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The maturing role of COPI vesicles in intra-Golgi transport

Nature Reviews Molecular Cell Biology volume 6, pages 812–817 (2005)Cite this article

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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Figure 1: An electron microscopy image of a Golgi region in a high-pressure-frozen and freeze-substituted D1 dendritic cell.
Figure 2: A schematic representation of four different models of intra-Golgi transport.
Figure 3: An overview of the proposed roles of COPI vesicles.
Figure 4: A three-dimensional tomographic reconstruction of a Golgi stack in a high-pressure-frozen and freeze-substituted HepG2 hepatoma cell.

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References

  1. Warren, G. & Malhotra, V. The organisation of the Golgi apparatus. Curr. Opin. Cell Biol. 10, 493–498 (1998).

    Article  CAS  Google Scholar 

  2. Mellman, I. & Warren, G. The road taken: past and future foundations of membrane traffic. Cell 100, 99–112 (2000).

    Article  CAS  Google Scholar 

  3. Pelham, H. R. & Rothman, J. E. The debate about transport in the Golgi — two sides of the same coin? Cell 102, 713–719 (2000).

    Article  CAS  Google Scholar 

  4. Glick, B. S. Organisation of the Golgi apparatus. Curr. Opin. Cell Biol. 12, 450–456 (2000).

    Article  CAS  Google Scholar 

  5. Storrie, B. & Nilsson, T. The Golgi apparatus: balancing new with old. Traffic. 3, 521–529 (2002).

    Article  CAS  Google Scholar 

  6. Marsh, B. J. & Howell, K. E. The mammalian Golgi-complex debates. Nature Rev. Mol. Cell Biol. 3, 789–795 (2002).

    Article  CAS  Google Scholar 

  7. Elsner, M., Hashimoto, H. & Nilsson, T. Cisternal maturation and vesicle transport: join the band wagon! Mol. Membr. Biol. 20, 221–229 (2003).

    Article  CAS  Google Scholar 

  8. 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).

    Article  CAS  Google Scholar 

  9. 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).

    CAS  PubMed  Google Scholar 

  10. Orci, L. et al. Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90, 335–349 (1997).

    Article  CAS  Google Scholar 

  11. 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).

    Article  Google Scholar 

  12. Ostermann, J. et al. Stepwise assembly of functionally active transport vesicles. Cell 75, 1015–1025 (1993).

    Article  CAS  Google Scholar 

  13. Rothman, J. E. Mechanisms of intracellular protein transport. Nature 372, 55–63 (1994).

    Article  CAS  Google Scholar 

  14. 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).

    Article  CAS  Google Scholar 

  15. Pelham, H. R. Getting through the Golgi complex. Trends Cell Biol. 8, 45–49 (1998).

    Article  CAS  Google Scholar 

  16. 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).

    Article  CAS  Google Scholar 

  17. 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).

    Article  CAS  Google Scholar 

  18. Allan, B. B. & Balch, W. E. Protein sorting by directed maturation of Golgi compartments. Science 285, 63–66 (1999).

    Article  CAS  Google Scholar 

  19. 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).

    Article  CAS  Google Scholar 

  20. 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).

    Article  CAS  Google Scholar 

  21. Melkonian, M., Becker, B. & Becker, D. Scale formation in algae. J. Electron Microsc. Tech. 17, 165–178 (1991).

    Article  CAS  Google Scholar 

  22. 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).

    Article  CAS  Google Scholar 

  23. Bonfanti, L. et al. Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell 95, 993–1003 (1998).

    Article  CAS  Google Scholar 

  24. Malsam, J., Satoh, A., Pelletier, L. & Warren, G. Golgin tethers define sub-populations of COPI vesicles. Science 307, 1095–1098 (2005).

    Article  CAS  Google Scholar 

  25. 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).

    Article  CAS  Google Scholar 

  26. 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).

    Article  CAS  Google Scholar 

  27. 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).

