Trends in Cell Biology
ReviewVesicle coats: structure, function, and general principles of assembly
Section snippets
Transport vesicle formation
Eukaryotic cells segregate functions in membrane-delimited compartments. These intracellular compartments are not static: they exchange proteins and lipids continuously in a directional and regulated manner [1]. The exchange of material (cargoes) between compartments is mostly conducted by coated transport vesicles that bud from one membrane and fuse with another. Transport vesicles are hence essential for maintaining organelle identity and lipid homeostasis and for the secretion of proteins.
Structures of coat components
Vast efforts have been invested in unraveling the structures of protein components of the three archetypal coats. X-ray crystallography (Box 1) has provided atomic models of coat fragments and also identified protein–protein interactions involved in coat polymerization 14, 15, 16 and cargo binding 3, 17. In some cases, X-ray crystallography has been combined with single-particle EM (Box 1) to derive the overall shape of coat subcomplexes 18, 19.
Structural homology between coats and evolutionary relationship
The three coat systems perform similar tasks on different membranes, but how are they evolutionarily related? It is widely accepted that the tetrameric adaptors of clathrin share distant sequence homology and structural similarity with the adaptor subcomplex of COPI (β-, γ-, δ-, and ζ-COPs) 38, 47. Sequence similarities between γ- and β-COPs and between ζ- and δ-COPs suggest that the adaptor subcomplex may originate from the duplication of a protodimer of a large and a small subunit [37].
Clathrin cages
The first high-resolution glimpse of how coat proteins assemble into a coated vesicle came from cryo-EM reconstruction of a clathrin cage assembled in vitro from purified cage components (Figure 2 and Box 1). The structure of a hexagonal clathrin barrel with D6 symmetry could accommodate the atomic structures of clathrin, leading to a model for the assembly of clathrin triskelia [18]. Each triskelion represents the vertex of a cage, with the legs of the triskelia intertwining to link the
Concluding remarks
Different assembly principles are found in the three types of coated vesicle. In clathrin and COPII cages, the same building blocks interact by making the same local contacts with the same interaction valence. Changes in size of the cage are accommodated by local flexibility of the triskelion leg (clathrin) or by the interaction angle of different rods (COPII). Clathrin cages purified from brain and COPII cages assembled with the adaptor Sec23 can deviate from point-group symmetry to form
Acknowledgments
The writing of this review was supported by a grant from the Deutsche Forschungsgemeinschaft within SFB638 (A16) to J.A.G.B. and F.T.W.
References (81)
A large-scale conformational change couples membrane recruitment to cargo binding in the AP2 clathrin adaptor complex
Cell
(2010)A functional phosphatidylinositol 3,4,5-trisphosphate/phosphoinositide binding domain in the clathrin adaptor AP-2 alpha subunit. Implications for the endocytic pathway
J. Biol. Chem.
(1996)Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle
Cell
(2005)Structural basis for cargo regulation of COPII coat assembly
Cell
(2008)Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle
Dev. Cell
(2007)Structures and mechanisms of vesicle coat components and multisubunit tethering complexes
Curr. Opin. Cell Biol.
(2012)Accessory protein recruitment motifs in clathrin-mediated endocytosis
Structure
(2002)Molecular switches involving the AP-2 beta2 appendage regulate endocytic cargo selection and clathrin coat assembly
Dev. Cell
(2006)Atomic structure of clathrin: a beta propeller terminal domain joins an alpha zigzag linker
Cell
(1998)Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi
Cell
(2003)
Molecular architecture and functional model of the endocytic AP2 complex
Cell
Deep-etch views of clathrin assemblies
J. Ultrastruct. Res.
Structure of an arrestin2-clathrin complex reveals a novel clathrin binding domain that modulates receptor trafficking
J. Biol. Chem.
COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum
Cell
Structure and organization of coat proteins in the COPII cage
Cell
Insights into COPII coat nucleation from the structure of Sec23.Sar1 complexed with the active fragment of Sec31
Dev. Cell
A structure-based mechanism for arf1-dependent recruitment of coatomer to membranes
Cell
Structure of coatomer cage proteins and the relationship among COPI, COPII, and clathrin vesicle coats
Cell
Molecular basis for recognition of dilysine trafficking motifs by COPI
Dev. Cell
Molecular structure and flexibility of the yeast coatomer as revealed by electron microscopy
J. Mol. Biol.
Functional organization of clathrin in coats: combining electron cryomicroscopy and X-ray crystallography
Mol. Cell
Cryo-electron tomography of clathrin-coated vesicles: structural implications for coat assembly
J. Mol. Biol.
The structure of the Sec13/31 COPII cage bound to Sec23
J. Mol. Biol.
Coupling of coat assembly and vesicle budding to packaging of putative cargo receptors
Cell
Reconstitution of coat protein complex II (COPII) vesicle formation from cargo-reconstituted proteoliposomes reveals the potential role of GTP hydrolysis by Sar1p in protein sorting
J. Biol. chem.
Dynamin undergoes a GTP-dependent conformational change causing vesiculation
Cell
Membrane shape at the edge of the dynamin helix sets location and duration of the fission reaction
Cell
Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains
Cell
Purification of a novel class of coated vesicles mediating biosynthetic protein-transport through the Golgi stack
Cell
Involvement of GTP-binding “G” proteins in transport through the Golgi stack
Cell
COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes
Cell
Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle
Cell
The BAR domain protein arfaptin-1 controls secretory granule biogenesis at the trans-Golgi network
Dev. Cell
SNARE selectivity of the COPII coat
Cell
Conformational changes of coat proteins during vesicle formation
FEBS Lett.
Molecular Biology of the Cell
Coatomer, the coat protein of COPI transport vesicles, discriminates endoplasmic reticulum residents from p24 proteins
Mol. Cell. Biol.
Structural basis of cargo membrane protein discrimination by the human COPII coat machinery
EMBO J.
En bloc incorporation of coatomer subunits during the assembly of COP-coated vesicles
J. Cell Biol.
Coatomer and dimeric ADP ribosylation factor 1 promote distinct steps in membrane scission
J. Cell Biol.
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