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Title: Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser

Abstract

To understand how molecules function in biological systems, new methods are required to obtain atomic resolution structures from biological material under physiological conditions. Intense femtosecond-duration pulses from X-ray free-electron lasers (XFELs) can outrun most damage processes, vastly increasing the tolerable dose before the specimen is destroyed. This in turn allows structure determination from crystals much smaller and more radiation sensitive than previously considered possible, allowing data collection from room temperature structures and avoiding structural changes due to cooling. Regardless, high-resolution structures obtained from XFEL data mostly use crystals far larger than 1 μm3 in volume, whereas the X-ray beam is often attenuated to protect the detector from damage caused by intense Bragg spots. Here, we describe the 2 Å resolution structure of native nanocrystalline granulovirus occlusion bodies (OBs) that are less than 0.016 μm3 in volume using the full power of the Linac Coherent Light Source (LCLS) and a dose up to 1.3 GGy per crystal. The crystalline shell of granulovirus OBs consists, on average, of about 9,000 unit cells, representing the smallest protein crystals to yield a high-resolution structure by X-ray crystallography to date. The XFEL structure shows little to no evidence of radiation damage and is more completemore » than a model determined using synchrotron data from recombinantly produced, much larger, cryocooled granulovirus granulin microcrystals. Furthermore, our measurements suggest that it should be possible, under ideal experimental conditions, to obtain data from protein crystals with only 100 unit cells in volume using currently available XFELs and suggest that single-molecule imaging of individual biomolecules could almost be within reach.« less

Authors:
 [1];  [2];  [2]; ORCiD logo [3];  [2];  [4];  [4];  [5];  [6];  [5];  [2];  [7];  [8];  [9];  [10];  [11];  [2];  [11];  [11];  [12] more »;  [13];  [14];  [15];  [11];  [13];  [16];  [11];  [2];  [17];  [11];  [11];  [11];  [18];  [19];  [4];  [2]; ORCiD logo [20] « less
  1. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); MRC Lab. of Molecular Biology, Cambridge (United Kingdom)
  2. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany)
  3. The Univ. of Auckland, Auckland (New Zealand); Friedrich Miescher Institute for Biomedical Research, Basel (Switzerland)
  4. The Univ. of Auckland, Auckland (New Zealand)
  5. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); European XFEL GmbH, Hamburg (Germany)
  6. Arizona State Univ., Tempe, AZ (United States); Paul Scherrer Inst. (PSI), Villigen (Switzerland)
  7. Max Planck Institute for Medical Research, Heidelberg (Germany); Univ. of Hamburg, Hamburg (Germany)
  8. SLAC National Accelerator Lab., Menlo Park, CA (United States)
  9. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); SLAC National Accelerator Lab., Menlo Park, CA (United States)
  10. Arizona State Univ., Tempe, AZ (United States); Max Planck Institute for Medical Research, Heidelberg (Germany)
  11. Arizona State Univ., Tempe, AZ (United States)
  12. Arizona State Univ., Tempe, AZ (United States); Univ. of Wisconsin-Milwaukee, Milwaukee, WI (United States)
  13. Max Planck Institute for Medical Research, Heidelberg (Germany)
  14. SLAC National Accelerator Lab., Menlo Park, CA (United States); National Science Foundation BioXFEL Science and Technology Center, Buffalo, NY (United States)
  15. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); Paul Scherrer Inst. (PSI), Villigen (Switzerland)
  16. Arizona State Univ., Tempe, AZ (United States); ShanghaiTech Univ., Shanghai (China)
  17. SLAC National Accelerator Lab., Menlo Park, CA (United States); Brookhaven National Lab. (BNL), Upton, NY (United States)
  18. Univ. Basel, Basel (Switzerland)
  19. Julius Kuehn Institute (JKI), Darmstadt (Germany)
  20. Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany); Univ. of Hamburg, Hamburg (Germany)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1353189
Grant/Contract Number:  
617095583; UOA1221; AC02-76SF00515
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 114; Journal Issue: 9; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; XFEL; nanocrystals; structural biology; bioimaging; SFX

