Mitochondria-Mediated oxidative stress: Old target for new drugs

Current Medicinal Chemistry

Volumn 22, Issue 26, 2015, Pages 3040-3053

  Lyakhovich, Alex ^a,b   Graifer, Dmitri ^c  

^a MASARYK UNIVERSITY   (Czech Republic)

^b INSTITUTE OF MOLECULAR BIOLOGY AND BIOPHYSICS   (Russian Federation)

^c NOVOSIBIRSK STATE UNIVERSITY   (Russian Federation)

Author keywords

Apoptosis; Chemoprevention; Mitochondria; Mitophagy; Oxidative stress; RNS; ROS

Indexed keywords

AGENTS AFFECTING METABOLISM; ALPHA TOCOPHEROL SUCCINATE; ANTINEOPLASTIC AGENT; ANTIOXIDANT; CARNITINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; NEW DRUG; POLYUNSATURATED FATTY ACID; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SCAVENGER; THIOREDOXIN INHIBITOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOPHAGY; BIOGENESIS; CANCER CELL; CANCER PREVENTION; CELL AGING; CELL DEATH; DRUG MECHANISM; DRUG TARGETING; HUMAN; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MITOPHAGY; NONHUMAN; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; ANIMAL; DRUG DEVELOPMENT; DRUG EFFECTS; METABOLISM; MOLECULARLY TARGETED THERAPY; PROCEDURES;

ANIMALS; DRUG DISCOVERY; HUMANS; MITOCHONDRIA; MOLECULAR TARGETED THERAPY; OXIDATIVE STRESS;

EID: 84942134314     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/0929867322666150729114036     Document Type: Article

References (150)

1. Benz, C.C.; Yau, C. Ageing, oxidative stress and cancer: paradigms in parallax. Nat. Rev. Cancer, 2008, 8(11), 875- 879.
2. Pagano, G.; Shyamsunder, P.; Verma, R.; Lyakhovich, A. Damaged mitochondria in Fanconi anemia - An isolated event or a general phenomenon? Oncoscience, 2014, 4, 187-296.
3. Chen, E.I. Mitochondrial dysfunction and cancer metastasis. J. Bioenerg. Biomembr., 2012, 44(6), 619-622.
4. Wallace, D.C. Bioenergetic origins of complexity and disease. Cold Spring Harb. Symp. Quant. Biol., 2011, 76, 1-16.
5. Heller, A.; Brockhoff, G.; Goepferich, A. Targeting drugs to mitochondria. Eur. J. Pharm. Biopharm., 2012, 82(1), 1- 18.
6. m-Dependent and - independent production of reactive oxygen species by rat brain mitochondria. J. Neurochem., 2001, 79, 266-277.
7. Adam-Vizi, V.; Chinopoulos, C. Bioenergetics and the formation of mitochondrial reactive oxygen species. Trends Pharmacol. Sci., 2006, 27, 639-645.
8. Sugioka, K.; Nakano, M.; Naito, I.; Tero-Kubota, S.; Ikegami, Y. Properties of a coenzyme, pyrroloquinoline quinone: generation of an active oxygen species during a reduction- oxidation cycle in the presence of NAD(P)H and O2. Biochim. Biophys. Acta, 1988, 964(2), 175-182.
9. Sawa, T.; Ihara, H.; Ida, T.; Fujii, S.; Nishida, M.; Akaike, T. Formation, signaling functions, and metabolisms of nitrated cyclic nucleotide. Nitric Oxide, 2013, 34, 10-18.
10. Saeidnia, S.; Abdollahi, M. Toxicological and pharmacological concerns on oxidative stress and related diseases. Toxicol. Appl. Pharmacol., 2013, 273(3), 442-455.
11. Wang, X.; Peralta, S.; Moraes, C.T. Mitochondrial alterations during carcinogenesis: A review of metabolic transformation and targets for anticancer treatments. Adv. Cancer Res., 2013, 119, 127-160.
12. Kussmaul, L.; Hirst, J. The mechanism of superoxide production by NADH:ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc. Natl. Acad. Sci. USA, 2006, 103, 7607-7612.
13. Kushnareva, Y.; Murphy, A.N.; Andreyev, A. Complex Imediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+oxidation-reduction state. Biochem. J., 2002, 368, 545-553.
14. Guzy, R.D.; Schumacker, P.T. Oxygen sensing by mitochondria at complex III: The paradox of increased reactive oxygen species during hypoxia. Exp. Physiol., 2006, 91, 807-819.
15. Mailloux, R.J.; Jin, X.; Willmore, W.G. Redox regulation of mitochondrial function with emphasis on cysteine oxidation reactions. Redox. Biol., 2013, 2, 123-139.
16. Vamecq, J.; Dessein, A.F.; Fontaine, M.; Briand, G.; Porchet, N.; Latruffe, N.; Andreolotti, P.; Cherkaoui-Malki, M. Mitochondrial dysfunction and lipid homeostasis. Curr. Drug. Metab., 2012, 13(10), 1388-1400.
17. Ferreira, I.L.; Resende, R.; Ferreiro, E.; Rego, A.C.; Pereira, C.F. Curr. Drug Targets, 2010, 11(10), 1193-1120.
18. Chaturvedi, R.K.; Flint, B. M. Mitochondrial diseases of the brain. Free Radic. Biol. Med., 2013, 63, 1-29.
19. Phillips, D.C.; Dias, H.K.; Kitas, G.D.; Griffiths, H.R. Aberrant reactive oxygen and nitrogen species generation in rheumatoid arthritis (RA): causes and consequences for immune function, cell survival, and therapeutic intervention. Antioxid. Redox. Signal., 2010, 12(6), 743-785.
