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

被引:96
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
[11]   Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation [J].
Doma, MK ;
Parker, R .
NATURE, 2006, 440 (7083) :561-564
[12]   Uncharged tRNA activates GCN2 by displacing the protein kinase moiety from a bipartite tRNA-Binding domain [J].
Dong, JS ;
Qiu, HF ;
Garcia-Barrio, M ;
Anderson, J ;
Hinnebusch, AG .
MOLECULAR CELL, 2000, 6 (02) :269-279
[13]   The hybrid state of tRNA binding is an authentic translation elongation intermediate [J].
Dorner, S ;
Brunelle, JL ;
Sharma, D ;
Green, R .
NATURE STRUCTURAL & MOLECULAR BIOLOGY, 2006, 13 (03) :234-241
[14]   Eukaryotic Release Factor 3 Is Required for Multiple Turnovers of Peptide Release Catalysis by Eukaryotic Release Factor 1 [J].
Eyler, Daniel E. ;
Wehner, Karen A. ;
Green, Rachel .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2013, 288 (41) :29530-29538
[15]   EIF2AK4 mutations cause pulmonary veno-occlusive disease, a recessive form of pulmonary hypertension [J].
Eyries, Melanie ;
Montani, David ;
Girerd, Barbara ;
Perret, Claire ;
Leroy, Anne ;
Lonjou, Christine ;
Chelghoum, Nadjim ;
Coulet, Florence ;
Bonnet, Damien ;
Dorfmueller, Peter ;
Fadel, Elie ;
Sitbon, Olivier ;
Simonneau, Gerald ;
Tregouet, David-Alexandre ;
Humbert, Marc ;
Soubrier, Florent .
NATURE GENETICS, 2014, 46 (01) :65-+
[16]   Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish ability of human eRF1 to trigger peptidyl-tRNA hydrolysis [J].
Frolova, LY ;
Tsivkovskii, RY ;
Sivolobova, GF ;
Oparina, NY ;
Serpinsky, OI ;
Blinov, VM ;
Tatkov, SI ;
Kisselev, LL .
RNA, 1999, 5 (08) :1014-1020
[17]   Association of GCN1-GCN20 regulatory complex with the N-terminus of elF2α kinase GCN2 is required for GCN2 activation [J].
Garcia-Barrio, M ;
Dong, JS ;
Ufano, S ;
Hinnebusch, AG .
EMBO JOURNAL, 2000, 19 (08) :1887-1899
[18]   The E3 ubiquitin ligase and RNA-binding protein ZNF598 orchestrates ribosome quality control of premature polyadenylated mRNAs [J].
Garzia, Aitor ;
Jafarnejad, Seyed Mehdi ;
Meyer, Cindy ;
Chapat, Clement ;
Gogakos, Tasos ;
Morozov, Pavel ;
Amiri, Mehdi ;
Shapiro, Maayan ;
Molina, Henrik ;
Tuschl, Thomas ;
Sonenberg, Nahum .
NATURE COMMUNICATIONS, 2017, 8
[19]  
Gietz RD, 2002, METHOD ENZYMOL, V350, P87
[20]   Characterization of the minimal catalytic domain within eIF2B: the guanine-nucleotide exchange factor for translation initiation [J].
Gomez, E ;
Mohammad, SS ;
Pavitt, GD .
EMBO JOURNAL, 2002, 21 (19) :5292-5301