR labels have been introduced into three regions (methyl groups) of retinal that are crucially important for the photochemical function of rhodopsin. Despite its phenomenal stability 2H NMR spectroscopy indicates retinal undergoes rapid fluctuations within the protein binding cavity. The spectral lineshapes reveal the methyl groups spin rapidly about their three-fold (C3) axes with an order parameter for the off-axial motion of For the dark state, the 2H NMR structure of 11-cis-retinal manifests torsional twisting of both the polyene chain and the β-ionone ring due to steric interactions of the ligand and the protein. Retinal is accommodated within the rhodopsin binding pocket with a negative pretwist about the C11=C12 double bond. Conformational distortion explains its rapid photochemistry and reveals the trajectory of the 11-cis to trans isomerization. In addition, 2H NMR has been applied to study the retinylidene dynamics in the dark and light-activated states. Upon isomerization there are drastic changes in the mobility of all three methyl groups. The relaxation data support an activation mechanism whereby the β-ionone ring of retinal stays in nearly the same environment, without a large displacement of the ligand. Interactions of the β-ionone ring and the retinylidene Schiff base with the protein transmit the force of the retinal isomerization. Solid-state 2H NMR thus provides information about the flow of energy that triggers changes in hydrogen-bonding networks and helix movements in the activation mechanism of the photoreceptor.

UR - http://www.scopus.com/inward/record.url?scp=60849085720&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=60849085720&partnerID=8YFLogxK

U2 - 10.1111/j.1751-1097.2008.00510.x

DO - 10.1111/j.1751-1097.2008.00510.x

M3 - Article

C2 - 19267870

AN - SCOPUS:60849085720

VL - 85

SP - 442

EP - 453

JO - Photochemistry and Photobiology

JF - Photochemistry and Photobiology

SN - 0031-8655

IS - 2

ER -