Differential translation tunes uneven production of operon-encoded proteins

Cell Reports

Volumn 4, Issue 5, 2013, Pages 938-944

  Quax, TessaE F ^a   Wolf, YuriI ^b   Koehorst, JasperJ ^a   Wurtzel, Omri ^c   vanderOost, Richard ^a   Ran, Wenqi ^b   Blombach, Fabian ^a   Makarova, KiraS ^b   Brouns, StanJ J ^a   Forster, AnthonyC ^d   Wagner, E GerhartH ^d   Sorek, Rotem ^c   Koonin, EugeneV ^b   vanderOost, John ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CISTRON; CODON; COMPARATIVE GENE MAPPING; ESCHERICHIA COLI; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSCRIPTION; IN VIVO STUDY; LISTERIA MONOCYTOGENES; NONHUMAN; OPERON; PRIORITY JOURNAL; PROTEIN ANALYSIS; PSEUDOMONAS AERUGINOSA; RIBOSOME; STOICHIOMETRY; SULFOLOBUS SOLFATARICUS; TRANSLATION INITIATION;

BASE SEQUENCE; CODON; GENE EXPRESSION; MOLECULAR SEQUENCE DATA; OPERON; PEPTIDE CHAIN ELONGATION, TRANSLATIONAL; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PROTEIN BIOSYNTHESIS; PROTEINS; RIBOSOMES; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 84884141974     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.07.049     Document Type: Article

References (46)

