Ribosome quality control antagonizes the activation of the integrated stress response on colliding ribosomes

被引:105
作者
Yan, Liewei L. [1 ]
Zaher, Hani S. [1 ]
机构
[1] Washington Univ, Dept Biol, Campus Box 1137, St Louis, MO 63130 USA
基金
美国国家卫生研究院;
关键词
TRANSFER-RNA-BINDING; PROTEIN-KINASE GCN2; NUCLEOTIDE EXCHANGE FACTOR; TRANSLATION INITIATION; COMPREHENSIVE ANALYSIS; GENE-EXPRESSION; ACTIVE-ROLE; PHOSPHORYLATION; DOMAIN; EIF2-ALPHA;
D O I
10.1016/j.molcel.2020.11.033
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Stalling during translation triggers ribosome quality control (RQC) to maintain proteostasis. Recently, stalling has also been linked to the activation of integrated stress response (ISR) by Gcn2. How the two processes are coordinated is unclear. Here, we show that activation of RQC by Hel2 suppresses that of Gcn2. We further show that Hel2 and Gcn2 are activated by a similar set of agents that cause ribosome stalling, with maximal activation of Hel2 observed at a lower frequency of stalling. Interestingly, inactivation of one pathway was found to result in the overactivation of the other, suggesting that both are activated by the same signal of ribosome collisions. Notably, the processes do not appear to be in direct competition with each other; ISR prefers a vacant A site, whereas RQC displays no preference. Collectively, our findings provide important details about how multiple pathways that recognize stalled ribosomes coordinate to mount the appropriate response.
引用
收藏
页码:614 / 628.e4
页数:20
相关论文
共 82 条
[71]   Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells [J].
Vattem, KM ;
Wek, RC .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2004, 101 (31) :11269-11274
[72]   Overexpression of Eukaryotic Translation Elongation Factor 3 Impairs Gcn2 Protein Activation [J].
Visweswaraiah, Jyothsna ;
Lee, Su Jung ;
Hinnebusch, Alan G. ;
Sattlegger, Evelyn .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2012, 287 (45) :37757-37768
[73]   RSeQC: quality control of RNA-seq experiments [J].
Wang, Liguo ;
Wang, Shengqin ;
Li, Wei .
BIOINFORMATICS, 2012, 28 (16) :2184-2185
[74]  
WEK SA, 1995, MOL CELL BIOL, V15, P4497
[75]   Ribosome Collisions Trigger General Stress Responses to Regulate Cell Fate [J].
Wu, Colin Chih-Chien ;
Peterson, Amy ;
Zinshteyn, Boris ;
Regot, Sergi ;
Green, Rachel .
CELL, 2020, 182 (02) :404-+
[76]   High-Resolution Ribosome Profiling Defines Discrete Ribosome Elongation States and Translational Regulation during Cellular Stress [J].
Wu, Colin Chih-Chien ;
Zinshteyn, Boris ;
Wehner, Karen A. ;
Green, Rachel .
MOLECULAR CELL, 2019, 73 (05) :959-+
[77]   Oxidation and alkylation stresses activate ribosome-quality control [J].
Yan, Liewei L. ;
Simms, Carrie L. ;
McLoughlin, Fionn ;
Vierstra, Richard D. ;
Zaher, Hani S. .
NATURE COMMUNICATIONS, 2019, 10 (1)
[78]   How do cells cope with RNA damage and its consequences? [J].
Yan, Liewei L. ;
Zaher, Hani S. .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2019, 294 (41) :15158-15171
[79]   The GCN2-ATF4 pathway is critical for tumour cell survival and proliferation in response to nutrient deprivation [J].
Ye, Jiangbin ;
Kumanova, Monika ;
Hart, Lori S. ;
Sloane, Kelly ;
Zhang, Haiyan ;
De Panis, Diego N. ;
Bobrovnikova-Marjon, Ekaterina ;
Diehl, J. Alan ;
Ron, David ;
Koumenis, Constantinos .
EMBO JOURNAL, 2010, 29 (12) :2082-2096
[80]   Position-dependent effects of regioisomeric methylated adenine and guanine ribonucleosides on translation [J].
You, Changjun ;
Dai, Xiaoxia ;
Wang, Yinsheng .
NUCLEIC ACIDS RESEARCH, 2017, 45 (15) :9059-9067