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. 1975 Jul;123(1):128–136. doi: 10.1128/jb.123.1.128-136.1975

Role of adenylate kinase in the regulation of macromolecular biosynthesis in a putative mutant of Escherichia coli defective in membrane phospholipid biosynthesis.

M Glaser, W Nulty, P R Vagelos
PMCID: PMC235699  PMID: 166976

Abstract

The regulation of macromolecular biosynthesis was studied in a temperature-sensitive mutant of Escherichia coli previously identified as containing a single mutation causing a thermolabile sn-glycerol-3-phosphate acyltransferase, the first enzyme of the pathway for phospholipid biosynthesis. When this mutant was shifted to a nonpermissive temperature, phospholipid synthesis, as well as ribonucleic acid, deoxyribonucleic acid, and protein synthesis, decreased in a coordinate manner, suggesting the existence of a common regulatory mechanism. During the same time that the rate of macromolecular synthesis was decreasing at the nonpermissive temperature, the intracellular concentration of adenosine 5'-triphosphate dropped dramatically and the concentration of adenosine monophosphate increased. The concentration of adenosine 5'-diphosphate dropped, but not as markedly. The decrease in macromolecular synthesis and the changes in the adenine nucleotide concentrations can now be attributed to a thermolabile adenylate kinase. The inactivation of adenylate kinase prevented the cell from converting adenosine 5'-monophosphate to adenosine 5'-diphosphate and consequently from making adenosine 5'-triphosphate. This in turn caused a decrease in the rate of macromolecular synthesis and cell growth. Adenylate kinase, therefore, is a key enzyme in controlling the rate of cell growth. The nature of the possible relationship between adenylate kinase and glycerol-3-phosphate acyltransferase is discussed.

