Intermolecular correlations are necessary to explain diffuse scattering from protein crystals

Peck, Ariana; Poitevin, Frederic; Lane, Thomas Joseph

doi:10.1107/S2052252518001124

Title: Intermolecular correlations are necessary to explain diffuse scattering from protein crystals

Journal Article · 20 February 2018 · IUCrJ

DOI: https://doi.org/10.1107/S2052252518001124 · OSTI ID:1417038

Peck, Ariana ^[1]; Poitevin, Frederic ^[2]; Lane, Thomas Joseph ^[3]

Stanford Univ., CA (United States). Dept. of Biochemistry; SLAC National Accelerator Laboratory
Stanford Univ., CA (United States). Dept. of Structural Biology; SLAC National Accelerator Lab., Menlo Park, CA (United States). Photon Ultrafast Laser Science and Engineering Inst. (PULSE)
SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS) and Bioscience Division

Conformational changes drive protein function, including catalysis, allostery, and signaling. X-ray diffuse scattering from protein crystals has frequently been cited as a probe of these correlated motions, with significant potential to advance our understanding of biological dynamics. However, recent work challenged this prevailing view, suggesting instead that diffuse scattering primarily originates from rigid body motions and could therefore be applied to improve structure determination. To investigate the nature of the disorder giving rise to diffuse scattering, and thus the potential applications of this signal, a diverse repertoire of disorder models was assessed for its ability to reproduce the diffuse signal reconstructed from three protein crystals. This comparison revealed that multiple models of intramolecular conformational dynamics, including ensemble models inferred from the Bragg data, could not explain the signal. Models of rigid body or short-range liquid-like motions, in which dynamics are confined to the biological unit, showed modest agreement with the diffuse maps, but were unable to reproduce experimental features indicative of long-range correlations. Extending a model of liquid-like motions to include disorder across neighboring proteins in the crystal significantly improved agreement with all three systems and highlighted the contribution of intermolecular correlations to the observed signal. These findings anticipate a need to account for intermolecular disorder in order to advance the interpretation of diffuse scattering to either extract biological motions or aid structural inference.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1417038

Journal Information:: IUCrJ, Journal Name: IUCrJ Journal Issue: 2 Vol. 5; ISSN 2052-2525

Publisher:: International Union of CrystallographyCopyright Statement

Country of Publication:: United States

Language:: English

References (68)

