Abstract
COPI vesicles that surround the Golgi stack were first implicated in the anterograde movement of cargo, and then in the retrograde movement of Golgi enzymes. Recently, their role has been challenged again, and we discuss new data that both confirm and modify our view of these carriers.
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References
Warren, G. & Malhotra, V. The organisation of the Golgi apparatus. Curr. Opin. Cell Biol. 10, 493–498 (1998).
Mellman, I. & Warren, G. The road taken: past and future foundations of membrane traffic. Cell 100, 99–112 (2000).
Pelham, H. R. & Rothman, J. E. The debate about transport in the Golgi — two sides of the same coin? Cell 102, 713–719 (2000).
Glick, B. S. Organisation of the Golgi apparatus. Curr. Opin. Cell Biol. 12, 450–456 (2000).
Storrie, B. & Nilsson, T. The Golgi apparatus: balancing new with old. Traffic. 3, 521–529 (2002).
Marsh, B. J. & Howell, K. E. The mammalian Golgi-complex debates. Nature Rev. Mol. Cell Biol. 3, 789–795 (2002).
Elsner, M., Hashimoto, H. & Nilsson, T. Cisternal maturation and vesicle transport: join the band wagon! Mol. Membr. Biol. 20, 221–229 (2003).
Oprins, A., Duden, R., Kreis, T. E., Geuze, H. J. & Slot, J. W. βCOP localizes mainly to the cis-Golgi side in exocrine pancreas. J. Cell Biol. 121, 49–59 (1993).
Griffiths, G., Pepperkok, R., Locker, J. K. & Kreis, T. E. Immunocytochemical localization of βCOP to the ER–Golgi boundary & the TGN. J. Cell Sci. 108, 2839–2856 (1995).
Orci, L. et al. Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90, 335–349 (1997).
Martínez-Menárguez, J. A. et al. Peri-Golgi vesicles contain retrograde but not anterograde proteins consistent with the cisternal progression model of intra-Golgi transport. J. Cell Biol. 155, 1213–1224 (2001).
Ostermann, J. et al. Stepwise assembly of functionally active transport vesicles. Cell 75, 1015–1025 (1993).
Rothman, J. E. Mechanisms of intracellular protein transport. Nature 372, 55–63 (1994).
Glick, B. S., Elston, T. & Oster, G. A cisternal maturation mechanism can explain the asymmetry of the Golgi stack. FEBS Lett. 414, 177–181 (1997).
Pelham, H. R. Getting through the Golgi complex. Trends Cell Biol. 8, 45–49 (1998).
Lanoix, J. et al. GTP hydrolysis by arf-1 mediates sorting & concentration of Golgi resident enzymes into functional COP I vesicles. EMBO J. 18, 4935–4948 (1999).
Lanoix, J. et al. Sorting of Golgi resident proteins into different subpopulations of COPI vesicles: a role for ArfGAP1. J. Cell Biol. 155, 1199–1212 (2001).
Allan, B. B. & Balch, W. E. Protein sorting by directed maturation of Golgi compartments. Science 285, 63–66 (1999).
Karim, A., Cournil, I. & Leblond, C. P. Immunohistochemical localization of procollagens. II. Electron microscopic distribution of procollagen I antigenicity in the odontoblasts and predentin of rat incisor teeth by a direct method using peroxidase linked antibodies. J. Histochem. Cytochem. 27, 1070–1083 (1979).
Holthuis, J. C., Nichols, B. J., Dhruvakumar, S. & Pelham, H. R. Two syntaxin homologues in the TGN/endosomal system of yeast. EMBO J. 17, 113–126 (1998).
Melkonian, M., Becker, B. & Becker, D. Scale formation in algae. J. Electron Microsc. Tech. 17, 165–178 (1991).
Mironov, A. A., Weidman, P. & Luini, A. Variations on the intracellular transport theme: maturing cisternae and trafficking tubules. J. Cell Biol. 138, 481–484 (1997).
Bonfanti, L. et al. Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell 95, 993–1003 (1998).
