Induction of mitochondrial destabilization and necrotic cell death by apolar mitochondria-directed SOD mimetics

Mitochondrion

Volumn 11, Issue 3, 2011, Pages 476-487

  Szabo, Aliz ^a   Balog, Maria ^b   Mark, Laszlo ^a   Montsko, Gergely ^a   Turi, Zsuzsanna ^a   Gallyas, Ferenc ^a   Sumegi, Balazs ^a   Kalai, Tamas ^b   Hideg, Kalman ^b   Kovacs, Krisztina ^a  

^a UNIVERSITY OF PÉCS   (Hungary)

^b UNIVERSITY OF PÉCS   (Hungary)

Author keywords

Mitochondria; Necrosis; SOD mimetic; Triphenylphosphonium; Tumor cell line

Indexed keywords

2 (3 TRIPHENYLPHOSPHONIUMPROP 1 ENYL) 2,5,5 TRIMETHYLPYRROLIDIN 1 YLOXYL; ANTINEOPLASTIC AGENT; ANTIOXIDANT; CASPASE; CISPLATIN; CYCLOPHILIN D; CYCLOSPORIN A; GEMCITABINE; HO 3814; HO 4223; HO 435; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PROTEIN BCL 2; PROTEIN KINASE B INHIBITOR; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL MEMBRANE DEPOLARIZATION; CELL PROTECTION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; DRUG SCREENING; DRUG STRUCTURE; DRUG TARGETING; ENZYME INHIBITION; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; LIPOPHILICITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION SWELLING; NONHUMAN; PRIORITY JOURNAL; RAT; TUMOR CELL CULTURE;

ANIMALS; CELL DEATH; CELL LINE; FREE RADICAL SCAVENGERS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; RATS; RATS, WISTAR; SUPEROXIDE DISMUTASE;

EID: 79953747559     PISSN: 15677249     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mito.2011.01.006     Document Type: Article

References (53)

