Disruption of the mitochondrial thioredoxin system as a cell death mechanism of cationic triphenylmethanes

Free Radical Biology and Medicine

Volumn 50, Issue 7, 2011, Pages 811-820

  Zhang, Xu ^a   Zheng, Yujuan ^a   Fried, Levi E ^b   Du, Yatao ^a   Montano, Sergio J ^a   Sohn, Allie ^b   Lefkove, Benjamin ^b   Holmgren, Lars ^a   Arbiser, Jack L ^b,c   Holmgren, Arne ^a   Lu, Jun ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

Anticancer target; Brilliant green; Free radicals; Lon protease; Mitochondria; Thioredoxin; Triphenylmethane

Indexed keywords

APOPTOSIS INDUCING FACTOR; BRILLIANT GREEN; CATION; CRYSTAL VIOLET; CYTOCHROME C; ENDOPEPTIDASE LA; MESSENGER RNA; MITOCHONDRIAL PROTEIN; SMALL INTERFERING RNA; THIOREDOXIN 1; THIOREDOXIN 2; TRIPHENYLMETHANE DERIVATIVE;

ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL DEATH; CELL ULTRASTRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; DRUG TARGETING; FIBROBLAST; HELA CELL; HUMAN; HUMAN CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ANGIOGENESIS INHIBITORS; ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CATIONS; CELL SURVIVAL; CYTOCHROMES C; FIBROBLASTS; GENTIAN VIOLET; HELA CELLS; HUMANS; MITOCHONDRIA; NEOPLASMS; OXIDATION-REDUCTION; PROTEASE LA; QUATERNARY AMMONIUM COMPOUNDS; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; THIOREDOXINS; TRITYL COMPOUNDS; UP-REGULATION;

GENTIANA;

EID: 79952041072     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.12.036     Document Type: Article

References (54)

