Hexokinase inhibits flux of fluorescently labeled ATP through mitochondrial outer membrane porin

FEBS Letters

Volumn 584, Issue 11, 2010, Pages 2397-2402

  Perevoshchikova, Irina V ^a   Zorov, Savva D ^a   Kotova, Elena A ^a   Zorov, Dmitry B ^a   Antonenko, Yuri N ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Fluorescence correlation spectroscopy; Hexokinase; Mitochondria; Voltage dependent anion channel

Indexed keywords

ADENOSINE TRIPHOSPHATE; HEXOKINASE; HEXOKINASE 2; PORIN; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; FLUORESCENCE CORRELATION SPECTROSCOPY; HEART MITOCHONDRION; LIVER MITOCHONDRION; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; HEXOKINASE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PORINS; RATS; VOLTAGE-DEPENDENT ANION CHANNEL 1; VOLTAGE-DEPENDENT ANION CHANNELS;

RATTUS;

EID: 77952951097     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.04.033     Document Type: Article

References (44)

1. Colombini M. A candidate for the permeability pathway of the outer mitochondrial membrane. Nature 1979, 279:643-645.
2. Colombini M. VDAC: the channel at the interface between mitochondria and the cytosol. Mol. Cell. Biochem. 2004, 256-257:107-115.
3. Mannella C.A., Forte M., Colombini M. Toward the molecular structure of the mitochondrial channel. VDAC J. Bioenergy Biomembrane 1992, 24:7-19.
4. Mannella C.A., Kinnally K.W. Reflections on VDAC as a voltage-gated channel and a mitochondrial regulator. J. Bioenergy Biomembrane 2008, 40:149-155.
5. Ujwal R., Cascio D., Colletier J.P., Faham S., Zhang J., Toro L., Ping P., Abramson J. The crystal structure of mouse VDAC1 at 2.3Å resolution reveals mechanistic insights into metabolite gating. Proc. Natl. Acad. Sci. USA 2008, 105:17742-17747.
6. Rostovtseva T., Colombini M. ATP flux is controlled by a voltage-gated channel from the mitochondrial outer membrane. J. Biol. Chem. 1996, 271:28006-28008.
7. Rostovtseva T., Colombini M. VDAC channels mediate and gate the flow of ATP: implications for the regulation of mitochondrial function. Biophys. J. 1997, 72:1954-1962.
8. Brdiczka D.G., Zorov D.B., Sheu S.S. Mitochondrial contact sites: their role in energy metabolism and apoptosis. Biochim. Biophys. Acta 2006, 1762:148-163.
9. Rostovtseva T.K., Bezrukov S.M. VDAC regulation: role of cytosolic proteins and mitochondrial lipids. J. Bioenergy Biomembrane 2008, 40:163-170.
10. Wilson J.E. Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J. Exp. Biol. 2003, 206:2049-2057.
11. Pastorino J.G., Hoek J.B. Regulation of hexokinase binding to VDAC. J. Bioenergy Biomembrane 2008, 40:171-182.
12. Shoshan-Barmatz V., Keinan N., Zaid H. Uncovering the role of VDAC in the regulation of cell life and death. J. Bioenergy Biomembrane 2008, 40:183-191.
13. Shoshan-Barmatz V., Zakar M., Rosenthal K., Abu-Hamad S. Key regions of VDAC1 functioning in apoptosis induction and regulation by hexokinase. Biochim. Biophys. Acta 2009, 1787:421-430.
14. Lemasters J.J., Holmuhamedov E. Voltage-dependent anion channel (VDAC) as mitochondrial governator - thinking outside the box. Biochim. Biophys. Acta 2006, 1762:181-190.
15. Zorov D.B., Isaev N.K., Plotnikov E.Y., Zorova L.D., Stelmashook E.V., Vasileva A.K., Arkhangelskaya A.A., Khrjapenkova T.G. The mitochondrion as janus bifrons. Biochemistry (Moscow) 2007, 72:1115-1126.
16. Robey R.B., Hay N. Mitochondrial hexokinases, novel mediators of the antiapoptotic effects of growth factors and Akt. Oncogene 2006, 25:4683-4696.
17. Arzoine L., Zilberberg N., Ben Romano R., Shoshan-Barmatz V. Voltage-dependent anion channel 1-based peptides interact with hexokinase to prevent its anti-apoptotic activity. J. Biol. Chem. 2009, 284:3946-3955.
18. Azoulay-Zohar H., Israelson A., Abu-Hamad S., Shoshan-Barmatz V. In self-defence: hexokinase promotes voltage-dependent anion channel closure and prevents mitochondria-mediated apoptotic cell death. Biochem. J. 2004, 377:347-355.
19. Abu-Hamad S., Zaid H., Israelson A., Nahon E., Shoshan-Barmatz V. Hexokinase-I protection against apoptotic cell death is mediated via interaction with the voltage-dependent anion channel-1: mapping the site of binding. J. Biol. Chem. 2008, 283:13482-13490.
20. Armbruster A., Hohn C., Hermesdorf A., Schumacher K., Borsch M., Gruber G. Evidence for major structural changes in subunit C of the vacuolar ATPase due to nucleotide binding. FEBS Lett. 2005, 579:1961-1967.
