Key Points
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Protein transport between the endoplasmic reticulum (ER) and Golgi is a highly dynamic process, and the organization of this conserved trafficking pathway differs in mammalian and plant cells.
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Membrane traffic in the early secretory pathway initiates at the ER through the action of conserved coat complexes and transport machineries. There are distinct differences in structural organization of the ER–Golgi interface across species, including variations in the regulation of the core machinery, dependence on cytoskeletal components and cell-specific accessory molecules.
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Emerging evidence indicates that the assembly of transport carriers and the organization of ER export sites (ERES) can be influenced by the type, size and quantity of the secreted cargo.
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Current molecular models and hypotheses on the establishment and maintenance of ER–Golgi organization in mammalian and plant cells highlight evolutionary differences. Continued comparative analyses across a range of species should provide powerful insights into the structure, function and molecular mechanisms that control trafficking between the ER and the Golgi.
Abstract
Coat protein complex I (COPI) and COPII are required for bidirectional membrane trafficking between the endoplasmic reticulum (ER) and the Golgi. While these core coat machineries and other transport factors are highly conserved across species, high-resolution imaging studies indicate that the organization of the ER–Golgi interface is varied in eukaryotic cells. Regulation of COPII assembly, in some cases to manage distinct cellular cargo, is emerging as one important component in determining this structure. Comparison of the ER–Golgi interface across different systems, particularly mammalian and plant cells, reveals fundamental elements and distinct organization of this interface. A better understanding of how these interfaces are regulated to meet varying cellular secretory demands should provide key insights into the mechanisms that control efficient trafficking of proteins and lipids through the secretory pathway.
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References
Ward, T. H., Polishchuk, R. S., Caplan, S., Hirschberg, K. & Lippincott-Schwartz, J. Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol. 155, 557–570 (2001).
Brandizzi, F., Snapp, E. L., Roberts, A. G., Lippincott-Schwartz, J. & Hawes, C. Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching. Plant Cell 14, 1293–1309 (2002).
Altan-Bonnet, N., Sougrat, R. & Lippincott-Schwartz, J. Molecular basis for Golgi maintenance and biogenesis. Curr. Opin. Cell Biol. 16, 364–372 (2004).
Farquhar, M. G. & Palade, G. E. The Golgi apparatus: 100 years of progress and controversy. Trends Cell Biol. 8, 2–10 (1998).
Driouich, A. & Staehelin, L. A. in The Golgi Apparatus (eds. Berger, E. G. and Roth, J.) 275–301 (Birkhäuser Verlag, 1997).
Carpita, N. C. & Gibeaut, D. M. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 3, 1–30 (1993).
Cavalier, D. M. et al. Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell 20, 1519–1537 (2008).
Dirnberger, D., Bencur, P., Mach, L. & Steinkellner, H. The Golgi localization of Arabidopsis thaliana β1,2-xylosyltransferase in plant cells is dependent on its cytoplasmic and transmembrane sequences. Plant Mol. Biol. 50, 273–281 (2002).
Fitchette, A. C. et al. Biosynthesis and immunolocalization of Lewis a-containing N-glycans in the plant cell. Plant Physiol. 121, 333–344 (1999).
Keegstra, K. & Raikhel, N. Plant glycosyltransferases. Curr. Opin. Plant Biol. 4, 219–224 (2001).
De Matteis, M. A. & Morrow, J. S. Spectrin tethers and mesh in the biosynthetic pathway. J. Cell Sci. 113, 2331–2343 (2000).
Kondoh, K., Torii, S. & Nishida, E. Control of MAP kinase signaling to the nucleus. Chromosoma 114, 86–91 (2005).
Saint- Jore-Dupas, C. et al. Plant N-glycan processing enzymes employ different targeting mechanisms for their spatial arrangement along the secretory pathway. Plant Cell 18, 3182–3200 (2006).
