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

Abstract

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 A2A adenosine receptor (A2AAR), 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 A2AAR,more » phycocyanin, Flpp3, proteinase K and lysozyme, and the structures of A2AAR, 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.« less

Authors:
ORCiD logo [1];  [2];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [3];  [3];  [3];  [4];  [1];  [1];  [1];  [1];  [1]; ORCiD logo [5];  [1] more »;  [3];  [3];  [3];  [3];  [1];  [1];  [4];  [1];  [3];  [1] « less
+ Show Author Affiliations
  1. Arizona State Univ., Tempe, AZ (United States)
  2. Arizona State Univ., Tempe, AZ (United States); National Cancer Institute, Frederick, MD (United States)
  3. Argonne National Lab. (ANL), Lemont, IL (United States)
  4. Univ. of Southern California, Los Angeles, CA (United States)
  5. Paul Scherrer Inst. (PSI), Villigen (Switzerland)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Science Foundation (NSF); National Institutes of Health (NIH), National Cancer Institute; National Institutes of Health (NIH); USDOE
OSTI Identifier:
1374440
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
IUCrJ
Additional Journal Information:
Journal Volume: 4; Journal Issue: 4; Journal ID: ISSN 2052-2525
Publisher:
International Union of Crystallography
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 46 INSTRUMENTATION RELATED TO NUCLEAR SCIENCE AND TECHNOLOGY; serial millisecond crystallography; synchrotron radiation; Advanced Photon Source; high-viscosity injector

Citation Formats

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., and Liu, Wei. Serial millisecond crystallography of membrane and soluble protein microcrystals using synchrotron radiation. United States: N. p., 2017. Web. doi:10.1107/S205225251700570X.
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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. Serial millisecond crystallography of membrane and soluble protein microcrystals using synchrotron radiation. United States. https://doi.org/10.1107/S205225251700570X
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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., and Liu, Wei. Wed . "Serial millisecond crystallography of membrane and soluble protein microcrystals using synchrotron radiation". United States. https://doi.org/10.1107/S205225251700570X. https://www.osti.gov/servlets/purl/1374440.
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@article{osti_1374440,
title = {Serial millisecond crystallography of membrane and soluble protein microcrystals using synchrotron radiation},
author = {Martin-Garcia, Jose M. and Conrad, Chelsie E. and Nelson, Garrett and Stander, Natasha and Zatsepin, Nadia A. and Zook, James and Zhu, Lan and Geiger, James and Chun, Eugene and Kissick, David and Hilgart, Mark C. and Ogata, Craig and Ishchenko, Andrii and Nagaratnam, Nirupa and Roy-Chowdhury, Shatabdi and Coe, Jesse and Subramanian, Ganesh and Schaffer, Alexander and James, Daniel and Ketwala, Gihan and Venugopalan, Nagarajan and Xu, Shenglan and Corcoran, Stephen and Ferguson, Dale and Weierstall, Uwe and Spence, John C. H. and Cherezov, Vadim and Fromme, Petra and Fischetti, Robert F. and Liu, Wei},
abstractNote = {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 A2A adenosine receptor (A2AAR), 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 A2AAR, phycocyanin, Flpp3, proteinase K and lysozyme, and the structures of A2AAR, 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.},
doi = {10.1107/S205225251700570X},
journal = {IUCrJ},
number = 4,
volume = 4,
place = {United States},
year = {Wed May 24 00:00:00 EDT 2017},
month = {Wed May 24 00:00:00 EDT 2017}
}
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  • Springer Science and Business Media LLC
  • DOI: 10.17863/cam.52320

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)
  • DOI: 10.17863/cam.52329

Genome-Wide Identification of Francisella tularensis Virulence Determinants
text, January 2007

  • J. -R., Zhang,; J., Yang,; A., Banas, J.
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/thcx-v290

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
  • DOI: 10.17863/cam.45787

Serial femtosecond crystallography of soluble proteins in lipidic cubic phase
text, January 2015

  • Fromme, Raimund; Ishchenko, Andrii; Metz, Markus
  • Deutsches Elektronen-Synchrotron, DESY, Hamburg
  • DOI: 10.3204/pubdb-2015-04280

Allosteric sodium in class A GPCR signaling
text, January 2014

  • Vsevolod, Katritch,; Vadim, Cherezov,; C., Stevens, Raymond
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/5vt2-kp93
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