Protein dynamics from X-ray crystallography: Anisotropic, global motion in diffuse scattering patterns Meinhold, Lars; Smith, Jeremy C. Proteins: Structure, Function, and Bioinformatics, Vol. 66, Issue 4 https://doi.org/10.1002/prot.21246	journal	December 2006
Correlations of atomic movements in lysozyme crystals Clarage, James B.; Clarage, Michael S.; Phillips, Walter C. Proteins: Structure, Function, and Genetics, Vol. 12, Issue 2 https://doi.org/10.1002/prot.340120208	journal	February 1992
X-ray diffuse scattering and rigid-body motion in crystalline lysozyme probed by molecular dynamics simulation 1 1Edited by R. Huber Héry, Stéphanie; Genest, Daniel; Smith, Jeremy C. Journal of Molecular Biology, Vol. 279, Issue 1 https://doi.org/10.1006/jmbi.1998.1754	journal	May 1998
Similarities and differences between human cyclophilin A and other β-barrel structures Ke, Hengming Journal of Molecular Biology, Vol. 228, Issue 2 https://doi.org/10.1016/0022-2836(92)90841-7	journal	November 1992
Diffuse x-ray scattering from tropomyosin crystals Chacko, S.; Phillips, G. N. Biophysical Journal, Vol. 61, Issue 5 https://doi.org/10.1016/S0006-3495(92)81934-3	journal	May 1992
Motions of calmodulin characterized using both Bragg and diffuse X-ray scattering Wall, Michael E.; Clarage, James B.; Phillips, George N. Structure, Vol. 5, Issue 12 https://doi.org/10.1016/S0969-2126(97)00308-0	journal	December 1997
Optimized Torsion-Angle Normal Modes Reproduce Conformational Changes More Accurately Than Cartesian Modes Bray, Jenelle K.; Weiss, Dahlia R.; Levitt, Michael Biophysical Journal, Vol. 101, Issue 12 https://doi.org/10.1016/j.bpj.2011.10.054	journal	December 2011
High-Resolution Analysis of Zn2+ Coordination in the Alkaline Phosphatase Superfamily by EXAFS and X-ray Crystallography Bobyr, Elena; Lassila, Jonathan K.; Wiersma-Koch, Helen I. Journal of Molecular Biology, Vol. 415, Issue 1 https://doi.org/10.1016/j.jmb.2011.10.040	journal	January 2012
Tungstate as a Transition State Analog for Catalysis by Alkaline Phosphatase Peck, Ariana; Sunden, Fanny; Andrews, Logan D. Journal of Molecular Biology, Vol. 428, Issue 13 https://doi.org/10.1016/j.jmb.2016.05.007	journal	July 2016
On the Relationship between Diffraction Patterns and Motions in Macromolecular Crystals Moore, Peter B. Structure, Vol. 17, Issue 10 https://doi.org/10.1016/j.str.2009.08.015	journal	October 2009
Diffuse X-Ray Scattering to Model Protein Motions Wall, Michael E.; Adams, Paul D.; Fraser, James S. Structure, Vol. 22, Issue 2 https://doi.org/10.1016/j.str.2014.01.002	journal	February 2014
Diffuse x-ray scattering from tropomyosin crystals Chacko, S.; Phillips, G. N. Biophysical Journal, Vol. 61, Issue 5 https://doi.org/10.1016/s0006-3495(92)81934-3	journal	May 1992
Motions of calmodulin characterized using both Bragg and diffuse X-ray scattering Wall, Michael E.; Clarage, James B.; Phillips, George N. Structure, Vol. 5, Issue 12 https://doi.org/10.1016/s0969-2126(97)00308-0	journal	December 1997
Diffuse scattering in protein crystallography Benoit, Jean-Pierre; Doucet, Jean Quarterly Reviews of Biophysics, Vol. 28, Issue 2 https://doi.org/10.1017/S0033583500003048	journal	May 1995
Diffuse scattering in protein crystallography Benoit, Jean-Pierre; Doucet, Jean Quarterly Reviews of Biophysics, Vol. 28, Issue 2 https://doi.org/10.1017/s0033583500003048	journal	May 1995
X-ray Scattering Studies of Protein Structural Dynamics Meisburger, Steve P.; Thomas, William C.; Watkins, Maxwell B. Chemical Reviews, Vol. 117, Issue 12 https://doi.org/10.1021/acs.chemrev.6b00790	journal	May 2017
Molecular dynamics studied by analysis of the X-ray diffuse scattering from lysozyme crystals Doucet, J.; Benoit, J. P. Nature, Vol. 325, Issue 6105 https://doi.org/10.1038/325643a0	journal	February 1987
Hidden alternative structures of proline isomerase essential for catalysis Fraser, James S.; Clarkson, Michael W.; Degnan, Sheena C. Nature, Vol. 462, Issue 7273 https://doi.org/10.1038/nature08615	journal	December 2009
Macromolecular diffractive imaging using imperfect crystals Ayyer, Kartik; Yefanov, Oleksandr M.; Oberthür, Dominik Nature, Vol. 530, Issue 7589, p. 202-206 https://doi.org/10.1038/nature16949	journal	February 2016
Visualizing networks of mobility in proteins Wilson, Mark A. Nature Methods, Vol. 10, Issue 9 https://doi.org/10.1038/nmeth.2606	journal	August 2013
Correlated intramolecular motions and diffuse x–ray scattering in lysozyme Faure, P.; Micu, A.; Pérahia, D. Nature Structural & Molecular Biology, Vol. 1, Issue 2 https://doi.org/10.1038/nsb0294-124	journal	February 1994
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
A high-quality x-ray scattering experiment on liquid water at ambient conditions Hura, Greg; Sorenson, Jon M.; Glaeser, Robert M. The Journal of Chemical Physics, Vol. 113, Issue 20 https://doi.org/10.1063/1.1319614	journal	November 2000
Accessing protein conformational ensembles using room-temperature X-ray crystallography Fraser, J. S.; van den Bedem, H.; Samelson, A. J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 39 https://doi.org/10.1073/pnas.1111325108	journal	September 2011
Conformational dynamics of a crystalline protein from microsecond-scale molecular dynamics simulations and diffuse X-ray scattering Wall, Michael E.; Van Benschoten, Andrew H.; Sauter, Nicholas K. Proceedings of the National Academy of Sciences, Vol. 111, Issue 50 https://doi.org/10.1073/pnas.1416744111	journal	December 2014
Measuring and modeling diffuse scattering in protein X-ray crystallography Van Benschoten, Andrew H.; Liu, Lin; Gonzalez, Ana Proceedings of the National Academy of Sciences, Vol. 113, Issue 15 https://doi.org/10.1073/pnas.1524048113	journal	March 2016
One hundred years of diffuse scattering Welberry, T. R.; Weber, T. Crystallography Reviews, Vol. 22, Issue 1 https://doi.org/10.1080/0889311X.2015.1046853	journal	July 2015
One hundred years of diffuse scattering Welberry, T. R.; Weber, T. Crystallography Reviews, Vol. 22, Issue 1 https://doi.org/10.1080/0889311x.2015.1046853	journal	July 2015
Correlated Dynamics Determining X-Ray Diffuse Scattering from a Crystalline Protein Revealed by Molecular Dynamics Simulation Meinhold, Lars; Smith, Jeremy C. Physical Review Letters, Vol. 95, Issue 21 https://doi.org/10.1103/PhysRevLett.95.218103	journal	November 2005
Lattice Dynamics of a Protein Crystal Meinhold, Lars; Merzel, Franci; Smith, Jeremy C. Physical Review Letters, Vol. 99, Issue 13 https://doi.org/10.1103/PhysRevLett.99.138101	journal	September 2007