Rabouille, C. et al. Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J. Cell Sci. 108, 1617–1627 (1995).
Klumperman, J. The growing Golgi: in search of its independence. Nature Cell Biol. 2, E217–E219 (2000).
van Meel, E. & Klumperman, J. Imaging and imagination: understanding the endo-lysosomal system. Histochem. Cell Biol. 129, 253–266 (2008).
Dettmer, J., Hong-Hermesdorf, A., Stierhof, Y. D. & Schumacher, K. Arabidopsis vacuolar H-ATPase subunit E isoform 1 is required for Golgi organization and vacuole function in embryogenesis. Plant Cell 18, 715–730 (2006).
Nickel, W. & Rabouille, C. Mechanisms of regulated unconventional protein secretion. Nature Rev. Mol. Cell Biol. 10, 148–155 (2009).
Bannykh, S. I., Rowe, T. & Balch, W. E. The organization of endoplasmic reticulum export complexes. J. Cell Biol. 135, 19–35 (1996).
Hammond, A. T. & Glick, B. S. Dynamics of transitional endoplasmic reticulum sites in vertebrate cells. Mol. Biol. Cell 11, 3013–3030 (2000).
Shaywitz, D. A., Orci, L., Ravazzola, M., Swaroop, A. & Kaiser, C. A. Human SEC13Rp functions in yeast and is located on transport vesicles budding from the endoplasmic reticulum. J. Cell Biol. 128, 769–777 (1995).
Rossanese, O. W. et al. Golgi structure correlates with transitional endoplasmic reticulum organization in Pichia pastoris and Saccharomyces cerevisiae. J. Cell Biol. 145, 69–81 (1999). Demonstrates that P. pastoris and S. cerevisiae have distinct ERES and Golgi organizations and proposes a model in which Golgi organization correlates with ERES organization.
Horton, A. C. & Ehlers, M. D. Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J. Neurosci. 23, 6188–6199 (2003).
daSilva, L. L. et al. Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell 16, 1753–1771 (2004). Shows that ERES and motile Golgi stacks form a secretory unit system that is unique to eukaryotic cells.
Connerly, P. L. et al. Sec16 is a determinant of transitional ER organization. Curr. Biol. 15, 1439–1447 (2005).
Watson, P., Townley, A. K., Koka, P., Palmer, K. J. & Stephens, D. J. Sec16 defines endoplasmic reticulum exit sites and is required for secretory cargo export in mammalian cells. Traffic 7, 1678–1687 (2006).
Miller, E. A. & Barlowe, C. Regulation of coat assembly — sorting things out at the ER. Curr. Opin. Cell Biol. 22, 447–453 (2010).
Lorente-Rodriguez, A. & Barlowe, C. Entry and exit mechanisms at the cis-face of the Golgi complex. Cold Spring Harb. Perspect. Biol. 11 Apr 2011 (doi:10.1101/cshperspect.a005207).
Cao, X., Ballew, N. & Barlowe, C. Initial docking of ER-derived vesicles requires Uso1p and Ypt1p but is independent of SNARE proteins. EMBO J. 17, 2156–2165 (1998).
Allan, B. B., Moyer, B. D. & Balch, W. E. Rab1 recruitment of p115 into a cis-SNARE complex: programming budding COPII vesicles for fusion. Science 289, 444–448 (2000).
Cai, H. et al. TRAPPI tethers COPII vesicles by binding the coat subunit Sec23. Nature 445, 941–944 (2007).
Zink, S., Wenzel, D., Wurm, C. A. & Schmitt, H. D. A link between ER tethering and COP-I vesicle uncoating. Dev. Cell 17, 403–416 (2009).
Bonfanti, L. et al. Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell 95, 993–1003 (1998).
Barlowe, C. et al. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895–907 (1994). Reports, for the first time, that COPII-coated transport intermediates exist and reconstitutes COPII carriers in vitro.
