Initiation of Quality Control during Poly(A) Translation Requires Site-Specific Ribosome Ubiquitination

Molecular Cell

Volumn 65, Issue 4, 2017, Pages 743-750.e4

  Juszkiewicz, Szymon ^a   Hegde, Ramanujan S ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

nonstop mRNA; poly(A); protein quality control; ribosome stalling; translation; ubiquitination

Indexed keywords

POLYADENYLIC ACID; POLYLYSINE; UBIQUITIN LIGASE ZNF598; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; MESSENGER RNA; RIBOSOME PROTEIN; UBIQUITIN; ZNF598 PROTEIN, HUMAN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; MAMMAL CELL; NONHUMAN; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN TARGETING; QUALITY CONTROL; RIBOSOME; SOLUBILITY; TRANSLATION INITIATION; UBIQUITINATION; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MUTATION; PROTEIN SYNTHESIS; RNA INTERFERENCE;

CARRIER PROTEINS; HEK293 CELLS; HUMANS; MUTATION; PROTEIN BIOSYNTHESIS; PROTEOLYSIS; RIBOSOMAL PROTEINS; RIBOSOMES; RNA INTERFERENCE; RNA, MESSENGER; TRANSFECTION; UBIQUITIN; UBIQUITINATION;

EID: 85008439822     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.11.039     Document Type: Article

References (37)

