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ESCRT machinery mediates selective microautophagy of endoplasmic reticulum in yeast

ER‐phagy, the selective autophagy of endoplasmic reticulum (ER), safeguards organelle homeostasis by eliminating misfolded proteins and regulating ER size. ER‐phagy can occur by macroautophagic and microautophagic mechanisms. While dedicated machinery for macro‐ER‐phagy has been discovered, the mole...

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Autores principales: Schäfer, Jasmin A, Schessner, Julia P, Bircham, Peter W, Tsuji, Takuma, Funaya, Charlotta, Pajonk, Oliver, Schaeff, Katharina, Ruffini, Giulia, Papagiannidis, Dimitrios, Knop, Michael, Fujimoto, Toyoshi, Schuck, Sebastian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6960443/
https://www.ncbi.nlm.nih.gov/pubmed/31802527
http://dx.doi.org/10.15252/embj.2019102586
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author Schäfer, Jasmin A
Schessner, Julia P
Bircham, Peter W
Tsuji, Takuma
Funaya, Charlotta
Pajonk, Oliver
Schaeff, Katharina
Ruffini, Giulia
Papagiannidis, Dimitrios
Knop, Michael
Fujimoto, Toyoshi
Schuck, Sebastian
author_facet Schäfer, Jasmin A
Schessner, Julia P
Bircham, Peter W
Tsuji, Takuma
Funaya, Charlotta
Pajonk, Oliver
Schaeff, Katharina
Ruffini, Giulia
Papagiannidis, Dimitrios
Knop, Michael
Fujimoto, Toyoshi
Schuck, Sebastian
author_sort Schäfer, Jasmin A
collection PubMed
description ER‐phagy, the selective autophagy of endoplasmic reticulum (ER), safeguards organelle homeostasis by eliminating misfolded proteins and regulating ER size. ER‐phagy can occur by macroautophagic and microautophagic mechanisms. While dedicated machinery for macro‐ER‐phagy has been discovered, the molecules and mechanisms mediating micro‐ER‐phagy remain unknown. Here, we first show that micro‐ER‐phagy in yeast involves the conversion of stacked cisternal ER into multilamellar ER whorls during microautophagic uptake into lysosomes. Second, we identify the conserved Nem1‐Spo7 phosphatase complex and the ESCRT machinery as key components for micro‐ER‐phagy. Third, we demonstrate that macro‐ and micro‐ER‐phagy are parallel pathways with distinct molecular requirements. Finally, we provide evidence that the ESCRT machinery directly functions in scission of the lysosomal membrane to complete the microautophagic uptake of ER. These findings establish a framework for a mechanistic understanding of micro‐ER‐phagy and, thus, a comprehensive appreciation of the role of autophagy in ER homeostasis.
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spelling pubmed-69604432020-01-17 ESCRT machinery mediates selective microautophagy of endoplasmic reticulum in yeast Schäfer, Jasmin A Schessner, Julia P Bircham, Peter W Tsuji, Takuma Funaya, Charlotta Pajonk, Oliver Schaeff, Katharina Ruffini, Giulia Papagiannidis, Dimitrios Knop, Michael Fujimoto, Toyoshi Schuck, Sebastian EMBO J Articles ER‐phagy, the selective autophagy of endoplasmic reticulum (ER), safeguards organelle homeostasis by eliminating misfolded proteins and regulating ER size. ER‐phagy can occur by macroautophagic and microautophagic mechanisms. While dedicated machinery for macro‐ER‐phagy has been discovered, the molecules and mechanisms mediating micro‐ER‐phagy remain unknown. Here, we first show that micro‐ER‐phagy in yeast involves the conversion of stacked cisternal ER into multilamellar ER whorls during microautophagic uptake into lysosomes. Second, we identify the conserved Nem1‐Spo7 phosphatase complex and the ESCRT machinery as key components for micro‐ER‐phagy. Third, we demonstrate that macro‐ and micro‐ER‐phagy are parallel pathways with distinct molecular requirements. Finally, we provide evidence that the ESCRT machinery directly functions in scission of the lysosomal membrane to complete the microautophagic uptake of ER. These findings establish a framework for a mechanistic understanding of micro‐ER‐phagy and, thus, a comprehensive appreciation of the role of autophagy in ER homeostasis. John Wiley and Sons Inc. 2019-12-05 2020-01-15 /pmc/articles/PMC6960443/ /pubmed/31802527 http://dx.doi.org/10.15252/embj.2019102586 Text en © 2019 The Authors. Published under the terms of the CC BY NC ND 4.0 license This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Articles
Schäfer, Jasmin A
Schessner, Julia P
Bircham, Peter W
Tsuji, Takuma
Funaya, Charlotta
Pajonk, Oliver
Schaeff, Katharina
Ruffini, Giulia
Papagiannidis, Dimitrios
Knop, Michael
Fujimoto, Toyoshi
Schuck, Sebastian
ESCRT machinery mediates selective microautophagy of endoplasmic reticulum in yeast
title ESCRT machinery mediates selective microautophagy of endoplasmic reticulum in yeast
title_full ESCRT machinery mediates selective microautophagy of endoplasmic reticulum in yeast
title_fullStr ESCRT machinery mediates selective microautophagy of endoplasmic reticulum in yeast
title_full_unstemmed ESCRT machinery mediates selective microautophagy of endoplasmic reticulum in yeast
title_short ESCRT machinery mediates selective microautophagy of endoplasmic reticulum in yeast
title_sort escrt machinery mediates selective microautophagy of endoplasmic reticulum in yeast
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6960443/
https://www.ncbi.nlm.nih.gov/pubmed/31802527
http://dx.doi.org/10.15252/embj.2019102586
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