Stagg, S. M. et al. Structural basis for cargo regulation of COPII coat assembly. Cell 134, 474–484 (2008).
O'Donnell, J., Maddox, K. & Stagg, S. The structure of a COPII tubule. J. Struct. Biol. 173, 358–364 (2011).
Stagg, S. M. et al. Structure of the Sec13/31 COPII coat cage. Nature 439, 234–238 (2006). Reveals the three-dimensional reconstruction of SEC13–SEC31 cages at 30 Å resolution that defined a flexible cuboctahedron geometry of the COPII outer coat.
Fath, S., Mancias, J. D., Bi, X. & Goldberg, J. Structure and organization of coat proteins in the COPII cage. Cell 129, 1325–1336 (2007).
Bhattacharya, N., J., O. D. & Stagg, S. M. The structure of the Sec13/31 COPII cage bound to Sec23. J. Mol. Biol. 420, 324–334 (2012).
Zeuschner, D. et al. Immuno-electron tomography of ER exit sites reveals the existence of free COPII-coated transport carriers. Nature Cell Biol. 8, 377–383 (2006).
Bacia, K. et al. Multibudded tubules formed by COPII on artificial liposomes. Sci. Rep. 1, 17 (2011).
Boyadjiev, S. A. et al. Cranio-lenticulo-sutural dysplasia is caused by a SEC23A mutation leading to abnormal endoplasmic-reticulum-to-Golgi trafficking. Nature Genet. 38, 1192–1197 (2006).
Lang, M. R., Lapierre, L. A., Frotscher, M., Goldenring, J. R. & Knapik, E. W. Secretory COPII coat component Sec23a is essential for craniofacial chondrocyte maturation. Nature Genet. 38, 1198–1203 (2006).
Fromme, J. C. et al. The genetic basis of a craniofacial disease provides insight into COPII coat assembly. Dev. Cell 13, 623–634 (2007).
Jones, B. et al. Mutations in a Sar1 GTPase of COPII vesicles are associated with lipid absorption disorders. Nature Genet. 34, 29–31 (2003).
Silvain, M. et al. Anderson's disease (chylomicron retention disease): a new mutation in the SARA2 gene associated with muscular and cardiac abnormalities. Clin. Genet. 74, 546–552 (2008).
Jin, L. et al. Ubiquitin-dependent regulation of COPII coat size and function. Nature 482, 495–500 (2012).
Saito, K. et al. TANGO1 facilitates cargo loading at endoplasmic reticulum exit sites. Cell 136, 891–902 (2009).
Saito, K. et al. cTAGE5 mediates collagen secretion through interaction with TANGO1 at endoplasmic reticulum exit sites. Mol. Biol. Cell 22, 2301–2308 (2011).
Keegstra, K. Plant cell walls. Plant Physiol. 154, 483–486 (2010).
Hanton, S. L., Chatre, L., Renna, L., Matheson, L. A. & Brandizzi, F. De novo formation of plant endoplasmic reticulum export sites is membrane cargo induced and signal mediated. Plant Physiol. 143, 1640–1650 (2007).
Farhan, H., Weiss, M., Tani, K., Kaufman, R. J. & Hauri, H. P. Adaptation of endoplasmic reticulum exit sites to acute and chronic increases in cargo load. EMBO J. 27, 2043–2054 (2008).
Walter, P. & Ron, D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081–1086 (2011).
Presley, J. F. et al. ER-to-Golgi transport visualized in living cells. Nature 389, 81–85 (1997). A pioneering study that uses fluorescent protein technology to visualize ER export of secretory cargo along microtubules in live mammalian cells.
Stephens, D. J. Functional coupling of microtubules to membranes — implications for membrane structure and dynamics. J. Cell Sci. 125, 2795–2804 (2012).
Mogelsvang, S., Gomez-Ospina, N., Soderholm, J., Glick, B. S. & Staehelin, L. A. Tomographic evidence for continuous turnover of Golgi cisternae in Pichia pastoris. Mol. Biol. Cell 14, 2277–2291 (2003).
