Abortive translation caused by peptidyl-tRNA drop-off at NGG codons in the early coding region of mRNA

FEBS Journal

Volumn 272, Issue 20, 2005, Pages 5306-5316

  Gonzalez De Valdivia, Ernesto I ^a   Isaksson, Leif A ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Abortive translation; Early elongation; Escherichia coli; NGG codons; Peptidyl tRNA drop off

Indexed keywords

BETA GALACTOSIDASE; MESSENGER RNA; PEPTIDE; TRANSFER RNA;

ARTICLE; CODON; CONTROLLED STUDY; ENZYME INHIBITION; GENE OVEREXPRESSION; GROWTH INHIBITION; NONHUMAN; PLASMID; PRIORITY JOURNAL; RNA TRANSLATION; WILD TYPE;

BASE SEQUENCE; CARBOXYLIC ESTER HYDROLASES; CELL DIVISION; CODON; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; LAC OPERON; MOLECULAR SEQUENCE DATA; MUTATION; PLASMIDS; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; RNA, TRANSFER, AMINO ACYL; RNA, TRANSFER, ARG; RNA, TRANSFER, GLY; STAPHYLOCOCCAL PROTEIN A; TEMPERATURE; TRANSFORMATION, BACTERIAL;

ESCHERICHIA COLI;

EID: 27144528592     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2005.04926.x     Document Type: Article

References (46)

