Ultrafast structural changes direct the first molecular events of vision

Gruhl, Thomas; Weinert, Tobias; Rodrigues, Matthew J.; Milne, Christopher J.; Ortolani, Giorgia; Nass, Karol; Nango, Eriko; Sen, Saumik; Johnson, Philip M.; Cirelli, Claudio; Furrer, Antonia; Mous, Sandra; Skopintsev, Petr; James, Daniel; Dworkowski, Florian; Båth, Petra; Kekilli, Demet; Ozerov, Dmitry; Tanaka, Rie; Glover, Hannah; Bacellar, Camila; Brünle, Steffen; Casadei, Cecilia M.; Diethelm, Azeglio D.; Gashi, Dardan; Gotthard, Guillaume; Guixà-González, Ramon; Joti, Yasumasa; Kabanova, Victoria; Knopp, Gregor; Lesca, Elena; Ma, Pikyee; Martiel, Isabelle; Mühle, Jonas; Owada, Shigeki; Pamula, Filip; Sarabi, Daniel; Tejero, Oliver; Tsai, Ching-Ju; Varma, Niranjan; Wach, Anna; Boutet, Sébastien; Tono, Kensuke; Nogly, Przemyslaw; Deupi, Xavier; Iwata, So; Neutze, Richard; Standfuss, Jörg; Schertler, Gebhard; Panneels, Valerie

doi:10.1038/s41586-023-05863-6

Ultrafast structural changes direct the first molecular events of vision

Journal Article · Wed Mar 22 00:00:00 EDT 2023 · Nature (London)

DOI:https://doi.org/10.1038/s41586-023-05863-6· OSTI ID:1971214

^[1]; ^[2]; ^[2]; ^[3]; ^[4]; Nass, Karol ^[3]; Nango, Eriko ^[5]; ^[6]; ^[7]; ^[3]; ^[2]; ^[8]; ^[2]; ^[2]; ^[9]; ^[4]; ^[2]; ^[10]; ^[11]; ^[2] more »

Paul Scherrer Institute (PSI), Villigen (Switzerland). Laboratory for Biomolecular Research; SLAC
Paul Scherrer Institute (PSI), Villigen (Switzerland). Laboratory for Biomolecular Research
Paul Scherrer Institute (PSI), Villigen (Switzerland). Laboratory for Femtochemistry
University of Gothenburg (Sweden)
Tohoku University, Sendai (Japan); RIKEN SPring-8 Center, Hyogo (Japan)
Paul Scherrer Institute (PSI), Villigen (Switzerland). Laboratory for Theoretical and Computational Physics; Swiss Institute of Bioinformatics (SIB), Lausanne (Switzerland)
Paul Scherrer Institute (PSI), Villigen (Switzerland). Laboratory for Nonlinear Optics
Eidgenoessische Technische Hochschule (ETH), Zurich (Switzerland)
Paul Scherrer Institute (PSI), Villigen (Switzerland). Laboratory for Macromolecules and Bioimaging
Paul Scherrer Institute (PSI), Villigen (Switzerland)
RIKEN SPring-8 Center, Hyogo (Japan); Kyoto University (Japan)
Japan Synchrotron Radiation Research Institute, Hyogo (Japan)
Paul Scherrer Institute (PSI), Villigen (Switzerland). Laboratory for Femtochemistry; Ecole Polytechnique Federale Lausanne (EPFL) (Switzerland)
RIKEN SPring-8 Center, Hyogo (Japan); Japan Synchrotron Radiation Research Institute, Hyogo (Japan)
Polish Academy of Sciences (PAS), Krakow (Poland); Paul Scherrer Institute (PSI), Villigen (Switzerland)
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
Paul Scherrer Institute (PSI), Villigen (Switzerland). Laboratory for Biomolecular Research; Paul Scherrer Institute (PSI), Villigen (Switzerland). Laboratory for Theoretical and Computational Physics; Swiss Institute of Bioinformatics (SIB), Lausanne (Switzerland)

Vision is initiated by the rhodopsin family of light-sensitive G protein-coupled receptors (GPCRs). A photon is absorbed by the 11-cis retinal chromophore of rhodopsin, which isomerizes within 200 femtoseconds to the all-transconformation, 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 temperature 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.

View Accepted Manuscript (DOE)

Research Organization:: Leland Stanford Junior University, CA (United States); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: ETH Zürich; Japan Society for the Promotion of Science (JSPS); Marie Skłodowska-Curie Grant; National Institutes of Health (NIH); National Science Centre (Poland); Swedish Research Council; Swiss National Science Foundation; USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1971214

Alternate ID(s):: OSTI ID: 2478280

Journal Information:: Nature (London), Journal Name: Nature (London) Journal Issue: 7954 Vol. 615; ISSN 0028-0836

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (100)

Crystallographic Analysis of Primary Visual Photochemistry Nakamichi, Hitoshi; Okada, Tetsuji Angewandte Chemie International Edition, Vol. 45, Issue 26 https://doi.org/10.1002/anie.200600595	journal	June 2006
QM/MM Methods for Biomolecular Systems Senn, Hans Martin; Thiel, Walter Angewandte Chemie International Edition, Vol. 48, Issue 7 https://doi.org/10.1002/anie.200802019	journal	January 2009
Hartree–Fock exchange fitting basis sets for H to Rn Weigend, Florian Journal of Computational Chemistry, Vol. 29, Issue 2 https://doi.org/10.1002/jcc.20702	journal	January 2007
Effect of the damping function in dispersion corrected density functional theory Grimme, Stefan; Ehrlich, Stephan; Goerigk, Lars Journal of Computational Chemistry, Vol. 32, Issue 7 https://doi.org/10.1002/jcc.21759	journal	March 2011
MDAnalysis: A toolkit for the analysis of molecular dynamics simulations Michaud-Agrawal, Naveen; Denning, Elizabeth J.; Woolf, Thomas B. Journal of Computational Chemistry, Vol. 32, Issue 10 https://doi.org/10.1002/jcc.21787	journal	April 2011
A combined quantum mechanical and molecular mechanical potential for molecular dynamics simulations Field, Martin J.; Bash, Paul A.; Karplus, Martin Journal of Computational Chemistry, Vol. 11, Issue 6 https://doi.org/10.1002/jcc.540110605	journal	July 1990
Turbomole Furche, Filipp; Ahlrichs, Reinhart; Hättig, Christof Wiley Interdisciplinary Reviews: Computational Molecular Science, Vol. 4, Issue 2 https://doi.org/10.1002/wcms.1162	journal	July 2013
C hem S hell—a modular software package for QM / MM simulations Metz, Sebastian; Kästner, Johannes; Sokol, Alexey A. Wiley Interdisciplinary Reviews: Computational Molecular Science, Vol. 4, Issue 2 https://doi.org/10.1002/wcms.1163	journal	July 2013
Insight into the isomerization mechanism of retinal proteins from hybrid quantum mechanics/molecular mechanics simulations Sen, Saumik; Kar, Rajiv K.; Borin, Veniamin A. WIREs Computational Molecular Science, Vol. 12, Issue 1 https://doi.org/10.1002/wcms.1562	journal	July 2021
The ORCA program system: The ORCA program system Neese, Frank Wiley Interdisciplinary Reviews: Computational Molecular Science, Vol. 2, Issue 1 https://doi.org/10.1002/wcms.81	journal	June 2011
Dynamic Structural Biology Experiments at XFEL or Synchrotron Sources Aller, Pierre; Orville, Allen M. Methods in Molecular Biology https://doi.org/10.1007/978-1-0716-1406-8_11	book	January 2021
Assembly of functional rhodopsin requires a disulfide bond between cysteine residues 110 and 187. Karnik, S. S.; Khorana, H. G. Journal of Biological Chemistry, Vol. 265, Issue 29 https://doi.org/10.1016/S0021-9258(18)38195-X	journal	October 1990
Mapping of the amino acids in membrane-embedded helices that interact with the retinal chromophore in bovine rhodopsin Nakayama, T. A.; Khorana, H. G. Journal of Biological Chemistry, Vol. 266, Issue 7 https://doi.org/10.1016/S0021-9258(20)64317-4	journal	March 1991
Structure Optimizations for Excited States with Correlated Second-Order Methods: CC2 and ADC(2) Hättig, Christof Response Theory and Molecular Properties (A Tribute to Jan Linderberg and Poul Jørgensen) https://doi.org/10.1016/S0065-3276(05)50003-0	book	January 2005
