Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser

David Arnlund; Linda C. Johansson; Cecilia Wickstrand; Anton Barty; Garth J. Williams; Erik Malmerberg; Jan Davidsson; Despina Milathianaki; Daniel P. DePonte; Robert L. Shoeman; Dingjie Wang; Daniel James; Gergely Katona; Sebastian Westenhoff; Thomas A. White; Andrew Aquila; Sadia Bari; Peter Berntsen; Mike Bogan; Tim Brandt Van Driel; R. Bruce Doak; Kasper Skov Kjær; Matthias Frank; Raimund Fromme; Ingo Grotjohann; Robert Henning; Mark S. Hunter; Richard Kirian; Irina Kosheleva; Christopher Kupitz; Mengning Liang; Andrew V. Martin; Martin Meedom Nielsen; Marc Messerschmidt; M. Marvin Seibert; Jennie Sjöhamn; Francesco Stellato; Uwe Weierstall; Nadia Zatsepin; John Spence; Petra Fromme; Ilme Schlichting; Sébastien Boutet; Gerrit Groenhof; Henry N. Chapman; Richard Neutze

doi:10.1038/nmeth.3067

Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser

David Arnlund, Linda C. Johansson, Cecilia Wickstrand, Anton Barty, Garth J. Williams, Erik Malmerberg, Jan Davidsson, Despina Milathianaki, Daniel P. DePonte, Robert L. Shoeman, Dingjie Wang, Daniel James, Gergely Katona, Sebastian Westenhoff, Thomas A. White, Andrew Aquila, Sadia Bari, Peter Berntsen, Mike Bogan, Tim Brandt Van DrielR. Bruce Doak, Kasper Skov Kjær, Matthias Frank, Raimund Fromme, Ingo Grotjohann, Robert Henning, Mark S. Hunter, Richard Kirian, Irina Kosheleva, Christopher Kupitz, Mengning Liang, Andrew V. Martin, Martin Meedom Nielsen, Marc Messerschmidt, M. Marvin Seibert, Jennie Sjöhamn, Francesco Stellato, Uwe Weierstall, Nadia Zatsepin, John Spence, Petra Fromme, Ilme Schlichting, Sébastien Boutet, Gerrit Groenhof, Henry N. Chapman, Richard Neutze

Research output: Contribution to journal › Article › peer-review

157 Scopus citations

Abstract

We describe a method to measure ultrafast protein structural changes using time-resolved wide-angle X-ray scattering at an X-ray free-electron laser. We demonstrated this approach using multiphoton excitation of the Blastochloris viridis photosynthetic reaction center, observing an ultrafast global conformational change that arises within picoseconds and precedes the propagation of heat through the protein. This provides direct structural evidence for a 'protein quake': the hypothesis that proteins rapidly dissipate energy through quake-like structural motions.

Original language	English (US)
Pages (from-to)	923-926
Number of pages	4
Journal	Nature Methods
Volume	11
Issue number	9
DOIs	https://doi.org/10.1038/nmeth.3067
State	Published - Sep 2014

ASJC Scopus subject areas

Biotechnology
Biochemistry
Molecular Biology
Cell Biology

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Arnlund, D., Johansson, L. C., Wickstrand, C., Barty, A., Williams, G. J., Malmerberg, E., Davidsson, J., Milathianaki, D., DePonte, D. P., Shoeman, R. L., Wang, D., James, D., Katona, G., Westenhoff, S., White, T. A., Aquila, A., Bari, S., Berntsen, P., Bogan, M., ... Neutze, R. (2014). Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser. Nature Methods, 11(9), 923-926. https://doi.org/10.1038/nmeth.3067

