DOI: 10.7554/elife.32493. The structure of the COPI coat determined within the cell

The structure of the COPI coat determined within the cell

10.7554/elife.32493

Crossref journal-article

eLife Sciences Publications, Ltd

eLife (4374)

Abstract

COPI-coated vesicles mediate trafficking within the Golgi apparatus and from the Golgi to the endoplasmic reticulum. The structures of membrane protein coats, including COPI, have been extensively studied with in vitro reconstitution systems using purified components. Previously we have determined a complete structural model of the in vitro reconstituted COPI coat (Dodonova et al., 2017). Here, we applied cryo-focused ion beam milling, cryo-electron tomography and subtomogram averaging to determine the native structure of the COPI coat within vitrified Chlamydomonas reinhardtii cells. The native algal structure resembles the in vitro mammalian structure, but additionally reveals cargo bound beneath β’–COP. We find that all coat components disassemble simultaneously and relatively rapidly after budding. Structural analysis in situ, maintaining Golgi topology, shows that vesicles change their size, membrane thickness, and cargo content as they progress from cis to trans, but the structure of the coat machinery remains constant.

Bibliography

Bykov, Y. S., Schaffer, M., Dodonova, S. O., Albert, S., Plitzko, J. M., Baumeister, W., Engel, B. D., & Briggs, J. A. (2017). The structure of the COPI coat determined within the cell. ELife, 6. CLOCKSS.

Authors 8

Yury S Bykov (first)
Miroslava Schaffer (additional)
Svetlana O Dodonova (additional)
Sahradha Albert (additional)
Jürgen M Plitzko (additional)
Wolfgang Baumeister (additional)
Benjamin D Engel (additional)
John AG Briggs (additional)

