Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1986 Dec;83(24):9333–9337. doi: 10.1073/pnas.83.24.9333

Promoter domain mediates guanosine tetraphosphate activation of the histidine operon.

D L Riggs, R D Mueller, H S Kwan, S W Artz
PMCID: PMC387132  PMID: 3540936

Abstract

We have analyzed the effects of the "alarmone" guanosine 5'-diphosphate 3'-diphosphate (ppGpp) on regulation of the Salmonella typhimurium histidine operon in vitro. Expression of the wild-type promoter, measured in a DNA-dependent transcription-translation system, was strongly dependent on ppGpp; addition of ppGpp stimulated his expression 22-fold with plasmid DNA templates. Oligonucleotide-directed, site-specific mutations that increase the homology of the -10 hexamer to the consensus sequence of the E sigma 70 promoters dramatically increased his expression in the absence of ppGpp and reduced the stimulation to less than a factor of 2. A deletion mutation that alters the sequence between the -10 hexamer and the start point of transcription, generated by BAL-31 nuclease, affected ppGpp regulation in a similar manner. We propose that the -10 hexamer sequence and the adjacent downstream region are both important in regulating transcription by ppGpp. Mechanisms to account for activation and repression of transcription by ppGpp are discussed.

Full text

PDF
9333

Images in this article

9336Image
on p.9336

Selected References

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

  1. Artz S., Holzschu D., Blum P., Shand R. Use of M13mp phages to study gene regulation, structure and function: cloning and recombinational analysis of genes of the Salmonella typhimurium histidine operon. Gene. 1983 Dec;26(2-3):147–158. doi: 10.1016/0378-1119(83)90184-1. [DOI] [PubMed] [Google Scholar]
  2. Bennett G. N., Brown K. D., Yanofsky C. Nucleotide sequence of the promoter--operator region of the tryptophan operon of Salmonella typhimurium. J Mol Biol. 1978 May 15;121(2):139–152. doi: 10.1016/s0022-2836(78)80002-3. [DOI] [PubMed] [Google Scholar]
  3. Borowiec J. A., Gralla J. D. Supercoiling response of the lac ps promoter in vitro. J Mol Biol. 1985 Aug 20;184(4):587–598. doi: 10.1016/0022-2836(85)90305-5. [DOI] [PubMed] [Google Scholar]
  4. Buc H., McClure W. R. Kinetics of open complex formation between Escherichia coli RNA polymerase and the lac UV5 promoter. Evidence for a sequential mechanism involving three steps. Biochemistry. 1985 May 21;24(11):2712–2723. doi: 10.1021/bi00332a018. [DOI] [PubMed] [Google Scholar]
  5. Burton Z. F., Gross C. A., Watanabe K. K., Burgess R. R. The operon that encodes the sigma subunit of RNA polymerase also encodes ribosomal protein S21 and DNA primase in E. coli K12. Cell. 1983 Feb;32(2):335–349. doi: 10.1016/0092-8674(83)90453-1. [DOI] [PubMed] [Google Scholar]
  6. Cassan M., Ronceray J., Patte J. C. Nucleotide sequence of the promoter region of the E. coli lysC gene. Nucleic Acids Res. 1983 Sep 24;11(18):6157–6166. doi: 10.1093/nar/11.18.6157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Duchange N., Zakin M. M., Ferrara P., Saint-Girons I., Park I., Tran S. V., Py M. C., Cohen G. N. Structure of the metJBLF cluster in Escherichia coli K12. Sequence of the metB structural gene and of the 5'- and 3'-flanking regions of the metBL operon. J Biol Chem. 1983 Dec 25;258(24):14868–14871. [PubMed] [Google Scholar]
  8. Fayat G., Mayaux J. F., Sacerdot C., Fromant M., Springer M., Grunberg-Manago M., Blanquet S. Escherichia coli phenylalanyl-tRNA synthetase operon region. Evidence for an attenuation mechanism. Identification of the gene for the ribosomal protein L20. J Mol Biol. 1983 Dec 15;171(3):239–261. doi: 10.1016/0022-2836(83)90092-x. [DOI] [PubMed] [Google Scholar]
  9. Fournier M. J., Ozeki H. Structure and organization of the transfer ribonucleic acid genes of Escherichia coli K-12. Microbiol Rev. 1985 Dec;49(4):379–397. doi: 10.1128/mr.49.4.379-397.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gallant J. A. Stringent control in E. coli. Annu Rev Genet. 1979;13:393–415. doi: 10.1146/annurev.ge.13.120179.002141. [DOI] [PubMed] [Google Scholar]
