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Research Article
Vacuolar protein Tag1 and Atg1–Atg13 regulate autophagy termination during persistent starvation in S. cerevisiae
Shintaro Kira, Masafumi Noguchi, Yasuhiro Araki, Yu Oikawa, Tamotsu Yoshimori, Aiko Miyahara, Takeshi Noda
Journal of Cell Science 2021 134: jcs253682 doi: 10.1242/jcs.253682 Published 26 February 2021
Shintaro Kira
1Center for Frontier Oral Science, Graduate School of Dentistry, Osaka University, Yamadaoka 1-8, Suita, Osaka 565-0871, Japan
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Masafumi Noguchi
2Department of Oral Frontier Biology, Graduate School of Frontier Biosciences, Osaka University, Yamadaoka 1-8, Suita, Osaka 565-0871, Japan
3Laboratory of Intracellular Membrane Dynamics, Graduate School of Frontier Biosciences, Osaka University, Yamadaoka 2-2, Suita, Osaka 565-0871, Japan
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  • ORCID record for Masafumi Noguchi
Yasuhiro Araki
1Center for Frontier Oral Science, Graduate School of Dentistry, Osaka University, Yamadaoka 1-8, Suita, Osaka 565-0871, Japan
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Yu Oikawa
4Research Center of Cell Biology, Institute of Innovative Research, Tokyo Institute of Technology, Nagatsuta 4259, Yokohama, Kanagawa 226-8503, Japan
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Tamotsu Yoshimori
3Laboratory of Intracellular Membrane Dynamics, Graduate School of Frontier Biosciences, Osaka University, Yamadaoka 2-2, Suita, Osaka 565-0871, Japan
5Department of Genetics, Graduate School of Medicine, Osaka University, Yamadaoka 2-2, Suita, Osaka 565-0871, Japan
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Aiko Miyahara
2Department of Oral Frontier Biology, Graduate School of Frontier Biosciences, Osaka University, Yamadaoka 1-8, Suita, Osaka 565-0871, Japan
5Department of Genetics, Graduate School of Medicine, Osaka University, Yamadaoka 2-2, Suita, Osaka 565-0871, Japan
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Takeshi Noda
1Center for Frontier Oral Science, Graduate School of Dentistry, Osaka University, Yamadaoka 1-8, Suita, Osaka 565-0871, Japan
2Department of Oral Frontier Biology, Graduate School of Frontier Biosciences, Osaka University, Yamadaoka 1-8, Suita, Osaka 565-0871, Japan
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  • For correspondence: takenoda@dent.osaka-u.ac.jp

Handling Editor: Jennifer Lippincott-Schwartz

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ABSTRACT

Under starvation conditions, cells degrade their own components via autophagy in order to provide sufficient nutrients to ensure their survival. However, even if starvation persists, the cell is not completely degraded through autophagy, implying the existence of some kind of termination mechanism. In the yeast Saccharomyces cerevisiae, autophagy is terminated after 10–12 h of nitrogen starvation. In this study, we found that termination is mediated by re-phosphorylation of Atg13 by the Atg1 protein kinase, which is also affected by PP2C phosphatases, and the eventual dispersion of the pre-autophagosomal structure, also known as the phagophore assembly site (PAS). In a genetic screen, we identified an uncharacterized vacuolar membrane protein, Tag1, as a factor responsible for the termination of autophagy. Re-phosphorylation of Atg13 and eventual PAS dispersal were defective in the Δtag1 mutant. The vacuolar luminal domain of Tag1 and autophagic progression are important for the behaviors of Tag1. Together, our findings reveal the mechanism and factors responsible for termination of autophagy in yeast.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: S.K., T.N.; Methodology: Y.A.; Validation: Y.A.; Formal analysis: S.K.; Investigation: S.K., M.N., Y.O., A.M.; Resources: Y.A., T.Y.; Data curation: S.K., Y.O.; Writing - original draft: S.K.; Writing - review & editing: T.N.; Visualization: S.K.; Supervision: T.N.; Project administration: T.N.; Funding acquisition: T.N.

  • Funding

    This research was supported by the Japan Society for the Promotion of Science (grant number 16K18539 to S.K.) and the Ministry of Education, Culture, Sports, Science and Technology of Japan (grant numbers 16H01202 and 20H05326 to T.N.).

  • Supplementary information

    Supplementary information available online at https://jcs.biologists.org/lookup/doi/10.1242/jcs.253682.supplemental

  • Received September 2, 2020.
  • Accepted January 19, 2021.
  • © 2021. Published by The Company of Biologists Ltd
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Keywords

  • Tag1
  • Atg1
  • Atg13
  • PP2C phosphatase
  • Microautophagy
  • Autophagy
  • Yeast

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Research Article
Vacuolar protein Tag1 and Atg1–Atg13 regulate autophagy termination during persistent starvation in S. cerevisiae
Shintaro Kira, Masafumi Noguchi, Yasuhiro Araki, Yu Oikawa, Tamotsu Yoshimori, Aiko Miyahara, Takeshi Noda
Journal of Cell Science 2021 134: jcs253682 doi: 10.1242/jcs.253682 Published 26 February 2021
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Research Article
Vacuolar protein Tag1 and Atg1–Atg13 regulate autophagy termination during persistent starvation in S. cerevisiae
Shintaro Kira, Masafumi Noguchi, Yasuhiro Araki, Yu Oikawa, Tamotsu Yoshimori, Aiko Miyahara, Takeshi Noda
Journal of Cell Science 2021 134: jcs253682 doi: 10.1242/jcs.253682 Published 26 February 2021

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