1887

Abstract

Repression of tryptophanase (tryptophan indole-lyase) by glucose and its non-metabolizable analogue methyl α-glucoside has been studied employing a series of isogenic strains of lacking cyclic AMP phosphodiesterase and altered for two of the proteins of the phosphoenolpyruvate:sugar phosphotransferase system (PTS), Enzyme I and Enzyme IIA. Basal activity of tryptophanase was depressed mildly by inclusion of glucose in the growth medium, but inducible tryptophanase synthesis was subject to strong glucose repression in the parental strain, which exhibited normal PTS enzyme activities. Methyl α-glucoside was without effect in this strain. Loss of Enzyme I decreased sensitivity to repression by glucose but enhanced sensitivity to repression by methyl α-glucoside. Loss of Enzyme IIA activity largely abolished repression by methyl α-glucoside but had a less severe effect on glucose repression. The repressive effects of both sugars were fully reversed by inclusion of cyclic AMP in the growth medium. Tryptophan uptake under the same conditions was inhibited weakly by glucose and more strongly by methyl α-glucoside in the parental strain. Inhibition by both sugars was alleviated by partial loss of Enzyme I. Inhibition by methyl α-glucoside appeared to be largely due to energy competition and was not responsible for repression of tryptophanase synthesis. Measurement of net production of cyclic AMP as well as intracellular concentrations of cyclic AMP revealed a good correlation with intensity of repression. The results suggest that while basal tryptophanase synthesis is relatively insensitive to catabolite repression, inducible synthesis is subject to strong repression by two distinct mechanisms, one dependent on enzyme IIA of the PTS and the other independent of this protein. Both mechanisms are attributable to depressed rates of cyclic AMP synthesis. No evidence for a cyclic-AMP-independent mechanism of catabolite repression was obtained.

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1994-08-01
2021-07-31
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References

  1. Aboud M., Burger M. The effect of catabolite repression and of cyclic 3': 5'-adenosine monophosphate on the translation of the lactose messenger RNA in Escherichia coli. Biochem Biophys Res Commzin 1970; 38:1023–1032
    [Google Scholar]
  2. Blazy B., Ullmann A. Two different mechanisms for urea action at the LAC and TNA operons in Escherichia coli. Mol & Gen Genet 1990; 220:419–424
    [Google Scholar]
  3. Botsford J.L., De Moss R.D. Catabolite repression of tryptophanase in Escherichia coli. J Bacteriol 1971; 105:303–312
    [Google Scholar]
  4. Botsford J.L., Harman J.G. Cyclic AMP in prokaryotes. Microbiof Rev 1992; 56:100–122
    [Google Scholar]
  5. Castro L., Feucht B.U., Morse M.L., Saier M.H. Jr Regulation of carbohydrate permeases and adenylate cyclase in Escherichia coli. Studies with mutant strains in which Enzyme I of the phosphoenolpyruvate: sugar phosphotransferase system is thermolabile. J Biol Chem 1976; 251:5522–5527
    [Google Scholar]
  6. Chambliss G.H. Carbon source-mediated catabolite repression. In Bacillus subtilis and other Gram-Positive Bacteria: Biochemistry 1993 Edited by Sonenshein A.L., Hoch J.A., Losick R. Washington, DC: American Society for Microbiology; Physiology, and Molecular Genetics, pp 213–228
    [Google Scholar]