  11. Gamper H. B., Hearst J. E. A topological model for transcription based on unwinding angle analysis of E. coli RNA polymerase binary, initiation and ternary complexes. Cell. 1982 May;29(1):81–90. doi: 10.1016/0092-8674(82)90092-7. [DOI] [PubMed] [Google Scholar]
  12. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983 Jun 5;166(4):557–580. doi: 10.1016/s0022-2836(83)80284-8. [DOI] [PubMed] [Google Scholar]
  13. Haughn G. W., Squires C. H., De Felice M., Largo C. T., Calvo J. M. Unusual organization of the ilvIH promoter of Escherichia coli. J Bacteriol. 1985 Jul;163(1):186–198. doi: 10.1128/jb.163.1.186-198.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hawley D. K., McClure W. R. Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res. 1983 Apr 25;11(8):2237–2255. doi: 10.1093/nar/11.8.2237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hirschman J., Wong P. K., Sei K., Keener J., Kustu S. Products of nitrogen regulatory genes ntrA and ntrC of enteric bacteria activate glnA transcription in vitro: evidence that the ntrA product is a sigma factor. Proc Natl Acad Sci U S A. 1985 Nov;82(22):7525–7529. doi: 10.1073/pnas.82.22.7525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hsieh T., Wang J. C. Physiochemical studies on interactions between DNA and RNA polymerase. Ultraviolet absorption measurements. Nucleic Acids Res. 1978 Sep;5(9):3337–3345. doi: 10.1093/nar/5.9.3337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hudson G. S., Davidson B. E. Nucleotide sequence and transcription of the phenylalanine and tyrosine operons of Escherichia coli K12. J Mol Biol. 1984 Dec 25;180(4):1023–1051. doi: 10.1016/0022-2836(84)90269-9. [DOI] [PubMed] [Google Scholar]
  18. Kajitani M., Ishihama A. Promoter selectivity of Escherichia coli RNA polymerase. Differential stringent control of the multiple promoters from ribosomal RNA and protein operons. J Biol Chem. 1984 Feb 10;259(3):1951–1957. [PubMed] [Google Scholar]
  19. Kingston R. E., Chamberlin M. J. Pausing and attenuation of in vitro transcription in the rrnB operon of E. coli. Cell. 1981 Dec;27(3 Pt 2):523–531. doi: 10.1016/0092-8674(81)90394-9. [DOI] [PubMed] [Google Scholar]
  20. Kölling R., Lother H. AsnC: an autogenously regulated activator of asparagine synthetase A transcription in Escherichia coli. J Bacteriol. 1985 Oct;164(1):310–315. doi: 10.1128/jb.164.1.310-315.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lamond A. I., Travers A. A. Genetically separable functional elements mediate the optimal expression and stringent regulation of a bacterial tRNA gene. Cell. 1985 Feb;40(2):319–326. doi: 10.1016/0092-8674(85)90146-1. [DOI] [PubMed] [Google Scholar]
  22. Lamond A. I., Travers A. A. Stringent control of bacterial transcription. Cell. 1985 May;41(1):6–8. doi: 10.1016/0092-8674(85)90050-9. [DOI] [PubMed] [Google Scholar]
  23. Little R., Ryals J., Bremer H. rpoB mutation in Escherichia coli alters control of ribosome synthesis by guanosine tetraphosphate. J Bacteriol. 1983 May;154(2):787–792. doi: 10.1128/jb.154.2.787-792.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Malan T. P., Kolb A., Buc H., McClure W. R. Mechanism of CRP-cAMP activation of lac operon transcription initiation activation of the P1 promoter. J Mol Biol. 1984 Dec 25;180(4):881–909. doi: 10.1016/0022-2836(84)90262-6. [DOI] [PubMed] [Google Scholar]
  25. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  26. Mizushima-Sugano J., Kaziro Y. Regulation of the expression of the tufB operon: DNA sequences directly involved in the stringent control. EMBO J. 1985 Apr;4(4):1053–1058. doi: 10.1002/j.1460-2075.1985.tb03738.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nene V., Glass R. E. Relaxed mutants of Escherichia coli RNA polymerase. FEBS Lett. 1983 Mar 21;153(2):307–310. doi: 10.1016/0014-5793(83)80630-9. [DOI] [PubMed] [Google Scholar]
  28. Norrander J., Kempe T., Messing J. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983 Dec;26(1):101–106. doi: 10.1016/0378-1119(83)90040-9. [DOI] [PubMed] [Google Scholar]
  29. Pedersen S., Skouv J., Kajitani M., Ishihama A. Transcriptional organization of the rpsA operon of Escherichia coli. Mol Gen Genet. 1984;196(1):135–140. doi: 10.1007/BF00334105. [DOI] [PubMed] [Google Scholar]