Arnlund, D, Johansson, LC, Wickstrand, C, Barty, A, Williams, GJ, Malmerberg, E, Davidsson, J, Milathianaki, D, DePonte, DP, Shoeman, RL, Wang, D, James, D, Katona, G, Westenhoff, S, White, TA, Aquila, A, Bari, S, Berntsen, P, Bogan, M, Van Driel, TB, Doak, RB, Kjær, KS, Frank, M, Fromme, R, Grotjohann, I, Henning, R, Hunter, MS, Kirian, R, Kosheleva, I, Kupitz, C, Liang, M, Martin, AV, Nielsen, MM, Messerschmidt, M, Seibert, MM, Sjöhamn, J, Stellato, F, Weierstall, U, Zatsepin, N, Spence, J, Fromme, P, Schlichting, I, Boutet, S, Groenhof, G, Chapman, HN & Neutze, R 2014, 'Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser', Nature Methods, vol. 11, no. 9, pp. 923-926. https://doi.org/10.1038/nmeth.3067

@article{07feac0b0db64161905dc238aa777609,

title = "Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser",

abstract = "We describe a method to measure ultrafast protein structural changes using time-resolved wide-angle X-ray scattering at an X-ray free-electron laser. We demonstrated this approach using multiphoton excitation of the Blastochloris viridis photosynthetic reaction center, observing an ultrafast global conformational change that arises within picoseconds and precedes the propagation of heat through the protein. This provides direct structural evidence for a 'protein quake': the hypothesis that proteins rapidly dissipate energy through quake-like structural motions.",

author = "David Arnlund and Johansson, {Linda C.} and Cecilia Wickstrand and Anton Barty and Williams, {Garth J.} and Erik Malmerberg and Jan Davidsson and Despina Milathianaki and DePonte, {Daniel P.} and Shoeman, {Robert L.} and Dingjie Wang and Daniel James and Gergely Katona and Sebastian Westenhoff and White, {Thomas A.} and Andrew Aquila and Sadia Bari and Peter Berntsen and Mike Bogan and {Van Driel}, {Tim Brandt} and Doak, {R. Bruce} and Kj{\ae}r, {Kasper Skov} and Matthias Frank and Raimund Fromme and Ingo Grotjohann and Robert Henning and Hunter, {Mark S.} and Richard Kirian and Irina Kosheleva and Christopher Kupitz and Mengning Liang and Martin, {Andrew V.} and Nielsen, {Martin Meedom} and Marc Messerschmidt and Seibert, {M. Marvin} and Jennie Sj{\"o}hamn and Francesco Stellato and Uwe Weierstall and Nadia Zatsepin and John Spence and Petra Fromme and Ilme Schlichting and S{\'e}bastien Boutet and Gerrit Groenhof and Chapman, {Henry N.} and Richard Neutze",

note = "Funding Information: Experiments were carried out at the LCLS, a national user facility operated by Stanford University on behalf of the US Department of Energy (DOE), Office of Basic Energy Sciences. We acknowledge financial support from the Swedish Science Research Council (VR), the Swedish Foundation for International Cooperation in Research and Higher Education (STINT), the Swedish Strategic Research Foundation (SSF), the Knut and Alice Wallenberg Foundation, the US National Science Foundation (NSF) and its bioXFEL Science and Technology Center (NSF 1231306), the US National Institute of Health (NIH), the DOE Office of Basic Energy Sciences, the Hamburg Ministry of Science and Research, the Joachim Herz Stiftung, the Deutsche Forschungsgemeinschaft (DFG), the German Federal Ministry for Education and Research (BMBF), a Marie Curie International Incoming Fellowship of the European Union, the Academy of Finland, the Max Planck Society, the Danish National Research Foundations Centre for Molecular Movies, DANSCATT, the UCOP Lab Fee Program (award no. 118036) and the LLNL Lab-directed Research & Development Program (12-ERD-031).",

year = "2014",

month = sep,

doi = "10.1038/nmeth.3067",

language = "English (US)",

volume = "11",

pages = "923--926",

journal = "Nature Methods",

issn = "1548-7091",

publisher = "Nature Publishing Group",

number = "9",

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TY - JOUR

T1 - Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser

AU - Arnlund, David

AU - Johansson, Linda C.

