Regulation of hexokinase I: Crystal structure of recombinant human brain hexokinase complexed with glucose and phosphate

Journal of Molecular Biology

Volumn 282, Issue 2, 1998, Pages 345-357

  Aleshin, Alexander E ^a   Zeng, Chenbo ^a,c   Bartunik, Hans D ^b   Fromm, Herbert J ^a   Honzatko, Richard B ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b DESY   (Germany)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Allosteric enzyme; Brain hexokinase; Glycolysis; Hexokinase I; X ray structure

Indexed keywords

BRAIN ENZYME; GLUCOSE; HEXOKINASE; PHOSPHATE;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; ENZYME REGULATION; ENZYME SUBSTRATE COMPLEX; GLYCOLYSIS; HUMAN; MITOCHONDRION; PRIORITY JOURNAL;

EID: 0032544488     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2017     Document Type: Article

References (47)

1. Aleshin, A. E., Zeng, C., Fromm, H. J. & Honzatko, R. B. (1996). Crystallization and preliminary X-ray analysis of human brain hexokinase. FEBS Letters, 391, 9-10.
2. Aleshin, A. E., Zeng, C., Bourenkov, G. P., Bartunik, H. D., Fromm, H. J. & Honzatko, R. B. (1998). Crystal structure of recombinant human brain hexokinase complexed with glucose and glucose-6-phosphate. Structure, 6, 39-50.
3. Anderson, C. M., Stenkamp, R. E. & Steitz, T. A. (1978). Sequencing a protein by X-ray crystallography. II. Refinement of yeast hexokinase B co-ordinates and sequence at 2.1 Å resolution. J. Mol. Biol. 123, 15-34.
4. Andrews, L. C. & Harrison, R. W. (1991). Modeling conformational change in macromolecules as an elastic deformation. Proteins: Struct. Funct. Genet. 10, 162-170.
5. Arora, K. K., Filburn, C. R. & Pedersen, P. L. (1991). Glucose phosphorylation. Site-directed mutations which impair the catalytic function of hexokinase. J. Biol. Chem. 266, 5359-5362.
6. Arora, K. K., Filburn, C. R. & Pedersen, P. L. (1993). Structure/function relationships in hexokinase. Site-directed mutational analyses and characterization of overexpressed fragments implicate different functions for the N- and C-terminal halves of the enzyme. J. Biol. Chem. 268, 18259-18266.
7. Bennett, W. S., Jr & Steitz, T. A. (1980a). Structure of a complex between yeast hexokinase A and glucose. I. Structure and determination and refinement at 3.5 Å resolution. J. Mol. Biol. 140, 183-209.
8. Bennett, W. S., Jr & Steitz, T. A. (1980b). Structure of a complex between yeast hexokinase A and glucose. II. Detailed comparisons of conformation and active site configuration with native hexokinase B monomer and dimer. J. Mol. Biol. 140, 211-230.
9. Beutner, G., Rück, A., Riede, B., Welte, W. & Brdiczka, D. (1996). Complexes between kinases, mitochondrial porin and adenylate translocator in rat brain resemble the permeability transition pore. FEBS Letters, 396, 189-195.
10. Beutner, G., Rück, A., Riede, B., Welte, W. & Brdiczka, D. (1997). Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator in brain: regulation of hexokinase, oxidative phosphorylation and permeability transition pore. Biochem. Soc. Trans, 25, 151-157.
11. Beutner, G., Rück, A., Riede, B., Welte, W. & Brdiczka, D. (1998). Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator display properties of the permeability transition pore. Implication for regulation of permeability transition by the kinases. Biochim. Biophys. Acta, 1368, 7-18.
12. Brünger, A. T. (1992). X-PLOR: Version 3.1. A system for X-ray crystallography and NMR. Yale University Press, New Haven and London.
13. Cambillau, C. & Horjales, E. (1987). TOM: a FRODO subpackage for protein-ligand fitting with interactive energy minimization. J. Mol. Graph. 5, 174-177.
14. Collaborative Computational Project Number 4 (1994). The CCP4 suite: programs for crystallography. Acta Crystallog. sect D, 50, 760-763.
15. de Cerqueira Cesar, M. & Wilson, J. E. (1998). Further studies on the coupling of mitochondrially bound hexokinase to intramitochondrially compartmented ATP, generated by oxidative phosphorylation. Arch. Biochem. Biophys. 350, 109-117.
16. Easterby, J. S. & O'Brien, M. J. (1973). Purification and properties of pig-heart hexokinase. Eur. J. Biochem. 38, 201-211.
17. Ellison, W. R., Lueck, J. D. & Fromm, H. J. (1975). Studies on the mechanism of orthophosphate regulation of bovine brain hexokinase. J. Biol. Chem. 250, 1864-1841.
18. Engh, R. A. & Huber, R. (1991). Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect A, 47, 392-400.
19. Fang, T.-Y., Alechina, O., Aleshin, A. E., Fromm, H. J. & Honzatko, R. B. (1998). Identification of a phosphate regulatory site and a low affinity binding site for glucose 6-phosphate in the N-terminal half of human brain hexokinase. J. Biol. Chem. 273, 19548-19553.
20. Fromm, H. J. (1981). Mechanism and mode of regulation of brain hexokinase. In The Regulation of Carbohydrate Formation and Utilization in Mammals (Veneziale, C. M., ed.), pp. 45-68, University Park Press, Baltimore.
21. Holroyde, M. J. & Trayer, I. P. (1976). Purification and properties of skeletal muscle hexokinase. FEBS Letters, 62, 215-219.
22. Katzen, H. M. & Schimke, R. T. (1065). Multiple forms of hexokinase in the rat: tissue distribution, age dependency, and properties. Proc. Natl Acad. Sci. USA, 54, 1218-1225.
23. Kraulis, J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
24. Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. (1993). PROCHECK: a program to check the stereochemical quality of proteins structures. J. Appl. Crystallog. 26, 283-291.
25. Laterveer, F. D., Gellerich, F. N. & Nicolay, K. (1995). Macromolecules increase the channeling of ADP from externally associated hexokinase to the matrix mitochondria. Eur. J. Biochem. 232, 569-577.
26. Lowry, O. H. & Passonneau, J. V. (1964). The relationship between substrates and enzymes of glycolysis in brain. J. Biol. Chem. 239, 31-42.
27. McRee, D. E. (1992). A visual protein crystallographic software system for X11/XView. J. Mol. Graph. 10, 44-46.
28. Magnani, M., Bianchi, M., Casabianca, A., Stocchi, V., Daniele, A., Altruda, F., Ferrone, M. & Silengo, L. (1992). A recombinant human 'mini'-hexokinase is catalytically active and regulated by hexose 6-phosphates. Biochem. J. 285, 193-199.
29. Manning, T. A. & Wilson, J. E. (1984). Inhibition of brain hexokinase by a multisubstrate analog results from binding to a discrete regulatory site. Biochem. Biophys. Res. Commun. 118, 90-96.
30. Mehta, A., Jarori, G. K. & Kenkare, U. W. (1988). Brain hexokinase has no preexisting allosteric site for glucose-6-phosphate. J. Biol. Chem. 263, 15492-15497.
31. Navaza, J. (1994). AMoRe: an automated package for molecular replacement. Acta Crystallog. sect. A, 50, 157-163.
32. Otwinowski, Z. (1993). Oscillation data reduction program. In Proceedings of the CCP4 Study Weekend: Data Collection and Processing, 29-30 January 1993. pp. 56-62 (Compiled by L. Sawyer, N. Isaacs & S. Bailey), SERC Daresbury Laboratory, England.
33. Polakis, P. G. & Wilson, J. E. (1985). An intact hydrophobic N-terminal sequence is critical for binding of rat brain hexokinase to mitochondria. Arch. Biochem. Biophys. 236, 328-337.
34. Rose, I. & Warms, J. V. B. (1967). Mitochondrial hexokinase. J. Biol. Chem. 242, 1635-1645.
35. Schwab, D. A. & Wilson, J. E. (1989). Complete amino acid sequence of rat brain hexokinase, deduced from the cloned cDNA and proposed structure of mammalian hexokinase. Proc. Natl Acad. Sci. USA, 86, 2563-2567.
36. Solheim, L. P. & Fromm, H. J. (1981). Kinetic evidence that the high affinity glucose-6-phosphate site on hexokinase I is the active site. Arch. Biochem. Biophys. 211, 92-99.
37. Tsai, H. J. & Wilson, J. E. (1996). Functional organization of mammalian hexokinases: both N- and C-terminal halves of the rat type II isozyme possess catalytic sites. Arch. Biochem. Biophys. 329, 17-23.
38. Ureta, T. (1975). Phylogeny, ontogeny, and properties of the hexokinases from vertebrates. In Isozymes III (Markert, C. L., ed.), pp. 575-601, Academic Press, Inc., New York.
39. Ureta, T. (1982). The comparative isozymology of vertebrate hexokinases. Comp. Biochem. Physiol. 71B, 549-555.
40. White, T. K. & Wilson, J. E. (1987). Rat brain hexokinase: location of the allosteric regulatory site in a structural domain at the N-terminus of the enzyme. Arch. Biochem. Biophys. 259, 402-411.
41. White, T. K. & Wilson, J. E. (1989). Isolation and characterization of the discrete N- and C-terminal halves of rat brain hexokinase: retention of full catalytic activity in the isolated C-terminal half. Arch. Biochem. Biophys. 274, 375-393.
42. Wicker, U., Bücheler, K., Gellerich, F. N., Wagner, M., Kapischke, M. & Brdiczka, D. (1993). Effect of macromolecules on the structure of the mitochondrial inter-membrane space and regulation of hexokinase. Biochim. Biophys. Acta, 1142, 228-239.
43. Wilson, J. E. (1995). Hexokinases. Rev. Physiol. Biochem. Pharmacol. 126, 65-198.
44. Xie, G. & Wilson, J. E. (1990). Tetrameric structure of mitochondrially bound rat brain hexokinase: a crosslinking study. Arch. Biochem. Biophys. 276, 285-293.
45. Zeng, C. & Fromm, H. J. (1995). Active site residues of human brain hexokinase as studied by site-specific mutagenesis. J. Biol. Chem. 270, 10509-10513.
46. Zeng, C., Aleshin, A. E., Hardie, J. B., Harrison, R. W. & Fromm, H. J. (1996). ATP-binding site of human brain hexokinase as studied by molecular modeling and site-directed mutagenesis. Biochemistry, 35, 13157-13164.
47. Zeng, C., Aleshin, A. E., Guanjin, C., Honzatko, R. B. & Fromm, H J. (1998). The roles of glycine residues in the ATP-binding site of human brain hexokinase. J. Biol. Chem. 273, 700-704.