Citation Formats

Gati, Cornelius, Oberthuer, Dominik, Yefanov, Oleksandr, Bunker, Richard D., Stellato, Francesco, Chiu, Elaine, Yeh, Shin -Mei, Aquila, Andrew, Basu, Shibom, Bean, Richard, Beyerlein, Kenneth R., Botha, Sabine, Boutet, Sebastien, DePonte, Daniel P., Doak, R. Bruce, Fromme, Raimund, Galli, Lorenzo, Grotjohann, Ingo, James, Daniel R., Kupitz, Christopher, Lomb, Lukas, Messerschmidt, Marc, Nass, Karol, Rendek, Kimberly, Shoeman, Robert L., Wang, Dingjie, Weierstall, Uwe, White, Thomas A., Williams, Garth J., Zatsepin, Nadia A., Fromme, Petra, Spence, John C. H., Goldie, Kenneth N., Jehle, Johannes A., Metcalf, Peter, Barty, Anton, and Chapman, Henry N. Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser. United States: N. p., 2017. Web. https://doi.org/10.1073/pnas.1609243114.
Gati, Cornelius, Oberthuer, Dominik, Yefanov, Oleksandr, Bunker, Richard D., Stellato, Francesco, Chiu, Elaine, Yeh, Shin -Mei, Aquila, Andrew, Basu, Shibom, Bean, Richard, Beyerlein, Kenneth R., Botha, Sabine, Boutet, Sebastien, DePonte, Daniel P., Doak, R. Bruce, Fromme, Raimund, Galli, Lorenzo, Grotjohann, Ingo, James, Daniel R., Kupitz, Christopher, Lomb, Lukas, Messerschmidt, Marc, Nass, Karol, Rendek, Kimberly, Shoeman, Robert L., Wang, Dingjie, Weierstall, Uwe, White, Thomas A., Williams, Garth J., Zatsepin, Nadia A., Fromme, Petra, Spence, John C. H., Goldie, Kenneth N., Jehle, Johannes A., Metcalf, Peter, Barty, Anton, & Chapman, Henry N. Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser. United States. https://doi.org/10.1073/pnas.1609243114
Gati, Cornelius, Oberthuer, Dominik, Yefanov, Oleksandr, Bunker, Richard D., Stellato, Francesco, Chiu, Elaine, Yeh, Shin -Mei, Aquila, Andrew, Basu, Shibom, Bean, Richard, Beyerlein, Kenneth R., Botha, Sabine, Boutet, Sebastien, DePonte, Daniel P., Doak, R. Bruce, Fromme, Raimund, Galli, Lorenzo, Grotjohann, Ingo, James, Daniel R., Kupitz, Christopher, Lomb, Lukas, Messerschmidt, Marc, Nass, Karol, Rendek, Kimberly, Shoeman, Robert L., Wang, Dingjie, Weierstall, Uwe, White, Thomas A., Williams, Garth J., Zatsepin, Nadia A., Fromme, Petra, Spence, John C. H., Goldie, Kenneth N., Jehle, Johannes A., Metcalf, Peter, Barty, Anton, and Chapman, Henry N. Wed . "Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser". United States. https://doi.org/10.1073/pnas.1609243114. https://www.osti.gov/servlets/purl/1353189.
@article{osti_1353189,
title = {Atomic structure of granulin determined from native nanocrystalline granulovirus using an X-ray free-electron laser},
author = {Gati, Cornelius and Oberthuer, Dominik and Yefanov, Oleksandr and Bunker, Richard D. and Stellato, Francesco and Chiu, Elaine and Yeh, Shin -Mei and Aquila, Andrew and Basu, Shibom and Bean, Richard and Beyerlein, Kenneth R. and Botha, Sabine and Boutet, Sebastien and DePonte, Daniel P. and Doak, R. Bruce and Fromme, Raimund and Galli, Lorenzo and Grotjohann, Ingo and James, Daniel R. and Kupitz, Christopher and Lomb, Lukas and Messerschmidt, Marc and Nass, Karol and Rendek, Kimberly and Shoeman, Robert L. and Wang, Dingjie and Weierstall, Uwe and White, Thomas A. and Williams, Garth J. and Zatsepin, Nadia A. and Fromme, Petra and Spence, John C. H. and Goldie, Kenneth N. and Jehle, Johannes A. and Metcalf, Peter and Barty, Anton and Chapman, Henry N.},
abstractNote = {To understand how molecules function in biological systems, new methods are required to obtain atomic resolution structures from biological material under physiological conditions. Intense femtosecond-duration pulses from X-ray free-electron lasers (XFELs) can outrun most damage processes, vastly increasing the tolerable dose before the specimen is destroyed. This in turn allows structure determination from crystals much smaller and more radiation sensitive than previously considered possible, allowing data collection from room temperature structures and avoiding structural changes due to cooling. Regardless, high-resolution structures obtained from XFEL data mostly use crystals far larger than 1 μm3 in volume, whereas the X-ray beam is often attenuated to protect the detector from damage caused by intense Bragg spots. Here, we describe the 2 Å resolution structure of native nanocrystalline granulovirus occlusion bodies (OBs) that are less than 0.016 μm3 in volume using the full power of the Linac Coherent Light Source (LCLS) and a dose up to 1.3 GGy per crystal. The crystalline shell of granulovirus OBs consists, on average, of about 9,000 unit cells, representing the smallest protein crystals to yield a high-resolution structure by X-ray crystallography to date. The XFEL structure shows little to no evidence of radiation damage and is more complete than a model determined using synchrotron data from recombinantly produced, much larger, cryocooled granulovirus granulin microcrystals. Furthermore, our measurements suggest that it should be possible, under ideal experimental conditions, to obtain data from protein crystals with only 100 unit cells in volume using currently available XFELs and suggest that single-molecule imaging of individual biomolecules could almost be within reach.},
doi = {10.1073/pnas.1609243114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 9,
volume = 114,
place = {United States},
year = {2017},
month = {2}
}