    Article  CAS  Google Scholar 

  28. Trucco, A. et al. Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments. Nature Cell Biol. 6, 1071–1081 (2004).

    Article  CAS  Google Scholar 

  29. 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).

    Article  CAS  Google Scholar 

  30. 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).

    Article  CAS  Google Scholar 

  31. 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).

    Article  CAS  Google Scholar 

  32. Cosson, P. & Letourneur, F. Coatomer interaction with di-lysine endoplasmic reticulum retention motifs. Science 263, 1629–1631 (1994).

    Article  CAS  Google Scholar 

  33. 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).

    Article  CAS  Google Scholar 

  34. 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).

    Article  CAS  Google Scholar 

  35. 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).

    CAS  PubMed  Google Scholar 

  36. 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).

    Article  CAS  Google Scholar 

  37. Goldberg, J. Decoding of sorting signals by coatomer through a GTPase switch in the COPI coat complex. Cell 100, 671–679 (2000).

    Article  CAS  Google Scholar 

  38. Kartberg, F., Elsner, M., Froderberg, L., Asp, L. & Nilsson, T. Commuting between Golgi cisternae — mind the gap. Biochim. Biophys. Acta (in the press).

  39. 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).

    Article  CAS  Google Scholar 

  40. 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).

    Article  CAS  Google Scholar 

  41. 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).

    Article  CAS  Google Scholar 

  42. 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).

    Article  CAS  Google Scholar 

  43. Rabouille, C. & Nilsson, T. Redrawing compartmental boundaries in the exocytic pathway. FEBS Lett. 369, 97–100 (1995).

    Article  CAS  Google Scholar 

  44. 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).

    Article  CAS  Google Scholar 

  45. 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).

    CAS  PubMed  Google Scholar 

  46. 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).

    Article  CAS  Google Scholar 

  47. Volchuk, A. et al. Megavesicles implicated in the rapid transport of intracisternal aggregates across the Golgi stack. Cell 102, 335–348 (2000).

    Article  CAS  Google Scholar 

  48. Nilsson, T. et al. Overlapping distribution of two glycosyltransferases in the Golgi apparatus of HeLa cells. J. Cell Biol. 120, 5–13 (1993).

    Article  CAS  Google Scholar 

  49. Rabouille, C. et al. Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J. Cell Sci. 108, 1617–1627 (1995).

    CAS  PubMed  Google Scholar 

  50. 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).

    Article  CAS  Google Scholar 

  51. Munro, S. Sequences within and adjacent to the transmembrane segment of α2,6-sialyltransferase specify Golgi retention. EMBO J. 10, 3577–3588 (1991).

    Article  CAS  Google Scholar 

  52. Nilsson, T. et al. Kin recognition between medial Golgi enzymes in HeLa cells. EMBO J. 13, 562–574 (1994).

    Article  CAS  Google Scholar 

  53. Nilsson, T. & Warren, G. Retention and retrieval in the endoplasmic reticulum and the Golgi apparatus. Curr. Opin. Cell Biol. 6, 517–521 (1994).

    Article  CAS  Google Scholar 

  54. Munro, S. An investigation of the role of transmembrane domains in Golgi protein retention. EMBO J. 14, 4695–4704 (1995).

    Article  CAS  Google Scholar 

  55. Munro, S. Localization of proteins to the Golgi apparatus. Trends Cell Biol. 8, 11–15 (1998).

    Article  CAS  Google Scholar 

  56. Letourneur, F. et al. Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79, 1199–1207 (1994).

    Article  CAS  Google Scholar 

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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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  1. Department of Cell Biology and Institute of Biomembranes, The Cell Microscopy Center, University Medical Center Utrecht, Heidelberglaan 100, Utrecht, 3584 CX, The Netherlands

    Catherine Rabouille & Judith Klumperman

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  1. Catherine Rabouille
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Correspondence to Judith Klumperman.

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Supplementary information

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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ARF1

Mannosidase II

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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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