Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1986 Feb;49(2):425–435. doi: 10.1016/S0006-3495(86)83652-9

Theoretical evaluation of transcriptional pausing effect on the attenuation in trp leader sequence.

H Suzuki, T Kunisawa, J Otsuka
PMCID: PMC1329482  PMID: 3513858

Abstract

The effect of transcriptional pausing on attenuation is investigated theoretically on the basis of the attenuation control mechanism presented by Oxender et al. (Oxender, D. L., G. Zurawski, and C. Yanofsky, 1979, Proc. Natl. Acad. Sci. USA. 76:5524-5528). An extended stochastic model including the RNA polymerase pausing in the leader region is developed to calculate the probability of relative position between the RNA polymerase transcribing the trp leader sequence and the ribosome translating the transcript. The present study results in a new rationale that the transcriptional pausing site in the leader sequence makes the attenuation control both more sensitive as an on/off switch and less sensitive to variations in the concentration of cellular metabolites not connected with the need for expressing, or not expressing, the particular operon. It is also proposed that the transcriptional pausing diminishes the dependence of attenuation control characteristics on the number of nucleotides in the leader sequence. This result may be useful for understanding the attenuation control efficiencies of other amino acid leader sequences with different lengths of nucleotides.

Full text

PDF
425

Selected References

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

  1. Barnes W. M. DNA sequence from the histidine operon control region: seven histidine codons in a row. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4281–4285. doi: 10.1073/pnas.75.9.4281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bertrand K., Korn L. J., Lee F., Yanofsky C. The attenuator of the tryptophan operon of Escherichia coli. Heterogeneous 3'-OH termini in vivo and deletion mapping of functions. J Mol Biol. 1977 Nov 25;117(1):227–247. doi: 10.1016/0022-2836(77)90032-8. [DOI] [PubMed] [Google Scholar]
  3. Blumenberg M., Yanofsky C. Evolutionary divergence of the Citrobacter freundii tryptophan operon regulatory region: comparison with other enteric bacteria. J Bacteriol. 1982 Oct;152(1):57–62. doi: 10.1128/jb.152.1.57-62.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blumenberg M., Yanofsky C. Regulatory region of the Klebsiella aerogenes tryptophan operon. J Bacteriol. 1982 Oct;152(1):49–56. doi: 10.1128/jb.152.1.49-56.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Crawford I. P., Stauffer G. V. Regulation of tryptophan biosynthesis. Annu Rev Biochem. 1980;49:163–195. doi: 10.1146/annurev.bi.49.070180.001115. [DOI] [PubMed] [Google Scholar]
  6. Farnham P. J., Platt T. A model for transcription termination suggested by studies on the trp attenuator in vitro using base analogs. Cell. 1980 Jul;20(3):739–748. doi: 10.1016/0092-8674(80)90320-7. [DOI] [PubMed] [Google Scholar]
  7. Fisher R., Yanofsky C. A complementary DNA oligomer releases a transcription pause complex. J Biol Chem. 1983 Aug 10;258(15):9208–9212. [PubMed] [Google Scholar]
  8. Friden P., Newman T., Freundlich M. Nucleotide sequence of the ilvB promoter-regulatory region: a biosynthetic operon controlled by attenuation and cyclic AMP. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6156–6160. doi: 10.1073/pnas.79.20.6156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gardner J. F. Initiation, pausing, and termination of transcription in the threonine operon regulatory region of Escherichia coli. J Biol Chem. 1982 Apr 10;257(7):3896–3904. [PubMed] [Google Scholar]
  10. Grantham R., Gautier C., Gouy M., Jacobzone M., Mercier R. Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res. 1981 Jan 10;9(1):r43–r74. doi: 10.1093/nar/9.1.213-b. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hauser C. A., Sharp J. A., Hatfield L. K., Hatfield G. W. Pausing of RNA polymerase during in vitro transcription through the ilvB and ilvGEDA attenuator regions of Escherichia coli K12. J Biol Chem. 1985 Feb 10;260(3):1765–1770. [PubMed] [Google Scholar]
  12. 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 Feb 15;146(1):1–21. doi: 10.1016/0022-2836(81)90363-6. [DOI] [PubMed] [Google Scholar]
  13. 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 Sep 25;151(3):389–409. doi: 10.1016/0022-2836(81)90003-6. [DOI] [PubMed] [Google Scholar]
  14. Lacroute F., Stent G. S. Peptide chain growth of -galactosidase in Escherichia coli. J Mol Biol. 1968 Jul 14;35(1):165–173. doi: 10.1016/s0022-2836(68)80044-0. [DOI] [PubMed] [Google Scholar]
  15. Lawther R. P., Hatfield G. W. Multivalent translational control of transcription termination at attenuator of ilvGEDA operon of Escherichia coli K-12. Proc Natl Acad Sci U S A. 1980 Apr;77(4):1862–1866. doi: 10.1073/pnas.77.4.1862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lee F., Bertrand K., Bennett G., Yanofsky C. Comparison of the nucleotide sequences of the initial transcribed regions of the tryptophan operons of Escherichia coli and Salmonella typhimurium. J Mol Biol. 1978 May 15;121(2):193–217. doi: 10.1016/s0022-2836(78)80005-9. [DOI] [PubMed] [Google Scholar]
