Ultrafast structural changes direct the first molecular events of vision

Thomas Gruhl, Tobias Weinert, Matthew J. Rodrigues, Christopher J. Milne, Giorgia Ortolani, Karol Nass, Eriko Nango, Saumik Sen, Philip J. M. Johnson, Claudio Cirelli, Antonia Furrer, Sandra Mous, Petr Skopintsev, Daniel James, Florian Dworkowski, Petra Båth, Demet Kekilli, Dmitry Ozerov, Rie Tanaka, Hannah Glover, Camila Bacellar, Steffen Brünle, Cecilia M. Casadei, Azeglio D. Diethelm, Dardan Gashi, Guillaume Gotthard, Ramon Guixà-González, Yasumasa Joti, Victoria Kabanova, Gregor Knopp, Elena Lesca, Pikyee Ma, Isabelle Martiel, Jonas Mühle, Shigeki Owada, Filip Pamula, Daniel Sarabi, Oliver Tejero, Ching-Ju Tsai, Niranjan Varma, Anna Wach, Sébastien Boutet, Kensuke Tono, Przemyslaw Nogly, Xavier Deupi, So Iwata, Richard Neutze, Jörg Standfuss, Gebhard Schertler () and Valerie Panneels ()
Additional contact information
Thomas Gruhl: Paul Scherrer Institute
Tobias Weinert: Paul Scherrer Institute
Matthew J. Rodrigues: Paul Scherrer Institute
Christopher J. Milne: Paul Scherrer Institute
Giorgia Ortolani: University of Gothenburg
Karol Nass: Paul Scherrer Institute
Eriko Nango: Tohoku University
Saumik Sen: Paul Scherrer Institute
Philip J. M. Johnson: Paul Scherrer Institute
Claudio Cirelli: Paul Scherrer Institute
Antonia Furrer: Paul Scherrer Institute
Sandra Mous: ETH Zurich
Petr Skopintsev: Paul Scherrer Institute
Daniel James: Paul Scherrer Institute
Florian Dworkowski: Paul Scherrer Institute
Petra Båth: University of Gothenburg
Demet Kekilli: Paul Scherrer Institute
Dmitry Ozerov: Paul Scherrer Institute
Rie Tanaka: RIKEN SPring-8 Center
Hannah Glover: Paul Scherrer Institute
Camila Bacellar: Paul Scherrer Institute
Steffen Brünle: Paul Scherrer Institute
Cecilia M. Casadei: ETH Zurich
Azeglio D. Diethelm: Paul Scherrer Institute
Dardan Gashi: Paul Scherrer Institute
Guillaume Gotthard: Paul Scherrer Institute
Ramon Guixà-González: Paul Scherrer Institute
Yasumasa Joti: Japan Synchrotron Radiation Research Institute
Victoria Kabanova: Paul Scherrer Institute
Gregor Knopp: Paul Scherrer Institute
Elena Lesca: ETH Zurich
Pikyee Ma: Paul Scherrer Institute
Isabelle Martiel: Paul Scherrer Institute
Jonas Mühle: Paul Scherrer Institute
Shigeki Owada: RIKEN SPring-8 Center
Filip Pamula: Paul Scherrer Institute
Daniel Sarabi: University of Gothenburg
Oliver Tejero: Paul Scherrer Institute
Ching-Ju Tsai: Paul Scherrer Institute
Niranjan Varma: Paul Scherrer Institute
Anna Wach: Institute of Nuclear Physics Polish Academy of Sciences
Sébastien Boutet: SLAC National Accelerator Laboratory
Kensuke Tono: Japan Synchrotron Radiation Research Institute
Przemyslaw Nogly: ETH Zurich
Xavier Deupi: Paul Scherrer Institute
So Iwata: RIKEN SPring-8 Center
Richard Neutze: University of Gothenburg
Jörg Standfuss: Paul Scherrer Institute
Gebhard Schertler: Paul Scherrer Institute
Valerie Panneels: Paul Scherrer Institute

Nature, 2023, vol. 615, issue 7954, 939-944

Abstract: Abstract Vision is initiated by the rhodopsin family of light-sensitive G protein-coupled receptors (GPCRs)1. A photon is absorbed by the 11-cis retinal chromophore of rhodopsin, which isomerizes within 200 femtoseconds to the all-trans conformation2, thereby initiating the cellular signal transduction processes that ultimately lead to vision. However, the intramolecular mechanism by which the photoactivated retinal induces the activation events inside rhodopsin remains experimentally unclear. Here we use ultrafast time-resolved crystallography at room temperature3 to determine how an isomerized twisted all-trans retinal stores the photon energy that is required to initiate the protein conformational changes associated with the formation of the G protein-binding signalling state. The distorted retinal at a 1-ps time delay after photoactivation has pulled away from half of its numerous interactions with its binding pocket, and the excess of the photon energy is released through an anisotropic protein breathing motion in the direction of the extracellular space. Notably, the very early structural motions in the protein side chains of rhodopsin appear in regions that are involved in later stages of the conserved class A GPCR activation mechanism. Our study sheds light on the earliest stages of vision in vertebrates and points to fundamental aspects of the molecular mechanisms of agonist-mediated GPCR activation.

Date: 2023
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DOI: 10.1038/s41586-023-05863-6

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