1. Armstrong J.S. Mitochondria-directed therapeutics. Antioxid. Redox Signal. 2008, 10(3):575-578.
2. Balog M., Abé C., Kálai T., Steinhoff H.J., Jek J., Hideg K. Synthesis of new paramagnetic fatty acids and lipophilic spin labels. Synthesis-Stuttgart 2007, 11:1663-1670.
3. Belikova N.A., Jiang J., Stoyanovsky D.A., Glumac A., Bayir H., Greenberger J.S., Kagan V.E. Mitochondria-targeted (2-hydroxyamino-vinyl)-triphenyl-phosphonium releases NO and protects mouse embryonic cells against irradiation-induced apoptosis. FEBS Lett. 2009, 583(12):1945-1950.
4. Belkin S., Mehlhorn R.J., Hideg K., Hankovszky H.O., Packer L. Reduction and destruction rates of nitroxide spin probes. Arch. Biochem. Biophys. 1987, 256:232-243.
5. Biasutto L., Sassi N., Mattarei A., Marotta E., Cattelan P., Toninello A., Garbisa S., Zoratti M., Paradisi C. Impact of mitochondriotropic quercetin derivatives on mitochondria. Biochim. Biophys. Acta. 2010, 1797(2):189-196.
6. Bobko A., Kirilyuk I.A., Grigor'ev I.A., Zweier J.L., Khramtsov V.V. Reversible reduction of nitroxides to hydroxilamines: roles of ascorbate and glutathione. Free Radical Biol. Med. 2007, 42:404-412.
7. Bognar Z., Kalai T., Palfi A., Hanto K., Bognar B., Mark L., Szabo Z., Tapodi A., Radnai B., Sarszegi Z., Szanto A., Gallyas F., Hideg K., Sumegi B., Varbiro G. A novel SOD-mimetic permeability transition inhibitor agent protects ischemic heart by inhibiting both apoptotic and necrotic cell death. Free Radic. Biol. Med. 2006, 41(5):835-848.
8. Brown S.E., Ross M.F., Sanjuan-Pla A., Manas A.R., Smith R.A., Murphy M.P. Targeting lipoic acid to mitochondria: synthesis and characterization of a triphenylphosphonium-conjugated alpha-lipoyl derivative. Free Radic. Biol. Med. 2007, 42:1766-1780.
9. Cafiso D.S., Hubbell W.L. EPR determination of membrane potentials. Annu. Rev. Biophys. Bioeng. 1981, 10:217-244.
10. Cheng Z., Winant R.C., Gambhir S.S. A new strategy to screen molecular imaging probe uptake in cell culture without radiolabeling using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J. Nucl. Med. 2005, 46(5):878-886.
11. Dhanasekaran A., Kotamraju S., Karunakaran C., Kalivendi S.V., Thomas S., Joseph J., Kalyanaraman B. Mitochondria superoxide dismutase mimetic inhibits peroxide-induced oxidative damage and apoptosis: role of mitochondrial superoxide. Free Radic. Biol. Med. 2005, 39(5):567-583.
12. Deassolin J., Schuler M., Quinart A., De Giorgi F., Ghosez L., Ichas F. Selective targeting of synthetic antioxidants to mitochondria: towards a mitochondrial medicine for neurodegenerative diseases?. Eur. J. Pharmacol. 2002, 447:155-161.
13. Eberle J., Kurbanov B.M., Hossini A.M., Trefzer U., Fecker L.F. Overcoming apoptosis deficiency of melanoma-hope for new therapeutic approaches. Drug Resist. Updat. 2007, 10(6):218-234.
14. Filipovska A., Kelso G.F., Brown S.E., Beer S.M., Smith R.A., Murphy M.P. Synthesis and characterization of a triphenylphosphonium-conjugated peroxidase mimetic: insights into the interaction of ebselen with mitochondria. J. Biol. Chem. 2005, 280(25):24113-24126.
15. Fischer U., Schulze-Osthoff K. New approaches and therapeutics targeting apoptosis in disease. Pharmacol. Rev. 2005, 57(2):187-215.
16. Galluzzi L., Blomgren K., Kroemer G. Mitochondrial membrane permeabilization in neuronal injury. Nat. Rev. Neurosci. 2009, 10(7):481-494.
17. Garber K. Targeting mitochondria emerges as therapeutic strategy. J. Natl Cancer Inst. 2005, 97:1800-1801.
18. Glebska J., Pulaski L., Gwozdzinski K., Kolimowski J. Structureactivity relationship studies of protective function of nitroxides in Fenton system. Biometals 2001, 14:159-170.
19. Hail N. Mitochondria: a novel target for the chemoprevention of cancer. Apoptosis 2005, 10:687-705.
20. Hockings P.D., Rogers P.J. The measurement of transmembrane electrical potential with lipophilic cations. Biochim. Biophys. Acta 1996, 1282(1):101-106.
21. Hoye A.T., Davoren J.E., Wipf P., Fink P.M., Kagan V.E., 2008. Targeting Mitochondria Accounts of Chem Res. 41:87-97.
22. Huang S.G. Development of a high throughput screening assay for mitochondrial membrane potential in living cells. J. Biomol. Screen. 2002, 7(4):383-389.
23. Huanwen W., Zhiyong L., Xiaohua S., Xinyu R., Kai W., Tonghua L. Intrinsic chemoresistance to gemcitabine is associated with constitutive and laminin-induced phosphorylation of FAK in pancreatic cancer cell lines. Mol. Cancer 2009, 8:125-140.
24. Kálai T., Balog M., Szabó A., Gulyás G., Jeko J., Sümegi B., Hideg K. New poly(ADP-ribose) polymerase-1 inhibitors with antioxidant activity based on 4-carboxamidobenzimidazole-2-ylpyrroline and -tetrahydropyridine nitroxides and their precursors. J. Med. Chem. 2009, 52(6):1619-1629.
25. Kálai T., Várbiró G., Bognár Z., Pálfi A., Hantó K., Bognár B., Osz E., Sümegi B., Hideg K. Synthesis and evaluation of the permeability transition inhibitory characteristics of paramagnetic and diamagnetic amiodarone derivatives. Bioorg. Med. Chem. 2005, 13(7):2629-2636.
26. Kelso G.F., Porteous C.M., Coulter C.V., Hughes G., Porteous W.K., Ledgerwood E.C., Smith R.A., Murphy M.P. Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties. J. Biol. Chem. 2001, 276:4588-4596.
