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. 1993 May;175(10):3204–3207. doi: 10.1128/jb.175.10.3204-3207.1993

Frameshifting in the expression of the Escherichia coli trpR gene is modulated by translation initiation.

I Benhar 1, C Miller 1, H Engelberg-Kulka 1
PMCID: PMC204645  PMID: 8491735

Abstract

The Escherichia coli trpR gene encodes the 108-amino-acid-long Trp repressor. We have shown previously that a +1 frameshifting event occurs during the expression of trpR, resulting in the synthesis of an additional (+1 frame) polypeptide. Using trpR-lac'Z fusions, we have recently found that the transition from the 0 to the +1 frame occurs via the bypassing of a 55-nucleotide-long segment of the trpR+1-lac'Z mRNA (I. Benhar, and H. Engelberg-Kulka, Cell 72:121-130, 1993). Here we show that the frequency of trpR frameshifting (or bypassing) can be regulated both in vivo and in vitro. This frequency is inversely proportional to the rate of initiation of translation of the trpR gene. Hence, modulating the level of translation initiation affects the frequency of frameshifting.

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Selected References

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  1. Atkins J. F., Weiss R. B., Gesteland R. F. Ribosome gymnastics--degree of difficulty 9.5, style 10.0. Cell. 1990 Aug 10;62(3):413–423. doi: 10.1016/0092-8674(90)90007-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Atkins J. F., Weiss R. B., Thompson S., Gesteland R. F. Towards a genetic dissection of the basis of triplet decoding, and its natural subversion: programmed reading frame shifts and hops. Annu Rev Genet. 1991;25:201–228. doi: 10.1146/annurev.ge.25.120191.001221. [DOI] [PubMed] [Google Scholar]
  3. Benhar I., Engelberg-Kulka H. Frameshifting in the expression of the E. coli trpR gene occurs by the bypassing of a segment of its coding sequence. Cell. 1993 Jan 15;72(1):121–130. doi: 10.1016/0092-8674(93)90056-v. [DOI] [PubMed] [Google Scholar]
  4. Benhar I., Miller C., Engelberg-Kulka H. Frameshifting in the expression of the Escherichia coli trpR gene. Mol Microbiol. 1992 Oct;6(19):2777–2784. doi: 10.1111/j.1365-2958.1992.tb01457.x. [DOI] [PubMed] [Google Scholar]
  5. Blinkowa A. L., Walker J. R. Programmed ribosomal frameshifting generates the Escherichia coli DNA polymerase III gamma subunit from within the tau subunit reading frame. Nucleic Acids Res. 1990 Apr 11;18(7):1725–1729. doi: 10.1093/nar/18.7.1725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bogosian G., Bertrand K., Somerville R. Trp repressor protein controls its own structural gene. J Mol Biol. 1981 Jul 15;149(4):821–825. doi: 10.1016/0022-2836(81)90361-2. [DOI] [PubMed] [Google Scholar]
  7. Condron B. G., Gesteland R. F., Atkins J. F. An analysis of sequences stimulating frameshifting in the decoding of gene 10 of bacteriophage T7. Nucleic Acids Res. 1991 Oct 25;19(20):5607–5612. doi: 10.1093/nar/19.20.5607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Craigen W. J., Caskey C. T. Expression of peptide chain release factor 2 requires high-efficiency frameshift. Nature. 1986 Jul 17;322(6076):273–275. doi: 10.1038/322273a0. [DOI] [PubMed] [Google Scholar]
  9. Craigen W. J., Caskey C. T. The function, structure and regulation of E. coli peptide chain release factors. Biochimie. 1987 Oct;69(10):1031–1041. doi: 10.1016/0300-9084(87)90003-4. [DOI] [PubMed] [Google Scholar]
  10. Curran J. F., Yarus M. Use of tRNA suppressors to probe regulation of Escherichia coli release factor 2. J Mol Biol. 1988 Sep 5;203(1):75–83. doi: 10.1016/0022-2836(88)90092-7. [DOI] [PubMed] [Google Scholar]
  11. Flower A. M., McHenry C. S. The gamma subunit of DNA polymerase III holoenzyme of Escherichia coli is produced by ribosomal frameshifting. Proc Natl Acad Sci U S A. 1990 May;87(10):3713–3717. doi: 10.1073/pnas.87.10.3713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Folley L. S., Yarus M. Codon contexts from weakly expressed genes reduce expression in vivo. J Mol Biol. 1989 Oct 5;209(3):359–378. doi: 10.1016/0022-2836(89)90003-x. [DOI] [PubMed] [Google Scholar]
  13. Gunsalus R. P., Yanofsky C. Nucleotide sequence and expression of Escherichia coli trpR, the structural gene for the trp aporepressor. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7117–7121. doi: 10.1073/pnas.77.12.7117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jacks T., Townsley K., Varmus H. E., Majors J. Two efficient ribosomal frameshifting events are required for synthesis of mouse mammary tumor virus gag-related polyproteins. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4298–4302. doi: 10.1073/pnas.84.12.4298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jacks T., Varmus H. E. Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting. Science. 1985 Dec 13;230(4731):1237–1242. doi: 10.1126/science.2416054. [DOI] [PubMed] [Google Scholar]
  16. Kelley R. L., Yanofsky C. Trp aporepressor production is controlled by autogenous regulation and inefficient translation. Proc Natl Acad Sci U S A. 1982 May;79(10):3120–3124. doi: 10.1073/pnas.79.10.3120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Paluh J. L., Yanofsky C. High level production and rapid purification of the E. coli trp repressor. Nucleic Acids Res. 1986 Oct 24;14(20):7851–7860. doi: 10.1093/nar/14.20.7851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Parker J. Errors and alternatives in reading the universal genetic code. Microbiol Rev. 1989 Sep;53(3):273–298. doi: 10.1128/mr.53.3.273-298.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Russel M., Model P. Replacement of the fip gene of Escherichia coli by an inactive gene cloned on a plasmid. J Bacteriol. 1984 Sep;159(3):1034–1039. doi: 10.1128/jb.159.3.1034-1039.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Tabor S., Richardson C. C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1074–1078. doi: 10.1073/pnas.82.4.1074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tsuchihashi Z., Kornberg A. Translational frameshifting generates the gamma subunit of DNA polymerase III holoenzyme. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2516–2520. doi: 10.1073/pnas.87.7.2516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Varmus H. Retroviruses. Science. 1988 Jun 10;240(4858):1427–1435. doi: 10.1126/science.3287617. [DOI] [PubMed] [Google Scholar]
  24. Varshney U., RajBhandary U. L. Initiation of protein synthesis from a termination codon. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1586–1590. doi: 10.1073/pnas.87.4.1586. [DOI] [PMC free article] [PubMed] [Google Scholar]

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