High-viscosity injector-based pink-beam serial crystallography of microcrystals at a synchrotron radiation source

Martin-Garcia, Jose M.; Zhu, Lan; Mendez, Derek; Lee, Ming-Yue; Chun, Eugene; Li, Chufeng; Hu, Hao; Subramanian, Ganesh; Kissick, David; Ogata, Craig; Henning, Robert; Ishchenko, Andrii; Dobson, Zachary; Zhang, Shangji; Weierstall, Uwe; Spence, John C. H.; Fromme, Petra; Zatsepin, Nadia A.; Fischetti, Robert F.; Cherezov, Vadim; Liu, Wei

doi:10.1107/S205225251900263X

Title: High-viscosity injector-based pink-beam serial crystallography of microcrystals at a synchrotron radiation source

Journal Article · 05 April 2019 · IUCrJ

DOI: https://doi.org/10.1107/S205225251900263X · OSTI ID:1617937

; Zhu, Lan; Mendez, Derek; Lee, Ming-Yue; Chun, Eugene;

; Hu, Hao; Subramanian, Ganesh; Kissick, David; Ogata, Craig; Henning, Robert;

; Dobson, Zachary; Zhang, Shangji; Weierstall, Uwe;

; Fromme, Petra;

;

; Cherezov, Vadim more »

Since the first successful serial crystallography (SX) experiment at a synchrotron radiation source, the popularity of this approach has continued to grow showing that third-generation synchrotrons can be viable alternatives to scarce X-ray free-electron laser sources. Synchrotron radiation flux may be increased ∼100 times by a moderate increase in the bandwidth (`pink beam' conditions) at some cost to data analysis complexity. Here, we report the first high-viscosity injector-based pink-beam SX experiments. The structures of proteinase K (PK) and A _2A adenosine receptor (A _2A AR) were determined to resolutions of 1.8 and 4.2 Å using 4 and 24 consecutive 100 ps X-ray pulse exposures, respectively. Strong PK data were processed using existing Laue approaches, while weaker A _2A AR data required an alternative data-processing strategy. This demonstration of the feasibility presents new opportunities for time-resolved experiments with microcrystals to study structural changes in real time at pink-beam synchrotron beamlines worldwide.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE; National Institutes of Health (NIH), National Institute of General Medical Sciences; National Institutes of Health (NIH), National Cancer Institute; Mayo Clinic; Arizona State University; National Science Foundation (NSF), BioXFEL; National Science Foundation (NSF)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1617937

Alternate ID(s):: OSTI ID: 1542189

Journal Information:: IUCrJ, Journal Name: IUCrJ Vol. 6 Journal Issue: 3; ISSN 2052-2525

Publisher:: International Union of Crystallography (IUCr)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 29 works

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References (73)

