Copii collar defines the boundary between er and er exit site and does not coat cargo containers

Olga Shomron; Inbar Nevo-Yassaf; Tamar Aviad; Yakey Yaffe; Eitan Erez Zahavi; Anna Dukhovny; Eran Perlson; Ilya Brodsky; Adva Yeheskel; Metsada Pasmanik-Chor; Anna Mironov; Galina V. Beznoussenko; Alexander A. Mironov; Ella H. Sklan; George H. Patterson; Yoji Yonemura; Mara Sannai; Christoph Kaether; Koret Hirschberg

doi:10.1083/jcb.201907224

Copii collar defines the boundary between er and er exit site and does not coat cargo containers

Olga Shomron, Inbar Nevo-Yassaf, Tamar Aviad, Yakey Yaffe, Eitan Erez Zahavi, Anna Dukhovny, Eran Perlson, Ilya Brodsky, Adva Yeheskel, Metsada Pasmanik-Chor, Anna Mironov, Galina V. Beznoussenko, Alexander A. Mironov, Ella H. Sklan, George H. Patterson, Yoji Yonemura, Mara Sannai, Christoph Kaether^*, Koret Hirschberg^*

^*Corresponding author for this work

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

51 Scopus citations

Abstract

COPII and COPI mediate the formation of membrane vesicles translocating in opposite directions within the secretory pathway. Live-cell and electron microscopy revealed a novel mode of function for COPII during cargo export from the ER. COPII is recruited to membranes defining the boundary between the ER and ER exit sites, facilitating selective cargo concentration. Using direct observation of living cells, we monitored cargo selection processes, accumulation, and fission of COPII-free ERES membranes. CRISPR/Cas12a tagging, the RUSH system, and pharmaceutical and genetic perturbations of ER-Golgi transport demonstrated that the COPII coat remains bound to the ER–ERES boundary during protein export. Manipulation of the cargobinding domain in COPII Sec24B prohibits cargo accumulation in ERES. These findings suggest a role for COPII in selecting and concentrating exported cargo rather than coating Golgi-bound carriers. These findings transform our understanding of coat proteins’ role in ER-to-Golgi transport.

Original language	English
Article number	e201907224
Journal	Journal of Cell Biology
Volume	220
Issue number	6
DOIs	https://doi.org/10.1083/jcb.201907224
State	Published - 2021

Funding

Funders	Funder number
Nihal Altan Bonnet
National Institutes of Health
National Institute of Biomedical Imaging and Bioengineering	ZIAEB000071
Israel Science Foundation	1063/16

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10.1083/jcb.201907224

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Shomron, O., Nevo-Yassaf, I., Aviad, T., Yaffe, Y., Zahavi, E. E., Dukhovny, A., Perlson, E., Brodsky, I., Yeheskel, A., Pasmanik-Chor, M., Mironov, A., Beznoussenko, G. V., Mironov, A. A., Sklan, E. H., Patterson, G. H., Yonemura, Y., Sannai, M., Kaether, C., & Hirschberg, K. (2021). Copii collar defines the boundary between er and er exit site and does not coat cargo containers. Journal of Cell Biology, 220(6), Article e201907224. https://doi.org/10.1083/jcb.201907224

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title = "Copii collar defines the boundary between er and er exit site and does not coat cargo containers",

abstract = "COPII and COPI mediate the formation of membrane vesicles translocating in opposite directions within the secretory pathway. Live-cell and electron microscopy revealed a novel mode of function for COPII during cargo export from the ER. COPII is recruited to membranes defining the boundary between the ER and ER exit sites, facilitating selective cargo concentration. Using direct observation of living cells, we monitored cargo selection processes, accumulation, and fission of COPII-free ERES membranes. CRISPR/Cas12a tagging, the RUSH system, and pharmaceutical and genetic perturbations of ER-Golgi transport demonstrated that the COPII coat remains bound to the ER–ERES boundary during protein export. Manipulation of the cargobinding domain in COPII Sec24B prohibits cargo accumulation in ERES. These findings suggest a role for COPII in selecting and concentrating exported cargo rather than coating Golgi-bound carriers. These findings transform our understanding of coat proteins{\textquoteright} role in ER-to-Golgi transport.",

