Widespread co-translational RNA decay reveals ribosome dynamics

Cell

Volumn 161, Issue 6, 2015, Pages 1400-1412

  Pelechano, Vicent ^a   Wei, Wu ^b   Steinmetz, Lars M ^a,b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RIBONUCLEASE; RNY1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSFER RNA;

ARTICLE; GENETIC CONSERVATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHOSPHORYLATION; PRIORITY JOURNAL; RIBOSOME; RNA DEGRADATION; RNA SEQUENCE; RNA TRANSCRIPTION; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS; CYTOLOGY; GENETIC ASSOCIATION; GENETICS; METABOLISM; PROTEIN SYNTHESIS; RNA STABILITY; SCHIZOSACCHAROMYCES;

GENOME-WIDE ASSOCIATION STUDY; OXIDATIVE STRESS; PEPTIDE CHAIN TERMINATION, TRANSLATIONAL; PROTEIN BIOSYNTHESIS; RIBONUCLEASES; RIBOSOMES; RNA STABILITY; RNA, MESSENGER; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES;

EID: 84930682682     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.05.008     Document Type: Article

References (50)

1. Addo-Quaye, C., Eshoo, T.W., Bartel, D.P., and Axtell, M.J. (2008). Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr. Biol. 18, 758-762.
2. Anderson, J.S., and Parker, R.P. (1998). The 3′ to 5′ degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3′ to 5′ exonucleases of the exosome complex. EMBO J. 17, 1497-1506.
3. Arava, Y., Wang, Y., Storey, J.D., Liu, C.L., Brown, P.O., and Herschlag, D. (2003). Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 100, 3889-3894.
4. Arava, Y., Boas, F.E., Brown, P.O., and Herschlag, D. (2005). Dissecting eukaryotic translation and its control by ribosome density mapping. Nucleic Acids Res. 33, 2421-2432.
5. Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W., and Noble, W.S. (2009). MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202-W208.
6. Bentele, K., Saffert, P., Rauscher, R., Ignatova, Z., and Blüthgen, N. (2013). Efficient translation initiation dictates codon usage at gene start. Mol. Syst. Biol. 9, 675.
7. Brar, G.A., Yassour, M., Friedman, N., Regev, A., Ingolia, N.T., and Weissman, J.S. (2012). High-resolution view of the yeast meiotic program revealed by ribosome profiling. Science 335, 552-557.
8. Decker, C.J., and Parker, R. (2012). P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harb. Perspect. Biol. 4, a012286.
9. Ding, Y., Tang, Y., Kwok, C.K., Zhang, Y., Bevilacqua, P.C., and Assmann, S.M. (2014). In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features. Nature 505, 696-700.
10. Gasch, A.P., Spellman, P.T., Kao, C.M., Carmel-Harel, O., Eisen, M.B., Storz, G., Botstein, D., and Brown, P.O. (2000). Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11, 4241-4257.
11. Gerashchenko, M.V., and Gladyshev, V.N. (2014). Translation inhibitors cause abnormalities in ribosome profiling experiments. Nucleic Acids Res. 42, e134.
12. Gerashchenko, M.V., Lobanov, A.V., and Gladyshev, V.N. (2012). Genome-wide ribosome profiling reveals complex translational regulation in response to oxidative stress. Proc. Natl. Acad. Sci. USA 109, 17394-17399.
13. German, M.A., Pillay, M., Jeong, D.H., Hetawal, A., Luo, S., Janardhanan, P., Kannan, V., Rymarquis, L.A., Nobuta, K., German, R., et al. (2008). Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat. Biotechnol. 26, 941-946.
14. Gregory, B.D., O'Malley, R.C., Lister, R., Urich, M.A., Tonti-Filippini, J., Chen, H., Millar, A.H., and Ecker, J.R. (2008). A link between RNA metabolism and silencing affecting Arabidopsis development. Dev. Cell 14, 854-866.
15. Guydosh, N.R., and Green, R. (2014). Dom34 rescues ribosomes in 3′ untranslated regions. Cell 156, 950-962.
16. Han, Y., Gao, X., Liu, B., Wan, J., Zhang, X., and Qian, S.B. (2014). Ribosome profiling reveals sequence-independent post-initiation pausing as a signature of translation. Cell Res. 24, 842-851.
17. Harigaya, Y., and Parker, R. (2012). Global analysis of mRNA decay intermediates in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 109, 11764-11769.
18. Hsu, C.L., and Stevens, A. (1993). Yeast cells lacking 5′3′ exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5′ cap structure. Mol. Cell. Biol. 13, 4826-4835.
19. Hu, W., Sweet, T.J., Chamnongpol, S., Baker, K.E., and Coller, J. (2009). Co-translational mRNA decay in Saccharomyces cerevisiae. Nature 461, 225-229.
20. Ingolia, N.T., Ghaemmaghami, S., Newman, J.R., and Weissman, J.S. (2009). Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324, 218-223.
21. Ingolia, N.T., Lareau, L.F., and Weissman, J.S. (2011). Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics ofmammalian proteomes. Cell 147, 789-802.
22. Ingolia, N.T., Brar, G.A., Rouskin, S., McGeachy, A.M., and Weissman, J.S. (2012). The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat. Protoc. 7, 1534-1550.
