Kinematic Flexibility Analysis: Hydrogen Bonding Patterns Impart a Spatial Hierarchy of Protein Motion
Abstract
Elastic network models (ENMs) and constraint-based, topological rigidity analysis are two distinct, coarse-grained approaches to study conformational flexibility of macromolecules. In the two decades since their introduction, both have contributed significantly to insights into protein molecular mechanisms and function. However, despite a shared purpose of these approaches, the topological nature of rigidity analysis, and thereby the absence of motion modes, has impeded a direct comparison. We present an alternative, kinematic approach to rigidity analysis, which circumvents these drawbacks. We introduce a novel protein hydrogen bond network spectral decomposition, which provides an orthonormal basis for collective motions modulated by noncovalent interactions, analogous to the eigenspectrum of normal modes. The zero modes decompose proteins into rigid clusters identical to those from topological rigidity, while nonzero modes rank protein motions by their hydrogen bond collective energy penalty. Our kinematic flexibility analysis bridges topological rigidity theory and ENM, enabling a detailed analysis of motion modes obtained from both approaches. Analysis of a large, structurally diverse data set revealed that collectivity of protein motions, reported by the Shannon entropy, is significantly reduced for rigidity theory compared to normal mode approaches. Strikingly, kinematic flexibility analysis suggests that the hydrogen bonding network encodes a protein-fold specific, spatialmore »
- Authors:
-
- Univ. of Erlangen–Nuremberg, Erlangen (Germany). Chair of Applied Dynamics
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Biosciences Division; Univ. of California, San Francisco, CA (United States). Dept. of Bioengineering and Therapeutic Sciences
- Publication Date:
- Research Org.:
- SLAC National Accelerator Lab., Menlo Park, CA (United States); Univ. of California, San Francisco, CA (United States); Univ. of Erlangen–Nuremberg, Erlangen (Germany)
- Sponsoring Org.:
- USDOE; National Inst. of Health (NIH) (United States); Deutsche Telekom Stiftung (Germany)
- OSTI Identifier:
- 1490788
- Grant/Contract Number:
- AC02-76SF00515; GM123159
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Chemical Information and Modeling
- Additional Journal Information:
- Journal Volume: 58; Journal Issue: 10; Journal ID: ISSN 1549-9596
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Citation Formats
Budday, Dominik, Leyendecker, Sigrid, and van den Bedem, Henry. Kinematic Flexibility Analysis: Hydrogen Bonding Patterns Impart a Spatial Hierarchy of Protein Motion. United States: N. p., 2018.
Web. doi:10.1021/acs.jcim.8b00267.
Budday, Dominik, Leyendecker, Sigrid, & van den Bedem, Henry. Kinematic Flexibility Analysis: Hydrogen Bonding Patterns Impart a Spatial Hierarchy of Protein Motion. United States. https://doi.org/10.1021/acs.jcim.8b00267
Budday, Dominik, Leyendecker, Sigrid, and van den Bedem, Henry. Fri .
"Kinematic Flexibility Analysis: Hydrogen Bonding Patterns Impart a Spatial Hierarchy of Protein Motion". United States. https://doi.org/10.1021/acs.jcim.8b00267. https://www.osti.gov/servlets/purl/1490788.
