Reactome | Ribosome-associated quality control

Ribosome-associated quality control

Stable Identifier

R-HSA-9948299

DOI

10.3180/R-HSA-9948299.2

Type

Pathway

Species

Homo sapiens

ReviewStatus

5/5

Locations in the PathwayBrowser

Expand all

General

SBML | | PDF

SVG | | PPTX | SBGN

Click the image above or here to open this pathway in the Pathway Browser

Features such as damaged nucleotides, strong secondary structure, presence of stretches of more than four uninterrupted AAA codons in a mRNA coding region (designated a no-go mRNA) or the absence of a stop codon in a mRNA (a non-stop mRNA) can cause a ribosome to stall during translation and the stalled ribosome can cause collisions with trailing ribosomes on the mRNA (reviewed in Joazeiro 2017, Eisenack and Trentini 2022, Filbeck et al. 2022, McGirr et al. 2025).
In cases in which the ribosome stalls internally on the mRNA and a 3' region of the mRNA protrudes from the ribosome, ZNF598, a ubiquitin E3 ligase that is the homolog of yeast HEL2, binds the ribosome (Garzia et al. 2017, Juszkiewicz and Hegde 2017, Sundaramoorthy et al. 2017) and catalyzes the lysine-63 (K63) linked ubiquitination of the 40S subunit ribosomal proteins eS10 (RPS10) at residues K138 and K139 and uS10 (RPS20) at residues K4 and K8 to initiate splitting of the 40S and 60S ribosomal subunits (Juszkiewicz and Hegde 2017, Sundaramoorthy et al. 2017, Garzia et al. 2017, Juszkiewicz et al. 2018, Narita et al. 2022, Miścicka et al. 2024, also inferred from yeast homologs in Matsuo et al. 2017, Sitron et al. 2017, Ikeuchi et al. 2019, reviewed in Ford et al. 2024). RACK1 then stabilizes the interface between the 40S subunits of the collided ribosomes to enable the ubiquitination of ribosomal proteins by ZNF598 (Sundaramoorthy et al. 2017). RACK1 is also required for the recruitment of EDF1 which has been proposed by structural studies to stabilize the collision interface through a conserved KKW motif and an alpha-helical segment that clamps the mRNA (Sinha et al. 2020). Additionally, EDF1 recruits the 4EHP-GIGYF2 complex to the collided ribosome to mediate translational repression of aberrant mRNAs (Sinha et al. 2020, Juszkiewicz et al. 2020), a mechanism which can also be initiated by ZNF598 (Hickey et al. 2020).
The ASCC2 subunit (Narita et al. 2022) of the ribosome quality control trigger complex (ASCC, ASC-1 complex, ASCC2:ASCC3:TRIP4, homologue of the RQT complex in yeast) binds K63-linked polyubiquitin conjugated to the 40S protein uS10 (Hashimoto et al. 2020, Juszkiewicz et al. 2020, Narita et al. 2022, and inferred from yeast homologs in Matsuo et al. 2023). The ASCC3 subunit of the RQT complex splits stalled 80S ribosomes with K63-polyubiquitinated uS10 into 60S and 40S subunits (Hashimoto et al. 2020, Juszkiewicz et al. 2020, Narita et al. 2022, Miścicka et al. 2024) apparently by exerting a pulling force on the mRNA (inferred from the yeast homolog Slh1 in Best et al. 2023). The peptidyl-tRNA remains bound in the 60S subunit, with the tRNA positioned in the P site. The problematic mRNA dissociates after splitting and is thought to be degraded at this time. In the case of collided yeast ribosomes, the mRNA is first endonucleolytically cleaved and the cleavage products are exonucleolytically degraded by XRN1 and the exosome (Ikeuchi et al. 2019).