1. S. Srivastava, R. Sinha, and D. Roy Toxicological effects of malachite green Aquat. Toxicol. 66 2004 319 329 (Pubitemid 38201237)
2. M. Balabanova, L. Popova, and R. Tchipeva Dyes in dermatology Clin. Dermatol. 21 2003 2 6 (Pubitemid 36287025)
3. R. Docampo, and S.N. Moreno The metabolism and mode of action of gentian violet Drug Metab. Rev. 22 1990 161 178 (Pubitemid 20283478)
4. B.N. Perry, B. Govindarajan, S.S. Bhandarkar, U.G. Knaus, M. Valo, C. Sturk, C.O. Carrillo, A. Sohn, F. Cerimele, D. Dumont, A. Losken, J. Williams, L.F. Brown, X. Tan, E. Ioffe, G.D. Yancopoulos, and J.L. Arbiser Pharmacologic blockade of angiopoietin-2 is efficacious against model hemangiomas in mice J. Invest. Dermatol. 126 2006 2316 2322 (Pubitemid 44413180)
5. M. Lapidoth, D. Ben-Amitai, S. Bhandarkar, L. Fried, and J.L. Arbiser Efficacy of topical application of eosin for ulcerated hemangiomas J. Am. Acad. Dermatol. 60 2009 350 351
6. C.H. Lillig, and A. Holmgren Thioredoxin and related molecules-from biology to health and disease Antioxid. Redox Signaling 9 2007 25 47 (Pubitemid 44901873)
7. P. Nordlund, and P. Reichard Ribonucleotide reductases Annu. Rev. Biochem. 75 2006 681 706 (Pubitemid 44118048)
8. A. Holmgren Thioredoxin and glutaredoxin systems J. Biol. Chem. 264 1989 13963 13966 (Pubitemid 19214215)
9. E.S. Arnér, and A. Holmgren Physiological functions of thioredoxin and thioredoxin reductase Eur. J. Biochem. 267 2000 6102 6109
10. G.T. Wondrak Redox-directed cancer therapeutics: molecular mechanisms and opportunities Antioxid. Redox Signaling 11 2009 3013 3069
11. E.S. Arnér, and A. Holmgren The thioredoxin system in cancer Semin. Cancer Biol. 16 2006 420 426 (Pubitemid 44780139)
12. J. Lu, L.V. Papp, J. Fang, S. Rodriguez-Nieto, B. Zhivotovsky, and A. Holmgren Inhibition of mammalian thioredoxin reductase by some flavonoids: implications for myricetin and quercetin anticancer activity Cancer Res. 66 2006 4410 4418
13. J. Lu, E.H. Chew, and A. Holmgren Targeting thioredoxin reductase is a basis for cancer therapy by arsenic trioxide Proc. Natl Acad. Sci. USA 104 2007 12288 12293 (Pubitemid 47206130)
14. G. Spyrou, E. Enmark, A. Miranda-Vizuete, and J. Gustafsson Cloning and expression of a novel mammalian thioredoxin J. Biol. Chem. 272 1997 2936 2941 (Pubitemid 27053344)
15. G. Saxena, J. Chen, and A. Shalev Intracellular shuttling and mitochondrial function of thioredoxin-interacting protein J. Biol. Chem. 285 2009 3997 4005
16. T. Tanaka, F. Hosoi, Y. Yamaguchi-Iwai, H. Nakamura, H. Masutani, S. Ueda, A. Nishiyama, S. Takeda, H. Wada, G. Spyrou, and J. Yodoi Thioredoxin-2 (TRX-2) is an essential gene regulating mitochondria-dependent apoptosis EMBO J. 21 2002 1695 1703 (Pubitemid 34614625)
17. R. Zhang, R. Al-Lamki, L. Bai, J.W. Streb, J.M. Miano, J. Bradley, and W. Min Thioredoxin-2 inhibits mitochondria-located ASK1-mediated apoptosis in a JNK-independent manner Circ. Res. 94 2004 1483 1491 (Pubitemid 38780321)
18. M. He, J. Cai, Y.M. Go, J.M. Johnson, W.D. Martin, J.M. Hansen, and D.P. Jones Identification of thioredoxin-2 as a regulator of the mitochondrial permeability transition Toxicol. Sci. 105 2008 44 50
19. D. Wang, H. Masutani, S. Oka, T. Tanaka, Y. Yamaguchi-Iwai, H. Nakamura, and J. Yodoi Control of mitochondrial outer membrane permeabilization and Bcl-xL levels by thioredoxin 2 in DT40 cells J. Biol. Chem. 281 2006 7384 7391 (Pubitemid 43847508)
20. A.E. Damdimopoulos, A. Miranda-Vizuete, M. Pelto-Huikko, J.A. Gustafsson, and G. Spyrou Human mitochondrial thioredoxin: involvement in mitochondrial membrane potential and cell death J. Biol. Chem. 277 2002 33249 33257 (Pubitemid 34984845)