Ward, T. H. & Brandizzi, F. Dynamics of proteins in Golgi membranes: comparisons between mammalian and plant cells highlighted by photobleaching techniques. Cell. Mol. Life Sci. 61, 172–185 (2004).
Nebenfuhr, A. et al. Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol. 121, 1127–1142 (1999).
Boevink, P. et al. Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J. 15, 441–447 (1998).
Bard, F. et al. Functional genomics reveals genes involved in protein secretion and Golgi organization. Nature 439, 604–607 (2006).
He, C. Y. et al. Golgi duplication in Trypanosoma brucei. J. Cell Biol. 165, 313–321 (2004).
Hager, K. M., Striepen, B., Tilney, L. G. & Roos, D. S. The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. J. Cell Sci. 112, 2631–2638 (1999).
Avisar, D., Prokhnevsky, A. I., Makarova, K. S., Koonin, E. V. & Dolja, V. V. Myosin XI-K is required for rapid trafficking of Golgi stacks, peroxisomes, and mitochondria in leaf cells of Nicotiana benthamiana. Plant Physiol. 146, 1098–1108 (2008).
Peremyslov, V. V., Prokhnevsky, A. I., Avisar, D. & Dolja, V. V. Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol. 146, 1109–1116 (2008).
Sparkes, I. A., Teanby, N. A. & Hawes, C. Truncated myosin XI tail fusions inhibit peroxisome, Golgi, and mitochondrial movement in tobacco leaf epidermal cells: a genetic tool for the next generation. J. Exp. Bot. 59, 2499–2512 (2008).
Hawes, C. & Satiat-Jeunemaitre, B. The plant Golgi apparatus — going with the flow. Biochim. Biophys. Acta 1744, 93–107 (2005).
Donohoe, B. S. et al. Cis-Golgi cisternal assembly and biosynthetic activation occur sequentially in plants and algae. Traffic 14, 551–567 (2013).
Bentley, M. et al. SNARE status regulates tether recruitment and function in homotypic COPII vesicle fusion. J. Biol. Chem. 281, 38825–38833 (2006).
Xu, D. & Hay, J. C. Reconstitution of COPII vesicle fusion to generate a pre-Golgi intermediate compartment. J. Cell Biol. 167, 997–1003 (2004).
Bonifacino, J. S. & Glick, B. S. The mechanisms of vesicle budding and fusion. Cell 116, 153–166 (2004).
Sitia, R. & Meldolesi, J. Endoplasmic reticulum: a dynamic patchwork of specialized subregions. Mol. Biol. Cell 3, 1067–1072 (1992).
Mellman, I. & Simons, K. The Golgi complex: in vitro veritas? Cell 68, 829–840 (1992).
Klumperman, J. et al. The recycling pathway of protein ERGIC-53 and dynamics of the ER–Golgi intermediate compartment. J. Cell Sci. 111, 3411–3425 (1998).
Appenzeller-Herzog, C. & Hauri, H. P. The ER–Golgi intermediate compartment (ERGIC): in search of its identity and function. J. Cell Sci. 119, 2173–2183 (2006).
Martinez-Menarguez, J. A., Geuze, H. J., Slot, J. W. & Klumperman, J. Vesicular tubular clusters between the ER and Golgi mediate concentration of soluble secretory proteins by exclusion from COPI-coated vesicles. Cell 98, 81–90 (1999).
Breuza, L. et al. Proteomics of endoplasmic reticulum-Golgi intermediate compartment (ERGIC) membranes from brefeldin A-treated HepG2 cells identifies ERGIC-32, a new cycling protein that interacts with human Erv46. J. Biol. Chem. 279, 47242–47253 (2004).
