Increased ribosome density associated to positively charged residues is evident in ribosome profiling experiments performed in the absence of translation inhibitors

RNA Biology

Volumn 13, Issue 6, 2016, Pages 561-568

  Requião, Rodrigo D ^a   de Souza, Henrique José Araujo ^a   Rossetto, Silvana ^a   Domitrovic, Tatiana ^a   Palhano, Fernando L ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Cycloheximide; polyA sequences; polybasic sequences; ribosome profiling; ribosome translation

Indexed keywords

ANISOMYCIN; CYCLOHEXIMIDE; FUNGAL RNA; MESSENGER RNA; PROTEIN SYNTHESIS INHIBITOR;

AMINO ACID SEQUENCE; ARTICLE; CELL DENSITY; CODING; FUNGAL GENOME; NONHUMAN; RIBOSOME; RIBOSOME DENSITY; RNA ISOLATION; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; TRANSLATION INITIATION; GENETICS; METABOLISM; PROCEDURES; PROTEIN SYNTHESIS; SEQUENCE ANALYSIS;

PROTEIN BIOSYNTHESIS; PROTEIN SYNTHESIS INHIBITORS; RIBOSOMES; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, RNA;

EID: 84966708267     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.1080/15476286.2016.1172755     Document Type: Article

References (28)