Non-stop mRNAs result in ribosomal stalls proximal to the 3' end of the mRNA, which are resolved by a distinct pathway. In this case, a complex comprising PELO, a paralog of the ribosome release factor eRF1, and HBS1L:GTP, a paralog of the ribosome release factor eRF3:GTP, binds the stalled ribosome near the subunit interface and the mRNA entry site (Shao et al. 2013, and inferred from human PELO:HBS1L and rabbit ribosomes in Pisareva et al. 2011, inferred from yeast homologs DOM34:HBS1 in Shoemaker et al. 2010, Tsuboi et al. 2012, Guydosh and Green 2014, reviewed in Franckenberg et al. 2012). PELO:HBS1L preferentially acts on ribosomes that are bound to mRNAs that have fewer than 12 nucleotides extending 3' of the ribosomal P site (Pisareva et al. 2011).
HBS1L hydrolyzes GTP and dissociates from PELO and the ribosome, exposing a site on PELO to which ABCE1 binds. ABCE1 then hydrolyzes ATP to cause a conformational change that splits the ribosome into 40S and 60S subunits (Shao et al. 2013, Shao and Hegde 2014, and inferred from the yeast homologs DOM34:HBS1 and archaeal homologs in Becker et al. 2012, inferred from the yeast homologs in Saito et al. 2013). ABCE1 and possibly the mRNA remain bound to the 40S ribosomal subunit, while the peptidyl-tRNA remains bound to the 60S ribosomal subunit as in the ASCC-mediated rescue pathway (Becker et al. 2012, reviewed in Franckenberg et al. 2012).
At this stage of either pathway, the 40S subunit can be deubiquitinated [by OTUD3, USP21, or USP10] which may be necessary to license the 40S for further rounds of translation (Garshott et al. 2020, Meyer et al. 2020). In contrast, the 60S-peptidyl-tRNA complex requires additional steps to extract and destroy the nascent polypeptide before the 60S subunit can be recycled.
NEMF (the human homolog of yeast RQC2) binds the exposed peptidyl-tRNA of the isolated 60S ribosomal subunit produced by either the RQT complex or ABCE1 and transfers alanine residues from aminoacyl tRNAs to the C-terminus of the nascent peptide, a process termed Carboxy-terminal Alanine and Threonine tailing (CAT-tailing) after the alanine and threonine tails observed in yeast (Udagawa et al. 2021, Thrun et al. 2021, inferred from the yeast homolog RQC2 in Shen et al. 2015, Kostova et al. 2017, Osuna et al. 2017). Structures of CAT-tailing intermediates in yeast indicate that RQC2 positions an aminoacyl-tRNA in the A site of the 60S subunit and eIF5A enables peptidyl transfer (Shen et al. 2015, Tesina et al. 2023).
The alanine C-terminal tails are believed to push the nascent peptide through the exit tunnel of the 60S ribosomal subunit to expose lysine residues for K48-linked ubiquitination by Listerin (LTN1), however alanine tails can cause aggregation of nascent peptides (Udagawa et al. 2021, and inferred from yeast homologs in Yonashiro et al. 2016). The alanine tails can also act as degrons by binding the CRL2-KHDC10 ubiquitin E3 ligase complex (Thrun et al. 2021, Patil et al. 2023) or the RCHY1 (PIRH2) ubiquitin E3 ligase (Thrun et al. 2021, Patil et al. 2023, Wang et al. 2023) CRL2-KHDC10 and RCHY1 ubiquitinate the nascent peptide using K48 polyubiquitin linkages, targeting the nascent peptide for destruction by the 26S proteasome.