20. Mittal, M.; Siddiqui, M.R.; Tran, K.; Reddy, S.P.; Malik, A.B. Reactive oxygen species in inflammation and tissue injury. Antioxid. Redox. Signal., 2014, 20(7), 1126-1167.
21. Rochette, L.; Lorin, J.; Zeller, M.; Guilland, J.C.; Lorgis, L.; Cottin, Y.; Vergely, C. Nitric oxide synthase inhibition and oxidative stress in cardiovascular diseases: possible therapeutic targets? Pharmacol. Ther., 2013, 140(3), 239- 257.
22. Murphy, M.P. How mitochondria produce reactive oxygen species. Biochem. J., 2009, 417(1), 1-13.
23. Tokarz, P.; Kaarniranta, K.; Blasiak, J. Biogerontology, 2013, 14(5), 461-482.
24. Lu, J.; Holmgren, A. The thioredoxin antioxidant system. Free Radic. Biol. Med., 2014, 66, 75-87.
25. Yuzhalin, A.E.; Kutikhin, A.G. Inherited variations in the SOD and GPX gene families and cancer risk. Free. Radic. Res., 2012, 46(5), 581-599.
26. Reszka, E.; Wasowicz, W.; Gromadzinska, J. Genetic polymorphism of xenobiotic metabolising enzymes, diet and cancer susceptibility. Br. J. Nutr., 2006, 96(4), 609- 619.
27. Pagano, G.; Talamanca, A.A.; Castello, G.; d'Ischia, M.; Pallardó, F.V.; Petrović, S.; Porto, B.; Tiano, L.; Zatterale, A. From clinical description, to in. vitro and animal studies, and backward to patients: oxidative stress and mitochondrial dysfunction in Fanconi anemia. Free Radic. Biol. Med., 2013, 58, 118-125.
28. Wang, C.H.; Wu, S.B.; Wu, Y.T.; Wei, Y.H. Oxidative stress response elicited by mitochondrial dysfunction: implication in the pathophysiology of aging. Exp. Biol. Med., 2013, 238(5), 450-460.
29. Pagano, G.; Castello, G.; Pallardó, F.V. Sjøgren's syndrome- Associated oxidative stress and mitochondrial dysfunction: prospects for chemoprevention trials. Free Radic. Res., 2013, 47(2), 71-73.
30. Ralph, S.J.; Neuzil, J. Mitochondria as targets for cancer therapy. Mol. Nutr. Food Res., 2009, 53(1), 9-28.
31. Skulachev, V.P. Mitochondria in the programmed death phenomena; a principle of biology: "it is better to die than to be wrong". IUBMB. Life, 2000, 49(5), 365-73.
32. Wang, K. Molecular mechanisms of hepatic apoptosis. Cell. Death. Dis., 2014, 5: e996.
33. Circu, M.L.; Aw, T.Y. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med., 2010, 48(6), 749-762.
34. Marzetti, E.; Calvani, R.; Cesari, M.; Buford, T.W.; Lorenzi, M.; Behnke, B.J.; Leeuwenburgh, C. Mitochondrial dysfunction and sarcopenia of aging: from signaling pathways to clinical trials. Int. J. Biochem. Cell. Biol., 2013, 45(10), 2288-2301.
35. Murphy, M.P. Modulating mitochondrial intracellular location as a redox signal. Sci. Signal., 2012, 5(242), pe39.
36. Yuan, S.; Akey, C.W. Apoptosome structure, assembly, and procaspase activation. Structure, 2013, 21(4), 501-515.
37. Krishna, S.; Low, I.C.; Pervaiz, S. Regulation of mitochondrial metabolism: yet another facet in the biology of the oncoprotein Bcl-2. Biochem. J., 2011, 435(3), 545-551.
38. Filomeni, G.; De, ZD.; Cecconi, F. Oxidative stress and autophagy: The clash between damage and metabolic needs. Cell. Death Differ., 2014, doi:10.1038/cdd.2014.150.
39. Aki, T.; Funakoshi, T.; Unuma, K.; Uemura, K. Impairment of autophagy: from hereditary disorder to drug intoxication. Toxicology, 2013, 311(3), 205-215.
40. Zhao, Y.; Li, R.; Xia, W.; Neuzil, J.; Lu, Y.; Zhang, H.; Zhao, X.; Zhang, X.; Sun, C.; Wu, K. Bid integrates intrinsic and extrinsic signaling in apoptosis induced by alphatocopheryl succinate in human gastric carcinoma cells. Cancer Lett., 2010, 288(1), 42-49.
41. Dong, L.F.; Low, P.; Dyason, J.C.; Wang, X.F.; Prochazka, L.; Witting, P.K.; Freeman, R.; Swettenham, E.; Valis, K.; Liu, J.; Zobalova, R.; Turanek, J.; Spitz, D.R.; Domann, F.E.; Scheffler, I.E.; Ralph, S.J.; Neuzil, J. Alphatocopheryl succinate induces apoptosis by targeting ubiquinone- binding sites in mitochondrial respiratory complex II. Oncogene, 2008, 27(31), 4324-4335.