1. J.W.Hershey, N.Sonenberg, M.B.Mathews. Principles of translational control: an overview. Cold Spring Harb Perspect Biol 2012; 4; PMID:23209153; http://dx.doi.org/10.1101/cshperspect.a011528
2. J.Lu, W.R.Kobertz, C.Deutsch. Mapping the electrostatic potential within the ribosomal exit tunnel. J Mol Biol 2007; 371:1378-91; PMID:17631312; http://dx.doi.org/10.1016/j.jmb.2007.06.038
3. J.Lu, C.Deutsch. Electrostatics in the ribosomal tunnel modulate chain elongation rates. J Mol Biol. 2008; 384:73-86; PMID:18822297; http://dx.doi.org/10.1016/j.jmb.2008.08.089
4. S.Ito-Harashima, K.Kuroha, T.Tatematsu, T.Inada. 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 2007; 21:519-24; PMID:17344413; http://dx.doi.org/10.1101/gad.1490207
5. L.N.Dimitrova, K.Kuroha, T.Tatematsu, T.Inada. Nascent peptide-dependent translation arrest leads to Not4p-mediated protein degradation by the proteasome. J Biol Chem 2009; 284:10343-52; PMID:19204001; http://dx.doi.org/10.1074/jbc.M808840200
6. O.Brandman, J.Stewart-Ornstein, D.Wong, A.Larson, C.C.Williams, G.W.Li, S.Zhou, D.King, P.S.Shen, J.Weibezahn, J.G.Dunn, S.Rouskin, T.Inada, A.Frost, J.S.Weissman. A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress. Cell 2012; 151:1042-54; PMID:23178123; http://dx.doi.org/10.1016/j.cell.2012.10.044
7. M.H.Bengtson, C.A.Joazeiro. Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 2010; 467:470-3; PMID:20835226; http://dx.doi.org/10.1038/nature09371
8. D.Lyumkis, D.Oliveira dos Passos, E.B.Tahara, K.Webb, E.J.Bennett, S.Vinterbo, C.S.Potter, B.Carragher, C.A.Joazeiro. Structural basis for translational surveillance by the large ribosomal subunit-associated protein quality control complex. Proc Natl Acad Sci USA 2014; 111:15981-6; PMID:25349383; http://dx.doi.org/10.1073/pnas.1413882111
9. P.S.Shen, J.Park, Y.Qin, X.Li, K.Parsawar, M.H.Larson, J.Cox, Y.Cheng, A.M.Lambowitz, J.S.Weissman, O.Brandman, A.Frost. Protein synthesis. Rqc2p and 60S ribosomal subunits mediate mRNA-independent elongation of nascent chains. Science 2015; 347:75-8; PMID:25554787; http://dx.doi.org/10.1126/science.1259724
10. N.T.Ingolia, G.A.Brar, S.Rouskin, A.M.McGeachy, J.S.Weissman. The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat Protoc 2012; 7:1534-50; PMID:22836135; http://dx.doi.org/10.1038/nprot.2012.086
11. N.T.Ingolia, S.Ghaemmaghami, J.R.Newman, J.S.Weissman. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 2009; 324:218-23; PMID:19213877; http://dx.doi.org/10.1126/science.1168978
12. C.A.Charneski, L.D.Hurst. Positively charged residues are the major determinants of ribosomal velocity. PLoS Biol 2013; 11:e1001508; PMID:23554576; http://dx.doi.org/10.1371/journal.pbio.1001508
13. C.G.Artieri, H.B.Fraser. Accounting for biases in riboprofiling data indicates a major role for proline in stalling translation. Genome Res 2014; 24:2011-21; PMID:25294246; http://dx.doi.org/10.1101/gr.175893.114
14. R.Sabi, T.Tuller. A comparative genomics study on the effect of individual amino acids on ribosome stalling. BMC Genomics 2015; 16 Suppl 10:S5; PMID:26449596; http://dx.doi.org/10.1186/1471-2164-16-S10-S5
15. L.F.Lareau, D.H.Hite, G.J.Hogan, P.O.Brown. Distinct stages of the translation elongation cycle revealed by sequencing ribosome-protected mRNA fragments. eLife 2014; 3:e01257; PMID:24842990; http://dx.doi.org/10.7554/eLife.01257
16. M.V.Gerashchenko, V.N.Gladyshev. Translation inhibitors cause abnormalities in ribosome profiling experiments. Nucleic Acids Res 2014; 42:e134; PMID:25056308; http://dx.doi.org/10.1093/nar/gku671
17. D.D.Nedialkova, S.A.Leidel. Optimization of codon translation rates via tRNA modifications maintains proteome integrity. Cell 2015; 161:1606-18; PMID:26052047; http://dx.doi.org/10.1016/j.cell.2015.05.022
18. C.J.McManus, G.E.May, P.Spealman, A.Shteyman. Ribosome profiling reveals post-transcriptional buffering of divergent gene expression in yeast. Genome Res 2014; 24:422-30; PMID:24318730; http://dx.doi.org/10.1101/gr.164996.113
19. C.Pop, S.Rouskin, N.T.Ingolia, L.Han, E.M.Phizicky, J.S.Weissman, D.Koller. Causal signals between codon bias, mRNA structure, and the efficiency of translation and elongation. Mol Syst Biol 2014; 10:770; PMID:25538139; http://dx.doi.org/10.15252/msb.20145524
20. D.V.Fedyukina, S.Cavagnero. Protein Folding at the Exit Tunnel. Annu Rev Biophys 2011; 40:337-59; PMID:21370971; http://dx.doi.org/10.1146/annurev-biophys-042910-155338
21. T.Tuller, A.Carmi, K.Vestsigian, S.Navon, Y.Dorfan, J.Zaborske, T.Pan, O.Dahan, I.Furman, Y.Pilpel. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 2010; 141:344-54.22; PMID:20403328; http://dx.doi.org/10.1016/j.cell.2010.03.031
22. D.P.Letzring, K.M.Dean, E.J.Grayhack. Control of translation efficiency in yeast by codon-anticodon interactions. RNA 2010; 16:2516-28; PMID:20971810; http://dx.doi.org/10.1261/rna.2411710
23. J.A.Hussmann, S.Patchett, A.Johnson, S.Sawyer, W.H.Press. Understanding biases in ribosome profiling experiments reveals signatures of translation dynamics in yeast. PLoS Genet 2015; 11:e1005732; PMID:26656907; http://dx.doi.org/10.1371/journal.pgen.1005732
24. N.T.Ingolia, L.F.Lareau, J.S.Weissman. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 2011; 147:789-802; PMID:22056041; http://dx.doi.org/10.1016/j.cell.2011.10.002
25. K.S.Koutmou, A.P.Schuller, J.L.Brunelle, A.Radhakrishnan, S.Djuranovic, R.Green. Ribosomes slide on lysine-encoding homopolymeric A stretches. eLife 2015; 4:e05534; PMID:25695637; http://dx.doi.org/10.7554/eLife.05534
26. L.Arthur, S.Pavlovic-Djuranovic, K.Smith-Koutmou, R.Green, P.Szczesny, S.Djuranovic. Translational control by lysine-encoding A-rich sequences. Sci Adv 2015; 1:e1500154; PMID:26322332; http://dx.doi.org/10.1126/sciadv.1500154
27. M.Chiabudini, A.Tais, Y.Zhang, S.Hayashi, T.Wölfle, E.Fitzke, S.Rospert. Release factor eRF3 mediates premature translation termination on polylysine-stalled ribosomes in Saccharomyces cerevisiae. Mol Cell Biol 2014; 34:4062-76; PMID:25154418; http://dx.doi.org/10.1128/MCB.00799-14
28. D.E.Weinberg, P.Shah, S.W.Eichhorn, J.A.Hussmann, J.B.Plotkin, D.P.Bartel. Improved ribosome-footprint and mRNA measurements provide insights into dynamics and regulation of yeast translation. Cell Rep 2016; 14:1787-99; PMID:26876183; http://dx.doi.org/10.1016/j.celrep.2016.01.043