  7. Dahl R., Wang R.J., Morse M.L. Effect of pleiotropic carbohydrate mutations (ctr) on tryptophan catabolism. J Bacteriol 1971; 107:513–518
    [Google Scholar]
  8. Dean D.A., Reizer J., Nikaido H., Saier M.H. Jr Regulation of the maltose transport system of Escherichia coli by the glucose-specific Enzyme III of the phosphoenolpyruvate-sugar phosphotransferase system. Characterization of inducer exclusion-resistant mutants and reconstitution of inducer exclusion in proteoliposomes. J Biol Chem 1990; 265:21005–21010
    [Google Scholar]
  9. De Crombrugghe B., Perlman R.L., Varmus H.E., Pastan I. Regulation of inducible enzyme synthesis in Escherichia coli by cyclic adenosine 3', 5'-monophosphate. J Biol Chem 1969; 244:5828–5835
    [Google Scholar]
  10. Deeley M.C., Yanofsky C. Nucleotide sequence of the structural gene for tryptophanase of Escherichia coli K-12. J Bacteriol 1981; 147:787–796
    [Google Scholar]
  11. De Moss R.D., Moser K. Tryptophanase in diverse bacterial species. J Bacteriol 1969; 98:167–171
    [Google Scholar]
  12. Dessein A., Schwartz M., Ullmann A. Catabolite repression in Escherichia coli mutants lacking cyclic AMP. Mol & Gen Genet 1978; 162:83–87
    [Google Scholar]
  13. Dills S.S., Schmidt M.R., Saier M.H. Jr Regulation of lactose transport by the phosphoenolpyruvate: sugar phosphotransferase system in membrane vesicles of Escherichia coli. J Cell Biochem 1982; 18:239–244
    [Google Scholar]
  14. Emmer M., De Crombrugghe B., Pastan I., Perlman R. Cyclic AMP receptor protein of E coli: its role in the synthesis of inducible enzymes. Proc Natl Acad Sci USA 1970; 66:480–487
    [Google Scholar]
  15. Freundlich M., Lichstein H.C. Inhibitory effect of glucose on tryptophanase. J Bacteriol 1960; 80:633–640
    [Google Scholar]
  16. Gilman A.G. A protein binding assay for adenosine 3': 5'-cyclic monophosphate. Proc Natl Acad Sci USA 1970; 67:305–312
    [Google Scholar]
  17. Gollnick P., Yanofsky C. tRNA(Trp) translation of leader peptide codon 12 and other factors that regulate expression of the tryptophanase operon. J Bacteriol 1990; 172:3100–3107
    [Google Scholar]
  18. Guidi-Rontani C., Danchin A., Ullmann A. Catabolite repression in Escherichia coli mutants lacking cylic AMP receptor protein. Proc Natl Acad Sci USA 1980; 77:5799–5801
    [Google Scholar]
  19. Hoch J.A., De Moss R.D. Physiological effects of a constitutive tryptophanase in Bacillus alvei. J Bacteriol 1965; 90:604–610
    [Google Scholar]
  20. Lowry O.H., Carter J., Ward J.B., Glaser L. The effect of carbon and nitrogen sources on the level of metabolic intermediates in Escherichia coli. J Biol Chem 1971; 246:6511–6521
    [Google Scholar]
  21. Mach H., Hecker M., Mach F. Physiological studies on cAMP synthesis in Bacillus subtilis. FEMS Microbiol Eett 1988; 52:189–192
    [Google Scholar]
  22. Magasanik B. Glucose effects: inducer exclusion and repression. In The Lactose Operon 1970 Edited by Beckwith J.R., Zipser D. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; pp 189–219
    [Google Scholar]
  23. Magasanik B., Neidhardt F.C. Regulation of carbon and nitrogen utilization. In Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology 1987 Edited by Neidhardt F.C., Ingraham J.L., Low K.B., Magasanik B., Schaechter M., Umbarger H.E. Washington, DC: American Society for Microbiology; 2 pp 1318–1325
    [Google Scholar]
  24. Makman R.S., Sutherland E.W. Adenosine 3', 5'-phosphate in Escherichia coli. J Biol Chem 1965; 240:1309–1314