42. 2+and ROS in alpha-tocopheryl succinate- induced mitochondrial permeabilization. Int. J. Cancer, 2010, 127(8), 1823-1832.
43. Angulo-Molina, A.; Reyes-Leyva, J.; López-Malo, A.; Hernández, J. The role of alpha tocopheryl succinate (α- TOS) as a potential anticancer agent. Nutr. Cancer, 2014, 66(2), 167-176.
44. Tang, D.G.; Li, L.; Zhu, Z.; Joshi, B.; Johnson, C.R.; Marnett, L.J.; Honn, K.V.; Crissman, J.D.; Krajewski, S.; Reed, J.C.; Timar, J.; Porter, A.T. BMD188, A novel hydroxamic acid compound, demonstrates potent anti-prostate cancer effects in vitro and in vivo by inducing apoptosis: requirements for mitochondria, reactive oxygen species, and proteases. Pathol. Oncol. Res., 1998, 4(3), 179-190.
45. Chandra, D.; Choy, G.; Tang, D.G. Cytosolic accumulation of HSP60 during apoptosis with or without apparent mitochondrial release: evidence that its pro-apoptotic or prosurvival functions involve differential interactions with caspase-3. J. Biol. Chem., 2007, 282(43), 31289-31301.
46. Hulleman, E.; Kazemier, K.M.; Holleman, A.; Vander- Weele, D.J.; Rudin, C.M.; Broekhuis, M.J.; Evans, W.E.; Pieters, R.; Den Boer, M.L. Inhibition of glycolysis modulates prednisolone resistance in acute lymphoblastic leukemia cells. Blood, 2009, 113(9), 2014-2021.
47. Calviño, E.; Estañ, M.C.; Simón, G.P.; Sancho, P.; Boyano- Adánez, M. C.; de Blas, E.; Bréard, J.; Aller, P. Increased apoptotic efficacy of lonidamine plus arsenic trioxide combination in human leukemia cells. Reactive oxygen species generation and defensive protein kinase (MEK/ERK, Akt/mTOR) modulation. Biochem. Pharmacol., 2011, 82(11), 1619-1629.
48. Xu, R.; Tian, E.; Tang, H.; Liu, C.; Wang, Q. Proteomic analysis of gossypol induces necrosis in multiple myeloma cells. Biomed. Res. Int., 2014, 2014, 839232.
49. Sadahira, K.; Sagawa, M.; Nakazato, T.; Uchida, H.; Ikeda, Y.; Okamoto, S.; Nakajima, H.; Kizaki, M. Gossypol induces apoptosis in multiple myeloma cells by inhibition of interleukin-6 signaling and Bcl-2/Mcl-1 pathway. Int. J. Oncol., 2014 doi:10.3892/ijo.2014.2652.
50. Ni, Z.; Dai, X.; Wang, B.; Ding, W.; Cheng, P.; Xu, L.; Lian, J.; He, F. Natural Bcl-2 inhibitor (-)- gossypol induces protective autophagy via reactive oxygen species-high mobility group box 1 pathway in Burkitt lymphoma. Leuk. Lymphoma, 2013, 54(10), 2263-2268.
51. Cheng, P.; Ni, Z.; Dai, X.; Wang, B.; Ding, W.; Rae, S. A.; Xu, L.; Wu, D.; He, F.; Lian, J. The novel BH-3 mimeticapogossypolone induces Beclin-1- And ROS-mediated autophagy in human hepatocellular carcinoma [corrected] cells. Cell. Death Dis., 2013, 4, e489.
52. Al-Gubory, K.H. Mitochondria: omega-3 in the route of mitochondrial reactive oxygen species. Int. J. Biochem. Cell. Biol., 2012, 44(9), 1569-1573.
53. Legrand-Poels, S.; Esser, N.; L'homme, L.; Scheen, A.; Paquot, N.; Piette, J. Free fatty acids as modulators of the NLRP3 inflammasome in obesity/type 2 diabetes. Biochem. Pharmacol., 2014, doi: 0.1016/j.bcp.2014.08.013.
54. Shin, S.; Jing, K.; Jeong, S.; Kim, N.; Song, K.S.; Heo, J.Y.; Park, J.H.; Seo, K.S.; Han, J.; Park, J.I.; Kweon, G.R.; Park, S.K.; Wu, T.; Hwang, B.D.; Lim, K. The omega-3 polyunsaturated fatty acid DHA induces simultaneous apoptosis and autophagy via mitochondrial ROS-mediated Akt-mTOR signaling in prostate cancer cells expressing mutant p53. Biomed. Res. Int., 2013, 2013, 568671.
55. Hernlund, E.; Ihrlund, L.S.; Khan, O.; Ates, Y.O.; Linder, S.; Panaretakis, T.; Shoshan, M.C. Potentiation of chemotherapeutic drugs by energy metabolism inhibitors 2- deoxyglucose and etomoxir. Int. J. Cancer, 2008, 123(2), 476-483.
56. Holubarsch, C.J.; Rohrbach, M.; Karrasch, M.; Boehm, E.; Polonski, L.; Ponikowski, P.; Rhein, S. A double-blind randomized multicentre clinical trial to evaluate the efficacy and safety of two doses of etomoxir in comparison with placebo in patients with moderate congestive heart failure: The ERGO (etomoxir for the recovery of glucose oxidation) study. Clin. Sci. (Lond)., 2007, 113(4), 205-212.
