Voltage-dependent anion channels modulate mitochondrial metabolism in cancer cells: Regulation by free tubulin and erastin

Journal of Biological Chemistry

Volumn 288, Issue 17, 2013, Pages 11920-11929

  Maldonado, Eduardo N ^a,b,c   Sheldon, Kely L ^d,e   Dehart, David N ^a,b   Patnaik, Jyoti ^a,b   Manevich, Yefim ^a   Townsend, Danyelle M ^b,c   Bezrukov, Sergey M ^d   Rostovtseva, Tatiana K ^d   Lemasters, John J ^a,b,c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b Department of Drug Discovery and Biomedical Sciences ^*  (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^e JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE; HUMAN HEPATOMA CELLS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL METABOLISM; OUTER MEMBRANE; PLANAR BILAYERS; RESPIRATORY SUBSTRATES; VOLTAGE-DEPENDENT ANION CHANNELS;

DEPOLARIZATION; LIPID BILAYERS; METABOLISM; PHYSIOLOGY; PLANTS (BOTANY);

MITOCHONDRIA;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ERASTIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SMALL INTERFERING RNA; TUBULIN; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 1; VOLTAGE DEPENDENT ANION CHANNEL 2; VOLTAGE DEPENDENT ANION CHANNEL 3;

ARTICLE; CELL STRAIN HEPG2; CONTROLLED STUDY; DEPOLARIZATION; HEPATOMA CELL; HUMAN; HUMAN CELL; LIPID BILAYER; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CARCINOMA, HEPATOCELLULAR; GENE KNOCKDOWN TECHNIQUES; HEP G2 CELLS; HUMANS; LIPID BILAYERS; LIVER NEOPLASMS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NADP; NEOPLASM PROTEINS; OXIDATION-REDUCTION; PIPERAZINES; TUBULIN; VOLTAGE-DEPENDENT ANION CHANNELS;

EID: 84876936843     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.433847     Document Type: Article

References (51)