  17. Lee F., Yanofsky C. Transcription termination at the trp operon attenuators of Escherichia coli and Salmonella typhimurium: RNA secondary structure and regulation of termination. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4365–4369. doi: 10.1073/pnas.74.10.4365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Manabe T. Theory of regulation by the attenuation mechanism: stochastic model for the attenuation fo the Escherichia coli tryptophan operon. J Theor Biol. 1981 Aug 21;91(4):527–544. doi: 10.1016/0022-5193(81)90210-1. [DOI] [PubMed] [Google Scholar]
  19. Manor H., Goodman D., Stent G. S. RNA chain growth rates in Escherichia coli. J Mol Biol. 1969 Jan 14;39(1):1–29. doi: 10.1016/0022-2836(69)90329-5. [DOI] [PubMed] [Google Scholar]
  20. Miozzari G. F., Yanofsky C. The regulatory region of the trp operon of Serratia marcescens. Nature. 1978 Dec 14;276(5689):684–689. doi: 10.1038/276684a0. [DOI] [PubMed] [Google Scholar]
  21. Morse D. E., Morse A. N. Dual-control of the tryptophan operon is mediated by both tryptophanyl-tRNA synthetase and the repressor. J Mol Biol. 1976 May 15;103(2):209–226. doi: 10.1016/0022-2836(76)90310-7. [DOI] [PubMed] [Google Scholar]
  22. Otsuka J., Kunisawa T. Characteristic base sequence patterns of promoter and terminator sites in phi X174 and fd phage DNAs. J Theor Biol. 1982 Aug 7;97(3):415–436. doi: 10.1016/0022-5193(82)90374-5. [DOI] [PubMed] [Google Scholar]
  23. Oxender D. L., Zurawski G., Yanofsky C. Attenuation in the Escherichia coli tryptophan operon: role of RNA secondary structure involving the tryptophan codon region. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5524–5528. doi: 10.1073/pnas.76.11.5524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Parsot C., Saint-Girons I., Cossart P. DNA sequence change of a deletion mutation abolishing attenuation control of the threonine operon of E. coli K12. Mol Gen Genet. 1982;188(3):455–458. doi: 10.1007/BF00330048. [DOI] [PubMed] [Google Scholar]
  25. Rose J. K., Mosteller R. D., Yanofsky C. Tryptophan messenger ribonucleic acid elongation rates and steady-state levels of tryptophan operon enzymes under various growth conditions. J Mol Biol. 1970 Aug;51(3):541–550. doi: 10.1016/0022-2836(70)90007-0. [DOI] [PubMed] [Google Scholar]
  26. Stauffer G. V., Zurawski G., Yanofsky C. Single base-pair alterations in the Escherichia coli trp operon leader region that relieve transcription termination at the trp attenuator. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4833–4837. doi: 10.1073/pnas.75.10.4833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Steitz J. A., Jakes K. How ribosomes select initiator regions in mRNA: base pair formation between the 3' terminus of 16S rRNA and the mRNA during initiation of protein synthesis in Escherichia coli. Proc Natl Acad Sci U S A. 1975 Dec;72(12):4734–4738. doi: 10.1073/pnas.72.12.4734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Taillon M. P., Gotto D. A., Lawther R. P. The DNA sequence of the promoter-attenuator of the ilvGEDA operon of Salmonella typhimurium. Nucleic Acids Res. 1981 Jul 24;9(14):3419–3432. doi: 10.1093/nar/9.14.3419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Verde P., Frunzio R., di Nocera P. P., Blasi F., Bruni C. B. Identification, nucleotide sequence and expression of the regulatory region of the histidine operon of Escherichia coli K-12. Nucleic Acids Res. 1981 May 11;9(9):2075–2086. doi: 10.1093/nar/9.9.2075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wessler S. R., Calvo J. M. Control of leu operon expression in Escherichia coli by a transcription attenuation mechanism. J Mol Biol. 1981 Jul 15;149(4):579–597. doi: 10.1016/0022-2836(81)90348-x. [DOI] [PubMed] [Google Scholar]
  31. Winkler M. E., Yanofsky C. Pausing of RNA polymerase during in vitro transcription of the tryptophan operon leader region. Biochemistry. 1981 Jun 23;20(13):3738–3744. doi: 10.1021/bi00516a011. [DOI] [PubMed] [Google Scholar]
  32. Yanofsky C. Mutations affecting tRNATrp and its charging and their effect on regulation of transcription termination at the attenuator of the tryptophan operon. J Mol Biol. 1977 Jul 15;113(4):663–677. doi: 10.1016/0022-2836(77)90229-7. [DOI] [PubMed] [Google Scholar]
  33. Zurawski G., Brown K., Killingly D., Yanofsky C. Nucleotide sequence of the leader region of the phenylalanine operon of Escherichia coli. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4271–4275. doi: 10.1073/pnas.75.9.4271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Zurawski G., Elseviers D., Stauffer G. V., Yanofsky C. Translational control of transcription termination at the attenuator of the Escherichia coli tryptophan operon. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5988–5992. doi: 10.1073/pnas.75.12.5988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. von Heijne G. A theoretical study of the attenuation control mechanism. J Theor Biol. 1982 Jul 21;97(2):227–238. doi: 10.1016/0022-5193(82)90100-x. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES