Sequential interactions with Sec23 control the direction of vesicle traffic

Christopher Lord; Deepali Bhandari; Shekar Menon; Majid Ghassemian; Deborah Nycz; Jesse Hay; Pradipta Ghosh; Susan Ferro-Novick

doi:10.1038/nature09969

Sequential interactions with Sec23 control the direction of vesicle traffic

Christopher Lord
, Deepali Bhandari
, Shekar Menon
, Majid Ghassemian
, Deborah Nycz
, Jesse Hay
, Pradipta Ghosh
, Susan Ferro-Novick

Research output: Contribution to journal › Article › peer-review

157 Scopus citations

Abstract

How the directionality of vesicle traffic is achieved remains an important unanswered question in cell biology. The Sec23p/Sec24p coat complex sorts the fusion machinery (SNAREs) into vesicles as they bud from the endoplasmic reticulum (ER). Vesicle tethering to the Golgi begins when the tethering factor TRAPPI binds to Sec23p. Where the coat is released and how this event relates to membrane fusion is unknown. Here we use a yeast transport assay to demonstrate that an ER-derived vesicle retains its coat until it reaches the Golgi. A Golgi-associated kinase, Hrr25p (CK1Î́ orthologue), then phosphorylates the Sec23p/Sec24p complex. Coat phosphorylation and dephosphorylation are needed for vesicle fusion and budding, respectively. Additionally, we show that Sec23p interacts in a sequential manner with different binding partners, including TRAPPI and Hrr25p, to ensure the directionality of ER-Golgi traffic and prevent the back-fusion of a COPII vesicle with the ER. These events are conserved in mammalian cells.

Original language	English
Pages (from-to)	181-186
Number of pages	6
Journal	Nature
Volume	473
Issue number	7346
DOIs	https://doi.org/10.1038/nature09969
State	Published - May 12 2011

Funding

Acknowledgements We thank R. Schekman, M. Cyert, L. Miller, B. Glick, M. Lowe and E. Mizuno-Yamasaki for strains, constructs, purified protein and antibody; K. Reinisch for discussions; S. Chen, H. Cai and M. Garcia-Marcos for advice; W. Zhou and A. Lougheed for technical assistance. This work was supported by the Howard Hughes Medical Institute. Salary support for S.F.-N., D.B. and S.M. was provided by the Howard Hughes Medical Institute, P.G. was funded by the Burroughs Wellcome Fund and M.G. by the SRP Super Fund Research Program. Work at the University of Montana was supported by National Institutes of Health grant GM-059378 (to J.C.H.) and the National Institutes of Health COBRE Center grant RR-015583.

Funders	Funder number
GM-059378
Howard Hughes Medical Institute
P20RR015583
Burroughs Wellcome Fund

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10.1038/nature09969

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title = "Sequential interactions with Sec23 control the direction of vesicle traffic",

abstract = "How the directionality of vesicle traffic is achieved remains an important unanswered question in cell biology. The Sec23p/Sec24p coat complex sorts the fusion machinery (SNAREs) into vesicles as they bud from the endoplasmic reticulum (ER). Vesicle tethering to the Golgi begins when the tethering factor TRAPPI binds to Sec23p. Where the coat is released and how this event relates to membrane fusion is unknown. Here we use a yeast transport assay to demonstrate that an ER-derived vesicle retains its coat until it reaches the Golgi. A Golgi-associated kinase, Hrr25p (CK1{\^I}́ orthologue), then phosphorylates the Sec23p/Sec24p complex. Coat phosphorylation and dephosphorylation are needed for vesicle fusion and budding, respectively. Additionally, we show that Sec23p interacts in a sequential manner with different binding partners, including TRAPPI and Hrr25p, to ensure the directionality of ER-Golgi traffic and prevent the back-fusion of a COPII vesicle with the ER. These events are conserved in mammalian cells.",

author = "Christopher Lord and Deepali Bhandari and Shekar Menon and Majid Ghassemian and Deborah Nycz and Jesse Hay and Pradipta Ghosh and Susan Ferro-Novick",