Malsam, J., Satoh, A., Pelletier, L. & Warren, G. Golgin tethers define sub-populations of COPI vesicles. Science 307, 1095–1098 (2005).
Cosson, P., Amherdt, M., Rothman, J. E. & Orci, L. A resident Golgi protein is excluded from peri-Golgi vesicles in NRK cells. Proc. Natl Acad. Sci. USA 99, 12831–12834 (2002).
Orci, L., Amherdt, M., Ravazzola, M., Perrelet, A. & Rothman, J. E. Exclusion of Golgi residents from transport vesicles budding from Golgi cisternae in intact cells. J. Cell Biol. 150, 1263–1270 (2000).
Kweon, H. S. et al. Golgi enzymes are enriched in perforated zones of Golgi cisternae but are depleted in COPI vesicles. Mol. Biol. Cell 15, 4710–4724 (2004).
Trucco, A. et al. Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments. Nature Cell Biol. 6, 1071–1081 (2004).
Dahan, S., Ahluwalia, J. P., Wong, L., Posner, B. I. & Bergeron, J. J. Concentration of intracellular hepatic apolipoprotein E in Golgi apparatus saccular distensions and endosomes. J. Cell Biol. 127, 1859–1869 (1994).
Mironov, A. A. et al. Small cargo proteins and large aggregates can traverse the Golgi by a common mechanism without leaving the lumen of cisternae. J. Cell Biol. 155, 1225–1238 (2001).
Dunn, K. W., McGraw, T. E. & Maxfield, F. R. Iterative fractionation of recycling receptors from lysosomally destined ligands in an early sorting endosome. J. Cell Biol. 109, 3303–3314 (1989).
Cosson, P. & Letourneur, F. Coatomer interaction with di-lysine endoplasmic reticulum retention motifs. Science 263, 1629–1631 (1994).
Nelson, D. S., Alvarez, C., Garcia-Mata, R., Fialkowski, E. & Sztul, E. The membrane transport factor TAP/p115 cycles between the Golgi and earlier secretory compartments and contains distinct domains required for its localization and function. J. Cell Biol. 143, 319–331 (1998).
Malsam, J., Gommel, D., Wieland, F. T. & Nickel, W. A role for ADP ribosylation factor in the control of cargo uptake during COPI-coated vesicle biogenesis. FEBS Lett. 462, 267–272 (1999).
Pepperkok, R., Whitney, J. A., Gomez, M. & Kreis, T. E. COPI vesicles accumulating in the presence of a GTP restricted arf1 mutant are depleted of anterograde and retrograde cargo. J. Cell Sci. 113, 135–144 (2000).
Lee, S. Y., Yang, J. S., Hong, W., Premont, R. T. & Hsu, V. W. ARFGAP1 plays a central role in coupling COPI cargo sorting with vesicle formation. J. Cell Biol. 168, 281–290 (2005).
Goldberg, J. Decoding of sorting signals by coatomer through a GTPase switch in the COPI coat complex. Cell 100, 671–679 (2000).
Kartberg, F., Elsner, M., Froderberg, L., Asp, L. & Nilsson, T. Commuting between Golgi cisternae — mind the gap. Biochim. Biophys. Acta (in the press).
Wegmann, D., Hess, P., Baier, C., Wieland, F. T. & Reinhard, C. Novel isotypic γ/ξ subunits reveal three coatomer complexes in mammals. Mol. Cell Biol. 24, 1070–1080 (2004).
Gillingham, A. K., Pfeifer, A. C., Munro, S. CASP, the alternatively spliced product of the gene encoding the CCAAT-displacement protein transcription factor, is a Golgi membrane protein related to giantin. Mol. Biol. Cell. 13, 3761–3774 (2002).
Linstedt, A. D. & Hauri, H. P. Giantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa. Mol. Biol. Cell 4, 679–693 (1993).
Marsh, B. J., Mastronarde, D. N., Buttle, K. F., Howell, K. E. & McIntosh, J. R. Organellar relationships in the Golgi region of the pancreatic β cell line, HIT-T15, visualized by high resolution electron tomography. Proc. Natl Acad. Sci. USA 98, 2399–2406 (2001).
