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Ribosomal protein S7 ubiquitination during ER stress in yeast is associated with selective mRNA translation and stress outcome

Yasuko Matsuki, Yoshitaka Matsuo, Yu Nakano, Shintaro Iwasaki, Hideyuki Yoko, Tsuyoshi Udagawa, Sihan Li, Yasushi Saeki, Tohru Yoshihisa, Keiji Tanaka, View ORCID ProfileNicholas T. Ingolia, Toshifumi Inada
doi: https://doi.org/10.1101/2020.09.24.311365
Yasuko Matsuki
1Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai 980-8578, Japan
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Yoshitaka Matsuo
1Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai 980-8578, Japan
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Yu Nakano
1Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai 980-8578, Japan
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Shintaro Iwasaki
2Department of Molecular and Cell Biology, University of California, Berkeley, CA94720, United States
3Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba 277-8561, Japan
4RNA Systems Biochemistry Laboratory, RIKEN Cluster for Pioneering Research, Wako, Saitama 351-0198, Japan
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Hideyuki Yoko
1Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai 980-8578, Japan
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Tsuyoshi Udagawa
1Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai 980-8578, Japan
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Sihan Li
1Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai 980-8578, Japan
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Yasushi Saeki
5Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan
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Tohru Yoshihisa
6Graduate School of Life Science, University of Hyogo, Hyogo 678-1297, Japan
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Keiji Tanaka
5Laboratory of Protein Metabolism, Tokyo Metropolitan Institute of Medical Science, Setagaya-ku, Tokyo 156-8506, Japan
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Nicholas T. Ingolia
2Department of Molecular and Cell Biology, University of California, Berkeley, CA94720, United States
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  • ORCID record for Nicholas T. Ingolia
Toshifumi Inada
1Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai 980-8578, Japan
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  • For correspondence: toshifumi.inada.a3@tohoku.ac.jp
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ABSTRACT

eIF2α phosphorylation-mediated translational regulation is crucial for global translation repression by various stresses, including the unfolded protein response (UPR). However, translational control during UPR has not been demonstrated in yeast. This study investigated ribosome ubiquitination-mediated translational controls during UPR. Tunicamycin-induced ER stress enhanced the levels of ubiquitination of the ribosomal proteins uS10, uS3 and eS7. Not4-mediated monoubiquitination of eS7A was required for resistance to tunicamycin, whereas E3 ligase Hel2-mediated ubiquitination of uS10 was not. Ribosome profiling showed that the monoubiquitination of eS7A was crucial for translational regulation, including the upregulation of the spliced form of HAC1 (HAC1i) mRNA and the downregulation of Histidine triad NucleoTide-binding 1 (HNT1) mRNA. Downregulation of the deubiquitinating enzyme complex Upb3-Bre5 increased the levels of ubiquitinated eS7A during UPR in an Ire1-independent manner. These findings suggest that the monoubiquitination of ribosomal protein eS7A plays a crucial role in translational controls during the ER stress response in yeast.

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 4.0 International license.
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Posted September 25, 2020.
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Ribosomal protein S7 ubiquitination during ER stress in yeast is associated with selective mRNA translation and stress outcome
Yasuko Matsuki, Yoshitaka Matsuo, Yu Nakano, Shintaro Iwasaki, Hideyuki Yoko, Tsuyoshi Udagawa, Sihan Li, Yasushi Saeki, Tohru Yoshihisa, Keiji Tanaka, Nicholas T. Ingolia, Toshifumi Inada
bioRxiv 2020.09.24.311365; doi: https://doi.org/10.1101/2020.09.24.311365
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Ribosomal protein S7 ubiquitination during ER stress in yeast is associated with selective mRNA translation and stress outcome
Yasuko Matsuki, Yoshitaka Matsuo, Yu Nakano, Shintaro Iwasaki, Hideyuki Yoko, Tsuyoshi Udagawa, Sihan Li, Yasushi Saeki, Tohru Yoshihisa, Keiji Tanaka, Nicholas T. Ingolia, Toshifumi Inada
bioRxiv 2020.09.24.311365; doi: https://doi.org/10.1101/2020.09.24.311365

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