    [Google Scholar]
  25. Osumi T., Saier M.H. Jr Regulation of lactose permease activity by the phosphoenolpyruvate: sugar phosphotransferase system: evidence for direct binding of the glucose-specific enzyme III to the lactose permease. Proc Natl Acad Sci USA 1982; 79:1457–1461
    [Google Scholar]
  26. Pastan I., Adhya S. Cyclic adenosine 5'-monophosphate in Escherichia coli. Bacteriol Rev 1976; 40:527–551
    [Google Scholar]
  27. Pastan I., Perlman R.L. Stimulation of tryptophanase synthesis in Escherichia coli by cyclic 3', 5'-adenosine monophosphate. J Biol Chem 1969; 244:2226–2232
    [Google Scholar]
  28. Pastan I., Perlman R.L. Cyclic adenosine monophosphate in bacteria. Science 1970; 169:339–344
    [Google Scholar]
  29. Perlman R., Pastan I. Cyclic 3,: 5'-AMP: stimulation of β-galactosidase and tryptophanase induction in E coli. Biochem Biophys Res Commun 1968; 30:656–664
    [Google Scholar]
  30. Phillips R.S., Gollnick P. Evidence that cysteine 298 is in the active site of tryptophan indole-lyase. J Biol Chem 1989; 264:10627–10632
    [Google Scholar]
  31. Ramirez J.M., Conde F., Del Campo F.F. Transcriptional control of tryptophanase synthesis by cyclic AMP in Escherichia coli. Eur J Biochem 1972; 25:471–475
    [Google Scholar]
  32. Reizer J., Reizer A., Saier M.H. Jr, Jacobson G.R. A proposed link between nitrogen and carbon metabolism involving protein phosphorylation in bacteria. Prot Sci 1992; 1:722–726
    [Google Scholar]
  33. Saier M.H. Jr Mechanisms and Regulation of Carbohydrate Transport in Bacteria 1985 New York: Academic Press;
    [Google Scholar]
  34. Saier M.H. Jr Protein phosphorylation and allosteric control of inducer exclusion and catabolite repression by the bacterial phosphoenolpyruvate: sugar phosphotransferase system. Microbiol Rev 1989; 53:109–120
    [Google Scholar]
  35. Saier M.H. Jr A multiplicity of potential carbon catabolite repression mechanisms in prokaryotic and eukaryotic microorganisms. New Biologist 1991; 3:1137–1147
    [Google Scholar]
  36. Saier M.H. Jr, Chin M. Energetics of the bacterial phosphotransferase system in sugar transport and the regulation of carbon metabolism. In Bacterial Energetics 1990 Edited by Krulwich T.A. New York: Academic Press; pp 273–299
    [Google Scholar]
  37. Saier M.H. Jr, Fagan M.J. Catabolite repression. In Encyclopedia of Microbiology 1992 Edited by Lederberg J. San Diego: Academic Press; 1 pp 431–442
    [Google Scholar]
  38. Saier M.H. Jr, Feucht B.U. Coordinate regulation of adenylate cyclase and carbohydrate permeases by the phosphoenolpyruvate: sugar phosphotransferase system in Salmonella typhimurium. J Biol Chem 1975; 250:7078–7080
    [Google Scholar]
  39. Saier M.H. Jr, Reizer J. A uniform nomenclature for the permeases and permease domains of the bacterial phosphoenolpyruvate: sugar phosphotransferase system. J Bacteriol 1992; 174:1433–1438
    [Google Scholar]
  40. Saier M.H. Jr, Roseman S. Inducer exclusion and repression of enzyme synthesis in mutants of Salmonella typhimurium defective in Enzyme I of the phosphoenolpyruvate: sugar phosphotransferase system. J Biol Chem 1972; 247:972–975
    [Google Scholar]
  41. Saier M.H. Jr, Roseman S. Sugar transport. The err mutation: its effect on repression of enzyme synthesis. J Biol Chem 1976; 251:6598–6605
    [Google Scholar]
