Using synchrotrons and XFELs for time-resolved X-ray crystallography and solution scattering experiments on biomolecules.

Time-resolved structural information is key to understand the mechanism of biological processes, such as catalysis and signalling. Recent developments in X-ray sources as well as data collection and analysis methods are making routine time-resolved X-ray crystallography and solution scattering experiments a real possibility for structural biologists. Here we review the information that can be obtained from these techniques and discuss the considerations that must be taken into account when designing a time-resolved experiment.

[1]  R D Young,et al.  Protein states and proteinquakes. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Anton Barty,et al.  Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser , 2014, Nature.

[3]  J. Trincao,et al.  Dynamic structural science: recent developments in time-resolved spectroscopy and X-ray crystallography. , 2013, Biochemical Society transactions.

[4]  R. Neutze Opportunities and challenges for time-resolved studies of protein structural dynamics at X-ray free-electron lasers , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[5]  Time evolution of the quaternary structure of Escherichia coli aspartate transcarbamoylase upon reaction with the natural substrates and a slow, tight-binding inhibitor. , 2008, Journal of molecular biology.

[6]  Jaehyun Park,et al.  In vivo crystallography at X-ray free-electron lasers: the next generation of structural biology? , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[7]  U. Weierstall,et al.  Double-focusing mixing jet for XFEL study of chemical kinetics , 2014, Journal of synchrotron radiation.

[8]  Sébastien Boutet,et al.  Simultaneous Femtosecond X-ray Spectroscopy and Diffraction of Photosystem II at Room Temperature , 2013, Science.

[9]  Alessandro Spilotros,et al.  The Monod-Wyman-Changeux allosteric model accounts for the quaternary transition dynamics in wild type and a recombinant mutant human hemoglobin , 2012, Proceedings of the National Academy of Sciences.

[10]  Ville R. I. Kaila,et al.  Watching a signaling protein function in real time via 100-ps time-resolved Laue crystallography , 2012, Proceedings of the National Academy of Sciences.

[11]  E. Kondrashkina,et al.  Microsecond Hydrophobic Collapse in the Folding of Escherichia coli Dihydrofolate Reductase, an α/β-Type Protein , 2007 .

[12]  Aaron S. Brewster,et al.  Raster-scanning serial protein crystallography using micro- and nano-focused synchrotron beams , 2015, Acta crystallographica. Section D, Biological crystallography.

[13]  M. Wulff,et al.  Probing in cell protein structural changes with time-resolved X-ray scattering , 2012 .

[14]  A. Fersht,et al.  Time-resolved small-angle X-ray scattering study of the folding dynamics of barnase. , 2011, Journal of molecular biology.

[15]  Henry N. Chapman,et al.  Serial crystallography on in vivo grown microcrystals using synchrotron radiation , 2014, IUCrJ.

[16]  Garth J. Williams,et al.  Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein , 2014, Science.

[17]  R. Owen,et al.  Time-resolved crystallography using the Hadamard Transform , 2014, Nature Methods.

[18]  M. Wulff,et al.  Unveiling the timescale of the R-T transition in human hemoglobin. , 2010, Journal of molecular biology.

[19]  Jae Hyuk Lee,et al.  Reply to 'contradictions in X-ray structures of intermediates in the photocycle of photoactive yellow protein'. , 2014, Nature chemistry.

[20]  Michael Wulff,et al.  Structural dynamics of light-driven proton pumps. , 2009, Structure.

[21]  D. Svergun,et al.  Small-angle X-ray scattering on biological macromolecules and nanocomposites in solution. , 2013, Annual review of physical chemistry.

[22]  F. Schotte,et al.  Protein structural dynamics in solution unveiled via 100-ps time-resolved x-ray scattering , 2010, Proceedings of the National Academy of Sciences.

[23]  Anton Barty,et al.  Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser , 2014, Nature Methods.

[24]  Matteo Levantino,et al.  Ultrafast myoglobin structural dynamics observed with an X-ray free-electron laser , 2015, Nature Communications.

[25]  Anton Barty,et al.  Natively Inhibited Trypanosoma brucei Cathepsin B Structure Determined by Using an X-ray Laser , 2013, Science.

[26]  J. Hub,et al.  Validating solution ensembles from molecular dynamics simulation by wide-angle X-ray scattering data. , 2014, Biophysical journal.

