Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1975 Dec;124(3):1366–1373. doi: 10.1128/jb.124.3.1366-1373.1975

Derepression and repression of the histidine operon: role of the feedback site of the first enzyme.

V M Fernández, R Martíndelrío, A R Tébar, J M Guisán, A O Ballesteros
PMCID: PMC236049  PMID: 1104584

Abstract

Thiazolealanine, a false feedback inhibitor, causes transient repression of the his operon previously derepressed by a severe histidine limitation in strains with a wild-type or feedback-hypersensitive first enzyme but not in feedback-resistant mutants. Since experiments reported here clearly demonstrate that thiazolealanine is not transferred to tRNAHis, it is proposed that this "transient repression" is effected through the interaction of thiazolealanine with the feedback site of the enzyme. Experiments in the presence of rifampin indicate that this thiazolealanine-mediated effect is exerted at the level of translation. We conclude that histidine (free), in addition to forming co-repressor, also represses the operon at the level of translation through feedback interaction with the first enzyme of the pathway (adenosine 5'-triphosphate phosphoribosyltransferase). Rates of derepression in feedback-resistant strains are roughly half of those observed in controls, suggesting a positive role played by a first enzyme with a normal but unoccupied feedback site. Some feedback-resistant mutants, in contrast to the wild type, were unable to exhibit derepression under histidine limitation caused by aminotriazole.