Scales, S. J., Pepperkok, R. & Kreis, T. E. Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell 90, 1137–1148 (1997). Demonstrates in vivo a temporal uncoupling of the roles of the COPI and COPII machineries in bidirectional membrane traffic at the ER–Golgi interface in mammalian cells.
Stephens, D. J. & Pepperkok, R. Illuminating the secretory pathway: when do we need vesicles? J. Cell Sci. 114, 1053–1059 (2001).
Lippincott-Schwartz, J., Cole, N. B., Marotta, A., Conrad, P. A. & Bloom, G. S. Kinesin is the motor for microtubule-mediated Golgi-to-ER membrane traffic. J. Cell Biol. 128, 293–306 (1995).
Roghi, C. & Allan, V. J. Dynamic association of cytoplasmic dynein heavy chain 1a with the Golgi apparatus and intermediate compartment. J. Cell Sci. 112, 4673–4685 (1999).
Beck, K. A. Spectrins and the Golgi. Biochim. Biophys. Acta 1744, 374–382 (2005).
Chen, J. L. et al. Coatomer-bound Cdc42 regulates dynein recruitment to COPI vesicles. J. Cell Biol. 169, 383–389 (2005).
Ben-Tekaya, H., Miura, K., Pepperkok, R. & Hauri, H. P. Live imaging of bidirectional traffic from the ERGIC. J. Cell Sci. 118, 357–367 (2005).
Sparkes, I. A., Ketelaar, T., Ruijter, N. C. & Hawes, C. Grab a Golgi: laser trapping of Golgi bodies reveals in vivo interactions with the endoplasmic reticulum. Traffic 10, 567–571 (2009). Uses laser-trap technology in live cells and demonstrates that the ER and the Golgi are physically attached in highly vacuolated plant cells.
Hanton, S. L., Matheson, L. A., Chatre, L. & Brandizzi, F. Dynamic organization of COPII coat proteins at endoplasmic reticulum export sites in plant cells. Plant J. 57, 963–974 (2009).
Stefano, G. et al. In tobacco leaf epidermal cells, the integrity of protein export from the endoplasmic reticulum and of ER export sites depends on active COPI machinery. Plant J. 46, 95–110 (2006).
Hanton, S. L. et al. Plant Sar1 isoforms with near-identical protein sequences exhibit different localisations and effects on secretion. Plant Mol. Biol. 67, 283–294 (2008).
Wei, T. & Wang, A. Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at endoplasmic reticulum exit sites in a COPI- and COPII-dependent manner. J. Virol. 82, 12252–12264 (2008).
Robinson, D. G., Herranz, M. C., Bubeck, J., Pepperkok, R. & Ritzenthaler, C. Membrane dynamics in the early secretory pathway. Crit. Rev. Plant Sci. 26, 199–225 (2007).
Sieben, C., Mikosch, M., Brandizzi, F. & Homann, U. Interaction of the K+-channel KAT1 with the coat protein complex II coat component Sec24 depends on a di-acidic endoplasmic reticulum export motif. Plant J. 56, 997–1006 (2008).
Osterrieder, A., Hummel, E., Carvalho, C. M. & Hawes, C. Golgi membrane dynamics after induction of a dominant-negative mutant Sar1 GTPase in tobacco. J. Exp. Bot. 61, 405–422 (2009).
Hawes, C., Osterrieder, A., Hummel, E. & Sparkes, I. The plant ER–Golgi interface. Traffic 9, 1571–1580 (2008).
Schoberer, J. et al. Arginine/lysine residues in the cytoplasmic tail promote ER export of plant glycosylation enzymes. Traffic 10, 101–115 (2009).
Faso, C. et al. A missense mutation in the Arabidopsis COPII coat protein Sec24A induces the formation of clusters of the endoplasmic reticulum and Golgi apparatus. Plant Cell 21, 3655–3671 (2009).
Ito, Y. et al. cis-Golgi proteins accumulate near the ER exit sites and act as the scaffold for Golgi regeneration after brefeldin A treatment in tobacco BY-2 cells. Mol. Biol. Cell 23, 3203–3214 (2012).
