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. 1991 Oct 11;19(19):5247–5251. doi: 10.1093/nar/19.19.5247

Codon choice and potential complementarity between mRNA downstream of the initiation codon and bases 1471-1480 in 16S ribosomal RNA affects expression of glnS.

M Faxén 1, J Plumbridge 1, L A Isaksson 1
PMCID: PMC328883  PMID: 1681509

Abstract

A cis-acting expression mutation, GAG to GAA, in the third codon of the glnS gene is analyzed. Both codons code for glutamic acid but the mutation is known to increase gene expression by four fold. We show that the mutation has an effect only if it is located in the beginning of a gene but not if located internally. Data are presented that suggest that the reason for the increased expression by the mutation is the potential formation of one more base pair between the mRNA and 16S ribosomal RNA. Gene expression varies about 16 fold as the number of potential base pairs within the sequence 1471-1480 in 16S RNA increase from two to ten. We also give evidence that supports the idea that the presence of rare codons near the beginning of the mRNA can affect expression.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abrahmsén L., Moks T., Nilsson B., Uhlén M. Secretion of heterologous gene products to the culture medium of Escherichia coli. Nucleic Acids Res. 1986 Sep 25;14(18):7487–7500. doi: 10.1093/nar/14.18.7487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amann E., Ochs B., Abel K. J. Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene. 1988 Sep 30;69(2):301–315. doi: 10.1016/0378-1119(88)90440-4. [DOI] [PubMed] [Google Scholar]
  3. Bonekamp F., Dalbøge H., Christensen T., Jensen K. F. Translation rates of individual codons are not correlated with tRNA abundances or with frequencies of utilization in Escherichia coli. J Bacteriol. 1989 Nov;171(11):5812–5816. doi: 10.1128/jb.171.11.5812-5816.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bonekamp F., Jensen K. F. The AGG codon is translated slowly in E. coli even at very low expression levels. Nucleic Acids Res. 1988 Apr 11;16(7):3013–3024. doi: 10.1093/nar/16.7.3013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chen G. F., Inouye M. Suppression of the negative effect of minor arginine codons on gene expression; preferential usage of minor codons within the first 25 codons of the Escherichia coli genes. Nucleic Acids Res. 1990 Mar 25;18(6):1465–1473. doi: 10.1093/nar/18.6.1465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chen K. S., Peters T. C., Walker J. R. A minor arginine tRNA mutant limits translation preferentially of a protein dependent on the cognate codon. J Bacteriol. 1990 May;172(5):2504–2510. doi: 10.1128/jb.172.5.2504-2510.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Curran J. F., Yarus M. Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. J Mol Biol. 1989 Sep 5;209(1):65–77. doi: 10.1016/0022-2836(89)90170-8. [DOI] [PubMed] [Google Scholar]
  8. Dreyfus M. What constitutes the signal for the initiation of protein synthesis on Escherichia coli mRNAs? J Mol Biol. 1988 Nov 5;204(1):79–94. doi: 10.1016/0022-2836(88)90601-8. [DOI] [PubMed] [Google Scholar]
  9. Gallie D. R., Kado C. I. A translational enhancer derived from tobacco mosaic virus is functionally equivalent to a Shine-Dalgarno sequence. Proc Natl Acad Sci U S A. 1989 Jan;86(1):129–132. doi: 10.1073/pnas.86.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gold L., Pribnow D., Schneider T., Shinedling S., Singer B. S., Stormo G. Translational initiation in prokaryotes. Annu Rev Microbiol. 1981;35:365–403. doi: 10.1146/annurev.mi.35.100181.002053. [DOI] [PubMed] [Google Scholar]
  11. Gren E. J. Recognition of messenger RNA during translational initiation in Escherichia coli. Biochimie. 1984 Jan;66(1):1–29. doi: 10.1016/0300-9084(84)90188-3. [DOI] [PubMed] [Google Scholar]
