Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1972 Oct;112(1):102–113. doi: 10.1128/jb.112.1.102-113.1972

Repression of Enzymes of Arginine Biosynthesis by l-Canavanine in Arginyl-Transfer Ribonucleic Acid Synthetase Mutants of Escherichia coli

Ronald Faanes 1, Palmer Rogers 1
PMCID: PMC251385  PMID: 4562386

Abstract

We show that the arginine analogue, l-canavanine, repressed the accumulation of translatable messenger ribonucleic acid (RNA) for three arginine biosynthetic enzymes in Escherichia coli. The method used to determine the level of translatable messenger RNA depended upon measurement of a burst of enzyme synthesis as described previously. E. coli strains with defective arginyltransfer ribonucleic acid (tRNA) synthetase (argS mutants) were insensitive to canavanine repression. When deprived of leucine, a leu argS strain regained normal sensitivity to canavanine repression. The level of in vivo canavanyl-tRNAarg was determined for a normal strain and an argS mutant. After 20 min of growth with canavanine only 9% of tRNAarg from the argS strain was protected from periodate oxidation, while 42% of the tRNAarg from an argS+ strain was charged. When deprived of leucine, leu argS or leu argS+ strains grown with canavanine contained more than 60% charged tRNAarg. Reverse phase column chromatography of periodate-oxidized tRNA from canavanine-grown argS and argS+ strains showed no preferential charging of any isoaccepting species of tRNAarg. Therefore, we failed to detect a specific arginyl-tRNA species that might be involved in repression by canavanine. However, the data suggest that canavanine repression of the arginine pathway occurs only when high levels of canavanyl-tRNA are present, and thus support the notion that arginyl-tRNA synthetase plays a role in generating a repression signal.