@article{osti_1490788,
title = {Kinematic Flexibility Analysis: Hydrogen Bonding Patterns Impart a Spatial Hierarchy of Protein Motion},
author = {Budday, Dominik and Leyendecker, Sigrid and van den Bedem, Henry},
abstractNote = {Elastic network models (ENMs) and constraint-based, topological rigidity analysis are two distinct, coarse-grained approaches to study conformational flexibility of macromolecules. In the two decades since their introduction, both have contributed significantly to insights into protein molecular mechanisms and function. However, despite a shared purpose of these approaches, the topological nature of rigidity analysis, and thereby the absence of motion modes, has impeded a direct comparison. We present an alternative, kinematic approach to rigidity analysis, which circumvents these drawbacks. We introduce a novel protein hydrogen bond network spectral decomposition, which provides an orthonormal basis for collective motions modulated by noncovalent interactions, analogous to the eigenspectrum of normal modes. The zero modes decompose proteins into rigid clusters identical to those from topological rigidity, while nonzero modes rank protein motions by their hydrogen bond collective energy penalty. Our kinematic flexibility analysis bridges topological rigidity theory and ENM, enabling a detailed analysis of motion modes obtained from both approaches. Analysis of a large, structurally diverse data set revealed that collectivity of protein motions, reported by the Shannon entropy, is significantly reduced for rigidity theory compared to normal mode approaches. Strikingly, kinematic flexibility analysis suggests that the hydrogen bonding network encodes a protein-fold specific, spatial hierarchy of motions, which goes nearly undetected in ENM. This hierarchy reveals distinct motion regimes that rationalize experimental and simulated protein stiffness variations. Kinematic motion modes highly correlate with reported crystallographic B factors and molecular dynamics simulations of adenylate kinase. A formal expression for changes in free energy derived from the spectral decomposition indicates that motions across nearly 40% of modes obey enthalpy–entropy compensation. Taken together, our results suggest that hydrogen bond networks have evolved to modulate protein structure and dynamics, which can be efficiently probed by kinematic flexibility analysis.},
doi = {10.1021/acs.jcim.8b00267},
journal = {Journal of Chemical Information and Modeling},
number = 10,
volume = 58,
place = {United States},
year = {Fri Sep 21 00:00:00 EDT 2018},
month = {Fri Sep 21 00:00:00 EDT 2018}
}
Web of Science
Figures / Tables:
Works referenced in this record:
Large Amplitude Elastic Motions in Proteins from a Single-Parameter, Atomic Analysis
journal, August 1996
- Tirion, Monique M.
- Physical Review Letters, Vol. 77, Issue 9
On graphs and rigidity of plane skeletal structures
journal, October 1970
- Laman, G.
- Journal of Engineering Mathematics, Vol. 4, Issue 4
Generic Rigidity Percolation: The Pebble Game
journal, November 1995
- Jacobs, D. J.; Thorpe, M. F.
- Physical Review Letters, Vol. 75, Issue 22
iMod: multipurpose normal mode analysis in internal coordinates
journal, August 2011
- Lopéz-Blanco, José Ramón; Garzón, José Ignacio; Chacón, Pablo
- Bioinformatics, Vol. 27, Issue 20
A Method of Rapid Calculation of a Second Derivative Matrix of Conformational Energy for Large Molecules
journal, October 1983
- Noguti, Toshiyuki; Gō, Nobuhiro
- Journal of the Physical Society of Japan, Vol. 52, Issue 10
Atomic torsional modal analysis for high-resolution proteins
journal, March 2015
- Tirion, Monique M.; ben-Avraham, Daniel
- Physical Review E, Vol. 91, Issue 3
A new approach for determining low-frequency normal modes in macromolecules
journal, June 1994
- Durand, Philippe; Trinquier, Georges; Sanejouand, Yves-Henri
- Biopolymers, Vol. 34, Issue 6
Building-block approach for determining low-frequency normal modes of macromolecules
journal, January 2000
- Tama, Florence; Gadea, Florent Xavier; Marques, Osni
- Proteins: Structure, Function, and Genetics, Vol. 41, Issue 1
ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement
journal, July 2004
- Suhre, K.; Sanejouand, Y. -H.
- Nucleic Acids Research, Vol. 32, Issue Web Server
Protein normal-mode dynamics: Trypsin inhibitor, crambin, ribonuclease and lysozyme
journal, February 1985
- Levitt, Michael; Sander, Christian; Stern, Peter S.
- Journal of Molecular Biology, Vol. 181, Issue 3
Conventional NMA as a better standard for evaluating elastic network models: NMA as a Better Standard for Evaluating ENMs
journal, December 2014
- Na, Hyuntae; Song, Guang
- Proteins: Structure, Function, and Bioinformatics, Vol. 83, Issue 2
Bridging between NMA and Elastic Network Models: Preserving All-Atom Accuracy in Coarse-Grained Models
journal, October 2015
- Na, Hyuntae; Jernigan, Robert L.; Song, Guang
- PLOS Computational Biology, Vol. 11, Issue 10
Functional Modes of Proteins Are among the Most Robust
journal, February 2006
- Nicolay, S.; Sanejouand, Y. -H.
