Codon optimality controls differential mRNA translation during amino acid starvation

RNA

Volumn 22, Issue 11, 2016, Pages 1719-1727

  Saikia, Mridusmita ^a   Wang, Xiaoyun ^b   Mao, Yuanhui ^a   Wan, Ji ^a   Pan, Tao ^b   Qian, Shu Bing ^a  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Adaptation; Codon bias; Genetic code; Starvation; Translation; tRNA

Indexed keywords

AMINO ACID; MESSENGER RNA; RIBOSOME PROTEIN; TRANSFER RNA; CODON;

ADAPTATION; ARTICLE; CODON; ESCHERICHIA COLI; GENE SEQUENCE; GENETIC CODE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RNA TRANSLATION; STARVATION; GENETICS; METABOLISM; PROTEIN SYNTHESIS; RIBOSOME;

AMINO ACIDS; CODON; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA, TRANSFER;

EID: 84992672006     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.058180.116     Document Type: Article

References (43)

1. Adams J. 2003. The proteasome: structure, function, and role in the cell. Cancer Treat Rev 29(Suppl 1): 3-9.
2. Arava Y, Wang Y, Storey JD, Liu CL, Brown PO, Herschlag D. 2003. Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci 100: 3889-3894.
3. Berlanga JJ, Santoyo J, De Haro C. 1999. Characterization of a mammalian homolog of the GCN2 eukaryotic initiation factor 2α kinase. Eur J Biochem 265: 754-762.
4. Bulmer M. 1987. Coevolution of codon usage and transfer RNA abundance. Nature 325: 728-730.
5. Dever TE, Feng L, Wek RC, Cigan AM, Donahue TF, Hinnebusch AG. 1992. Phosphorylation of initiation factor 2α by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68: 585-596.
6. Dittmar KA, Sorensen MA, Elf J, Ehrenberg M, Pan T. 2005. Selective charging of tRNA isoacceptors induced by amino-acid starvation. EMBO Rep 6: 151-157.
7. dos Reis M, Savva R, Wernisch L. 2004. Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res 32: 5036-5044.
8. Drummond DA, Wilke CO. 2009. The evolutionary consequences of erroneous protein synthesis. Nat Rev Genet 10: 715-724.
9. Elf J, Nilsson D, Tenson T, Ehrenberg M. 2003. Selective charging of tRNA isoacceptors explains patterns of codon usage. Science 300: 1718-1722.
10. Firczuk H, Kannambath S, Pahle J, Claydon A, Beynon R, Duncan J, Westerhoff H, Mendes P, McCarthy JE. 2013. An in vivo control map for the eukaryotic mRNA translation machinery. Mol Syst Biol 9: 635.
11. Gao X, Wan J, Liu B, Ma M, Shen B, Qian SB. 2015. Quantitative profiling of initiating ribosomes in vivo. Nat Methods 12: 147-153.
12. Gingold H, Tehler D, Christoffersen NR, Nielsen MM, Asmar F, Kooistra SM, Christophersen NS, Christensen LL, Borre M, Sorensen KD, et al. 2014. A dual program for translation regulation in cellular proliferation and differentiation. Cell 158: 1281-1292.
13. Gingras AC, Raught B, Sonenberg N. 2004. mTOR signaling to translation. Curr Top Microbiol Immunol 279: 169-197.
14. Hay N, Sonenberg N. 2004. Upstream and downstream of mTOR. Genes Dev 18: 1926-1945.
15. He C, Klionsky DJ. 2009. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43: 67-93.
16. Hershberg R, Petrov DA. 2008. Selection on codon bias. Annu Rev Genet 42: 287-299.
17. Heyer EE, Moore MJ. 2016. Redefining the translational status of 80S monosomes. Cell 164: 757-769.
18. Hsieh AC, Liu Y, Edlind MP, Ingolia NT, Janes MR, Sher A, Shi EY, Stumpf CR, Christensen C, Bonham MJ, et al. 2012. The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature 485: 55-61.
19. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS. 2009. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324: 218-223.