Listerin (LTN1, also called RKR1 in yeast), a ubiquitin E3 ligase, is also capable of catalyzing the K48-linked ubiquitination of the nascent peptide after NEMF recruits LTN1 to the 60S ribosomal subunit (Shao et al. 2015). The N-terminal region of LTN1 contacts the 60S ribosomal subunit and NEMF while the C-terminal region of LTN1 binds the 60S ribosomal subunit near the exit tunnel (Shao et al. 2015, inferred from yeast homologs in Lyumkis et al. 2014). TCF25 (the homolog of RQC1 in yeast) interacts with LTN1 (inferred from yeast homologs in Defenouillère et al. 2013).
LTN1 ubiquitinates exposed lysine residues on the nascent peptide after the residues have emerged from the exit tunnel of the 60S ribosomal subunit (Osuna et al. 2017, Kuroha et al. 2018, Abaeva et al. 2025, inferred from yeast homologs in Bengtson and Joazeiro 2010, Shao et al. 2013, Shao and Hegde 2014, reviewed in Mishra et al. 2021). TCF25, the human homolog of RQC1 in yeast, interacts with the RING domain of LTN1 to orient the ubiquitin substrate molecules to produce lysine-48 (K48) linkages in the polyubiquitin product (Kuroha et al. 2018, Abaeva et al. 2025).
A hexamer of VCP subunits plus a heterodimer of UFDL1 (UFD1) and NPLOC4 bind polyubiquitin that contains lysine-48 linkages (K48polyUb) and is conjugated to the nascent peptide emerging from the exit tunnel of the 60S ribosomal subunit (Tsuchiya et al. 2017, Sato et al. 2019, Williams et al. 2023, and inferred from CDC48, the yeast orthologue of VCP, in Brandman et al. 2012, Defenouillère et al. 2013, Verma et al. 2013). In yeast, the Npl4:Ufd1 heterodimer (homolog of NPLOC4:UFD1L) acts as an adapter that binds K48-linked polyubiquitin and inserts it into the pore of the VCP hexamer (inferred from rat p97 and Ufd1:Npl4 in Meyer et al. 2000, reviewed in Meyer and van den Boom 2023).
ANKZF1, which interacts with VCP, cleaves the C-terminal 3 nucleotides, CCA, of the tRNA in the peptidyl-tRNA bound to the 60S ribosomal subunit, yielding a free tRNA and the nascent peptide covalently bound to the CCA sequence (Verma et al. 2018, Yip et al. 2019, and inferred from the yeast homolog, VMS1, in Verma et al. 2018, Yip et al. 2019). In yeast, Arb1 (mammalian ABCF2) occupies the E-site of the collided ribosome, extending a domain towards the peptidyl-tRNA that may help position it for release by Vms1/ANKZF1 (SU et al. 2019).
The VCP hexamer then extracts the ubiquitinated nascent peptide from the 60S ribosomal subunit. Six subunits of VCP surround the substrate protein, which is located in the central pore of the hexamer. Hydrolysis of ATP by a subunit causes it to disengage from the hexamer. Release of ADP and binding of ATP causes the subunit to rebind the hexamer more proximally to the 60S ribosomal subunit (reviewed in Meyer and van den Boom 2023). The result is a ratcheting effect that withdraws the nascent peptide from the 60S subunit. The extracted nascent peptide remains bound to the ribosome-associated quality control complex (RQC complex, LTN1:NEMF:TCF25:VCP hexamer) which dissociates from the 60S ribosomal subunit and escorts the nascent peptide to the proteasome (inferred from yeast homologs in Defenouillère et al. 2017). The region of the nascent peptide that is unfolded by the VCP hexamer is able to enter the proteasome, resulting in degradation of the nascent peptide (inferred from the yeast homolog CDC48 in Olszewski et al. 2019). After removal of the ubiquitinated nascent peptide and tRNA, and mRNA, the 60S subunit is able to be re-used in translation. The 40 S subunit is deubiquitinated by OTUD3 and USP21.

Literature References

PubMed ID	Title	Journal	Year
32099016	Identification of a novel trigger complex that facilitates ribosome-associated quality control in mammalian cells Hashimoto, S, Sugiyama, T, Yamazaki, R, Nobuta, R, Inada, T	Sci Rep	2020
36736315	The Ufd1 cofactor determines the linkage specificity of polyubiquitin chain engagement by the AAA+ ATPase Cdc48 Williams, C, Dong, KC, Arkinson, C, Martin, A	Mol Cell	2023
20835226	Role of a ribosome-associated E3 ubiquitin ligase in protein quality control Bengtson, MH, Joazeiro, CA	Nature	2010
36302773	A distinct mammalian disome collision interface harbors K63-linked polyubiquitination of uS10 to trigger hRQT-mediated subunit dissociation Narita, M, Denk, T, Matsuo, Y, Sugiyama, T, Kikuguchi, C, Ito, S, Sato, N, Suzuki, T, Hashimoto, S, Machová, I, Tesina, P, Beckmann, R, Inada, T	Nat Commun	2022
25554787	Protein synthesis. Rqc2p and 60S ribosomal subunits mediate mRNA-independent elongation of nascent chains Shen, PS, Park, J, Qin, Y, Li, X, Parsawar, K, Larson, MH, Cox, J, Cheng, Y, Lambowitz, AM, Weissman, JS, Brandman, O, Frost, A	Science	2015
24581494	Dom34 rescues ribosomes in 3' untranslated regions Guydosh, NR, Green, R	Cell	2014
36825201	Targeting of client proteins to the VCP/p97/Cdc48 unfolding machine Meyer, H, van den Boom, J	Front Mol Biosci	2023
28715909	Ribosomal Stalling During Translation: Providing Substrates for Ribosome-Associated Protein Quality Control Joazeiro, CAP	Annu Rev Cell Dev Biol	2017
28223409	Asc1, Hel2, and Slh1 couple translation arrest to nascent chain degradation Sitron, CS, Park, JH, Brandman, O	RNA	2017
30293783	ZNF598 Is a Quality Control Sensor of Collided Ribosomes Juszkiewicz, S, Chandrasekaran, V, Lin, Z, Kraatz, S, Ramakrishnan, V, Hegde, RS	Mol Cell	2018
36804914	Molecular basis of eIF5A-dependent CAT tailing in eukaryotic ribosome-associated quality control Tesina, P, Ebine, S, Buschauer, R, Thoms, M, Matsuo, Y, Inada, T, Beckmann, R	Mol Cell	2023
28685749	The E3 ubiquitin ligase and RNA-binding protein ZNF598 orchestrates ribosome quality control of premature polyadenylated mRNAs Garzia, A, Jafarnejad, SM, Meyer, C, Chapat, C, Gogakos, T, Morozov, P, Amiri, M, Shapiro, M, Molina, H, Tuschl, T, Sonenberg, N	Nat Commun	2017
23178123	A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress Brandman, O, Stewart-Ornstein, J, Wong, D, Larson, A, Williams, CC, Li, GW, Zhou, S, King, D, Shen, PS, Weibezahn, J, Dunn, JG, Rouskin, S, Inada, T, Frost, A, Weissman, JS	Cell	2012
35452614	Ribosome-associated quality-control mechanisms from bacteria to humans Filbeck, S, Cerullo, F, Pfeffer, S, Joazeiro, CAP	Mol Cell	2022
28525741	In Vivo Ubiquitin Linkage-type Analysis Reveals that the Cdc48-Rad23/Dsk2 Axis Contributes to K48-Linked Chain Specificity of the Proteasome Tsuchiya, H, Ohtake, F, Arai, N, Kaiho, A, Yasuda, S, Tanaka, K, Saeki, Y	Mol Cell	2017
31011209	Mechanism for recycling tRNAs on stalled ribosomes Yip, MCJ, Keszei, AFA, Feng, Q, Chu, V, McKenna, MJ, Shao, S	Nat Struct Mol Biol	2019