Lerich, A. et al. ER import sites and their relationship to ER exit sites: a new model for bidirectional ER–Golgi transport in higher plants. Front. Plant Sci. 3, 143 (2012).
Langhans, M., Meckel, T., Kress, A., Lerich, A. & Robinson, D. G. ERES (ER exit sites) and the 'secretory unit concept'. J. Microsc. 247, 48–59 (2012).
Hawes, C. The ER/Golgi interface — is there anything in-between? Front. Plant Sci. 3, 73 (2012).
Donohoe, B. S., Kang, B. H. & Staehelin, L. A. Identification and characterization of COPIa- and COPIb-type vesicle classes associated with plant and algal Golgi. Proc. Natl Acad. Sci. 104, 163–168 (2007).
Wright, G. D., Arlt, J., Poon, W. C. & Read, N. D. Optical tweezer micromanipulation of filamentous fungi. Fungal Genet. Biol. 44, 1–13 (2007).
Witte, K. et al. TFG-1 function in protein secretion and oncogenesis. Nature Cell Biol. 13, 550–558 (2011).
Lord, C. et al. Sequential interactions with Sec23 control the direction of vesicle traffic. Nature 473, 181–186 (2011).
Craig, S. & Staehelin, L. A. High pressure freezing of intact plant tissues. Evaluation and characterization of novel features of the endoplasmic reticulum and associated membrane systems. Eur. J. Cell Biol. 46, 81–93 (1988).
Ritzenthaler, C. et al. Reevaluation of the effects of brefeldin A on plant cells using tobacco Bright Yellow 2 cells expressing Golgi-targeted green fluorescent protein and COPI antisera. Plant Cell 14, 237–261 (2002).
Staehelin, L. A. The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J. 11, 1151–1165 (1997).
Kang, B. H. & Staehelin, L. A. ER-to-Golgi transport by COPII vesicles in Arabidopsis involves a ribosome-excluding scaffold that is transferred with the vesicles to the Golgi matrix. Protoplasma 234, 51–64 (2008).
Faini, M. et al. The structures of COPI-coated vesicles reveal alternate coatomer conformations and interactions. Science 336, 1451–1454 (2012).
Latijnhouwers, M., Hawes, C. & Carvalho, C. Holding it all together? Candidate proteins for the plant Golgi matrix. Curr. Opin. Plant Biol. 8, 632–639 (2005).
Osterrieder, A. Tales of tethers and tentacles: golgins in plants. J. Microsc. 247, 68–77 (2012).
Puthenveedu, M. A., Bachert, C., Puri, S., Lanni, F. & Linstedt, A. D. GM130 and GRASP65-dependent lateral cisternal fusion allows uniform Golgi–enzyme distribution. Nature Cell Biol. 8, 238–248 (2006).
Iwata, Y. & Koizumi, N. Plant transducers of the endoplasmic reticulum unfolded protein response. Trends Plant Sci. 17, 720–727 (2012).
Bielli, A. et al. Regulation of Sar1 NH2 terminus by GTP binding and hydrolysis promotes membrane deformation to control COPII vesicle fission. J. Cell Biol. 171, 919–924 (2005).
Yoshihisa, T., Barlowe, C. & Schekman, R. Requirement for a GTPase-activating protein in vesicle budding from the endoplasmic reticulum. Science 259, 1466–1468 (1993).
Bi, X., Corpina, R. A. & Goldberg, J. Structure of the Sec23/24-Sar1 pre-budding complex of the COPII vesicle coat. Nature 419, 271–277 (2002).
Thor, F., Gautschi, M., Geiger, R. & Helenius, A. Bulk flow revisited: transport of a soluble protein in the secretory pathway. Traffic 10, 1819–1830 (2009).
