Cellular quiescence is a nonproliferative state required for cell survival under stress and during development. In most quiescent cells, proliferation is stopped in a reversible state of low Cdk1 kinase activity; in many organisms, however, quiescent states with high-Cdk1 activity can also be established through still uncharacterized stress or developmental mechanisms. Here, we used a microfluidics approach coupled to phenotypic classification by machine learning to identify stress pathways associated with starvation-triggered high-Cdk1 quiescent states in Saccharomyces cerevisiae. We found that low- and high-Cdk1 quiescent states shared a core of stress-associated processes, such as autophagy, protein aggregation, and mitochondrial up-regulation, but differed in the nuclear accumulation of the stress transcription factors Xbp1, Gln3, and Sfp1. The decision between low- or high-Cdk1 quiescence was controlled by cell cycle–independent accumulation of Xbp1, which acted as a time-delayed integrator of the duration of stress stimuli. Our results show how cell cycle–independent stress-activated factors promote cellular quiescence outside G1/G0.
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3 January 2022
Article|
October 25 2021
Cell cycle–independent integration of stress signals by Xbp1 promotes Non-G1/G0 quiescence entry
Orlando Argüello-Miranda
,
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
2
Lyda Hill Department of Bioinformatics, University of Texas Southwestern Medical Center, Dallas, TX
Correspondence to Orlando Argüello-Miranda: orlando.arguellomiranda@utsouthwestern.edu
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Ashley J. Marchand,
Ashley J. Marchand
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
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Taylor Kennedy
,
Taylor Kennedy
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
3
School of Natural Sciences and Mathematics, University of Texas at Dallas, Richardson, TX
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Marielle A.X. Russo
,
Marielle A.X. Russo
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
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Jungsik Noh
Jungsik Noh
2
Lyda Hill Department of Bioinformatics, University of Texas Southwestern Medical Center, Dallas, TX
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1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
2
Lyda Hill Department of Bioinformatics, University of Texas Southwestern Medical Center, Dallas, TX
Ashley J. Marchand
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
Taylor Kennedy
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
3
School of Natural Sciences and Mathematics, University of Texas at Dallas, Richardson, TX
Marielle A.X. Russo
1
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX
Jungsik Noh
2
Lyda Hill Department of Bioinformatics, University of Texas Southwestern Medical Center, Dallas, TX
Correspondence to Orlando Argüello-Miranda: orlando.arguellomiranda@utsouthwestern.edu
O. Argüello-Miranda’s present address is Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC.
A preprint of this paper was posted in bioRxiv on March 24, 2021.
Received:
March 29 2021
Revision Received:
August 27 2021
Accepted:
October 05 2021
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding
Funder(s):
Cancer Prevention and Research Institute of Texas
- Award Id(s): RP150596,RR150058
Funder(s):
Welch Foundation
- Award Id(s): I-1919-20170325
Funder(s):
National Institute of General Medical Sciences
Funder(s):
National Institutes of Health
- Award Id(s): K99GM135487
© 2021 Argüello-Miranda 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 (2022) 221 (1): e202103171.
Article history
Received:
March 29 2021
Revision Received:
August 27 2021
Accepted:
October 05 2021
Connected Content
Commentary
Stressed-out yeast do not pass GO
Citation
Orlando Argüello-Miranda, Ashley J. Marchand, Taylor Kennedy, Marielle A.X. Russo, Jungsik Noh; Cell cycle–independent integration of stress signals by Xbp1 promotes Non-G1/G0 quiescence entry. J Cell Biol 3 January 2022; 221 (1): e202103171. doi: https://doi.org/10.1083/jcb.202103171
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