Full text

PDF
102

Selected References

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

  1. Alexander R. R., Calvo J. M., Freundlich M. Mutants of Salmonella typhimurium with an altered leucyl-transfer ribonucleic acid synthetase. J Bacteriol. 1971 Apr;106(1):213–220. doi: 10.1128/jb.106.1.213-220.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Celis T. F., Maas W. K. Studies on the mechanism of repression of arginine biosynthesis in Escherichia coli. IV. Further studies on the role of arginine transfer RNA repression of the enzymes of arginine biosynthesis. J Mol Biol. 1971 Nov 28;62(1):179–188. doi: 10.1016/0022-2836(71)90138-0. [DOI] [PubMed] [Google Scholar]
  3. DAVIS B. D., MINGIOLI E. S. Mutants of Escherichia coli requiring methionine or vitamin B12. J Bacteriol. 1950 Jul;60(1):17–28. doi: 10.1128/jb.60.1.17-28.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Demerec M., Adelberg E. A., Clark A. J., Hartman P. E. A proposal for a uniform nomenclature in bacterial genetics. Genetics. 1966 Jul;54(1):61–76. doi: 10.1093/genetics/54.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dwyer S. B., Umbarger H. E. Isoleucine and valine metabolism of Escherichia coli. XVI. Pattern of multivalent repression in strain K-12. J Bacteriol. 1968 May;95(5):1680–1684. doi: 10.1128/jb.95.5.1680-1684.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. EDLIN G. GENE REGULATION DURING BACTERIOPHAGE T4 DEVLOPMENT. I. PHENOTYPIC REVERSION OF T4 AMBER MUTANTS BY 5-FLUOROURACIL. J Mol Biol. 1965 Jun;12:363–374. doi: 10.1016/s0022-2836(65)80260-1. [DOI] [PubMed] [Google Scholar]
  7. EIDLIC L., NEIDHARDT F. C. ROLE OF VALYL-SRNA SYNTHETASE IN ENZYME REPRESSION. Proc Natl Acad Sci U S A. 1965 Mar;53:539–543. doi: 10.1073/pnas.53.3.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Faanes R., Rogers P. Roles of arginine and canavanine in the synthesis and repression of ornithine transcarbamylase by Escherichia coli. J Bacteriol. 1968 Aug;96(2):409–420. doi: 10.1128/jb.96.2.409-420.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hirshfield I. N., Bloemers H. P. The biochemical characterization of two mutant arginyl transfer ribonucleic acid synthetases from Escherichia coli K-12. J Biol Chem. 1969 Jun 10;244(11):2911–2916. [PubMed] [Google Scholar]
  10. Hirshfield I. N., Horn P. C., Hopwood D. A., Maas W. K., DeDeken R. Studies on the mechanism of repression of arginine biosynthesis in Escherichia coli. 3. Repression of enzymes of arginine biosynthesis in arginyl-tRNA synthetase mutants. J Mol Biol. 1968 Jul 14;35(1):83–93. doi: 10.1016/s0022-2836(68)80038-5. [DOI] [PubMed] [Google Scholar]
  11. Iaccarino M., Berg P. Isoleucine auxotrophy as a consequence of a mutationally altered isoleucyl-transfer ribonucleic acid synthetase. J Bacteriol. 1971 Feb;105(2):527–537. doi: 10.1128/jb.105.2.527-537.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ito K., Hiraga S., Yura T. Temperature-sensitive repression of the tryptophan operon in Escherichia coli. J Bacteriol. 1969 Jul;99(1):279–286. doi: 10.1128/jb.99.1.279-286.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ito K., Hiraga S., Yura T. Tryptophanyl transfer RNA synthetase and expression of the tryptophan operon in the trpS mutants of Escherichia coli. Genetics. 1969 Mar;61(3):521–538. doi: 10.1093/genetics/61.3.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Krzyzek R., Rogers P. Arginine control of transcription of argECBH messenger ribonucleic acid in Escherichia coli. J Bacteriol. 1972 Jun;110(3):945–954. doi: 10.1128/jb.110.3.945-954.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  16. LUBIN M. Enrichment of auxotrophic mutant populations by recycling. J Bacteriol. 1962 Mar;83:696–697. doi: 10.1128/jb.83.3.696-697.1962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lavallé R., De Hauwer G. Tryptophan messenger translation in Escherichia coli. J Mol Biol. 1970 Jul 28;51(2):435–447. doi: 10.1016/0022-2836(70)90153-1. [DOI] [PubMed] [Google Scholar]
  18. Lavallé R. Regulation at the level of translation in the arginine pathway of Escherichia coli K12. J Mol Biol. 1970 Jul 28;51(2):449–451. doi: 10.1016/0022-2836(70)90154-3. [DOI] [PubMed] [Google Scholar]
  19. Mosteller R. D., Yanofsky C. Evidence that tryptophanyl transfer ribonucleic acid is not the corepressor of the tryptophan operon of Escherichia coli. J Bacteriol. 1971 Jan;105(1):268–275. doi: 10.1128/jb.105.1.268-275.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. NISHIMURA S., NOVELLI G. D. AMINO ACID ACCEPTOR ACTIVITY OF ENZYMICALLY ALTERED SOLUBLE RNA FROM ESCHERICHIA COLI. Biochim Biophys Acta. 1964 Apr 27;80:574–586. doi: 10.1016/0926-6550(64)90302-0. [DOI] [PubMed] [Google Scholar]
  21. NOVICK R. P., MAAS W. K. Control by endogenously synthesized arginine of the formation of ornithine transcarbamylase in Escherichia coli. J Bacteriol. 1961 Feb;81:236–240. doi: 10.1128/jb.81.2.236-240.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nass G., Poralla K., Zähner H. Effect of the antibiotic Borrelidin on the regulation of threonine biosynthetic enzymes in E. coli. Biochem Biophys Res Commun. 1969 Jan 6;34(1):84–91. doi: 10.1016/0006-291x(69)90532-4. [DOI] [PubMed] [Google Scholar]
  23. ROGERS P., NOVELLI G. D. Formation of ornithine transcarbamylase in cells and protoplasts of Escherichia coli. Biochim Biophys Acta. 1959 Jun;33(2):423–436. doi: 10.1016/0006-3002(59)90132-5. [DOI] [PubMed] [Google Scholar]
  24. Ravel J. M., White M. N., Shive W. Activation of tyrosine analogs in relation to enzyme repression. Biochem Biophys Res Commun. 1965 Jul 26;20(3):352–359. doi: 10.1016/0006-291x(65)90372-4. [DOI] [PubMed] [Google Scholar]
  25. Rogers P., Krzyzek R., Kaden T. M., Arfman E. Effect of arginine and canavanine on arginine messenger RNA synthesis. Biochem Biophys Res Commun. 1971 Sep;44(5):1220–1226. doi: 10.1016/s0006-291x(71)80216-4. [DOI] [PubMed] [Google Scholar]
  26. Roth J. R., Ames B. N. Histidine regulatory mutants in Salmonella typhimurium II. Histidine regulatory mutants having altered histidyl-tRNA synthetase. J Mol Biol. 1966 Dec 28;22(2):325–333. doi: 10.1016/0022-2836(66)90135-5. [DOI] [PubMed] [Google Scholar]
  27. SCHLESINGER S., MAGASANIK B. EFFECT OF ALPHA-METHYLHISTIDINE ON THE CONTROL OF HISTIDINE SYNTHESIS. J Mol Biol. 1964 Sep;9:670–682. doi: 10.1016/s0022-2836(64)80174-1. [DOI] [PubMed] [Google Scholar]
  28. Schachtele C. F., Anderson D. L., Rogers P. Mechanism of canavanine death in Escherichia coli. II. Membranes-bound canavanyl-protein and nuclear disruption. J Mol Biol. 1968 May 14;33(3):861–872. doi: 10.1016/0022-2836(68)90324-0. [DOI] [PubMed] [Google Scholar]
  29. Schachtele C. F., Rogers P. Canavanine death in Escherichia coli. J Mol Biol. 1965 Dec;14(2):474–489. doi: 10.1016/s0022-2836(65)80197-8. [DOI] [PubMed] [Google Scholar]
  30. Umbarger H. E. Regulation of amino acid metabolism. Annu Rev Biochem. 1969;38:323–370. doi: 10.1146/annurev.bi.38.070169.001543. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Waters L. C., Novelli G. D. The early change in E. coli leucine tRNA after infection with bacteriophage T2. Biochem Biophys Res Commun. 1968 Sep 30;32(6):971–976. doi: 10.1016/0006-291x(68)90123-x. [DOI] [PubMed] [Google Scholar]
  33. Weiss J. F., Kelmers A. D. A new chromatographic system for increased resolution of transfer ribonucleic acids. Biochemistry. 1967 Aug;6(8):2507–2513. doi: 10.1021/bi00860a030. [DOI] [PubMed] [Google Scholar]
  34. Wilson O. H., Holden J. T. Arginine transport and metabolism in osmotically shocked and unshocked cells of Escherichia coli W. J Biol Chem. 1969 May 25;244(10):2737–2742. [PubMed] [Google Scholar]
  35. Yang W. K., Novelli G. D. Isoaccepting +RNA's in mouse plasma cell tumors that synthesize different myeloma protein. Biochem Biophys Res Commun. 1968 May 23;31(4):534–539. doi: 10.1016/0006-291x(68)90510-x. [DOI] [PubMed] [Google Scholar]

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

RESOURCES