Raster-scanning serial protein crystallography using micro- and nano-focused synchrotron beams
Abstract
A raster scanning serial protein crystallography approach is presented, that consumes as low ∼200–700 nl of sedimented crystals. New serial data pre-analysis software, NanoPeakCell, is introduced. High-resolution structural information was obtained from lysozyme microcrystals (20 µm in the largest dimension) using raster-scanning serial protein crystallography on micro- and nano-focused beamlines at the ESRF. Data were collected at room temperature (RT) from crystals sandwiched between two silicon nitride wafers, thereby preventing their drying, while limiting background scattering and sample consumption. In order to identify crystal hits, new multi-processing and GUI-driven Python-based pre-analysis software was developed, named NanoPeakCell, that was able to read data from a variety of crystallographic image formats. Further data processing was carried out using CrystFEL, and the resultant structures were refined to 1.7 Å resolution. The data demonstrate the feasibility of RT raster-scanning serial micro- and nano-protein crystallography at synchrotrons and validate it as an alternative approach for the collection of high-resolution structural data from micro-sized crystals. Advantages of the proposed approach are its thriftiness, its handling-free nature, the reduced amount of sample required, the adjustable hit rate, the high indexing rate and the minimization of background scattering.
- Authors:
-
- Université Grenoble Alpes, IBS, 38044 Grenoble (France)
- Lawrence Berkeley National Laboratory, Berkeley, CA 94720 (United States)
- European Synchrotron Radiation Facility, BP 220, 38043 Grenoble (France)
- Publication Date:
- OSTI Identifier:
- 22351153
- Resource Type:
- Journal Article
- Journal Name:
- Acta Crystallographica. Section D: Biological Crystallography
- Additional Journal Information:
- Journal Volume: 71; Journal Issue: Pt 5; Other Information: PMCID: PMC4427202; PMID: 25945583; PUBLISHER-ID: kw5115; OAI: oai:pubmedcentral.nih.gov:4427202; Copyright (c) Coquelle et al. 2015; This is an open-access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are cited.; Country of input: International Atomic Energy Agency (IAEA); Journal ID: ISSN 0907-4449
- Country of Publication:
- Denmark
- Language:
- English
- Subject:
- 75 CONDENSED MATTER PHYSICS, SUPERCONDUCTIVITY AND SUPERFLUIDITY; BEAMS; CRYSTALLOGRAPHY; CRYSTALS; EUROPEAN SYNCHROTRON RADIATION FACILITY; IMAGES; LYSOZYME; MINIMIZATION; RADIATION EFFECTS; RESOLUTION; SCATTERING; SILICON; SILICON NITRIDES; SYNCHROTRONS
Citation Formats
Coquelle, Nicolas, CNRS, IBS, 38044 Grenoble, CEA, IBS, 38044 Grenoble, Brewster, Aaron S., Kapp, Ulrike, Shilova, Anastasya, Weinhausen, Britta, Burghammer, Manfred, Ghent University, Ghent B-9000, Colletier, Jacques-Philippe, CNRS, IBS, 38044 Grenoble, and CEA, IBS, 38044 Grenoble. Raster-scanning serial protein crystallography using micro- and nano-focused synchrotron beams. Denmark: N. p., 2015.
Web. doi:10.1107/S1399004715004514.
Coquelle, Nicolas, CNRS, IBS, 38044 Grenoble, CEA, IBS, 38044 Grenoble, Brewster, Aaron S., Kapp, Ulrike, Shilova, Anastasya, Weinhausen, Britta, Burghammer, Manfred, Ghent University, Ghent B-9000, Colletier, Jacques-Philippe, CNRS, IBS, 38044 Grenoble, & CEA, IBS, 38044 Grenoble. Raster-scanning serial protein crystallography using micro- and nano-focused synchrotron beams. Denmark. https://doi.org/10.1107/S1399004715004514
Coquelle, Nicolas, CNRS, IBS, 38044 Grenoble, CEA, IBS, 38044 Grenoble, Brewster, Aaron S., Kapp, Ulrike, Shilova, Anastasya, Weinhausen, Britta, Burghammer, Manfred, Ghent University, Ghent B-9000, Colletier, Jacques-Philippe, CNRS, IBS, 38044 Grenoble, and CEA, IBS, 38044 Grenoble. 2015.
"Raster-scanning serial protein crystallography using micro- and nano-focused synchrotron beams". Denmark. https://doi.org/10.1107/S1399004715004514.
