Enabling X-ray free electron laser crystallography for challenging biological systems from a limited number of crystals

Uervirojnangkoorn, Monarin; Zeldin, Oliver B.; Lyubimov, Artem Y.; Hattne, Johan; Brewster, Aaron S.; Sauter, Nicholas K.; Brunger, Axel T.; Weis, William I.

doi:10.7554/eLife.05421

Title: Enabling X-ray free electron laser crystallography for challenging biological systems from a limited number of crystals

Journal Article · Tue Mar 17 00:00:00 EDT 2015 · eLife

DOI:https://doi.org/10.7554/eLife.05421· OSTI ID:1184051

Uervirojnangkoorn, Monarin ^[1]; Zeldin, Oliver B. ^[1]; Lyubimov, Artem Y. ^[1];

^[2]; Brewster, Aaron S. ^[3]; Sauter, Nicholas K. ^[3];

^[4];

^[5]

Department of Molecular and Cellular Physiology, Stanford University, Stanford, United States
Janelia Research Campus, Ashburn, United States
Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, United States
Department of Molecular and Cellular Physiology, Stanford University, Stanford, United States, Department of Neurology and Neurological Sciences, Howard Hughes Medical Institute, Stanford University, Stanford, United States, Department of Photon Science, Stanford University, Stanford, United States
Department of Molecular and Cellular Physiology, Stanford University, Stanford, United States, Department of Photon Science, Stanford University, Stanford, United States, Department of Structural Biology, Stanford University, Stanford, United States

There is considerable potential for X-ray free electron lasers (XFELs) to enable determination of macromolecular crystal structures that are difficult to solve using current synchrotron sources. Prior XFEL studies often involved the collection of thousands to millions of diffraction images, in part due to limitations of data processing methods. We implemented a data processing system based on classical post-refinement techniques, adapted to specific properties of XFEL diffraction data. When applied to XFEL data from three different proteins collected using various sample delivery systems and XFEL beam parameters, our method improved the quality of the diffraction data as well as the resulting refined atomic models and electron density maps. Moreover, the number of observations for a reflection necessary to assemble an accurate data set could be reduced to a few observations. These developments will help expand the applicability of XFEL crystallography to challenging biological systems, including cases where sample is limited.

View Journal Article

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231; GM103393; GM095887; GM102520

OSTI ID:: 1184051

Alternate ID(s):: OSTI ID: 1209798; OSTI ID: 1257268; OSTI ID: 1512179

Journal Information:: eLife, Journal Name: eLife Vol. 4; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 86 works

Citation information provided by
Web of Science

References (39)