57. Iversen, P.O.; Sørensen, D.R.; Tronstad, K.J.; Gudbrandsen, O.A.; Rustan, A.C.; Berge, R.K.; Drevon, C.A. A bioactively modified fatty acid improves survival and impairs metastasis in preclinical models of acute leukemia. Clin. Cancer Res., 2006, 12, 3525-3231.
58. Berge, K.; Tronstad, K.J.; Bohov, P.; Madsen, L.; Berge, R.K. Impact of mitochondrial beta-oxidation in fatty acidmediated inhibition of glioma cell proliferation. J. Lipid. Res., 2003, 44(1), 118-127.
59. An, N.; Kang, Y. Thioredoxin and hematologic malignancies. Adv. Cancer Res., 2014, 122, 245-279.
60. Luo, Z.; Yu, L.; Yang, F.; Zhao, Z.; Yu, B.; Lai, H.; Wong, K.H.; Ngai, S.M.; Zheng, W.; Chen, T. Ruthenium polypyridyl complexes as inducer of ROS-mediated apoptosis in cancer cells by targeting thioredoxin reductase. Metallomics, 2014, 6(8), 1480-1490.
61. Liu, J.J.; Liu, Q.; Wei, H.L.; Yi, J.; Zhao, H.S.; Gao, L.P. Inhibition of thioredoxin reductase by auranofin induces apoptosis in adriamycin-resistant human K562 chronic myeloid leukemia cells. Pharmazie, 2011, 66(6), 440-444.
62. Wang, L.; Fu, J.N.; Wang, J.Y.; Jin, C.J.; Ren, X.Y.; Tan, Q., Li, J.; Yin, H.W.; Xiong, K.; Wang, T.Y.; Liu, X.M.; Zeng, H.H. Selenium-containing thioredoxin reductase inhibitor ethaselen sensitizes non-small cell lung cancer to radiotherapy. Anticancer Drugs, 2011, 22(8), 732-740.
63. Xing, F.; Li, S.; Ge, X.; Wang, C.; Zeng, H.; Li, D.; Dong, L. The inhibitory effect of a novel organoselenium compound BBSKE on the tongue cancer Tca8113 in vitro and in vivo. Oral. Oncol., 2008, 44(10), 963-969.
64. Tao, M.; You, C.P.; Zhao, R.R.; Liu, S.J.; Zhang, Z.H.; Zhang, C.; Liu, Y. Animal mitochondria: evolution, function, and disease. Curr. Mol. Med., 2014, 14(1), 115-124.
65. Dorn, G.W.; Kitsis, R.N. The mitochondrial dynamismmitophagy- cell death interactome: multiple roles performed by members of a mitochondrial molecular ensemble. Circ. Res., 2014, pii:CIRCRESAHA.114.303554.
66. Frank, M.; Duvezin-Caubet, S.; Koob, S.; Occhipinti, A.; Jagasia, R.; Petcherski, A.; Ruonala, M.O.; Priault, M.; Salin, B.; Reichert, A.S. Mitophagy is triggered by mild oxidative stress in a mitochondrial fission dependent manner. Biochim. Biophys. Acta, 2012, 1823(12), 2297-2310.
67. Tanida, I. Autophagosome formation and molecular mechanism of autophagy. Antioxid. Redox. Signal., 2011, 14(11), 2201-2214.
68. Houten, S.M.; Denis, S.; Te Brinke, H.; Jongejan, A.; van Kampen, A.H.; Bradley, E.J.; Baas, F.; Hennekam, R.C.; Millington, D.S.; Young, S.P.; Frazier, D.M.; Gucsavas- Calikoglu, M.; Wanders, R.J. Mitochondrial NADP(H) deficiency due to a mutation in NADK2 causes dienoyl-CoA reductase deficiency with hyperlysinemia. Hum. Mol. Genet., 2014, 23(18), 5009-5016.
69. Marino, M.L.; Fais, S.; Djavaheri-Mergny, M.; Villa, A.; Meschini, S.; Lozupone, F.; Venturi, G.; Della Mina, P.; Pattingre, S.; Rivoltini, L.; Codogno, P.; De Milito, A. Proton pump inhibition induces autophagy as a survival mechanism following oxidative stress in human melanoma cells. Cell. Death Dis., 2010, 1, e87.
70. Duan, Y.; Zhao, X.; Ren, W.; Wang, X.; Yu, K.F.; Li, D.; Zhang, X.; Zhang, Q. Antitumor activity of dichloroacetate on C6 glioma cell: in. vitro and in. vivo evaluation. Onco Targets Ther., 2013, 6, 189-198.
71. Lin, G.; Hill, D.K.; Andrejeva, G.; Boult, J.K.; Troy, H.; Fong, A.C.; Orton, M.R.; Panek, R.; Parkes, H.G.; Jafar, M.; Koh, D.M.; Robinson, S.P.; Judson, I.R.; Griffiths, J.R.; Leach, M.O.; Eykyn, T.R.; Chung, Y.L. Dichloroacetate induces autophagy in colorectal cancer cells and tumours. Br. J. Cancer, 2014, 111(2), 375-385.
72. Kim, K.Y.; Yu, S.N.; Lee, S.Y.; Chun, S.S.; Choi, Y.L.; Park, Y.M.; Song, C.S.; Chatterjee, B.; Ahn, S.C. Salinomycin- induced apoptosis of human prostate cancer cells due to accumulated reactive oxygen species and mitochondrial membrane depolarization. Biochem. Biophys. Res. Commun., 2011, 413(1), 80-86.