- Physical Review Letters, Vol. 96, Issue 7
Torsional Network Model: Normal Modes in Torsion Angle Space Better Correlate with Conformation Changes in Proteins
journal, June 2010
- Mendez, Raul; Bastolla, Ugo
- Physical Review Letters, Vol. 104, Issue 22
Optimized Torsion-Angle Normal Modes Reproduce Conformational Changes More Accurately Than Cartesian Modes
journal, December 2011
- Bray, Jenelle K.; Weiss, Dahlia R.; Levitt, Michael
- Biophysical Journal, Vol. 101, Issue 12
Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential
journal, June 1997
- Bahar, Ivet; Atilgan, Ali Rana; Erman, Burak
- Folding and Design, Vol. 2, Issue 3
Correlation between Native-State Hydrogen Exchange and Cooperative Residue Fluctuations from a Simple Model
journal, January 1998
- Bahar, I.; Wallqvist, A.; Covell, D. G.
- Biochemistry, Vol. 37, Issue 4
Anisotropy of Fluctuation Dynamics of Proteins with an Elastic Network Model
journal, January 2001
- Atilgan, A. R.; Durell, S. R.; Jernigan, R. L.
- Biophysical Journal, Vol. 80, Issue 1
An Algorithm for Two-Dimensional Rigidity Percolation: The Pebble Game
journal, November 1997
- Jacobs, Donald J.; Hendrickson, Bruce
- Journal of Computational Physics, Vol. 137, Issue 2
Protein flexibility and dynamics using constraint theory
journal, February 2001
- Thorpe, M. F.; Lei, Ming; Rader, A. J.
- Journal of Molecular Graphics and Modelling, Vol. 19, Issue 1
Generic rigidity in three-dimensional bond-bending networks
journal, August 1998
- Jacobs, D. J.
- Journal of Physics A: Mathematical and General, Vol. 31, Issue 31
Counting out to the flexibility of molecules
journal, November 2005
- Whiteley, Walter
- Physical Biology, Vol. 2, Issue 4
A proof of the molecular conjecture
conference, January 2009
- Katoh, Naoki; Tanigawa, Shin-ichi
- Proceedings of the 25th annual symposium on Computational geometry - SCG '09
KINARI-Web: a server for protein rigidity analysis
journal, June 2011
- Fox, N.; Jagodzinski, F.; Li, Y.
- Nucleic Acids Research, Vol. 39, Issue suppl
Floppy modes in network glasses
journal, November 1989
- Cai, Y.; Thorpe, M. F.
- Physical Review B, Vol. 40, Issue 15
Algorithms for three-dimensional rigidity analysis and a first-order percolation transition
journal, October 2007
- Chubynsky, M. V.; Thorpe, M. F.
- Physical Review E, Vol. 76, Issue 4
Protein flexibility predictions using graph theory
journal, January 2001
- Jacobs, Donald J.; Rader, A. J.; Kuhn, Leslie A.
- Proteins: Structure, Function, and Genetics, Vol. 44, Issue 2
Global and local indices for characterizing biomolecular flexibility and rigidity
journal, September 2012
- Pfleger, Christopher; Radestock, Sebastian; Schmidt, Elena
- Journal of Computational Chemistry, Vol. 34, Issue 3
Protein unfolding: Rigidity lost
journal, March 2002
- Rader, A. J.; Hespenheide, Brandon M.; Kuhn, Leslie A.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 6
Analyzing the Flexibility of RNA Structures by Constraint Counting
journal, June 2008
- Fulle, Simone; Gohlke, Holger
- Biophysical Journal, Vol. 94, Issue 11
Detecting the native ligand orientation by interfacial rigidity: SiteInterlock: Identifying Ligand Binding Poses by Rigidity
journal, October 2016
- Raschka, Sebastian; Bemister-Buffington, Joseph; Kuhn, Leslie A.
- Proteins: Structure, Function, and Bioinformatics, Vol. 84, Issue 12
Nonadditivity in Conformational Entropy upon Molecular Rigidification Reveals a Universal Mechanism Affecting Folding Cooperativity
journal, February 2011
- Vorov, Oleg K.; Livesay, Dennis R.; Jacobs, Donald J.