note = "Funding Information: Acknowledgements We thank R. Schekman, M. Cyert, L. Miller, B. Glick, M. Lowe and E. Mizuno-Yamasaki for strains, constructs, purified protein and antibody; K. Reinisch for discussions; S. Chen, H. Cai and M. Garcia-Marcos for advice; W. Zhou and A. Lougheed for technical assistance. This work was supported by the Howard Hughes Medical Institute. Salary support for S.F.-N., D.B. and S.M. was provided by the Howard Hughes Medical Institute, P.G. was funded by the Burroughs Wellcome Fund and M.G. by the SRP Super Fund Research Program. Work at the University of Montana was supported by National Institutes of Health grant GM-059378 (to J.C.H.) and the National Institutes of Health COBRE Center grant RR-015583.",

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AU - Lord, Christopher

AU - Bhandari, Deepali

AU - Menon, Shekar

AU - Ghassemian, Majid

AU - Nycz, Deborah

AU - Hay, Jesse

AU - Ghosh, Pradipta

AU - Ferro-Novick, Susan

N1 - Funding Information: Acknowledgements We thank R. Schekman, M. Cyert, L. Miller, B. Glick, M. Lowe and E. Mizuno-Yamasaki for strains, constructs, purified protein and antibody; K. Reinisch for discussions; S. Chen, H. Cai and M. Garcia-Marcos for advice; W. Zhou and A. Lougheed for technical assistance. This work was supported by the Howard Hughes Medical Institute. Salary support for S.F.-N., D.B. and S.M. was provided by the Howard Hughes Medical Institute, P.G. was funded by the Burroughs Wellcome Fund and M.G. by the SRP Super Fund Research Program. Work at the University of Montana was supported by National Institutes of Health grant GM-059378 (to J.C.H.) and the National Institutes of Health COBRE Center grant RR-015583.

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N2 - How the directionality of vesicle traffic is achieved remains an important unanswered question in cell biology. The Sec23p/Sec24p coat complex sorts the fusion machinery (SNAREs) into vesicles as they bud from the endoplasmic reticulum (ER). Vesicle tethering to the Golgi begins when the tethering factor TRAPPI binds to Sec23p. Where the coat is released and how this event relates to membrane fusion is unknown. Here we use a yeast transport assay to demonstrate that an ER-derived vesicle retains its coat until it reaches the Golgi. A Golgi-associated kinase, Hrr25p (CK1Î́ orthologue), then phosphorylates the Sec23p/Sec24p complex. Coat phosphorylation and dephosphorylation are needed for vesicle fusion and budding, respectively. Additionally, we show that Sec23p interacts in a sequential manner with different binding partners, including TRAPPI and Hrr25p, to ensure the directionality of ER-Golgi traffic and prevent the back-fusion of a COPII vesicle with the ER. These events are conserved in mammalian cells.

AB - How the directionality of vesicle traffic is achieved remains an important unanswered question in cell biology. The Sec23p/Sec24p coat complex sorts the fusion machinery (SNAREs) into vesicles as they bud from the endoplasmic reticulum (ER). Vesicle tethering to the Golgi begins when the tethering factor TRAPPI binds to Sec23p. Where the coat is released and how this event relates to membrane fusion is unknown. Here we use a yeast transport assay to demonstrate that an ER-derived vesicle retains its coat until it reaches the Golgi. A Golgi-associated kinase, Hrr25p (CK1Î́ orthologue), then phosphorylates the Sec23p/Sec24p complex. Coat phosphorylation and dephosphorylation are needed for vesicle fusion and budding, respectively. Additionally, we show that Sec23p interacts in a sequential manner with different binding partners, including TRAPPI and Hrr25p, to ensure the directionality of ER-Golgi traffic and prevent the back-fusion of a COPII vesicle with the ER. These events are conserved in mammalian cells.

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Sequential interactions with Sec23 control the direction of vesicle traffic

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