1. Arthur, L., Pavlovic-Djuranovic, S., Smith-Koutmou, K., Green, R., Szczesny, P., Djuranovic, S., Translational control by lysine-encoding A-rich sequences. Sci. Adv., 1, 2015, e1500154.
2. Bengtson, M.H., Joazeiro, C.A., Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 467 (2010), 470–473.
3. Brandman, O., Hegde, R.S., Ribosome-associated protein quality control. Nat. Struct. Mol. Biol. 23 (2016), 7–15.
4. Brandman, O., Stewart-Ornstein, J., Wong, D., Larson, A., Williams, C.C., Li, G.-W., Zhou, S., King, D., Shen, P.S., Weibezahn, J., et al. A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress. Cell 151 (2012), 1042–1054.
5. Chakrabarti, O., Hegde, R.S., Functional depletion of mahogunin by cytosolically exposed prion protein contributes to neurodegeneration. Cell 137 (2009), 1136–1147.
6. Chiabudini, M., Tais, A., Zhang, Y., Hayashi, S., Wölfle, T., Fitzke, E., Rospert, S., Release factor eRF3 mediates premature translation termination on polylysine-stalled ribosomes in Saccharomyces cerevisiae. Mol. Cell. Biol. 34 (2014), 4062–4076.
7. Defenouillère, Q., Yao, Y., Mouaikel, J., Namane, A., Galopier, A., Decourty, L., Doyen, A., Malabat, C., Saveanu, C., Jacquier, A., et al. Cdc48-associated complex bound to 60S particles is required for the clearance of aberrant translation products. Proc. Natl. Acad. Sci. USA 110 (2013), 5046–5051.
8. Doma, M.K., Parker, R., Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 440 (2006), 561–564.
9. Flicek, P., Amode, M.R., Barrell, D., Beal, K., Billis, K., Brent, S., Carvalho-Silva, D., Clapham, P., Coates, G., Fitzgerald, S., et al. Ensembl 2014. Nucleic Acids Res. 42 (2014), D749–D755.
10. Higgins, R., Gendron, J.M., Rising, L., Mak, R., Webb, K., Kaiser, S.E., Zuzow, N., Riviere, P., Yang, B., Fenech, E., et al. The unfolded protein response triggers site-specific regulatory ubiquitylation of 40S ribosomal proteins. Mol. Cell 59 (2015), 35–49.
11. Ito-Harashima, S., Kuroha, K., Tatematsu, T., Inada, T., Translation of the poly(A) tail plays crucial roles in nonstop mRNA surveillance via translation repression and protein destabilization by proteasome in yeast. Genes Dev. 21 (2007), 519–524.
12. Kaida, D., Berg, M.G., Younis, I., Kasim, M., Singh, L.N., Wan, L., Dreyfuss, G., U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 468 (2010), 664–668.
13. Koutmou, K.S., Schuller, A.P., Brunelle, J.L., Radhakrishnan, A., Djuranovic, S., Green, R., Ribosomes slide on lysine-encoding homopolymeric A stretches. eLife, 4, 2015, 4.
14. Kuroha, K., Akamatsu, M., Dimitrova, L., Ito, T., Kato, Y., Shirahige, K., Inada, T., Receptor for activated C kinase 1 stimulates nascent polypeptide-dependent translation arrest. EMBO Rep. 11 (2010), 956–961.
15. Kwon, I., Xiang, S., Kato, M., Wu, L., Theodoropoulos, P., Wang, T., Kim, J., Yun, J., Xie, Y., McKnight, S.L., Poly-dipeptides encoded by the C9orf72 repeats bind nucleoli, impede RNA biogenesis, and kill cells. Science 345 (2014), 1139–1145.
16. Letzring, D.P., Wolf, A.S., Brule, C.E., Grayhack, E.J., Translation of CGA codon repeats in yeast involves quality control components and ribosomal protein L1. RNA 19 (2013), 1208–1217.
17. Lin, Y.J., Huang, L.H., Huang, C.T., Enhancement of heterologous gene expression in Flammulina velutipes using polycistronic vectors containing a viral 2A cleavage sequence. PLoS ONE, 8, 2013, e59099.
18. Lu, J., Deutsch, C., Electrostatics in the ribosomal tunnel modulate chain elongation rates. J. Mol. Biol. 384 (2008), 73–86.
19. Lyumkis, D., Oliveira dos Passos, D., Tahara, E.B., Webb, K., Bennett, E.J., Vinterbo, S., Potter, C.S., Carragher, B., Joazeiro, C.A.P., Structural basis for translational surveillance by the large ribosomal subunit-associated protein quality control complex. Proc. Natl. Acad. Sci. USA 111 (2014), 15981–15986.
20. Mizielinska, S., Grönke, S., Niccoli, T., Ridler, C.E., Clayton, E.L., Devoy, A., Moens, T., Norona, F.E., Woollacott, I.O.C., Pietrzyk, J., et al. C9orf72 repeat expansions cause neurodegeneration in Drosophila through arginine-rich proteins. Science 345 (2014), 1192–1194.
21. Pisareva, V.P., Skabkin, M.A., Hellen, C.U.T., Pestova, T.V., Pisarev, A.V., Dissociation by Pelota, Hbs1 and ABCE1 of mammalian vacant 80S ribosomes and stalled elongation complexes. EMBO J. 30 (2011), 1804–1817.
22. Presnyak, V., Alhusaini, N., Chen, Y.H., Martin, S., Morris, N., Kline, N., Olson, S., Weinberg, D., Baker, K.E., Graveley, B.R., Coller, J., Codon optimality is a major determinant of mRNA stability. Cell 160 (2015), 1111–1124.
23. Ran, F.A., Hsu, P.D., Wright, J., Agarwala, V., Scott, D.A., Zhang, F., Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8 (2013), 2281–2308.
24. Saito, K., Horikawa, W., Ito, K., Inhibiting K63 polyubiquitination abolishes no-go type stalled translation surveillance in Saccharomyces cerevisiae. PLoS Genet., 11, 2015, e1005197.
25. Shao, S., Hegde, R.S., Reconstitution of a minimal ribosome-associated ubiquitination pathway with purified factors. Mol. Cell 55 (2014), 880–890.
26. Shao, S., von der Malsburg, K., Hegde, R.S., Listerin-dependent nascent protein ubiquitination relies on ribosome subunit dissociation. Mol. Cell 50 (2013), 637–648.
27. Shao, S., Brown, A., Santhanam, B., Hegde, R.S., Structure and assembly pathway of the ribosome quality control complex. Mol. Cell 57 (2015), 433–444.
28. Shcherbik, N., Chernova, T.A., Chernoff, Y.O., Pestov, D.G., Distinct types of translation termination generate substrates for ribosome-associated quality control. Nucleic Acids Res. 44 (2016), 6840–6852.
29. Shen, P.S., Park, J., Qin, Y., Li, X., Parsawar, K., Larson, M.H., Cox, J., Cheng, Y., Lambowitz, A.M., Weissman, J.S., et al. Protein synthesis. Rqc2p and 60S ribosomal subunits mediate mRNA-independent elongation of nascent chains. Science 347 (2015), 75–78.
30. Shoemaker, C.J., Green, R., Kinetic analysis reveals the ordered coupling of translation termination and ribosome recycling in yeast. Proc. Natl. Acad. Sci. USA 108 (2011), E1392–E1398.
31. Shoemaker, C.J., Green, R., Translation drives mRNA quality control. Nat. Struct. Mol. Biol. 19 (2012), 594–601.
32. Shoemaker, C.J., Eyler, D.E., Green, R., Dom34:Hbs1 promotes subunit dissociation and peptidyl-tRNA drop-off to initiate no-go decay. Science 330 (2010), 369–372.
33. Subtelny, A.O., Eichhorn, S.W., Chen, G.R., Sive, H., Bartel, D.P., Poly(A)-tail profiling reveals an embryonic switch in translational control. Nature 508 (2014), 66–71.
34. Tsuboi, T., Kuroha, K., Kudo, K., Makino, S., Inoue, E., Kashima, I., Inada, T., Dom34:hbs1 plays a general role in quality-control systems by dissociation of a stalled ribosome at the 3′ end of aberrant mRNA. Mol. Cell 46 (2012), 518–529.
35. Verma, R., Oania, R.S., Kolawa, N.J., Deshaies, R.J., Cdc48/p97 promotes degradation of aberrant nascent polypeptides bound to the ribosome. eLife, 2, 2013, e00308.
36. Wang, F., Canadeo, L.A., Huibregtse, J.M., Ubiquitination of newly synthesized proteins at the ribosome. Biochimie 114 (2015), 127–133.
37. Yonashiro, R., Tahara, E.B., Bengtson, M.H., Khokhrina, M., Lorenz, H., Chen, K.C., Kigoshi-Tansho, Y., Savas, J.N., Yates, J.R., Kay, S.A., et al. The Rqc2/Tae2 subunit of the ribosome-associated quality control (RQC) complex marks ribosome-stalled nascent polypeptide chains for aggregation. eLife, 5, 2016, e11794.