- Biophysical Journal, Vol. 100, Issue 4
Rigidity Theory-Based Approximation of Vibrational Entropy Changes upon Binding to Biomolecules
journal, March 2017
- Gohlke, Holger; Ben-Shalom, Ido Y.; Kopitz, Hannes
- Journal of Chemical Theory and Computation, Vol. 13, Issue 4
Efficient Approximation of Ligand Rotational and Translational Entropy Changes upon Binding for Use in MM-PBSA Calculations
journal, January 2017
- Ben-Shalom, Ido Y.; Pfeiffer-Marek, Stefania; Baringhaus, Karl-Heinz
- Journal of Chemical Information and Modeling, Vol. 57, Issue 2
Maintaining and Enhancing Diversity of Sampled Protein Conformations in Robotics-Inspired Methods
journal, January 2018
- Abella, Jayvee R.; Moll, Mark; Kavraki, Lydia E.
- Journal of Computational Biology, Vol. 25, Issue 1
Simulating Protein Motions with Rigidity Analysis
journal, July 2007
- Thomas, Shawna; Tang, Xinyu; Tapia, Lydia
- Journal of Computational Biology, Vol. 14, Issue 6
Multi-Resolution Rigidity-Based Sampling of Protein Conformational Paths
conference, September 2013
- Luo, Dong; Haspel, Nurit
- BCB'13: ACM-BCB2013, Proceedings of the International Conference on Bioinformatics, Computational Biology and Biomedical Informatics
Thermostability in rubredoxin and its relationship to mechanical rigidity
journal, December 2009
- Rader, A. J.
- Physical Biology, Vol. 7, Issue 1
Protein rigidity and thermophilic adaptation
journal, January 2011
- Radestock, Sebastian; Gohlke, Holger
- Proteins: Structure, Function, and Bioinformatics, Vol. 79, Issue 4
Application of Rigidity Theory to the Thermostabilization of Lipase A from Bacillus subtilis
journal, March 2016
- Rathi, Prakash Chandra; Fulton, Alexander; Jaeger, Karl-Erich
- PLOS Computational Biology, Vol. 12, Issue 3
Identifying protein folding cores from the evolution of flexible regions during unfolding
journal, December 2002
- Hespenheide, Brandon M.; Rader, A. J.; Thorpe, M. F.
- Journal of Molecular Graphics and Modelling, Vol. 21, Issue 3
Hydrogen bond networks determine emergent mechanical and thermodynamic properties across a protein family
journal, August 2008
- Livesay, Dennis R.; Huynh, Dang H.; Dallakyan, Sargis
- Chemistry Central Journal, Vol. 2, Issue 1
Sampling protein conformations and pathways
journal, January 2004
- Lei, Ming; Zavodszky, Maria I.; Kuhn, Leslie A.
- Journal of Computational Chemistry, Vol. 25, Issue 9
Constrained geometric simulation of diffusive motion in proteins
journal, November 2005
- Wells, Stephen; Menor, Scott; Hespenheide, Brandon
- Physical Biology, Vol. 2, Issue 4
Multiscale modeling of macromolecular conformational changes combining concepts from rigidity and elastic network theory
journal, February 2006
- Ahmed, Aqeel; Gohlke, Holger
- Proteins: Structure, Function, and Bioinformatics, Vol. 63, Issue 4
Rapid simulation of protein motion: merging flexibility, rigidity and normal mode analyses
journal, February 2012
- Jimenez-Roldan, J. E.; Freedman, R. B.; Römer, R. A.
- Physical Biology, Vol. 9, Issue 1
Geometric analysis characterizes molecular rigidity in generic and non-generic protein configurations
journal, October 2015
- Budday, Dominik; Leyendecker, Sigrid; van den Bedem, Henry
- Journal of the Mechanics and Physics of Solids, Vol. 83
Nullspace Sampling with Holonomic Constraints Reveals Molecular Mechanisms of Protein Gαs
journal, July 2015
- Pachov, Dimitar V.; van den Bedem, Henry
- PLOS Computational Biology, Vol. 11, Issue 7
Coupled Motions in β 2 AR:Gαs Conformational Ensembles
journal, February 2016
- Pachov, Dimitar V.; Fonseca, Rasmus; Arnol, Damien
- Journal of Chemical Theory and Computation, Vol. 12, Issue 3
Elasticity, strength and resilience: A comparative study on mechanical signatures of α-Helix, β-sheet and tropocollagen domains
journal, July 2008
- Buehler, Markus J.; Keten, Sinan
- Nano Research, Vol. 1, Issue 1
Automated design of the surface positions of protein helices: Protein surface design
journal, June 1997
- Dahiyat, Bassil I.; Benjamin Gordon, D.; Mayo, Stephen L.