@article{osti_22351153,
title = {Raster-scanning serial protein crystallography using micro- and nano-focused synchrotron beams},
author = {Coquelle, Nicolas and CNRS, IBS, 38044 Grenoble and CEA, IBS, 38044 Grenoble and Brewster, Aaron S. and Kapp, Ulrike and Shilova, Anastasya and Weinhausen, Britta and Burghammer, Manfred and Ghent University, Ghent B-9000 and Colletier, Jacques-Philippe and CNRS, IBS, 38044 Grenoble and CEA, IBS, 38044 Grenoble},
abstractNote = {A raster scanning serial protein crystallography approach is presented, that consumes as low ∼200–700 nl of sedimented crystals. New serial data pre-analysis software, NanoPeakCell, is introduced. High-resolution structural information was obtained from lysozyme microcrystals (20 µm in the largest dimension) using raster-scanning serial protein crystallography on micro- and nano-focused beamlines at the ESRF. Data were collected at room temperature (RT) from crystals sandwiched between two silicon nitride wafers, thereby preventing their drying, while limiting background scattering and sample consumption. In order to identify crystal hits, new multi-processing and GUI-driven Python-based pre-analysis software was developed, named NanoPeakCell, that was able to read data from a variety of crystallographic image formats. Further data processing was carried out using CrystFEL, and the resultant structures were refined to 1.7 Å resolution. The data demonstrate the feasibility of RT raster-scanning serial micro- and nano-protein crystallography at synchrotrons and validate it as an alternative approach for the collection of high-resolution structural data from micro-sized crystals. Advantages of the proposed approach are its thriftiness, its handling-free nature, the reduced amount of sample required, the adjustable hit rate, the high indexing rate and the minimization of background scattering.},
doi = {10.1107/S1399004715004514},
url = {https://www.osti.gov/biblio/22351153},
journal = {Acta Crystallographica. Section D: Biological Crystallography},
issn = {0907-4449},
number = Pt 5,
volume = 71,
place = {Denmark},
year = {Fri May 01 00:00:00 EDT 2015},
month = {Fri May 01 00:00:00 EDT 2015}
}
Works referenced in this record:
Crystallographic dissection of the thermal motion of protein-sugar complex
journal, May 2002
- Harata, Kazuaki; Kanai, Ryuta
- Proteins: Structure, Function, and Genetics, Vol. 48, Issue 1
SEM imaging of liquid jets
journal, June 2009
- DePonte, Daniel P.; Doak, R. B.; Hunter, Mark
- Micron, Vol. 40, Issue 4, p. 507-509
Observation of Decreased Radiation Damage at Higher Dose Rates in Room Temperature Protein Crystallography
journal, December 2007
- Southworth-Davies, Robert J.; Medina, Melissa A.; Carmichael, Ian
- Structure, Vol. 15, Issue 12
Raman-Assisted Crystallography Suggests a Mechanism of X-Ray-Induced Disulfide Radical Formation and Reparation
journal, November 2010
- Carpentier, Philippe; Royant, Antoine; Weik, Martin
- Structure, Vol. 18, Issue 11
Acoustically Mounted Microcrystals Yield High-Resolution X-ray Structures
journal, May 2011
- Soares, Alexei S.; Engel, Matthew A.; Stearns, Richard
- Biochemistry, Vol. 50, Issue 21
ChipX: A Novel Microfluidic Chip for Counter-Diffusion Crystallization of Biomolecules and in Situ Crystal Analysis at Room Temperature
journal, July 2013
- Pinker, Franziska; Brun, Mathieu; Morin, Pierre
- Crystal Growth & Design, Vol. 13, Issue 8
Potential for biomolecular imaging with femtosecond X-ray pulses
journal, August 2000
- Neutze, Richard; Wouts, Remco; van der Spoel, David
- Nature, Vol. 406, Issue 6797
Femtosecond X-ray protein nanocrystallography
journal, February 2011
- Chapman, Henry N.; Fromme, Petra; Barty, Anton
- Nature, Vol. 470, Issue 7332, p. 73-77
The ensemble nature of allostery
journal, April 2014
- Motlagh, Hesam N.; Wrabl, James O.; Li, Jing
- Nature, Vol. 508, Issue 7496
Lipidic cubic phase injector facilitates membrane protein serial femtosecond crystallography
journal, February 2014
- Weierstall, Uwe; James, Daniel; Wang, Chong
- Nature Communications, Vol. 5, Issue 1
In vivo protein crystallization opens new routes in structural biology
journal, January 2012
- Koopmann, Rudolf; Cupelli, Karolina; Redecke, Lars
- Nature Methods, Vol. 9, Issue 3
Grease matrix as a versatile carrier of proteins for serial crystallography
journal, November 2014
- Sugahara, Michihiro; Mizohata, Eiichi; Nango, Eriko
- Nature Methods, Vol. 12, Issue 1
Hard x-ray nanoprobe based on refractive x-ray lenses
journal, September 2005
- Schroer, C. G.; Kurapova, O.; Patommel, J.