73. Zhu, L.Q.; Zhen, Y.F.; Zhang, Y.; Guo, Z.X.; Dai, J.; Wang, X.D. Salinomycin activates AMP-activated protein kinase-dependent autophagy in cultured osteoblastoma cells: A negative regulator against cell apoptosis. PLoS One, 2013, 8(12), e84175.
74. Leskovar, A.; Wegele, H.; Werbeck, N. D.; Buchner, J.; Reinstein, J. The ATPase cycle of the mitochondrial Hsp90 analog Trap1. J. Biol. Chem., 2006, 283, 11677-11688.
75. Kang, B. H.; Altieri, D. C. Compartmentalized cancer drug discovery targeting mitochondrial Hsp90 chaperones. Oncogene, 2009, 28, 3681-3688.
76. Pridgeon, J. W.; Olzmann, J. A.; Chin, L. S.; Li, L. PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1. PLoS Biol., 2007, 5, e172.
77. Montesano, G. N.; Chirico, G.; Pirozzi, G.; Costantino, E.; Landriscina, M.; Esposito, F. Tumor necrosis factorassociated protein 1 (TRAP-1) protects cells from oxidative stress and apoptosis. Stress, 2007, 10, 342-350.
78. Yan, C.; Oh, J.S.; Yoo, S.H.; Lee, J.S.; Yoon, Y.G.; Oh, Y.J.; Jang, M.S.; Lee, S.Y.; Yang, J.; Lee, S.H.; Kim, H.Y.; Yoo, Y.H. The targeted inhibition of mitochondrial Hsp90 overcomes the apoptosis resistance conferred by Bcl-2 in Hep3B cells via necroptosis. Toxicol. Appl. Pharmacol., 2013, 266(1), 9-18.
79. Fulda, S.; Galluzzi, L.; Kroemer, G. Targeting mitochondria for cancer therapy. Nat. Rev. Drug Discov., 2009, 9, 447- 464.
80. Rico-Bautista, E.; Zhu, W.; Kitada, S.; Ganapathy, S.; Lau, E.; Krajewski, S.; Ramirez, J.; Bush, J.A.; Yuan, Z.; Wolf, D.A. Small molecule-induced mitochondrial disruption directs prostate cancer inhibition via UPR signaling. Oncotarget, 2013, 4(8), 1212-1229.
81. Rico-Bautista, E.; Yang, C.C.; Lu, L.; Roth, G.P.; Wolf, D.A. Chemical genetics approach to restoring p27Kip1 reveals novel compounds with antiproliferative activity in prostate cancer cells. BMC Biol., 2010, 8, 153.
82. Chen, S.; Sun, L.; Koya, K.; Tatsuta, N.; Xia, Z.; Korbut, T.; Du, Z.; Wu, J.; Liang, G.; Jiang, J.; Ono, M.; Zhou, D.; Sonderfan, A. Syntheses and antitumor activities of N'1, N'3-dialkyl-N'1, N'3-di-(alkylcarbonothioyl) malonohydrazide: The discovery of elesclomol. Bioorg. Med. Chem. Lett., 2013, 23(18), 5070-5076.
83. Kirshner, J.R.; He, S.; Balasubramanyam, V. Elesclomol induces cancer cell apoptosis through oxidative stress. Mol. Cancer Ther., 2008, 7(8): 2319-2327.
84. Qu, Y.; Wang, J.; Sim, M.S.; Liu, B.; Giuliano, A.; Barsoum, J.; Cui, X. Elesclomol, counteracted by Akt survival signaling, enhances the apoptotic effect of chemotherapy drugs in breast cancer cells. Breast Cancer Res. Treat., 2010, 121(2), 311-321.
85. Yadav, A.A.; Patel, D.; Hasinoff, B.B. Molecular mechanisms of the biological activity of the anticancer drug elesclomol and its complexes with Cu(II), Ni(II) and Pt(II)". J. Inorg. Biochem., 2013, 126, 1-6.
86. Horton, K.L.; Stewart, K.M.; Fonseca, S.B.; Guo, Q.; Kelley, S.O. Mitochondria-penetrating peptides. Chem. Biol., 2008, 15(4), 375-382.
87. Kelley, S.O.; Stewart, K.M.; Mourtada, R. Development of novel peptides for mitochondrial drug delivery: Amino acids featuring delocalized lipophilic cations. Pharm. Res., 2011, 28(11), 2808-2819.
88. Horton, K.L.; Pereira, M.P.; Stewart, K.M.; Fonseca, S.B.; Kelley, S.O. Tuning the activity of mitochondriapenetrating peptides for delivery or disruption. ChemBio- Chem, 2012; 13(3), 476-485.
89. Prezma, T.; Shteinfer, A.; Admoni, L.; Raviv, Z.; Sela, I.; Levi, I.; Shoshan-Barmatz, V. VDAC1-based peptides: novel pro-apoptotic agents and potential therapeutics for Bcell chronic lymphocytic leukemia. Cell. Death Dis., 2013, 4, e809.
90. Blatt, N.B.; Boitano, A.E.; Lyssiotis, C.A.; Opipari, A.W. Jr.; Glick, G.D. Bz-423 superoxide signals apoptosis via selective activation of JNK, Bak, and Bax. Free Radic. Biol. Med., 2008, 45(9), 1232-1242.