1. Abrahams J.P., Leslie A.G., Lutter R., Walker J.E. Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 1994, 370:621-628.
2. Beyenbach K.W., Wieczorek H. The V-type H+ ATPase: molecular structure and function, physiological roles and regulation. J.Exp. Biol. 2006, 209:577-589.
3. Brenner S., Jacob F., Meselson M. An unstable intermediate carrying information from genes to ribosomes for protein synthesis. Nature 1961, 190:576-581.
4. Cannarozzi G., Schraudolph N.N., Faty M., von Rohr P., Friberg M.T., Roth A.C., Gonnet P., Gonnet G., Barral Y. A role for codon order in translation dynamics. Cell 2010, 141:355-367.
5. Cho B.K., Zengler K., Qiu Y., Park Y.S., Knight E.M., Barrett C.L., Gao Y., Palsson B.O. The transcription unit architecture of the Escherichia coli genome. Nat. Biotechnol. 2009, 27:1043-1049.
6. Drummond D.A., Wilke C.O. Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 2008, 134:341-352.
7. Dunkle J.A., Wang L., Feldman M.B., Pulk A., Chen V.B., Kapral G.J., Noeske J., Richardson J.S., Blanchard S.C., Cate J.H. Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science 2011, 332:981-984.
8. Efremov R.G., Baradaran R., Sazanov L.A. The architecture of respiratory complex I. Nature 2010, 465:441-445.
9. Errington J. Dynamic proteins and a cytoskeleton in bacteria. Nat. Cell Biol. 2003, 5:175-178.
10. Forster A.C. Synthetic biology challenges long-held hypotheses in translation, codon bias and transcription. Biotechnol. J. 2012, 7:835-845.
11. Fredrick K., Ibba M. How the sequence of a gene can tune its translation. Cell 2010, 141:227-229.
12. French S.L., Santangelo T.J., Beyer A.L., Reeve J.N. Transcription and translation are coupled in Archaea. Mol. Biol. Evol. 2007, 24:893-895.
13. Ghosh A., Albers S.V. Assembly and function of the archaeal flagellum. Biochem. Soc. Trans. 2011, 39:64-69.
14. Gingold H., Pilpel Y. Determinants of translation efficiency and accuracy. Mol. Syst. Biol. 2011, 7:481.
15. Goldberger R.F., Deeley R.G., Mullinix K.P. Regulation of gene expression in prokaryotic organisms. Adv. Genet. 1976, 18:1-67.
16. Grundy F.J., Henkin T.M. From ribosome to riboswitch: control of gene expression in bacteria by RNA structural rearrangements. Crit. Rev. Biochem. Mol. Biol. 2006, 41:329-338.
17. Gur E., Biran D., Ron E.Z. Regulated proteolysis in Gram-negative bacteria-how and when?. Nat. Rev. Microbiol. 2011, 9:839-848.
18. Ikemura T. Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J.Mol. Biol. 1981, 146:1-21.
19. Ingolia N.T., Ghaemmaghami S., Newman J.R., Weissman J.S. Genome-wide analysis invivo of translation with nucleotide resolution using ribosome profiling. Science 2009, 324:218-223.
20. Jacob F., Monod J. Genetic regulatory mechanisms in the synthesis of proteins. J.Mol. Biol. 1961, 3:318-356.
21. Jakob M., Kaiser S., Gutensohn M., Hanner P., Klösgen R.B. Tat subunit stoichiometry in Arabidopsis thaliana challenges the proposed function of TatA as the translocation pore. Biochim. Biophys. Acta 2009, 1793:388-394.
22. Johnson T.L., Abendroth J., Hol W.G., Sandkvist M. Type II secretion: from structure to function. FEMS Microbiol. Lett. 2006, 255:175-186.
23. Jore M.M., Lundgren M., van Duijn E., Bultema J.B., Westra E.R., Waghmare S.P., Wiedenheft B., Pul U., Wurm R., Wagner R., et al. Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat. Struct. Mol. Biol. 2011, 18:529-536.
24. Kaberdin V.R., Bläsi U. Translation initiation and the fate of bacterial mRNAs. FEMS Microbiol. Rev. 2006, 30:967-979.
25. Koide T., Reiss D.J., Bare J.C., Pang W.L., Facciotti M.T., Schmid A.K., Pan M., Marzolf B., Van P.T., Lo F.Y., et al. Prevalence of transcription promoters within archaeal operons and coding sequences. Mol. Syst. Biol. 2009, 5:285.
26. Koonin E.V. Evolution of genome architecture. Int. J. Biochem. Cell Biol. 2009, 41:298-306.
27. Kudla G., Murray A.W., Tollervey D., Plotkin J.B. Coding-sequence determinants of gene expression in Escherichia coli. Science 2009, 324:255-258.
28. Lange S.J., Maticzka D., Möhl M., Gagnon J.N., Brown C.M., Backofen R. Global or local? Predicting secondary structure and accessibility in mRNAs. Nucleic Acids Res. 2012, 40:5215-5226.
29. Li Y., Altman S. Polarity effects in the lactose operon of Escherichia coli. J.Mol. Biol. 2004, 339:31-39.
30. Li G.W., Oh E., Weissman J.S. The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 2012, 484:538-541.
31. Marzi S., Myasnikov A.G., Serganov A., Ehresmann C., Romby P., Yusupov M., Klaholz B.P. Structured mRNAs regulate translation initiation by binding to the platform of the ribosome. Cell 2007, 130:1019-1031.
32. McCarthy J.E. Post-transcriptional control in the polycistronic operon environment: studies of the atp operon of Escherichia coli. Mol. Microbiol. 1990, 4:1233-1240.
33. Mendoza-Vargas A., Olvera L., Olvera M., Grande R., Vega-Alvarado L., Taboada B., Jimenez-Jacinto V., Salgado H., Juárez K., Contreras-Moreira B., et al. Genome-wide identification of transcription start sites, promoters and transcription factor binding sites in E. coli. PLoS ONE 2009, 4:e7526.
34. Oppenheim D.S., Yanofsky C. Translational coupling during expression of the tryptophan operon of Escherichia coli. Genetics 1980, 95:785-795.
35. Shao Z.Q., Zhang Y.M., Feng X.Y., Wang B., Chen J.Q. Synonymous codon ordering: a subtle but prevalent strategy of bacteria to improve translational efficiency. PLoS ONE 2012, 7:e33547.
36. Sharp P.M., Li W.H. The codon Adaptation Index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987, 15:1281-1295.
37. Stenström C.M., Jin H., Major L.L., Tate W.P., Isaksson L.A. Codon bias at the 3'-side of the initiation codon is correlated with translation initiation efficiency in Escherichia coli. Gene 2001, 263:273-284.
38. Timmermans J., Van Melderen L. Post-transcriptional global regulation by CsrA in bacteria. Cell. Mol. Life Sci. 2010, 67:2897-2908.
39. Toledo-Arana A., Dussurget O., Nikitas G., Sesto N., Guet-Revillet H., Balestrino D., Loh E., Gripenland J., Tiensuu T., Vaitkevicius K., et al. The Listeria transcriptional landscape from saprophytism to virulence. Nature 2009, 459:950-956.
40. Tuller T., Carmi A., Vestsigian K., Navon S., Dorfan Y., Zaborske J., Pan T., Dahan O., Furman I., Pilpel Y. An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell 2010, 141:344-354.
41. Vellanoweth R.L., Rabinowitz J.C. The influence of ribosome-binding-site elements on translational efficiency in Bacillus subtilis and Escherichia coli invivo. Mol. Microbiol. 1992, 6:1105-1114.
42. Welch M., Govindarajan S., Ness J.E., Villalobos A., Gurney A., Minshull J., Gustafsson C. Design parameters to control synthetic gene expression in Escherichia coli. PLoS ONE 2009, 4:e7002.
43. Wiedenheft B., van Duijn E., Bultema J.B., Waghmare S.P., Zhou K., Barendregt A., Westphal W., Heck A.J., Boekema E.J., Dickman M.J., Doudna J.A. RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc. Natl. Acad. Sci. USA 2011, 108:10092-10097.
44. Wurtzel O., Sapra R., Chen F., Zhu Y., Simmons B.A., Sorek R. A single-base resolution map of an archaeal transcriptome. Genome Res. 2010, 20:133-141.
45. Wurtzel O., Sesto N., Mellin J.R., Karunker I., Edelheit S., Bécavin C., Archambaud C., Cossart P., Sorek R. Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol. Syst. Biol. 2012, 8:583.
46. Wurtzel O., Yoder-Himes D.R., Han K., Dandekar A.A., Edelheit S., Greenberg E.P., Sorek R., Lory S. The single-nucleotide resolution transcriptome of Pseudomonas aeruginosa grown in body temperature. PLoS Pathog. 2012, 8:e1002945.