23. Ito, K., and Chiba, S. (2013). Arrest peptides: cis-acting modulators of translation. Annu. Rev. Biochem. 82, 171-202.
24. Kertesz, M., Wan, Y., Mazor, E., Rinn, J.L., Nutter, R.C., Chang, H.Y., and Segal, E. (2010). Genome-wide measurement of RNA secondary structure in yeast. Nature 467, 103-107.
25. Klopotowski, T., and Wiater, A. (1965). Synergism of aminotriazole and phosphate on the inhibition of yeast imidazole glycerol phosphate dehydratase. Arch. Biochem. Biophys. 112, 562-566.
26. Lareau, L.F., Hite, D.H., Hogan, G.J., and Brown, P.O. (2014). Distinct stages of the translation elongation cycle revealed by sequencing ribosome-protected mRNA fragments. eLife 3, e01257.
27. Lee, S., Liu, B., Lee, S., Huang, S.X., Shen, B., and Qian, S.B. (2012). Global mapping of translation initiation sites in mammalian cells at single-nucleotide resolution. Proc. Natl. Acad. Sci. USA 109, E2424-E2432.
28. Letzring, D.P., Dean, K.M., and Grayhack, E.J. (2010). Control of translation efficiency in yeast by codon-anticodon interactions. RNA 16, 2516-2528.
29. Li, G.W., Oh, E., and Weissman, J.S. (2012). The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 484, 538-541.
30. Mortimer, S.A., Kidwell, M.A., and Doudna, J.A. (2014). Insights into RNA structure and function from genome-wide studies. Nat. Rev. Genet. 15, 469-479.
31. Muhlrad, D., Decker, C.J., and Parker, R. (1994). Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5′-> 3′ digestion of the transcript. Genes Dev. 8, 855-866.
32. Parker, R. (2012). RNA degradation in Saccharomyces cerevisae. Genetics 191, 671-702.
33. Pelechano, V., Wei, W., and Steinmetz, L.M. (2013). Extensive transcriptional heterogeneity revealed by isoform profiling. Nature 497, 127-131.
34. Pelechano, V., Wei, W., Jakob, P., and Steinmetz, L.M. (2014). Genome-wide identification of transcript start and end sites by transcript isoform sequencing. Nat. Protoc. 9, 1740-1759.
35. Pestova, T.V., and Hellen, C.U. (2003). Translation elongation after assembly of ribosomes on the Cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA. Genes Dev. 17, 181-186.
36. Roy, B., and Jacobson, A. (2013). The intimate relationships of mRNA decay and translation. Trends Genet. 29, 691-699.
37. Rudra, D., and Warner, J.R. (2004). What better measure than ribosome synthesis? Genes Dev. 18, 2431-2436.
38. Schneider-Poetsch, T., Ju, J., Eyler, D.E., Dang, Y., Bhat, S., Merrick, W.C., Green, R., Shen, B., and Liu, J.O. (2010). Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nat. Chem. Biol. 6, 209-217.
39. Shah, P., Ding, Y., Niemczyk, M., Kudla, G., and Plotkin, J.B. (2013). Ratelimiting steps in yeast protein translation. Cell 153, 1589-1601.
40. Shenton, D., Smirnova, J.B., Selley, J.N., Carroll, K., Hubbard, S.J., Pavitt, G.D., Ashe, M.P., and Grant, C.M. (2006). Global translational responses to oxidative stress impact upon multiple levels of protein synthesis. J. Biol. Chem. 281, 29011-29021.
41. Stevens, A., and Maupin, M.K. (1987). A 5′-3′ exoribonuclease of Saccharomyces cerevisiae: size and novel substrate specificity. Arch. Biochem. Biophys. 252, 339-347.
42. Subramaniam, A.R., Zid, B.M., and O'Shea, E.K. (2014). An integrated approach reveals regulatory controls on bacterial translation elongation. Cell 159, 1200-1211.
43. Tarrant, D., and von der Haar, T. (2014). Synonymous codons, ribosome speed, and eukaryotic gene expression regulation. Cell. Mol. Life Sci. 71, 4195-4206.
44. Thompson, D.M., and Parker, R. (2009). The RNase Rny1p cleaves tRNAs and promotes cell death during oxidative stress in Saccharomyces cerevisiae. J. Cell Biol. 185, 43-50.
45. Thompson, D.M., Lu, C., Green, P.J., and Parker, R. (2008). tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 14, 2095-2103.
46. Tuck, A.C., and Tollervey, D. (2013). A transcriptome-wide atlas of RNP composition reveals diverse classes of mRNAs and lncRNAs. Cell 154, 996-1009.
47. Tuller, T., Carmi, A., Vestsigian, K., Navon, S., Dorfan, Y., Zaborske, J., Pan, T., Dahan, O., Furman, I., and Pilpel, Y. (2010). An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 141, 344-354.
48. Tuller, T., Veksler-Lublinsky, I., Gazit, N., Kupiec, M., Ruppin, E., and Ziv-Ukelson, M. (2011). Composite effects of gene determinants on the translation speed and density of ribosomes. Genome Biol. 12, R110.
49. Wilson, D.N., and Beckmann, R. (2011). The ribosomal tunnel as a functional environment for nascent polypeptide folding and translational stalling. Curr. Opin. Struct. Biol. 21, 274-282.
50. Yang, J.R., Chen, X., and Zhang, J. (2014). Codon-by-codon modulation of translational speed and accuracy via mRNA folding. PLoS Biol. 12, e1001910.