Light-Induced Structural Changes in a Photosynthetic Reaction Center Caught by Laue Diffraction Wohri, A. B.; Katona, G.; Johansson, L. C. Science, Vol. 328, Issue 5978 https://doi.org/10.1126/science.1186159	journal	April 2010
Serial femtosecond crystallography at the SACLA: breakthrough to dynamic structural biology Mizohata, Eiichi; Nakane, Takanori; Fukuda, Yohta Biophysical Reviews, Vol. 10, Issue 2 https://doi.org/10.1007/s12551-017-0344-9	journal	December 2017
Structural enzymology using X-ray free electron lasers Kupitz, Christopher; Olmos, Jose L.; Holl, Mark Structural Dynamics, Vol. 4, Issue 4 https://doi.org/10.1063/1.4972069	journal	December 2016
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
Protein Conformational Relaxation and Ligand Migration in Myoglobin: A Nanosecond to Millisecond Molecular Movie from Time-Resolved Laue X-ray Diffraction ^† Šrajer, Vukica; Ren, Zhong; Teng, Tsu-Yi Biochemistry, Vol. 40, Issue 46 https://doi.org/10.1021/bi010715u	journal	November 2001
Lifetimes and spatio-temporal response of protein crystals in intense X-ray microbeams Warkentin, Matthew A.; Atakisi, Hakan; Hopkins, Jesse B. IUCrJ, Vol. 4, Issue 6 https://doi.org/10.1107/S2052252517013495	journal	October 2017
Serial crystallography on in vivo grown microcrystals using synchrotron radiation Gati, Cornelius; Bourenkov, Gleb; Klinge, Marco IUCrJ, Vol. 1, Issue 2 https://doi.org/10.1107/S2052252513033939	journal	February 2014
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
MeshAndCollect : an automated multi-crystal data-collection workflow for synchrotron macromolecular crystallography beamlines Zander, Ulrich; Bourenkov, Gleb; Popov, Alexander N. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 11 https://doi.org/10.1107/S1399004715017927	journal	October 2015
BioCARS: a synchrotron resource for time-resolved X-ray science Graber, T.; Anderson, S.; Brewer, H. Journal of Synchrotron Radiation, Vol. 18, Issue 4 https://doi.org/10.1107/S0909049511009423	journal	May 2011
Developing 100 ps-resolved X-ray structural analysis capabilities on beamline NW14A at the Photon Factory Advanced Ring Nozawa, Shunsuke; Adachi, Shin-ichi; Takahashi, Jun-ichi Journal of Synchrotron Radiation, Vol. 14, Issue 4 https://doi.org/10.1107/S0909049507025496	journal	June 2007
Room-temperature macromolecular serial crystallography using synchrotron radiation Stellato, Francesco; Oberthür, Dominik; Liang, Mengning IUCrJ, Vol. 1, Issue 4, p. 204-212 https://doi.org/10.1107/S2052252514010070	journal	May 2014
Crystallographic data processing for free-electron laser sources White, Thomas A.; Barty, Anton; Stellato, Francesco Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913013620	journal	June 2013
Native phasing of x-ray free-electron laser data for a G protein–coupled receptor Batyuk, Alexander; Galli, Lorenzo; Ishchenko, Andrii Science Advances, Vol. 2, Issue 9 https://doi.org/10.1126/sciadv.1600292	journal	September 2016
Serial femtosecond crystallography: A revolution in structural biology Martin-Garcia, Jose M.; Conrad, Chelsie E.; Coe, Jesse Archives of Biochemistry and Biophysics, Vol. 602 https://doi.org/10.1016/j.abb.2016.03.036	journal	July 2016
Low- Z polymer sample supports for fixed-target serial femtosecond X-ray crystallography Feld, Geoffrey K.; Heymann, Michael; Benner, W. Henry Journal of Applied Crystallography, Vol. 48, Issue 4 https://doi.org/10.1107/S1600576715010493	journal	June 2015
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
Trapping Reaction Intermediates in Macromolecular Crystals for Structural Analyses Stoddard, Barry L. Methods, Vol. 24, Issue 2 https://doi.org/10.1006/meth.2001.1174	journal	June 2001
Serial millisecond crystallography of membrane and soluble protein microcrystals using synchrotron radiation Martin-Garcia, Jose M.; Conrad, Chelsie E.; Nelson, Garrett IUCrJ, Vol. 4, Issue 4, p. 439-454 https://doi.org/10.1107/S205225251700570X	journal	May 2017
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
Towards an understanding of radiation damage in cryocooled macromolecular crystals Nave, Colin; Garman, Elspeth F. Journal of Synchrotron Radiation, Vol. 12, Issue 3 https://doi.org/10.1107/S0909049505007132	journal	April 2005
Complex landscape of protein structural dynamics unveiled by nanosecond Laue crystallography Bourgeois, D.; Vallone, B.; Schotte, F. Proceedings of the National Academy of Sciences, Vol. 100, Issue 15 https://doi.org/10.1073/pnas.1430900100	journal	July 2003
Cooperative macromolecular device revealed by meta-analysis of static and time-resolved structures Ren, Z.; Srajer, V.; Knapp, J. E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 1 https://doi.org/10.1073/pnas.1109213108	journal	December 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
Outrunning free radicals in room-temperature macromolecular crystallography Owen, Robin L.; Axford, Danny; Nettleship, Joanne E. Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 7 https://doi.org/10.1107/S0907444912012553	journal	June 2012
