Effect of codon adaptation on codon-level and gene-level translation efficiency in vivo

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Nakahigashi, Kenji ^a   Takai, Yuki ^a   Shiwa, Yuh ^b,c   Wada, Mei ^a   Honma, Masayuki ^a   Yoshikawa, Hirofumi ^b   Tomita, Masaru ^a   Kanai, Akio ^a,b   Mori, Hirotada ^d  

^a KEIO UNIVERSITY   (Japan)

^b TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^c IWATE MEDICAL UNIVERSITY   (Japan)

^d NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

Chloramphenicol; Codon preference; Codon usage; Ribosome profiling; Translation efficiency

Indexed keywords

MESSENGER RNA; CODON; ESCHERICHIA COLI PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ARTICLE; BACTERIAL CELL; BACTERIUM CULTURE; CODON ADAPTATION; CODON USAGE; CONTROLLED STUDY; ESCHERICHIA COLI; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; GENE POOL; GENETIC ASSOCIATION; GENETIC PROCEDURES; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; IN VIVO STUDY; NONHUMAN; RIBOSOME PROFILING; RNA SEQUENCE; SEQUENCE ANALYSIS; TRANSLATION INITIATION; UPREGULATION; BACTERIAL GENOME; CHEMISTRY; CODON; GENETICS; METABOLISM; PROTEIN SYNTHESIS; RIBOSOME;

ESCHERICHIA COLI;

CODON; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENOME, BACTERIAL; PROTEIN BIOSYNTHESIS; PROTON-TRANSLOCATING ATPASES; RIBOSOMES; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA;

EID: 84925659421     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-1115     Document Type: Article

References (52)