21. Hess S.T., Huang S., Heikal A.A., Webb W.W. Biological and chemical applications of fluorescence correlation spectroscopy: a review. Biochemistry 2002, 41:697-705.
22. Chiantia S., Ries J., Schwille P. Fluorescence correlation spectroscopy in membrane structure elucidation. Biochim. Biophys. Acta 2009, 1788:225-233.
23. Perevoshchikova I.V., Zorov D.B., Antonenko Y.N. Peak intensity analysis as a method for estimation of fluorescent probe binding to artificial and natural nanoparticles: tetramethylrhodamine uptake by isolated mitochondria. Biochim. Biophys. Acta 2008, 1778:2182-2190.
24. Krichevsky O., Bonnet G. Fluorescence correlation spectroscopy: the technique and its applications. Rep. Prog. Phys. 2002, 65:251-297.
25. van den Bogaart G., Kusters I., Velasquez J., Mika J.T., Krasnikov V., Driessen A.J., Poolman B. Dual-color fluorescence-burst analysis to study pore formation and protein-protein interactions. Methods 2008, 46:123-130.
26. Johnson D., Lardy H. Isolation of liver or kidney mitochondria. Methods Enzymol. 1967, 10:94-96.
27. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., Klenk D.C. Measurement of protein using bicinchoninic acid. Anal. Biochem. 1985, 150:76-85.
28. Zelenina E.V., Avramova L.V., Goncharova N.I. Preparation of hexokinase isoenzyme II with expressed adsorption properties. Biokhimiia 1991, 56:1096-1103.
29. Abu-Hamad S., Sivan S., Shoshan-Barmatz V. The expression level of the voltage-dependent anion channel controls life and death of the cell. Proc. Natl. Acad. Sci. USA 2006, 103:5787-5792.
30. Vignais P.V. Molecular and physiological aspects of adenine nucleotide transport in mitochondria. Biochim. Biophys. Acta 1976, 456:1-38.
31. Colombini M., Yeung C.L., Tung J., Konig T. The mitochondrial outer membrane channel, VDAC, is regulated by a synthetic polyanion. Biochim. Biophys. Acta 1987, 905:279-286.
32. Benz R., Wojtczak L., Bosch W., Brdiczka D. Inhibition of adenine nucleotide transport through the mitochondrial porin by a synthetic polyanion. FEBS Lett. 1988, 231:75-80.
33. Pfaff E., Klingenberg M., Heldt H.W. Unspecific permeation and specific exchange of adenine nucleotides in liver mitochondria. Biochim. Biophys. Acta 1965, 104:312-315.
34. Winkler H.H., Bygrave F.L., Lehninger A.L. Characterization of the atractyloside-sensitive adenine nucleotide transport system in rat liver mitochondria. J. Biol. Chem. 1968, 243:20-28.
35. Florke H., Thinnes F.P., Winkelbach H., Stadtmuller U., Paetzold G., Morys-Wortmann C., Hesse D., Sternbach H., Zimmermann B., Kaufmann-Kolle P., Heiden M., Karabinos A., Reymann S., Lalk V.E., Hilschmann N. Channel active mammalian porin, purified from crude membrane fractions of human B lymphocytes and bovine skeletal muscle, reversibly binds adenosine triphosphate (ATP). Biol. Chem. Hoppe Seyler 1994, 375:513-520.
36. Yehezkel G., Hadad N., Zaid H., Sivan S., Shoshan-Barmatz V. Nucleotide-binding sites in the voltage-dependent anion channel: characterization and localization. J. Biol. Chem. 2006, 281:5938-5946.
37. Rostovtseva T.K., Komarov A., Bezrukov S.M., Colombini M. Dynamics of nucleotides in VDAC channels: structure-specific noise generation. Biophys. J. 2002, 82:193-205.
38. Lee A.C., Zizi M., Colombini M. Beta-NADH decreases the permeability of the mitochondrial outer membrane to ADP by a factor of 6. J. Biol. Chem. 1994, 269:30974-30980.
39. Nakashima R.A., Mangan P.S., Colombini M., Pedersen P.L. Hexokinase receptor complex in hepatoma mitochondria: evidence from N,N'-dicyclohexylcarbodiimide-labeling studies for the involvement of the pore-forming protein VDAC. Biochemistry 1986, 25:1015-1021.
40. Pastorino J.G., Shulga N., Hoek J.B. Mitochondrial binding of hexokinase II inhibits Bax-induced cytochrome c release and apoptosis. J. Biol. Chem. 2002, 277:7610-7618.
41. Beltrandelrio H., Wilson J.E. Coordinated regulation of cerebral glycolytic and oxidative metabolism, mediated by mitochondrially bound hexokinase dependent on intramitochondrially generated ATP. Arch. Biochem. Biophys. 1992, 296:667-677.
42. Bacterial and Eukaryotic Porins: Structure, Function, Mechanism 2004, Wiley-VCH, Weinheim. R. Benz (Ed.).
43. Kholodenko B.N., Cascante M., Westerhoff H.V. Control theory of metabolic channelling. Mol. Cell. Biochem. 1995, 143:151-168.
44. Lemasters J.J. Modulation of mitochondrial membrane permeability in pathogenesis, autophagy and control of metabolism. J. Gastroenterol. Hepatol. 2007, 22(Suppl. 1):S31-S37.