COPI Selectively Drives Maturation of the Early Golgi

Overview

Journal Elife

Specialty Biology

Date 2015 Dec 29

PMID 26709839

Citations 46

Authors

Effrosyni Papanikou

Kasey J Day

Jotham Austin

Benjamin S Glick

Affiliations

Soon will be listed here.

Abstract

COPI coated vesicles carry material between Golgi compartments, but the role of COPI in the secretory pathway has been ambiguous. Previous studies of thermosensitive yeast COPI mutants yielded the surprising conclusion that COPI was dispensable both for the secretion of certain proteins and for Golgi cisternal maturation. To revisit these issues, we optimized the anchor-away method, which allows peripheral membrane proteins such as COPI to be sequestered rapidly by adding rapamycin. Video fluorescence microscopy revealed that COPI inactivation causes an early Golgi protein to remain in place while late Golgi proteins undergo cycles of arrival and departure. These dynamics generate partially functional hybrid Golgi structures that contain both early and late Golgi proteins, explaining how secretion can persist when COPI has been inactivated. Our findings suggest that cisternal maturation involves a COPI-dependent pathway that recycles early Golgi proteins, followed by multiple COPI-independent pathways that recycle late Golgi proteins.

Citing Articles

RudLOV is an optically synchronized cargo transport method revealing unexpected effects of dynasore.

Tago T, Ogawa T, Goto Y, Toyooka K, Tojima T, Nakano A EMBO Rep. 2024; 26(3):613-634.

PMID: 39658747 PMC: 11811055. DOI: 10.1038/s44319-024-00342-z.

Illuminating the Cryptococcus neoformans species complex: unveiling intracellular structures with fluorescent-protein-based markers.

Shi R, Lin X Genetics. 2024; 227(3).

PMID: 38752295 PMC: 11228865. DOI: 10.1093/genetics/iyae059.

Spatiotemporal dissection of the Golgi apparatus and the ER-Golgi intermediate compartment in budding yeast.

Tojima T, Suda Y, Jin N, Kurokawa K, Nakano A Elife. 2024; 13.

PMID: 38501165 PMC: 10950332. DOI: 10.7554/eLife.92900.

A CUG codon-adapted anchor-away toolkit for functional analysis of genes in .

Teli B, Nagar P, Priyadarshini Y, Poonia P, Natarajan K mSphere. 2024; 9(2):e0070323.

PMID: 38251906 PMC: 10900876. DOI: 10.1128/msphere.00703-23.

The Arf-GAP Age2 localizes to the late-Golgi via a conserved amphipathic helix.

Manzer K, Fromme J Mol Biol Cell. 2023; 34(12):ar119.

PMID: 37672345 PMC: 10846627. DOI: 10.1091/mbc.E23-07-0283.

References

Malsam J, Satoh A, Pelletier L, Warren G . Golgin tethers define subpopulations of COPI vesicles. Science. 2005; 307(5712):1095-8. DOI: 10.1126/science.1108061. View

Bonifacino J . Adaptor proteins involved in polarized sorting. J Cell Biol. 2014; 204(1):7-17. PMC: 3882786. DOI: 10.1083/jcb.201310021. View

Orci L, Malhotra V, Amherdt M, Serafini T, Rothman J . Dissection of a single round of vesicular transport: sequential intermediates for intercisternal movement in the Golgi stack. Cell. 1989; 56(3):357-68. DOI: 10.1016/0092-8674(89)90239-0. View

Yu X, Breitman M, Goldberg J . A structure-based mechanism for Arf1-dependent recruitment of coatomer to membranes. Cell. 2012; 148(3):530-42. PMC: 3285272. DOI: 10.1016/j.cell.2012.01.015. View

Ren Y, Yip C, Tripathi A, Huie D, Jeffrey P, Walz T . A structure-based mechanism for vesicle capture by the multisubunit tethering complex Dsl1. Cell. 2009; 139(6):1119-29. PMC: 2806190. DOI: 10.1016/j.cell.2009.11.002. View

