Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser

Yanyong Kang, X. Edward Zhou, Xiang Gao, Yuanzheng He, Wei Liu, Andrii Ishchenko, Anton Barty, Thomas A. White, Oleksandr Yefanov, Gye Won Han, Qingping Xu, Parker W. de Waal, Jiyuan Ke, M. H. Eileen Tan, Chenghai Zhang, Arne Moeller, Graham M. West, Bruce D. Pascal, Ned Van Eps, Lydia N. Caro, Sergey A. Vishnivetskiy, Regina J. Lee, Kelly M. Suino-Powell, Xin Gu, Kuntal Pal, Jinming Ma, Xiaoyong Zhi, Sébastien Boutet, Garth J. Williams, Marc Messerschmidt, Cornelius Gati, Nadia A. Zatsepin, Dingjie Wang, Daniel James, Shibom Basu, Shatabdi Roy-Chowdhury, Chelsie E. Conrad, Jesse Coe, Haiguang Liu, Stella Lisova, Christopher Kupitz, Ingo Grotjohann, Raimund Fromme, Yi Jiang, Minjia Tan, Huaiyu Yang, Jun Li, Meitian Wang, Zhong Zheng, Dianfan Li, Nicole Howe, Yingming Zhao, Jörg Standfuss, Kay Diederichs, Yuhui Dong, Clinton S. Potter, Bridget Carragher, Martin Caffrey, Hualiang Jiang, Henry N. Chapman, John C. H. Spence, Petra Fromme, Uwe Weierstall, Oliver P. Ernst, Vsevolod Katritch, Vsevolod V. Gurevich, Patrick R. Griffin, Wayne L. Hubbell, Raymond C. Stevens, Vadim Cherezov, Karsten Melcher and H. Eric Xu ()
Additional contact information
Yanyong Kang: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
X. Edward Zhou: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
Xiang Gao: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
Yuanzheng He: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
Wei Liu: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Andrii Ishchenko: Bridge Institute, University of Southern California
Anton Barty: Center for Free Electron Laser Science, Deutsches Elektronen-Synchrotron DESY
Thomas A. White: Center for Free Electron Laser Science, Deutsches Elektronen-Synchrotron DESY
Oleksandr Yefanov: Center for Free Electron Laser Science, Deutsches Elektronen-Synchrotron DESY
Gye Won Han: Bridge Institute, University of Southern California
Qingping Xu: Joint Center for Structural Genomics, Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory
Parker W. de Waal: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
Jiyuan Ke: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
M. H. Eileen Tan: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
Chenghai Zhang: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
Arne Moeller: The National Resource for Automated Molecular Microscopy, New York Structural Biology Center
Graham M. West: The Scripps Research Institute, Scripps Florida
Bruce D. Pascal: The Scripps Research Institute, Scripps Florida
Ned Van Eps: University of California
Lydia N. Caro: University of Toronto
Sergey A. Vishnivetskiy: Vanderbilt University
Regina J. Lee: Vanderbilt University
Kelly M. Suino-Powell: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
Xin Gu: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
Kuntal Pal: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
Jinming Ma: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
Xiaoyong Zhi: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
Sébastien Boutet: Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory
Garth J. Williams: Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory
Marc Messerschmidt: Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory
Cornelius Gati: Center for Free Electron Laser Science, Deutsches Elektronen-Synchrotron DESY
Nadia A. Zatsepin: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Dingjie Wang: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Daniel James: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Shibom Basu: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Shatabdi Roy-Chowdhury: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Chelsie E. Conrad: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Jesse Coe: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Haiguang Liu: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Stella Lisova: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Christopher Kupitz: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Ingo Grotjohann: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Raimund Fromme: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Yi Jiang: State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences
Minjia Tan: State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences
Huaiyu Yang: State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences
Jun Li: Yong Loo Lin School of Medicine, National University of Singapore
Meitian Wang: Swiss Light Source at Paul Scherrer Institute
Zhong Zheng: Bridge Institute, University of Southern California
Dianfan Li: School of Medicine and School of Biochemistry and Immunology, Trinity College
Nicole Howe: School of Medicine and School of Biochemistry and Immunology, Trinity College
Yingming Zhao: BioXFEL, NSF Science and Technology Center
Jörg Standfuss: Laboratory of Biomolecular Research at Paul Scherrer Institute
Kay Diederichs: Universität Konstanz
Yuhui Dong: Beijing Synchrotron Radiation Facility, Institute of High Energy Physics, Chinese Academy of Sciences
Clinton S. Potter: The National Resource for Automated Molecular Microscopy, New York Structural Biology Center
Bridget Carragher: The National Resource for Automated Molecular Microscopy, New York Structural Biology Center
Martin Caffrey: School of Medicine and School of Biochemistry and Immunology, Trinity College
Hualiang Jiang: State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences
Henry N. Chapman: Center for Free Electron Laser Science, Deutsches Elektronen-Synchrotron DESY
John C. H. Spence: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Petra Fromme: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Uwe Weierstall: and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University
Oliver P. Ernst: University of Toronto
Vsevolod Katritch: Bridge Institute, University of Southern California
Vsevolod V. Gurevich: Vanderbilt University
Patrick R. Griffin: The Scripps Research Institute, Scripps Florida
Wayne L. Hubbell: University of California
Raymond C. Stevens: Bridge Institute, University of Southern California
Vadim Cherezov: Bridge Institute, University of Southern California
Karsten Melcher: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute
H. Eric Xu: Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute

Nature, 2015, vol. 523, issue 7562, 561-567

Abstract: Abstract G-protein-coupled receptors (GPCRs) signal primarily through G proteins or arrestins. Arrestin binding to GPCRs blocks G protein interaction and redirects signalling to numerous G-protein-independent pathways. Here we report the crystal structure of a constitutively active form of human rhodopsin bound to a pre-activated form of the mouse visual arrestin, determined by serial femtosecond X-ray laser crystallography. Together with extensive biochemical and mutagenesis data, the structure reveals an overall architecture of the rhodopsin–arrestin assembly in which rhodopsin uses distinct structural elements, including transmembrane helix 7 and helix 8, to recruit arrestin. Correspondingly, arrestin adopts the pre-activated conformation, with a ∼20° rotation between the amino and carboxy domains, which opens up a cleft in arrestin to accommodate a short helix formed by the second intracellular loop of rhodopsin. This structure provides a basis for understanding GPCR-mediated arrestin-biased signalling and demonstrates the power of X-ray lasers for advancing the frontiers of structural biology.

Date: 2015
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DOI: 10.1038/nature14656

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