Full text

PDF
1366

Selected References

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

  1. AMES B. N., MARTIN R. G., GARRY B. J. The first step of histidine biosynthesis. J Biol Chem. 1961 Jul;236:2019–2026. [PubMed] [Google Scholar]
  2. Ames B. N., Garry B. COORDINATE REPRESSION OF THE SYNTHESIS OF FOUR HISTIDINE BIOSYNTHETIC ENZYMES BY HISTIDINE. Proc Natl Acad Sci U S A. 1959 Oct;45(10):1453–1461. doi: 10.1073/pnas.45.10.1453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BERG P., LAGERKVIST U., DIECKMANN M. The enzymic synthesis of amino acyl derivatives of ribonucleic acid. VI. Nucleotide sequences adjacent to the ... pCpCpA end groups of isoleucine- and leucine-specific chains. J Mol Biol. 1962 Aug;5:159–171. doi: 10.1016/s0022-2836(62)80081-3. [DOI] [PubMed] [Google Scholar]
  4. Bollon A. P. Fine structure analysis of a eukaryotic multifunctional gene. Nature. 1974 Aug 23;250(5468):630–634. doi: 10.1038/250630a0. [DOI] [PubMed] [Google Scholar]
  5. Bollon A. P., Magee P. T. Involvement of threonine deaminase in multivalent repression of the isoleucine-valine pathway in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1971 Sep;68(9):2169–2172. doi: 10.1073/pnas.68.9.2169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bollon A. P., Magee P. T. Involvement of threonine deaminase in repression of the isoleucine-valine and leucine pathways in Saccharomyces cerevisiae. J Bacteriol. 1973 Mar;113(3):1333–1344. doi: 10.1128/jb.113.3.1333-1344.1973. [DOI] [PMC free article] [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. Folk W. R., Berg P. Characterization of altered forms of glycyl transfer ribonucleic acid synthetase and the effects of such alterations on aminoacyl transfer ribonucleic acid synthesis in vivo. J Bacteriol. 1970 Apr;102(1):204–212. doi: 10.1128/jb.102.1.204-212.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Freundlich M. Valyl-Transfer RNA: Role in Repression of the Isoleucine-Valine Enzymes in Escherichia coli. Science. 1967 Aug 18;157(3790):823–825. doi: 10.1126/science.157.3790.823-a. [DOI] [PubMed] [Google Scholar]
  10. Hartman P. E., Hartman Z., Stahl R. C. Classification and mapping of spontaneous and induced mutations in the histidine operon of Salmonella. Adv Genet. 1971;16:1–34. doi: 10.1016/s0065-2660(08)60352-1. [DOI] [PubMed] [Google Scholar]
  11. Hatfield G. W., Burns R. O. Specific binding of leucyl transfer RNA to an immature form of L-threonine deaminase: its implications in repression. Proc Natl Acad Sci U S A. 1970 Aug;66(4):1027–1035. doi: 10.1073/pnas.66.4.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hilton J. L., Kearney P. C., Ames B. N. Mode of action of the herbicide, 3-amino-1,2,4-triazole(amitrole): inhibition of an enzyme of histidine biosynthesis. Arch Biochem Biophys. 1965 Dec;112(3):544–547. doi: 10.1016/0003-9861(65)90093-7. [DOI] [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. JACOB F., MONOD J. Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol. 1961 Jun;3:318–356. doi: 10.1016/s0022-2836(61)80072-7. [DOI] [PubMed] [Google Scholar]
  15. Kasai T. Regulation of the expression of the histidine operon in Salmonella typhimurium. Nature. 1974 Jun 7;249(457):523–527. doi: 10.1038/249523a0. [DOI] [PubMed] [Google Scholar]
  16. Kovach J. S., Ballesteros A. O., Meyers M., Soria M., Goldberger R. F. A cis-trans test of the effect of the first enzyme for histidine biosynthesis on regulation of the histidine operon. J Bacteriol. 1973 Apr;114(1):351–356. doi: 10.1128/jb.114.1.351-356.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kovach J. S., Berberich M. A., Venetianer P., Goldberger R. F. Repression of the histidine operon: effect of the first enzyme on the kinetics of repression. J Bacteriol. 1969 Mar;97(3):1283–1290. doi: 10.1128/jb.97.3.1283-1290.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kovach J. S., Phang J. M., Blasi F., Barton R. W., Ballesteros-Olmo A., Goldberger R. F. Interaction between histidyl transfer ribonucleic acid and the first enzyme for histidine biosynthesis of Salmonella typhimurium. J Bacteriol. 1970 Nov;104(2):787–792. doi: 10.1128/jb.104.2.787-792.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kovach J. S., Phang J. M., Ference M., Goldberger R. F. Studies on repression of the histidine operon. II. The role of the first enzyme in control of the histidine system. Proc Natl Acad Sci U S A. 1969 Jun;63(2):481–488. doi: 10.1073/pnas.63.2.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. LEVIN A. P., HARTMAN P. E. ACTION OF A HISTIDINE ANALOGUE, 1,2,4-TRIAZOLE-3-ALANINE, IN SALMONELLA TYPHIMURIUM. J Bacteriol. 1963 Oct;86:820–828. doi: 10.1128/jb.86.4.820-828.1963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. 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]
  24. Leisinger T., Vogel R. H., Vogel H. J. Repression-dependent alteration of an arginine enzyme in Escherichia coli. Proc Natl Acad Sci U S A. 1969 Oct;64(2):686–692. doi: 10.1073/pnas.64.2.686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Levinthal M., Williams L. S., Umbarger H. E. Role of threonine deaminase in the regulation of isoleucine and valine biosynthesis. Nat New Biol. 1973 Nov 21;246(151):65–68. doi: 10.1038/newbio246065a0. [DOI] [PubMed] [Google Scholar]
  26. Lewis J. A., Ames B. N. Histidine regulation in Salmonella typhimurium. XI. The percentage of transfer RNA His charged in vivo and its relation to the repression of the histidine operon. J Mol Biol. 1972 Apr 28;66(1):131–142. doi: 10.1016/s0022-2836(72)80011-1. [DOI] [PubMed] [Google Scholar]
  27. MOYED H. S. Interference with the feed-back control of histidine biosynthesis. J Biol Chem. 1961 Aug;236:2261–2267. [PubMed] [Google Scholar]
  28. McLellan W. L., Vogel H. J. Translational repression in the arginine system of Escherichia coli. Proc Natl Acad Sci U S A. 1970 Dec;67(4):1703–1709. doi: 10.1073/pnas.67.4.1703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. PARDEE A. B., YATES R. A. Control of pyrimidine biosynthesis in Escherichia coli by a feed-back mechanism. J Biol Chem. 1956 Aug;221(2):757–770. [PubMed] [Google Scholar]
  30. Patthy L., Dénes G. Altered repression behaviour in a feedback insensitive mutant of Escherichia coli K12. Acta Biochim Biophys Acad Sci Hung. 1970;5(2):147–157. [PubMed] [Google Scholar]
  31. 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]
  32. Roth J. R., Silbert D. F., Fink G. R., Voll M. J., Antón D., Hartman P. E., Ames B. N. Transfer RNA and the control of the histidine operon. Cold Spring Harb Symp Quant Biol. 1966;31:383–392. doi: 10.1101/sqb.1966.031.01.050. [DOI] [PubMed] [Google Scholar]
  33. Rothman-Denes L., Martin R. G. Two mutations in the first gene of the histidine operon of Salmonella typhimurium affecting control. J Bacteriol. 1971 Apr;106(1):227–237. doi: 10.1128/jb.106.1.227-237.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. SHEPPARD D. E. MUTANTS OF SALMONELLA TYPHIMURIUM RESISTANT TO FEEDBACK INHIBITION BY L-HISTIDINE. Genetics. 1964 Oct;50:611–623. doi: 10.1093/genetics/50.4.611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. SOMERVILLE R. L., YANOFSKY C. STUDIES ON THE REGULATION OF TRYPTOPHAN BIOSYNTHESIS IN ESCHERICHIA COLI. J Mol Biol. 1965 Apr;11:747–759. doi: 10.1016/s0022-2836(65)80032-8. [DOI] [PubMed] [Google Scholar]
  37. St Pierre M. L. Mutations creating a new initiation point for expression of the histidine operon in Salmonella typhimurium. J Mol Biol. 1968 Jul 14;35(1):71–82. doi: 10.1016/s0022-2836(68)80037-3. [DOI] [PubMed] [Google Scholar]
  38. Stieglitz B., Calvo J. M. Effect of 4-azaleucine upon leucine metabolism in Salmonella typhimurium. J Bacteriol. 1971 Oct;108(1):95–104. doi: 10.1128/jb.108.1.95-104.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Szentirmai A., Szentirmai M., Umbarger H. E. Isoleucine and valine metabolism of Escherichia coli. XV. Biochemical properties of mutants resistant to thiaisoleucine. J Bacteriol. 1968 May;95(5):1672–1679. doi: 10.1128/jb.95.5.1672-1679.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. UMBARGER H. E. Evidence for a negative-feedback mechanism in the biosynthesis of isoleucine. Science. 1956 May 11;123(3202):848–848. doi: 10.1126/science.123.3202.848. [DOI] [PubMed] [Google Scholar]
  41. 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]
  42. Wasmuth J. J., Umbarger H. E. Role for free isoleucine of glycyl-leucine in the repression of threonine deaminase in Escherichia coli. J Bacteriol. 1974 Jan;117(1):29–39. doi: 10.1128/jb.117.1.29-39.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Yaniv M., Jacob F., Gros F. Mutations thermosensibles des systèmes activant la valine chez E. coli. Bull Soc Chim Biol (Paris) 1965;47(8):1609–1626. [PubMed] [Google Scholar]

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

RESOURCES