Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1990 Jun;172(6):3201–3207. doi: 10.1128/jb.172.6.3201-3207.1990

Regulation of Escherichia coli pyrC by the purine regulon repressor protein.

K Y Choi 1, H Zalkin 1
PMCID: PMC209125  PMID: 1971620

Abstract

The purine regulon repressor, PurR, was identified as a component of the Escherichia coli regulatory system for pyrC, the gene that encodes dihydroorotase, an enzyme in de novo pyrimidine nucleotide synthesis. PurR binds to a pyrC control site that resembles a pur regulon operator and represses expression by twofold. Mutations that increase binding of PurR to the control site in vitro concomitantly increase in vivo regulation. There are completely independent mechanisms for regulation of pyrC by purine and pyrimidine nucleotides. Cross pathway regulation of pyrC by PurR may provide one mechanism to coordinate synthesis of purine and pyrimidine nucleotides.

Full text

PDF
3206

Images in this article

Selected References

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

  1. Bonekamp F., Clemmesen K., Karlström O., Jensen K. F. Mechanism of UTP-modulated attenuation at the pyrE gene of Escherichia coli: an example of operon polarity control through the coupling of translation to transcription. EMBO J. 1984 Dec 1;3(12):2857–2861. doi: 10.1002/j.1460-2075.1984.tb02220.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bower S. G., Hove-Jensen B., Switzer R. L. Structure of the gene encoding phosphoribosylpyrophosphate synthetase (prsA) in Salmonella typhimurium. J Bacteriol. 1988 Jul;170(7):3243–3248. doi: 10.1128/jb.170.7.3243-3248.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bussey L. B., Ingraham J. L. Isolation and mapping of a uracil-sensitive mutant of Salmonella typhimurium. Mol Gen Genet. 1982;185(3):513–514. doi: 10.1007/BF00334151. [DOI] [PubMed] [Google Scholar]
  4. Clemmesen K., Bonekamp F., Karlström O., Jensen K. F. Role of translation in the UTP-modulated attenuation at the pyrBI operon of Escherichia coli. Mol Gen Genet. 1985;201(2):247–251. doi: 10.1007/BF00425666. [DOI] [PubMed] [Google Scholar]
  5. Cunin R., Glansdorff N., Piérard A., Stalon V. Biosynthesis and metabolism of arginine in bacteria. Microbiol Rev. 1986 Sep;50(3):314–352. doi: 10.1128/mr.50.3.314-352.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Hove-Jensen B., Harlow K. W., King C. J., Switzer R. L. Phosphoribosylpyrophosphate synthetase of Escherichia coli. Properties of the purified enzyme and primary structure of the prs gene. J Biol Chem. 1986 May 25;261(15):6765–6771. [PubMed] [Google Scholar]
  7. Jensen K. F. Apparent involvement of purines in the control of expression of Salmonella typhimurium pyr genes: analysis of a leaky guaB mutant resistant to pyrimidine analogs. J Bacteriol. 1979 Jun;138(3):731–738. doi: 10.1128/jb.138.3.731-738.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Jensen K. F. Regulation of Salmonella typhimurium pyr gene expression: effect of changing both purine and pyrimidine nucleotide pools. J Gen Microbiol. 1989 Apr;135(4):805–815. doi: 10.1099/00221287-135-4-805. [DOI] [PubMed] [Google Scholar]
  9. Kilstrup M., Lu C. D., Abdelal A., Neuhard J. Nucleotide sequence of the carA gene and regulation of the carAB operon in Salmonella typhimurium. Eur J Biochem. 1988 Sep 15;176(2):421–429. doi: 10.1111/j.1432-1033.1988.tb14299.x. [DOI] [PubMed] [Google Scholar]
  10. Kilstrup M., Meng L. M., Neuhard J., Nygaard P. Genetic evidence for a repressor of synthesis of cytosine deaminase and purine biosynthesis enzymes in Escherichia coli. J Bacteriol. 1989 Apr;171(4):2124–2127. doi: 10.1128/jb.171.4.2124-2127.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
  12. Larsen J. N., Jensen K. F. Nucleotide sequence of the pyrD gene of Escherichia coli and characterization of the flavoprotein dihydroorotate dehydrogenase. Eur J Biochem. 1985 Aug 15;151(1):59–65. doi: 10.1111/j.1432-1033.1985.tb09068.x. [DOI] [PubMed] [Google Scholar]
  13. Levin H. L., Park K., Schachman H. K. Attenuation in the regulation of the pyrBI operon in Escherichia coli. In vivo studies of transcriptional termination. J Biol Chem. 1989 Sep 5;264(25):14638–14645. [PubMed] [Google Scholar]
  14. Levin H. L., Schachman H. K. Regulation of aspartate transcarbamoylase synthesis in Escherichia coli: analysis of deletion mutations in the promoter region of the pyrBI operon. Proc Natl Acad Sci U S A. 1985 Jul;82(14):4643–4647. doi: 10.1073/pnas.82.14.4643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Liu C. G., Turnbough C. L., Jr Multiple control mechanisms for pyrimidine-mediated regulation of pyrBI operon expression in Escherichia coli K-12. J Bacteriol. 1989 Jun;171(6):3337–3342. doi: 10.1128/jb.171.6.3337-3342.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Makaroff C. A., Zalkin H. Regulation of Escherichia coli purF. Analysis of the control region of a pur regulon gene. J Biol Chem. 1985 Aug 25;260(18):10378–10387. [PubMed] [Google Scholar]