QUASI: A general purpose implementation of the QM/MM approach and its application to problems in catalysis Sherwood, Paul; de Vries, Alex H.; Guest, Martyn F. Journal of Molecular Structure: THEOCHEM, Vol. 632, Issue 1-3 https://doi.org/10.1016/S0166-1280(03)00285-9	journal	August 2003
[19] Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G protein-coupled receptors Ballesteros, Juan A.; Weinstein, Harel Receptor Molecular Biology, Vol. 25, p. 366-428 https://doi.org/10.1016/S1043-9471(05)80049-7	book	January 1995
The Retinal Conformation and its Environment in Rhodopsin in Light of a New 2.2Å Crystal Structure Okada, Tetsuji; Sugihara, Minoru; Bondar, Ana-Nicoleta Journal of Molecular Biology, Vol. 342, Issue 2 https://doi.org/10.1016/j.jmb.2004.07.044	journal	September 2004
Crystals of Native and Modified Bovine Rhodopsins and Their Heavy Atom Derivatives Edwards, Patricia C.; Li, Jade; Burghammer, Manfred Journal of Molecular Biology, Vol. 343, Issue 5 https://doi.org/10.1016/j.jmb.2004.08.089	journal	November 2004
Structure of Bovine Rhodopsin in a Trigonal Crystal Form Li, Jade; Edwards, Patricia C.; Burghammer, Manfred Journal of Molecular Biology, Vol. 343, Issue 5 https://doi.org/10.1016/j.jmb.2004.08.090	journal	November 2004
Transmembrane signaling by GPCRs: Insight from rhodopsin and opsin structures Choe, Hui-Woog; Park, Jung Hee; Kim, Yong Ju Neuropharmacology, Vol. 60, Issue 1 https://doi.org/10.1016/j.neuropharm.2010.07.018	journal	January 2011
Structure of the rhodopsin dimer: a working model for G-protein-coupled receptors Fotiadis, Dimitrios; Jastrzebska, Beata; Philippsen, Ansgar Current Opinion in Structural Biology, Vol. 16, Issue 2 https://doi.org/10.1016/j.sbi.2006.03.013	journal	April 2006
A G protein-coupled receptor at work: the rhodopsin model Hofmann, Klaus Peter; Scheerer, Patrick; Hildebrand, Peter W. Trends in Biochemical Sciences, Vol. 34, Issue 11 https://doi.org/10.1016/j.tibs.2009.07.005	journal	November 2009
Theory and Simulation of the Ultrafast Double-Bond Isomerization of Biological Chromophores Gozem, Samer; Luk, Hoi Ling; Schapiro, Igor Chemical Reviews, Vol. 117, Issue 22 https://doi.org/10.1021/acs.chemrev.7b00177	journal	October 2017
ff14SB: Improving the Accuracy of Protein Side Chain and Backbone Parameters from ff99SB Maier, James A.; Martinez, Carmenza; Kasavajhala, Koushik Journal of Chemical Theory and Computation, Vol. 11, Issue 8 https://doi.org/10.1021/acs.jctc.5b00255	journal	July 2015
Resonance Raman Analysis of the Mechanism of Energy Storage and Chromophore Distortion in the Primary Visual Photoproduct Yan, Elsa C. Y.; Ganim, Ziad; Kazmi, Manija A. Biochemistry, Vol. 43, Issue 34 https://doi.org/10.1021/bi0400148	journal	August 2004
Time-Resolved Photointermediate Changes in Rhodopsin Glutamic Acid 181 Mutants Lewis, James W.; Szundi, Istvan; Kazmi, Manija A. Biochemistry, Vol. 43, Issue 39 https://doi.org/10.1021/bi049581l	journal	September 2004
Microbial and Animal Rhodopsins: Structures, Functions, and Molecular Mechanisms Ernst, Oliver P.; Lodowski, David T.; Elstner, Marcus Chemical Reviews, Vol. 114, Issue 1 https://doi.org/10.1021/cr4003769	journal	September 2013
PROPKA3: Consistent Treatment of Internal and Surface Residues in Empirical p K _a Predictions Olsson, Mats H. M.; Søndergaard, Chresten R.; Rostkowski, Michal Journal of Chemical Theory and Computation, Vol. 7, Issue 2 https://doi.org/10.1021/ct100578z	journal	December 2010
Improved Treatment of Ligands and Coupling Effects in Empirical Calculation and Rationalization of p K _a Values Søndergaard, Chresten R.; Olsson, Mats H. M.; Rostkowski, Michał Journal of Chemical Theory and Computation, Vol. 7, Issue 7 https://doi.org/10.1021/ct200133y	journal	June 2011
A new photolysis intermediate in artificial and native visual pigments Randall, C. E.; Lewis, J. W.; Hug, S. J. Journal of the American Chemical Society, Vol. 113, Issue 9 https://doi.org/10.1021/ja00009a037	journal	April 1991
Isomer-Specific Interaction of the Retinal Chromophore with Threonine-118 in Rhodopsin Nagata, Tomoko; Oura, Tomonori; Terakita, Akihisa The Journal of Physical Chemistry A, Vol. 106, Issue 10 https://doi.org/10.1021/jp0124488	journal	February 2002
Bicycle-pedal model for the first step in the vision process Warshel, Arieh Nature, Vol. 260, Issue 5553 https://doi.org/10.1038/260679a0	journal	April 1976
Potential for biomolecular imaging with femtosecond X-ray pulses Neutze, Richard; Wouts, Remco; van der Spoel, David Nature, Vol. 406, Issue 6797 https://doi.org/10.1038/35021099	journal	August 2000
The structural basis of agonist-induced activation in constitutively active rhodopsin Standfuss, Jörg; Edwards, Patricia C.; D’Antona, Aaron Nature, Vol. 471, Issue 7340 https://doi.org/10.1038/nature09795	journal	March 2011
Molecular signatures of G-protein-coupled receptors Venkatakrishnan, A. J.; Deupi, Xavier; Lebon, Guillaume Nature, Vol. 494, Issue 7436 https://doi.org/10.1038/nature11896	journal	February 2013
Diverse activation pathways in class A GPCRs converge near the G-protein-coupling region Venkatakrishnan, A. J.; Deupi, Xavier; Lebon, Guillaume Nature, Vol. 536, Issue 7617 https://doi.org/10.1038/nature19107	journal	August 2016
Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography Coquelle, Nicolas; Sliwa, Michel; Woodhouse, Joyce Nature Chemistry, Vol. 10, Issue 1 https://doi.org/10.1038/nchem.2853	journal	September 2017
Retinal orientation and interactions in rhodopsin reveal a two-stage trigger mechanism for activation Kimata, Naoki; Pope, Andreyah; Eilers, Markus Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12683	journal	September 2016
Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser Arnlund, David; Johansson, Linda C.; Wickstrand, Cecilia Nature Methods, Vol. 11, Issue 9 https://doi.org/10.1038/nmeth.3067	journal	August 2014
Counterion displacement in the molecular evolution of the rhodopsin family Terakita, Akihisa; Koyanagi, Mitsumasa; Tsukamoto, Hisao Nature Structural & Molecular Biology, Vol. 11, Issue 3 https://doi.org/10.1038/nsmb731	journal	February 2004
Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin Nass Kovacs, Gabriela; Colletier, Jacques-Philippe; Grünbein, Marie Luise Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10758-0	journal	July 2019
Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin in the multiphoton regime and biological relevance Miller, R. J. Dwayne; Paré-Labrosse, Olivier; Sarracini, Antoine Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14971-0	journal	March 2020
Watching the release of a photopharmacological drug from tubulin using time-resolved serial crystallography Wranik, Maximilian; Weinert, Tobias; Slavov, Chavdar Nature Communications, Vol. 14, Issue 1 https://doi.org/10.1038/s41467-023-36481-5	journal	February 2023
Evidence for a vibrational phase-dependent isotope effect on the photochemistry of vision Schnedermann, C.; Yang, X.; Liebel, M. Nature Chemistry, Vol. 10, Issue 4 https://doi.org/10.1038/s41557-018-0014-y	journal	March 2018
Quantum–classical simulations of rhodopsin reveal excited-state population splitting and its effects on quantum efficiency Yang, Xuchun; Manathunga, Madushanka; Gozem, Samer Nature Chemistry, Vol. 14, Issue 4 https://doi.org/10.1038/s41557-022-00892-6	journal	March 2022
Femtosecond-to-millisecond structural changes in a light-driven sodium pump Skopintsev, Petr; Ehrenberg, David; Weinert, Tobias Nature, Vol. 583, Issue 7815 https://doi.org/10.1038/s41586-020-2307-8	journal	May 2020
Ultrafast structural changes within a photosynthetic reaction centre Dods, Robert; Båth, Petra; Morozov, Dmitry Nature, Vol. 589, Issue 7841, p. 310-314 https://doi.org/10.1038/s41586-020-3000-7	journal	December 2020
Time-resolved serial femtosecond crystallography at the European XFEL Pandey, Suraj; Bean, Richard; Sato, Tokushi Nature Methods https://doi.org/10.1038/s41592-019-0628-z	journal	November 2019
Illumination guidelines for ultrafast pump–probe experiments by serial femtosecond crystallography Grünbein, Marie Luise; Stricker, Miriam; Nass Kovacs, Gabriela Nature Methods, Vol. 17, Issue 7 https://doi.org/10.1038/s41592-020-0847-3	journal	May 2020
GPCRmd uncovers the dynamics of the 3D-GPCRome Rodríguez-Espigares, Ismael; Torrens-Fontanals, Mariona; Tiemann, Johanna K. S. Nature Methods, Vol. 17, Issue 8 https://doi.org/10.1038/s41592-020-0884-y	journal	July 2020
GPCR activation mechanisms across classes and macro/microscales Hauser, Alexander S.; Kooistra, Albert J.; Munk, Christian Nature Structural & Molecular Biology, Vol. 28, Issue 11 https://doi.org/10.1038/s41594-021-00674-7	journal	November 2021
The frontiers of time-resolved macromolecular crystallography: movies and chirped X-ray pulses Moffat, Keith Faraday Discussions, Vol. 122 https://doi.org/10.1039/b201620f	journal	October 2002
Molecular recognition by proteins: Protein-ligand interactions from a structural perspective Wallace, A. C.; Laskowski, R. A.; Singh, J. Biochemical Society Transactions, Vol. 24, Issue 1 https://doi.org/10.1042/bst0240280	journal	February 1996
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
Gaussian basis sets for use in correlated molecular calculations. I. The atoms boron through neon and hydrogen Dunning, Thom H. The Journal of Chemical Physics, Vol. 90, Issue 2 https://doi.org/10.1063/1.456153	journal	January 1989
A tool for visualizing protein motions in time-resolved crystallography Wickstrand, Cecilia; Katona, Gergely; Nakane, Takanori Structural Dynamics, Vol. 7, Issue 2 https://doi.org/10.1063/1.5126921	journal	March 2020
Structure, initial excited-state relaxation, and energy storage of rhodopsin resolved at the multiconfigurational perturbation theory level Andruniow, T.; Ferre, N.; Olivucci, M. Proceedings of the National Academy of Sciences, Vol. 101, Issue 52 https://doi.org/10.1073/pnas.0407997101	journal	December 2004
Local peptide movement in the photoreaction intermediate of rhodopsin Nakamichi, H.; Okada, T. Proceedings of the National Academy of Sciences, Vol. 103, Issue 34 https://doi.org/10.1073/pnas.0601765103	journal	August 2006
Tracking the excited-state time evolution of the visual pigment with multiconfigurational quantum chemistry Frutos, L. M.; Andruniow, T.; Santoro, F. Proceedings of the National Academy of Sciences, Vol. 104, Issue 19 https://doi.org/10.1073/pnas.0701732104	journal	April 2007
Stabilized G protein binding site in the structure of constitutively active metarhodopsin-II Deupi, X.; Edwards, P.; Singhal, A. Proceedings of the National Academy of Sciences, Vol. 109, Issue 1 https://doi.org/10.1073/pnas.1114089108	journal	December 2011
Evolutionary steps involving counterion displacement in a tunicate opsin Kojima, Keiichi; Yamashita, Takahiro; Imamoto, Yasushi Proceedings of the National Academy of Sciences, Vol. 114, Issue 23 https://doi.org/10.1073/pnas.1701088114	journal	May 2017
Crystal structure of jumping spider rhodopsin-1 as a light sensitive GPCR Varma, Niranjan; Mutt, Eshita; Mühle, Jonas Proceedings of the National Academy of Sciences, Vol. 116, Issue 29 https://doi.org/10.1073/pnas.1902192116	journal	June 2019
Highly conserved glutamic acid in the extracellular IV–V loop in rhodopsins acts as the counterion in retinochrome, a member of the rhodopsin family Terakita, Akihisa; Yamashita, Takahiro; Shichida, Yoshinori Proceedings of the National Academy of Sciences, Vol. 97, Issue 26 https://doi.org/10.1073/pnas.260349597	journal	December 2000
Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Sakmar, T. P.; Franke, R. R.; Khorana, H. G. Proceedings of the National Academy of Sciences, Vol. 86, Issue 21 https://doi.org/10.1073/pnas.86.21.8309	journal	November 1989
