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2000 | 47 | 4 | 1045-1060
Article title

Further studies on the role of phospholipids in determining the characteristics of mitochondrial binding sites for type I hexokinase.

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Abstracts
EN
Previous work has indicated that two types (A and B) of binding sites for hexokinase exist, but in different proportions, on brain mitochondria from various species. Hexokinase is readily solubilized from Type A sites by glucose 6-phosphate (Glc-6-P), while hexokinase bound to Type B sites remains bound even in the presence of Glc-6-P. Type A:Type B ratios are approximately 90:10, 60:40, 40:60, and 20:80 for brain mitochondria from rat, rabbit, bovine and human brain, respectively. The present study has indicated that MgCl2-dependent partitioning of mitochondrially bound hexokinase into a hydrophobic (Triton X-114) phase is generally correlated with the proportion of Type B sites. This partitioning behavior is sensitive to phospholipase C, implying that the factor(s) responsible for conferring hydrophobic character is(are) phospholipid(s). Substantial differences were also seen in the resistance of hexokinase, bound to brain mitochondria from various species, to solubilization by Triton X-100, Triton X-114, or digitonin. This resistance increased with proportion of Type B sites. Enrichment of bovine brain mitochondria in acidic phospholipids (phosphatidylserine or phosphatidylinositol), but not phosphatidylcholine or phosphatidylethanolamine, substantially increased solubilization of the enzyme after incubation at 37°C. Collectively, the results imply that the Type A and Type B sites are located in membrane domains of different lipid composition, the Type A sites being in domains enriched in acidic phospholipids which lead to greater susceptibility to solubilisation by Glc-6-P.
Publisher