[27]  J. Kubelka Time-resolved methods in biophysics. 9. Laser temperature-jump methods for investigating biomolecular dynamics , 2009, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[28]  Jae Hyuk Lee,et al.  Volume-conserving trans-cis isomerization pathways in photoactive yellow protein visualized by picosecond X-ray crystallography , 2013, Nature chemistry.

[29]  R. Neutze,et al.  Time-resolved WAXS reveals accelerated conformational changes in iodoretinal-substituted proteorhodopsin. , 2011, Biophysical journal.

[30]  R. Neutze,et al.  Conformational activation of visual rhodopsin in native disc membranes , 2015, Science Signaling.

[31]  T. Narayanan,et al.  Time-resolved small-angle x-ray scattering study of the early stage of amyloid formation of an apomyoglobin mutant. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[32]  Satoshi Takahashi,et al.  Conformational landscape of cytochrome c folding studied by microsecond-resolved small-angle x-ray scattering , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Chin,et al.  Cellular incorporation of unnatural amino acids and bioorthogonal labeling of proteins. , 2014, Chemical reviews.

[34]  Marius Schmidt,et al.  Application of singular value decomposition to the analysis of time-resolved macromolecular x-ray data. , 2003, Biophysical journal.

[35]  P. Coppens,et al.  New methods in time-resolved Laue pump–probe crystallography at synchrotron sources , 2015, Journal of synchrotron radiation.

[36]  Marius Schmidt,et al.  Mix and Inject: Reaction Initiation by Diffusion for Time-Resolved Macromolecular Crystallography , 2013 .

[37]  Stephan Förster,et al.  Microfluidic liquid jet system with compatibility for atmospheric and high-vacuum conditions. , 2014, Lab on a chip.

[38]  M. Messerschmidt,et al.  The RATIO method for time-resolved Laue crystallography. , 2009, Journal of synchrotron radiation.

[39]  U Weierstall,et al.  X-ray lasers for structural and dynamic biology , 2012, Reports on progress in physics. Physical Society.

[40]  Ezequiel Panepucci,et al.  Room-temperature serial crystallography at synchrotron X-ray sources using slowly flowing free-standing high-viscosity microstreams. , 2015, Acta crystallographica. Section D, Biological crystallography.

[41]  Anton Barty,et al.  Room-temperature macromolecular serial crystallography using synchrotron radiation , 2014, IUCrJ.

[42]  Andreas Menzel,et al.  Signal amplification and transduction in phytochrome photosensors , 2014, Nature.

[43]  E. Henry,et al.  Nanosecond absorption spectroscopy of hemoglobin: elementary processes in kinetic cooperativity. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Henry N. Chapman,et al.  Femtosecond X-ray protein nanocrystallography , 2010 .

[45]  Georg Weidenspointner,et al.  Time-resolved protein nanocrystallography using an X-ray free-electron laser , 2012, Optics express.

[46]  Jae Hyuk Lee,et al.  The short-lived signaling state of the photoactive yellow protein photoreceptor revealed by combined structural probes. , 2011, Journal of the American Chemical Society.

[47]  David van der Spoel,et al.  Deciphering Solution Scattering Data with Experimentally Guided Molecular Dynamics Simulations , 2015, Journal of chemical theory and computation.

[48]  Ville R. I. Kaila,et al.  Contradictions in X-ray structures of intermediates in the photocycle of photoactive yellow protein. , 2014, Nature chemistry.

[49]  Jörg Enderlein,et al.  Time-resolved methods in biophysics. 3. Fluorescence lifetime correlation spectroscopy , 2007, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[50]  Ilme Schlichting,et al.  Serial femtosecond crystallography: the first five years , 2015, IUCrJ.

[51]  David S Lawrence,et al.  Illuminating the chemistry of life: design, synthesis, and applications of "caged" and related photoresponsive compounds. , 2009, ACS chemical biology.

[52]  Dmitri I Svergun,et al.  A Helical Structural Nucleus Is the Primary Elongating Unit of Insulin Amyloid Fibrils , 2007, PLoS biology.

[53]  Jesper Søndergaard Pedersen,et al.  A SAXS study of glucagon fibrillation. , 2009, Journal of molecular biology.

[54]  Jae Hyuk Lee,et al.  Direct observation of myoglobin structural dynamics from 100 picoseconds to 1 microsecond with picosecond X-ray solution scattering. , 2011, Chemical communications.