Density-functional exchange-energy approximation with correct asymptotic behavior Becke, A. D. Physical Review A, Vol. 38, Issue 6 https://doi.org/10.1103/PhysRevA.38.3098	journal	September 1988
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
CrystFEL : a software suite for snapshot serial crystallography White, Thomas A.; Kirian, Richard A.; Martin, Andrew V. Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812002312	journal	March 2012
Indexing in single-crystal diffractometry with an obstinate list of reflections Duisenberg, A. J. M. Journal of Applied Crystallography, Vol. 25, Issue 2 https://doi.org/10.1107/S0021889891010634	journal	April 1992
Thermal motion in protein crystals estimated using laser-generated ultrasound and Young's modulus measurements Edwards, C.; Palmer, S. B.; Emsley, P. Acta Crystallographica Section A Foundations of Crystallography, Vol. 46, Issue 4 https://doi.org/10.1107/S0108767389012912	journal	April 1990
PHENIX : building new software for automated crystallographic structure determination Adams, Paul D.; Grosse-Kunstleve, Ralf W.; Hung, Li-Wei Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 11 https://doi.org/10.1107/S0907444902016657	journal	October 2002
Correction of X-ray intensities from single crystals containing lattice-translocation defects Wang, Jimin; Kamtekar, Satwik; Berman, Andrea J. Acta Crystallographica Section D Biological Crystallography, Vol. 61, Issue 1 https://doi.org/10.1107/S0907444904026721	journal	December 2004
The integration of macromolecular diffraction data Leslie, Andrew G. W. Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1 https://doi.org/10.1107/S0907444905039107	journal	December 2005
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
JLigand : a graphical tool for the CCP 4 template-restraint library Lebedev, Andrey A.; Young, Paul; Isupov, Michail N. Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S090744491200251X	journal	March 2012
The CCP4 suite programs for protein crystallography No authors listed Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763 https://doi.org/10.1107/S0907444994003112	journal	September 1994
High-viscosity sample-injection device for serial femtosecond crystallography at atmospheric pressure Shimazu, Yoshiaki; Tono, Kensuke; Tanaka, Tomoyuki Journal of Applied Crystallography, Vol. 52, Issue 6 https://doi.org/10.1107/S1600576719012846	journal	October 2019
Diverse application platform for hard X-ray diffraction in SACLA (DAPHNIS): application to serial protein crystallography using an X-ray free-electron laser Tono, Kensuke; Nango, Eriko; Sugahara, Michihiro Journal of Synchrotron Radiation, Vol. 22, Issue 3 https://doi.org/10.1107/S1600577515004464	journal	April 2015
Discerning best practices in XFEL-based biological crystallography – standards for nonstandard experiments Gorel, Alexander; Schlichting, Ilme; Barends, Thomas R. M. IUCrJ, Vol. 8, Issue 4 https://doi.org/10.1107/S205225252100467X	journal	June 2021
XGANDALF – extended gradient descent algorithm for lattice finding Gevorkov, Yaroslav; Yefanov, Oleksandr; Barty, Anton Acta Crystallographica Section A Foundations and Advances, Vol. 75, Issue 5 https://doi.org/10.1107/S2053273319010593	journal	August 2019
Processing serial crystallography data with CrystFEL : a step-by-step guide White, Thomas A. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2 https://doi.org/10.1107/S205979831801238X	journal	January 2019
Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10 https://doi.org/10.1107/S2059798319011471	journal	October 2019
Correction of rhodopsin serial crystallography diffraction intensities for a lattice-translocation defect Rodrigues, Matthew J.; Casadei, Cecilia M.; Weinert, Tobias Acta Crystallographica Section D Structural Biology, Vol. 79, Issue 3 https://doi.org/10.1107/S2059798323000931	journal	February 2023