91. Giorgio, V.; von Stockum, S.; Antoniel, M.; Fabbro, A.; Fogolari, F.; Forte, M.; Glick, G.D.; Petronilli, V.; Zoratti, M.; Szabó, I.; Lippe, G.; Bernardi, P. Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc. Natl. Acad. Sci. USA, 2013, 110(15), 5887-5892.
92. Sheu, S.S.; Nauduri, D.; Anders, M.W. Targeting antioxidants to mitochondria: A new therapeutic direction. Biochim. Biophys. Acta, 2006, 1762(2), 256-265.
93. Smith, R.A.; Hartley, R.C.; Cochemé, H.M.; Murphy, M.P. Mitochondrial pharmacology. Trends Pharmacol. Sci., 2012, 33(6), 341-352.
94. Benrahmoune, M.; Thérond, P.; Abedinzadeh, Z. The reaction of superoxide radical with N-acetylcysteine. Free. Radic. Biol. Med., 2000, 29(8), 775-782.
95. Slyshenkov, V.S.; Dymkowska, D.; Wojtczak, L. Pantothenic acid and pantothenol increase biosynthesis of glutathione by boosting cell energetics. FEBS Lett., 2004, 569(1-3), 169-172.
96. Sharma, R.A.; Gescher, A.J.; Steward, W.P. Curcumin: The story so far. Eur. J. Cancer, 2005, 41(13), 1955-1968.
97. KC, S.; Cárcamo, J.M.; Golde, D.W. Vitamin C enters mitochondria via facilitative glucose transporter 1 (Glut1) and confers mitochondrial protection against oxidative injury. FASEB J., 2005, 19(12), 1657-1667.
98. Liu, Y.; Dai, C.; Gao, R.; Li, J. Ascorbic acid protects against colistin sulfate-induced neurotoxicity in PC12 cells. Toxicol. Mech. Methods, 2013, 23(8), 584-590.
99. Sliwa, A.; Góralska, J.; Czech, U.; Gruca, A.; Polus, A.; Zapała, B.; Dembinska-Kieć, A. Modulation of the human preadipocyte mitochondrial activity by beta-carotene. Acta Biochim. Pol., 2012, 59(1), 39-41.
100. Rochette, L.; Ghibu, S.; Richard, C.; Zeller, M.; Cottin, Y.; Vergely, C. Direct and indirect antioxidant properties of α- lipoic acid and therapeutic potential. Mol. Nutr. Food Res., 2013, 57(1), 114-125.
101. Valdecantos, M.P.; Pérez-Matute, P.; Quintero, P.; Martínez, J.A. Vitamin C, resveratrol and lipoic acid actions on isolated rat liver mitochondria: All antioxidants but different. Redox Rep., 2010, 15(5), 207-216.
102. Salvemini, D.; Riley, D.P.; Cuzzocrea, S. SOD mimetics are coming of age. Nat. Rev. Drug Discov., 2002, 1(5), 367- 374.
103. Shibuta, S.; Kosaka, J.; Mashimo, T.; Fukuda, Y.; Yoshiya, I. Nitric oxide-induced cytotoxicity attenuation by thiopentone sodium but not pentobarbitone sodium in primary brain cultures. Br. J. Pharmacol., 1998, 124(4), 804-810.
104. Dogan, Z.; Yuzbasioglu, M.F.; Kurutas, E.B.; Yildiz, H.; Coskuner, I.; Senoglu, N.; Oksuz, H.; Bülbüloglu, E. Thiopental improves renal ischemia-reperfusion injury. Ren. Fail., 2010, 32(3), 391-395.
105. Ariyama, J.; Shimada, H.; Aono, M.; Tsuchida, H.; Hirai, K.I. Propofol improves recovery from paraquat acute toxicity in. vitro and in. vivo. Intensive. Care Med., 2000, 26(7), 981-987.
106. Prabhakar, H.; Bindra, A.; Singh, G.P.; Kalaivani, M. Propofol versus thiopental sodium for the treatment of refractory status epilepticus. Evid. Based Child Health, 2013, 8(4), 1488-1508.
107. Ernster, L., Dallner, G. Biochemical, physiological and medical aspects of ubiquinone function. Biochim. Biophys. Acta, 1995, 1271(1), 195-204.
108. Crofts, A.R.; Hong, S.; Wilson, C.; Burton, R.; Victoria, D.; Harrison, C.; Schulten, K. The mechanism of ubihydroquinone oxidation at the Qo-site of the cytochrome bc1 complex. Biochim. Biophys. Acta, 2013, 1827(11-12), 1362- 1377.
109. Bolognesi, M.L.; Matera, R.; Minarini, A.; Rosini, M.; Melchiorre, C. Alzheimer's disease: new approaches to drug discovery. Curr. Opin. Chem. Biol., 2009, 13(3), 303-308.
110. Naia, L.; Ribeiro, M.J.; Rego, A.C. Mitochondrial and metabolic-based protective strategies in Huntington's disease: The case of creatine and coenzyme Q. Rev. Neurosci., 2011, 23(1), 13-28.
111. Ebadi, M.; Govitrapong, P.; Sharma, S.; Muralikrishnan, D.;, Shavali, S.; Pellett, L.; Schafer, R.; Albano, C.; Eken, J. Ubiquinone (coenzyme q10) and mitochondria in oxidative stress of parkinson's disease. Biol. Signals Recept., 2001, 10(3-4), 224-253.
