Evidence for a catalytic Mg2+ ion and effect of phosphate on the activity of Escherichia coli phosphofructokinase-2: Regulatory properties of a ribokinase family member

Biochemistry

Volumn 45, Issue 30, 2006, Pages 9291-9299

  Parducci, Rafael E ^a   Cabrera, Ricardo ^a   Baez, Mauricio ^a   Guixé, Victoria ^a  

^a UNIVERSITY OF CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CATALYSIS; ESCHERICHIA COLI; IONS; MAGNESIUM COMPOUNDS; PHOSPHATES; REACTION KINETICS; SUGAR (SUCROSE);

ENZYMATIC ACTIVITIES; ESCHERICHIA COLI PHOSPHOFRUCTOKINASE; RIBOKINASE; SUGAR KINASES;

ENZYMES;

6 PHOSPHOFRUCTO 2 KINASE; ADENOSINE KINASE; ADENOSINE TRIPHOSPHATE MAGNESIUM; FRUCTOSE 6 PHOSPHATE; INORGANIC COMPOUND; MAGNESIUM; PHOSPHATE; RIBOKINASE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; ESCHERICHIA COLI PROTEIN; GLUTAMIC ACID; GLUTAMINE; PHOSPHOTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; ION TRANSPORT; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN MOTIF; QUALITATIVE ANALYSIS; WILD TYPE; ALLOSTERISM; AMINO ACID SUBSTITUTION; CHEMISTRY; COMPARATIVE STUDY; DRUG ANTAGONISM; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY;

ESCHERICHIA COLI;

ADENOSINE TRIPHOSPHATE; ALLOSTERIC REGULATION; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CATALYSIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GLUTAMIC ACID; GLUTAMINE; MAGNESIUM; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PHOSPHATES; PHOSPHOFRUCTOKINASE-2; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR);

EID: 33746623652     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060026o     Document Type: Article

References (52)