27. Kim Y.S., Yang C.T., Wang J., Wang L., Li Z.B., Chen X., Liu S.J. Effects of targeting moiety, linker, bifunctional chelator, and molecular charge on biological properties of 64Cu-labeled triphenylphosphonium cations. Med. Chem. 2008, 51(10):2971-2984.
28. Krause B.J., Szabo Z., Becker L.C., Dannals R.F., Scheffel U., Seki C., Ravert H.T., Dipaola A.F., Wagner H.N. Myocardial perfusion with [11C]methyl triphenyl phosphonium: measurements of the extraction fraction and myocardial uptake. J. Nucl. Biol. Med. 1994, 38(3):521-526.
29. Krishna M.C., Russo A., Mitchell J.B., Goldstein S., Hafni H., Samuni A. Do nitroxide antioxidants act as scavengers of O2•- or as SOD mimics?. J. Biol. Chem. 1996, 271:26026-26031.
30. Kroemer G., Dallaporta B., Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol. 1998, 60:619-642.
31. Lam A.M., Pattison D.I., Bottle S.E., Keddie J.D., Davies J.M. Nitric oxide and nitroxides can act as efficient scavengers of proteinderived free radicals. Chem. Res. Toxicol. 2008, 21:2111-2119.
32. Lemasters J.J., Nieminen A.L., Qian T., Trost L.C., Elmore S.P., Nishimura Y., Crowe R.A., Cascio W.E., Bradham C.A., Brenner D.A., Herman B. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta 1998, 1366(1-2):177-196.
33. Lemasters J.J., Theruvath T.P., Zhong Z., Nieminen A.L. Mitochondrial calcium and the permeability transition in cell death. Biochim. Biophys. Acta 2009, 1787(11):1395-1401.
34. Lena A., Rechichi M., Salvetti A., Bartoli B., Vecchio D., Scarcelli V., Amoroso R., Benvenuti L., Gagliardi R., Gremigni V., Rossi L. Drugs targeting the mitochondrial pore act as cytotoxic and cytostatic agents in temozolomide-resistant glioma cells. J. Transl. Med. 2009, 7:13.
35. Madar I., Ravert H.T., Du Y., Hilton J., Volokh L., Dannals R.F., Frost J.J., Hare J.M. Characterization of uptake of the new PET imaging compound 18F-fluorobenzyl triphenyl phosphonium in dog myocardium. J. Nucl. Med. 2006, 47(8):1359-1366.
36. Min J.J., Biswal S., Deroose C., Gambhir S.S. Tetraphenylphosphonium as a novel molecular probe for imaging tumors. J. Nucl. Med. 2004, 45(4):636-643.
37. Murphy M.P. Targeting bioactive compounds to mitochondria. Trends Biotechnol. 1997, 15:326-330.
38. Murphy M.P., Echtay K.S., Blaikie F.H., Asin-Cayuela J., Cocheme H.M., Green K., Buckingham J.A., Taylor E.R., Hurrell F., Hughes G., Miwa S., Cooper C.E., Svistunenko D.A., Smith R.A., Brand M.D. Superoxide activates uncoupling proteins by generating carbon-centered radicals and initiating lipid peroxidation: studies using a mitochondria targeted spin trap derived from alpha-phenyl-N-tert-butylnitrone. J. Biol. Chem. 2003, 278:48534-48545.
39. Proskuryakov S.Y., Gabai V.L. Mechanisms of tumor cell necrosis. Curr. Pharm. Des. 2010, 16(1):56-68.
40. Reed J.C., Pellecchia M. Apoptosis-based therapies for hematologic malignancies. Blood 2005, 106(2):408-418.
41. Sasi N., Hwang M., Jaboin J., Csiki I., Lu B. Regulated cell death pathways: new twists in modulation of BCL2 family function. Mol. Cancer Ther. 2009, 8(6):1421-1429.
42. Schneider W.C., Hageboom G.H. Cytochemical studies of mammalian tissues: III. Isocitric dehydrogenase and triphosphopyridine nucleotide-cytochrome c reductase of mouse liver. J. Biol. Chem. 1950, 186:417-427.
43. Sims N.R. Rapid isolation of metabolically active mitochondria from rat brain and subregions using Percoll density gradient centrifugation. J. Neurochem. 1990, 55:698-707.
44. Sjöström J., Bergh J. How apoptosis is regulated, and what goes wrong in cancer. BMJ 2001, 322(7301):1538-1539.
45. Smith R.A., Porteous C.M., Coulter C.V., Murphy M.P. Selective targeting of an antioxidant to mitochondria. Eur. J. Biochem. 1999, 263:709-716.
46. Szewczyk A., Wojtczak L. Mitochondria as a pharmacological target. Pharmacol. Rev. 2002, 54:101-127.
47. Szigeti A., Bellyei S., Gasz B., Boronkai A., Hocsak E., Minik O., Bognar Z., Varbiro G., Sumegi B., Gallyas F. Induction of necrotic cell death and mitochondrial permeabilization by heme binding protein 2/SOUL. FEBS Lett. 2006, 580(27):6447-6454.
48. Tsujimoto Y., Shimizu S. Role of the mitochondrial membrane permeability transition in cell death. Apoptosis 2007, 12(5):835-840.
49. Tsujimoto Y., Nakagawa T., Shimizu S. Mitochondrial membrane permeability transition and cell death. Biochim. Biophys. Acta 2006, 1757(9-10):1297-1300.
50. Twomey P., Taira J., DeGraff W., Mitchell J.B., Russo A., Krishna M.C., Hankovszky H.O., Frank L., Hideg K. Direct evidence for in vivo nitroxide free radical production from a new antiarrhythmic drug by EPR spectroscopy. Free Radical Biol. Med. 1997, 22:909-916.
51. Varbiro G., Veres B., Gallyas F., Sumegi B. Direct effect of Taxol on free radical formation and mitochondrial permeability transition. Free Radic. Biol. Med. 2001, 31:548-558.
52. Wang J., Yang C.T., Kim Y.S., Sreerama S.G., Cao Q., Li Z.B., He Z., Chen X., Liu S. 64Cu-Labeled triphenylphosphonium and triphenylarsonium cations as highly tumor-selective imaging agents. J. Med. Chem. 2007, 18(21):5057-5069. 50.
53. Yang C.T., Kim Y.S., Wang J., Wang L., Shi J., Li Z.B., Chen X., Fan M., Li J.J., Liu S. 64Cu-labeled 2-(diphenylphosphoryl)ethyldiphenylphosphonium cations as highly selective tumor imaging agents: effects of linkers and chelates on radiotracer biodistribution characteristics. Bioconjug. Chem. 2008, 19(10):2008-2022.