21. L. Nonn, R.R. Williams, R.P. Erickson, and G. Powis The absence of mitochondrial thioredoxin 2 causes massive apoptosis, exencephaly, and early embryonic lethality in homozygous mice Mol. Cell. Biol. 23 2003 916 922 (Pubitemid 36133510)
22. M. Conrad, C. Jakupoglu, S.G. Moreno, S. Lippl, A. Banjac, M. Schneider, H. Beck, A.K. Hatzopoulos, U. Just, F. Sinowatz, W. Schmahl, K.R. Chien, W. Wurst, G.W. Bornkamm, and M. Brielmeier Essential role for mitochondrial thioredoxin reductase in hematopoiesis, heart development, and heart function Mol. Cell. Biol. 24 2004 9414 9423 (Pubitemid 39391679)
23. A. Stammati, C. Nebbia, I.D. Angelis, A.G. Albo, M. Carletti, C. Rebecchi, F. Zampaglioni, and M. Dacasto Effects of malachite green (MG) and its major metabolite, leucomalachite green (LMG), in two human cell lines Toxicol. In Vitro 19 2005 853 858 (Pubitemid 41563217)
24. M.A. Ingraham The bacteriostatic action of gentian violet and dependence on the oxidation-reduction potential J. Bacteriol. 26 1933 573 598
25. R. Docampo, S.N. Moreno, R.P. Muniz, F.S. Cruz, and R.P. Mason Light-enhanced free radical formation and trypanocidal action of gentian violet (crystal violet) Science 220 1983 1292 1295 (Pubitemid 13104193)
26. S.S. Bhandarkar, M. Jaconi, L.E. Fried, M.Y. Bonner, B. Lefkove, B. Govindarajan, B.N. Perry, R. Parhar, J. Mackelfresh, A. Sohn, M. Stouffs, U. Knaus, G. Yancopoulos, Y. Reiss, A.V. Benest, H.G. Augustin, and J.L. Arbiser Fulvene-5 potently inhibits NADPH oxidase 4 and blocks the growth of endothelial tumors in mice J. Clin. Investig. 119 2009 2359 2365
27. G. Repetto, A. del Peso, and J.L. Zurita Neutral red uptake assay for the estimation of cell viability/cytotoxicity Nat. Protoc. 3 2008 1125 1131
28. N.A. Bersani, J.R. Merwin, N.I. Lopez, G.D. Pearson, and G.F. Merrill Protein electrophoretic mobility shift assay to monitor redox state of thioredoxin in cells Meth. Enzymol. 347 2002 317 326 (Pubitemid 34233284)
29. I.A. Wadman, H. Osada, G.G. Grutz, A.D. Agulnick, H. Westphal, A. Forster, and T.H. Rabbitts The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins EMBO J. 16 1997 3145 3157 (Pubitemid 27234954)
30. L.V. Papp, J. Lu, F. Striebel, D. Kennedy, A. Holmgren, and K.K. Khanna The redox state of SECIS binding protein 2 controls its localization and selenocysteine incorporation function Mol. Cell. Biol. 26 2006 4895 4910 (Pubitemid 43955807)
31. M. Luthman, and A. Holmgren Rat liver thioredoxin and thioredoxin reductase: purification and characterization Biochemistry 21 1982 6628 6633
32. D. Hinton Results of the intravenous use of gentian violet in cases of extreme septicaemia Ann. Surg. 81 1925 687 692
33. P. Hakansson, A. Hofer, and L. Thelander Regulation of mammalian ribonucleotide reduction and dNTP pools after DNA damage and in resting cells J. Biol. Chem. 281 2006 7834 7841 (Pubitemid 43847398)
34. G. Pontarin, P. Ferraro, P. Hakansson, L. Thelander, P. Reichard, and V. Bianchi p53R2-dependent ribonucleotide reduction provides deoxyribonucleotides in quiescent human fibroblasts in the absence of induced DNA damage J. Biol. Chem. 282 2007 16820 16828 (Pubitemid 47093192)
35. F.Z. Avval, and A. Holmgren Molecular mechanisms of thioredoxin and glutaredoxin as hydrogen donors for mammalian S phase ribonucleotide reductase J. Biol. Chem. 284 2009 8233 8240