  30. Primakoff P., Artz S. W. Positive control of lac operon expression in vitro by guanosine 5'-diphosphate 3'-diphosphate. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1726–1730. doi: 10.1073/pnas.76.4.1726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Primakoff P. In vivo role of the relA+ gene in regulation of the lac operon. J Bacteriol. 1981 Jan;145(1):410–416. doi: 10.1128/jb.145.1.410-416.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Roe J. H., Burgess R. R., Record M. T., Jr Temperature dependence of the rate constants of the Escherichia coli RNA polymerase-lambda PR promoter interaction. Assignment of the kinetic steps corresponding to protein conformational change and DNA opening. J Mol Biol. 1985 Aug 5;184(3):441–453. doi: 10.1016/0022-2836(85)90293-1. [DOI] [PubMed] [Google Scholar]
  33. Siebenlist U., Simpson R. B., Gilbert W. E. coli RNA polymerase interacts homologously with two different promoters. Cell. 1980 Jun;20(2):269–281. doi: 10.1016/0092-8674(80)90613-3. [DOI] [PubMed] [Google Scholar]
  34. Simons R. W., Hoopes B. C., McClure W. R., Kleckner N. Three promoters near the termini of IS10: pIN, pOUT, and pIII. Cell. 1983 Sep;34(2):673–682. doi: 10.1016/0092-8674(83)90400-2. [DOI] [PubMed] [Google Scholar]
  35. Stephens J. C., Artz S. W., Ames B. N. Guanosine 5'-diphosphate 3'-diphosphate (ppGpp): positive effector for histidine operon transcription and general signal for amino-acid deficiency. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4389–4393. doi: 10.1073/pnas.72.11.4389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Stragier P., Danos O., Patte J. C. Regulation of diaminopimelate decarboxylase synthesis in Escherichia coli. II. Nucleotide sequence of the lysA gene and its regulatory region. J Mol Biol. 1983 Aug 5;168(2):321–331. doi: 10.1016/s0022-2836(83)80021-7. [DOI] [PubMed] [Google Scholar]
  37. Takata R., Mukai T., Hori K. Attenuation and processing of RNA from the rpsO-pnp transcription unit of Escherichia coli. Nucleic Acids Res. 1985 Oct 25;13(20):7289–7297. doi: 10.1093/nar/13.20.7289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Travers A. A. A tRNATyr promoter with an altered in vitro response to ppgpp. J Mol Biol. 1980 Jul 25;141(1):91–97. doi: 10.1016/s0022-2836(80)80030-1. [DOI] [PubMed] [Google Scholar]
  39. Travers A. A. Conserved features of coordinately regulated E. coli promoters. Nucleic Acids Res. 1984 Mar 26;12(6):2605–2618. doi: 10.1093/nar/12.6.2605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Turnbough C. L., Jr, Hicks K. L., Donahue J. P. Attenuation control of pyrBI operon expression in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1983 Jan;80(2):368–372. doi: 10.1073/pnas.80.2.368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Urdea M. S., Merryweather J. P., Mullenbach G. T., Coit D., Heberlein U., Valenzuela P., Barr P. J. Chemical synthesis of a gene for human epidermal growth factor urogastrone and its expression in yeast. Proc Natl Acad Sci U S A. 1983 Dec;80(24):7461–7465. doi: 10.1073/pnas.80.24.7461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wallace R. B., Johnson M. J., Suggs S. V., Miyoshi K., Bhatt R., Itakura K. A set of synthetic oligodeoxyribonucleotide primers for DNA sequencing in the plasmid vector pBR322. Gene. 1981 Dec;16(1-3):21–26. doi: 10.1016/0378-1119(81)90057-3. [DOI] [PubMed] [Google Scholar]
  43. Yanofsky C. Attenuation in the control of expression of bacterial operons. Nature. 1981 Feb 26;289(5800):751–758. doi: 10.1038/289751a0. [DOI] [PubMed] [Google Scholar]
  44. Zoller M. J., Smith M. Oligonucleotide-directed mutagenesis of DNA fragments cloned into M13 vectors. Methods Enzymol. 1983;100:468–500. doi: 10.1016/0076-6879(83)00074-9. [DOI] [PubMed] [Google Scholar]
  45. von Hippel P. H., Bear D. G., Morgan W. D., McSwiggen J. A. Protein-nucleic acid interactions in transcription: a molecular analysis. Annu Rev Biochem. 1984;53:389–446. doi: 10.1146/annurev.bi.53.070184.002133. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES