Batch crystallization of rhodopsin for structural dynamics using an X-ray free-electron laser

Wu, Wenting; Nogly, Przemyslaw; Rheinberger, Jan; Kick, Leonhard M.; Gati, Cornelius; Nelson, Garrett; Deupi, Xavier; Standfuss, Jörg; Schertler, Gebhard; Panneels, Valérie

doi:10.1107/S2053230X15009966

Batch crystallization of rhodopsin for structural dynamics using an X-ray free-electron laser

Journal Article · Sat Jun 27 04:00:00 EDT 2015 · Acta crystallographica. Section F, Structural biology communications

DOI:https://doi.org/10.1107/S2053230X15009966· OSTI ID:22389083

Wu, Wenting; Nogly, Przemyslaw; Rheinberger, Jan; Kick, Leonhard M.; Gati, Cornelius; Nelson, Garrett; Deupi, Xavier; Standfuss, Jörg; Schertler, Gebhard; Panneels, Valérie ^[1]

Paul Scherrer Institute, OFLC/103, 5232 Villigen-PSI (Switzerland)

A new batch preparation method is presented for high-density micrometre-sized crystals of the G protein-coupled receptor rhodopsin for use in time-resolved serial femtosecond crystallography at an X-ray free-electron laser using a liquid jet. Rhodopsin is a membrane protein from the G protein-coupled receptor family. Together with its ligand retinal, it forms the visual pigment responsible for night vision. In order to perform ultrafast dynamics studies, a time-resolved serial femtosecond crystallography method is required owing to the nonreversible activation of rhodopsin. In such an approach, microcrystals in suspension are delivered into the X-ray pulses of an X-ray free-electron laser (XFEL) after a precise photoactivation delay. Here, a millilitre batch production of high-density microcrystals was developed by four methodical conversion steps starting from known vapour-diffusion crystallization protocols: (i) screening the low-salt crystallization conditions preferred for serial crystallography by vapour diffusion, (ii) optimization of batch crystallization, (iii) testing the crystal size and quality using second-harmonic generation (SHG) imaging and X-ray powder diffraction and (iv) production of millilitres of rhodopsin crystal suspension in batches for serial crystallography tests; these crystals diffracted at an XFEL at the Linac Coherent Light Source using a liquid-jet setup.

OSTI ID:: 22389083

Journal Information:: Acta crystallographica. Section F, Structural biology communications, Journal Name: Acta crystallographica. Section F, Structural biology communications Journal Issue: Pt 7 Vol. 71; ISSN ACSFEN; ISSN 2053-230X

Country of Publication:: United States

Language:: English

References (29)