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Figures / Tables:

Figure 1 Figure 1: Granulovirus OBs contain a single virion surrounded by a crystalline protein layer that diffracts to high resolution. (A) Powder X-ray diffraction from a pellet of granulovirus OBs at 100 K (Materials and Methods). Protein diffraction rings extend to a resolution between 3 and 3.5 Å. The detector panelsmore » on the left with enhanced contrast show evidence of diffraction at even higher resolution. Resolution rings are shown at 4, 3.5, and 3 Å. (B) Freeze etch electron micrograph showing the uniform size distribution of the particles (Materials and Methods). (C) Cryo-EM. The sequence of four 20 e/Å2 exposures shows the effects of radiation damage on granulovirus OBs. The crystalline lattice is visible only in the first image and hydrogen gas bubbles produced by radiolysis eventually reveal the virion. (Scale bar, 100 nm.)« less

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Works referenced in this record:

Temperature-dependent radiation sensitivity and order of 70S ribosome crystals
journal, October 2014

  • Warkentin, Matthew; Hopkins, Jesse B.; Haber, Jonah B.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 11
  • DOI: 10.1107/S1399004714017672

Cheetah : software for high-throughput reduction and analysis of serial femtosecond X-ray diffraction data
journal, May 2014

  • Barty, Anton; Kirian, Richard A.; Maia, Filipe R. N. C.
  • Journal of Applied Crystallography, Vol. 47, Issue 3
  • DOI: 10.1107/S1600576714007626

Linking Crystallographic Model and Data Quality
journal, May 2012


CrystFEL : a software suite for snapshot serial crystallography
journal, March 2012

  • White, Thomas A.; Kirian, Richard A.; Martin, Andrew V.
  • Journal of Applied Crystallography, Vol. 45, Issue 2
  • DOI: 10.1107/S0021889812002312

Overview of the CCP 4 suite and current developments
journal, March 2011

  • Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
  • DOI: 10.1107/S0907444910045749

Crystallographic data processing for free-electron laser sources
journal, June 2013

  • White, Thomas A.; Barty, Anton; Stellato, Francesco
  • Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7
  • DOI: 10.1107/S0907444913013620

Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard
journal, December 2007

  • Terwilliger, Thomas C.; Grosse-Kunstleve, Ralf W.; Afonine, Pavel V.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 1
  • DOI: 10.1107/S090744490705024X

Ultrafast self-gating Bragg diffraction of exploding nanocrystals in an X-ray laser
journal, January 2015

  • Caleman, Carl; Tîmneanu, Nicuşor; Martin, Andrew V.
  • Optics Express, Vol. 23, Issue 2
  • DOI: 10.1364/OE.23.001213

High-Resolution Protein Structure Determination by Serial Femtosecond Crystallography
journal, May 2012


Structure of CPV17 polyhedrin determined by the improved analysis of serial femtosecond crystallographic data
journal, March 2015

  • Ginn, Helen M.; Messerschmidt, Marc; Ji, Xiaoyun
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms7435

Femtosecond protein nanocrystallography—data analysis methods
journal, January 2010

  • Kirian, Richard A.; Wang, Xiaoyu; Weierstall, Uwe
  • Optics Express, Vol. 18, Issue 6
  • DOI: 10.1364/OE.18.005713

Femtosecond X-ray protein nanocrystallography
journal, February 2011

  • Chapman, Henry N.; Fromme, Petra; Barty, Anton
  • Nature, Vol. 470, Issue 7332, p. 73-77
  • DOI: 10.1038/nature09750

Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012

  • Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel
  • Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4
  • DOI: 10.1107/S0907444912001308

Injector for scattering measurements on fully solvated biospecies
journal, March 2012

  • Weierstall, U.; Spence, J. C. H.; Doak, R. B.
  • Review of Scientific Instruments, Vol. 83, Issue 3
  • DOI: 10.1063/1.3693040

How good are my data and what is the resolution?
journal, June 2013

  • Evans, Philip R.; Murshudov, Garib N.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7
  • DOI: 10.1107/S0907444913000061

Breaking the indexing ambiguity in serial crystallography
journal, December 2013

  • Brehm, Wolfgang; Diederichs, Kay
  • Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 1
  • DOI: 10.1107/S1399004713025431

The atomic structure of baculovirus polyhedra reveals the independent emergence of infectious crystals in DNA and RNA viruses
journal, December 2009

  • Coulibaly, Fasséli; Chiu, Elaine; Gutmann, Sascha
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 52
  • DOI: 10.1073/pnas.0910686106

Beam-induced motion correction for sub-megadalton cryo-EM particles
journal, August 2014


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
  • DOI: 10.1038/35021099

Baculovirus resistance in codling moth is virus isolate-dependent and the consequence of a mutation in viral gene pe38
journal, October 2014

  • Gebhardt, M. M.; Eberle, K. E.; Radtke, P.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 44
  • DOI: 10.1073/pnas.1411089111

XDS
journal, January 2010

  • Kabsch, Wolfgang
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
  • DOI: 10.1107/S0907444909047337

Inference of Macromolecular Assemblies from Crystalline State
journal, September 2007


Recent developments in CrystFEL
journal, March 2016

  • White, Thomas A.; Mariani, Valerio; Brehm, Wolfgang
  • Journal of Applied Crystallography, Vol. 49, Issue 2
  • DOI: 10.1107/S1600576716004751

Self-terminating diffraction gates femtosecond X-ray nanocrystallography measurements
journal, December 2011


Structure of the Angiotensin Receptor Revealed by Serial Femtosecond Crystallography
journal, May 2015


Radiation damage in protein serial femtosecond crystallography using an x-ray free-electron laser
journal, December 2011


Radiation damage in macromolecular crystallography: what is it and why should we care?
journal, March 2010

  • Garman, Elspeth F.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
  • DOI: 10.1107/S0907444910008656

Generation of Steady Liquid Microthreads and Micron-Sized Monodisperse Sprays in Gas Streams
journal, January 1998


Liquid explosions induced by X-ray laser pulses
journal, May 2016

  • Stan, Claudiu A.; Milathianaki, Despina; Laksmono, Hartawan
  • Nature Physics, Vol. 12, Issue 10
  • DOI: 10.1038/nphys3779

MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009

  • Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
  • DOI: 10.1107/S0907444909042073

Features and development of Coot
journal, March 2010

  • Emsley, P.; Lohkamp, B.; Scott, W. G.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
  • DOI: 10.1107/S0907444910007493

Ultratight crystal packing of a 10 kDa protein
journal, February 2013

  • Trillo-Muyo, Sergio; Jasilionis, Andrius; Domagalski, Marcin J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 3
  • DOI: 10.1107/S0907444912050135

An assessment of the resolution limitation due to radiation-damage in X-ray diffraction microscopy
journal, March 2009

  • Howells, M. R.; Beetz, T.; Chapman, H. N.
  • Journal of Electron Spectroscopy and Related Phenomena, Vol. 170, Issue 1-3
  • DOI: 10.1016/j.elspec.2008.10.008

Impact of hollow-atom formation on coherent x-ray scattering at high intensity
journal, March 2011


PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010

  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
  • DOI: 10.1107/S0907444909052925

The CSPAD megapixel x-ray camera at LCLS
conference, October 2012

  • Hart, Philip; Boutet, Sébastien; Carini, Gabriella
  • SPIE Optical Engineering + Applications, SPIE Proceedings
  • DOI: 10.1117/12.930924

Indications of radiation damage in ferredoxin microcrystals using high-intensity X-FEL beams
journal, February 2015

  • Nass, Karol; Foucar, Lutz; Barends, Thomas R. M.
  • Journal of Synchrotron Radiation, Vol. 22, Issue 2
  • DOI: 10.1107/S1600577515002349

Femtosecond crystallography of membrane proteins in the lipidic cubic phase
journal, July 2014