author = "Olga Shomron and Inbar Nevo-Yassaf and Tamar Aviad and Yakey Yaffe and Zahavi, {Eitan Erez} and Anna Dukhovny and Eran Perlson and Ilya Brodsky and Adva Yeheskel and Metsada Pasmanik-Chor and Anna Mironov and Beznoussenko, {Galina V.} and Mironov, {Alexander A.} and Sklan, {Ella H.} and Patterson, {George H.} and Yoji Yonemura and Mara Sannai and Christoph Kaether and Koret Hirschberg",

note = "Publisher Copyright: {\textcopyright} 2021 Shomron et al.",

year = "2021",

doi = "10.1083/jcb.201907224",

language = "אנגלית",

volume = "220",

journal = "Journal of Cell Biology",

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Shomron, O, Nevo-Yassaf, I, Aviad, T, Yaffe, Y, Zahavi, EE, Dukhovny, A, Perlson, E, Brodsky, I, Yeheskel, A, Pasmanik-Chor, M, Mironov, A, Beznoussenko, GV, Mironov, AA, Sklan, EH, Patterson, GH, Yonemura, Y, Sannai, M, Kaether, C & Hirschberg, K 2021, 'Copii collar defines the boundary between er and er exit site and does not coat cargo containers', Journal of Cell Biology, vol. 220, no. 6, e201907224. https://doi.org/10.1083/jcb.201907224

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T1 - Copii collar defines the boundary between er and er exit site and does not coat cargo containers

AU - Shomron, Olga

AU - Nevo-Yassaf, Inbar

AU - Aviad, Tamar

AU - Yaffe, Yakey

AU - Zahavi, Eitan Erez

AU - Dukhovny, Anna

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AU - Brodsky, Ilya

AU - Yeheskel, Adva

AU - Pasmanik-Chor, Metsada

AU - Mironov, Anna

AU - Beznoussenko, Galina V.

AU - Mironov, Alexander A.

AU - Sklan, Ella H.

AU - Patterson, George H.

AU - Yonemura, Yoji

AU - Sannai, Mara

AU - Kaether, Christoph

AU - Hirschberg, Koret

PY - 2021

Y1 - 2021

N2 - COPII and COPI mediate the formation of membrane vesicles translocating in opposite directions within the secretory pathway. Live-cell and electron microscopy revealed a novel mode of function for COPII during cargo export from the ER. COPII is recruited to membranes defining the boundary between the ER and ER exit sites, facilitating selective cargo concentration. Using direct observation of living cells, we monitored cargo selection processes, accumulation, and fission of COPII-free ERES membranes. CRISPR/Cas12a tagging, the RUSH system, and pharmaceutical and genetic perturbations of ER-Golgi transport demonstrated that the COPII coat remains bound to the ER–ERES boundary during protein export. Manipulation of the cargobinding domain in COPII Sec24B prohibits cargo accumulation in ERES. These findings suggest a role for COPII in selecting and concentrating exported cargo rather than coating Golgi-bound carriers. These findings transform our understanding of coat proteins’ role in ER-to-Golgi transport.

AB - COPII and COPI mediate the formation of membrane vesicles translocating in opposite directions within the secretory pathway. Live-cell and electron microscopy revealed a novel mode of function for COPII during cargo export from the ER. COPII is recruited to membranes defining the boundary between the ER and ER exit sites, facilitating selective cargo concentration. Using direct observation of living cells, we monitored cargo selection processes, accumulation, and fission of COPII-free ERES membranes. CRISPR/Cas12a tagging, the RUSH system, and pharmaceutical and genetic perturbations of ER-Golgi transport demonstrated that the COPII coat remains bound to the ER–ERES boundary during protein export. Manipulation of the cargobinding domain in COPII Sec24B prohibits cargo accumulation in ERES. These findings suggest a role for COPII in selecting and concentrating exported cargo rather than coating Golgi-bound carriers. These findings transform our understanding of coat proteins’ role in ER-to-Golgi transport.

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Copii collar defines the boundary between er and er exit site and does not coat cargo containers

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