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
Time-resolved structural studies at synchrotrons and X-ray free electron lasers: opportunities and challenges Neutze, Richard; Moffat, Keith Current Opinion in Structural Biology, Vol. 22, Issue 5 https://doi.org/10.1016/j.sbi.2012.08.006	journal	October 2012
Self-terminating diffraction gates femtosecond X-ray nanocrystallography measurements Barty, Anton; Caleman, Carl; Aquila, Andrew Nature Photonics, Vol. 6, Issue 1 https://doi.org/10.1038/nphoton.2011.297	journal	December 2011
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
Preparation of microcrystals in lipidic cubic phase for serial femtosecond crystallography Liu, Wei; Ishchenko, Andrii; Cherezov, Vadim Nature Protocols, Vol. 9, Issue 9 https://doi.org/10.1038/nprot.2014.141	journal	August 2014
Overcoming barriers to membrane protein structure determination Bill, Roslyn M.; Henderson, Peter J. F.; Iwata, So Nature Biotechnology, Vol. 29, Issue 4 https://doi.org/10.1038/nbt.1833	journal	April 2011
Injector for scattering measurements on fully solvated biospecies Weierstall, U.; Spence, J. C. H.; Doak, R. B. Review of Scientific Instruments, Vol. 83, Issue 3 https://doi.org/10.1063/1.3693040	journal	March 2012
Microcrystallization techniques for serial femtosecond crystallography using photosystem II from Thermosynechococcus elongatus as a model system Kupitz, Christopher; Grotjohann, Ingo; Conrad, Chelsie E. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647 https://doi.org/10.1098/rstb.2013.0316	journal	July 2014
Imaging Atomic Structure and Dynamics with Ultrafast X-ray Scattering Gaffney, K. J.; Chapman, H. N. Science, Vol. 316, Issue 5830 https://doi.org/10.1126/science.1135923	journal	June 2007
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
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
Introduction to Protein Crystallization Pusey, Marc L.; Aygün, Ramazan Savaş Data Analytics for Protein Crystallization https://doi.org/10.1007/978-3-319-58937-4_1	book	January 2017
Crystal structure of a photoactivated deprotonated intermediate of rhodopsin Salom, D.; Lodowski, D. T.; Stenkamp, R. E. Proceedings of the National Academy of Sciences, Vol. 103, Issue 44 https://doi.org/10.1073/pnas.0608022103	journal	October 2006
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
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
Protein crystallography microdiffraction Riekel, Christian; Burghammer, Manfred; Schertler, Gebhard Current Opinion in Structural Biology, Vol. 15, Issue 5 https://doi.org/10.1016/j.sbi.2005.08.013	journal	October 2005
Selective Detection of Protein Crystals by Second Harmonic Microscopy Wampler, Ronald D.; Kissick, David J.; Dehen, Christopher J. Journal of the American Chemical Society, Vol. 130, Issue 43 https://doi.org/10.1021/ja805983b	journal	October 2008
Lipidic Cubic Phases: New Matrices for the Three-Dimensional Crystallization of Membrane Proteins Rummel, Gabriele; Hardmeyer, Ariane; Widmer, Christine Journal of Structural Biology, Vol. 121, Issue 2 https://doi.org/10.1006/jsbi.1997.3952	journal	January 1998
Gas dynamic virtual nozzle for generation of microscopic droplet streams DePonte, D. P.; Weierstall, U.; Schmidt, K. Journal of Physics D: Applied Physics, Vol. 41, Issue 19, Article No. 195505 https://doi.org/10.1088/0022-3727/41/19/195505	journal	September 2008
Femtosecond X-ray protein nanocrystallography Chapman, Henry N.; Fromme, Petra; Barty, Anton Nature, Vol. 470, Issue 7332, p. 73-77 https://doi.org/10.1038/nature09750	journal	February 2011
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
Emerging opportunities in structural biology with X-ray free-electron lasers Schlichting, Ilme; Miao, Jianwei Current Opinion in Structural Biology, Vol. 22, Issue 5 https://doi.org/10.1016/j.sbi.2012.07.015	journal	October 2012
Experience with the CSPAD during dedicated detector runs at LCLS Carini, G. A.; Boutet, S.; Chollet, M. Journal of Physics: Conference Series, Vol. 493 https://doi.org/10.1088/1742-6596/493/1/012011	journal	March 2014
Micro-crystallography comes of age Smith, Janet L.; Fischetti, Robert F.; Yamamoto, Masaki Current Opinion in Structural Biology, Vol. 22, Issue 5 https://doi.org/10.1016/j.sbi.2012.09.001	journal	October 2012
High-Resolution Protein Structure Determination by Serial Femtosecond Crystallography Boutet, S.; Lomb, L.; Williams, G. J. Science, Vol. 337, Issue 6092 https://doi.org/10.1126/science.1217737	journal	May 2012
Introduction to protein crystallization McPherson, Alexander; Gavira, Jose A. Acta Crystallographica Section F Structural Biology Communications, Vol. 70, Issue 1 https://doi.org/10.1107/s2053230x13033141	journal	December 2013
X-ray lasers for structural and dynamic biology Spence, J. C. H.; Weierstall, U.; Chapman, H. N. Reports on Progress in Physics, Vol. 75, Issue 10 https://doi.org/10.1088/0034-4885/75/10/102601	journal	September 2012
A crystal clear solution for determining G-protein-coupled receptor structures Tate, Christopher G. Trends in Biochemical Sciences, Vol. 37, Issue 9 https://doi.org/10.1016/j.tibs.2012.06.003	journal	September 2012
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

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Time-resolved structural studies with serial crystallography: A new light on retinal proteins Panneels, Valérie; Wu, Wenting; Tsai, Ching-Ju Structural Dynamics, Vol. 2, Issue 4 https://doi.org/10.1063/1.4922774	journal	June 2015
Protein crystal screening and characterization for serial femtosecond nanocrystallography Darmanin, Connie; Strachan, Jamie; Adda, Christopher G. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep25345	journal	May 2016
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Strategies for sample delivery for femtosecond crystallography Martiel, Isabelle; Müller-Werkmeister, Henrike M.; Cohen, Aina E. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2 https://doi.org/10.1107/s2059798318017953	journal	February 2019
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Perspective: Opportunities for ultrafast science at SwissFEL Abela, Rafael; Beaud, Paul; Van Bokhoven, Jeroen A. ETH Zurich https://doi.org/10.3929/ethz-b-000231826	text	January 2017
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Strategies for sample delivery for femtosecond crystallography Martiel, Isabelle; Müller-Werkmeister, Henrike M.; Cohen, Aina E. International Union of Crystallography (IUCr) https://doi.org/10.1107/s2059798318017953/ba5296sup1.pdf	text	January 2019
Linac Coherent Light Source: The first five years Bostedt, Christoph; Boutet, Sébastien; Fritz, David M. Reviews of Modern Physics, Vol. 88, Issue 1 https://doi.org/10.1103/revmodphys.88.015007	journal	March 2016
Perspective: Opportunities for ultrafast science at SwissFEL Abela, Rafael; Beaud, Paul; van Bokhoven, Jeroen A. Structural Dynamics, Vol. 4, Issue 6 https://doi.org/10.1063/1.4997222	journal	November 2017
On-chip crystallization for serial crystallography experiments and on-chip ligand-binding studies Lieske, Julia; Cerv, Maximilian; Kreida, Stefan International Union of Crystallography (IUCr) https://doi.org/10.1107/s2052252519007395/mf5034sup1.pdf	text	January 2019
On-chip crystallization for serial crystallography experiments and on-chip ligand-binding studies Lieske, Julia; Cerv, Maximilian; Kreida, Stefan Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2019-02620	text	January 2019
Perspective: Opportunities for ultrafast science at SwissFEL Abela, Rafael; Beaud, Paul; Van Bokhoven, Jeroen A. AIP Publishing https://doi.org/10.7892/boris.114739	text	January 2017

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