Deuterium NMR structure of retinal in the ground state of rhodopsin

Gilmar F J Salgado, Andrey V. Struts, Katsunori Tanaka, Naoko Fujioka, Koji Nakanishi, Michael F Brown

Research output: Contribution to journalArticle

57 Citations (Scopus)

Abstract

The conformation of retinal bound to the G protein-coupled receptor rhodopsin is intimately linked to its photochemistry, which initiates the visual process. Site-directed deuterium (2H) NMR spectroscopy was used to investigate the structure of retinal within the binding pocket of bovine rhodopsin. Aligned recombinant membranes were studied containing rhodopsin that was regenerated with retinal 2H-labeled at the C5, C 9, or C13 methyl groups by total synthesis. Studies were conducted at temperatures below the gel to liquid-crystalline phase transition of the membrane lipid bilayer, where rotational and translational diffusion of rhodopsin is effectively quenched. The experimental tilt series of 2H NMR spectra were fit to a theoretical line shape analysis [Nevzorov, A. A., Moltke, S., Heyn, M. P., and Brown, M. F. (1999) J. Am. Chem. Soc. 121, 7636-7643] giving the retinylidene bond orientations with respect to the membrane normal in the dark state. Moreover, the relative orientations of pairs of methyl groups were used to calculate effective torsional angles between different planes of unsaturation of the retinal chromophore. Our results are consistent with significant conformational distortion of retinal, and they have important implications for quantum mechanical calculations of its electronic spectral properties. In particular, we find that the β-ionone ring has a twisted 6-s-cis conformation, whereas the polyene chain is twisted 12-s-trans. The conformational strain of retinal as revealed by solid-state 2H NMR is significant for explaining the quantum yields and mechanism of its ultrafast photoisomerization in visual pigments. This work provides a consensus view of the retinal conformation in rhodopsin as seen by X-ray diffraction, solid-state NMR spectroscopy, and quantum chemical calculations.

Original languageEnglish (US)
Pages (from-to)12819-12828
Number of pages10
JournalBiochemistry
Volume43
Issue number40
DOIs
StatePublished - Oct 12 2004

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Rhodopsin
Deuterium
Ground state
Nuclear magnetic resonance
Conformations
Nuclear magnetic resonance spectroscopy
Magnetic Resonance Spectroscopy
Norisoprenoids
Membranes
Polyenes
Photochemistry
Photoisomerization
Lipid bilayers
Retinal Pigments
Photochemical reactions
Phase Transition
Lipid Bilayers
Quantum yield
Chromophores
Membrane Lipids

ASJC Scopus subject areas

  • Biochemistry

Cite this

Salgado, G. F. J., Struts, A. V., Tanaka, K., Fujioka, N., Nakanishi, K., & Brown, M. F. (2004). Deuterium NMR structure of retinal in the ground state of rhodopsin. Biochemistry, 43(40), 12819-12828. https://doi.org/10.1021/bi0491191

Deuterium NMR structure of retinal in the ground state of rhodopsin. / Salgado, Gilmar F J; Struts, Andrey V.; Tanaka, Katsunori; Fujioka, Naoko; Nakanishi, Koji; Brown, Michael F.

In: Biochemistry, Vol. 43, No. 40, 12.10.2004, p. 12819-12828.

Research output: Contribution to journalArticle

Salgado, GFJ, Struts, AV, Tanaka, K, Fujioka, N, Nakanishi, K & Brown, MF 2004, 'Deuterium NMR structure of retinal in the ground state of rhodopsin', Biochemistry, vol. 43, no. 40, pp. 12819-12828. https://doi.org/10.1021/bi0491191
Salgado GFJ, Struts AV, Tanaka K, Fujioka N, Nakanishi K, Brown MF. Deuterium NMR structure of retinal in the ground state of rhodopsin. Biochemistry. 2004 Oct 12;43(40):12819-12828. https://doi.org/10.1021/bi0491191
Salgado, Gilmar F J ; Struts, Andrey V. ; Tanaka, Katsunori ; Fujioka, Naoko ; Nakanishi, Koji ; Brown, Michael F. / Deuterium NMR structure of retinal in the ground state of rhodopsin. In: Biochemistry. 2004 ; Vol. 43, No. 40. pp. 12819-12828.
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