Rabouille, C. & Nilsson, T. Redrawing compartmental boundaries in the exocytic pathway. FEBS Lett. 369, 97–100 (1995).
Clermont, Y., Rambourg, A. & Hermo, L. Connections between the various elements of the cis- and mid-compartments of the Golgi apparatus of early rat spermatids. Anat. Rec. 240, 469–480 (1994).
Tanaka, K., Mitsushima, A., Fukudome, H. & Kashima, Y. Three-dimensional architecture of the Golgi complex observed by high resolution scanning electron microscopy. J. Submicrosc. Cytol. 18, 1–9 (1986).
Marsh, B. J., Volkmann, N., McIntosh, J. R. & Howell, K. E. Direct continuities between cisternae at different levels of the Golgi complex in glucose-stimulated mouse islet β cells. Proc. Natl Acad. Sci. USA 101, 5565–5570 (2004).
Volchuk, A. et al. Megavesicles implicated in the rapid transport of intracisternal aggregates across the Golgi stack. Cell 102, 335–348 (2000).
Nilsson, T. et al. Overlapping distribution of two glycosyltransferases in the Golgi apparatus of HeLa cells. J. Cell Biol. 120, 5–13 (1993).
Rabouille, C. et al. Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J. Cell Sci. 108, 1617–1627 (1995).
Nilsson, T., Lucocq, J. M., Mackay, D. & Warren, G. The membrane spanning domain of β-1,4-galactosyltransferase specifies trans Golgi localization. EMBO J. 10, 3567–3575 (1991).
Munro, S. Sequences within and adjacent to the transmembrane segment of α2,6-sialyltransferase specify Golgi retention. EMBO J. 10, 3577–3588 (1991).
Nilsson, T. et al. Kin recognition between medial Golgi enzymes in HeLa cells. EMBO J. 13, 562–574 (1994).
Nilsson, T. & Warren, G. Retention and retrieval in the endoplasmic reticulum and the Golgi apparatus. Curr. Opin. Cell Biol. 6, 517–521 (1994).
Munro, S. An investigation of the role of transmembrane domains in Golgi protein retention. EMBO J. 14, 4695–4704 (1995).
Munro, S. Localization of proteins to the Golgi apparatus. Trends Cell Biol. 8, 11–15 (1998).
Letourneur, F. et al. Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79, 1199–1207 (1994).
Acknowledgements
Our thanks to J. L. Murk and H. Geuze (Department of Cell Biology, University Medical Center Utrecht, The Netherlands) and A. J. Koster (Department of Molecular Cell Biology, Faculty of Biology, Utrecht University, The Netherlands) for the electron microscopy figures and the Supplementary information S1 (movie). We especially thank W. J. Geerts (Department of Molecular Cell Biology, Faculty of Biology, Utrecht University, The Netherlands) for the acquisition of tomograms, and also T. Nilsson and G. Warren for sharing unpublished data. We apologize to our colleagues who have contributed to our understanding of the Golgi but whose work could not be mentioned in this article due to space constraints.
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Supplementary information S1
Movie S1 | A movie of a Golgi stack. A movie of the Golgi stack that is shown in FIG. 4. The movie zooms in on the cis side of the Golgi (light blue in FIG. 4), and an arrow highlights two coatomer protein complex-I (COPI)-coated vesicles (shown in pink in FIG. 4). By going up and down through the reconstructed volume, it is clear that the highlighted structures are free COPI vesicles. This movie was kindly provided by Jean Luc Murk and Hans Geuze (Department of Cell Biology, University Medical Center Utrecht, The Netherlands) and Willie Geerts and Bram Koster (Department of Molecular Cell Biology, Faculty of Biology, Utrecht University, The Netherlands). (AVI 3634 kb)
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Rabouille, C., Klumperman, J. The maturing role of COPI vesicles in intra-Golgi transport. Nat Rev Mol Cell Biol 6, 812–817 (2005). https://doi.org/10.1038/nrm1735
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DOI: https://doi.org/10.1038/nrm1735
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