32569528	Detection and Degradation of Stalled Nascent Chains via Ribosome-Associated Quality Control Sitron, CS, Brandman, O	Annu Rev Biochem	2020
37676773	Mechanism and evolutionary origins of alanine-tail C-degron recognition by E3 ligases Pirh2 and CRL2-KLHDC10 Patil, PR, Burroughs, AM, Misra, M, Cerullo, F, Costas-Insua, C, Hung, HC, Dikic, I, Aravind, L, Joazeiro, CAP	Cell Rep	2023
22503425	Dom34:hbs1 plays a general role in quality-control systems by dissociation of a stalled ribosome at the 3' end of aberrant mRNA Tsuboi, T, Kuroha, K, Kudo, K, Makino, S, Inoue, E, Kashima, I, Inada, T	Mol Cell	2012
38366554	Ribosomal collision is not a prerequisite for ZNF598-mediated ribosome ubiquitination and disassembly of ribosomal complexes by ASCC Miścicka, A, Bulakhov, AG, Kuroha, K, Zinoviev, A, Hellen, CUT, Pestova, TV	Nucleic Acids Res	2024
22358840	Structural basis of highly conserved ribosome recycling in eukaryotes and archaea Becker, T, Franckenberg, S, Wickles, S, Shoemaker, CJ, Anger, AM, Armache, JP, Sieber, H, Ungewickell, C, Berninghausen, O, Daberkow, I, Karcher, A, Thomm, M, Hopfner, KP, Green, R, Beckmann, R	Nature	2012
26943317	The Rqc2/Tae2 subunit of the ribosome-associated quality control (RQC) complex marks ribosome-stalled nascent polypeptide chains for aggregation Yonashiro, R, Tahara, EB, Bengtson, MH, Khokhrina, M, Lorenz, H, Chen, KC, Kigoshi-Tansho, Y, Savas, JN, Yates, JR, Kay, SA, Craig, EA, Mogk, A, Bukau, B, Joazeiro, CA	Elife	2016
37120596	Recognition of an Ala-rich C-degron by the E3 ligase Pirh2 Wang, X, Li, Y, Yan, X, Yang, Q, Zhang, B, Zhang, Y, Yuan, X, Jiang, C, Chen, D, Liu, Q, Liu, T, Mi, W, Yu, Y, Dong, C	Nat Commun	2023
30675527	The Cdc48 unfoldase prepares well-folded protein substrates for degradation by the 26S proteasome Olszewski, MM, Williams, C, Dong, KC, Martin, A	Commun Biol	2019
28065601	Initiation of Quality Control during Poly(A) Translation Requires Site-Specific Ribosome Ubiquitination Juszkiewicz, S, Hegde, RS	Mol Cell	2017
33406423	Failure to Degrade CAT-Tailed Proteins Disrupts Neuronal Morphogenesis and Cell Survival Udagawa, T, Seki, M, Okuyama, T, Adachi, S, Natsume, T, Noguchi, T, Matsuzawa, A, Inada, T	Cell Rep	2021
20947765	Dom34:Hbs1 promotes subunit dissociation and peptidyl-tRNA drop-off to initiate no-go decay Shoemaker, CJ, Eyler, DE, Green, R	Science	2010
23685075	Listerin-dependent nascent protein ubiquitination relies on ribosome subunit dissociation Shao, S, von der Malsburg, K, Hegde, RS	Mol Cell	2013
28751611	CAT-tailing as a fail-safe mechanism for efficient degradation of stalled nascent polypeptides Kostova, KK, Hickey, KL, Osuna, BA, Hussmann, JA, Frost, A, Weinberg, DE, Weissman, JS	Science	2017
28298488	The ribosome-bound quality control complex remains associated to aberrant peptides during their proteasomal targeting and interacts with Tom1 to limit protein aggregation Defenouillère, Q, Namane, A, Mouaikel, J, Jacquier, A, Fromont-Racine, M	Mol Biol Cell	2017
32579943	The ASC-1 Complex Disassembles Collided Ribosomes Juszkiewicz, S, Speldewinde, SH, Wan, L, Svejstrup, JQ, Hegde, RS	Mol Cell	2020
23667253	The Hbs1-Dom34 protein complex functions in non-stop mRNA decay in mammalian cells Saito, S, Hosoda, N, Hoshino, S	J Biol Chem	2013
30244831	Release of Ubiquitinated and Non-ubiquitinated Nascent Chains from Stalled Mammalian Ribosomal Complexes by ANKZF1 and Ptrh1 Kuroha, K, Zinoviev, A, Hellen, CUT, Pestova, TV	Mol Cell	2018
28132843	ZNF598 and RACK1 Regulate Mammalian Ribosome-Associated Quality Control Function by Mediating Regulatory 40S Ribosomal Ubiquitylation Sundaramoorthy, E, Leonard, M, Mak, R, Liao, J, Fulzele, A, Bennett, EJ	Mol Cell	2017
38949989	Dysregulated ribosome quality control in human diseases McGirr, T, Onar, O, Jafarnejad, SM	FEBS J	2025
32011234	Distinct regulatory ribosomal ubiquitylation events are reversible and hierarchically organized Garshott, DM, Sundaramoorthy, E, Leonard, M, Bennett, EJ	Elife	2020
25578875	Structure and assembly pathway of the ribosome quality control complex Shao, S, Brown, A, Santhanam, B, Hegde, RS	Mol Cell	2015
32657267	Ribosome collisions trigger cis-acting feedback inhibition of translation initiation Juszkiewicz, S, Slodkowicz, G, Lin, Z, Freire-Pritchett, P, Peak-Chew, SY, Hegde, RS	Elife	2020
39661518	Ubiquitin-dependent translation control mechanisms: Degradation and beyond Ford, PW, Narasimhan, M, Bennett, EJ	Cell Rep	2024
31981475	The G3BP1-Family-USP10 Deubiquitinase Complex Rescues Ubiquitinated 40S Subunits of Ribosomes Stalled in Translation from Lysosomal Degradation Meyer, C, Garzia, A, Morozov, P, Molina, H, Tuschl, T	Mol Cell	2020
36660423	Ending a bad start: Triggers and mechanisms of co-translational protein degradation Eisenack, TJ, Trentini, DB	Front Mol Biosci	2022
25132172	Reconstitution of a minimal ribosome-associated ubiquitination pathway with purified factors Shao, S, Hegde, RS	Mol Cell	2014
29632312	Vms1 and ANKZF1 peptidyl-tRNA hydrolases release nascent chains from stalled ribosomes Verma, R, Reichermeier, KM, Burroughs, AM, Oania, RS, Reitsma, JM, Aravind, L, Deshaies, RJ	Nature	2018
25349383	Structural basis for translational surveillance by the large ribosomal subunit-associated protein quality control complex Lyumkis, D, Oliveira dos Passos, D, Tahara, EB, Webb, K, Bennett, EJ, Vinterbo, S, Potter, CS, Carragher, B, Joazeiro, CA	Proc Natl Acad Sci U S A	2014
23479637	Cdc48-associated complex bound to 60S particles is required for the clearance of aberrant translation products Defenouillère, Q, Yao, Y, Mouaikel, J, Namane, A, Galopier, A, Decourty, L, Doyen, A, Malabat, C, Saveanu, C, Jacquier, A, Fromont-Racine, M	Proc Natl Acad Sci U S A	2013
34590243	LISTERIN E3 Ubiquitin Ligase and Ribosome-Associated Quality Control (RQC) Mechanism Mishra, R, Bansal, A, Mishra, A	Mol Neurobiol	2021
23031510	Structural view on recycling of archaeal and eukaryotic ribosomes after canonical termination and ribosome rescue Franckenberg, S, Becker, T, Beckmann, R	Curr Opin Struct Biol	2012