1. Roberts MW & Rabinowitz JC (1989) The effect of Escherichia coli ribosomal protein S1 on the translational specificity of bacterial ribosomes. J Biol Chem 264, 2228-2235.
2. Spanjaard RA & van Duin J (1989) Translational reinitiation in the presence and absence of a Shine and Dalgarno sequence. Nucleic Acids Res 17, 5501-5507.
3. Stenström CM, Holmgren E & Isaksson LA (2001b) Cooperative effects by the initiation codon and its flanking regions on translation initiation. Gene 273, 259-265.
4. O'Connor M, Asai T, Squires CL & Dahlberg AE (1999) Enhancement of translation by the downstream box does not involve base pairing of mRNA with the penultimate stem sequence of 16S rRNA. Proc Natl Acad Sci USA 96, 8973-8978.
5. Moll I, Huber M, Grill S, Sairafi P, Mueller F, Brimacombe R, Londei P & Blasi U (2001) Evidence against an Interaction between the mRNA downstream box and 16S rRNA in translation initiation. J Bacteriol 183, 3499-3505.
6. Chen G-FT & Inouye M (1990) Suppression of the negative effect of minor arginine codons on gene expression; preferential usage of minor codons within the first 25 codons of the Eschericia coli genes. Nucleic Acids Res 18, 1465-1473.
7. Looman AC, Bodlaender J, Comstock LJ, Eaton D, Jhurani P, deBoer HA & van Knippenberg PH (1987) Influence of the codon following the AUG initiation codon on the expression of a modified lacZ gene in Escherichia coli. EMBO J 6, 2489-2492.
8. Faxen M, Plumbridge J & Isaksson LA (1991) Codon choice and potential complementarity between mRNA downstream of the initiation codon and bases 1471-1480 in the 16S ribosomal RNA affects expression of gin S. Nucleic Acids Res 19, 5247-5251.
9. Stenström CM, Jin H, Major LL, Tate WP & Isaksson LA (2001a) Codon bias at the 3′-side of the initiation codon is correlated with translation initiation efficiency in Escherichia coli. Gene 263, 273-284.
10. Gonzalez de Valdivia EI & Isaksson LA (2004) A codon window in mRNA downstream of the initiation codon where NGG codons give strongly reduced gene expression in Escherichia coli. Nucleic Acids Res 32, 5198-5205.
11. Kurland CG, Hughes D & Ehrenberg M (1996) Limitations of translational accuracy. In Escherichia coli and Salmonella thyphimurium: Cellular and Molecular Biology (Neidhardt FC, ed.), pp. 979-999. ASM Press, Washington D.C.
12. Atherly AG & Menninger JR (1972) Mutant E. coli strain with temperature sensitive peptidyl-transfer RNA hydrolase. Nat New Biol 240, 245-246.
13. Menninger JR (1976) Peptidyl transfer RNA dissociates during protein synthesis from ribosomes of Escherichia coli. J Biol Chem 251, 3392-3398.
14. Menninger JR (1979) Accumulation of peptidyl tRNA is lethal to Escherichia coli. J Bacteriol 137, 694-696.
15. Hernandez-Sanchez J, Valadez JG, Herrera JV, Ontiveros C & Guarneros G (1998) lambda bar minigene-mediated inhibition of protein synthesis involves accumulation of peptidyl-tRNA and starvation for tRNA. EMBO J 17, 3758-3765.
16. Karimi R, Pavlov MY, Heurgue-Hamard V, Buckingham RH & Ehrenberg M (1998) Initiation factors IF1 and IF2 synergistically remove peptidyl-tRNAs with short polypeptides from the P-site of translating Escherichia coli ribosomes. J Mol Biol 281, 241-252.
17. Heurgue-Hamard V, Dincbas V, Buckingham RH & Ehrenberg M (2000) Origins of minigene-dependent growth inhibition in bacterial cells. EMBO J 19, 2701-2709.
18. Cruz-Vera LR, Hernandez-Ramon E, Perez-Zamorano B & Guarneros G (2003) The rate of peptidyl-tRNA dissociation from the ribosome during minigene expression depends on the nature of the last decoding interaction. J Biol Chem 278, 26065-26070.
19. Olivares-Trejo JJ, Bueno-Martinez JG, Guarneros G & Hernandez-Sanchez J (2003) The pair of arginine codons AGA AGG close to the initiation codon of the lambda int gene inhibits cell growth and protein synthesis by accumulating peptidyl-tRNAArg4. Mol Microbiol 49, 1043-1049.
20. Menez J, Heurgue-Hamard V & Buckingham RH (2000) Sequestration of specific tRNA species cognate to the last sense codon of an overproduced gratuitous protein. Nucleic Acids Res 28, 4725-4732.
21. Croitoru VV, Bucheli-Witschel M & Isaksson LA (2005) In vivo involvement of mutated initiation factor IF1 in gene expression control at the translational level. FEBS Lett 579, 995-1000.
22. Menninger JR (1978) The accumulation as peptidyl-transfer RNA of isoaccepting transfer RNA families in Escherichia coli with temperature- sensitive peptidyl-transfer RNA hydrolase. J Biol Chem 253, 6808-6813.
23. Stenström CM & Isaksson LA (2002) Influences on translation initiation and early elongation by the messenger RNA region flanking the initiation codon at the 3′ side. Gene 288, 1-8.
24. Spanjaard RA & Duin JV (1988) Translation of the sequence AGG-AGG yields 50% ribosomal frameshift. Proc Natl Acad Sci USA 85, 7967-7971.
25. Zahn K & Landy A (1996) Modulation of lambda integrase synthesis by rare arginine tRNA. Mol Microbiol 21, 69-76.
26. Varenne S, Baty D, Verheij H, Shire D & Lazdunski C (1989) The maximum rate of gene expression is dependent on the downstream context of unfavourable codons. Biochimie 71, 1221-1229.
27. Rosenberg AH, Goldman E, Dunn JJ, Studier FW & Zubay G (1993) Effects of consecutive AGG codons on translation in Escherichia coli, demonstrated with a versatile codon test system. J Bacteriol 175, 716-722.
28. Chen G-FT & Inouye M (1994) Role of the AGA/AGG codons, the rarest codons in global gene expression in Escherichia coli. Genes Dev 8, 2641-2652.
29. Gao W, Tyagi S, Kramer FR & Goldman E (1997) Messenger RNA release from ribosomes during 5′-translational blockage by consecutive low-usage arginine but not leucine codons in Escherichia coli. Mol Microbiol 25, 707-716.
30. Jin H, Björnsson A & Isaksson LA (2002) Cis control of gene expression in E.coli by ribosome queuing at an inefficient translational stop signal. EMBO J 21, 4357-4367.
31. Beyer D, Skripkin E, Wadzack J & Nierhaus KH (1994) How the ribosome moves along the mRNA during protein synthesis. J Biol Chem 269, 30713-30717.
32. Green R & Noller HF (1997) Ribosomes and translation. Annu Rev Biochem 66, 679-716.
33. Dinçbas V, Heurgué-Hamard V, Buckingham RH, Karimi R & Ehrenberg M (1999) Shutdown in protein synthesis due to the expression of mini-genes in bacteria. J Mol Biol 291, 745-759.
34. Brinkmann U, Mattes RE & Buckel P (1989) High-level expression of recombinant genes in Escherichia coli is dependent on the availability of the dnaY gene product. Gene 85, 109-114.
35. Zahn K (1996) Overexpression of an mRNA dependent on rare codons inhibits protein synthesis and cell growth. J Bacteriol 178, 2926-2933.
36. Cruz-Vera LR, Magos-Castro MA, Zamora-Romo E & Guarneros G (2004) Ribosome stalling and peptidyl-tRNA drop-off during translational delay at AGA codons. Nucleic Acids Res 32, 4462-4468.
37. Björk GR (1996) Escherichia coli and Salmonella typhimurium. In Escherichia coli and Salmonella thyphimurium: Cellular and Molecular Biology (Neidhardt FC, ed.), pp. 861-880. ASM Press, Washington D.C.
38. Gustafsson C, Govindarajan S & Minshull J (2004) Codon bias and heterologous protein expression. Trends Biotechnol 22, 346-353.
39. O'Connor M (1998) tRNA imbalance promotes-1 frameshifting via near-cognate decoding. J Mol Biol 279, 727-736.
40. Imamura H, Jeon B, Wakagi T & Matsuzawa H (1999) High level expression of Thermococcus litoralis 4-alpha-glucanotransferase in a soluble form in Escherichia coli with a novel expression system involving minor arginine tRNAs and GroELS. FEBS Lett 457, 393-396.
41. Sorensen HP, Sperling-Petersen HU & Mortensen KK (2003) Production of recombinant thermostable proteins expressed in Escherichia coli: completion of protein synthesis is the bottleneck. J Chromatogr B Analyt Technol Biomed Life Sci 786, 207-214.
42. Yonath A & Berkovitch-Yellin Z (1993) Hollow, voids, gaps and tunnel in the ribosome. Curr Opin Struct Biol 3, 175-181.
43. Coulondre C & Miller JH (1977) Genetic studies of the lac repressor. III. Additional correlation of mutational sites with specific amino acid residues. J Mol Biol 117, 525-567.
44. Sambrook J, Fritsch EF & Maniatis T (1989) Molecular Cloning a Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
45. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, New York.
46. Björnsson A, Mottagui-Tabar S & Isaksson LA (1998) The analysis of translational activity using a reporter gene constructed from repeats of an antibody-binding domain from protein A. In Methods in Molecular Biology, pp. 75-91. Edited by R. Martin© Human Press Inc, Totawa, NJ.