1. Lu P, Vogel C, Wang R, Yao X, Marcotte EM: Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat Biotechnol 2007, 25:117-124.
2. Maier T, Schmidt A, Guell M, Kuhner S, Gavin AC, Aebersold R, Serrano L: Quantification of mRNA and protein and integration with protein turnover in a bacterium. Mol Syst Biol 2011, 7:511.
3. Ishii N, Nakahigashi K, Baba T, Robert M, Soga T, Kanai A, Hirasawa T, Naba M, Hirai K, Hoque A, Ho PY, Kakazu Y, Sugawara K, Igarashi S, Harada S, Masuda T, Sugiyama N, Togashi T, Hasegawa M, Takai Y, Yugi K, Arakawa K, Iwata N, Toya Y, Nakayama Y, Nishioka T, Shimizu K, Mori H, Tomita M: Multiple high-throughput analyses monitor the response of E. coli to perturbations. Science 2007, 316:593-597.
4. Hoskisson PA, Hobbs G: Continuous culture-making a comeback? Microbiology 2005, 151:3153-3159.
5. Plotkin JB, Kudla G: Synonymous but not the same: the causes and consequences of codon bias. Nat Rev Genet 2011, 12:32-42.
6. Kudla G, Murray AW, Tollervey D, Plotkin JB: Coding-sequence determinants of gene expression in Escherichia coli . Science 2009, 324:255-258.
7. Goodman DB, Church GM, Kosuri S: Causes and effects of N-terminal codon bias in bacterial genes. Science 2013, 342:475-479.
8. Shah P, Ding Y, Niemczyk M, Kudla G, Plotkin JB: Rate-limiting steps in yeast protein translation. Cell 2013, 153:1589-1601.
9. Fluitt A, Pienaar E, Viljoen H: Ribosome kinetics and aa-tRNA competition determine rate and fidelity of peptide synthesis. Comput Biol Chem 2007, 31:335-346.
10. Curran JF, Yarus M: Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. J Mol Biol 1989, 209:65-77.
11. Bulmer M: The selection-mutation-drift theory of synonymous codon usage. Genetics 1991, 129:897-907.
12. Andersson SG, Kurland CG: Codon preferences in free-living microorganisms. Microbiol Rev 1990, 54:198-210.
13. Guimaraes JC, Rocha M, Arkin AP: Transcript level and sequence determinants of protein abundance and noise in Escherichia coli . Nucleic Acids Res 2014, 42:4791-4799.
14. Tuller T, Waldman YY, Kupiec M, Ruppin E: Translation efficiency is determined by both codon bias and folding energy. Proc Natl Acad Sci U S A 2010, 107:3645-3650.
15. Zong Q, Schummer M, Hood L, Morris DR: Messenger RNA translation state: the second dimension of high-throughput expression screening. Proc Natl Acad Sci U S A 1999, 96:10632-10636.
16. Beilharz TH, Preiss T: Translational profiling: the genome-wide measure of the nascent proteome. Brief Funct Genomic Proteomic 2004, 3:103-111.
17. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS: Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 2009, 324:218-223.
18. Ingolia NT: Ribosome profiling: new views of translation, from single codons to genome scale. Nat Rev Genet 2014, 15:205-213.
19. Jones PC, Fillingame RH: Genetic fusions of subunit c in the F0 sector of H+-transporting ATP synthase. Functional dimers and trimers and determination of stoichiometry by cross-linking analysis. J Biol Chem 1998, 273:29701-29705.
20. Schneider E, Altendorf K: Bacterial adenosine 5'-triphosphate synthase (F1F0): purification and reconstitution of F0 complexes and biochemical and functional characterization of their subunits. Microbiol Rev 1987, 51:477-497.
21. Kasimoglu E, Park SJ, Malek J, Tseng CP, Gunsalus RP: Transcriptional regulation of the proton-translocating ATPase ( atpIBEFHAGDC ) operon of Escherichia coli: control by cell growth rate. J Bacteriol 1996, 178:5563-5567.
22. Li G-W, Burkhardt D, Gross C, Weissman Jonathan S: Quantifying Absolute Protein Synthesis Rates Reveals Principles Underlying Allocation of Cellular Resources. Cell 2014, 157:624-635.
23. Deana A, Belasco JG: Lost in translation: the influence of ribosomes on bacterial mRNA decay. Genes Dev 2005, 19:2526-2533.
24. Tusher VG, Tibshirani R, Chu G: Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001, 98:5116-5121.
25. Huang da W, Sherman BT, Lempicki RA: Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37:1-13.
26. Riley M, Abe T, Arnaud MB, Berlyn MK, Blattner FR, Chaudhuri RR, Glasner JD, Horiuchi T, Keseler IM, Kosuge T, Mori H, Perna NT, Plunkett G, Rudd KE, Serres MH, Thomas GH, Thomson NR, Wishart D, Wanner BL: Escherichia coli K-12: a cooperatively developed annotation snapshot-2005. Nucleic Acids Res 2006, 34:1-9.
27. Wikstrom PM, Bjork GR: Noncoordinate translation-level regulation of ribosomal and nonribosomal protein genes in the Escherichia coli trmD operon. J Bacteriol 1988, 170:3025-3031.
28. Krishnan KM, Van Etten WJ III, Janssen GR: Proximity of the start codon to a leaderless mRNA's 5' terminus is a strong positive determinant of ribosome binding and expression in Escherichia coli . J Bacteriol 2010, 192:6482-6485.
29. Salis HM: The ribosome binding site calculator. Methods Enzymol 2011, 498:19-42.
30. Salis HM, Mirsky EA, Voigt CA: Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol 2009, 27:946-950.
31. Sharp PM, Li WH: The codon Adaptation Index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 1987, 15:1281-1295.
32. Oh E, Becker AH, Sandikci A, Huber D, Chaba R, Gloge F, Nichols RJ, Typas A, Gross CA, Kramer G, Weissman JS, Bukau B: Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell 2011, 147:1295-1308.
33. Nakatogawa H, Ito K: Secretion monitor, SecM, undergoes self-translation arrest in the cytosol. Mol Cell 2001, 7:185-192.
34. Ikemura T: Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. J Mol Biol 1981, 151:389-409.
35. Li GW, Oh E, Weissman JS: The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 2012, 484:538-541.
36. Sharp PM, Li WH: An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 1986, 24:28-38.
37. Sorensen MA, Pedersen S: Absolute in vivo translation rates of individual codons in Escherichia coli . The two glutamic acid codons GAA and GAG are translated with a threefold difference in rate. J Mol Biol 1991, 222:265-280.
38. Wilson DN: The A-Z of bacterial translation inhibitors. Crit Rev Biochem Mol Biol 2009, 44:393-433.
39. Schlunzen F, Zarivach R, Harms J, Bashan A, Tocilj A, Albrecht R, Yonath A, Franceschi F: Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 2001, 413:814-821.
40. Bulkley D, Innis CA, Blaha G, Steitz TA: Revisiting the structures of several antibiotics bound to the bacterial ribosome. Proc Natl Acad Sci U S A 2010, 107:17158-17163.
41. Hansen JL, Moore PB, Steitz TA: Structures of five antibiotics bound at the peptidyl transferase center of the large ribosomal subunit. J Mol Biol 2003, 330:1061-1075.
42. Long KS, Porse BT: A conserved chloramphenicol binding site at the entrance to the ribosomal peptide exit tunnel. Nucleic Acids Res 2003, 31:7208-7215.
43. Kucan Z, Lipmann F: Differences in Chloramphenicol Sensitivity of Cell-Free Amino Acid Polymerization Systems. J Biol Chem 1964, 239:516-520.
44. Datsenko KA, Wanner BL: One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 2000, 97:6640-6645.
45. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H: Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2006. 2. http://msb.embopress.org/content/2/1/2006.0008
46. Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y: The complete genome sequence of Escherichia coli K-12. Science 1997, 277:1453-1462.
47. Lawther RP, Calhoun DH, Adams CW, Hauser CA, Gray J, Hatfield GW: Molecular basis of valine resistance in Escherichia coli K-12. Proc Natl Acad Sci U S A 1981, 78:922-925.
48. Neidhardt FC, Bloch PL, Smith DF: Culture medium for enterobacteria. J Bacteriol 1974, 119:736-747.
49. Maki Y, Yoshida H, Wada A: Two proteins, YfiA and YhbH, associated with resting ribosomes in stationary phase Escherichia coli . Genes Cells 2000, 5:965-974.
50. Langmead B, Trapnell C, Pop M, Salzberg S: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25.
51. R Development Core Team: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2012.
52. Arakawa K, Mori K, Ikeda K, Matsuzaki T, Kobayashi Y, Tomita M: G-language genome analysis environment: a workbench for nucleotide sequence data mining. Bioinformatics 2003, 19:305-306.