33909987	Convergence of mammalian RQC and C-end rule proteolytic pathways via alanine tailing Thrun, A, Garzia, A, Kigoshi-Tansho, Y, Patil, PR, Umbaugh, CS, Dallinger, T, Liu, J, Kreger, S, Patrizi, A, Cox, GA, Tuschl, T, Joazeiro, CAP	Mol Cell	2021
28718767	In vitro analysis of RQC activities provides insights into the mechanism and function of CAT tailing Osuna, BA, Howard, CJ, Kc, S, Frost, A, Weinberg, DE	Elife	2017
10811609	A complex of mammalian ufd1 and npl4 links the AAA-ATPase, p97, to ubiquitin and nuclear transport pathways Meyer, HH, Shorter, JG, Seemann, J, Pappin, D, Warren, G	EMBO J	2000
21448132	Dissociation by Pelota, Hbs1 and ABCE1 of mammalian vacant 80S ribosomes and stalled elongation complexes Pisareva, VP, Skabkin, MA, Hellen, CU, Pestova, TV, Pisarev, AV	EMBO J	2011
32744497	EDF1 coordinates cellular responses to ribosome collisions Sinha, NK, Ordureau, A, Best, K, Saba, JA, Zinshteyn, B, Sundaramoorthy, E, Fulzele, A, Garshott, DM, Denk, T, Thoms, M, Paulo, JA, Harper, JW, Bennett, EJ, Beckmann, R, Green, R	Elife	2020
40169231	The ribosome-associated quality control factor TCF25 imposes K48 specificity on Listerin-mediated ubiquitination of nascent chains by binding and specifically orienting the acceptor ubiquitin Abaeva, IS, Bulakhov, AG, Hellen, CUT, Pestova, TV	Genes Dev	2025
30609991	Collided ribosomes form a unique structural interface to induce Hel2-driven quality control pathways Ikeuchi, K, Tesina, P, Matsuo, Y, Sugiyama, T, Cheng, J, Saeki, Y, Tanaka, K, Becker, T, Beckmann, R, Inada, T	EMBO J	2019
36801861	Structural basis for clearing of ribosome collisions by the RQT complex Best, K, Ikeuchi, K, Kater, L, Best, D, Musial, J, Matsuo, Y, Berninghausen, O, Becker, T, Inada, T, Beckmann, R	Nat Commun	2023
28757607	Ubiquitination of stalled ribosome triggers ribosome-associated quality control Matsuo, Y, Ikeuchi, K, Saeki, Y, Iwasaki, S, Schmidt, C, Udagawa, T, Sato, F, Tsuchiya, H, Becker, T, Tanaka, K, Ingolia, NT, Beckmann, R, Inada, T	Nat Commun	2017
31836717	Structural insights into ubiquitin recognition and Ufd1 interaction of Npl4 Sato, Y, Tsuchiya, H, Yamagata, A, Okatsu, K, Tanaka, K, Saeki, Y, Fukai, S	Nat Commun	2019
31189955	Structure and function of Vms1 and Arb1 in RQC and mitochondrial proteome homeostasis Su, T, Izawa, T, Thoms, M, Yamashita, Y, Cheng, J, Berninghausen, O, Hartl, FU, Inada, T, Neupert, W, Beckmann, R	Nature	2019
36627279	Decoding of the ubiquitin code for clearance of colliding ribosomes by the RQT complex Matsuo, Y, Uchihashi, T, Inada, T	Nat Commun	2023
23358411	Cdc48/p97 promotes degradation of aberrant nascent polypeptides bound to the ribosome Verma, R, Oania, RS, Kolawa, NJ, Deshaies, RJ	Elife	2013
32726578	GIGYF2 and 4EHP Inhibit Translation Initiation of Defective Messenger RNAs to Assist Ribosome-Associated Quality Control Hickey, KL, Dickson, K, Cogan, JZ, Replogle, JM, Schoof, M, D'Orazio, KN, Sinha, NK, Hussmann, JA, Jost, M, Frost, A, Green, R, Weissman, JS, Kostova, KK	Mol Cell	2020