1. Warburg, O., Wind, F., and Negelein, E. (1927) The Metabolism of Tumors in the Body. J. Gen. Physiol 8, 519-530
2. Warburg, O. (1956) On the origin of cancer cells. Science 123, 309-314
3. Gambhir, S. S. (2002) Molecular imaging of cancer with positron emission tomography. Nat. Rev. Cancer 2, 683-693
4. Vander Heiden, M. G., Cantley, L. C., and Thompson, C. B. (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029-1033
5. +channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 11, 37-51
6. Mathupala, S. P., Ko, Y. H., and Pedersen, P. L. (2009) Hexokinase-2 bound to mitochondria: cancer's stygian link to the "Warburg Effect" and a pivotal target for effective therapy. Semin. Cancer Biol. 19, 17-24
7. Pedersen, P. L. (2007) Warburg, me and Hexokinase 2: Multiple discoveries of key molecular events underlying one of cancers' most common phenotypes, the "Warburg Effect", i.e., elevated glycolysis in the presence of oxygen. J. Bioenerg. Biomembr. 39, 211-222
8. Nakashima, R. A., Paggi, M. G., and Pedersen, P. L. (1984) Contributions of glycolysis and oxidative phosphorylation to adenosine 5-triphosphate production in AS-30D hepatoma cells. Cancer Res. 44, 5702-5706
9. Maldonado, E. N., Patnaik, J., Mullins, M. R., and Lemasters, J. J. (2010) Free tubulin modulates mitochondrial membrane potential in cancer cells. Cancer Res. 70, 10192-10201
10. Gellerich, F. N., Wagner, M., Kapischke, M., Wicker, U., and Brdiczka, D. (1993) Effect of macromolecules on the regulation of the mitochondrial outer membrane pore and the activity of adenylate kinase in the intermembrane space. Biochim. Biophys. Acta 1142, 217-227
11. Hodge, T., and Colombini, M. (1997) Regulation of metabolite flux through voltage-gating of VDAC channels. J. Membr. Biol. 157, 271-279
12. Lee, A. C., Zizi, M., and Colombini, M. (1994) Beta-NADH decreases the permeability of the mitochondrial outer membrane to ADP by a factor of 6. J. Biol. Chem. 269, 30974-30980
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. Bayrhuber, M., Meins, T., Habeck, M., Becker, S., Giller, K., Villinger, S., Vonrhein, C., Griesinger, C., Zweckstetter, M., and Zeth, K. (2008) Structure of the human voltage-dependent anion channel. Proc. Natl. Acad. Sci. U. S. A. 105, 15370-15375
15. Hiller, S., Garces, R. G., Malia, T. J., Orekhov, V. Y., Colombini, M., and Wagner, G. (2008) Solution structure of the integral human membrane protein VDAC-1 in detergent micelles. Science 321, 1206-1210
16. Ujwal, R., Cascio, D., Colletier, J. P., Faham, S., Zhang, J., Toro, L., Ping, P., and Abramson, J. (2008) The crystal structure of mouse VDAC1 at 2.3 A resolution reveals mechanistic insights into metabolite gating. Proc. Natl. Acad. Sci. U. S. A. 105, 17742-17747
17. Colombini, M. (1980) Structure and mode of action of a voltage dependent anion-selective channel (VDAC) located in the outer mitochondrial membrane. Ann. N. Y. Acad. Sci. 341, 552-563
18. Colombini, M., Yeung, C. L., Tung, J., and König, T. (1987) The mitochondrial outer membrane channel, VDAC, is regulated by a synthetic polyanion. Biochim. Biophys. Acta 905, 279-286
19. Mannella, C. A., Forte, M., and Colombini, M. (1992) Toward the molecular structure of the mitochondrial channel, VDAC. J. Bioenerg. Biomembr. 24, 7-19
20. Song, J., and Colombini, M. (1996) Indications of a common folding pattern for VDAC channels from all sources. J. Bioenerg. Biomembr. 28, 153-161
21. Lemasters, J. J., and Holmuhamedov, E. (2006) Voltage-dependent anion channel (VDAC) as mitochondrial governator-thinking outside the box. Biochim. Biophys. Acta 1762, 181-190
22. Maldonado, E. N., and Lemasters, J. J. (2012) Warburg revisited: regulation of mitochondrial metabolism by voltage-dependent anion channels in cancer cells. J. Pharmacol. Exp. Ther. 342, 637-641
23. Gurnev, P. A., Rostovtseva, T. K., and Bezrukov, S. M. (2011) Tubulinblocked state of VDAC studied by polymer and ATP partitioning. FEBS Lett. 585, 2363-2366
24. Rostovtseva, T. K., Sheldon, K. L., Hassanzadeh, E., Monge, C., Saks, V., Bezrukov, S. M., and Sackett, D. L. (2008) Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration. Proc. Natl. Acad. Sci. U. S. A. 105, 18746-18751
25. Timohhina, N., Guzun, R., Tepp, K., Monge, C., Varikmaa, M., Vija, H., Sikk, P., Kaambre, T., Sackett, D., and Saks, V. (2009) Direct measurement of energy fluxes from mitochondria into cytoplasm in permeabilized cardiac cells in situ: some evidence for Mitochondrial Interactosome. J. Bioenerg. Biomembr. 41, 259-275
26. Lemasters, J. J., Holmuhamedov, E. L., Czerny, C., Zhong, Z., and Maldonado, E. N. (2012) Regulation of mitochondrial function by voltage dependent anion channels in ethanol metabolism and the Warburg effect. Biochim. Biophys. Acta 1818, 1536-1544