36. A. Bayot, N. Basse, I. Lee, M. Gareil, B. Pirotte, A.L. Bulteau, B. Friguet, and M. Reboud-Ravaux Towards the control of intracellular protein turnover: mitochondrial Lon protease inhibitors versus proteasome inhibitors Biochimie 90 2008 260 269 (Pubitemid 351181249)
37. Z. Granot, O. Kobiler, N. Melamed-Book, S. Eimerl, A. Bahat, B. Lu, S. Braun, M.R. Maurizi, C.K. Suzuki, A.B. Oppenheim, and J. Orly Turnover of mitochondrial steroidogenic acute regulatory (StAR) protein by Lon protease: the unexpected effect of proteasome inhibitors Mol. Endocrinol. 21 2007 2164 2177 (Pubitemid 47351216)
38. N. Ugarte, I. Petropoulos, and B. Friguet Oxidized mitochondrial protein degradation and repair in aging and oxidative stress Antioxid. Redox Signaling 13 2010 539 549
39. J.K. Ngo, and K.J. Davies Importance of the lon protease in mitochondrial maintenance and the significance of declining lon in aging Ann. NY Acad. Sci. 1119 2007 78 87 (Pubitemid 350191233)
40. O. Warburg On the origin of cancer cells Science 123 1956 309 314
41. S. Fulda, L. Galluzzi, and G. Kroemer Targeting mitochondria for cancer therapy Nat. Rev. Drug Discovery 9 2010 447 464
42. N.A. Littlefield, B.N. Blackwell, C.C. Hewitt, and D.W. Gaylor Chronic toxicity and carcinogenicity studies of gentian violet in mice Fundam. Appl. Toxicol. 5 1985 902 912 (Pubitemid 16169621)
43. S.J. Culp, P.W. Mellick, R.W. Trotter, K.J. Greenlees, R.L. Kodell, and F.A. Beland Carcinogenicity of malachite green chloride and leucomalachite green in B6C3F1 mice and F344 rats Food Chem. Toxicol. 44 2006 1204 1212
44. S. Ueda, H. Masutani, H. Nakamura, T. Tanaka, M. Ueno, and J. Yodoi Redox control of cell death Antioxid. Redox Signaling 4 2002 405 414 (Pubitemid 34753380)
45. H. Masutani, S. Ueda, and J. Yodoi The thioredoxin system in retroviral infection and apoptosis Cell Death Differ. 12 Suppl. 1 2005 991 998 (Pubitemid 41030612)
46. V.I. Pérez, C.M. Lew, L.A. Cortez, C.R. Webb, M. Rodriguez, Y. Liu, W. Qi, Y. Li, A. Chaudhuri, H. Van Remmen, A. Richardson, and Y. Ikeno Thioredoxin 2 haploinsufficiency in mice results in impaired mitochondrial function and increased oxidative stress Free Radic. Biol. Med. 44 2008 882 892
47. G. Pontarin, A. Fijolek, P. Pizzo, P. Ferraro, C. Rampazzo, T. Pozzan, L. Thelander, P.A. Reichard, and V. Bianchi Ribonucleotide reduction is a cytosolic process in mammalian cells independently of DNA damage Proc. Natl Acad. Sci. USA 105 2008 17801 17806
48. J.D. Heidel, J.Y. Liu, Y. Yen, B. Zhou, B.S. Heale, J.J. Rossi, D.W. Bartlett, and M.E. Davis Potent siRNA inhibitors of ribonucleotide reductase subunit RRM2 reduce cell proliferation in vitro and in vivo Clin. Cancer Res. 13 2007 2207 2215 (Pubitemid 46649891)
49. J. Shao, B. Zhou, B. Chu, and Y. Yen Ribonucleotide reductase inhibitors and future drug design Curr. Cancer Drug Targets 6 2006 409 431 (Pubitemid 44033390)
50. M.P. Murphy Targeting lipophilic cations to mitochondria Biochim. Biophys. Acta 1777 2008 1028 1031
51. F.R. Gadelha, S.N. Moreno, W. De Souza, F.S. Cruz, and R. Docampo The mitochondrion of Trypanosoma cruzi is a target of crystal violet toxicity Mol. Biochem. Parasitol. 34 1989 117 126 (Pubitemid 19098377)
52. A.J. Kowaltowski, J. Turin, G.L. Indig, and A.E. Vercesi Mitochondrial effects of triarylmethane dyes J. Bioenerg. Biomembr. 31 1999 581 590 (Pubitemid 30082901)
53. D.A. Bota, and K.J. Davies Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism Nat. Cell Biol. 4 2002 674 680 (Pubitemid 34993703)
54. J.K. Ngo, and K.J. Davies Mitochondrial Lon protease is a human stress protein Free Radic. Biol. Med. 46 2009 1042 1048