1. Bork, P., Sander, C., and Valencia, A. (1993) Convergent evolution of similar enzymatic function on different protein folds: the hexokinase, ribokinase, and galactokinase families of sugar kinases, Protein Sci. 2, 31-40.
2. Wu, L.-F., Reizer, A., Reizer, J., Cai, B., Tomich, J. M., and Saier, M. H. (1991) Nucleotide sequence of the Rhodobacter capsulatus fruK gene, which encodes fructose-1-phosphate: evidence for a kinase superfamily including both phosphofructokinases of Escherichia coli, J. Bacteriol. 173, 3117-3127.
3. Sigrell, J. A., Cameron, A. D., Jones, A. J., and Mowbray, S. L. (1998) Structure of Escherichia coli ribokinase in complex with ribose and dinucleotide determined to 1.8 Å resolution: insights into a new family of kinase structure, Structure 6, 183-193.
4. Sigrell, J. A., Cameron, A. D., and Mowbray, S. L. (1999) Induced fit on sugar binding activates ribokinase, J. Mol. Biol. 290, 1009-1018.
5. Mathews, I. I., Erion, M. D., and Ealick, S. E. (1998) Structure of human adenosine kinase at 1.5 Å resolution, Biochemistry 37, 15607-15620.
6. Schumacher, M. A., Scott, D. M., Mathews, I. I., Ealick, S. E., Roos, D. S., Ullman, B., and Brennan, R. G. (2000) Crystal structures of Toxoplasma gondii adenosine kinase reveal a novel catalytic mechanism and prodrug binding, J. Mol. Biol. 296, 549-567.
7. Tsuge, T., Sakuraba, H., Kobe, T., Kujime, A., Katunuma, N., and Ohshima, T. (2002) Crystal structure of the ADP-dependent glucokinase from Pyrococcus horikoshii at 2.0-Å resolution: A large conformational change in ADP-dependent glucokinase, Protein Sci. 11, 2456-2463.
8. Zhang, Y., Dougherty, M., Downs, D. M., and Ealick, S. E. (2004) Crystal structure of an aminoimidazole riboside kinase from Salmonella enterica: implications for the evolution of the ribokinase superfamily, Structure 12, 1809-1821.
9. Safo, M. K., Musayev, F. N., Hunt, S., di Salvo, M. L., Scarsdale, N., and Schirch, V. (2004) Crystal structure of the PdxY protein from Escherichia coli, J. Bacteriol. 186, 8074-8082.
10. Campobasso, N., Mathews, I., Begley, T. P., and Ealick, S. E. (2000) Crystal structure of 4-methyl-5-β-hydroyethylthiazole kinase from Bacillus subtilis at 1.5 Å resolution, Biochemistry 39, 7868-7877.
11. Cheng, G., Bennett, E. M., Begley, T. P., and Ealick, S. E. (2002) Crystal structure of 4-amino-5-hydroxymethyl-2-methylpyrimidine phosphate kinase from Salmonella typhimurium at 2.3 Å resolution, Structure 10, 225-235.
12. Ito, S., Fushinobu, S., Yoshioka, I., Koga, S., Matsuzawa, H., and Wakagi, T. (2001) Structural basis for the ADP-specificity of a novel glucokinase from hyperthermophilic archaeon, Structure 9, 205-214.
13. Ito, S., Fushinobu, S., Jeong, J.-J., Yoshioka, I., Koga, S., Shoun, H., and Wakagi, T. (2003) Crystal structure of an ADP-dependent glucokinase from Pyrococcus furiosus: implications for a sugar-induced conformational change in ADP-dependent kinase, J. Mol. Biol. 331, 871-883.
14. Tuininga, J. E., Verhees, C. H., van der Oost, J., Kengen, S. W. M., Stams, A. J. M., and de Vos, W. M. (1999) Molecular and biochemical characterization of the ADP-dependent phosphofructokinase from the hyperthermophilic archaeon Pyrococcus furiosus, J. Biol. Chem. 274, 21023-21028.
15. Guixé, V., and Babul, J. (1985) Effect of ATP on phosphofructokinase-2 from Escherichia coli. A mutant enzyme altered in the allosteric site for MgATP, J. Biol. Chem. 260, 11001-11005.
16. Guixé, V., and Babul, J. (1988) Influence of ligands on the aggregation of the normal and mutant forms of phosphofructokinase-2 of Escherichia coli, Arch. Biochem. Biophys. 264, 519-524.
17. Guixé, V., Rodríguez, P. H., and Babul, J. (1998) Ligand-induced conformational transitions in Escherichia coli phosphofructokinase-2: evidence for an allosteric site for MgATP, Biochemistry 37, 13269-13275.
18. Cabrera, R., Fischer, H., Trapani, S., Craievich, A. F., Garratt, R. C., Guixé, V., and Babul, J. (2003) Domain motions and quaternary packing of phosphofructokinase-2 from Escherichia coli studied by small angle X-ray scattering and homology modeling, J. Biol. Chem. 278, 12913-12919.
19. Andersson, C. E., and Mowbray, S. L. (2002) Activation of ribokinase by monovalent cations, J. Mol. Biol. 315, 409-419.
20. Maj, M. C., and Gupta, R. S. (2001) The effect of inorganic phosphate on the activity of bacterial ribokinase, J. Protein Chem. 20, 139-144.
21. Maj, M. C., Singh, B., and Gupta, R. S. (2002) Pentavalent ions dependency is a conserved property of adenosine kinase from diverse sources: identification of a novel motif implicated in phosphate and magnesium ion binding and substrate inhibition, Biochemistry 41, 4059-4069.
22. Fisher, M. N., and Newsholme, E. A. (1984) Properties of rat heart adenosine kinase, Biochem. J. 221, 521-528.
23. Baek, Y. H., and Nowak, T. (1982) Kinetic evidence for a dual cation role for muscle pyruvate kinase, Arch. Biochem. Biophys. 217, 491-497.
24. Lee, M. H., Hebda, C. A., and Nowak, T. (1981) The role of cations in avian liver phosphoenolpyruvate carboxykinase catalysis. Activation and regulation, J. Biol. Chem. 256, 12793-12801.