Goniometer-based femtosecond crystallography with X-ray free electron lasers Cohen, Aina E.; Soltis, S. Michael; González, Ana Proceedings of the National Academy of Sciences, Vol. 111, Issue 48, p. 17122-17127 https://doi.org/10.1073/pnas.1418733111	journal	October 2014
Processing and post-refinement of oscillation camera data Rossmann, M. G.; Leslie, A. G. W.; Abdel-Meguid, S. S. Journal of Applied Crystallography, Vol. 12, Issue 6 https://doi.org/10.1107/S0021889879013273	journal	December 1979
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Changes to crystals of Escherichia coli β-galactosidase during room-temperature/low-temperature cycling and their relation to cryo-annealing Juers, Douglas H.; Lovelace, Jeffrey; Bellamy, Henry D. Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 11 https://doi.org/10.1107/S0907444907045040	journal	October 2007
Radiation damage in macromolecular crystallography: what is it and why should we care? Garman, Elspeth F. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910008656	journal	March 2010
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
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
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
New Python-based methods for data processing Sauter, Nicholas K.; Hattne, Johan; Grosse-Kunstleve, Ralf W. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913000863	journal	June 2013
Processing of X-ray snapshots from crystals in random orientations Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 8 https://doi.org/10.1107/S1399004714013534	journal	July 2014
Demonstration of self-seeding in a hard-X-ray free-electron laser Amann, J.; Berg, W.; Blank, V. Nature Photonics, Vol. 6, Issue 10, p. 693-698 https://doi.org/10.1038/nphoton.2012.180	journal	August 2012
Structure of CPV17 polyhedrin determined by the improved analysis of serial femtosecond crystallographic data Ginn, Helen M.; Messerschmidt, Marc; Ji, Xiaoyun Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7435	journal	March 2015
Femtosecond protein nanocrystallography—data analysis methods Kirian, Richard A.; Wang, Xiaoyu; Weierstall, Uwe Optics Express, Vol. 18, Issue 6 https://doi.org/10.1364/OE.18.005713	journal	January 2010
Matching X-ray beam and detector properties to protein crystals of different perfection Nave, Colin Journal of Synchrotron Radiation, Vol. 21, Issue 3 https://doi.org/10.1107/S1600577514003609	journal	March 2014
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
The oscillation method for crystals with very large unit cells Winkler, F. K.; Schutt, C. E.; Harrison, S. C. Acta Crystallographica Section A, Vol. 35, Issue 6 https://doi.org/10.1107/S0567739479002035	journal	November 1979
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Imaging biological specimens with high-intensity soft x rays Solem, Johndale C. Journal of the Optical Society of America B, Vol. 3, Issue 11 https://doi.org/10.1364/JOSAB.3.001551	journal	January 1986
A single-shot transmissive spectrometer for hard x-ray free electron lasers Zhu, Diling; Cammarata, Marco; Feldkamp, Jan M. Applied Physics Letters, Vol. 101, Issue 3 https://doi.org/10.1063/1.4736725	journal	July 2012
Predicting the X-ray lifetime of protein crystals Zeldin, O. B.; Brockhauser, S.; Bremridge, J. Proceedings of the National Academy of Sciences, Vol. 110, Issue 51 https://doi.org/10.1073/pnas.1315879110	journal	December 2013
A Description of Imperfections in Protein Crystals Nave, C. Acta Crystallographica Section D Biological Crystallography, Vol. 54, Issue 5 https://doi.org/10.1107/S0907444998001875	journal	September 1998
XFEL diffraction: developing processing methods to optimize data quality Sauter, Nicholas K. Journal of Synchrotron Radiation, Vol. 22, Issue 2 https://doi.org/10.1107/S1600577514028203	journal	January 2015
Structural analysis of zinc substitutions in the active site of thermolysin Holland, Debra R.; Hausrath, Andrew C.; Juers, Doug Protein Science, Vol. 4, Issue 10 https://doi.org/10.1002/pro.5560041001	journal	October 1995
Collective instabilities and high-gain regime in a free electron laser Bonifacio, R.; Pellegrini, C.; Narducci, L. M. Optics Communications, Vol. 50, Issue 6 https://doi.org/10.1016/0030-4018(84)90105-6	journal	July 1984
The Computational Crystallography Toolbox : crystallographic algorithms in a reusable software framework Grosse-Kunstleve, Ralf W.; Sauter, Nicholas K.; Moriarty, Nigel W. Journal of Applied Crystallography, Vol. 35, Issue 1 https://doi.org/10.1107/S0021889801017824	journal	January 2002
Improved crystal orientation and physical properties from single-shot XFEL stills Sauter, Nicholas K.; Hattne, Johan; Brewster, Aaron S. Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 12 https://doi.org/10.1107/S1399004714024134	journal	November 2014
X-ray Free Electron Lasers Motivate Bioanalytical Characterization of Protein Nanocrystals: Serial Femtosecond Crystallography Bogan, Michael J. Analytical Chemistry, Vol. 85, Issue 7 https://doi.org/10.1021/ac303716r	journal	March 2013
Automated diffraction image analysis and spot searching for high-throughput crystal screening Zhang, Zepu; Sauter, Nicholas K.; van den Bedem, Henry Journal of Applied Crystallography, Vol. 39, Issue 1 https://doi.org/10.1107/S0021889805040677	journal	January 2006
Determination of damage-free crystal structure of an X-ray–sensitive protein using an XFEL Hirata, Kunio; Shinzawa-Itoh, Kyoko; Yano, Naomine Nature Methods, Vol. 11, Issue 7 https://doi.org/10.1038/nmeth.2962	journal	May 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
Python for Scientific Computing Oliphant, Travis E. Computing in Science & Engineering, Vol. 9, Issue 3 https://doi.org/10.1109/MCSE.2007.58	journal	January 2007
Macromolecular crystallography with synchrotron radiation: photographic data collection and polarization correction Kahn, R.; Fourme, R.; Gadet, A. Journal of Applied Crystallography, Vol. 15, Issue 3 https://doi.org/10.1107/S0021889882012060	journal	June 1982
Post-refinement method for snapshot serial crystallography White, Thomas A. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647 https://doi.org/10.1098/rstb.2013.0330	journal	July 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
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
Accurate macromolecular structures using minimal measurements from X-ray free-electron lasers Hattne, Johan; Echols, Nathaniel; Tran, Rosalie Nature Methods, Vol. 11, Issue 5 https://doi.org/10.1038/nmeth.2887	journal	March 2014
Crystallographic model quality at a glance Urzhumtseva, Ludmila; Afonine, Pavel V.; Adams, Paul D. Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 3 https://doi.org/10.1107/S0907444908044296	journal	February 2009
Better models by discarding data? Diederichs, K.; Karplus, P. A. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913001121	journal	June 2013
Nanoflow electrospinning serial femtosecond crystallography Sierra, Raymond G.; Laksmono, Hartawan; Kern, Jan Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 11, p. 1584-1587 https://doi.org/10.1107/S0907444912038152	journal	October 2012

Similar Records

Enabling X-ray free electron laser crystallography for challenging biological systems from a limited number of crystals

Journal Article · Tue Mar 17 00:00:00 EDT 2015 · eLife · OSTI ID:1184051

Uervirojnangkoorn, Monarin; Zeldin, Oliver B.; Lyubimov, Artem Y.; +5 more

Mapping the conformational landscape of a dynamic enzyme by multitemperature and XFEL crystallography

Journal Article · Wed Sep 30 00:00:00 EDT 2015 · eLife · OSTI ID:1184051

Keedy, Daniel A.; Kenner, Lillian R.; Warkentin, Matthew; +21 more