Serial femtosecond crystallography of soluble proteins in lipidic cubic phase

Fromme, Raimund; Ishchenko, Andrii; Metz, Markus; Chowdhury, Shatabdi Roy; Basu, Shibom; Boutet, Sébastien; Fromme, Petra; White, Thomas A.; Barty, Anton; Spence, John C. H.; Weierstall, Uwe; Liu, Wei; Cherezov, Vadim

doi:10.1107/S2052252515013160

Serial femtosecond crystallography of soluble proteins in lipidic cubic phase

Journal Article · Tue Aug 04 00:00:00 EDT 2015 · IUCrJ

DOI:https://doi.org/10.1107/S2052252515013160· OSTI ID:1224055

Fromme, Raimund ^[1]; Ishchenko, Andrii ^[2]; Metz, Markus ^[3]; Chowdhury, Shatabdi Roy ^[1]; Basu, Shibom ^[1]; Boutet, Sébastien ^[4]; Fromme, Petra ^[1]; White, Thomas A. ^[5]; Barty, Anton ^[5]; Spence, John C. H. ^[6]; Weierstall, Uwe ^[6]; Liu, Wei ^[1]; Cherezov, Vadim ^[2]

Arizona State Univ., Tempe, AZ (United States)
Univ. of Southern California, Los Angeles, CA (United States)
Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); Univ. of Hamburg, Hamburg (Germany)
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany)
Arizona State Univ., Mesa, AZ (United States)

Serial femtosecond crystallography (SFX) at X-ray free-electron lasers (XFELs) enables high-resolution protein structure determination using micrometre-sized crystals at room temperature with minimal effects from radiation damage. SFX requires a steady supply of microcrystals intersecting the XFEL beam at random orientations. An LCP–SFX method has recently been introduced in which microcrystals of membrane proteins are grown and delivered for SFX data collection inside a gel-like membrane-mimetic matrix, known as lipidic cubic phase (LCP), using a special LCP microextrusion injector. Here, it is shown enabling a dramatic reduction in the amount of crystallized protein required for data collection compared with crystals delivered by liquid injectors. High-quality LCP–SFX data sets were collected for two soluble proteins, lysozyme and phycocyanin, using less than 0.1 mg of each protein.

View Accepted Manuscript (DOE)

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC03-76SF00515

OSTI ID:: 1224055

Alternate ID(s):: OSTI ID: 1260560

Journal Information:: IUCrJ, Journal Name: IUCrJ Journal Issue: 5 Vol. 2; ISSN 2052-2525; ISSN IUCRAJ

Publisher:: International Union of CrystallographyCopyright Statement

Country of Publication:: United States

Language:: English

References (32)

