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Asymmetric inheritance of aggregated proteins and age reset in yeast are regulated by Vac17-dependent vacuolar functions

Asymmetric inheritance of aggregated proteins and age reset in yeast are regulated by Vac17-dependent vacuolar functions
Asymmetric inheritance of aggregated proteins and age reset in yeast are regulated by Vac17-dependent vacuolar functions
Age can be reset during mitosis in both yeast and stem cells to generate a young daughter cell from an aged and deteriorated one. This phenomenon requires asymmetry-generating genes (AGGs) that govern the asymmetrical inheritance of aggregated proteins. Using a genome-wide imaging screen to identify AGGs in Saccharomyces cerevisiae, we discovered a previously unknown role for endocytosis, vacuole fusion, and the myosin-dependent adaptor protein Vac17 in asymmetrical inheritance of misfolded proteins. Overproduction of Vac17 increases deposition of aggregates into cytoprotective vacuole-associated sites, counteracts age-related breakdown of endocytosis and vacuole integrity, and extends replicative lifespan. The link between damage asymmetry and vesicle trafficking can be explained by a direct interaction between aggregates and vesicles. We also show that the protein disaggregase Hsp104 interacts physically with endocytic vesicle-associated proteins, such as the dynamin-like protein, Vps1, which was also shown to be required for Vac17-dependent sequestration of protein aggregates. These data demonstrate that two physiognomies of aging-reduced endocytosis and protein aggregation-are interconnected and regulated by Vac17.
Dynamins/metabolism, Endocytosis/physiology, Protein Aggregates/physiology, Protein Transport/physiology, Receptors, Cell Surface/metabolism, Saccharomyces cerevisiae/metabolism, Saccharomyces cerevisiae Proteins/metabolism, Transport Vesicles/metabolism, Vacuoles/metabolism, Vesicular Transport Proteins/metabolism
2211-1247
826-38
Hill, Sandra Malmgren
9adee094-84b7-4c6a-a003-11ac8e6c2b45
Hao, Xinxin
8c494d27-4b95-4d23-b83f-28da1420ac43
Grönvall, Johan
e236dc26-0b31-4e36-acf8-0dc780a61c9f
Spikings-Nordby, Stephanie
da034187-c4b1-48f8-9987-fdca9a8f3f37
Widlund, Per O
72ae77f7-4843-43b5-8fbe-a2f15b7577f8
Amen, Triana
388dc540-e819-4d07-8f1e-ee0f3949a54b
Jörhov, Anna
d7b0ccbf-f625-4e9c-ae70-49c2f560f8fe
Josefson, Rebecca
f57ed03a-3352-426e-a370-9a8d6c9e24e5
Kaganovich, Daniel
ebb13f4e-e925-4aef-88e7-ddc25ef52d8f
Liu, Beidong
af49adb8-5e1a-4192-acbe-11819b01442c
Nyström, Thomas
4959c0fb-56e2-4385-a97e-dac7a969f95b
et al.
Hill, Sandra Malmgren
9adee094-84b7-4c6a-a003-11ac8e6c2b45
Hao, Xinxin
8c494d27-4b95-4d23-b83f-28da1420ac43
Grönvall, Johan
e236dc26-0b31-4e36-acf8-0dc780a61c9f
Spikings-Nordby, Stephanie
da034187-c4b1-48f8-9987-fdca9a8f3f37
Widlund, Per O
72ae77f7-4843-43b5-8fbe-a2f15b7577f8
Amen, Triana
388dc540-e819-4d07-8f1e-ee0f3949a54b
Jörhov, Anna
d7b0ccbf-f625-4e9c-ae70-49c2f560f8fe
Josefson, Rebecca
f57ed03a-3352-426e-a370-9a8d6c9e24e5
Kaganovich, Daniel
ebb13f4e-e925-4aef-88e7-ddc25ef52d8f
Liu, Beidong
af49adb8-5e1a-4192-acbe-11819b01442c
Nyström, Thomas
4959c0fb-56e2-4385-a97e-dac7a969f95b

Hill, Sandra Malmgren, Hao, Xinxin, Grönvall, Johan and Kaganovich, Daniel , et al. (2016) Asymmetric inheritance of aggregated proteins and age reset in yeast are regulated by Vac17-dependent vacuolar functions. Cell Reports, 16 (3), 826-38. (doi:10.1016/j.celrep.2016.06.016).

Record type: Article

Abstract

Age can be reset during mitosis in both yeast and stem cells to generate a young daughter cell from an aged and deteriorated one. This phenomenon requires asymmetry-generating genes (AGGs) that govern the asymmetrical inheritance of aggregated proteins. Using a genome-wide imaging screen to identify AGGs in Saccharomyces cerevisiae, we discovered a previously unknown role for endocytosis, vacuole fusion, and the myosin-dependent adaptor protein Vac17 in asymmetrical inheritance of misfolded proteins. Overproduction of Vac17 increases deposition of aggregates into cytoprotective vacuole-associated sites, counteracts age-related breakdown of endocytosis and vacuole integrity, and extends replicative lifespan. The link between damage asymmetry and vesicle trafficking can be explained by a direct interaction between aggregates and vesicles. We also show that the protein disaggregase Hsp104 interacts physically with endocytic vesicle-associated proteins, such as the dynamin-like protein, Vps1, which was also shown to be required for Vac17-dependent sequestration of protein aggregates. These data demonstrate that two physiognomies of aging-reduced endocytosis and protein aggregation-are interconnected and regulated by Vac17.

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More information

Published date: 19 July 2016
Additional Information: Copyright © 2016 The Author(s). Published by Elsevier Inc. All rights reserved.
Keywords: Dynamins/metabolism, Endocytosis/physiology, Protein Aggregates/physiology, Protein Transport/physiology, Receptors, Cell Surface/metabolism, Saccharomyces cerevisiae/metabolism, Saccharomyces cerevisiae Proteins/metabolism, Transport Vesicles/metabolism, Vacuoles/metabolism, Vesicular Transport Proteins/metabolism

Identifiers

Local EPrints ID: 475603
URI: http://eprints.soton.ac.uk/id/eprint/475603
ISSN: 2211-1247
PURE UUID: d48f8d22-912d-429e-bd95-69582c7fe137
ORCID for Triana Amen: ORCID iD orcid.org/0000-0003-4808-7806
ORCID for Daniel Kaganovich: ORCID iD orcid.org/0000-0003-2398-1596

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Date deposited: 22 Mar 2023 17:37
Last modified: 17 Mar 2024 04:22

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Contributors

Author: Sandra Malmgren Hill
Author: Xinxin Hao
Author: Johan Grönvall
Author: Stephanie Spikings-Nordby
Author: Per O Widlund
Author: Triana Amen ORCID iD
Author: Anna Jörhov
Author: Rebecca Josefson
Author: Daniel Kaganovich ORCID iD
Author: Beidong Liu
Author: Thomas Nyström
Corporate Author: et al.

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