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. 1982 May;150(2):604–615. doi: 10.1128/jb.150.2.604-615.1982

Phosphoenolpyruvate:sugar phosphotransferase system-mediated regulation of carbohydrate metabolism in Salmonella typhimurium.

S O Nelson, B J Scholte, P W Postma
PMCID: PMC216407  PMID: 6279563

Abstract

The crr mutation was shown to affect the phosphoenolpyruvate:sugar phosphotransferase system-mediated transient repression of the lac operon, intracellular cAMP levels, and sensitivity to inducer exclusion. Our results indicate that the presumed crr gene product, factor IIIGlc, plays a direct role in the regulation of inducer exclusion. We propose a mechanism in which inducer exclusion depends on both the level and state of phosphorylation of factor IIIGlc and the level of an inducer exclusion-sensitive transport system. The results of studies on the sensitivity to inducer exclusion of glycerol and maltose in cultures induced for short periods of time on these substrates (resulting in varying degrees of activity of the respective transport systems) support this model of inducer exclusion. Previously, the crp*-771 mutation has been shown to result in an altered cAMP receptor protein, which has a changed affinity for cAMP, and to affect the sensitivity for inducer exclusion of glycerol. Changes in other functions of the altered cAMP receptor protein were indicated by our results; these changes were in the roles of this protein in (i) the cAMP-dependent initiation of transcription of the lac operon and (ii) the regulation of intracellular cAMP levels and the export of cAMP. We propose that the crp*-771 mutation has an indirect effect in relieving inducer exclusion in repressed or hypersensitive strains, in which the crp*-771 mutation allows the synthesis of inducer exclusion-sensitive transport systems to higher levels than the levels found in strains containing wild-type cAMP receptor protein.

