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Retrograde trafficking and quality control of yeast synaptobrevin, Snc1, are conferred by its transmembrane domain

Synaptobrevin/vesicle-associated membrane protein 2 (VAMP2) is an essential soluble N-ethyl maleimide–sensitive factor attachment protein receptor (SNARE) protein that has been extensively studied in its role in synaptic vesicle fusion. However, sorting and trafficking of VAMP2 within the endosomal...

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Autores principales: Ma, Mengxiao, Burd, Christopher G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6727757/
https://www.ncbi.nlm.nih.gov/pubmed/31067149
http://dx.doi.org/10.1091/mbc.E19-02-0117
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author Ma, Mengxiao
Burd, Christopher G.
author_facet Ma, Mengxiao
Burd, Christopher G.
author_sort Ma, Mengxiao
collection PubMed
description Synaptobrevin/vesicle-associated membrane protein 2 (VAMP2) is an essential soluble N-ethyl maleimide–sensitive factor attachment protein receptor (SNARE) protein that has been extensively studied in its role in synaptic vesicle fusion. However, sorting and trafficking of VAMP2 within the endosomal system is not well understood. Here, we use the yeast VAMP2 homologue Snc1 to investigate the pathways and signals required for endocytic trafficking. We identify two genetically distinct retrieval pathways from the endosomal system: a plasma membrane recycling pathway that requires the Rcy1 F-box protein and a retrograde pathway originating from the multivesicular/prevacuole endosome dependent on the Snx4-Atg20 sorting nexin complex. Lysine residues within the transmembrane domain of Snc1 are necessary for presentation of a Snx4-Atg20–dependent sorting signal located within its juxtamembrane region. Mutations of the transmembrane lysine residues ablate retrograde sorting and subject Snc1 to quality control via sorting into the degradative multivesicular endosome pathway. Degradative sorting requires lysine residues in the juxtamembrane region of Snc1 and is mediated by the Rsp5 ubiquitin ligase and its transmembrane adapters, Ear1 and Ssh4, which localize to endosome and vacuole membranes. This study shows that Snc1 is trafficked between the endosomal system and the Golgi apparatus via multiple pathways and provides evidence for protein quality control surveillance of a SNARE protein in the endo-vacuolar system.
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spelling pubmed-67277572019-09-16 Retrograde trafficking and quality control of yeast synaptobrevin, Snc1, are conferred by its transmembrane domain Ma, Mengxiao Burd, Christopher G. Mol Biol Cell Articles Synaptobrevin/vesicle-associated membrane protein 2 (VAMP2) is an essential soluble N-ethyl maleimide–sensitive factor attachment protein receptor (SNARE) protein that has been extensively studied in its role in synaptic vesicle fusion. However, sorting and trafficking of VAMP2 within the endosomal system is not well understood. Here, we use the yeast VAMP2 homologue Snc1 to investigate the pathways and signals required for endocytic trafficking. We identify two genetically distinct retrieval pathways from the endosomal system: a plasma membrane recycling pathway that requires the Rcy1 F-box protein and a retrograde pathway originating from the multivesicular/prevacuole endosome dependent on the Snx4-Atg20 sorting nexin complex. Lysine residues within the transmembrane domain of Snc1 are necessary for presentation of a Snx4-Atg20–dependent sorting signal located within its juxtamembrane region. Mutations of the transmembrane lysine residues ablate retrograde sorting and subject Snc1 to quality control via sorting into the degradative multivesicular endosome pathway. Degradative sorting requires lysine residues in the juxtamembrane region of Snc1 and is mediated by the Rsp5 ubiquitin ligase and its transmembrane adapters, Ear1 and Ssh4, which localize to endosome and vacuole membranes. This study shows that Snc1 is trafficked between the endosomal system and the Golgi apparatus via multiple pathways and provides evidence for protein quality control surveillance of a SNARE protein in the endo-vacuolar system. The American Society for Cell Biology 2019-07-01 /pmc/articles/PMC6727757/ /pubmed/31067149 http://dx.doi.org/10.1091/mbc.E19-02-0117 Text en © 2019 Ma and Burd. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. http://creativecommons.org/licenses/by-nc-sa/3.0 This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.
spellingShingle Articles
Ma, Mengxiao
Burd, Christopher G.
Retrograde trafficking and quality control of yeast synaptobrevin, Snc1, are conferred by its transmembrane domain
title Retrograde trafficking and quality control of yeast synaptobrevin, Snc1, are conferred by its transmembrane domain
title_full Retrograde trafficking and quality control of yeast synaptobrevin, Snc1, are conferred by its transmembrane domain
title_fullStr Retrograde trafficking and quality control of yeast synaptobrevin, Snc1, are conferred by its transmembrane domain
title_full_unstemmed Retrograde trafficking and quality control of yeast synaptobrevin, Snc1, are conferred by its transmembrane domain
title_short Retrograde trafficking and quality control of yeast synaptobrevin, Snc1, are conferred by its transmembrane domain
title_sort retrograde trafficking and quality control of yeast synaptobrevin, snc1, are conferred by its transmembrane domain
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6727757/
https://www.ncbi.nlm.nih.gov/pubmed/31067149
http://dx.doi.org/10.1091/mbc.E19-02-0117
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