25. Waas, W., and Dalby, K. N. (2003) Physiological concentrations of divalent magnesium ion activate the serine/threonine specific protein kinase ERK2, Biochemistry 42, 2960-2970.
26. Berger, S. A., and Evans, P. R. (1992) Site-directed mutagenesis identifies catalytic residues in the active site of Escherichia coli phosphofructokinase, Biochemistry 31, 9237-9242.
27. Daldal, F. (1983) Molecular cloning of the gene for phosphofructokinase-2 of Escherichia coli and the nature of a mutation pfkB1, causing high level of the enzyme, J. Mol. Biol. 168, 285-305.
28. Tabor, S., and Richardson, C. C. (1985) A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes, Proc. Natl. Acad. Sci. U.S.A. 82, 1074-1078.
29. Babul, J. (1978) Phosphofructokinases from Escherichia coli. Purification and characterization of the nonallosteric isozyme, J. Biol. Chem. 253, 4350-4355.
30. Gaffney, T. J., and O'Sullivan, W. J. (1964) Kinetic studies of the activation of adenosine triphosphate-lombricine transferase by magnesium ions, Biochem. J. 90, 177-181.
31. Segel, I. H. (1975) Enzyme kinetics. Behavior and analysis of rapid equilibrium and steady-state enzyme systems, John Wiley & Sons, New York.
32. Cornish-Bowden, A. (1995) Fundamentals of enzyme kinetics, Portland Press Ltd., London.
33. Morrison, J. F. (1979) Approaches to kinetic studies on metal-activated enzymes, Methods Enzymol. 63, 257-294.
34. Zhang, Y., Dougherty, M., Downs, D. M., and Ealick, S. E. (2004) Crystal structure of an aminoimidazole riboside kinase from Salmonella enterica: implications for the evolution of the ribokinase superfamily, Structure 12, 1809-1821.
35. Ohshima, N., Inagaki, E., Yasuike, K., Takio, K., and Tahirov, T. H. (2004) Structure of Thermus themophilus 2-keto-3-deoxygluconate kinase: evidence for recognition of an open chain substrate, J. Mol. Biol. 340, 477-489.
36. Kotlarz, D., and Buc, H. (1981) Regulatory properties of phosphofructokinase-2 from Escherichia coli, Eur. J. Biochem. 117, 569-574.
37. Cabrera, R., Guixé, V., Alfaro, J., Rodríguez, P. H., and Babul, J. (2002) Ligand-dependent structural changes and limited proteolysis of Escherichia coli phosphofructokinase-2, Arch. Biochem. Biophys. 406, 289-295.
38. Maj, M. C., Singh, B., and Gupta, R. S. (2000) Structure-activity studies on mammalian adenosine kinase, Biochem. Biophys. Res. Commun. 275, 386-393.
39. Hao, W., and Gupta, R. S. (1996) Pentavalent ions dependency of mammalian adenosine kinase, Biochem. Mol. Biol. Int. 38, 889-899.
40. Matte, A., Tari, L. W., and Delbaere, L. (1998) How do kinases transfer phosphoryl groups?, Structure 6, 413-419.
41. Colombo, G., Carlson, G. M., and Lardy, H. A. (1981) Phosphoenolpyruvate carboxykinase (guanosine 5′-triphosphate) from rat liver cytosol. Dual-cation requirement for the carboxylation reaction, Biochemistry 20, 2749-2757.
42. Sun, G. S., and Budde, R. J. A. (1997) Requirement for an additional divalent metal cation to activate protein tyrosine kinases, Biochemistry 36, 2139-2146.
43. Boehr, D. D., Thompson, P. R., and Wright, G. D. (2001) Molecular mechanism of aminoglycoside antibiotic kinase APH-(3′)-IIIa. Roles of conserved active site residues, J. Biol. Chem. 276, 23929-23936.
44. Gibson, G. E., Harris, B. G., and Cook, P. F. (2006) Optimum activity of the phosphofructokinase from Ascaris suum requires more than one metal ion, Biochemistry 45, 2453-2460.
45. Dyguda, E., Szefczyk, W., and Sokalski (2004) The mechanism of phosphoryl transfer reaction and the role of active site residues on the basis of ribokinase-like kinases, Int. J. Mol. Sci. 5, 141-153.
46. Bañuelos, M., Gancedo, C., and Gancedo, J. (1977) Activation by phosphate of yeast phosphofructokinase, J. Biol. Chem. 252, 6394-6398.
47. Hofer, H. W., Allen, B. L., Kaeini, M. R., Pette, D. P., and Harris, B. G. (1982) Phosphofructokinase from Ascaris suum. Regulatory kinetic studies and activity near physiological conditions, J. Biol. Chem. 257, 3801-3806.
48. Kuhn, B., Jacobash, G., and Rapoport, S. M. (1974) Identity of sulfate and phosphate activation of the phosphofructokinase from erythrocytes, FEBS Lett. 38, 354-356.
49. Sugden, P. H., and Newsholme, E. A. (1975) The effects of ammonium, inorganic phosphate and potassium ions on the activity of phosphofructokinases from muscle and nervous tissues of vertebrates and invertebrates, Biochem. J. 150, 113-122.
50. Laloux, M., Van Schaftingen, E., Francois, J., and Hers, H. G. (1985) Phosphate dependency of phosphofructokinase 2, Eur. J. Biochem. 148, 155-159.
51. Park, J., Singh, B., Maj, M. C., and Gupta, R. S. (2004) Phosphorylated derivatives that activate or inhibit mammalian adenosine kinase provide insights into the role of pentavalent ions in AK catalysis, Protein J. 23, 167-177.
52. MacDonald, J. A., and Storey, K. B. (2005) Temperature and phosphate effects on allosteric phenomena of phosphofructokinase from a hibernating ground squirrel (Spermophilus lateralis), FEBS J. 272, 120-128.