  12. Inokuchi H., Hoben P., Yamao F., Ozeki H., Söll D. Transfer RNA mischarging mediated by a mutant Escherichia coli glutaminyl-tRNA synthetase. Proc Natl Acad Sci U S A. 1984 Aug;81(16):5076–5080. doi: 10.1073/pnas.81.16.5076. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kozak M. Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol Rev. 1983 Mar;47(1):1–45. doi: 10.1128/mr.47.1.1-45.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. McCarthy J. E., Sebald W., Gross G., Lammers R. Enhancement of translational efficiency by the Escherichia coli atpE translational initiation region: its fusion with two human genes. Gene. 1986;41(2-3):201–206. doi: 10.1016/0378-1119(86)90099-5. [DOI] [PubMed] [Google Scholar]
  15. Neidhardt F. C., Bloch P. L., Pedersen S., Reeh S. Chemical measurement of steady-state levels of ten aminoacyl-transfer ribonucleic acid synthetases in Escherichia coli. J Bacteriol. 1977 Jan;129(1):378–387. doi: 10.1128/jb.129.1.378-387.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nilsson B., Moks T., Jansson B., Abrahmsén L., Elmblad A., Holmgren E., Henrichson C., Jones T. A., Uhlén M. A synthetic IgG-binding domain based on staphylococcal protein A. Protein Eng. 1987 Feb-Mar;1(2):107–113. doi: 10.1093/protein/1.2.107. [DOI] [PubMed] [Google Scholar]
  17. Olins P. O., Rangwala S. H. A novel sequence element derived from bacteriophage T7 mRNA acts as an enhancer of translation of the lacZ gene in Escherichia coli. J Biol Chem. 1989 Oct 15;264(29):16973–16976. [PubMed] [Google Scholar]
  18. Perona J. J., Swanson R. N., Rould M. A., Steitz T. A., Söll D. Structural basis for misaminoacylation by mutant E. coli glutaminyl-tRNA synthetase enzymes. Science. 1989 Dec 1;246(4934):1152–1154. doi: 10.1126/science.2686030. [DOI] [PubMed] [Google Scholar]
  19. Petersen G. B., Stockwell P. A., Hill D. F. Messenger RNA recognition in Escherichia coli: a possible second site of interaction with 16S ribosomal RNA. EMBO J. 1988 Dec 1;7(12):3957–3962. doi: 10.1002/j.1460-2075.1988.tb03282.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Plumbridge J., Söll D. Characterization of cis-acting mutations which increase expression of a glnS-lacZ fusion in Escherichia coli. Mol Gen Genet. 1989 Mar;216(1):113–119. doi: 10.1007/BF00332238. [DOI] [PubMed] [Google Scholar]
  21. Scherer G. F., Walkinshaw M. D., Arnott S., Morré D. J. The ribosome binding sites recognized by E. coli ribosomes have regions with signal character in both the leader and protein coding segments. Nucleic Acids Res. 1980 Sep 11;8(17):3895–3907. doi: 10.1093/nar/8.17.3895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schneider T. D., Stormo G. D., Gold L., Ehrenfeucht A. Information content of binding sites on nucleotide sequences. J Mol Biol. 1986 Apr 5;188(3):415–431. doi: 10.1016/0022-2836(86)90165-8. [DOI] [PubMed] [Google Scholar]
  23. Sprengart M. L., Fatscher H. P., Fuchs E. The initiation of translation in E. coli: apparent base pairing between the 16srRNA and downstream sequences of the mRNA. Nucleic Acids Res. 1990 Apr 11;18(7):1719–1723. doi: 10.1093/nar/18.7.1719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Stormo G. D., Schneider T. D., Gold L. M. Characterization of translational initiation sites in E. coli. Nucleic Acids Res. 1982 May 11;10(9):2971–2996. doi: 10.1093/nar/10.9.2971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Swanson R., Hoben P., Sumner-Smith M., Uemura H., Watson L., Söll D. Accuracy of in vivo aminoacylation requires proper balance of tRNA and aminoacyl-tRNA synthetase. Science. 1988 Dec 16;242(4885):1548–1551. doi: 10.1126/science.3144042. [DOI] [PubMed] [Google Scholar]

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