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PMID: 26200343 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

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

Nature ·Vol. 523 ·No. 7562 ·2015-07-30 ·Pages 561-7

Kang Y, Zhou XE, Gao X, He Y, Liu W, Ishchenko A, Barty A, White TA, Yefanov O, Han GW, Xu Q, de Waal PW, Ke J, Tan MH, Zhang C, Moeller A, West GM, Pascal BD, Van Eps N, Caro LN, Vishnivetskiy SA, Lee RJ, Suino-Powell KM, Gu X, Pal K, Ma J, Zhi X, Boutet S, Williams GJ, Messerschmidt M, Gati C, Zatsepin NA, Wang D, James D, Basu S, Roy-Chowdhury S, Conrad CE, Coe J, Liu H, Lisova S, Kupitz C, Grotjohann I, Fromme R, Jiang Y, Tan M, Yang H, Li J, Wang M, Zheng Z, Li D, Howe N, Zhao Y, Standfuss J, Diederichs K, Dong Y, Potter CS, Carragher B, Caffrey M, Jiang H, Chapman HN, Spence JC, Fromme P, Weierstall U, Ernst OP, Katritch V, Gurevich VV, Griffin PR, Hubbell WL, Stevens RC, Cherezov V, Melcher K, Xu HE

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.

MeSH Terms
Animals Arrestin/chemistry,metabolism Binding Sites Crystallography, X-Ray Disulfides/chemistry,metabolism Humans Lasers Mice Models, Molecular Multiprotein Complexes/biosynthesis,chemistry,metabolism Protein Binding Reproducibility of Results Rhodopsin/chemistry,metabolism Signal Transduction X-Rays
Chemicals
Arrestin Disulfides Multiprotein Complexes Rhodopsin
Authors & Affiliations
72 authors, click to expand affiliations / ORCID
Kang Yanyong
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
Zhou X Edward
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
Gao Xiang
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
He Yuanzheng
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
Liu Wei
Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA.
Ishchenko Andrii
Department of Chemistry, Bridge Institute, University of Southern California, Los Angeles, California 90089, USA.
Barty Anton
Center for Free Electron Laser Science, Deutsches Elektronen-Synchrotron DESY, 22607 Hamburg, Germany.
White Thomas A
Center for Free Electron Laser Science, Deutsches Elektronen-Synchrotron DESY, 22607 Hamburg, Germany.
Yefanov Oleksandr
Center for Free Electron Laser Science, Deutsches Elektronen-Synchrotron DESY, 22607 Hamburg, Germany.
Han Gye Won
Department of Chemistry, Bridge Institute, University of Southern California, Los Angeles, California 90089, USA.
Xu Qingping
Joint Center for Structural Genomics, Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Menlo Park, California 94025, USA.
de Waal Parker W
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
Ke Jiyuan
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
Tan M H Eileen
1] Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA [2] Department of Obstetrics &Gynecology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore.
Zhang Chenghai
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
Moeller Arne
The National Resource for Automated Molecular Microscopy, New York Structural Biology Center, New York, New York 10027, USA.
West Graham M
Department of Molecular Therapeutics, The Scripps Research Institute, Scripps Florida, Jupiter, Florida 33458, USA.
Pascal Bruce D
Department of Molecular Therapeutics, The Scripps Research Institute, Scripps Florida, Jupiter, Florida 33458, USA.
Van Eps Ned
Jules Stein Eye Institute and Department of Chemistry and Biochemistry, University of California, Los Angeles, California 90095, USA.
Caro Lydia N
Department of Biochemistry, University of Toronto, Toronto, Ontario M5S 1A8, Canada.
Vishnivetskiy Sergey A
Department of Pharmacology, Vanderbilt University, Nashville, Tennessee 37232, USA.
Lee Regina J
Department of Pharmacology, Vanderbilt University, Nashville, Tennessee 37232, USA.
Suino-Powell Kelly M
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
Gu Xin
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
Pal Kuntal
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
Ma Jinming
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
Zhi Xiaoyong
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
Boutet Sébastien
Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory, Menlo Park, California 94025, USA.
Williams Garth J
Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory, Menlo Park, California 94025, USA.
Messerschmidt Marc
1] Linac Coherent Light Source (LCLS), SLAC National Accelerator Laboratory, Menlo Park, California 94025, USA [2] BioXFEL, NSF Science and Technology Center, 700 Ellicott Street, Buffalo, New York 14203, USA.
Gati Cornelius
Center for Free Electron Laser Science, Deutsches Elektronen-Synchrotron DESY, 22607 Hamburg, Germany.
Zatsepin Nadia A
1] Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA [2] Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
Wang Dingjie
1] Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA [2] Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
James Daniel
1] Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA [2] Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
Basu Shibom
1] Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA [2] Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
Roy-Chowdhury Shatabdi
1] Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA [2] Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
Conrad Chelsie E
Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA.
Coe Jesse
Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA.
Liu Haiguang
1] Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA [2] Beijing Computational Science Research Center, Haidian District, Beijing 10084, China.
Lisova Stella
Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA.
Kupitz Christopher
1] Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA [2] Department of Physics, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin 53211, USA.
Grotjohann Ingo
Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA.
Fromme Raimund
Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA.