20. Lee S, Liu B, Lee S, Huang SX, Shen B, Qian SB. 2012. Global mapping of translation initiation sites in mammalian cells at single-nucleotide resolution. Proc Natl Acad Sci 109: E2424-E2432.
21. Liu B, Qian SB. 2014. Translational reprogramming in cellular stress response. Wiley Interdiscip Rev RNA 5: 301-315.
22. Loayza-Puch F, Rooijers K, Buil LC, Zijlstra J, Oude Vrielink JF, Lopes R, Ugalde AP, van Breugel P, Hofland I, Wesseling J, et al. 2016. Tumour-specific proline vulnerability uncovered by differential ribosome codon reading. Nature 530: 490-494.
23. Ma XM, Blenis J. 2009. Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10: 307-318.
24. Mizushima N. 2010. The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 22: 132-139.
25. Murata S, Yashiroda H, Tanaka K. 2009. Molecular mechanisms of proteasome assembly. Nat Rev Mol Cell Biol 10: 104-115.
26. Pechmann S, Chartron JW, Frydman J. 2014. Local slowdown of translation by nonoptimal codons promotes nascent-chain recognition by SRP in vivo. Nat Struct Mol Biol 21: 1100-1105.
27. Plotkin JB, Kudla G. 2011. Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 12: 32-42.
28. Presnyak V, Alhusaini N, Chen YH, Martin S, Morris N, Kline N, Olson S, Weinberg D, Baker KE, Graveley BR, et al. 2015. Codon optimality is a major determinant of mRNA stability. Cell 160: 1111-1124.
29. Racle J, Picard F, Girbal L, Cocaign-Bousquet M, Hatzimanikatis V. 2013. A genome-scale integration and analysis of Lactococcus lactis translation data. PLoS Comput Biol 9: e1003240.
30. Saikia M, Krokowski D, Guan BJ, Ivanov P, Parisien M, Hu GF, Anderson P, Pan T, Hatzoglou M. 2012. Genome-wide identification and quantitative analysis of cleaved tRNA fragments induced by cellular stress. J Biol Chem 287: 42708-42725.
31. Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M. 2011. Global quantification of mammalian gene expression control. Nature 473: 337-342.
32. Shah P, Ding Y, Niemczyk M, Kudla G, Plotkin JB. 2013. Rate-limiting steps in yeast protein translation. Cell 153: 1589-1601.
33. Sharp PM, Li WH. 1986. An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24: 28-38.
34. Sharp PM, Li WH. 1987. The codon Adaptation Index - a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15: 1281-1295.
35. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731-745.
36. Sood R, Porter AC, Olsen DA, Cavener DR, Wek RC. 2000. A mammalian homologue of GCN2 protein kinase important for translational control by phosphorylation of eukaryotic initiation factor-2α. Genetics 154: 787-801.
37. Spriggs KA, Bushell M, Willis AE. 2010. Translational regulation of gene expression during conditions of cell stress. Mol Cell 40: 228-237.
38. Tuller T, Carmi A, Vestsigian K, Navon S, Dorfan Y, Zaborske J, Pan T, Dahan O, Furman I, Pilpel Y. 2010. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 141: 344-354.
39. Wek RC, Jiang HY, Anthony TG. 2006. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34: 7-11.
40. Xu Y, Ma P, Shah P, Rokas A, Liu Y, Johnson CH. 2013. Non-optimal codon usage is a mechanism to achieve circadian clock conditionality. Nature 495: 116-120.
41. Yu CH, Dang Y, Zhou Z, Wu C, Zhao F, Sachs MS, Liu Y. 2015. Codon usage influences the local rate of translation elongation to regulate co-translational protein folding. Mol Cell 59: 744-754.
42. Zhou M, Guo J, Cha J, Chae M, Chen S, Barral JM, Sachs MS, Liu Y. 2013. Non-optimal codon usage affects expression, structure and function of clock protein FRQ. Nature 495: 111-115.
43. Zoncu R, Efeyan A, Sabatini DM. 2011. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 12: 21-35.