Kuehn, M. J., Herrmann, J. M. & Schekman, R. COPII–cargo interactions direct protein sorting into ER-derived transport vesicles. Nature 391, 187–190 (1998).
Giraudo, C. G. & Maccioni, H. J. Endoplasmic reticulum export of glycosyltransferases depends on interaction of a cytoplasmic dibasic motif with Sar1. Mol. Biol. Cell 14, 3753–3766 (2003).
Wendeler, M. W., Paccaud, J. P. & Hauri, H. P. Role of Sec24 isoforms in selective export of membrane proteins from the endoplasmic reticulum. EMBO Rep. 8, 258–264 (2007).
Miller, E. A. et al. Multiple cargo binding sites on the COPII subunit Sec24p ensure capture of diverse membrane proteins into transport vesicles. Cell 114, 497–509 (2003). Identifies multiple independent cargo-binding sites in the COPII coat subunit SEC24 and describes the plasticity of this adaptor complex in selecting multiple cargo molecules with distinct sorting signals.
Bi, X., Mancias, J. D. & Goldberg, J. Insights into COPII coat nucleation from the structure of Sec23. Sar1 complexed with the active fragment of Sec31. Dev. Cell 13, 635–645 (2007).
Copic, A., Latham, C. F., Horlbeck, M. A., D'Arcangelo, J. G. & Miller, E. A. ER cargo properties specify a requirement for COPII coat rigidity mediated by Sec13p. Science 335, 1359–1362 (2012).
Matsuoka, K. et al. COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell 93, 263–275 (1998).
Lee, M. C., Miller, E. A., Goldberg, J., Orci, L. & Schekman, R. Bi-directional protein transport between the ER and Golgi. Annu. Rev. Cell Dev. Biol. 20, 87–123 (2004).
Routledge, K. E., Gupta, V. & Balch, W. E. Emergent properties of proteostasis–COPII coupled systems in human health and disease. Mol. Membr. Biol. 27, 385–397 (2010).
Waters, M. G., Griff, I. C. & Rothman, J. E. Proteins involved in vesicular transport and membrane fusion. Curr. Opin. Cell Biol. 3, 615–620 (1991).
Eugster, A., Frigerio, G., Dale, M. & Duden, R. COP I domains required for coatomer integrity, and novel interactions with ARF and ARF-GAP. EMBO J. 19, 3905–3917 (2000).
Szul, T. & Sztul, E. COPII and COPI traffic at the ER–Golgi interface. Physiol. (Bethesda) 26, 348–364 (2011).
Shiba, Y. & Randazzo, P. A. ArfGAP1 function in COPI mediated membrane traffic: currently debated models and comparison to other coat-binding ArfGAPs. Histol. Histopathol. 27, 1143–1153 (2012).
Wieland, F. T., Gleason, M. L., Serafini, T. A. & Rothman, J. E. The rate of bulk flow from the endoplasmic reticulum to the cell surface. Cell 50, 289–300 (1987).
Pelham, H. R. Evidence that luminal ER proteins are sorted from secreted proteins in a post-ER compartment. EMBO J. 7, 913–918 (1988).
Doms, R. W., Russ, G. & Yewdell, J. W. Brefeldin A redistributes resident and itinerant Golgi proteins to the endoplasmic reticulum. J. Cell Biol. 109, 61–72 (1989).
Lippincott-Schwartz, J., Yuan, L. C., Bonifacino, J. S. & Klausner, R. D. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801–813 (1989). The first demonstration that the Golgi is not a stable entity but that its integrity depends on constant membrane cycling with the ER.
Sciaky, N. et al. Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J. Cell Biol. 139, 1137–1155 (1997).
Niu, T. K., Pfeifer, A. C., Lippincott-Schwartz, J. & Jackson, C. L. Dynamics of GBF1, a brefeldin A-sensitive Arf1 exchange factor at the Golgi. Mol. Biol. Cell 16, 1213–1222 (2005).