Papanikou E, Glick B . The yeast Golgi apparatus: insights and mysteries. FEBS Lett. 2009; 583(23):3746-51. PMC: 2788027. DOI: 10.1016/j.febslet.2009.10.072. View

Serafini T, Orci L, Amherdt M, Brunner M, Kahn R, Rothman J . ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP-binding protein. Cell. 1991; 67(2):239-53. DOI: 10.1016/0092-8674(91)90176-y. View

Mowbrey K, Dacks J . Evolution and diversity of the Golgi body. FEBS Lett. 2009; 583(23):3738-45. DOI: 10.1016/j.febslet.2009.10.025. View

Kunz J, Henriquez R, Schneider U, Movva N, Hall M . Target of rapamycin in yeast, TOR2, is an essential phosphatidylinositol kinase homolog required for G1 progression. Cell. 1993; 73(3):585-96. DOI: 10.1016/0092-8674(93)90144-f. View

10.

Sipos G, Brickner J, Brace E, Chen L, Rambourg A, Kepes F . Soi3p/Rav1p functions at the early endosome to regulate endocytic trafficking to the vacuole and localization of trans-Golgi network transmembrane proteins. Mol Biol Cell. 2004; 15(7):3196-209. PMC: 452576. DOI: 10.1091/mbc.e03-10-0755. View

11.

Lorenz M, Heitman J . TOR mutations confer rapamycin resistance by preventing interaction with FKBP12-rapamycin. J Biol Chem. 1995; 270(46):27531-7. DOI: 10.1074/jbc.270.46.27531. View

12.

Park S, Yang J, Schmider A, Soberman R, Hsu V . Coordinated regulation of bidirectional COPI transport at the Golgi by CDC42. Nature. 2015; 521(7553):529-32. PMC: 4449304. DOI: 10.1038/nature14457. View

13.

Sherman F . Getting started with yeast. Methods Enzymol. 1991; 194:3-21. DOI: 10.1016/0076-6879(91)94004-v. View

14.

Hosobuchi M, Kreis T, Schekman R . SEC21 is a gene required for ER to Golgi protein transport that encodes a subunit of a yeast coatomer. Nature. 1992; 360(6404):603-5. DOI: 10.1038/360603a0. View

15.

Boehm J, Letourneur F, Ballensiefen W, Ossipov D, Demolliere C, Schmitt H . Sec12p requires Rer1p for sorting to coatomer (COPI)-coated vesicles and retrieval to the ER. J Cell Sci. 1997; 110 ( Pt 8):991-1003. DOI: 10.1242/jcs.110.8.991. View

16.

Michelsen K, Schmid V, Metz J, Heusser K, Liebel U, Schwede T . Novel cargo-binding site in the beta and delta subunits of coatomer. J Cell Biol. 2007; 179(2):209-17. PMC: 2064757. DOI: 10.1083/jcb.200704142. View

17.

Salama N, Chuang J, Schekman R . Sec31 encodes an essential component of the COPII coat required for transport vesicle budding from the endoplasmic reticulum. Mol Biol Cell. 1997; 8(2):205-17. PMC: 276074. DOI: 10.1091/mbc.8.2.205. View

18.

Zink S, Wenzel D, Wurm C, Schmitt H . A link between ER tethering and COP-I vesicle uncoating. Dev Cell. 2009; 17(3):403-16. DOI: 10.1016/j.devcel.2009.07.012. View

19.

Grunberg R, Ferrar T, van der Sloot A, Constante M, Serrano L . Building blocks for protein interaction devices. Nucleic Acids Res. 2010; 38(8):2645-62. PMC: 2860130. DOI: 10.1093/nar/gkq152. View

20.

Matsuura-Tokita K, Takeuchi M, Ichihara A, Mikuriya K, Nakano A . Live imaging of yeast Golgi cisternal maturation. Nature. 2006; 441(7096):1007-10. DOI: 10.1038/nature04737. View