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ATG9 vesicles comprise the seed membrane of mammalian autophagosomes
As the autophagosome forms, its membrane surface area expands rapidly, while its volume is kept low. Protein-mediated transfer of lipids from another organelle to the autophagosome likely drives this expansion, but as these lipids are only introduced into the cytoplasmic-facing leaflet of the organe...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Rockefeller University Press
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10148236/ https://www.ncbi.nlm.nih.gov/pubmed/37115958 http://dx.doi.org/10.1083/jcb.202208088 |
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author | Olivas, Taryn J. Wu, Yumei Yu, Shenliang Luan, Lin Choi, Peter Guinn, Emily D. Nag, Shanta De Camilli, Pietro V. Gupta, Kallol Melia, Thomas J. |
author_facet | Olivas, Taryn J. Wu, Yumei Yu, Shenliang Luan, Lin Choi, Peter Guinn, Emily D. Nag, Shanta De Camilli, Pietro V. Gupta, Kallol Melia, Thomas J. |
author_sort | Olivas, Taryn J. |
collection | PubMed |
description | As the autophagosome forms, its membrane surface area expands rapidly, while its volume is kept low. Protein-mediated transfer of lipids from another organelle to the autophagosome likely drives this expansion, but as these lipids are only introduced into the cytoplasmic-facing leaflet of the organelle, full membrane growth also requires lipid scramblase activity. ATG9 harbors scramblase activity and is essential to autophagosome formation; however, whether ATG9 is integrated into mammalian autophagosomes remains unclear. Here we show that in the absence of lipid transport, ATG9 vesicles are already competent to collect proteins found on mature autophagosomes, including LC3-II. Further, we use styrene–maleic acid lipid particles to reveal the nanoscale organization of protein on LC3-II membranes; ATG9 and LC3-II are each fully integrated into expanding autophagosomes. The ratios of these two proteins at different stages of maturation demonstrate that ATG9 proteins are not continuously integrated, but rather are present on the seed vesicles only and become diluted in the expanding autophagosome membrane. |
format | Online Article Text |
id | pubmed-10148236 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Rockefeller University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-101482362023-10-28 ATG9 vesicles comprise the seed membrane of mammalian autophagosomes Olivas, Taryn J. Wu, Yumei Yu, Shenliang Luan, Lin Choi, Peter Guinn, Emily D. Nag, Shanta De Camilli, Pietro V. Gupta, Kallol Melia, Thomas J. J Cell Biol Article As the autophagosome forms, its membrane surface area expands rapidly, while its volume is kept low. Protein-mediated transfer of lipids from another organelle to the autophagosome likely drives this expansion, but as these lipids are only introduced into the cytoplasmic-facing leaflet of the organelle, full membrane growth also requires lipid scramblase activity. ATG9 harbors scramblase activity and is essential to autophagosome formation; however, whether ATG9 is integrated into mammalian autophagosomes remains unclear. Here we show that in the absence of lipid transport, ATG9 vesicles are already competent to collect proteins found on mature autophagosomes, including LC3-II. Further, we use styrene–maleic acid lipid particles to reveal the nanoscale organization of protein on LC3-II membranes; ATG9 and LC3-II are each fully integrated into expanding autophagosomes. The ratios of these two proteins at different stages of maturation demonstrate that ATG9 proteins are not continuously integrated, but rather are present on the seed vesicles only and become diluted in the expanding autophagosome membrane. Rockefeller University Press 2023-04-28 /pmc/articles/PMC10148236/ /pubmed/37115958 http://dx.doi.org/10.1083/jcb.202208088 Text en © 2023 Olivas et al. https://creativecommons.org/licenses/by-nc-sa/4.0/http://www.rupress.org/terms/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/). |
spellingShingle | Article Olivas, Taryn J. Wu, Yumei Yu, Shenliang Luan, Lin Choi, Peter Guinn, Emily D. Nag, Shanta De Camilli, Pietro V. Gupta, Kallol Melia, Thomas J. ATG9 vesicles comprise the seed membrane of mammalian autophagosomes |
title | ATG9 vesicles comprise the seed membrane of mammalian autophagosomes |
title_full | ATG9 vesicles comprise the seed membrane of mammalian autophagosomes |
title_fullStr | ATG9 vesicles comprise the seed membrane of mammalian autophagosomes |
title_full_unstemmed | ATG9 vesicles comprise the seed membrane of mammalian autophagosomes |
title_short | ATG9 vesicles comprise the seed membrane of mammalian autophagosomes |
title_sort | atg9 vesicles comprise the seed membrane of mammalian autophagosomes |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10148236/ https://www.ncbi.nlm.nih.gov/pubmed/37115958 http://dx.doi.org/10.1083/jcb.202208088 |
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