27. Yagoda, N., von, Rechenberg, M., Zaganjor, E., Bauer, A. J., Yang, W. S., Fridman, D. J., Wolpaw, A. J., Smukste, I., Peltier, J. M., Boniface, J. J., Smith, R., Lessnick, S. L., Sahasrabudhe, S., and Stockwell, B. R. (2007) RAS-RAF-MEK-dependent oxidative cell death involving voltage-dependent anion channels. Nature 447, 864-868
28. Bauer, A. J., Gieschler, S., Lemberg, K. M., McDermott, A. E., and Stockwell, B. R. (2011) Functional model of metabolite gating by human voltagedependent anion channel 2. Biochemistry 50, 3408-3410
29. Lemasters, J. J., and Ramshesh, V. K. (2007) Imaging of mitochondrial polarization and depolarization with cationic fluorophores. Methods Cell Biol. 80, 283-295
30. Patterson, G. H., Knobel, S. M., Arkhammar, P., Thastrup, O., and Piston, D. W. (2000) Separation of the glucose-stimulated cytoplasmic and mitochondrial NAD (P) H responses in pancreatic islet beta cells. Proc. Natl. Acad. Sci. U. S. A. 97, 5203-5207
31. Moran, U., Phillips, R., and Milo, R. (2010) SnapShot: key numbers in biology. Cell 141, 1262
32. Rostovtseva, T. K., Kazemi, N., Weinrich, M., and Bezrukov, S. M. (2006) Voltage gating of VDAC is regulated by nonlamellar lipids of mitochondrial membranes. J. Biol. Chem. 281, 37496-37506
33. Colombini, M. (1989) Voltage gating in the mitochondrial channel, VDAC. J. Membr. Biol. 111, 103-111
34. Zizi, M., Byrd, C., Boxus, R., and Colombini, M. (1998) The voltage-gating process of the voltage-dependent anion channel is sensitive to ion flow. Biophys. J. 75, 704-713
35. Nieminen, A. L., Byrne, A. M., Herman, B., and Lemasters, J. J. (1997) Mitochondrial permeability transition in hepatocytes induced by t-BuOOH: NAD (P) H and reactive oxygen species. Am. J. Physiol. 272, C1286-C1294
36. Sies, H., and Gerstenecker, C. (1972) Oxidation in the NADP system and release of GSSG from hemoglobin-free perfused rat liver during peroxidatic oxidation of glutathione by hydroperoxides. FEBS Lett. 27, 171-175
37. Weinberg, F., and Chandel, N. S. (2009) Mitochondrial metabolism and cancer. Ann. N. Y. Acad. Sci. 1177, 66-73
38. Colombini, M. (2004) VDAC: the channel at the interface between mitochondria and the cytosol. Mol. Cell Biochem. 256-257, 107-115
39. Rostovtseva, T. K., and Bezrukov, S. M. (2008) VDAC regulation: role of cytosolic proteins and mitochondrial lipids. J. Bioenerg. Biomembr. 40, 163-170
40. Shoshan-Barmatz, V., De Pinto, V, Zweckstetter, M., Raviv, Z., Keinan, N., and Arbel, N. (2010) VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol. Aspects Med. 31, 227-285
41. De Pinto, V., Guarino, F., Guarnera, A., Messina, A., Reina, S., Tomasello, F. M., Palermo, V., and Mazzoni, C. (2010) Characterization of human VDAC isoforms: a peculiar function for VDAC3? Biochim. Biophys. Acta 1797, 1268-1275
42. Prins, J. M., Park, S., and Lurie, D. I. (2010) Decreased expression of the voltage-dependent anion channel in differentiated PC-12 and SH-SY5Y cells following low-level Pb exposure. Toxicol. Sci. 113, 169-176
43. Monge, C., Beraud, N., Kuznetsov, A. V., Rostovtseva, T., Sackett, D., Schlattner, U., Vendelin, M., and Saks, V. A. (2008) Regulation of respiration in brain mitochondria and synaptosomes: restrictions of ADP diffusion in situ, roles of tubulin, and mitochondrial creatine kinase. Mol. Cell Biochem. 318, 147-165
44. André, N., Braguer, D., Brasseur, G., Gonçalves, A., Lemesle-Meunier, D., Guise, S., Jordan, M. A., and Briand, C. (2000) Paclitaxel induces release of cytochrome c from mitochondria isolated from human neuroblastoma cells. Cancer Res. 60, 5349-5353
45. André, N., Carré, M., Brasseur, G., Pourroy, B., Kovacic, H., Briand, C., and Braguer, D. (2002) Paclitaxel targets mitochondria upstream of caspase activation in intact human neuroblastoma cells. FEBS Lett. 532, 256-260
46. Hu, Y., Moraes, C. T., Savaraj, N., Priebe, W., and Lampidis, T. J. (2000) Rho (0) tumor cells: a model for studying whether mitochondria are targets for rhodamine 123, doxorubicin, and other drugs. Biochem. Pharmacol. 60, 1897-1905
47. Craigen, W. J., and Graham, B. H. (2008) Genetic strategies for dissecting mammalian and Drosophila voltage-dependent anion channel functions. J. Bioenerg. Biomembr. 40, 207-212
48. Xu, X., Decker, W., Sampson, M. J., Craigen, W. J., and Colombini, M. (1999) Mouse VDAC isoforms expressed in yeast: channel properties and their roles in mitochondrial outer membrane permeability. J. Membr. Biol. 170, 89-102
49. Anflous, K., Armstrong, D. D., and Craigen, W. J. (2001) Altered mitochondrial sensitivity for ADP and maintenance of creatine-stimulated respiration in oxidative striated muscles from VDAC1-deficient mice. J. Biol. Chem. 276, 1954-1960
50. Cheng, E. H., Sheiko, T. V., Fisher, J. K., Craigen, W. J., and Korsmeyer, S. J. (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301, 513-517
51. Sampson, M. J., Decker, W. K., Beaudet, A. L., Ruitenbeek, W., Armstrong, D., Hicks, M. J., and Craigen, W. J. (2001) Immotile sperm and infertility in mice lacking mitochondrial voltage-dependent anion channel type 3. J. Biol. Chem. 276, 39206-39212