Molecular mechanism for the selective impairment of cancer mitochondrial function by a mitochondrially targeted vitamin e analogue

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 9, 2012, Pages 1597-1607

  Rodríguez Enríquez, Sara ^a,b   Hernández Esquivel, Luz ^a   Marín Hernández, Alvaro ^a   Dong, Lan Feng ^c   Akporiaye, Emmanuel T ^d   Neuzil, Jiri ^c,e   Ralph, Stephen J ^c   Moreno Sánchez, Rafael ^a  

^a INSTITUTO NACIONAL DE CARDIOLOGÍA IGNACIO CHÁVEZ   (Mexico)

^b INSTITUTO NACIONAL DE CANCEROLOGÍA   (Mexico)

^c GRIFFITH UNIVERSITY   (Australia)

^d EARLE A CHILES RESEARCH INSTITUTE   (United States)

^e INSTITUTE OF BIOTECHNOLOGY   (Czech Republic)

Author keywords

Mitochondria; Respiratory complex II; Tumor cells; Uncoupling; Vitamin E analogue

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA TOCOPHEROL; ALPHA TOCOPHEROL SUCCINATE; ALPHA TOCOPHERYL ACETYL ETHER; CALCIUM; TRIPHENYLPHOSPHONIUM TAGGED VITAMIN E SUCCINATE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BREATHING RATE; CALCIUM TRANSPORT; CELL ISOLATION; CELL LINE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG MECHANISM; HUMAN; HUMAN CELL; LIVER CELL; LIVER CELL CARCINOMA; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; RAT; SUBMITOCHONDRIAL PARTICLE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CATTLE; CELL LINE, TUMOR; CELL RESPIRATION; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NEOPLASMS; RATS; VITAMIN E;

BOVINAE; RATTUS; RODENTIA; TOSCANA VIRUS;

EID: 84862255369     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.05.005     Document Type: Article

References (47)

1. S. Rodríguez-Enríquez, A. Marín-Hernández, J.C. Gallardo-Pérez, L. Carreño-Fuentes, and R. Moreno-Sánchez Targeting of cancer energy metabolism Mol. Nutr. Food Res. 53 2009 29 48
2. J. Rohlena, L.F. Dong, S.J. Ralph, and J. Neuzil Anti-cancer drugs targeting the mitochondrial electron redox chain Antioxid. Redox Signal. 15 2011 2951 2974
3. P. Horak, A.R. Crawford, D.D. Vadysirisack, Z.M. Nash, M.P. DeYoung, D. Sgroi, and L.W. Ellisen Negative feedback control of HIF-1 through REDD1-regulated ROS suppresses tumorigenesis Proc. Natl. Acad. Sci. U. S. A. 107 2010 4675 4680
4. S.J. Ralph, S. Rodríguez-Enríquez, J. Neuzil, E. Saavedra, and R. Moreno-Sánchez The causes of cancer revisited: hypoxia and glucose deprivation drive mitochondrial ROS induced oncogenic mutation and malignant transformation - implication for the selective targeting of cancer therapy Mol. Aspects Med. 31 2010 145 170
5. L.R. Cavalli, and B.C. Liang Mutagenesis, tumorigenicity, and apoptosis: are the mitochondria involved? Mutat. Res. 398 1998 19 26
6. J.S. Penta, F.M. Johnson, J.T. Wachsman, and W.C. Copeland Mitochondrial DNA in human malignancy Mutat. Res. 488 2001 119 133 (Pubitemid 32436427)
7. T. Murata, H. Hibasami, S. Maekawa, T. Tagawa, and K. Nakashima Preferential binding of cisplatin to mitochondrial DNA and suppression of ATP generation in human malignant melanoma cells Biochem. Int. 20 1990 949 955 (Pubitemid 20142738)
8. O.A. Olivero, C. Semino, A. Kassim, D.M. Lopez-Larraza, and M.C. Poirer Preferential binding of cisplatin to mitochondrial DNA of Chinese hamster ovary cells Mutat. Res. 346 1995 221 230
9. D.A. Clayton, J.N. Doda, and E.C. Friedberg The absence of a pyrimidine dimer repair mechanism in mammalian mitochondria Proc. Natl. Acad. Sci. U. S. A. 71 1974 2777 2781
10. G. Ara, T. Kusumoto, T.T. Korbut, F. Cullere-Luengo, and B.A. Teicher Cisdiamminedichloroplatinum (II) resistant human tumor cell lines are collaterally sensitive to PtCl4 (RH-123) 2: evidence for mitochondrial involvement Cancer Res. 54 1994 1497 1502
11. J. Neuzil, T. Weber, N. Gellert, and C. Weber Selective cancer cell killing by a-tocopheryl succinate Br. J. Cancer 84 2001 87 89 (Pubitemid 32102509)
12. L.F. Dong, R. Freeman, J. Liu, R. Zobalova, A. Marín- Hernández, M. Stantic, J. Rohlena, S. Rodríguez-Enríquez, K. Valis, B. Butcher, J. Goodwin, U.T. Brunk, P.K. Witting, R. Moreno-Sánchez, I.E. Scheffler, S.J. Ralph, and J. Neuzil Suppression of tumour growth in vivo by the mitocan α-TOS requires respiratory complex II Clin. Cancer Res. 15 2009 1593 1600
13. L.F. Dong, V.J. Jameson, D. Tilly, J. Cerny, E. Mahdavian, A. Marín-Hernández, L. Hernández-Esquivel, S. Rodríguez-Enríquez, J. Stursa, P.K. Witting, B. Stantic, J. Rohlena, J. Truksa, K. Kluckova, J.C. Dyason, M. Ledvina, B.A. Salvatore, R. Moreno-Sánchez, M.J. Coster, S.J. Ralph, R.A. Smith, and J. Neuzil Mitochondrial targeting of vitamin E succinate enhances its pro-apoptotic and anti-cancer activity via mitochondrial complex II J. Biol. Chem. 286 2011 3717 3728
14. L.F. Dong, P. Low, J.C. Dyason, X.F. Wang, L. Prochazka, P.K. Witting, R. Freeman, E. Swettenham, K. Valis, J. Liu, R. Zobalova, J. Turanek, D.R. Spitz, F.E. Domann, I.E. Scheffler, S.J. Ralph, and J. Neuzil α-Tocopheryl succinate induces apoptosis by targeting ubiquinone-binding sites in mitochondrial respiratory complex II Oncogene 27 2008 4324 4335 (Pubitemid 352010000)
15. L/Bcl-2 function J. Biol. Chem. 281 2006 11819 11825 (Pubitemid 43855442)
16. S.J. Ralph, R. Moreno-Sánchez, R. Neuzil, and S. Rodríguez-Enríquez Inhibitors of succinate:quinone reductase/complex II regulating production of mitochondrial reactive oxygen species protect normal cells from ischemic damage but cause cancer cell death Pharm. Res. 112 2011 2703 2715
17. C. Beltrán, M. Tuena de Gómez-Puyou, A. Gómez-Puyou, and A. Darszon Release of the inhibitory action of the natural ATPase inhibitor protein on the mitochondrial ATPase Eur. J. Biochem. 144 1984 151 157 (Pubitemid 14012150)
18. + 2 concentrations J. Biol. Chem. 260 1985 4028 4034 (Pubitemid 15096469)
19. F. López-Gómez, M.E. Torres-Márquez, and R. Moreno-Sánchez Control of oxidative phosphorylation in AS-30D hepatoma mitochondria Int. J. Biochem. 25 1993 373 377 (Pubitemid 23071815)
20. S. Rodríguez-Enríquez, M.E. Torres-Márquez, and R. Moreno-Sánchez Substrate oxidation and ATP supply in AS-30D hepatoma cells Arch. Med. Res. 29 2000 1 12
21. S. Rodríguez-Enríquez, P.A. Vital-González, F.L. Flores-Rodríguez, A. Marín-Hernández, L. Ruiz-Azuara, and R. Moreno-Sánchez Control of cellular proliferation by modulation of oxidative phosphorylation in human and rodent fast-growing tumor cells Toxicol. Appl. Pharmacol. 215 2006 208 217 (Pubitemid 44190002)
22. M.N. Berry, and D.S. Friend High-yield preparation of isolated rat liver parenchymal cells. A biochemical and fine structural study J. Cell Biol. 43 1969 506 520
