Local slowdown of translation by nonoptimal codons promotes nascent-chain recognition by SRP in vivo

Nature Structural and Molecular Biology

Volumn 21, Issue 12, 2014, Pages 1100-1105

  Pechmann, Sebastian ^a   Chartron, Justin W ^a   Frydman, Judith ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; POLYPEPTIDE; SIGNAL RECOGNITION PARTICLE; CODON; FUNGAL PROTEIN; PEPTIDE;

ARTICLE; BINDING SITE; CODON; DNA BINDING MOTIF; HYDROPHOBICITY; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; RIBOSOME; TRANSLATION REGULATION; FUNGUS; METABOLISM; PROTEIN SYNTHESIS;

CODON; FUNGAL PROTEINS; FUNGI; PEPTIDES; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; RIBOSOMES; SIGNAL RECOGNITION PARTICLE;

EID: 84925553022     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2919     Document Type: Article

References (57)

1. Kim, Y.E., Hipp, M.S., Bracher, A., Hayer-Hartl, M. & Hartl, F.U. Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 82, 323-355 (2013).
2. Spencer, P.S., Siller, E., Anderson, J.F. & Barral, J.M. Silent substitutions predictably alter translation elongation rates and protein folding efficiencies. J. Mol. Biol. 422, 328-335 (2012).
3. Xu, Y. et al. Non-optimal codon usage is a mechanism to achieve circadian clock conditionality. Nature 495, 116-120 (2013).
4. Dana, A. & Tuller, T. The effect of tRNA levels on decoding times of mRNA codons. Nucleic Acids Res. 42, 9171-9181 (2014).
5. Keenan, R.J., Freymann, D.M., Stroud, R.M. & Walter, P. The signal recognition particle. Annu. Rev. Biochem. 70, 755-775 (2001).
6. Akopian, D., Shen, K., Zhang, X. & Shan, S.-o. Signal recognition particle: an essential protein-targeting machine. Annu. Rev. Biochem. 82, 693-721 (2013).
7. Powers, E.T., Morimoto, R.I., Dillin, A., Kelly, J.W. & Balch, W.E. Biological and chemical approaches to diseases of proteostasis deficiency. Annu. Rev. Biochem. 78, 959-991 (2009).
8. Landry, S.J. & Gierasch, L.M. Recognition of nascent polypeptides for targeting and folding. Trends Biochem. Sci. 16, 159-163 (1991).
9. Halic, M. et al. Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature 427, 808-814 (2004).
10. Noriega, T.R. et al. Signal recognition particle-ribosome binding is sensitive to nascent chain length. J. Biol. Chem. 289, 19294-19305 (2014).
11. Ast, T., Cohen, G. & Schuldiner, M. A network of cytosolic factors targets SRP-independent proteins to the endoplasmic reticulum. Cell 152, 1134-1145 (2013).
12. Rapoport, T.A. Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450, 663-669 (2007).
13. von Heijne, G. Signal sequences: the limits of variation. J. Mol. Biol. 184, 99-105 (1985).
14. Janda, C.Y. et al. Recognition of a signal peptide by the signal recognition particle. Nature 465, 507-510 (2010).
15. Hegde, R.S. & Kang, S.-W. The concept of translocational regulation. J. Cell Biol. 182, 225-232 (2008).
16. Zheng, N. & Gierasch, L.M. Signal sequences: the same yet different. Cell 86, 849-852 (1996).
17. Kaiser, C.A., Preuss, D., Grisafi, P. & Botstein, D. Many random sequences functionally replace the secretion signal sequence of yeast invertase. Science 235, 312-317 (1987).
18. Kraut-Cohen, J. & Gerst, J.E. Addressing mRNAs to the ER: cis sequences act up. Trends Biochem. Sci. 35, 459-469 (2010).
19. Flanagan, J.J. et al. Signal recognition particle binds to ribosome-bound signal sequences with fluorescence-detected subnanomolar affinity that does not diminish as the nascent chain lengthens. J. Biol. Chem. 278, 18628-18637 (2003).
20. del Alamo, M. et al. Defining the specificity of cotranslationally acting chaperones by systematic analysis of mRNAs associated with ribosome-nascent chain complexes. PLoS Biol. 9, e1001100 (2011).
21. Fedyukina, D.V. & Cavagnero, S. Protein folding at the exit tunnel. Annu. Rev. Biophys. 40, 337-359 (2011).
22. Komar, A.A. A pause for thought along the co-translational folding pathway. Trends Biochem. Sci. 34, 16-24 (2009).
23. Zhang, G. & Ignatova, Z. Folding at the birth of the nascent chain: coordinating translation with co-translational folding. Curr. Opin. Struct. Biol. 21, 25-31 (2011).
24. O'Brien, E.P., Vendruscolo, M. & Dobson, C.M. Prediction of variable translation rate effects on cotranslational protein folding. Nat. Commun. 3, 868 (2012).
25. Pechmann, S. & Frydman, J. Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nat. Struct. Mol. Biol. 20, 237-243 (2013).
26. Gingold, H. & Pilpel, Y. Determinants of translation efficiency and accuracy. Mol. Syst. Biol. 7, 481 (2011).
27. Tuller, T. et al. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 141, 344-354 (2010).
28. Ingolia, N.T., Ghaemmaghami, S., Newman, J.R.S. & Weissman, J.S. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324, 218-223 (2009).
29. Zinshteyn, B. & Gilbert, W.V. Loss of a conserved tRNA anticodon modification perturbs cellular signaling. PLoS Genet. 9, e1003675 (2013).
30. Berndt, U., Oellerer, S., Zhang, Y., Johnson, A.E. & Rospert, S. A signal-anchor sequence stimulates signal recognition particle binding to ribosomes from inside the exit tunnel. Proc. Natl. Acad. Sci. USA 106, 1398-1403 (2009).
31. Charneski, C.A. & Hurst, L.D. Positively charged residues are the major determinants of ribosomal velocity. PLoS Biol. 11, e1001508 (2013).
32. Dalley, J.A., Selkirk, A. & Pool, M.R. Access to ribosomal protein Rpl25p by the signal recognition particle is required for efficient cotranslational translocation. Mol. Biol. Cell 19, 2876-2884 (2008).
33. Zhang, D. & Shan, S.-o. Translation elongation regulates substrate selection by the signal recognition particle. J. Biol. Chem. 287, 7652-7660 (2012).
34. Mason, N., Ciufo, L.F. & Brown, J.D. Elongation arrest is a physiologically important function of signal recognition particle. EMBO J. 19, 4164-4174 (2000).
35. Doerfel, L.K. et al. EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 339, 85-88 (2013).
36. Yang, J.R., Chen, X. & Zhang, J. Codon-by-codon modulation of translational speed and accuracy via mRNA folding. PLoS Biol. 12, e1001910 (2014).
37. Sherman, M.Y. & Qian, S.-B. Less is more: improving proteostasis by translation slow down. Trends Biochem. Sci. 38, 585-591 (2013).
38. Kramer, G., Boehringer, D., Ban, N. & Bukau, B. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16, 589-597 (2009).
39. Fluman, N., Navon, S., Bibi, E. & Pilpel, Y. mRNA-programmed translation pauses in the targeting of E. coli membrane proteins. Elife 3, e03440 (2014).
40. El Yacoubi, B., Bailly, M. & De Crécy-Lagard, V. Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu. Rev. Genet. 46, 69-95 (2012).
41. Tusher, V.G., Tibshirani, R. & Chu, G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98, 5116-5121 (2001).
42. Willmund, F. et al. The cotranslational function of ribosome-associated Hsp70 in eukaryotic protein homeostasis. Cell 152, 196-209 (2013).
43. Krogh, A., Larsson, B., Von Heijne, G. & Sonnhammer, E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580 (2001).
44. Nielsen, H., Engelbrecht, J., Brunak, S. & Von Heijne, G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10, 1-6 (1997).
45. Käll, L., Krogh, A. & Sonnhammer, E.L. A combined transmembrane topology and signal peptide prediction method. J. Mol. Biol. 338, 1027-1036 (2004).
46. Holstege, F.C. et al. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95, 717-728 (1998).
47. Pechmann, S., Levy, E.D., Tartaglia, G.G. & Vendruscolo, M. Physicochemical principles that regulate the competition between functional and dysfunctional association of proteins. Proc. Natl. Acad. Sci. USA 106, 10159-10164 (2009).
48. D'haeseleer, P. What are DNA sequence motifs? Nat. Biotechnol. 24, 423-425 (2006).
49. Papadopoulos, J.S. & Agarwala, R. COBALT: constraint-based alignment tool for multiple protein sequences. Bioinformatics 23, 1073-1079 (2007).
50. dos Reis, M., Savva, R. & Wernisch, L. Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res. 32, 5036-5044 (2004).
51. Qian, W., Yang, J.R., Pearson, N.M., Maclean, C. & Zhang, J. Balanced codon usage optimizes eukaryotic translational efficiency. PLoS Genet. 8, e1002603 (2012).
52. Li, G.W., Oh, E. & Weissman, J.S. The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 484, 538-541 (2012).
53. Zhang, F., Saha, S., Shabalina, S.A. & Kashina, A. Differential arginylation of actin isoforms is regulated by coding sequence-dependent degradation. Science 329, 1534-1537 (2010).
54. Zhang, G., Hubalewska, M. & Ignatova, Z. Transient ribosomal attenuation coordinates protein synthesis and co-translational folding. Nat. Struct. Mol. Biol. 16, 274-280 (2009).
55. Kimchi-Sarfaty, C. et al. A "silent" polymorphism in the MDR1 gene changes substrate specificity. Science 315, 525-528 (2007).
56. Fedyunin, I. et al. tRNA concentration fine tunes protein solubility. FEBS Lett. 586, 3336-3340 (2012).
57. Coleman, J.R. et al. Virus attenuation by genome-scale changes in codon pair bias. science 320, 1784-1787 (2008).