Correlated Dynamics Determining X-Ray Diffuse Scattering from a Crystalline Protein Revealed by Molecular Dynamics Simulation Meinhold, Lars; Smith, Jeremy C. Physical Review Letters, Vol. 95, Issue 21 https://doi.org/10.1103/physrevlett.95.218103	journal	November 2005
Lattice Dynamics of a Protein Crystal Meinhold, Lars; Merzel, Franci; Smith, Jeremy C. Physical Review Letters, Vol. 99, Issue 13 https://doi.org/10.1103/physrevlett.99.138101	journal	September 2007
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Resolution corrections in diffuse scattering experiments Boysen, H.; Adlhart, W. Journal of Applied Crystallography, Vol. 20, Issue 3 https://doi.org/10.1107/S0021889887086825	journal	June 1987
The variety of X-ray diffuse scattering from macromolecular crystals and its respective components Glover, I. D.; Harris, G. W.; Helliwell, J. R. Acta Crystallographica Section B Structural Science, Vol. 47, Issue 6 https://doi.org/10.1107/S0108768191004585	journal	December 1991
Some implications of a theorem due to Shannon Sayre, D. Acta Crystallographica, Vol. 5, Issue 6 https://doi.org/10.1107/S0365110X52002276	journal	November 1952
Modeling discrete heterogeneity in X-ray diffraction data by fitting multi-conformers van den Bedem, Henry; Dhanik, Ankur; Latombe, Jean-Claude Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 10 https://doi.org/10.1107/S0907444909030613	journal	September 2009
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Integration, scaling, space-group assignment and post-refinement Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 133-144 https://doi.org/10.1107/S0907444909047374	journal	January 2010
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
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
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
Analysis of diffuse scattering from yeast initiator tRNA crystals Kolatkar, A. R.; Clarage, J. B.; Phillips Jnr, G. N. Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 2 https://doi.org/10.1107/S0907444993011692	journal	March 1994
Acoustic vibrations contribute to the diffuse scatter produced by ribosome crystals Polikanov, Yury S.; Moore, Peter B. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 10 https://doi.org/10.1107/S1399004715013838	journal	September 2015
Diffraction-geometry refinement in the DIALS framework Waterman, David G.; Winter, Graeme; Gildea, Richard J. Acta Crystallographica Section D Structural Biology, Vol. 72, Issue 4 https://doi.org/10.1107/S2059798316002187	journal	March 2016
DIALS : implementation and evaluation of a new integration package Winter, Graeme; Waterman, David G.; Parkhurst, James M. Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 2 https://doi.org/10.1107/S2059798317017235	journal	February 2018
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/s0021889807021206	journal	July 2007
Resolution corrections in diffuse scattering experiments Boysen, H.; Adlhart, W. Journal of Applied Crystallography, Vol. 20, Issue 3 https://doi.org/10.1107/s0021889887086825	journal	June 1987
The variety of X-ray diffuse scattering from macromolecular crystals and its respective components Glover, I. D.; Harris, G. W.; Helliwell, J. R. Acta Crystallographica Section B Structural Science, Vol. 47, Issue 6 https://doi.org/10.1107/s0108768191004585	journal	December 1991
Some implications of a theorem due to Shannon Sayre, D. Acta Crystallographica, Vol. 5, Issue 6 https://doi.org/10.1107/s0365110x52002276	journal	November 1952
Modeling discrete heterogeneity in X-ray diffraction data by fitting multi-conformers van den Bedem, Henry; Dhanik, Ankur; Latombe, Jean-Claude Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 10 https://doi.org/10.1107/s0907444909030613	journal	September 2009
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/s0907444909047337	journal	January 2010
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
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/s0907444910007493	journal	March 2010
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
Analysis of diffuse scattering from yeast initiator tRNA crystals Kolatkar, A. R.; Clarage, J. B.; Phillips Jnr, G. N. Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 2 https://doi.org/10.1107/s0907444993011692	journal	March 1994
Acoustic vibrations contribute to the diffuse scatter produced by ribosome crystals Polikanov, Yury S.; Moore, Peter B. Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 10 https://doi.org/10.1107/s1399004715013838	journal	September 2015
Diffraction-geometry refinement in the DIALS framework Waterman, David G.; Winter, Graeme; Gildea, Richard J. Acta Crystallographica Section D Structural Biology, Vol. 72, Issue 4 https://doi.org/10.1107/s2059798316002187	journal	March 2016
DIALS : implementation and evaluation of a new integration package Winter, Graeme; Waterman, David G.; Parkhurst, James M. Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 2 https://doi.org/10.1107/s2059798317017235	journal	February 2018
Linking Crystallographic Model and Data Quality Karplus, P. A.; Diederichs, K. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1218231	journal	May 2012
WrpA Is an Atypical Flavodoxin Family Protein under Regulatory Control of the Brucella abortus General Stress Response System Herrou, Julien; Czyż, Daniel M.; Willett, Jonathan W. Journal of Bacteriology, Vol. 198, Issue 8 https://doi.org/10.1128/JB.00982-15	journal	February 2016
WrpA Is an Atypical Flavodoxin Family Protein under Regulatory Control of the Brucella abortus General Stress Response System Herrou, Julien; Czyż, Daniel M.; Willett, Jonathan W. Journal of Bacteriology, Vol. 198, Issue 8 https://doi.org/10.1128/jb.00982-15	journal	February 2016
Fluctuations and Correlations in Crystalline Protein Dynamics: A Simulation Analysis of Staphylococcal Nuclease Meinhold, Lars; Smith, Jeremy C. Biophysical Journal, Vol. 88, Issue 4 https://doi.org/10.1529/biophysj.104.056101	journal	April 2005
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Macromolecular diffractive imaging using imperfect crystals Ayyer, Kartik; Yefanov, Oleksandr; Oberthür, Dominik Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2016-01028	text	January 2016
Mapping the conformational landscape of a dynamic enzyme by multitemperature and XFEL crystallography Keedy, Daniel A.; Kenner, Lillian R.; Warkentin, Matthew eLife, Vol. 4 https://doi.org/10.7554/eLife.07574	journal	September 2015
Mapping the conformational landscape of a dynamic enzyme by multitemperature and XFEL crystallography Keedy, Daniel A.; Kenner, Lillian R.; Warkentin, Matthew eLife, Vol. 4 https://doi.org/10.7554/elife.07574	journal	September 2015

Cited By (6)

Diffuse X-ray scattering from correlated motions in a protein crystal Meisburger, Steve P.; Case, David A.; Ando, Nozomi Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14933-6	journal	March 2020
Liquid-like and rigid-body motions in molecular-dynamics simulations of a crystalline protein Wych, David C.; Fraser, James S.; Mobley, David L. Structural Dynamics, Vol. 6, Issue 6 https://doi.org/10.1063/1.5132692	journal	November 2019
Atomic form factors, incoherent scattering functions, and photon scattering cross sections Hubbell, J. H.; Veigele, Wm. J.; Briggs, E. A. Journal of Physical and Chemical Reference Data, Vol. 4, Issue 3 https://doi.org/10.1063/1.555523	journal	July 1975
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
Rigid-body motion is the main source of diffuse scattering in protein crystallography de Klijn, T.; Schreurs, A. M. M.; Kroon-Batenburg, L. M. J. IUCrJ, Vol. 6, Issue 2 https://doi.org/10.1107/s2052252519000927	journal	February 2019
Structure Determination by Continuous Diffraction from Imperfect Crystals Ayyer, Kartik; Yefanov, Oleksandr; Chapman, Henry N. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2019-00073	text	January 2018

Similar Records

Internal protein motions in molecular-dynamics simulations of Bragg and diffuse X-ray scattering

Journal Article · 2018 · IUCrJ · OSTI ID:1418076

Wall, Michael E.

Predicting X-ray diffuse scattering from translation–libration–screw structural ensembles

Journal Article · 2015 · Acta Crystallographica. Section D: Biological Crystallography (Online) · OSTI ID:1214720

Van Benschoten, Andrew H.; Afonine, Pavel V.; Terwilliger, Thomas C.; +6 more

Predicting X-ray diffuse scattering from translation–libration–screw structural ensembles

Journal Article · 2015 · Acta Crystallographica. Section D: Biological Crystallography · OSTI ID:22389077

Van Benschoten, Andrew H.; Afonine, Pavel V.; Terwilliger, Thomas C.; +5 more

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
diffuse scattering
intermolecular correlations

Title: Intermolecular correlations are necessary to explain diffuse scattering from protein crystals

Citation Formats

References (68)

Cited By (6)

Similar Records

Related Subjects