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

被引:592
作者
Kang, Yanyong [1 ]
Zhou, X. Edward [1 ]
Gao, Xiang [1 ]
He, Yuanzheng [1 ]
Liu, Wei [2 ,3 ]
Ishchenko, Andrii [4 ]
Barty, Anton [5 ]
Sathish, D. [5 ]
Yefanov, Oleksandr [5 ]
Han, Gye Won [4 ]
Xu, Qingping [6 ]
de Waal, Parker W. [1 ]
Ke, Jiyuan [1 ]
Tan, M. H. Eileen [1 ,7 ]
Zhang, Chenghai [1 ]
Moeller, Arne [8 ]
West, Graham M. [9 ]
Pascal, Bruce D. [9 ]
Van Eps, Ned [10 ,11 ]
Caro, Lydia N. [12 ]
Vishnivetskiy, Sergey A. [13 ]
Lee, Regina J. [13 ]
Suino-Powell, Kelly M. [13 ]
Gu, Xin [1 ]
Pal, Kuntal [1 ]
Ma, Jinming [1 ]
Zhi, Xiaoyong [1 ]
Boutet, Sebastien [14 ]
Williams, Garth J. [14 ]
Messerschmidt, Marc [14 ,15 ]
Gati, Cornelius [5 ]
Zatsepin, Nadia A. [2 ,3 ,16 ]
Wang, Dingjie [2 ,3 ,16 ]
James, Daniel [2 ,3 ,16 ]
Basu, Shibom [2 ,3 ,16 ]
Roy-Chowdhury, Shatabdi [2 ,3 ,16 ]
Conrad, Chelsie E. [2 ,3 ]
Coe, Jesse [2 ,3 ]
Liu, Haiguang [2 ,3 ,17 ]
Lisova, Stella [2 ,3 ]
Kupitz, Christopher [2 ,3 ,18 ]
Grotjohann, Ingo [2 ,3 ]
Fromme, Raimund [2 ,3 ]
Jiang, Yi [19 ]
Tan, Minjia [19 ]
Yang, Huaiyu [19 ]
Li, Jun [7 ]
Wang, Meitian [20 ]
Zheng, Zhong [21 ]
Li, Dianfan [22 ]
机构
[1] Van Andel Res Inst, Ctr Struct Biol & Drug Discovery, Lab Struct Sci, Grand Rapids, MI 49503 USA
[2] Arizona State Univ, Dept Chem & Biochem, Biodesign Inst, Tempe, AZ 85287 USA
[3] Arizona State Univ, Ctr Appl Struct Discovery, Biodesign Inst, Tempe, AZ 85287 USA
[4] Univ So Calif, Bridge Inst, Dept Chem, Los Angeles, CA 90089 USA
[5] Deutsch Elektronen Synchrotron DESY, Ctr Free Elect Laser Sci, D-22607 Hamburg, Germany
[6] SLAC Natl Accelerator Lab, Stanford Synchrotron Radiat Lightsource, Joint Ctr Struct Genom, Menlo Pk, CA 94025 USA
[7] Natl Univ Singapore, Yong Loo Lin Sch Med, Dept Obstet & Gynecol, Singapore 117595, Singapore
[8] New York Struct Biol Ctr, Natl Resource Automated Mol Microscopy, New York, NY 10027 USA
[9] Scripps Florida, Scripps Res Inst, Dept Mol Therapeut, Jupiter, FL 33458 USA
[10] Univ Calif Los Angeles, Jules Stein Eye Inst, Los Angeles, CA 90095 USA
[11] Univ Calif Los Angeles, Dept Chem & Biochem, Los Angeles, CA 90095 USA
[12] Univ Toronto, Dept Biochem, Toronto, ON M5S 1A8, Canada
[13] Vanderbilt Univ, Dept Pharmacol, Nashville, TN 37232 USA
[14] SLAC Natl Accelerator Lab, LCLS, Menlo Pk, CA 94025 USA
[15] NSF Sci & Technol Ctr, BioXFEL, Buffalo, NY 14203 USA
[16] Arizona State Univ, Dept Phys, Tempe, AZ 85287 USA
[17] Beijing Computat Sci Res Ctr, Beijing 10084, Peoples R China
[18] Univ Wisconsin, Dept Phys, Milwaukee, WI 53211 USA
[19] Chinese Acad Sci, Shanghai Inst Mat Med, State Key Lab Drug Res, Shanghai 201203, Peoples R China
[20] Paul Scherrer Inst, Swiss Light Source, CH-5232 Villigen, Switzerland
[21] Univ So Calif, Bridge Inst, Dept Biol Sci, Los Angeles, CA 90089 USA
[22] Univ Dublin Trinity Coll, Sch Med & Sch Biochem & Immunol, Dublin 2, Ireland
[23] Univ Chicago, Ben May Dept Canc Res, Chicago, IL 60637 USA
[24] Paul Scherrer Inst, Lab Biomol Res, CH-5232 Villigen, Switzerland
[25] Univ Konstanz, Dept Biol, D-78457 Constance, Germany
[26] Chinese Acad Sci, Beijing Synchrotron Radiat Facil, Beijing 100049, Peoples R China
[27] Ctr Ultrafast Imaging, D-22761 Hamburg, Germany
[28] Univ Toronto, Dept Mol Genet, Toronto, ON M5S 1A8, Canada
[29] ShanghaiTech Univ, iHuman Inst, Shanghai 201210, Peoples R China
[30] Chinese Acad Sci, Shanghai Inst Mat Med, CAS Key Lab Receptor Res, VARI SIMM Ctr,Ctr Struct & Funct Drug Targets, Shanghai 201203, Peoples R China
基金
美国国家卫生研究院; 瑞士国家科学基金会; 爱尔兰科学基金会;
关键词
LIPIDIC CUBIC PHASE; VISUAL ARRESTIN; SPACE-GROUP; PROTEIN; ACTIVATION; BINDING; EXPRESSION; MICROSCOPY; PIGGYBAC; SYSTEM;
D O I
10.1038/nature14656
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
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 similar to 20 degrees 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.
