Key Points
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Endoplasmic reticulum (ER) export by the coat protein complex-II (COPII) machinery involves the transport of nearly a third of the proteins that are encoded by the eukaryotic genome. The wide range of protein-folding stabilities that are accommodated by the COPII machinery indicates that the current view of the ER as a quality-control device should now be tempered with the more general principle that the energetics of the protein fold, independently of the final functional fold, directs ER export under physiological conditions.
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Cargo selection by the Sec23–Sec24 adaptor protein complex involves a high valency cargo adaptor platform. Through its binding to this cargo adaptor platform, cargo has an important role in directing vesicle formation and membrane traffic.
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The self-assembly properties of the Sec13–Sec31 complex, which result in the formation of a highly flexible cuboctahedral cage, direct the concentration of cargo into budding vesicles and coordinate cargo recruitment with membrane curvature and fission.
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The GTPase Sar1, which is involved in Sec23–Sec24 membrane recruitment during the early steps of coat protein complex (CPC) assembly, also has an important role in late events — it directs vesicle fission. Vesicle release that is mediated by Sar1–GTP hydrolysis is likely to be coordinated with the function of lipid-remodelling factors.
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The structural and biochemical properties that are involved in the function of the COPII export machinery combined with those that have been observed for cargo selection and the generation of coat complexes by clathrin-mediated pathways now provide a unifying model for CPC assembly in eukaryotic cells. The assembly of CPCs is driven by various kinetic parameters that control the individual steps of protein folding, cargo selection and collection, and membrane curvature and fission dynamics. These complexes are therefore highly versatile and robust trafficking machineries.
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CPCs — which include the COPII, clathrin and COPI coats — probably evolved from the more flexible cage structure that is found in the COPII-based pathway, which directs ER export, to the more selective and rigid clathrin-based and COPI-based cage structures, which are involved in post-ER trafficking pathways.
Abstract
Communication between compartments of the exocytic and endocytic pathways in eukaryotic cells involves transport carriers — vesicles and tubules — that mediate the vectorial movement of cargo. Recent studies of transport-carrier formation in the early secretory pathway have provided new insights into the mechanisms of cargo selection by coat protein complex-II (COPII) adaptor proteins, the construction of cage-protein scaffolds and fission. These studies are beginning to produce a unifying molecular and structural model of coat function in the formation and fission of vesicles and tubules in endomembrane traffic.
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Acknowledgements
This work was supported by a National Institutes of Health (NIH) grant to W.E.B. and an NIH postdoctoral fellowship to S.M.S. Postdoctoral fellowships to P.L. and C.G. were from the Cystic Fibrosis Foundation. We thank G. Palade for providing an image of the ER–Golgi system in the pancreas (Box 1).
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DATABASES
Protein Data Bank
FURTHER INFORMATION
Macromolecular Structure Database — Structure of the Sec13/31 COPII coat cage
Macromolecular Structure Database — EM-Search Tool for Electron Microscopy Depositions
Movie of the Sec13–Sec31 COPII cage
The Scripps Research Institute Automated Molecular Imaging group
Glossary
- Coat protein complexes (CPCs)
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CPCs are a collection of cytosolic proteins that interact to form a coat on membranes and drive cargo selection and vesicle formation.
- Clathrin
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The main cage component of the coat that is associated with clathrin-coated vesicles, which are involved in membrane transport in both the endocytic and the exocytic pathways. Clathrin forms vesicles that originate on the trans-Golgi network and the plasma membrane.
- Coat protein complex-I (COPI)
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A specialized coat protein complex that is involved in the retrograde transport of cargo between the compartments of the Golgi and from the Golgi to the endoplasmic reticulum.
- Coat protein complex-II (COPII)
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A specialized coat protein complex that is involved in the anterograde transport of cargo from the endoplasmic reticulum to the Golgi.
- Adaptor protein (AP) complexes
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An AP complex is a collection of interacting proteins that link cargo to the polymeric lattice that forms a vesicle cage.
- Ras superfamily
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A superfamily of small, monomeric GTPases that are involved in membrane trafficking, growth, differentiation and cellular signalling.
- Cuboctahedral geometry
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An Archimedean solid, with 24 identical edges or 12 identical vertices, in which 8 triangular faces and 6 square faces are arranged such that 2 triangles and 2 squares meet at each vertex and each edge separates a triangle and a square.
- Guanine nucleotide-exchange factor
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(GEF). A GEF interacts with a GTPase to promote the exchange of bound GDP for GTP.
- Endoplasmic-reticulum-associated folding pathway (ERAF)
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A pathway in which endoplasmic reticulum (ER)-associated chaperones direct the folding of soluble and transmembrane cargo proteins that have been translocated into the ER.
- GTPase-activating protein
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(GAP). A GAP interacts with an activated GTPase to promote the hydrolysis of the bound GTP, which converts the GTPase protein to its GDP-bound state.
- SNAREs
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(Soluble N-ethylmaleimide-sensitive factor attachment protein receptors). A protein family that consists of a cognate group of integral and peripheral membrane proteins that are required for bilayer recognition and fusion during membrane traffic.
- Nuclear pore complex
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(NPC). The NPC is a multiprotein complex that stabilizes the continuity between the inner and outer nuclear membranes by forming protein-permeable pores in the nuclear envelope.
- Rab GTPases
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Rab proteins form the largest subfamily of small GTPases of the Ras superfamily. They regulate membrane budding, tethering, fusion, and vesicle and tubule motility at various sites within cells.
- WD40 domain
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A protein structural arrangement in which several 'blades', which each consist of a four-stranded antiparallel β-sheet that is formed by WD40 repeats, are arranged radially around a central axis. WD40 repeats are short ∼40-amino-acid motifs that often terminate in a Trp–Asp (W–D) dipeptide.
- α-solenoid structure
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A protein structural motif in which numerous pairs of antiparallel α-helices are stacked to form a solenoid.
- Chylomicrons
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Lipoproteins that are involved in the transfer of lipids that are absorbed in the small intestine.
- ARF GTPases
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ADP-ribosylation factor (ARF) GTPases constitute a subfamily of the Ras-GTPase superfamily. They are involved in the regulation of intracellular transport by modulating the interactions of adaptor protein complexes with cage assemblies.
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Gürkan, C., Stagg, S., LaPointe, P. et al. The COPII cage: unifying principles of vesicle coat assembly. Nat Rev Mol Cell Biol 7, 727–738 (2006). https://doi.org/10.1038/nrm2025
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DOI: https://doi.org/10.1038/nrm2025
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