  17. Navre M., Schachman H. K. Synthesis of aspartate transcarbamoylase in Escherichia coli: transcriptional regulation of the pyrB-pyrI operon. Proc Natl Acad Sci U S A. 1983 Mar;80(5):1207–1211. doi: 10.1073/pnas.80.5.1207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nowlan S. F., Kantrowitz E. R. Identification of a trans-acting regulatory factor involved in the control of the pyrimidine pathway in E. coli. Mol Gen Genet. 1983;192(1-2):264–271. doi: 10.1007/BF00327676. [DOI] [PubMed] [Google Scholar]
  19. Piette J., Nyunoya H., Lusty C. J., Cunin R., Weyens G., Crabeel M., Charlier D., Glansdorff N., Piérard A. DNA sequence of the carA gene and the control region of carAB: tandem promoters, respectively controlled by arginine and the pyrimidines, regulate the synthesis of carbamoyl-phosphate synthetase in Escherichia coli K-12. Proc Natl Acad Sci U S A. 1984 Jul;81(13):4134–4138. doi: 10.1073/pnas.81.13.4134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Piérard A., Glansdorff N., Gigot D., Crabeel M., Halleux P., Thiry L. Repression of Escherichia coli carbamoylphosphate synthase: relationships with enzyme synthesis in the arginine and pyrimidine pathways. J Bacteriol. 1976 Jul;127(1):291–301. doi: 10.1128/jb.127.1.291-301.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Poulsen P., Bonekamp F., Jensen K. F. Structure of the Escherichia coli pyrE operon and control of pyrE expression by a UTP modulated intercistronic attentuation. EMBO J. 1984 Aug;3(8):1783–1790. doi: 10.1002/j.1460-2075.1984.tb02046.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Roland K. L., Powell F. E., Turnbough C. L., Jr Role of translation and attenuation in the control of pyrBI operon expression in Escherichia coli K-12. J Bacteriol. 1985 Sep;163(3):991–999. doi: 10.1128/jb.163.3.991-999.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rolfes R. J., Zalkin H. Escherichia coli gene purR encoding a repressor protein for purine nucleotide synthesis. Cloning, nucleotide sequence, and interaction with the purF operator. J Biol Chem. 1988 Dec 25;263(36):19653–19661. [PubMed] [Google Scholar]
  24. Rolfes R. J., Zalkin H. Regulation of Escherichia coli purF. Mutations that define the promoter, operator, and purine repressor gene. J Biol Chem. 1988 Dec 25;263(36):19649–19652. [PubMed] [Google Scholar]
  25. Roof W. D., Foltermann K. F., Wild J. R. The organization and regulation of the pyrBI operon in E. coli includes a rho-independent attenuator sequence. Mol Gen Genet. 1982;187(3):391–400. doi: 10.1007/BF00332617. [DOI] [PubMed] [Google Scholar]
  26. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Schendel F. J., Mueller E., Stubbe J., Shiau A., Smith J. M. Formylglycinamide ribonucleotide synthetase from Escherichia coli: cloning, sequencing, overproduction, isolation, and characterization. Biochemistry. 1989 Mar 21;28(6):2459–2471. doi: 10.1021/bi00432a017. [DOI] [PubMed] [Google Scholar]
  28. Schwartz M., Neuhard J. Control of expression of the pyr genes in Salmonella typhimurium: effects of variations in uridine and cytidine nucleotide pools. J Bacteriol. 1975 Mar;121(3):814–822. doi: 10.1128/jb.121.3.814-822.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Smith J. M., Daum H. A., 3rd Nucleotide sequence of the purM gene encoding 5'-phosphoribosyl-5-aminoimidazole synthetase of Escherichia coli K12. J Biol Chem. 1986 Aug 15;261(23):10632–10636. [PubMed] [Google Scholar]
  30. Tiedeman A. A., Keyhani J., Kamholz J., Daum H. A., 3rd, Gots J. S., Smith J. M. Nucleotide sequence analysis of the purEK operon encoding 5'-phosphoribosyl-5-aminoimidazole carboxylase of Escherichia coli K-12. J Bacteriol. 1989 Jan;171(1):205–212. doi: 10.1128/jb.171.1.205-212.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  33. Watanabe W., Sampei G., Aiba A., Mizobuchi K. Identification and sequence analysis of Escherichia coli purE and purK genes encoding 5'-phosphoribosyl-5-amino-4-imidazole carboxylase for de novo purine biosynthesis. J Bacteriol. 1989 Jan;171(1):198–204. doi: 10.1128/jb.171.1.198-204.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wilson H. R., Chan P. T., Turnbough C. L., Jr Nucleotide sequence and expression of the pyrC gene of Escherichia coli K-12. J Bacteriol. 1987 Jul;169(7):3051–3058. doi: 10.1128/jb.169.7.3051-3058.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES