Binding of non-catalytic ATP to human hexokinase I highlights the structural components for enzyme-membrane association control

Structure

Volumn 7, Issue 11, 1999, Pages 1427-1437

  Rosano, Camillo ^a   Sabini, Elisabetta ^a,b   Rizzi, Menico ^c   Deriu, Daniela ^a   Murshudov, Garib ^b   Bianchi, Marzia ^d   Serafini, Giordano ^d   Magnani, Mauro ^d   Bolognesi, Martino ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF YORK   (United Kingdom)

^c UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^d UNIVERSITY OF URBINO   (Italy)

Author keywords

ATP; Glucose recognition; Glycolysis; Human hexokinase I; Mitochondrial membrane

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUCOSE; HEXOKINASE;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; GLYCOLYSIS; HYDROGEN BOND; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MOLECULAR INTERACTION; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL;

EID: 0033571093     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(00)80032-5     Document Type: Article

References (51)

1. Wilson, J.E. (1995). Hexokinases. J. Rev. Physiol. Biochem. Pharmacol. 126, 65-198.
2. Aleshin, A.E., Zeng, C., Bourenkov, G.P., Bartunik, H.D., Fromm, H.J. & Honzatko, R.B. (1998). The mechanism of regulation of hexokinase: New insights from the crystal structure of recombinant human brain hexokinase complexed with glucose and glucose-6-phosphate. Structure 6, 39-50.
3. Aleshin, A.E., Zeng, C., Bartunik, H.D., Fromm, H.J. & Honzatko, R.B. (1998). Regulation of hexokinase I: Crystal structure of recombinant human brain hexokinase complexed with glucose and phosphate. J. Mol. Biol. 282, 345-357.
4. Aleshin, A.E., Fromm, H.J. & Honzatko, R.B. (1998). Multiple crystal forms of hexokinase I: New insights regarding conformational dynamics, subunit interactions, and membrane association. FEBS Lett. 434, 42-46.
5. Mulichak, A.M., Wilson, J.E., Padmanabhan, K. & Garavito, R.M. (1998). The structure of mammalian hexokinase I. Nat. Struct. Biol. 5, 555-560.
6. Anderson, C.M., Stenkamp, R.E. & Steitz, T.A. (1978) Sequencing a protein by X-ray crystallography II. Refinement of yeast hexokinase B. Coordinates and sequence at 2.1 Å resolution. J. Mol. Biol. 123, 15-33.
7. Bennet, W.S. Jr & Steitz, T.A. (1980). Structure of a complex between yeast hexokinase A and glucose. Configuration with the native hexokinase B monomer and dimer. J. Mol. Biol. 140, 211-230.
8. Nishi, S., Seino, S. & Bell, G.I. (1988). Human hexokinase: Sequences of amino- and carboxy-terminal halves are homologous. Biochem. Biophys. Res. Commun. 157, 937-943.
9. Griffin, L.D., Gelb, B.D., Wheeler, D.A., Davison, D., Adams, V. & MacCabe E.R.B. (1991). Mammalian hexokinase I: Evolutionary conservation and structure to function analysis. Genomics 11, 1014-1024.
10. Ureta, T. (1975). The comparative isoenzymology of vertebrate hexokinases. Comp. Biochem. Physiol. 71, 545-555.
11. Shoham, M. & Steitz, T.A. (1982). The 6-hydroxymethyl group of a hexose is essential for the substrate-induced closure of the cleft in hexokinase. Biochim. Biophys. Acta 705, 380-384.
12. 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 6-phosphate in the N-terminal half of human brain hexokinase. J. Biol. Chem. 273, 19548-19553.
13. Lazo, P.A., Sols, A. & Wilson, J.E. (1980). Brain hexokinase has two spatially discrete sites for binding of glucose 6-phosphate. J. Biol. Chem. 255, 7548-7551.
14. 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.
15. Gelb, B.D., Adams, V., Jones, S.N., Griffin, L.D., MacGregor, G.R. & McCabe, E.R.B. (1992). Targeting of hexokinase I to liver and hepatoma mitochondria. Proc. Natl Acad. Sci. USA 89, 202-206.
16. Xie, G. & Wilson J.E. (1990). Tetrameric structure of mitochondrially bound rat brain hexokinase: A crosslinking study. Arch. Biochem. Biophys. 276, 285-293.
17. 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.
18. Sui, D. & Wilson, J.E. (1997). Structural determinants for the intracellular localization of the isozymes of mammalian hexokinase: Intracellular localization of fusion constructs incorporating structural elements from the hexokinase isozymes and the green fluorescent protein. Arch. Biochem. Biophys. 345, 111-125.
19. Rose, I. & Warms, J.V.B. (1967). Mitochondrial hexokinase. Release, rebinding and location. J. Biol. Chem. 242, 1635-1645.
20. Kabir, F. & Wilson, J.E. (1993). Mitochondrial hexokinase in brain of various species: Differences in sensitivity to solubilization by glucose-6-phosphate. Arch. Biochem. Biophys. 300, 641-650.
21. Smith, A.D. & Wilson, J.E. (1991). Disposition of mitochondrially bound hexokinase at the membrane surface, deduced from reactivity with monoclonal antibodies recognizing epitopes of defined location. Arch. Biochem. Biophys. 287, 359-366.
22. Navaza, J. (1994). AMoRe, an automated package for molecule replacement. Acta Crystallogr. A 50, 157-163.
23. Lawskowski, R.A., MacArthur M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK: A program to check the stereochemical quality of protein structure. J. Appl. Crystallogr. 26, 283-291.
24. Shoham, M. & Steitz, T.A. (1980). Crystallographic studies and model building of ATP at the active site of hexokinase. J. Mol. Biol. 140, 1-14.
25. Woolfit, A.R., Kellett, G.L. & Hogget, J.G. (1988). The binding of glucose and nucleotides to hexokinase from Saccharomyces cerevisiae. Biochim. Biophys. Acta 952, 238-243.
26. Giroix, M.H., Sener, A. & Malaisse, W.J. (1985). Reciprocal influence of glucose anomers upon their respective phosphorylation by hexokinase. Biol. Chem. Hoppe-seyler 367, 47-51.
27. Malaisse, W.J., Giroix, M.H., Dufrane, S.P., Malaisse-Lagae, F. & Sener, A. (1985). Environmental modulation of the anomeric specificity of glucose metabolism in normal and tumoral cells. Biochim. Biophys. Acta 847, 48-52.
28. Kenkare, U.W., Jarori, G.K., Kasturi, S.R., Metha, A. & Pitale, M.P. (1985). Biophysical investigations on the active site of brain hexokinase. J. Biosci. 8, 107-119.
29. 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.
30. 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.
31. Flocco, M.M. & Mowbray, S.L. (1994). Planar stacking of arginine and aromatic sidechains in proteins. J. Mol. Biol. 235, 709-717.
32. Burley, S.K. & Petsko, G.A. (1985). Aromatic-aromatic interaction: A mechanism of protein structure stabilization. Science 229, 23-28.
33. Moller, F. & Wilson, J.E. (1983). The influence of specific phospholipids on the interaction of hexokinase with the outer mitochondrial membrane. J. Neurochem. 41, 1109-1118.
34. Aubert-Foucher, E., Font, B. & Gautheron, D.C. (1984). Rabbit heart mitochondrial hexokinase: Solubilization and general properties. Arch. Biochem. Biophys. 232, 391-399.
35. Kodaira, T. & Yokoyama, N. (1983). Distribution and regulation of mitochondrial hexokinase in rat submandibular gland. Comp. Biochem. Physiol. 74, 235-241.
36. Bustamante, E. & Pedersen, P.L. (1980). Mitochondrial hexokinase of rat hepatoma cells in culture: Solubilization and kinetic properties. Biochemistry 19, 4972-4977.
37. Easterday, R.L. & Easterday, I.M. (1974). Affinity chromatography of kinases and dehydrogenases on Sephadex and Sepharose dye derivatives. Adv. Exp. Med. Biol. 42, 123-133.
38. Bottomley, M.J., Salim, K. & Panayotou, G. (1998). Phospholipid-binding protein domains. Biochim. Biophys. Acta 1436, 165-183.
39. Konstantin, A., Denessiou, K.A., Lehtonen, J.V. & Johnson, M.J. (1998). Enzyme-mononucleotide interactions: Three different folds share common structural elements for ATP recognition. Protein Sci. 7, 1768-1771.
40. Matte, A., Tari, L.W. & Delbaere, T.J. (1998). How do kinases transfer phosphoryl groups? Structure 6, 413-419
41. Bianchi, M., Serafini, G., Corsi, D. & Magnani, M. (1996). High level expression and purification of a human 'mini'-hexokinase. Protein Expression Purif. 7, 58-66.
42. Bianchi, M., Crinelli, R., Serafini, G., Giammarini, C. & Magnani, M. (1997). Molecular bases of hexokinase deficiency. Biochim. Biophys. Acta 1360, 211-221.
43. Sabini, E., et al., & Magnani, M. (1998) Expression purification and preliminary crystallographic studies of human hexokinase I. Prot. Pept. Lett. 5, 237-242.
44. Otwinowski Z. & Minor, W. (1997). Processing of the X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
45. Brünger, A.T. (1992). X-PLOR, Version 3.1. A System for X-ray Crystallography and NMR. Yale University, New Haven, USA.
46. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53, 240-255.
47. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119.
48. Engh, R.A. & Huber, R. (1991). Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallogr. A 47, 392-400.
49. Abola, E.E., Sussman, J.L., Prilusky, J. & Manning, N.O. (1997) Protein data bank archives of three-dimensional macromolecular structures. Methods Enzymol. 277, 556-571.
50. Kraulis, P.J. (1991). MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.
51. Nicholls, A.J., Sharp K. & Honig B. (1991). Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296.