Year
Volume
47
Issue
4
Pages
1045-1060
Physical description
Dates
published
2000
received
2000-05-17
revised
2000-08-10
accepted
2000-08-29
Contributors
author
  • Department of Biochemistry, Michigan State University, East Lansing, MI 48824-1319, U.S.A.
author
  • Department of Biochemistry, Michigan State University, East Lansing, MI 48824-1319, U.S.A.
References
  • 1. Katzen, H.M. (1967) The multiple forms of mammalian hexokinase and their significance to the action of insulin. Adv. Enzyme Regul. 5, 335-356.
  • 2. Wilson, J.E. & Felgner, P.L. (1977) An inverse relation between mitochondrial hexokinase content and phosphoglucomutase activity of rat tissues. Mol. Cell. Biochem. 18, 39-47.
  • 3. Clarke, D.D. & Sokoloff, L. (1994) Circulation and energy metabolism in the brain; in Basic Neurochemistry (Siegel, G.J., Agranoff, B.W., Albers, R.W. & Molinoff, P.B., eds.) pp. 645- 680, Raven Press, New York.
  • 4. Crane, R.K. & Sols, A. (1953) The associacion of hexokinase with particulate fractions of brain and other tissue homogenates. J. Biol. Chem. 203, 273-292.
  • 5. Johnson, M.K. (1960) The intracellular distribution of glycolytic and other enzymes in rat-brain homogenates and mitochondrial preparations. Biochem. J. 77, 610-618
  • 6. Schwartz, G.P. & Basford, R.E. (1967) The isolation and purification of solubilized hexokinase from bovine brain. Biochemistry 6, 1070-1079.
  • 7. Bachelard, H.S. (1967) The subcellular distribution and properties of hexokinase in the guinea-pig cerebral cortex. Biochem. J. 104, 286-292.
  • 8. Redkar, V.D. & Kenkare, U.W. (1972) Bovine brain mitochondrial hexokinase. Solubilisation, purification, and role of sulfhydryl residues. J. Biol. Chem. 247, 7576-7584.
  • 9. Magnani, M., Serafini, G., Stocchi, V., Bossø, M. & Dacha, M. (1982) Solubilisation, purification, and properties of rabbit brain hexokinase. Arch. Biochem. Biophys. 216, 449- 454.
  • 10. BeltrandelRio, H. & Wilson, J.E. (1992) Coordinated regulation of cerebral glycolytic and oxidative metabolism, mediated by mitochondrially bound hexokinase dependent on intramitochondrially generated ATP. Arch. Biochem. Biophys. 296, 667-677.
  • 11. 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.
  • 12. Felgner, P.L., Messer, J.L. & Wilson, J.E. (1979) Purification of a hexokinase-binding protein from the outer mitochondrial membrane. J. Biol. Chem. 254, 4946-4949.
  • 13. Fiek, C., Benz, R., Roos, N. & Brdiczka, D. (1982) Evidence for identity between the hexokinase-binding protein and the mitochondrial porin in the outer membrane of rat liver mitochondria. Biochim. Biophys. Acta 688, 429-440.
  • 14. Lindén, M. Gellerfors, P. & Nelson, B.D. (1982) Pore protein and the hexokinase-binding protein from the outer membrane of rat liver mitochondria are identical. FEBS Lett. 141, 189-192.
  • 15. Colombini, M., Blachly-Dyson, E. & Forte, M. (1996) VDAC, a channel in the outer mitochondrial membrane; in Ion Channels (Narahishi, T., ed.) vol. 4, pp. 169-202, Plenum Press, New York.
  • 16. Kabir, F. & Wilson, J.E. (1993) Mitochondrial hexokinase in brain of various species: Differences in sensitivity to solubilisation by glucose-6-phosphate. Arch. Biochem. Biophys. 300, 641-650.
  • 17. Felgner, P.L. & Wilson, J.E. (1977) Effect of neutral salts on the interaction of rat brain hexokinase with the outer mitochondrial membrane. Arch. Biochem. Biophys. 182, 282-294.
  • 18. Kabir, F. & Wilson, J.E. (1994) Mitochondrial hexokinase in brain: Coexistence of forms differing in solubilisation by glucose-6-phosphate on the same mitochondria. Arch. Biochem. Biophys. 310, 410-416.
  • 19. Tolani, A.J. & Talwar, G.P. (1963) Differential metabolism of various brain regions: Biochemical heterogeneity of mitochondria. Biochem. J. 88, 357-362.
  • 20. Neidle, A., Van den Berg, C.J. & Grynbaum, A. (1969) The heterogeneity of rat brain mitochondria isolated on continuous sucrose gradients. J. Neurochem. 16, 225-234.
  • 21. Blokhuis, G.G.D. & Veldstra, H. (1970) Heterogeneity of mitochondria in rat brain. FEBS Lett. 11, 197-199.
  • 22. Wilson, J.E. (1972) The localization of latent brain hexokinase on synaptosomal mitochondria. Arch. Biochem. Biophys. 150, 96-104.
  • 23. De Pinto, V., Ludwig, O., Krause, J., Benz, R. & Palmieri, F. (1987) Porin pores of mitochondrial outer membranes from high and low eukaryotic cells: Biochemical and biophysical characterization. Biochim. Biophys. Acta 894, 109-119.
  • 24. Wilson, J.E. (1989) Rapid purification of mitochondrial hexokinase from rat brain by a single affinity chromatography step on Affi-Gel Blue. Prep. Biochem. 19, 13-21.
  • 25. Tuttle, J.P. & Wilson, J.E. (1970) Rat brain hexokinase: A kinetic comparison of soluble and particulate forms. Biochim. Biophys. Acta 212, 185-188.
  • 26. Bordier, C. (1981) Phase separation of integral membrane proteins in Triton X-114 solution. J. Biol. Chem. 256, 1604-1607.
  • 27. Needels, D.L. & Wilson, J.E. (1983) The identity of hexokinase activities from mitochondrial and cytoplasmic fractions of rat brain homogenates. J. Neurochem. 40, 1134-1143.
  • 28. Bligh, E.G. & Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Can. J. Med. Sci. 37, 911-917.
  • 29. Rouser, G. & Fleischer, S. (1967) Isolation characterisation, and determination of polar lipids of mitochondria. Methods Enzymol. 10, 385-406.
  • 30. Skipski, V.P. & Barclay, M. (1969) Thin-layer chromatography of lipids. Methods Enzymol. 14, 530-598.
  • 31. Parlo, R.A. & Coleman, P.S. (1984) Enhanced rate of citrate export from cholesterol-rich hepatoma mitochondria. The truncated Krebs cycle and other metabolic ramifications of mitochondrial membrane cholesterol. J. Biol. Chem. 259, 9997-10003.
  • 32. Singer, S.J. & Nicolson, G.L. (1972) The fluid mosaic model of the structure of cell membranes. Science 175, 720-731.
  • 33. Ureta, T., Smith, A.D. & Wilson, J.E. (1986) Hexokinase A from mammalian brain: Comparative peptide mapping and immunological studies with monoclonal antibodies. Arch. Biochem. Biophys. 246, 419-427.
  • 34. 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.
  • 35. Dorbani, L., Jancsik, V., Linden, M., Leterrier, J.F., Nelson, B.D. & Rendon, A. (1987) Subfractionation of the outer membrane of rat brain mitochondria: Evidence for the existence of a domain containing the porin-hexokinase complex. Arch. Biochem. Biophys. 252, 188-196.
  • 36. Parry, D.M. & Pedersen, P.L. (1990) Glucose catabolism in brain. Intracellular localization of hexokinase. J. Biol. Chem. 265, 1059-1066.
  • 37. Nishikawa, M., Nojima, S., Akiyama, T., Sankawa, U. & Inoue, K. (1984) Interaction of digitonin and its analogs with membrane cholesterol. J. Biochem. (Tokyo) 96, 1231-1239.
  • 38. Brdiczka, D. (1990) Interaction of mitochondrial porin with cytosolic proteins. Experientia 46, 161-167.
  • 39. Kottke, M., Adam, V., Riesinger, I., Bremm, G., Bosch, W., Brdiczka, D., Sandri, G. & Panfili, E. (1988) Mitochondrial boundary membrane contact sites in brain: Points of hexokinase and creatine kinase location, and control of Ca2+ transport. Biochim. Biophys. Acta 935, 87-102.
  • 40. Brdiczka, D. (1991) Contact sites between mitochondrial envelope membranes. Structure and function in energy- and protein-transfer. Biochim. Biophys. Acta 1071, 291-312.
  • 41. Craven, P.A., Goldblatt, P.J. & Basford, R.E. (1969) Brain hexokinase. The preparation of inner and outer mitochondrial membranes. Biochemistry 8, 3525-3532.
  • 42. Karnovsky, M.J., Kleinfeld, A.M., Hoover, R.L. & Klausner, R.D. (1982) The concept of lipid domains in membranes. J. Cell Biol. 94, 1-6.
  • 43. Hinderliter, A.K., Huang, J. & Feigenson, G.W. (1994) Detection of phase separation in fluid phosphatidylserine/phosphatidylcholine mixtures. Biophys. J. 67, 1906-1911.
  • 44. Brown, D.A. & London, E. (1997) Structure of detergent-resistent membrane domains: Does phase separation occur in biological membranes? Biochem. Biophys. Res. Commun. 240, 1-7.
  • 45. Boggs, J.M., Wood, D.D., Moscarello, M.A. & Papahadjopoulos, D. (1977) Phase separation of acidic and neutral phospholipids induced by human myelin basic protein. Biochemistry 16, 2325-2329.
Document Type
Publication order reference
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YADDA identifier
bwmeta1.element.bwnjournal-article-abpv47i4p1045kz
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