In self-defence: Hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death

Biochemical Journal

Volumn 377, Issue 2, 2004, Pages 347-355

  Azoulay Zohar, Heftsi ^a   Israelson, Adrian ^a   Abu Hamad, Salah ^a   Shoshan Barmatz, Varda ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Apoptosis; Hexokinase; Mitochondria; Permeability transition pore; Voltage dependent anion channel (VDAC)

Indexed keywords

ANTIBODIES; BIOSYNTHESIS; CELLS; TUMORS;

APOPTOSIS; MITOCHONDRIA;

BIOCHEMISTRY;

GLUCOSE 6 PHOSPHATE; HEXOKINASE; STAUROSPORINE; VOLTAGE GATED CALCIUM CHANNEL;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIBODY SPECIFICITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL DEATH; CELL MEMBRANE PERMEABILITY; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; DEFENSE MECHANISM; HYDROPHOBICITY; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL; VASCULAR SMOOTH MUSCLE; YEAST;

ANIMALS; APOPTOSIS; CELL LINE; CYTOCHROMES C; GLUCOSE-6-PHOSPHATE; HEXOKINASE; HUMANS; ION CHANNELS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; PATCH-CLAMP TECHNIQUES; PORINS; RATS; STAUROSPORINE; U937 CELLS; VOLTAGE-DEPENDENT ANION CHANNELS;

ANIMALIA;

EID: 0942290437     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031465     Document Type: Article

References (50)

1. Arora, K. K. and Pedersen, P. L. (1988) Functional significance of mitochondrial bound hexokinase in tumor cell metabolism. Evidence for preferential phosphorylation of glucose by intramitochondrially generated ATP. J. Biol. Chem. 263, 17422-17428
2. Pedersen, P. L., Mathupala, S., Rempel, A., Geschwind, J. F. and Ko, Y. H. (2002) Mitochondrial bound type II hexokinase: a key player in the growth and survival of many cancers and an ideal prospect for therapeutic intervention. Biochim Biophys. Acta 1555, 14-20
3. Rempel, A., Bannasch, P. and Mayer, D. (1994) Differences in expression and intracellular distribution of hexokinase isoenzymes in rat liver cells of different transformation stages. Biochim. Biophys. Acta 1219, 660-668
4. Sebastian, S. and Kenkare, U. W. (1997) Insulin like growth factor I induces tumor hexokinase RNA expression in cancer cells. Biochem. Biophys. Res. Commun. 235, 389-393
5. Rose, I. A., Warms, J. V. and Kosow, D. P. (1974) Specificity for the glucose-6-P inhibition site of hexokinase. Arch. Biochem. Biophys. 164, 729-735
6. Gottlob, K., Majewski, N., Kennedy, S., Kandel, E., Robey, R. B. and Hay, N. (2001) Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev. 1 1406-1418
7. Bryson, J. M., Coy, P. E., Gottlob, K., Hay, N. and Robey, R. (2002) Increased hexokinase activity, of either ectopic or endogenous origin, protects renal epithelial cells against acute oxidant-induced cell death. J. Biol. Chem. 277, 11392-11400
8. Pastorino, J. G., Shulga, N. and Hoek, J. B. (2002) Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis. J. Biol. Chem. 277, 7610-7618
9. Shinohara, Y., Ishida, T., Hino, M., Yamazaki, N., Baba, Y. and Terada, H. (2000) Characterization of porin isoforms expressed in tumor cells. Eur. J. Biochem. 267, 6067-6073
10. Benz, R. (1994) Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins. Biochim. Biophys. Acta 1197, 167-196
11. Colombini, M. (1994) Anion channel in the mitochondrial outer membrane. Curr. Top. Membr. 42, 73-101
12. Gincel, D., Zaid, H. and Shoshan-Barmatz, V. (2001) Calcium binding and translocation by the voltage-dependent anion channel: a possible regulatory mechanism in mitochondrial function. Biochem. J. 358, 147-155
13. Rostovtseva, T. and Colombini, M. (1997) VDAC channels mediate and gate the flow of ATP: implications for the regulation of mitochondrial function. Biophys. J. 72, 1954-1962
14. Hodge, T. and Colombini, M. (1997) Regulation of metabolite flux through voltage-gating of VDAC channels. J. Membr. Biol. 157, 271-279
15. Zoratti, M. and Szabo, I. (1995) The mitochondrial permeability transition. Biochim. Biophys. Acta 1241, 139-176
16. Crompton, M., Virji, S., Doyle, V., Johnson, N. and Ward, J. M. (1999) The mitochondrial permeability transition pore. Biochem. Soc. Symp. 66, 167-79
17. Zamzami, N. and Kroemer, G. (2003) Apoptosis: mitochondrial membrane permeabilization - the (w)hole story? Curr. Biol. 13, 71-73
18. Crompton, M. (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341, 233-249
19. Lemasters, J. J., Qian, T., Bradham, C. A., Brenner, D. A., Cascio, W. E., Trost, L. C., Nishimura, Y., Nieminen, A. L. and Herman, B. (1999) Mitochondrial dysfunction in the pathogenesis of necrotic and apoptotic cell death. J. Bioenerg. Biomembr. 31, 305-319
20. Wilson, J. E. (1995) Hexokinases. Rev. Physiol. Biochem. Pharmacol. 126, 65-198
21. Xie, G. and Wilson, J. E. (1988) Rat brain hexokinase: Hydrophobic amino-terminus of the mitochondrially bound enzyme is inserted in the lipid bilayer. Arch. Biochem. Biophys. 267, 803-810
22. Beutner, G., Ruck, A., Riede, B. and 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
23. Vyssokikh, M. Y. and Brdiczka, D. (2003) The function of complexes between the outer mitochondrial membrane pore (VDAC) and the adenine nucleotide translocase in regulation of energy metabolism and apoptosis, Acta Biochim. Pol. 50, 389-404
24. Linden, M., Gellerfors, P. and 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
25. Babel, D., Walter, G., Gotz, H., Thinnes, F. P., Jurgens, L., Konig, U., and Hilschmann, N. (1991) Studies on human porin. VI. Production and characterization of eight monoclonal mouse antibodies against the human VDAC "Porin 31HL" and their application for histotopological studies in human skeletal muscle. Biol. Chem. Hoppe Seyler 372, 1027-1034
26. Johnson, D. L. H. (1967) Rat liver mitochondria preparation. Methods Enzymol. 10, 94-96
27. 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
28. Azoulay-Zohar, H. and Aflalo, C. (2000) Binding of rat brain hexokinase to recombinant yeast mitochondria: identification of necessary physico-chemical determinants. Eur. J. Biochem. 267, 2973-2980
29. Gornall, A. G., Bardawill, C. J. and David, M. M. (1949) Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 177, 751-766
30. Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem, 72, 248-254
31. Gincel, D., Silberberg, S. D. and Shoshan-Barmatz, V. (2000) Modulation of the voltage-dependent anion channel (VDAC) by glutamate. J. Bioenerg. Biomembr. 32, 571-583
32. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature (London) 227, 680-685
33. Shoshan-Barmatz, V. and Gincel, D. (2003) The voltage-dependent anion channel: characterization, modulation and role in mitochondrial function in cell life and death. Cell. Biochem. Biophys. 39, in the press
34. Tsujimoto Y. and Shimizu, S. (2002) The voltage-dependent anion channel: an essential player in apoptosis. Biochimie 84, 187-193
35. Halestrap, A. P., Doran, E., Gillespie, J. P. and O'Toole, A. (2000) Mitochondria and cell death. Biochem. Soc. Trans. 28, 170-177
36. Zamzami, N. and Kroemer, G. (2001) The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell. Biol. 2, 67-71
37. Xie, G. and Wilson, J. E. (1990) Tetrameric structure of mitochondrially bound rat brain hexokinase: a crosslinking study. Arch. Biochem. Biophys. 276, 285-293
38. Aflalo, C. and Azoulay, H. (1998) Binding of rat brain hexokinase to recombinant yeast mitochondria: effect of environmental factors and the source of porin. J. Bioenerg. Biomembr. 30, 245-255
39. Vieira, H. L., Haouzi, D., El Hamel, C., Jacotot, E., Belzacq, A. S., Brenner, C. and Kroemer, G. (2000) Permeabilization of the mitochondrial inner membrane during apoptosis: impact of the adenine nucleotide translocator. Cell Death Differ. 7, 1146-1154
40. 2+-activated hydrophilic channel of the mitochondrial inner membrane by nucleotides. J. Membr. Biol. 54, 231-236
41. Novgorodov, S. A., Gudz, T. I., Jung, D. W. and Brierley, G. P. (1991) The nonspecific inner membrane pore of liver mitochondria: modulation of cyclosporin sensitivity by ADP at carboxyatractyloside-sensitive and insensitive sites. Biochem. Biophys. Res. Commun. 180, 33-38
42. Shimizu, S., Matsuoka, Y., Shinohara, Y., Yoneda, Y. and Tsujimoto, Y. (2001) Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. J. Cell Biol. 152, 237-250
43. Adams, J. M. and Cory, S. (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281, 1322-1326
44. Ichas, F. and Mazat, J. P. (1998) From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low-to high-conductance state. Biochim. Biophys. Acta 1366, 33-50
45. Liu, X., Kim, C. N., Yang, J., Jemmerson, R. and Wang, X. (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86, 147-157
46. Brdiczka, D., Beutner, G., Ruck, A., Dolder, M. and Wallimann, T. (1998) The molecular structure of mitochondrial contact sites. Their role in regulation of energy metabolism and permeability transition. Biofactors 8, 235-242
47. Fanciulli, M., Paggi, M. G., Bruno, T., Del Carlo, C., Bonetto, F., Gentile, F. P. and Floridi, A. (1994) Glycolysis and growth rate in normal and in hexokinase-transfected NIH-3T3 cells. Oncol. Res. 6, 405-409
48. Oltvai, Z. N., Milliman, C. L. and Korsmeyer, S. J. (1993) Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74, 609-619
49. Hashimoto, M. and Wilson, J. E. (2000) Membrane potential-dependent conformational changes in mitochondrially bound hexokinase of brain. Arch. Biochem. Biophys. 384, 163-173
50. Bustamante, E., Morris, H. P. and Pedersen, P. L. (1981) Energy metabolism of tumor cells. Requirement for a form of hexokinase with a propensity for mitochondrial binding. J. Biol. Chem. 256, 8699-8704