Richter, S. et al. Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature 448, 488–492 (2007).
Peyroche, A. et al. Brefeldin A acts to stabilize an abortive ARF-GDP–Sec7 domain protein complex: involvement of specific residues of the Sec7 domain. Mol. Cell 3, 275–285 (1999).
Moyer, B. D., Allan, B. B. & Balch, W. E. Rab1 interaction with a GM130 effector complex regulates COPII vesicle cis-Golgi tethering. Traffic 2, 268–276 (2001).
Shorter, J., Beard, M. B., Seemann, J., Dirac-Svejstrup, A. B. & Warren, G. Sequential tethering of Golgins and catalysis of SNAREpin assembly by the vesicle-tethering protein p115. J. Cell Biol. 157, 45–62 (2002).
Sacher, M. et al. TRAPP I implicated in the specificity of tethering in ER-to-Golgi transport. Mol. Cell 7, 433–442 (2001).
Cai, Y. et al. The structural basis for activation of the Rab Ypt1p by the TRAPP membrane-tethering complexes. Cell 133, 1202–1213 (2008).
Hay, J. C., Chao, D. S., Kuo, C. S. & Scheller, R. H. Protein interactions regulating vesicle transport between the endoplasmic reticulum and Golgi apparatus in mammalian cells. Cell 89, 149–158 (1997).
Rowe, T., Dascher, C., Bannykh, S., Plutner, H. & Balch, W. E. Role of vesicle-associated syntaxin 5 in the assembly of pre-Golgi intermediates. Science 279, 696–700 (1998).
Xu, D., Joglekar, A. P., Williams, A. L. & Hay, J. C. Subunit structure of a mammalian ER/Golgi SNARE complex. J. Biol. Chem. 275, 39631–39639 (2000).
Weber, T. et al. SNAREpins: minimal machinery for membrane fusion. Cell 92, 759–772 (1998).
Parlati, F. et al. Topological restriction of SNARE-dependent membrane fusion. Nature 407, 194–198 (2000).
Yamaguchi, T. et al. Sly1 binds to Golgi and ER syntaxins via a conserved N-terminal peptide motif. Dev. Cell 2, 295–305 (2002).
Bhattacharya, N., O'Donnell, J. & Stagg, S. M. The structure of the Sec13/31 COPII cage bound to Sec23. J. Mol. Biol. 420, 324–334 (2012).
Acknowledgements
F.B is supported by grants from the US National Institutes of Health (R01 GM101038), Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, U.S. DOE (DE-FG02-91ER20021), NASA (NNX12AN71G) and the National Science Foundation (MCB 0948584; 1243792). C.B. acknowledges support from the US National Institutes of Health (R01 GM52549).
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Glossary
- Anterograde transport
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Membrane traffic pathway in which a linear assembly of membrane-bound compartments facilitates cargo movement towards the cell surface.
- Retrograde transport
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Membrane traffic pathway in which a linear assembly of membrane-bound compartments facilitates cargo movement towards the ER.
- ER exit sites
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(ERES). Specialized regions on the surface of endoplasmic reticulum (ER) membranes where coat protein complex II (COPII) coat subunits are recruited and assembled into COPII carrier vesicles that transport secretory cargo from the ER.
- Unfolded protein response
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(UPR). A system of ancestral signalling pathways that are activated upon increased secretory protein load in the endoplasmic reticulum to ensure maintenance of cellular homeostasis.
- ER–Golgi intermediate compartment
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(ERGIC). An organelle that is visible in most mammalian cells at the interface between the endoplasmic reticulum (ER) and the Golgi and that is implicated in cargo concentration and sorting.
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Brandizzi, F., Barlowe, C. Organization of the ER–Golgi interface for membrane traffic control. Nat Rev Mol Cell Biol 14, 382–392 (2013). https://doi.org/10.1038/nrm3588
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DOI: https://doi.org/10.1038/nrm3588
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