- Applied Physics Letters, Vol. 87, Issue 12
Experimental determination of the radiation dose limit for cryocooled protein crystals
journal, March 2006
- Owen, R. L.; Rudino-Pinera, E.; Garman, E. F.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 13
Shoot-and-Trap: Use of specific x-ray damage to study structural protein dynamics by temperature-controlled cryo-crystallography
journal, August 2008
- Colletier, J. -P.; Bourgeois, D.; Sanson, B.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 33
Accessing protein conformational ensembles using room-temperature X-ray crystallography
journal, September 2011
- Fraser, J. S.; van den Bedem, H.; Samelson, A. J.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 39
Protein crystal structure obtained at 2.9 A resolution from injecting bacterial cells into an X-ray free-electron laser beam
journal, August 2014
- Sawaya, M. R.; Cascio, D.; Gingery, M.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 35
Goniometer-based femtosecond crystallography with X-ray free electron lasers
journal, October 2014
- Cohen, Aina E.; Soltis, S. Michael; González, Ana
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 48, p. 17122-17127
Opportunities and challenges for time-resolved studies of protein structural dynamics at X-ray free-electron lasers
journal, July 2014
- Neutze, Richard
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647
Transmission electron microscopy as a tool for nanocrystal characterization pre- and post-injector
journal, July 2014
- Stevenson, H. P.; DePonte, D. P.; Makhov, A. M.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647
Use of a `caged' analogue to study the traffic of choline within acetylcholinesterase by kinetic crystallography
journal, October 2007
- Colletier, Jacques-Philippe; Royant, Antoine; Specht, Alexandre
- Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 11
Insights into the mechanism of X-ray-induced disulfide-bond cleavage in lysozyme crystals based on EPR, optical absorption and X-ray diffraction studies
journal, November 2013
- Sutton, Kristin A.; Black, Paul J.; Mercer, Kermit R.
- Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 12
Absorbed dose calculations for macromolecular crystals: improvements to RADDOSE
journal, February 2009
- Paithankar, Karthik S.; Owen, Robin Leslie; Garman, Elspeth F.
- Journal of Synchrotron Radiation, Vol. 16, Issue 2
Linking Crystallographic Model and Data Quality
journal, May 2012
- Karplus, P. A.; Diederichs, K.
- Science, Vol. 336, Issue 6084
Natively Inhibited Trypanosoma brucei Cathepsin B Structure Determined by Using an X-ray Laser
journal, November 2012
- Redecke, L.; Nass, K.; DePonte, D. P.
- Science, Vol. 339, Issue 6116
Absorption of 20-eV to 50,000-eV Electron Beams in Air and Plastic
journal, April 1969
- Cole, Arthur
- Radiation Research, Vol. 38, Issue 1
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen
journal, August 2020
- Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe
- JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6
Advances in kinetic protein crystallography
journal, October 2005
- Bourgeois, Dominique; Royant, Antoine
- Current Opinion in Structural Biology, Vol. 15, Issue 5
Fixed-target protein serial microcrystallography with an x-ray free electron laser
journal, August 2014
- Hunter, Mark S.; Segelke, Brent; Messerschmidt, Marc
- Scientific Reports, Vol. 4, Issue 1
Hard X-Ray Nanoprobe based on Refractive X-Ray Lenses
conference, January 2007
- Schroer, C. G.; Kurapova, O.; Patommel, J.
- SYNCHROTRON RADIATION INSTRUMENTATION: Ninth International Conference on Synchrotron Radiation Instrumentation, AIP Conference Proceedings
Crystallography on a chip
journal, February 2012
- Zarrine-Afsar, Arash; Barends, Thomas R. M.; Müller, Christina
- Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 3
Overview of the CCP4 suite and current developments.
text, January 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Apollo - University of Cambridge Repository
Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard.
journalarticle, January 2008
- Terwilliger, Thomas C.; Grosse-Kunstleve, Ralf W.; Afonine, Pavel V.
- International Union of Crystallography (IUCr)
High-Resolution Protein Structure Determination by Serial Femtosecond Crystallography
journal, May 2012
- Boutet, S.; Lomb, L.; Williams, G. J.