Highly Selective Separation of Rhodopsin from Bovine Rod Outer Segment Membranes Using Combination of Divalent Cation and Alkyl(thio)glucoside Okada, Tetsuji; Takeda, Kazuki; Kouyama, Tsutomu Photochemistry and Photobiology, Vol. 67, Issue 5 https://doi.org/10.1111/j.1751-1097.1998.tb09445.x	journal	May 1998
Structural Observation of the Primary Isomerization in Vision with Femtosecond-Stimulated Raman Kukura, P. Science, Vol. 310, Issue 5750 https://doi.org/10.1126/science.1118379	journal	November 2005
Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein Tenboer, Jason; Basu, Shibom; Zatsepin, Nadia Science, Vol. 346, Issue 6214 https://doi.org/10.1126/science.1259357	journal	December 2014
The first step in vision: femtosecond isomerization of rhodopsin Schoenlein, R.; Peteanu, L.; Mathies, R. Science, Vol. 254, Issue 5030 https://doi.org/10.1126/science.1925597	journal	October 1991
Crystal Structure of Rhodopsin: A G Protein-Coupled Receptor Palczewski, K. Science, Vol. 289, Issue 5480 https://doi.org/10.1126/science.289.5480.739	journal	August 2000
Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation Barends, T. R. M.; Foucar, L.; Ardevol, A. Science, Vol. 350, Issue 6259 https://doi.org/10.1126/science.aac5492	journal	September 2015
Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein Pande, K.; Hutchison, C. D. M.; Groenhof, G. Science, Vol. 352, Issue 6286 https://doi.org/10.1126/science.aad5081	journal	May 2016
Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser Nogly, Przemyslaw; Weinert, Tobias; James, Daniel Science https://doi.org/10.1126/science.aat0094	journal	June 2018
Advances and challenges in time-resolved macromolecular crystallography Brändén, Gisela; Neutze, Richard Science, Vol. 373, Issue 6558 https://doi.org/10.1126/science.aba0954	journal	August 2021
Dynamics and mechanism of a light-driven chloride pump Mous, Sandra; Gotthard, Guillaume; Ehrenberg, David Science, Vol. 375, Issue 6583 https://doi.org/10.1126/science.abj6663	journal	February 2022
Second-Order Nonlinear Optical Imaging of Chiral Crystals Kissick, David J.; Wanapun, Debbie; Simpson, Garth J. Annual Review of Analytical Chemistry, Vol. 4, Issue 1 https://doi.org/10.1146/annurev.anchem.111808.073722	journal	July 2011
Crystallizing Membrane Proteins for Structure Determination: Use of Lipidic Mesophases Caffrey, Martin Annual Review of Biophysics, Vol. 38, Issue 1 https://doi.org/10.1146/annurev.biophys.050708.133655	journal	June 2009
Energy Landscapes as a Tool to Integrate GPCR Structure, Dynamics, and Function Deupi, Xavier; Kobilka, Brian K. Physiology, Vol. 25, Issue 5 https://doi.org/10.1152/physiol.00002.2010	journal	October 2010
Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography Coquelle, Coquelle Coherent X-ray Imaging Data Bank (Lawrence Berkeley National Laboratory); Institut Laue Langevin https://doi.org/10.11577/1369547	dataset	January 2017
Time-resolved protein nanocrystallography using an X-ray free-electron laser Aquila, Andrew; Hunter, Mark S.; Doak, R. Bruce Optics Express, Vol. 20, Issue 3 https://doi.org/10.1364/OE.20.002706	journal	January 2012
MDAnalysis: A Python Package for the Rapid Analysis of Molecular Dynamics Simulations Gowers, Richard; Linke, Max; Barnoud, Jonathan Proceedings of the Python in Science Conference https://doi.org/10.25080/Majora-629e541a-00e	conference	January 2016
Improving High Viscosity Extrusion of Microcrystals for Time-resolved Serial Femtosecond Crystallography at X-ray Lasers James, Daniel; Weinert, Tobias; Skopintsev, Petr Journal of Visualized Experiments, Issue 144 https://doi.org/10.3791/59087-v	journal	February 2019
The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser Claesson, Elin; Wahlgren, Weixiao Yuan; Takala, Heikki eLife, Vol. 9 https://doi.org/10.7554/eLife.53514	journal	March 2020

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