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Selected References

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

  1. Ames G. F. Lipids of Salmonella typhimurium and Escherichia coli: structure and metabolism. J Bacteriol. 1968 Mar;95(3):833–843. doi: 10.1128/jb.95.3.833-843.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  3. Bell R. M. Mutants of Escherichia coli defective in membrane phospholipid synthesis: macromolecular synthesis in an sn-glycerol 3-phosphate acyltransferase Km mutant. J Bacteriol. 1974 Mar;117(3):1065–1076. doi: 10.1128/jb.117.3.1065-1076.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cashel M., Lazzarini R. A., Kalbacher B. An improved method for thin-layer chromatography of nucleotide mixtures containing 32P-labelled orthophosphate. J Chromatogr. 1969 Mar 11;40(1):103–109. doi: 10.1016/s0021-9673(01)96624-5. [DOI] [PubMed] [Google Scholar]
  5. Cousin D., Belaïch J. P. Sur une mutatio thermosensible d'Escherichia coli affectant une fonction énergétique. C R Acad Sci Hebd Seances Acad Sci D. 1966 Sep 19;263(12):886–888. [PubMed] [Google Scholar]
  6. Cousin D., Buttin G. Mutants thermosensibles d'Escherichia coli K12. 3. Une mutation létale d'E. coli affectant l'activité de l'adénylate-kinase. Ann Inst Pasteur (Paris) 1969 Nov;117(5):612–630. [PubMed] [Google Scholar]
  7. Cousin D. Mutants thermosensibles d'Escherichia coli K12. II. Etude d'une mutation létale affectant une réaction génératrice d'énercie. Ann Inst Pasteur (Paris) 1967 Sep;113(3):309–325. [PubMed] [Google Scholar]
  8. Cronan J. E., Jr, Bell R. M. Mutants of Escherichia coli defective in membrane phospholipid synthesis: mapping of sn-glycerol 3-phosphate acyltransferase Km mutants. J Bacteriol. 1974 Oct;120(1):227–233. doi: 10.1128/jb.120.1.227-233.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cronan J. E., Jr, Birge C. H., Vagelos P. R. Evidence for two genes specifically involved in unsaturated fatty acid biosynthesis in Escherichia coli. J Bacteriol. 1969 Nov;100(2):601–604. doi: 10.1128/jb.100.2.601-604.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cronan J. E., Jr, Godson G. N. Mutants of Escherichia coli with temperature-sensitive lesions in membrane phospholipid synthesis: genetic analysis of glycerol-3-phosphate acyltransferase mutants. Mol Gen Genet. 1972;116(3):199–210. doi: 10.1007/BF00269765. [DOI] [PubMed] [Google Scholar]
  11. Cronan J. E., Jr, Ray T. K., Vagelos P. R. Selection and characterization of an E. coli mutant defective in membrane lipid biosynthesis. Proc Natl Acad Sci U S A. 1970 Mar;65(3):737–744. doi: 10.1073/pnas.65.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cronan J. E., Vagelos P. R. Metabolism and function of the membrane phospholipids of Escherichia coli. Biochim Biophys Acta. 1972 Feb 14;265(1):25–60. doi: 10.1016/0304-4157(72)90018-4. [DOI] [PubMed] [Google Scholar]
  13. Glaser M., Bayer W. H., Bell R. M., Vagelos P. R. Regulation of macromolecular biosynthesis in a mutant of Escherichia coli defective in membrane phospholipid biosynthesis. Proc Natl Acad Sci U S A. 1973 Feb;70(2):385–389. doi: 10.1073/pnas.70.2.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hochstadt-Ozer J., Cashel M. The regulation of purine utilization in bacteria. V. Inhibition of purine phosphoribosyltransferase activities and purine uptake in isolated membrane vesicles by guanosine tetraphosphate. J Biol Chem. 1972 Nov 10;247(21):7067–7072. [PubMed] [Google Scholar]
  15. Holmes R. K., Singer M. F. Purification and characterization of adenylate kinase as an apparent adenosine triphosphate-dependent inhibitor of ribonuclease II in Escherichia coli. J Biol Chem. 1973 Mar 25;248(6):2014–2021. [PubMed] [Google Scholar]
  16. Kito M., Lubin M., Pizer L. I. A mutant of Escherichia coli defective in phosphatidic acid synthesis. Biochem Biophys Res Commun. 1969 Feb 21;34(4):454–458. doi: 10.1016/0006-291x(69)90403-3. [DOI] [PubMed] [Google Scholar]
  17. Kito M., Pizer L. I. Phosphatidic acid synthesis in Escherichia coli. J Bacteriol. 1969 Mar;97(3):1321–1327. doi: 10.1128/jb.97.3.1321-1327.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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 Nov;246(21):6511–6521. [PubMed] [Google Scholar]
  20. Merlie J. P., Pizer L. I. Regulation of phospholipid synthesis in Escherichia coli by guanosine tetraphosphate. J Bacteriol. 1973 Oct;116(1):355–366. doi: 10.1128/jb.116.1.355-366.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. OLIVER I. T., PEEL J. L. Myokinase activity in microorganisms. Biochim Biophys Acta. 1956 May;20(2):390–392. doi: 10.1016/0006-3002(56)90302-x. [DOI] [PubMed] [Google Scholar]
  22. Pizer L. I., Merlie J. P., De Leon M. P. Metabolic consequences of limited phospholipid synthesis in Escherichia coli. J Biol Chem. 1974 May 25;249(10):3212–3224. [PubMed] [Google Scholar]
  23. Ray T. K., Cronan J. E., Jr, Mavis R. D., Vagelos P. R. The specific acylation of glycerol 3-phosphate to monoacylglycerol 3-phosphate in Escherichia coli. Evidence for a single enzyme conferring this specificity. J Biol Chem. 1970 Dec 10;245(23):6442–6448. [PubMed] [Google Scholar]
  24. Singer S. J. The molecular organization of membranes. Annu Rev Biochem. 1974;43(0):805–833. doi: 10.1146/annurev.bi.43.070174.004105. [DOI] [PubMed] [Google Scholar]
  25. Theze J., Margarita D. Etude de l'adénylate kinase chez "E. coli" K 12 et chez un mutant thermosensible. Ann Inst Pasteur (Paris) 1972 Aug;123(2):157–169. [PubMed] [Google Scholar]
  26. 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]
  27. Winslow R. M., Lazzarini R. A. The rates of synthesis and chain elongation of ribonucleic acid in Escherichia coli. J Biol Chem. 1969 Mar 10;244(5):1128–1136. [PubMed] [Google Scholar]

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