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Atg39 selectively captures inner nuclear membrane into lumenal vesicles for delivery to the autophagosome

View ORCID ProfileSunandini Chandra, View ORCID ProfilePhilip J. Mannino, View ORCID ProfileDavid J. Thaller, View ORCID ProfileNicholas R. Ader, View ORCID ProfileMegan C. King, View ORCID ProfileThomas J. Melia, View ORCID ProfileC. Patrick Lusk
doi: https://doi.org/10.1101/2021.02.22.432332
Sunandini Chandra
1Department of Cell Biology, Yale School of Medicine, 295 Congress Ave, New Haven, CT, 06520
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Philip J. Mannino
1Department of Cell Biology, Yale School of Medicine, 295 Congress Ave, New Haven, CT, 06520
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David J. Thaller
1Department of Cell Biology, Yale School of Medicine, 295 Congress Ave, New Haven, CT, 06520
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Nicholas R. Ader
1Department of Cell Biology, Yale School of Medicine, 295 Congress Ave, New Haven, CT, 06520
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Megan C. King
1Department of Cell Biology, Yale School of Medicine, 295 Congress Ave, New Haven, CT, 06520
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Thomas J. Melia
1Department of Cell Biology, Yale School of Medicine, 295 Congress Ave, New Haven, CT, 06520
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  • For correspondence: patrick.lusk@yale.edu thomas.melia@yale.edu
C. Patrick Lusk
1Department of Cell Biology, Yale School of Medicine, 295 Congress Ave, New Haven, CT, 06520
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  • For correspondence: patrick.lusk@yale.edu thomas.melia@yale.edu
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Abstract

Mechanisms that turnover components of the nucleus and inner nuclear membrane (INM) remain to be fully defined. We explore how components of the INM are selected by a cytosolic autophagy apparatus through a transmembrane nuclear envelope-localized cargo adaptor, Atg39. A split-GFP reporter shows that Atg39 localizes to the outer nuclear membrane (ONM) and thus targets the INM across the nuclear envelope lumen. Consistent with this, sequence elements that confer both nuclear envelope localization and a membrane remodeling activity are mapped to the Atg39 lumenal domain; these lumenal motifs are required for the autophagy-mediated degradation of an integral INM protein. Interestingly, correlative light and electron tomography shows that the overexpression of Atg39 leads to the expansion of the ONM and the enclosure of a network of INM-derived vesicles in the nuclear envelope lumen. Thus, we propose an outside-in model of nucleophagy where INM is delivered into vesicles in the nuclear envelope lumen, which can be targeted by the autophagosome.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted February 22, 2021.
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Atg39 selectively captures inner nuclear membrane into lumenal vesicles for delivery to the autophagosome
Sunandini Chandra, Philip J. Mannino, David J. Thaller, Nicholas R. Ader, Megan C. King, Thomas J. Melia, C. Patrick Lusk
bioRxiv 2021.02.22.432332; doi: https://doi.org/10.1101/2021.02.22.432332
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Atg39 selectively captures inner nuclear membrane into lumenal vesicles for delivery to the autophagosome
Sunandini Chandra, Philip J. Mannino, David J. Thaller, Nicholas R. Ader, Megan C. King, Thomas J. Melia, C. Patrick Lusk
bioRxiv 2021.02.22.432332; doi: https://doi.org/10.1101/2021.02.22.432332

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