  42. Saier M.H. Jr, Feucht B.U., McCaman M.T. Regulation of intracellular adenosine cyclic 3': 5'-monophosphate levels in Escherichia coli and Salmonella typhimurium Evidence for energy-dependent excretion of the cyclic nucleotide. J Biol Chem 1975; 250:7593–7601
    [Google Scholar]
  43. Saier M.H. Jr, Feucht B.U., Hofstadter L.J. Regulation of carbohydrate uptake and adenylate cyclase activity mediated by the Enzymes II of the phosphoenolpyruvate: sugar phosphotransferase system in Escherichia coli. J Biol Chem 1976; 251:883–892
    [Google Scholar]
  44. Saier M.H. Jr, Novotny M.J., Comeau-Fuhrman D., Osumi T., Desai J.D. In vivo evidence for cooperative binding of the sugar substrates and the allosteric regulatory protein (Enzyme IIIgl' of the phosphotransferase system) to the lactose and melibiose permeases in Escherichia coli and Salmonella typhimurium. J Bacteriol 1983; 155:1351–1357
    [Google Scholar]
  45. Saier M.H. Jr, Fagan M.J., Hoischen C., Reizer J. Transport mechanisms in Gram-positive bacteria. In Bacillus subtilis and other Gram-Positive Bacteria: Biochemistry Physiology, and Molecular Genetics 1993 Edited by Sonenshein A.L., Hoch J.A., Losick R. Washington, DC: American Society for Microbiologv; pp 133–156
    [Google Scholar]
  46. Sanzey B., Ullmann A. Urea, a specific inhibitor of catabolite sensitive operons. Biochem Biophys Res Commun 1976; 71:1062–1068
    [Google Scholar]
  47. Sarsero J.P., Wookey P.J., Gollnick P., Yanofsky C., Pittard A.J. A new family of integral membrane proteins involved in transport of aromatic amino acids in Escherichia coli. J Bacteriol 1991; 173:3231–3234
    [Google Scholar]
  48. Stewart G.C. Catabolite repression in the Gram-positive bacteria: generation of negative regulators of transcription. J Cell Biochem 1993; 51:25–28
    [Google Scholar]
  49. Stewart V.J., Yanofsky C. Evidence for transcription antitermination control of tryptophanase operon expression in Escherichia coli K-12. J Bacteriol 1985; 164:731–740
    [Google Scholar]
  50. Suelter C.H., Wang J., Snell E.E. Direct spectro-photometric assay of tryptophanase. FEBS Lett 1976; 66:230–232
    [Google Scholar]
  51. Tyler B., Wishnow R., Loomis W.F. Jr, Magasanik B. Catabolite repression gene of Escherichia coli. J Bacteriol 1969; 100:809–816
    [Google Scholar]
  52. Ullmann A., Monod J. Cyclic AMP as an antagonist of catabolite repression in Escherichia coli. FEBS Eett 1968; 2:57–60
    [Google Scholar]
  53. Ullmann A., Contesse G., Crepin M., Cros F., Monod J. Cyclic AMP and catabolite repression in Escherichia coli. Fogarty Inti Center Proc 1969 Bethesda, MD: National Institutes of Health; 4 pp 215–231
    [Google Scholar]
  54. Ullmann A., Joseph E., Danchin A. Cyclic AMP as a modulator of polarity in polycistronic transcriptional units. Proc Natl Acad Sci USA 1979; 76:3194–3197
    [Google Scholar]
  55. Vogel H.J., Bonner D.M. Acetylomithinase of Escherichia coli: partial purification and some properties. Biol Chem 1956; 218:97–106
    [Google Scholar]
  56. Yang J.K., Bloom R.W., Epstein W. Catabolite and transient repression in Escherichia coli do not require Enzyme I of the phosphotransferase system. J Bacteriol 1979; 138:275–279
    [Google Scholar]
  57. Yanofsky C., Horn V., Gollnick P. Physiological studies of tryptophan transport and tryptophanase operon induction in Escherichia coli. J Bacteriol 1991; 173:6009–6017
    [Google Scholar]
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