23. A. Atlante, S. Passarella, P. Pierro, C. Di Martino, and E. Quagliariello The mechanism of proline/glutamate antiport in rat kidney mitochondria. Energy dependence and glutamate-carrier involvement Eur. J. Biochem. 241 1996 171 177 (Pubitemid 26342986)
24. H. Rottenberg, and R. Moreno-Sánchez The proton pumping activity of H(+)-ATPases: an improved fluorescence assay Biochim. Biophys. Acta 1183 1993 161 170 (Pubitemid 23322964)
25. M. Mandalá, G. Serck-Hanssen, G. Martino, and K.B. Helle The fluorescent cationic dye rhodamine 6G as a probe for membrane potential in bovine aortic endothelial cells Anal. Biochem. 274 1999 1 6 (Pubitemid 29466348)
26. L.V. Johnson, M.L. Walsh, B.J. Bockis, and L.B. Chen Monitoring of relative mitochondrial membrane potential in living cells by fluorescence microscopy J. Cell Biol. 88 1981 526 535 (Pubitemid 11097944)
27. F. Pacheco-Moisés, J.J. García, J.S. Rodríguez- Zavala, and R. Moreno-Sánchez Sulfite and membrane energization induce two different active states of the Paracoccus denitrificans F0F1-ATPase Eur. J. Biochem. 267 2000 993 1000 (Pubitemid 30108316)
28. M. Nishimura, T. Ito, and B. Chance Studies on bacterial phosphorylation. III. A sensitive and rapid method of determination of photophosphorylation Biochim. Biophys. Acta 59 1962 177 182
29. 2 + from heart and kidney mitochondria by peripheral-type benzodiazepine receptor ligands Int. J. Biochem. 23 1991 207 213
30. J.M. Armstrong The molar extinction coefficient of 2,6 dichlorophenol indophenols Biochim. Biophys. Acta 86 1964 194 197
31. R. Covián, and R. Moreno-Sánchez Role of protonatable groups of bovine heart bc1 complex in ubiquinol binding and oxidation Eur. J. Biochem. 268 2001 5783 5790 (Pubitemid 33079312)
32. H.U. Bergmeyer Metabolites 1, carbohydrates H.U. Bergmeyer, Methods of Enzymatic Analysis 1983 Weinheim Verlag Chemie Germany
33. C.A. Yu, L. Yu, and T.E. King Reconstitution of succinate-Q reductase Biochem. Biophys. Res. Commun. 79 1977 939 946 (Pubitemid 8236086)
34. B.L. Trumpower, and Z. Simmons Diminished inhibition of mitochondrial electron transfer from succinate to cytochrome c by thenoyltrifluoroacetone induced by antimycin J. Biol. Chem. 176 1979 4608 4616 (Pubitemid 9203490)
35. R.F. Thorne, and F.L. Bygrave Energy-linked functions of tightly coupled mitochondria isolated from Ehrlich acsites tumor cells Cancer Res. 33 1973 2562 2567
36. J.S. Modica-Napolitano, and J.R. Aprille Basis for the selective cytotoxicity of rhodamine 123 Cancer Res. 47 1987 4361 4365 (Pubitemid 17128145)
37. S. Davis, M.J. Weiss, J.R. Wong, T.J. Lampidis, and L.B. Chen Mitochondrial and plasma membrane potentials cause unusual accumulation and retention of rhodamine 123 by human breast adenocarcinoma-derived MCF-7 cells J. Biol. Chem. 260 1985 13844 13850 (Pubitemid 16233244)
38. R. Moreno-Sánchez, S. Rodríguez-Enríquez, A. Marín-Hernández, and E. Saavedra Energy metabolism in tumor cells FEBS J. 273 2007 5703 5713
39. V.R. Fantin, M.J. Berardi, L. Scorrano, S.J. Korsmeyer, and P. Leder A novel mitochondriotoxic small molecule that selectively inhibits tumor cell growth Cancer Cell 2 2002 29 42 (Pubitemid 41043986)
40. V.P. Skulachev Uncoupling: new approaches to an old problem of bioenergetics Biochim. Biophys. Acta 1363 1998 125 133
41. S. Miwa, and M.D. Brand Mitochondrial matrix reactive oxygen species production is very sensitive to mild uncoupling Biochem. Soc. Trans. 31 2003 1300 1301 (Pubitemid 38030960)
42. G.L. Pardo-Andreu, Y. Nuñez-Figueredo, V.G. Tudella, O. Cuesta-Rubio, F.P. Rodrigues, C.R. Pestana, S.A. Uyemura, A.M. Leopoldino, L.C. Alberici, and C. Curti The anti-cancer agent guttiferone-A permeabilizes mitochondrial membrane: ensuing energetic and oxidative stress implications Toxicol. Appl. Pharmacol. 253 2011 282 289
43. A.V. Kuznetsov, R. Margreiter, A. Amberger, V. Saks, and M. Grimm Changes in mitochondrial redox state, membrane potential and calcium precede mitochondrial dysfunction in doxorubicin-induced cell death Biochim. Biophys. Acta 1813 2011 1144 1152
44. L.F. Dong, V.J.A. Jameson, D. Tilly, L. Prochazka, J. Rohlena, K. Valis, J. Truksa, R. Zobalova, E. Mahdavian, K. Kluckova, M. Stantic, J. Stursa, X.F. Wang, R. Freeman, P.K. Witting, E. Norberg, J. Goodwin, B.A. Salvatore, J. Novotna, J. Turanek, M. Ledvina, P. Hozak, B. Zhivotovsky, M.J. Coster, S.J. Ralph, R.A.J. Smith, and J. Neuzil Mitochondrial targeting of α-tocopheryl succinate enhances its pro-apoptotic efficacy: a new paradigm of efficient anti-cancer therapy Free Radic. Biol. Med. 50 2011 1546 1555
45. M.P. Murphy, and R.A. Smith Targeting antioxidants to mitochondria by conjugation to lipophilic cations Annu. Rev. Pharmacol. Toxicol. 47 2007 629 656
46. R.A. Smith, R.C. Hartley, and M.P. Murphy Mitochondria-targeted small molecule therapeutics and probes Antioxid. Redox Signal. 15 2011 3021 3038
47. F. Liewald, N. Demmel, R. Wirsching, H. Kahle, and G. Valet Intracellular pH, esterase activity, and DNA measurements of human lung carcinomas by flow cytometry Cytometry 11 1990 341 348 (Pubitemid 20123073)