Optimizing the spatial distribution of dose in X-ray macromolecular crystallography Zeldin, Oliver B.; Gerstel, Markus; Garman, Elspeth F. Journal of Synchrotron Radiation, Vol. 20, Issue 1 https://doi.org/10.1107/S0909049512044706	journal	November 2012
Mix-and-diffuse serial synchrotron crystallography Beyerlein, Kenneth R.; Dierksmeyer, Dennis; Mariani, Valerio IUCrJ, Vol. 4, Issue 6 https://doi.org/10.1107/S2052252517013124	journal	October 2017
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 high-transparency, micro-patternable chip for X-ray diffraction analysis of microcrystals under native growth conditions Murray, Thomas D.; Lyubimov, Artem Y.; Ogata, Craig M. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 10 https://doi.org/10.1107/S1399004715015011	journal	September 2015
Structural Basis for Allosteric Regulation of GPCRs by Sodium Ions Liu, W.; Chun, E.; Thompson, A. A. Science, Vol. 337, Issue 6091 https://doi.org/10.1126/science.1219218	journal	July 2012
First operation of a free-electron laser generating GW power radiation at 32 nm wavelength Ayvazyan, V.; Baboi, N.; Bähr, J. The European Physical Journal D, Vol. 37, Issue 2 https://doi.org/10.1140/epjd/e2005-00308-1	journal	November 2005
Ligand migration pathway and protein dynamics in myoglobin: A time-resolved crystallographic study on L29W MbCO Schmidt, M.; Nienhaus, K.; Pahl, R. Proceedings of the National Academy of Sciences, Vol. 102, Issue 33 https://doi.org/10.1073/pnas.0504932102	journal	August 2005
Five-dimensional crystallography Schmidt, Marius; Graber, Tim; Henning, Robert Acta Crystallographica Section A Foundations of Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0108767309054166	journal	February 2010
Global radiation damage: temperature dependence, time dependence and how to outrun it Warkentin, Matthew; Hopkins, Jesse B.; Badeau, Ryan Journal of Synchrotron Radiation, Vol. 20, Issue 1 https://doi.org/10.1107/S0909049512048303	journal	November 2012
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
Mutagenesis and Laue structures of enzyme intermediates: isocitrate dehydrogenase Bolduc, J.; Dyer, D.; Scott, W. Science, Vol. 268, Issue 5215 https://doi.org/10.1126/science.7761851	journal	June 1995
Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser Kupitz, Christopher; Basu, Shibom; Grotjohann, Ingo Nature, Vol. 513, Issue 7517 https://doi.org/10.1038/nature13453	journal	July 2014
Derivatization of Proteinase K with Heavy Atoms Enhances Its Thermal Stability Yazawa, Kenjiro; Sugahara, Michihiro; Yutani, Katsuhide ACS Catalysis, Vol. 6, Issue 5 https://doi.org/10.1021/acscatal.6b00100	journal	April 2016
A statistic for local intensity differences: robustness to anisotropy and pseudo-centering and utility for detecting twinning Padilla, Jennifer E.; Yeates, Todd O. Acta Crystallographica Section D Biological Crystallography, Vol. 59, Issue 7 https://doi.org/10.1107/S0907444903007947	journal	June 2003
Autoindexing diffraction images with iMosflm Powell, Harold R.; Johnson, Owen; Leslie, Andrew G. W. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444912048524	journal	June 2013
Serial millisecond crystallography for routine room-temperature structure determination at synchrotrons Weinert, Tobias; Olieric, Natacha; Cheng, Robert Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00630-4	journal	September 2017
Feasibility and Realization of Single-Pulse Laue Diffraction on Macromolecular Crystals at ESRF Bourgeois, D.; Ursby, T.; Wulff, M. Journal of Synchrotron Radiation, Vol. 3, Issue 2 https://doi.org/10.1107/S090904959501661X	journal	March 1996
Recent developments in CrystFEL White, Thomas A.; Mariani, Valerio; Brehm, Wolfgang Journal of Applied Crystallography, Vol. 49, Issue 2 https://doi.org/10.1107/S1600576716004751	journal	March 2016
X-ray Laue Diffraction from Protein Crystals Moffat, K.; Szebenyi, D.; Bilderback, D. Science, Vol. 223, Issue 4643 https://doi.org/10.1126/science.223.4643.1423	journal	March 1984
From The Cover: Visualizing reaction pathways in photoactive yellow protein from nanoseconds to seconds Ihee, H.; Rajagopal, S.; Srajer, V. Proceedings of the National Academy of Sciences, Vol. 102, Issue 20 https://doi.org/10.1073/pnas.0409035102	journal	May 2005
Picosecond time-resolved X-ray crystallography: probing protein function in real time Schotte, Friedrich; Soman, Jayashree; Olson, John S. Journal of Structural Biology, Vol. 147, Issue 3 https://doi.org/10.1016/j.jsb.2004.06.009	journal	September 2004
Room-temperature serial crystallography at synchrotron X-ray sources using slowly flowing free-standing high-viscosity microstreams Botha, Sabine; Nass, Karol; Barends, Thomas R. M. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 2 https://doi.org/10.1107/S1399004714026327	journal	January 2015
Millisecond X-ray diffraction and the first electron density map from Laue photographs of a protein crystal Hajdu, Janos; Machin, Pella A.; Campbell, John W. Nature, Vol. 329, Issue 6135 https://doi.org/10.1038/329178a0	journal	September 1987
