Regulation of Glycogen Concentration by the Histidine-Containing Phosphocarrier Protein HPr in Escherichia coli

  • Koo, Byung-Mo (School of Biological Sciences and Institute of Microbiology, Seoul National University) ;
  • Seok, Yeong-Jae (School of Biological Sciences and Institute of Microbiology, Seoul National University)
  • 발행 : 2001.03.01

초록

In addition to effecting the catalysis of sugar uptake, the bacterial phosphoenolpyruvate::sugar phosphotransferase system regulates a variety of physiological processes. In a previous paper [Seok et al.,(1997) J. Biol. Chem. 272, 26511-26521], we reported the interaction with and allosteric regulation of Esiherichia coli glycogen phosphorylase activity by the histidine-containing phosphocarrier protein HPr in vitro. Here, we show that the specific interaction between HPr and glycogen phosphorylase occurs in vivo. To address the physiological role of the HPr-glycogen phosphorylase complex, intracellular glycogen levels were measured in E. coli strains transformed with various plasmids. While glycogen accumulated during the transition between exponential and stationary growth phases in wildtype cells, it did not accumulate in cells overproducing HPr or its inactive mutant regardless of the growth stage. From these results, we conclude that HPr mediates crosstalk between sugar uptake through the phosphoenolpyruvate:sugar phosphotransferase system and glycogen breakdown. The evolutionary significance of the HPr-glycogen phosphorylase complex is suggested.

키워드

참고문헌

  1. J. Bacteriol. v.181 Exponential-phase glycogen recycling is essential for growth of Mycobacterium smegmatis Belanger A.E.;G.F. Hatfull
  2. Arch. Biochem. Biophys. v.127 Purification and properties of glycogen phosphorylase from Escherichia coli Chen G.S.;I.H. Segel
  3. Biochemistry v.36 Identification by NMR of the binding surface for the histidine-containing phosphocarrier protein HPr on the N-terminal domain of enzyme I of the Escherichia coli phosphotransferase system Garrett D.S.;Y.-J. Seok;A. Peterkofsky;G.M. Clore;A.M. Gronenborn
  4. J. Mol. Biol. v.234 Evolution of allosteric control in glycogen phosphorylase Hudson J.W.;G.B. Golding;M.M. Crerar
  5. J. Biol. Chem. v.274 Purification of Mlc and analysis of its effects on the pts expression in Escherichia coli Kim S.-Y.;T.-W. Nam;D. Shin;B.-M. Koo;Y.-J. Seok;S. Ryu
  6. Proc. Natl. Acad. Sci. USA v.52 Phosphate bound to histidine in a protein as an intermediate in a novel phosphotransferase system Kundig W.;S. Ghosh;S. Roseman
  7. Bio/Technology v.11 A thioredoxin gene fusion expression system that circumvents inclusion body formation in he E. coli cytoplasm LaVallie E.R.;E.A. DiBlasio;S. Kovacic;K.L. Grant;P.F. Schendel;J.M. McCoy
  8. EMBO J. v.19 Signal transduction between a membrane-bound transporter, PtsG, and a soluble transcription factor, Mlc, of Escherichia coli Lee S.J.;W. Boos;J.P. Bouche;J. Plumbidge
  9. Proc. Natl. Acad. Sci. USA v.92 Coupling the phosphotransferase system and the methyl-accepting chemotaxis protein-dependent chemotaxis signaling pathways of Escherichia coli Lux R.;K. Jahreis;K. Bettenbrock;J.S> Parkinson;J.W. Lengeler
  10. Can. J. Biochem. Cell Biol. v.61 Determination of the levels of HPr and enzyme I of the phosphoenolpyruvate-sugar phosphotransferase system in Escherichia coli and Salmonella typhimurium Mattoo R.L.;E.B. Waygood
  11. EMBO J. v.20 The Escherichia coli glucose transporter enzyme IICGGlc recruits the global repressor Mlc. Nam T.-W.;S.-H. Cho;D. Shin;J.-H. Kim;J.-Y. Jeong;J.-H. Seok
  12. Anal. Biochem. v.248 A simplified procedure for a rapid and reliable assay of both glycogen and trehalose in whole yeast cells Parrou J.L.;J. Francois
  13. Prog. Nucleic Acid Res. Mol. Biol. v.44 Bacterial adenylyl cyclases Peterkofsky A.;A. Reizer;J. Reizer;N. Gollop;P.-P. Zhu;N. Amin
  14. Biochem. Biophys. Res. Commun. v.109 Polyglucose content in the cell and the rate of glucose comsumption during synchronous growth of Escherchia coli Planutis K.S.;M.V. Planutiene;A.V. Lazareva;E.E. Selkov;Yu.V. Evtodienko
  15. Mol. Microbiol. v.29 Expression of ptsG, the gene for the major glucose PTS transporter in Escherichia coli Plumbridge J.
  16. Mol. Microbiol. v.33 Expression of the phosphotransferase system both mediates and is mediated by Mlc regulation in Escherichia coli Plumbridge J.
  17. Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology Phosphoenolpyruvate:carbohydrate phosphotransferase systems Postma P.W.;J.W. Lengeler;G.R. Jacobson;F.C. Neidhardt(ed.)
  18. J. Biol. Chem. v.270 Novel proteins of the phosphotransferase system encoded within the rpoN operon of Escherichia coli;Enzyme IIANtr affects growth on organic nitrogen and the conditional lethality of an erats mutant Powell B.S.;D.L. Court;T. Inada;Y. Nakamura;V. Michotey;X. Cui;A. Reizer;M.H. Saier Jr.;J. Reizer
  19. Adv. Microb. Physiol. v.30 Physiology, biochemistry and genetics of bacterial glycogen synthesis Preiss J.;T. Romeo
  20. Nature Struct. Biol. v.1 Parallel evolution in two homologues of phosphorylase Rath V.;R.J. Fletterick
  21. Nucl. Acids Res. v.17 Hyper-expression and purification of Escherichia coli adenylate cyclase using a vector designed for expression of lethal gene products Reddy P.;A. Peterkofsky;K. McKenney
  22. FEMS Microbiol. Lett. v.118 Sequence of the fruB gene of Escherichia coli encoding the diphosphoryl transfer protein (DTP) of the phosphoenolpyruvate:sugar phosphotransferase system Reizer J.;A. Reizer;H.L. Kornberg;M.H. Saier Jr.
  23. J. Bacteriol. v.171 Genetic regulation of glycogen biosynthesis in Escherichia coli: invitro effects of cyclic AMP and guanosine 5'-diphosphate 3'-diphosphate and analysis of in vivo transcripts Romeo T.;J. Preiss
  24. Proc. Natl. Acad. Sci. USA v.93 Importance of the carboxyl-terminal domain of enzyme I of the Escherichia coli phosphoenolpyruvate: sugar phosphotransferase system for phosphoryl donor specificity Seok Y.-J.;B.R. Lee;P.-P. Zhu;A. Peterkofsky
  25. HPr. J. Biol. Chem. v.272 High affinity binding and allosteric regulation of Escherichia coli glycogen phosphorylase by the histidine phosphocarrier protein Seok Y.-J.;M. Sondej;P. Badawi;M.S. Lewis;M.C. Briggs;H. Jaffe;A. Peterkofsky
  26. Proc. Natl. Acad. Sci. USA v.94 Topology of allosteric regulation of lactose permease Seok Y.-J.;J. Sun;H.R. Kaback;A. Peterkofsky
  27. J. Bacteriol. v.181 Function of trehalose and glycogen in cell cycle progression and cell viability in Saccharomyces cerevisiae Sillje H.H.W.;J.W.G. Paalman;E.G. Ter Schure;S.Q.B. Olsthoorn;A.J. Verkleij;J. Boonstra;C.T. Verrips
  28. Nature v.220 Bacterial glycogen and survival Strange R.E.
  29. Science v.269 Regulatory subunit of protein kinase A: structure of deletion mutant with cAMP binding domains Su Y.;W.R. Dostmann;F.W. Herberg;K. Durick;N.H. Xuong;L. Ten Eyck;S.S. Taylor;K.I. Varughese
  30. EMBO J. v.19 A novel regulatory role of glucose transporter of Escherichia coli: membrane sequestration of a global repressor Mlc. Tanaka Y.;K. Kimata;H. Aiba
  31. EMBO J. v.16 The crystal structure of Escherichia coli maltodextrin phosphorylase provides an explanation for the activity without control in this basic archetype of a phosphorylase Watson K.A.;R. Schinzel;D. Palm;L.N. Johnson
  32. J. Bacteriol. v.178 Coordinate genetic regulation of glycogen catabolism and biosynthesis in Escherichia coli via the CsrA gene product Yang H.;M.Y. Liu;T. Romeo