112. Cleren, C.; Yang, L.; Lorenzo, B.; Calingasan, N.Y.; Schomer, A.; Sireci, A.; Wille, E.J.; Beal, M.F. Therapeutic effects of coenzyme Q10 (CoQ10) and reduced CoQ10 in the MPTP model of Parkinsonism. J. Neurochem., 2008, 104(6), 1613-1621.
113. Orsucci, D.; Mancuso, M.; Ienco, E.C.; LoGerfo, A.; Siciliano, G. Targeting mitochondrial dysfunction and neurodegeneration by means of coenzyme Q10 and its analogues. Curr. Med. Chem., 2011, 18(26), 4053-4064.
114. James, A.M.; Smith, RA.; Murphy, M.P. Antioxidant and prooxidant properties of mitochondrial Coenzyme Q. Arch. Biochem. Biophys., 2004, 423(1), 47-56.
115. Liberman, E.A.; Topaly, V.P.; Tsofina, L.M.; Jasaitis, A.A.; Skulachev, V.P. Mechanism of coupling of oxidative phosphorylation and the membrane potential of mitochondria. Nature, 1969, 222(5198), 1076-1078.
116. Filipovska, A.; Kelso, G.F.; Brown, S.E.; Beer, S.M.; Smith, R.A.; Murphy, M.P. Synthesis and characterization of a triphenylphosphonium- ubiquinonyl-decyltriphenylphosphonium (MitoQ) conjugated peroxidase mimetic. Insights into the interaction of ebselen with mitochondria. J. Biol. Chem., 2005, 280(25), 24113-24126.
117. 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(12), 1766-1780.
118. Cunniff, B.; Benson, K.; Stumpff, J.; Newick, K.; Held, P.; Taatjes, D.; Joseph, J.; Kalyanaraman, B., Heintz, N.H. Mitochondrial- Targeted nitroxides disrupt mitochondrial architecture and inhibit expression of peroxiredoxin 3 and FOXM1 in malignant mesothelioma cells. J. Cell. Physiol., 2013, 228(4), 835-845.
119. Cheng, G.; Lopez, M.; Zielonka, J.; Hauser, A.D.; Joseph, J.; McAllister, D.; Rowe, J.J.; Sugg, S.L.; Williams, C.L.; Kalyanaraman, B. Mitochondria-targeted nitroxides exacerbate fluvastatin-mediated cytostatic and cytotoxic effects in breast cancer cells. Cancer Biol. Ther., 2011, 12(8), 707- 717.
120. Tauskela, J.S. MitoQ-a mitochondria-targeted antioxidant. IDrugs, 2007, 10(6), 399-412.
121. Severin, F.F.; Severina, I.I.; Antonenko, Y.N.; Rokitskaya, T.I.; Cherepanov, D.A.; Mokhova, E.N.; Vyssokikh, M.Y.; Pustovidko, A.V.; Markova, O.V.; Yaguzhinsky, L.S.; Korshunov, G.A.; Sumbatyan, N.V.; Skulachev, M.V.; Skulachev, V.P. Penetrating cation/fatty acid anion pair as a mitochondria- Targeted protonophore. Proc. Natl. Acad. Sci. USA, 2010, 107(2), 663-668.
122. Skulachev, V.P.; Anisimov, V.N.; Antonenko, Y.N.; Bakeeva, L.E.; Chernyak, B.V.; Erichev, V.P., Filenko, O.F., Kalinina, N.I., Kapelko, V.I., Kolosova, N.G., Kopnin, B.P.; Korshunova, G.A.; Lichinitser, M.R.; Obukhova, L.A.; Pasyukova, E.G.; Pisarenko, O.I.; Roginsky, V.A.; Ruuge, E.K.; Senin, I.I.; Severina, I.I.; Skulachev, M.V.; Spivak, I.M.; Tashlitsky, V.N.; Tkachuk, VA.; Vyssokikh, M.Y.; Yaguzhinsky, L.S.; Zorov, D.B. An attempt to prevent senescence: A mitochondrial approach. Biochim. Biophys. Acta, 2009, 1787(5), 437-461.
123. Gruber, J.; Fong, S.; Chen, C.B.; Yoong, S.; Pastorin, G.; Schaffer, S.; Cheah, I.; Halliwell, B. Mitochondria-targeted antioxidants and metabolic modulators as pharmacological interventions to slow ageing. Biotechnol. Adv., 2013, 31(5), 563-592.
124. Ajith, T.A.; Jayakumar, T.G. Mitochondria-targeted agents: Future perspectives of mitochondrial pharmaceutics in cardiovascular diseases. World J. Cardiol., 2014, 6(10), 1091- 1099.
125. Szeto, H.H. Cell-permeable, mitochondrial-targeted, peptide antioxidants. AAPS J., 2006, 8(2), E277-E283.
126. Valero, T. Mitochondrial biogenesis: pharmacological approaches. Curr. Pharm. Des., 2014, 20(35), 5507-5509.
127. Kumaran, S.; Subathra, M.; Balu, M.; Panneerselvam, C. Age-associated decreased activities of mitochondrial electron transport chain complexes in heart and skeletal muscle: role of L-carnitine. Chem. Biol. Interact., 2004, 148(1-2), 11-18.
128. Ye, J.; Li, J.; Yu, Y.; Wei, Q.; Deng, W.; Yu, L. L-carnitine attenuates oxidant injury in HK-2 cells via ROSmitochondria pathway. Regul. Pept., 2010, 161(1-3), 58-66.