AU - Wickstrand, Cecilia

AU - Barty, Anton

AU - Williams, Garth J.

AU - Malmerberg, Erik

AU - Davidsson, Jan

AU - Milathianaki, Despina

AU - DePonte, Daniel P.

AU - Shoeman, Robert L.

AU - Wang, Dingjie

AU - James, Daniel

AU - Katona, Gergely

AU - Westenhoff, Sebastian

AU - White, Thomas A.

AU - Aquila, Andrew

AU - Bari, Sadia

AU - Berntsen, Peter

AU - Bogan, Mike

AU - Van Driel, Tim Brandt

AU - Doak, R. Bruce

AU - Kjær, Kasper Skov

AU - Frank, Matthias

AU - Fromme, Raimund

AU - Grotjohann, Ingo

AU - Henning, Robert

AU - Hunter, Mark S.

AU - Kirian, Richard

AU - Kosheleva, Irina

AU - Kupitz, Christopher

AU - Liang, Mengning

AU - Martin, Andrew V.

AU - Nielsen, Martin Meedom

AU - Messerschmidt, Marc

AU - Seibert, M. Marvin

AU - Sjöhamn, Jennie

AU - Stellato, Francesco

AU - Weierstall, Uwe

AU - Zatsepin, Nadia

AU - Spence, John

AU - Fromme, Petra

AU - Schlichting, Ilme

AU - Boutet, Sébastien

AU - Groenhof, Gerrit

AU - Chapman, Henry N.

AU - Neutze, Richard

N1 - Funding Information: Experiments were carried out at the LCLS, a national user facility operated by Stanford University on behalf of the US Department of Energy (DOE), Office of Basic Energy Sciences. We acknowledge financial support from the Swedish Science Research Council (VR), the Swedish Foundation for International Cooperation in Research and Higher Education (STINT), the Swedish Strategic Research Foundation (SSF), the Knut and Alice Wallenberg Foundation, the US National Science Foundation (NSF) and its bioXFEL Science and Technology Center (NSF 1231306), the US National Institute of Health (NIH), the DOE Office of Basic Energy Sciences, the Hamburg Ministry of Science and Research, the Joachim Herz Stiftung, the Deutsche Forschungsgemeinschaft (DFG), the German Federal Ministry for Education and Research (BMBF), a Marie Curie International Incoming Fellowship of the European Union, the Academy of Finland, the Max Planck Society, the Danish National Research Foundations Centre for Molecular Movies, DANSCATT, the UCOP Lab Fee Program (award no. 118036) and the LLNL Lab-directed Research & Development Program (12-ERD-031).

PY - 2014/9

Y1 - 2014/9

N2 - We describe a method to measure ultrafast protein structural changes using time-resolved wide-angle X-ray scattering at an X-ray free-electron laser. We demonstrated this approach using multiphoton excitation of the Blastochloris viridis photosynthetic reaction center, observing an ultrafast global conformational change that arises within picoseconds and precedes the propagation of heat through the protein. This provides direct structural evidence for a 'protein quake': the hypothesis that proteins rapidly dissipate energy through quake-like structural motions.

AB - We describe a method to measure ultrafast protein structural changes using time-resolved wide-angle X-ray scattering at an X-ray free-electron laser. We demonstrated this approach using multiphoton excitation of the Blastochloris viridis photosynthetic reaction center, observing an ultrafast global conformational change that arises within picoseconds and precedes the propagation of heat through the protein. This provides direct structural evidence for a 'protein quake': the hypothesis that proteins rapidly dissipate energy through quake-like structural motions.

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U2 - 10.1038/nmeth.3067

DO - 10.1038/nmeth.3067

M3 - Article

C2 - 25108686

AN - SCOPUS:84907023503

SN - 1548-7091

VL - 11

SP - 923

EP - 926

JO - Nature Methods

JF - Nature Methods

IS - 9

ER -

Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser

Abstract

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