引用
收藏
页码:561 / +
页数:31
相关论文
共 97 条
[1]   PHENIX: a comprehensive Python']Python-based system for macromolecular structure solution [J].
Adams, Paul D. ;
Afonine, Pavel V. ;
Bunkoczi, Gabor ;
Chen, Vincent B. ;
Davis, Ian W. ;
Echols, Nathaniel ;
Headd, Jeffrey J. ;
Hung, Li-Wei ;
Kapral, Gary J. ;
Grosse-Kunstleve, Ralf W. ;
McCoy, Airlie J. ;
Moriarty, Nigel W. ;
Oeffner, Robert ;
Read, Randy J. ;
Richardson, David C. ;
Richardson, Jane S. ;
Terwilliger, Thomas C. ;
Zwart, Peter H. .
ACTA CRYSTALLOGRAPHICA SECTION D-STRUCTURAL BIOLOGY, 2010, 66 :213-221
[2]   Microscale fluorescent thermal stability assay for membrane proteins [J].
Alexandrov, Alexander I. ;
Mileni, Mauro ;
Chien, Ellen Y. T. ;
Hanson, Michael A. ;
Stevens, Raymond C. .
STRUCTURE, 2008, 16 (03) :351-359
[3]   High-resolution distance mapping in rhodopsin reveals the pattern of helix movement due to activation [J].
Altenbach, Christian ;
Kusnetzow, Ana Karin ;
Ernst, Oliver P. ;
Hofmann, Klaus Peter ;
Hubbell, Wayne L. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2008, 105 (21) :7439-7444
[4]   Development of a new physics-based internal coordinate mechanics force field and its application to protein loop modeling [J].
Arnautova, Yelena A. ;
Abagyan, Ruben A. ;
Totrov, Maxim .
PROTEINS-STRUCTURE FUNCTION AND BIOINFORMATICS, 2011, 79 (02) :477-498
[5]  
Ballesteros J. A., 1995, Neuroscience Methods, V25, P366, DOI [10.1016/S1043-9471(05)80049-7, DOI 10.1016/S1043-9471(05)80049-7, DOI 10.1016/S1043-9471]
[6]   The genetic design of signaling cascades to record receptor activation [J].
Barnea, Gilad ;
Strapps, Walter ;
Herrada, Gilles ;
Berman, Yemiliya ;
Ong, Jane ;
Kloss, Brian ;
Axel, Richard ;
Lee, Kevin J. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2008, 105 (01) :64-69
[7]   Cheetah: software for high-throughput reduction and analysis of serial femtosecond X-ray diffraction data [J].
Barty, Anton ;
Kirian, Richard A. ;
Maia, Filipe R. N. C. ;
Hantke, Max ;
Yoon, Chun Hong ;
White, Thomas A. ;
Chapman, Henry .
JOURNAL OF APPLIED CRYSTALLOGRAPHY, 2014, 47 :1118-1131
[8]   iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM [J].
Battye, T. Geoff G. ;
Kontogiannis, Luke ;
Johnson, Owen ;
Powell, Harold R. ;
Leslie, Andrew G. W. .
ACTA CRYSTALLOGRAPHICA SECTION D-BIOLOGICAL CRYSTALLOGRAPHY, 2011, 67 :271-281
[9]   Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins [J].
Bayburt, Timothy H. ;
Leitz, Andrew J. ;
Xie, Guifu ;
Oprian, Daniel D. ;
Sligar, Stephen G. .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2007, 282 (20) :14875-14881
[10]   Monomeric Rhodopsin Is Sufficient for Normal Rhodopsin Kinase (GRK1) Phosphorylation and Arrestin-1 Binding [J].
Bayburt, Timothy H. ;
Vishnivetskiy, Sergey A. ;
McLean, Mark A. ;
Morizumi, Takefumi ;
Huang, Chih-chin ;
Tesmer, John J. G. ;
Ernst, Oliver P. ;
Sligar, Stephen G. ;
Gurevich, Vsevolod V. .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2011, 286 (02) :1420-1428