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
Laue diffraction study on the structure of cytochrome c peroxidase compound I Fülöp, Vilmos; Phizackerley, R. Paul; Soltis, S. Michael Structure, Vol. 2, Issue 3 https://doi.org/10.1016/S0969-2126(00)00021-6	journal	March 1994
Allosteric action in real time: Time-resolved crystallographic studies of a cooperative dimeric hemoglobin Knapp, J. E.; Pahl, R.; Srajer, V. Proceedings of the National Academy of Sciences, Vol. 103, Issue 20 https://doi.org/10.1073/pnas.0509411103	journal	May 2006
Millisecond Laue structures of an enzyme–product complex using photocaged substrate analogs Stoddard, Barry L.; Cohen, Bruce E.; Brubaker, Michael Nature Structural Biology, Vol. 5, Issue 10 https://doi.org/10.1038/2331	journal	October 1998
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Progress with Laue diffraction studies on protein and virus crystals Hajdu, Janos; Johnson, Louise N. Biochemistry, Vol. 29, Issue 7 https://doi.org/10.1021/bi00459a001	journal	February 1990
Advances in kinetic protein crystallography Bourgeois, Dominique; Royant, Antoine Current Opinion in Structural Biology, Vol. 15, Issue 5 https://doi.org/10.1016/j.sbi.2005.08.002	journal	October 2005
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
Raster-scanning serial protein crystallography using micro- and nano-focused synchrotron beams Coquelle, Nicolas; Brewster, Aaron S.; Kapp, Ulrike Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 5 https://doi.org/10.1107/S1399004715004514	journal	April 2015
Lipidic cubic phase serial millisecond crystallography using synchrotron radiation Nogly, Przemyslaw; James, Daniel; Wang, Dingjie IUCrJ, Vol. 2, Issue 2, p. 168-176 https://doi.org/10.1107/S2052252514026487	journal	March 2015
Watching a Protein as it Functions with 150-ps Time-Resolved X-ray Crystallography Schotte, F. Science, Vol. 300, Issue 5627 https://doi.org/10.1126/science.1078797	journal	June 2003
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
Using a non-monochromatic microbeam for serial snapshot crystallography Dejoie, Catherine; McCusker, Lynne B.; Baerlocher, Christian Journal of Applied Crystallography, Vol. 46, Issue 3 https://doi.org/10.1107/S0021889813005888	journal	April 2013
Pink-beam serial crystallography Meents, A.; Wiedorn, M. O.; Srajer, V. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01417-3	journal	November 2017
Structure of a Protein Photocycle Intermediate by Millisecond Time-Resolved Crystallography Genick, U. K. Science, Vol. 275, Issue 5305 https://doi.org/10.1126/science.275.5305.1471	journal	March 1997
Mix and Inject: Reaction Initiation by Diffusion for Time-Resolved Macromolecular Crystallography Schmidt, Marius Advances in Condensed Matter Physics, Vol. 2013 https://doi.org/10.1155/2013/167276	journal	January 2013
Room-temperature serial crystallography using a kinetically optimized microfluidic device for protein crystallization and on-chip X-ray diffraction Heymann, Michael; Opthalage, Achini; Wierman, Jennifer L. IUCrJ, Vol. 1, Issue 5 https://doi.org/10.1107/S2052252514016960	journal	August 2014
Iterative-build OMIT maps: map improvement by iterative model building and refinement without model bias Terwilliger, Thomas C.; Grosse-Kunstleve, Ralf W.; Afonine, Pavel V. Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 5 https://doi.org/10.1107/S0907444908004319	journal	April 2008
Synchrotron X-ray data collection and restrained least-squares refinement of the crystal structure of proteinase K at 1.5 Å resolution Betzel, Ch.; Pal, G. P.; Saenger, W. Acta Crystallographica Section B Structural Science, Vol. 44, Issue 2 https://doi.org/10.1107/S010876818700939X	journal	April 1988
MOLREP an Automated Program for Molecular Replacement Vagin, A.; Teplyakov, A. Journal of Applied Crystallography, Vol. 30, Issue 6, p. 1022-1025 https://doi.org/10.1107/S0021889897006766	journal	December 1997
Laue crystallography: coming of age Ren, Zhong; Bourgeois, Dominique; Helliwell, John R. Journal of Synchrotron Radiation, Vol. 6, Issue 4 https://doi.org/10.1107/S0909049599006366	journal	July 1999
Time-resolved X-ray crystallographic study of the conformational change in Ha-Ras p21 protein on GTP hydrolysis Schlichting, Ilme; Almo, Steven C.; Rapp, Gert Nature, Vol. 345, Issue 6273 https://doi.org/10.1038/345309a0	journal	May 1990
Structure of Hen Egg-White Lysozyme: A Three-dimensional Fourier Synthesis at 2 Å Resolution Blake, C. C. F.; Koenig, D. F.; Mair, G. A. Nature, Vol. 206, Issue 4986 https://doi.org/10.1038/206757a0	journal	May 1965
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

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Related Subjects

36 MATERIALS SCIENCE
lipidic cubic phase
pink beam
protein dynamics
serial crystallography
time-resolved
third-generation synchrotrons
injector-based serial crystallography
structure determination
membrane proteins
protein structures
X-ray crystallography
structural biology