- Protein Science, Vol. 6, Issue 6
Accessible Surfaces of Beta Proteins Increase with Increasing Protein Molecular Mass More Rapidly than Those of Other Proteins
journal, December 2011
- Glyakina, Anna V.; Bogatyreva, Natalya S.; Galzitskaya, Oxana V.
- PLoS ONE, Vol. 6, Issue 12
How soft is a single protein? The stress–strain curve of antibody pentamers with 5 pN and 50 pm resolutions
journal, January 2016
- Perrino, Alma P.; Garcia, Ricardo
- Nanoscale, Vol. 8, Issue 17
Collective protein dynamics and nuclear spin relaxation
journal, February 1995
- Brüschweiler, Rafael
- The Journal of Chemical Physics, Vol. 102, Issue 8
Accurate de novo design of hyperstable constrained peptides
journal, September 2016
- Bhardwaj, Gaurav; Mulligan, Vikram Khipple; Bahl, Christopher D.
- Nature, Vol. 538, Issue 7625
Universality of vibrational spectra of globular proteins
journal, February 2016
- Na, Hyuntae; Song, Guang; ben-Avraham, Daniel
- Physical Biology, Vol. 13, Issue 1
Geometric Confinement Governs the Rupture Strength of H-bond Assemblies at a Critical Length Scale
journal, February 2008
- Keten, Sinan; Buehler, Markus J.
- Nano Letters, Vol. 8, Issue 2
Adenylate Kinase and AMP Signaling Networks: Metabolic Monitoring, Signal Communication and Body Energy Sensing
journal, April 2009
- Dzeja, Petras; Terzic, Andre
- International Journal of Molecular Sciences, Vol. 10, Issue 4
Induced-fit movements in adenylate kinases
journal, June 1990
- Schulz, Georg E.; Müller, Christoph W.; Diederichs, Kay
- Journal of Molecular Biology, Vol. 213, Issue 4
Structure of the complex between adenylate kinase from Escherichia coli and the inhibitor Ap5A refined at 1.9 Å resolution
journal, March 1992
- Müller, Christoph W.; Schulz, Georg E.
- Journal of Molecular Biology, Vol. 224, Issue 1
Domain Closure in Adenylate Kinase
journal, January 1993
- Gerstein, Mark; Schulz, Georg; Chothia, Cyrus
- Journal of Molecular Biology, Vol. 229, Issue 2
Movie of the structural changes during a catalytic cycle of nucleoside monophosphate kinases
journal, May 1995
- Vonrhein, Clemens; Schlauderer, Gerd J.; Schulz, Georg E.
- Structure, Vol. 3, Issue 5
Adenylate kinase motions during catalysis: an energetic counterweight balancing substrate binding
journal, February 1996
- Müller, Cw; Schlauderer, Gj; Reinstein, J.
- Structure, Vol. 4, Issue 2
Zipping and Unzipping of Adenylate Kinase: Atomistic Insights into the Ensemble of Open↔Closed Transitions
journal, November 2009
- Beckstein, Oliver; Denning, Elizabeth J.; Perilla, Juan R.
- Journal of Molecular Biology, Vol. 394, Issue 1
Sampling large conformational transitions: adenylate kinase as a testing ground
journal, May 2014
- Seyler, Sean L.; Beckstein, Oliver
- Molecular Simulation, Vol. 40, Issue 10-11
Mapping the Dynamics Landscape of Conformational Transitions in Enzyme: The Adenylate Kinase Case
journal, August 2015
- Li, Dechang; Liu, Ming S.; Ji, Baohua
- Biophysical Journal, Vol. 109, Issue 3
Frustration-guided motion planning reveals conformational transitions in proteins: BUDDAY et al.
