Serial millisecond crystallography of membrane and soluble protein microcrystals using synchrotron radiation

Martin-Garcia, Jose M.; Conrad, Chelsie E.; Nelson, Garrett; Stander, Natasha; Zatsepin, Nadia A.; Zook, James; Zhu, Lan; Geiger, James; Chun, Eugene; Kissick, David; Hilgart, Mark C.; Ogata, Craig; Ishchenko, Andrii; Nagaratnam, Nirupa; Roy-Chowdhury, Shatabdi; Coe, Jesse; Subramanian, Ganesh; Schaffer, Alexander; James, Daniel; Ketwala, Gihan; Venugopalan, Nagarajan; Xu, Shenglan; Corcoran, Stephen; Ferguson, Dale; Weierstall, Uwe; Spence, John C. H.; Cherezov, Vadim; Fromme, Petra; Fischetti, Robert F.; Liu, Wei

doi:10.1107/S205225251700570X

Title: Serial millisecond crystallography of membrane and soluble protein microcrystals using synchrotron radiation

Journal Article · Wed May 24 00:00:00 EDT 2017 · IUCrJ

DOI:https://doi.org/10.1107/S205225251700570X· OSTI ID:1374440

^[1]; Conrad, Chelsie E. ^[2]; Nelson, Garrett ^[1]; Stander, Natasha ^[1]; Zatsepin, Nadia A. ^[1]; Zook, James ^[1]; Zhu, Lan ^[1]; Geiger, James ^[1]; Chun, Eugene ^[1]; Kissick, David ^[3]; Hilgart, Mark C. ^[3]; Ogata, Craig ^[3]; Ishchenko, Andrii ^[4]; Nagaratnam, Nirupa ^[1]; Roy-Chowdhury, Shatabdi ^[1]; Coe, Jesse ^[1]; Subramanian, Ganesh ^[1]; Schaffer, Alexander ^[1];

^[5]; Ketwala, Gihan ^[1] more »

Arizona State Univ., Tempe, AZ (United States)
Arizona State Univ., Tempe, AZ (United States); National Cancer Institute, Frederick, MD (United States)
Argonne National Lab. (ANL), Lemont, IL (United States)
Univ. of Southern California, Los Angeles, CA (United States)
Paul Scherrer Inst. (PSI), Villigen (Switzerland)

Crystal structure determination of biological macromolecules using the novel technique of serial femtosecond crystallography (SFX) is severely limited by the scarcity of X-ray free-electron laser (XFEL) sources. However, recent and future upgrades render microfocus beamlines at synchrotron-radiation sources suitable for room-temperature serial crystallography data collection also. Owing to the longer exposure times that are needed at synchrotrons, serial data collection is termed serial millisecond crystallography (SMX). As a result, the number of SMX experiments is growing rapidly, with a dozen experiments reported so far. Here, the first high-viscosity injector-based SMX experiments carried out at a US synchrotron source, the Advanced Photon Source (APS), are reported. Microcrystals (5–20 µm) of a wide variety of proteins, including lysozyme, thaumatin, phycocyanin, the human A_2A adenosine receptor (A_2AAR), the soluble fragment of the membrane lipoprotein Flpp3 and proteinase K, were screened. Crystals suspended in lipidic cubic phase (LCP) or a high-molecular-weight poly(ethylene oxide) (PEO; molecular weight 8 000 000) were delivered to the beam using a high-viscosity injector. In-house data-reduction (hit-finding) software developed at APS as well as the SFX data-reduction and analysis software suites Cheetah and CrystFEL enabled efficient on-site SMX data monitoring, reduction and processing. Complete data sets were collected for A_2AAR, phycocyanin, Flpp3, proteinase K and lysozyme, and the structures of A_2AAR, phycocyanin, proteinase K and lysozyme were determined at 3.2, 3.1, 2.65 and 2.05 Å resolution, respectively. The data demonstrate the feasibility of serial millisecond crystallography from 5–20 µm crystals using a high-viscosity injector at APS. The resolution of the crystal structures obtained in this study was dictated by the current flux density and crystal size, but upcoming developments in beamline optics and the planned APS-U upgrade will increase the intensity by two orders of magnitude. Furthermore, these developments will enable structure determination from smaller and/or weakly diffracting microcrystals.

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

Sponsoring Organization:: National Science Foundation (NSF); National Institutes of Health (NIH), National Cancer Institute; National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1374440

Journal Information:: IUCrJ, Vol. 4, Issue 4; ISSN 2052-2525

Publisher:: International Union of CrystallographyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 106 works