Jiang Yi
State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China.
Tan Minjia
State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China.
Yang Huaiyu
State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China.
Li Jun
Department of Obstetrics &Gynecology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore.
Wang Meitian
Swiss Light Source at Paul Scherrer Institute, CH-5232 Villigen, Switzerland.
Zheng Zhong
Department of Biological Sciences, Bridge Institute, University of Southern California, Los Angeles, California 90089, USA.
Li Dianfan
School of Medicine and School of Biochemistry and Immunology, Trinity College, Dublin 2, Ireland.
Howe Nicole
School of Medicine and School of Biochemistry and Immunology, Trinity College, Dublin 2, Ireland.
Zhao Yingming
1] BioXFEL, NSF Science and Technology Center, 700 Ellicott Street, Buffalo, New York 14203, USA [2] Ben May Department for Cancer Research, University of Chicago, Chicago, Illinois 60637, USA.
Standfuss Jörg
Laboratory of Biomolecular Research at Paul Scherrer Institute, CH-5232 Villigen, Switzerland.
Diederichs Kay
Department of Biology, Universität Konstanz, 78457 Konstanz, Germany.
Dong Yuhui
Beijing Synchrotron Radiation Facility, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, China.
Potter Clinton S
The National Resource for Automated Molecular Microscopy, New York Structural Biology Center, New York, New York 10027, USA.
Carragher Bridget
The National Resource for Automated Molecular Microscopy, New York Structural Biology Center, New York, New York 10027, USA.
Caffrey Martin
School of Medicine and School of Biochemistry and Immunology, Trinity College, Dublin 2, Ireland.
Jiang Hualiang
State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China.
Chapman Henry N
1] Center for Free Electron Laser Science, Deutsches Elektronen-Synchrotron DESY, 22607 Hamburg, Germany [2] Centre for Ultrafast Imaging, 22761 Hamburg, Germany.
Spence John C H
1] Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA [2] Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
Fromme Petra
Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA.
Weierstall Uwe
1] Department of Chemistry and Biochemistry, and Center for Applied Structural Discovery, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-1604, USA [2] Department of Physics, Arizona State University, Tempe, Arizona 85287, USA.
Ernst Oliver P
1] Department of Biochemistry, University of Toronto, Toronto, Ontario M5S 1A8, Canada [2] Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada.
Katritch Vsevolod
Department of Biological Sciences, Bridge Institute, University of Southern California, Los Angeles, California 90089, USA.
Gurevich Vsevolod V
Department of Pharmacology, Vanderbilt University, Nashville, Tennessee 37232, USA.
Griffin Patrick R
Department of Molecular Therapeutics, The Scripps Research Institute, Scripps Florida, Jupiter, Florida 33458, USA.
Hubbell Wayne L
Jules Stein Eye Institute and Department of Chemistry and Biochemistry, University of California, Los Angeles, California 90095, USA.
Stevens Raymond C
1] Department of Chemistry, Bridge Institute, University of Southern California, Los Angeles, California 90089, USA [2] Department of Biological Sciences, Bridge Institute, University of Southern California, Los Angeles, California 90089, USA [3] iHuman Institute, ShanghaiTech University, 2F Building 6, 99 Haike Road, Pudong New District, Shanghai 201210, China.
Cherezov Vadim
Department of Chemistry, Bridge Institute, University of Southern California, Los Angeles, California 90089, USA.
Melcher Karsten
Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA.
Xu H Eric
1] Laboratory of Structural Sciences, Center for Structural Biology and Drug Discovery, Van Andel Research Institute, Grand Rapids, Michigan 49503, USA [2] VARI-SIMM Center, Center for Structure and Function of Drug Targets, CAS-Key Laboratory of Receptor Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China.
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Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
DOI
10.1038/nature14656
Published
2015-07-30
Epub
2015-00-22
Pages
561-7
Language
English
Region
England
NLM ID
0410462
PMCID
PMC4521999
Subset
IM
Grants
NIDDK NIH HHS · R01 DK066202 · United States
NIGMS NIH HHS · GM097463 · United States
NIGMS NIH HHS · U54 GM094599 · United States
NIDDK NIH HHS · DK071662 · United States
NIGMS NIH HHS · P41 GM103310 · United States
NIGMS NIH HHS · GM073197 · United States
NCRR NIH HHS · P41RR001209 · United States
NIGMS NIH HHS · R01 GM077561 · United States
NIGMS NIH HHS · R01 GM097463 · United States
NIGMS NIH HHS · R01 GM095583 · United States
NIGMS NIH HHS · R01 GM109955 · United States
NIGMS NIH HHS · U54 GM094586 · United States
NEI NIH HHS · P30 EY000331 · United States
NEI NIH HHS · EY011500 · United States
NIGMS NIH HHS · P50 GM073197 · United States
NIGMS NIH HHS · U54 GM094618 · United States
NEI NIH HHS · R01 EY005216 · United States
NIGMS NIH HHS · R01 GM102545 · United States
NIGMS NIH HHS · GM095583 · United States
NIGMS NIH HHS · P41GM103393 · United States
NIDDK NIH HHS · R01 DK071662 · United States
NIGMS NIH HHS · R01 GM104212 · United States
NIGMS NIH HHS · GM103310 · United States
NIGMS NIH HHS · R01 GM108635 · United States
NIGMS NIH HHS · GM077561 · United States
NEI NIH HHS · EY005216 · United States
NEI NIH HHS · R01 EY011500 · United States
NIGMS NIH HHS · P50 GM073210 · United States
NIGMS NIH HHS · R01 GM087413 · United States
NIGMS NIH HHS · GM104212 · United States
NCRR NIH HHS · S10 RR027270 · United States
NEI NIH HHS · P30EY000331 · United States
NIGMS NIH HHS · GM108635 · United States
NIGMS NIH HHS · GM102545 · United States
Databases
PDB
4ZWJ
Corrections
CommentIn
PMID: 26200346
CommentIn
PMID: 27272251
External Links
PubMed source DOI: 10.1038/nature14656 PMC Full Text View journal details
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