The mechanism of isolation membrane formation in autophagy is receiving intensive study. We recently found that Atg9 translocates phospholipids across liposomal membranes and proposed that this functionality plays an essential role in the expansion of isolation membranes. The distribution of phosphatidylinositol 3-phosphate in both leaflets of yeast autophagosomal membranes supports this proposal, but if Atg9-mediated lipid transport is crucial, symmetrical distribution in autophagosomes should be found broadly for other phospholipids. To test this idea, we analyzed the distributions of phosphatidylcholine, phosphatidylserine, and phosphatidylinositol 4-phosphate by freeze-fracture electron microscopy. We found that all these phospholipids are distributed with comparable densities in the two leaflets of autophagosomes and autophagic bodies. Moreover, de novo–synthesized phosphatidylcholine is incorporated into autophagosomes preferentially and shows symmetrical distribution in autophagosomes within 30 min after synthesis, whereas this symmetrical distribution is compromised in yeast expressing an Atg9 mutant. These results indicate that transbilayer phospholipid movement that is mediated by Atg9 is involved in the biogenesis of autophagosomes.
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1 March 2021
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January 13 2021
Transmembrane phospholipid translocation mediated by Atg9 is involved in autophagosome formation
Minami Orii
,
1
Department of Anatomy and Molecular Cell Biology, Nagoya University Graduate School of Medicine, Nagoya, Japan
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Takuma Tsuji
,
2
Laboratory of Molecular Cell Biology, Research Institute for Diseases of Old Age, Juntendo University Graduate School of Medicine, Tokyo, Japan
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Yuta Ogasawara
,
Yuta Ogasawara
2
Laboratory of Molecular Cell Biology, Research Institute for Diseases of Old Age, Juntendo University Graduate School of Medicine, Tokyo, Japan
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Toyoshi Fujimoto
2
Laboratory of Molecular Cell Biology, Research Institute for Diseases of Old Age, Juntendo University Graduate School of Medicine, Tokyo, Japan
Correspondence to Toyoshi Fujimoto: t.fujimoto.xl@juntendo.ac.jp
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Minami Orii
1
Department of Anatomy and Molecular Cell Biology, Nagoya University Graduate School of Medicine, Nagoya, Japan
Takuma Tsuji
2
Laboratory of Molecular Cell Biology, Research Institute for Diseases of Old Age, Juntendo University Graduate School of Medicine, Tokyo, Japan
Yuta Ogasawara
2
Laboratory of Molecular Cell Biology, Research Institute for Diseases of Old Age, Juntendo University Graduate School of Medicine, Tokyo, Japan
Toyoshi Fujimoto
2
Laboratory of Molecular Cell Biology, Research Institute for Diseases of Old Age, Juntendo University Graduate School of Medicine, Tokyo, Japan
M. Orii’s present address is Department of Biochemistry, Showa University School of Medicine, Tokyo, Japan.
*
M. Orii and T. Tsuji contributed equally to this paper.
Correspondence to Toyoshi Fujimoto: t.fujimoto.xl@juntendo.ac.jp
Received:
September 28 2020
Revision Received:
December 14 2020
Accepted:
December 17 2020
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding:
Japan Society for the Promotion of Science
(15H05902, 18K15004, 19K07265, 20H05339)
© 2021 Orii et al.
2021
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/).
J Cell Biol (2021) 220 (3): e202009194.
Article history
Received:
September 28 2020
Revision Received:
December 14 2020
Accepted:
December 17 2020
Citation
Minami Orii, Takuma Tsuji, Yuta Ogasawara, Toyoshi Fujimoto; Transmembrane phospholipid translocation mediated by Atg9 is involved in autophagosome formation. J Cell Biol 1 March 2021; 220 (3): e202009194. doi: https://doi.org/10.1083/jcb.202009194
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