References 53 Referenced 165

10.1073/pnas.1603544113 / PNAS / δ-COP contains a helix C-terminal to its longin domain key to COPI dynamics and function by Arakel (2016)
10.1016/S0092-8674(03)01079-1 / Cell / The mechanisms of vesicle budding and fusion by Bonifacino (2004)
10.1111/j.1365-2818.2008.01988.x / Journal of Microscopy / Golgi apparatus studied in vitreous sections by Bouchet-Marquis (2008)
10.1016/j.ultramic.2013.06.004 / Ultramicroscopy / High-resolution noise substitution to measure overfitting and validate resolution in 3D structure determination by single particle electron cryomicroscopy by Chen (2013)
10.1371/journal.ppat.1001215 / PLoS Pathogens / Structural analysis of HIV-1 maturation using cryo-electron tomography by de Marco (2010)
10.1371/journal.pbio.0020380 / PLoS Biology / Components of coated vesicles and nuclear pore complexes share a common molecular architecture by Devos (2004)
10.7554/eLife.26691 / eLife / 9Å structure of the COPI coat reveals that the Arf1 GTPase occupies two contrasting molecular environments by Dodonova (2017)
10.1126/science.aab1121 / Science / VESICULAR TRANSPORT. A structure of the COPI coat and the role of coat proteins in membrane vesicle assembly by Dodonova (2015)
10.1111/tra.12052 / Traffic / Cis-Golgi cisternal assembly and biosynthetic activation occur sequentially in plants and algae by Donohoe (2013)
10.1073/pnas.0609818104 / PNAS / Identification and characterization of COPIa- and COPIb-type vesicle classes associated with plant and algal Golgi by Donohoe (2007)
10.1073/pnas.1515337112 / PNAS / In situ structural analysis of Golgi intracisternal protein arrays by Engel (2015)
10.1091/mbc.E03-10-0724 / Molecular Biology of the Cell / The alpha- and beta'-COP WD40 domains mediate cargo-selective interactions with distinct di-lysine motifs by Eugster (2004)
10.1073/pnas.0409178102 / PNAS / Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography by Förster (2005)
10.1126/science.1221443 / Science / The structures of COPI-coated vesicles reveal alternate coatomer conformations and interactions by Faini (2012)
10.1083/jcb.91.3.77s / The Journal of Cell Biology / The Golgi apparatus (complex)-(1954-1981)-from artifact to center stage by Farquhar (1981)
10.1016/j.cell.2017.08.008 / Cell / The eukaryotic CO2-concentrating organelle is liquid-like and exhibits dynamic reorganization by Freeman Rosenzweig (2017)
10.1146/annurev.cellbio.24.110707.175421 / Annual Review of Cell and Developmental Biology / Membrane traffic within the Golgi apparatus by Glick (2009)
10.7554/eLife.06980 / eLife / Measuring the optimal exposure for single particle cryo-EM using a 2.6 Å reconstruction of rotavirus VP6 by Grant (2015)
10.1016/j.jsb.2017.02.003 / Journal of Structural Biology / Helical reconstruction in RELION by He (2017)
10.1073/pnas.1006297107 / PNAS / Crystal structure of alpha-COP in complex with epsilon-COP provides insight into the architecture of the COPI vesicular coat by Hsia (2010)
10.1016/j.devcel.2012.10.017 / Developmental Cell / Molecular basis for recognition of dilysine trafficking motifs by COPI by Jackson (2012)
10.1111/tpj.12801 / The Plant Journal / Molecular techniques to interrogate and edit the Chlamydomonas nuclear genome by Jinkerson (2015)
10.1006/jsbi.1996.0013 / Journal of Structural Biology / Computer visualization of three-dimensional image data using IMOD by Kremer (1996)
10.1083/jcb.200108017 / The Journal of Cell Biology / Sorting of Golgi resident proteins into different subpopulations of COPI vesicles: a role for ArfGAP1 by Lanoix (2001)
10.1016/j.cell.2010.05.030 / Cell / Structure of coatomer cage proteins and the relationship among COPI, COPII, and clathrin vesicle coats by Lee (2010)
10.1016/0092-8674(94)90011-6 / Cell / Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum by Letourneur (1994)
10.1083/jcb.200410142 / The Journal of Cell Biology / ArfGAP1 dynamics and its role in COPI coat assembly on Golgi membranes of living cells by Liu (2005)
10.1038/emboj.2013.41 / The EMBO Journal / Rules for the recognition of dilysine retrieval motifs by coatomer by Ma (2013)
10.1016/0092-8674(89)90847-7 / Cell / Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack by Malhotra (1989)
10.1126/science.1108061 / Science / Golgin tethers define subpopulations of COPI vesicles by Malsam (2005)
10.1038/nmeth1014 / Nature Methods / Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy by Marko (2007)
10.1016/j.jsb.2005.07.007 / Journal of Structural Biology / Automated electron microscope tomography using robust prediction of specimen movements by Mastronarde (2005)
10.1073/pnas.0307332101 / PNAS / Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol by Mitra (2004)
10.1073/pnas.0611360104 / PNAS / Differential localization of coatomer complex isoforms within the Golgi apparatus by Moelleken (2007)
10.1016/j.jsb.2004.10.006 / Journal of Structural Biology / TOM software toolbox: acquisition and analysis for electron tomography by Nickell (2005)
10.1016/S0092-8674(00)80341-4 / Cell / Bidirectional transport by distinct populations of COPI-coated vesicles by Orci (1997)
10.1002/jcc.20084 / Journal of Computational Chemistry / UCSF Chimera--a visualization system for exploratory research and analysis by Pettersen (2004)
10.1038/ncomms14516 / Nature Communications / Dissecting the molecular organization of the translocon-associated protein complex by Pfeffer (2017)
10.1101/cshperspect.a005231 / Cold Spring Harbor Perspectives in Biology / COPI budding within the Golgi stack by Popoff (2011)
10.1073/pnas.1201333109 / PNAS / Focused ion beam micromachining of eukaryotic cells for cryoelectron tomography by Rigort (2012)
10.1016/j.jmb.2003.07.013 / Journal of Molecular Biology / Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy by Rosenthal (2003)
10.1016/j.jsb.2016.07.010 / Journal of Structural Biology / Optimized cryo-focused ion beam sample preparation aimed at in situ structural studies of membrane proteins by Schaffer (2017)
10.1038/nmeth.2019 / Nature Methods / Fiji: an open-source platform for biological-image analysis by Schindelin (2012)
10.1007/PL00006521 / Journal of Molecular Evolution / Phylogenetic analysis of components of the eukaryotic vesicle transport system reveals a common origin of adaptor protein complexes 1, 2, and 3 and the F subcomplex of the coatomer COPI by Schledzewski (1999)
10.1016/j.cell.2010.05.037 / Cell / A comprehensive comparison of transmembrane domains reveals organelle-specific properties by Sharpe (2010)
10.1101/gad.892101 / Genes & Development / Control of cell division by a retinoblastoma protein homolog in Chlamydomonas by Umen (2001)
10.1016/bs.mie.2016.04.014 / Methods in Enzymology / Cryo-electron tomography and subtomogram averaging by Wan (2016)
10.1111/j.1600-0854.2004.00158.x / Traffic / Gamma-COP appendage domain - structure and function by Watson (2004)
10.1016/j.jsb.2009.08.016 / Journal of Structural Biology / CTF determination and correction for low dose tomographic tilt series by Xiong (2009)
10.1083/jcb.200206015 / The Journal of Cell Biology / ARFGAP1 promotes the formation of COPI vesicles, suggesting function as a component of the coat by Yang (2002)
10.1016/j.jmb.2008.12.083 / Journal of Molecular Biology / Solution structure of human zeta-COP: direct evidences for structural similarity between COP I and clathrin-adaptor coats by Yu (2009)
10.1016/j.cell.2012.01.015 / Cell / A structure-based mechanism for Arf1-dependent recruitment of coatomer to membranes by Yu (2012)
10.1038/nmeth.4193 / Nature Methods / MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy by Zheng (2017)