Crystallization Screens: Compatibility with the Lipidic Cubic Phase for in Meso Crystallization of Membrane Proteins Cherezov, Vadim; Fersi, Hannan; Caffrey, Martin Biophysical Journal, Vol. 81, Issue 1 https://doi.org/10.1016/S0006-3495(01)75694-9	journal	July 2001
A simple mechanical mixer for small viscous lipid-containing samples Cheng, Anchi; Hummel, Bernard; Qiu, Hong Chemistry and Physics of Lipids, Vol. 95, Issue 1 https://doi.org/10.1016/S0009-3084(98)00060-7	journal	September 1998
Enabling membrane protein structure and dynamics with X-ray free electron lasers Feld, Geoffrey K.; Frank, Matthias Current Opinion in Structural Biology, Vol. 27 https://doi.org/10.1016/j.sbi.2014.05.002	journal	August 2014
Characterization of lipid matrices for membrane protein crystallization by high-throughput small angle X-ray scattering Joseph, Jeremiah S.; Liu, Wei; Kunken, Joshua Methods, Vol. 55, Issue 4 https://doi.org/10.1016/j.ymeth.2011.08.013	journal	December 2011
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
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
Structure of a photosynthetic reaction centre determined by serial femtosecond crystallography Johansson, Linda C.; Arnlund, David; Katona, Gergely Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3911	journal	December 2013
Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography Weierstall, Uwe; James, Daniel; Wang, Chong Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4309	journal	February 2014
Lipidic phase membrane protein serial femtosecond crystallography Johansson, Linda C.; Arnlund, David; White, Thomas A. Nature Methods, Vol. 9, Issue 3 https://doi.org/10.1038/nmeth.1867	journal	January 2012
Grease matrix as a versatile carrier of proteins for serial crystallography Sugahara, Michihiro; Mizohata, Eiichi; Nango, Eriko Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3172	journal	November 2014
Femtosecond diffractive imaging with a soft-X-ray free-electron laser Chapman, Henry N.; Barty, Anton; Bogan, Michael J. Nature Physics, Vol. 2, Issue 12 https://doi.org/10.1038/nphys461	journal	November 2006
Crystallizing membrane proteins using lipidic mesophases Caffrey, Martin; Cherezov, Vadim Nature Protocols, Vol. 4, Issue 5 https://doi.org/10.1038/nprot.2009.31	journal	April 2009
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
Protein crystal structure obtained at 2.9 A resolution from injecting bacterial cells into an X-ray free-electron laser beam Sawaya, M. R.; Cascio, D.; Gingery, M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 35 https://doi.org/10.1073/pnas.1413456111	journal	August 2014
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
The Coherent X-ray Imaging (CXI) instrument at the Linac Coherent Light Source (LCLS) Boutet, Sébastien; J. Williams, Garth New Journal of Physics, Vol. 12, Issue 3 https://doi.org/10.1088/1367-2630/12/3/035024	journal	March 2010
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
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
Structure-factor analysis of femtosecond microdiffraction patterns from protein nanocrystals Kirian, Richard A.; White, Thomas A.; Holton, James M. Acta Crystallographica Section A Foundations of Crystallography, Vol. 67, Issue 2 https://doi.org/10.1107/S0108767310050981	journal	February 2011
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
Integration, scaling, space-group assignment and post-refinement Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 133-144 https://doi.org/10.1107/S0907444909047374	journal	January 2010
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
Absorbed dose calculations for macromolecular crystals: improvements to RADDOSE Paithankar, Karthik S.; Owen, Robin Leslie; Garman, Elspeth F. Journal of Synchrotron Radiation, Vol. 16, Issue 2 https://doi.org/10.1107/S0909049508040430	journal	February 2009
Cheetah : software for high-throughput reduction and analysis of serial femtosecond X-ray diffraction data Barty, Anton; Kirian, Richard A.; Maia, Filipe R. N. C. Journal of Applied Crystallography, Vol. 47, Issue 3 https://doi.org/10.1107/S1600576714007626	journal	May 2014
The CSPAD megapixel x-ray camera at LCLS Hart, Philip; Boutet, Sébastien; Carini, Gabriella SPIE Optical Engineering + Applications, SPIE Proceedings https://doi.org/10.1117/12.930924	conference	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
Linking Crystallographic Model and Data Quality Karplus, P. A.; Diederichs, K. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1218231	journal	May 2012
Natively Inhibited Trypanosoma brucei Cathepsin B Structure Determined by Using an X-ray Laser Redecke, L.; Nass, K.; DePonte, D. P. Science, Vol. 339, Issue 6116 https://doi.org/10.1126/science.1229663	journal	November 2012
Simultaneous Femtosecond X-ray Spectroscopy and Diffraction of Photosystem II at Room Temperature Kern, J.; Alonso-Mori, R.; Tran, R. Science, Vol. 340, Issue 6131 https://doi.org/10.1126/science.1234273	journal	February 2013
Serial Femtosecond Crystallography of G Protein-Coupled Receptors Liu, W.; Wacker, D.; Gati, C. Science, Vol. 342, Issue 6165 https://doi.org/10.1126/science.1244142	journal	December 2013
Developments in X-ray Crystallographic Structure Determination of Biological Macromolecules Garman, E. F. Science, Vol. 343, Issue 6175 https://doi.org/10.1126/science.1247829	journal	March 2014

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