- Science, Vol. 337, Issue 6092
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
Works referencing / citing this record:
Efficient adsorptive extraction materials by surface protein-imprinted polymer over silica gel for selective recognition/separation of human serum albumin from urine: Efficient adsorptive extraction materials by surface protein-imprinted polymer over silica gel for selective recognition/separation of human serum alb
journal, August 2018
- Madhumanchi, Sreenu; Jadda, Ramana; Suedee, Roongnapa
- Journal of Applied Polymer Science, Vol. 136, Issue 1
Serial Millisecond Crystallography of Membrane Proteins
book, January 2016
- Jaeger, Kathrin; Dworkowski, Florian; Nogly, Przemyslaw
- Advances in Experimental Medicine and Biology
Pink-beam serial crystallography
journal, November 2017
- Meents, A.; Wiedorn, M. O.; Srajer, V.
- Nature Communications, Vol. 8, Issue 1
Liquid application method for time-resolved analyses by serial synchrotron crystallography
journal, September 2019
- Mehrabi, Pedram; Schulz, Eike C.; Agthe, Michael
- Nature Methods, Vol. 16, Issue 10
Graphene-based microfluidics for serial crystallography
journal, January 2016
- Sui, Shuo; Wang, Yuxi; Kolewe, Kristopher W.
- Lab on a Chip, Vol. 16, Issue 16
Data-driven challenges and opportunities in crystallography
journal, July 2019
- Glynn, Calina; Rodriguez, Jose A.
- Emerging Topics in Life Sciences, Vol. 3, Issue 4
Time-resolved structural studies with serial crystallography: A new light on retinal proteins
journal, June 2015
- Panneels, Valérie; Wu, Wenting; Tsai, Ching-Ju
- Structural Dynamics, Vol. 2, Issue 4
Microfluidics: From crystallization to serial time-resolved crystallography
journal, May 2017
- Sui, Shuo; Perry, Sarah L.
- Structural Dynamics, Vol. 4, Issue 3
Microscopy Instrumentation and Nanopositioning at NSLS-II: Current Status and Future Directions
journal, September 2018
- Nazaretski, E.; Xu, W.; Yan, H.
- Synchrotron Radiation News, Vol. 31, Issue 5
An outlook on using serial femtosecond crystallography in drug discovery
journal, May 2019
- Mishin, Alexey; Gusach, Anastasiia; Luginina, Aleksandra
- Expert Opinion on Drug Discovery, Vol. 14, Issue 9
Watching proteins function with time-resolved x-ray crystallography
journal, August 2017
- Šrajer, Vukica; Schmidt, Marius
- Journal of Physics D: Applied Physics, Vol. 50, Issue 37
Protein refractive index increment is determined by conformation as well as composition
journal, October 2018
- Khago, Domarin; Bierma, Jan C.; Roskamp, Kyle W.
- Journal of Physics: Condensed Matter, Vol. 30, Issue 43
Transforming X-ray detection with hybrid photon counting detectors
journal, April 2019
- Förster, Andreas; Brandstetter, Stefan; Schulze-Briese, Clemens
- Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 377, Issue 2147
X-ray free-electron laser: opportunities for drug discovery
journal, July 2018
- Cheng, Robert; Abela, Rafael; Hennig, Michael
- Acta Crystallographica Section A Foundations and Advances, Vol. 74, Issue a1
Protein crystals IR laser ablated from aqueous solution at high speed retain their diffractive properties: applications in high-speed serial crystallography
journal, November 2017
- Schulz, Eike C.; Kaub, Johannes; Busse, Frederik
- Journal of Applied Crystallography, Vol. 50, Issue 6
ClickX : a visualization-based program for preprocessing of serial crystallography data
journal, May 2019
- Li, Xuanxuan; Li, Chufeng; Liu, Haiguang
- Journal of Applied Crystallography, Vol. 52, Issue 3
High-viscosity injector-based pink-beam serial crystallography of microcrystals at a synchrotron radiation source
journal, April 2019
- Martin-Garcia, Jose M.; Zhu, Lan; Mendez, Derek
- IUCrJ, Vol. 6, Issue 3
ZOO : an automatic data-collection system for high-throughput structure analysis in protein microcrystallography
journal, January 2019
- Hirata, Kunio; Yamashita, Keitaro; Ueno, Go
- Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2
Strategies for sample delivery for femtosecond crystallography
journal, February 2019
- Martiel, Isabelle; Müller-Werkmeister, Henrike M.; Cohen, Aina E.
- Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2
Well-based crystallization of lipidic cubic phase microcrystals for serial X-ray crystallography experiments
journal, October 2019
- Andersson, Rebecka; Safari, Cecilia; Båth, Petra
- Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10
A guide to sample delivery systems for serial crystallography
journal, August 2019
- Zhao, Feng‐Zhu; Zhang, Bin; Yan, Er‐Kai
- The FEBS Journal, Vol. 286, Issue 22
Lipidic cubic phase injector is a viable crystal delivery system for time-resolved serial crystallography
text, January 2016
- Nogly, Przemyslaw; Panneels, Valerie; Nelson, Garrett
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography
journal, September 2017
- Coquelle, Nicolas; Sliwa, Michel; Woodhouse, Joyce
- Nature Chemistry, Vol. 10, Issue 1
Photoswitching mechanism of a fluorescent protein revealed by time-resolved crystallography and transient absorption spectroscopy
journal, February 2020
- Woodhouse, Joyce; Nass Kovacs, Gabriela; Coquelle, Nicolas
- Nature Communications, Vol. 11, Issue 1
X-ray free electron laser: opportunities for drug discovery
journal, November 2017
- Cheng, Robert K. Y.; Abela, Rafael; Hennig, Michael
- Essays in Biochemistry, Vol. 61, Issue 5
High-speed raster-scanning synchrotron serial microcrystallography with a high-precision piezo-scanner
text, January 2018
- Gao, Yuan; Xu, Weihe; Shi, Wuxian
- International Union of Crystallography (IUCr)
A microfluidic flow-focusing device for low sample consumption serial synchrotron crystallography experiments in liquid flow
text, January 2019
- Monteiro, Diana C. F.; Vakili, Mohammad; Harich, Jessica
- International Union of Crystallography (IUCr)
A multicrystal diffraction data-collection approach for studying structural dynamics with millisecond temporal resolution
journal, October 2016
- Schubert, Robin; Kapis, Svetlana; Gicquel, Yannig
- IUCrJ, Vol. 3, Issue 6
Carbonic anhydrase II microcrystals suitable for XFEL studies
journal, May 2018
- Lomelino, Carrie L.; Kim, Jin Kyun; Lee, Cheol
- Acta Crystallographica Section F Structural Biology Communications, Vol. 74, Issue 6
Time-resolved structural studies with serial crystallography: A new light on retinal proteins
text, January 2015
- Panneels, Valérie; Wu, Wenting; Tsai, Ching-Ju
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Lipidic cubic phase injector is a viable crystal delivery system for time-resolved serial crystallography
text, January 2016
- Nogly, Przemyslaw; Panneels, Valérie; Nelson, Garrett
- ETH Zurich
Radiation Damage in Macromolecular Crystallography
journal, November 2015
- Garman, Elspeth F.; Weik, Martin
- Synchrotron Radiation News, Vol. 28, Issue 6
Fixed-target serial oscillation crystallography at room temperature
text, January 2019
- Wierman, Jennifer L.; Paré-Labrosse, Olivier; Sarracini, Antoine
- International Union of Crystallography (IUCr)
Strategies for sample delivery for femtosecond crystallography
text, January 2019
- Martiel, Isabelle; Müller-Werkmeister, Henrike M.; Cohen, Aina E.
- International Union of Crystallography (IUCr)
Serial millisecond crystallography for routine room-temperature structure determination at synchrotrons
text, January 2017
- Weinert, Tobias; Olieric, Natacha; Cheng, Robert
- ETH Zurich
Serial millisecond crystallography for routine room-temperature structure determination at synchrotrons
journal, September 2017
- Weinert, Tobias; Olieric, Natacha; Cheng, Robert
- Nature Communications, Vol. 8, Issue 1
Sample manipulation and data assembly for robust microcrystal synchrotron crystallography
journal, July 2018
- Liu, Qun; Guo, Gongrui; Fuchs, Martin R.
- Acta Crystallographica Section A Foundations and Advances, Vol. 74, Issue a1
High-viscosity injector-based pink-beam serial crystallography of microcrystals at a synchrotron radiation source
text, January 2019
- Martin-Garcia, Jose M.; Zhu, Lan; Mendez, Derek
- International Union of Crystallography (IUCr)
Fixed-target serial oscillation crystallography at room temperature
text, January 2019
- Wierman, Jennifer L.; Paré-Labrosse, Olivier; Sarracini, Antoine
- International Union of Crystallography (IUCr)