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Selected References

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  1. Boos W., Lengeler J., Hermann K. O., Unsöld H. J. The regulation of the beta-methylgalactoside transport system and of the galactose binding protein of Escherichia coli K12. Eur J Biochem. 1971 Apr 30;19(4):457–470. doi: 10.1111/j.1432-1033.1971.tb01336.x. [DOI] [PubMed] [Google Scholar]
  2. Botsford J. L., Drexler M. The cyclic 3',5'-adenosine monophosphate receptor protein and regulation of cyclic 3',5'-adenosine monophosphate synthesis in Escherichia coli. Mol Gen Genet. 1978 Sep 20;165(1):47–56. doi: 10.1007/BF00270375. [DOI] [PubMed] [Google Scholar]
  3. COHN M., HORIBATA K. Inhibition by glucose of the induced synthesis of the beta-galactoside-enzyme system of Escherichia coli. Analysis of maintenance. J Bacteriol. 1959 Nov;78:601–612. doi: 10.1128/jb.78.5.601-612.1959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dills S. S., Apperson A., Schmidt M. R., Saier M. H., Jr Carbohydrate transport in bacteria. Microbiol Rev. 1980 Sep;44(3):385–418. doi: 10.1128/mr.44.3.385-418.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ferenci T., Klotz U. Affinity chromatographic isolation of the periplasmic maltose binding protein of Escherichia coli. FEBS Lett. 1978 Oct 15;94(2):213–217. doi: 10.1016/0014-5793(78)80940-5. [DOI] [PubMed] [Google Scholar]
  6. Feucht B. U., Saier M. H., Jr Fine control of adenylate cyclase by the phosphoenolpyruvate:sugar phosphotransferase systems in Escherichia coli and Salmonella typhimurium. J Bacteriol. 1980 Feb;141(2):603–610. doi: 10.1128/jb.141.2.603-610.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fraser A. D., Yamazaki H. Determination of the rates of synthesis and degradation of adenosine 3',5'-cyclic monophosphate in Escherichia coli CRP- and CRP+ strains. Can J Biochem. 1978 Sep;56(9):849–852. doi: 10.1139/o78-130. [DOI] [PubMed] [Google Scholar]
  8. Fraser D. E., Yamazaki H. Construction of an Escherichia coli strain which excretes abnormally large amounts of adenosine 3',5'-cyclic monophosphate. Can J Microbiol. 1978 Nov;24(11):1423–1425. doi: 10.1139/m78-228. [DOI] [PubMed] [Google Scholar]
  9. Goldenbaum P. E., Hall G. A. Transport of cyclic adenosine 3',5'-monophosphate across Escherichia coli vesicle membranes. J Bacteriol. 1979 Nov;140(2):459–467. doi: 10.1128/jb.140.2.459-467.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Harwood J. P., Gazdar C., Prasad C., Peterkofsky A., Curtis S. J., Epstein W. Involvement of the glucose enzymes II of the sugar phosphotransferase system in the regulation of adenylate cyclase by glucose in Escherichia coli. J Biol Chem. 1976 Apr 25;251(8):2462–2468. [PubMed] [Google Scholar]
  11. Harwood J. P., Peterkofsky A. Glucose-sensitive adenylate cyclase in toluene-treated cells of Escherichia coli B. J Biol Chem. 1975 Jun 25;250(12):4656–4662. [PubMed] [Google Scholar]
  12. Kornberg H. L., Reeves R. E. Inducible phosphoenolpyruvate-dependent hexose phosphotransferase activities in Escherichia coli. Biochem J. 1972 Aug;128(5):1339–1344. doi: 10.1042/bj1281339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Krishna G., Weiss B., Brodie B. B. A simple, sensitive method for the assay of adenyl cyclase. J Pharmacol Exp Ther. 1968 Oct;163(2):379–385. [PubMed] [Google Scholar]
  14. 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]
  15. Majerfeld I. H., Miller D., Spitz E., Rickenberg H. V. Regulation of the synthesis of adenylate cyclase in Escherichia coli by the cAMP -- cAMP receptor protein complex. Mol Gen Genet. 1981;181(4):470–475. doi: 10.1007/BF00428738. [DOI] [PubMed] [Google Scholar]
  16. Peterkofsky A., Gazdar C. Interaction of enzyme I of the phosphoenolpyruvate:sugar phosphotransferase system with adenylate cyclase of Escherichia coli. Proc Natl Acad Sci U S A. 1975 Aug;72(8):2920–2924. doi: 10.1073/pnas.72.8.2920. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Postma P. W. Galactose transport in Salmonella typhimurium. J Bacteriol. 1977 Feb;129(2):630–639. doi: 10.1128/jb.129.2.630-639.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Postma P. W., Roseman S. The bacterial phosphoenolpyruvate: sugar phosphotransferase system. Biochim Biophys Acta. 1976 Dec 14;457(3-4):213–257. doi: 10.1016/0304-4157(76)90001-0. [DOI] [PubMed] [Google Scholar]
  19. Postma P. W., Schuitema A., Kwa C. Regulation of methyl beta-galactoside permease activity in pts and crr mutants of Salmonella typhimurium. Mol Gen Genet. 1981;181(4):448–453. doi: 10.1007/BF00428734. [DOI] [PubMed] [Google Scholar]
  20. Potter K., Chaloner-Larsson G., Yamazaki H. Abnormally high rate of cyclic AMP excretion from an Escherichia coli mutant deficient in cyclic AMP receptor protein. Biochem Biophys Res Commun. 1974 Mar 25;57(2):379–385. doi: 10.1016/0006-291x(74)90941-3. [DOI] [PubMed] [Google Scholar]
  21. Rephaeli A. W., Saier M. H., Jr Effects of crp mutations on adenosine 3',5'-monophosphate metabolism in Salmonella typhimurium. J Bacteriol. 1976 Jul;127(1):120–127. doi: 10.1128/jb.127.1.120-127.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rephaeli A. W., Saier M. H., Jr Regulation of genes coding for enzyme constituents of the bacterial phosphotransferase system. J Bacteriol. 1980 Feb;141(2):658–663. doi: 10.1128/jb.141.2.658-663.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Saier M. H., Jr Bacterial phosphoenolpyruvate: sugar phosphotransferase systems: structural, functional, and evolutionary interrelationships. Bacteriol Rev. 1977 Dec;41(4):856–871. doi: 10.1128/br.41.4.856-871.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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 Sep 10;250(17):7078–7080. [PubMed] [Google Scholar]
  25. 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 Feb 10;251(3):883–892. [PubMed] [Google Scholar]
  26. Saier M. H., Jr, Roseman S. Sugar transport. 2nducer exclusion and regulation of the melibiose, maltose, glycerol, and lactose transport systems by the phosphoenolpyruvate:sugar phosphotransferase system. J Biol Chem. 1976 Nov 10;251(21):6606–6615. [PubMed] [Google Scholar]
  27. Saier M. H., Jr, Roseman S. Sugar transport. The crr mutation: its effect on repression of enzyme synthesis. J Biol Chem. 1976 Nov 10;251(21):6598–6605. [PubMed] [Google Scholar]
  28. Saier M. H., Jr, Straud H., Massman L. S., Judice J. J., Newman M. J., Feucht B. U. Permease-specific mutations in Salmonella typhimurium and Escherichia coli that release the glycerol, maltose, melibiose, and lactose transport systems from regulation by the phosphoenolpyruvate:sugar phosphotransferase system. J Bacteriol. 1978 Mar;133(3):1358–1367. doi: 10.1128/jb.133.3.1358-1367.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Saier M. H., 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 Feb 10;247(3):972–975. [PubMed] [Google Scholar]
  30. Salomon Y., Londos C., Rodbell M. A highly sensitive adenylate cyclase assay. Anal Biochem. 1974 Apr;58(2):541–548. doi: 10.1016/0003-2697(74)90222-x. [DOI] [PubMed] [Google Scholar]
  31. Scholte B. J., Postma P. W. Competition between two pathways for sugar uptake by the phosphoenolpyruvate-dependent sugar phosphotransferase system in Salmonella typhimurium. Eur J Biochem. 1981;114(1):51–58. doi: 10.1111/j.1432-1033.1981.tb06171.x. [DOI] [PubMed] [Google Scholar]
  32. Scholte B. J., Postma P. W. Mutation in the crp gene of Salmonella typhimurium which interferes with inducer exclusion. J Bacteriol. 1980 Feb;141(2):751–757. doi: 10.1128/jb.141.2.751-757.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Scholte B. J., Schuitema A. R., Postma P. W. Characterization of factor IIIGLc in catabolite repression-resistant (crr) mutants of Salmonella typhimurium. J Bacteriol. 1982 Feb;149(2):576–586. doi: 10.1128/jb.149.2.576-586.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Scholte B. J., Schuitema A. R., Postma P. W. Isolation of IIIGlc of the phosphoenolpyruvate-dependent glucose phosphotransferase system of Salmonella typhimurium. J Bacteriol. 1981 Oct;148(1):257–264. doi: 10.1128/jb.148.1.257-264.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Waygood E. B., Meadow N. D., Roseman S. Modified assay procedures for the phosphotransferase system in enteric bacteria. Anal Biochem. 1979 May;95(1):293–304. doi: 10.1016/0003-2697(79)90219-7. [DOI] [PubMed] [Google Scholar]
  36. Wayne P. K., Rosen O. M. Cyclic 3':5'-adenosine monophosphate in Escherichia coli during transient and catabolite repression. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1436–1440. doi: 10.1073/pnas.71.4.1436. [DOI] [PMC free article] [PubMed] [Google Scholar]

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