journal, July 2017
- Budday, Dominik; Fonseca, Rasmus; Leyendecker, Sigrid
- Proteins: Structure, Function, and Bioinformatics, Vol. 85, Issue 10
Direct observation of ultrafast large-scale dynamics of an enzyme under turnover conditions
journal, March 2018
- Aviram, Haim Yuval; Pirchi, Menahem; Mazal, Hisham
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 13
Fast, clash-free RNA conformational morphing using molecular junctions
journal, March 2017
- Héliou, Amélie; Budday, Dominik; Fonseca, Rasmus
- Bioinformatics, Vol. 33, Issue 14
Collision-free poisson motion planning in ultra high-dimensional molecular conformation spaces
journal, January 2018
- Fonseca, Rasmus; Budday, Dominik; van den Bedem, Henry
- Journal of Computational Chemistry, Vol. 39, Issue 12
Hydrogen bonds are a primary driving force for de novo protein folding
journal, November 2017
- Lee, Schuyler; Wang, Chao; Liu, Haolin
- Acta Crystallographica Section D Structural Biology, Vol. 73, Issue 12
Intermolecular hydrogen bonding strategy to fabricate mechanically strong hydrogels with high elasticity and fatigue resistance
journal, January 2013
- Zhang, Jinlong; Wang, Ning; Liu, Wenguang
- Soft Matter, Vol. 9, Issue 27
A comparison of successful and failed protein interface designs highlights the challenges of designing buried hydrogen bonds
journal, November 2012
- Stranges, P. Benjamin; Kuhlman, Brian
- Protein Science, Vol. 22, Issue 1
The coming of age of de novo protein design
journal, September 2016
- Huang, Po-Ssu; Boyken, Scott E.; Baker, David
- Nature, Vol. 537, Issue 7620
De novo design of protein homo-oligomers with modular hydrogen-bond network-mediated specificity
journal, May 2016
- Boyken, S. E.; Chen, Z.; Groves, B.
- Science, Vol. 352, Issue 6286
Integrative, dynamic structural biology at atomic resolution—it's about time
journal, March 2015
- van den Bedem, Henry; Fraser, James S.
- Nature Methods, Vol. 12, Issue 4
Entropic Elasticity Controls Nanomechanics of Single Tropocollagen Molecules
journal, July 2007
- Buehler, Markus J.; Wong, Sophie Y.
- Biophysical Journal, Vol. 93, Issue 1
Low-frequency modes in the Raman spectra of proteins
journal, July 1982
- Painter, P. C.; Mosher, L. E.; Rhoads, C.
- Biopolymers, Vol. 21, Issue 7
A Distinct Utility of the Amide III Infrared Band for Secondary Structure Estimation of Aqueous Protein Solutions Using Partial Least Squares Methods †
journal, March 2004
- Cai, Shuowei; Singh, Bal Ram
- Biochemistry, Vol. 43, Issue 9
Obtaining information about protein secondary structures in aqueous solution using Fourier transform IR spectroscopy
journal, February 2015
- Yang, Huayan; Yang, Shouning; Kong, Jilie
- Nature Protocols, Vol. 10, Issue 3
Mechanical Response of Silk Crystalline Units from Force-Distribution Analysis
journal, May 2009
- Xiao, Senbo; Stacklies, Wolfram; Cetinkaya, Murat
- Biophysical Journal, Vol. 96, Issue 10
On the coupling between the dynamics of protein and water
journal, January 2017
- Gavrilov, Yulian; Leuchter, Jessica D.; Levy, Yaakov
- Physical Chemistry Chemical Physics, Vol. 19, Issue 12
Hydration Water Dynamics Near Biological Interfaces
journal, December 2008
- Johnson, Margaret E.; Malardier-Jugroot, Cecile; Murarka, Rajesh K.
- The Journal of Physical Chemistry B, Vol. 113, Issue 13
A unified model of protein dynamics
journal, February 2009
- Frauenfelder, H.; Chen, G.; Berendzen, J.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 13
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- Dasgupta, Medhanjali; Budday, Dominik; de Oliveira, Saulo H. P.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 51
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journal, June 2019
- van den Bedem, Henry; Wilson, Mark A.
- Journal of Synchrotron Radiation, Vol. 26, Issue 4