Dates

Type	When
Created	7 years, 9 months ago (Nov. 17, 2017, 8 a.m.)
Deposited	1 year, 10 months ago (Oct. 11, 2023, 9:01 p.m.)
Indexed	18 hours, 52 minutes ago (Aug. 20, 2025, 8:32 a.m.)
Issued	7 years, 9 months ago (Nov. 17, 2017)
Published	7 years, 9 months ago (Nov. 17, 2017)
Published Online	7 years, 9 months ago (Nov. 17, 2017)

Funders 3

Deutsche Forschungsgemeinschaft 10.13039/501100001659
Region: Europe
gov (National government)
Labels3
1. German Research Association
2. German Research Foundation
3. DFG
Awards1
1. SFB-1035/Project A01
Deutsche Forschungsgemeinschaft 10.13039/501100001659
Region: Europe
gov (National government)
Labels3
1. German Research Association
2. German Research Foundation
3. DFG
Awards1
1. SFB1129 (Z2)
Medical Research Council 10.13039/501100000265
Region: Europe
gov (National government)
Labels3
1. Medical Research Council (United Kingdom)
2. UK Medical Research Council
3. MRC
Awards1
1. MC_UP_1201/16

BibTeX

@article{Bykov_2017, title={The structure of the COPI coat determined within the cell}, volume={6}, ISSN={2050-084X}, url={http://dx.doi.org/10.7554/elife.32493}, DOI={10.7554/elife.32493}, journal={eLife}, publisher={eLife Sciences Publications, Ltd}, author={Bykov, Yury S and Schaffer, Miroslava and Dodonova, Svetlana O and Albert, Sahradha and Plitzko, Jürgen M and Baumeister, Wolfgang and Engel, Benjamin D and Briggs, John AG}, year={2017}, month=nov }

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