  • Liu, Wei; Wacker, Daniel; Wang, Chong
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647
  • DOI: 10.1098/rstb.2013.0314

The linac coherent light source single particle imaging road map
journal, July 2015

  • Aquila, A.; Barty, A.; Bostedt, C.
  • Structural Dynamics, Vol. 2, Issue 4
  • DOI: 10.1063/1.4918726

Diffraction before destruction
journal, July 2014

  • Chapman, Henry N.; Caleman, Carl; Timneanu, Nicusor
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647
  • DOI: 10.1098/rstb.2013.0313

How baculovirus polyhedra fit square pegs into round holes to robustly package viruses
journal, December 2009


An anti-settling sample delivery instrument for serial femtosecond crystallography
journal, July 2012

  • Lomb, Lukas; Steinbrener, Jan; Bari, Sadia
  • Journal of Applied Crystallography, Vol. 45, Issue 4
  • DOI: 10.1107/S0021889812024557

Gas dynamic virtual nozzle for generation of microscopic droplet streams
journal, September 2008

  • DePonte, D. P.; Weierstall, U.; Schmidt, K.
  • Journal of Physics D: Applied Physics, Vol. 41, Issue 19, Article No. 195505
  • DOI: 10.1088/0022-3727/41/19/195505

Phaser crystallographic software
journal, July 2007

  • McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
  • Journal of Applied Crystallography, Vol. 40, Issue 4
  • DOI: 10.1107/S0021889807021206

A beginner's guide to radiation damage
journal, February 2009


Natively Inhibited Trypanosoma brucei Cathepsin B Structure Determined by Using an X-ray Laser
journal, November 2012


    Works referencing / citing this record:

    Pink-beam serial crystallography
    journal, November 2017


    Megahertz serial crystallography
    journal, October 2018


    3D printed nozzles on a silicon fluidic chip
    journal, March 2019

    • Bohne, Sven; Heymann, Michael; Chapman, Henry N.
    • Review of Scientific Instruments, Vol. 90, Issue 3
    • DOI: 10.1063/1.5080428

    Megahertz serial crystallography
    text, January 2018

    • Wiedorn, Max O.; Oberthür, Dominik; Bean, Richard
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
    • DOI: 10.3204/pubdb-2018-03102

    3D printed nozzles on a silicon fluidic chip
    text, January 2019

    • Chapman, Henry N.; Trieu, Hoc Khiem; Bajt, Sasa
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
    • DOI: 10.3204/pubdb-2019-01297

    Pink-beam serial crystallography
    journal, November 2017


    3D printed nozzles on a silicon fluidic chip
    journal, March 2019

    • Bohne, Sven; Heymann, Michael; Chapman, Henry N.
    • Review of Scientific Instruments, Vol. 90, Issue 3
    • DOI: 10.1063/1.5080428

    Megahertz serial crystallography
    text, January 2018

    • Wiedorn, Max O.; Oberthür, Dominik; Bean, Richard
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
    • DOI: 10.3204/pubdb-2018-03705

    Multi-wavelength anomalous diffraction de novo phasing using a two-colour X-ray free-electron laser with wide tunability
    journal, October 2017


    Ultracompact 3D microfluidics for time-resolved structural biology
    journal, January 2020


    Evaluation of serial crystallographic structure determination within megahertz pulse trains
    journal, November 2019

    • Yefanov, Oleksandr; Oberthür, Dominik; Bean, Richard
    • Structural Dynamics, Vol. 6, Issue 6
    • DOI: 10.1063/1.5124387

    Controlled beams of shock-frozen, isolated, biological and artificial nanoparticles
    journal, March 2020

    • Samanta, Amit K.; Amin, Muhamed; Estillore, Armando D.
    • Structural Dynamics, Vol. 7, Issue 2
    • DOI: 10.1063/4.0000004

    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
    • DOI: 10.1107/s0108767318095570

    Structure-factor amplitude reconstruction from serial femtosecond crystallography of two-dimensional membrane-protein crystals
    journal, January 2019


    Where is crystallography going?
    journal, February 2018

    • Grimes, Jonathan M.; Hall, David R.; Ashton, Alun W.
    • Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 2
    • DOI: 10.1107/s2059798317016709

    Sample delivery for serial crystallography at free-electron lasers and synchrotrons
    journal, January 2019

    • Grünbein, Marie Luise; Nass Kovacs, Gabriela
    • Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2
    • DOI: 10.1107/s205979831801567x

    Radiation damage in protein crystallography at X-ray free-electron lasers
    journal, January 2019


      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.