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The serial millisecond crystallography instrument at the Australian Synchrotron incorporating the “Lipidico” injector Berntsen, P.; Hadian Jazi, M.; Kusel, M. Review of Scientific Instruments, Vol. 90, Issue 8 https://doi.org/10.1063/1.5104298	journal	August 2019
Advances and opportunities in ultrafast X-ray crystallography and ultrafast structural optical crystallography of nuclear and electronic protein dynamics van Thor, Jasper J. Structural Dynamics, Vol. 6, Issue 5 https://doi.org/10.1063/1.5110685	journal	September 2019
Transforming X-ray detection with hybrid photon counting detectors Förster, Andreas; Brandstetter, Stefan; Schulze-Briese, Clemens Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 377, Issue 2147 https://doi.org/10.1098/rsta.2018.0241	journal	April 2019
Successful sample preparation for serial crystallography experiments Beale, John H.; Bolton, Rachel; Marshall, Stephen A. Journal of Applied Crystallography, Vol. 52, Issue 6 https://doi.org/10.1107/s1600576719013517	journal	November 2019
Stable sample delivery in viscous media via a capillary for serial crystallography Nam, Ki Hyun Journal of Applied Crystallography, Vol. 53, Issue 1 https://doi.org/10.1107/s1600576719014985	journal	February 2020
Toward G protein-coupled receptor structure-based drug design using X-ray lasers Ishchenko, Andrii; Stauch, Benjamin; Han, Gye Won IUCrJ, Vol. 6, Issue 6 https://doi.org/10.1107/s2052252519013137	journal	October 2019
Measuring energy-dependent photoelectron escape in microcrystals Storm, Selina L. S.; Crawshaw, Adam D.; Devenish, Nicholas E. IUCrJ, Vol. 7, Issue 1 https://doi.org/10.1107/s2052252519016178	journal	January 2020
Sample delivery for serial crystallography at free-electron lasers and synchrotrons Grünbein, Marie Luise; Nass Kovacs, Gabriela Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2 https://doi.org/10.1107/s205979831801567x	journal	January 2019
A guide to sample delivery systems for serial crystallography Zhao, Feng‐Zhu; Zhang, Bin; Yan, Er‐Kai The FEBS Journal, Vol. 286, Issue 22 https://doi.org/10.1111/febs.15099	journal	August 2019
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Polysaccharide-Based Injection Matrix for Serial Crystallography Nam, Ki Hyun International Journal of Molecular Sciences, Vol. 21, Issue 9 https://doi.org/10.3390/ijms21093332	journal	May 2020
Multi-wavelength anomalous diffraction de novo phasing using a two-colour X-ray free-electron laser with wide tunability Gorel, Alexander; Motomura, Koji; Fukuzawa, Hironobu Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00754-7	journal	October 2017
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A shared vision for macromolecular crystallography over the next five years Förster, Andreas; Schulze-Briese, Clemens Structural Dynamics, Vol. 6, Issue 6 https://doi.org/10.1063/1.5131017	journal	November 2019
An outlook on using serial femtosecond crystallography in drug discovery Mishin, Alexey; Gusach, Anastasiia; Luginina, Aleksandra Expert Opinion on Drug Discovery, Vol. 14, Issue 9 https://doi.org/10.1080/17460441.2019.1626822	journal	May 2019
MicroED methodology and development Nannenga, Brent L. Acta Crystallographica Section A Foundations and Advances, Vol. 75, Issue a1 https://doi.org/10.1107/s0108767319098763	journal	July 2019
Fixed-target serial oscillation crystallography at room temperature Wierman, Jennifer L.; Paré-Labrosse, Olivier; Sarracini, Antoine IUCrJ, Vol. 6, Issue 2 https://doi.org/10.1107/S2052252519001453	journal	February 2019
Role of Extracellular Loops and Membrane Lipids for Ligand Recognition in the Neuronal Adenosine Receptor Type 2A: An Enhanced Sampling Simulation Study Cao, Ruyin; Giorgetti, Alejandro; Bauer, Andreas Molecules, Vol. 23, Issue 10 https://doi.org/10.3390/molecules23102616	journal	October 2018
MicroED methodology and development Nannenga, Brent L. Structural Dynamics, Vol. 7, Issue 1 https://doi.org/10.1063/1.5128226	journal	January 2020
Shortening injection matrix for serial crystallography Nam, Ki Hyun https://doi.org/10.1101/687640	posted_content	July 2019
Sample manipulation and data assembly for robust microcrystal synchrotron crystallography Liu, Qun; Guo, Gongrui; Fuchs, Martin R. Acta Crystallographica Section A Foundations and Advances, Vol. 74, Issue a1 https://doi.org/10.1107/s0108767318096046	journal	July 2018
Fixed-target serial oscillation crystallography at room temperature Wierman, Jennifer L.; Paré-Labrosse, Olivier; Sarracini, Antoine International Union of Crystallography (IUCr) https://doi.org/10.1107/s2052252519001453/mf5030sup2.mp4	text	January 2019
Comparing serial X-ray crystallography and microcrystal electron diffraction (MicroED) as methods for routine structure determination from small macromolecular crystals Wolff, Alexander M.; Young, Iris D.; Sierra, Raymond G. IUCrJ, Vol. 7, Issue 2 https://doi.org/10.1107/s205225252000072x	journal	February 2020
Shortening injection matrix for serial crystallography Nam, Ki Hyun Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-019-56135-1	journal	January 2020
High-viscosity injector-based pink-beam serial crystallography of microcrystals at a synchrotron radiation source Martin-Garcia, Jose M.; Zhu, Lan; Mendez, Derek International Union of Crystallography (IUCr) https://doi.org/10.1107/s205225251900263x/ti5014sup1.pdf	text	January 2019
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
Fixed-target serial oscillation crystallography at room temperature Wierman, Jennifer L.; Paré-Labrosse, Olivier; Sarracini, Antoine International Union of Crystallography (IUCr) https://doi.org/10.1107/s2052252519001453/mf5030sup1.pdf	text	January 2019

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