The pathways of membrane traffic within the Golgi apparatus are not fully known. This question was addressed using the yeast Saccharomyces cerevisiae, in which the maturation of individual Golgi cisternae can be visualized. We recently proposed that the AP-1 clathrin adaptor mediates intra-Golgi recycling late in the process of cisternal maturation. Here, we demonstrate that AP-1 cooperates with the Ent5 clathrin adaptor to recycle a set of Golgi transmembrane proteins, including some that were previously thought to pass through endosomes. This recycling can be detected by removing AP-1 and Ent5, thereby diverting the AP-1/Ent5–dependent Golgi proteins into an alternative recycling loop that involves traffic to the plasma membrane followed by endocytosis. Unexpectedly, various AP-1/Ent5–dependent Golgi proteins show either intermediate or late kinetics of residence in maturing cisternae. We infer that the AP-1/Ent5 pair mediates two sequential intra-Golgi recycling pathways that define two classes of Golgi proteins. This insight can explain the polarized distribution of transmembrane proteins in the Golgi.
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3 January 2022
Article|
November 05 2021
Clathrin adaptors mediate two sequential pathways of intra-Golgi recycling
Jason C. Casler
,
Jason C. Casler
Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL
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Natalie Johnson
,
Natalie Johnson
Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL
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Adam H. Krahn
,
Adam H. Krahn
Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL
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Areti Pantazopoulou,
Areti Pantazopoulou
Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL
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Kasey J. Day
,
Kasey J. Day
Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL
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Benjamin S. Glick
Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL
Correspondence to Benjamin S. Glick: bsglick@uchicago.edu
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Jason C. Casler
Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL
Natalie Johnson
Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL
Adam H. Krahn
Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL
Areti Pantazopoulou
Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL
Kasey J. Day
Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, IL
Correspondence to Benjamin S. Glick: bsglick@uchicago.edu
Received:
March 29 2021
Revision Received:
September 16 2021
Accepted:
October 26 2021
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding
Funder(s):
National Institutes of Health
- Award Id(s): P30 CA014599
Funder(s):
NIH
- Award Id(s): R01 GM137004
Funder(s):
NIH
- Award Id(s): T32 GM007183
© 2021 Casler et al.
2021
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Cell Biol (2022) 221 (1): e202103199.
Article history
Received:
March 29 2021
Revision Received:
September 16 2021
Accepted:
October 26 2021
Citation
Jason C. Casler, Natalie Johnson, Adam H. Krahn, Areti Pantazopoulou, Kasey J. Day, Benjamin S. Glick; Clathrin adaptors mediate two sequential pathways of intra-Golgi recycling. J Cell Biol 3 January 2022; 221 (1): e202103199. doi: https://doi.org/10.1083/jcb.202103199
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