129. Wu, J.; Niu, J.; Li, X.; Wang, X.; Guo, Z.; Zhang, F. TGF- β1 induces senescence of bone marrow mesenchymal stem cells via increase of mitochondrial ROS production. BMC Dev. Biol., 2014, 14, 21.
130. Rucker, R.; Chowanadisai, W.; Nakano, M. Potential physiological importance of pyrroloquinoline quinone. Altern. Med. Rev., 2009, 14(3), 179-183.
131. Vos, M.; Esposito, G.; Edirisinghe, J.N.; Vilain, S.; Haddad, D.M.; Slabbaert, J.R.; Van Meensel, S.; Schaap, O.; De Strooper, B.; Meganathan, R.; Morais, V.A.; Verstreken, P. Vitamin K2 is a mitochondrial electron carrier that rescues pink1 deficiency. Science, 2012, 336(6086), 1306-1310.
132. Sai Varsha, M.K.; Raman, T.; Manikandan, R. Inhibition of diabetic-cataract by vitamin K1 involves modulation of hyperglycemia- induced alterations to lens calcium homeostasis. Exp. Eye. Res., 2014, A128, 73-82.
133. Pan, R.; Rong, Z.; She, Y.; Cao, Y.; Chang, L.W.; Lee, W.H. Sodium pyruvate reduces hypoxic-ischemic injury to neonatal rat brain. Pediatr. Res., 2012, 72(5), 479-489.
134. Simeone, K.A.; Matthews, S.A.; Samson, K.K.; Simeone, T.A. Targeting deficiencies in mitochondrial respiratory complex I and functional uncoupling exerts anti-seizure effects in a genetic model of temporal lobe epilepsy and in a model of acute temporal lobe seizures. Exp. Neurol., 2014, 251, 84-90.
135. Rambo, L.M.; Ribeiro, L.R.; Della-Pace, I.D.; Stamm, D.N.; da Rosa Gerbatin, R., Prigol, M.; Pinton, S.; Nogueira, C.W.; Furian, A.F.; Oliveira, M.S.; Fighera, M.R.; Royes, L.F. Acute creatine administration improves mitochondrial membrane potential and protects against pentylenetetrazol- induced seizures. Amino Acids, 2013, 44(3), 857- 868.
136. Webster, I.; Du Toit, E.F.; Huisamen, B.; Lochner, A. The effect of creatine supplementation on myocardial function and mitochondrial respiration to ischaemia/reperfusion injury in sedentary and exercised rats. Acta Physiol. (Oxf)., 2012, 206(1), 6-19.
137. Ribeiro, M.; Silva, A.C.; Rodrigues, J.; Naia, L.; Rego, A.C. Oxidizing effects of exogenous stressors in Huntington's disease knock-in striatal cells-protective effect of cystamine and creatine. Toxicol. Sci., 2013, 136(2), 487-499.
138. Schöls, L.; Vorgerd, M.; Schillings, M.; Skipka, G.; Zange, J. Idebenone in patients with Friedreich ataxia. Neurosci. Lett., 2001, 306(3), 169-172.
139. García-Giménez, J.L.; Gimeno, A.; Gonzalez-Cabo, P., Dasí, F.; Bolinches-Amorós, A.; Mollá, B.; Palau, F.; Pallardó, F.V. Differential expression of PGC-1α and metabolic sensors suggest age-dependent induction of mitochondrial biogenesis in Friedreich ataxia fibroblasts. PLoS One, 2011, 6(6), e20666.
140. Garrel, C.; Alessandri, J.M.; Guesnet, P.; Al-Gubory, K.H. Omega-3 fatty acids enhance mitochondrial superoxide dismutase activity in rat organs during post-natal development. Int. J. Biochem. Cell. Biol., 2012, 44(1), 123-131.
141. Zugno, A.I.; Chipindo, H.L.; Volpato, A.M.; Budni, J.; Steckert, A.V.; de Oliveira, M.B.; Heylmann, A.S.; da Rosa Silveira, F.; Mastella, G.A.; Maravai, S.G.; Wessler, P.G.; Binatti, A.R.; Panizzutti, B.; Schuck, P.F.; Quevedo, J.; Gama, C.S. Omega-3 prevents behavior response and brain oxidative damage in the ketamine model of schizophrenia. Neuroscience, 2014, 259, 223-231.
142. Kones, R. Mitochondrial therapy for Parkinson's disease: neuroprotective pharmaconutrition may be diseasemodifying. Clin. Pharmacol., 2010, 2, 185-198.
143. Kang, J.X. From fat to fat-1: A tale of omega-3 fatty acids. J. Membr. Biol., 2005, 206(2), 165-172.
144. Romanatto, T.; Fiamoncini, J.; Wang, B.; Curi, R.; Kang, J.X. Elevated tissue omega-3 fatty acid status prevents agerelated glucose intolerance in fat-1 transgenic mice. Biochim. Biophys. Acta, 2014, 1842(2), 186-191.
145. Rodrigo, R.; Prieto, J.C.; Castillo, R. Cardioprotection against ischaemia/reperfusion by vitamins C and E plus n-3 fatty acids: molecular mechanisms and potential clinical applications. Clin. Sci. (Lond), 2013, 124(1), 1-15.
146. Segal, A.W. How neutrophils kill microbes. Annu. Rev. Immunol., 2005, 9(5), 197-223.
147. Ray, P.D., Huang, B.W., Tsuji, Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal., 2012, 24(5), 981-990.
148. Ryter, S.W., Kim, H.P., Hoetzel, A., Park, J.W., Nakahira, K., Wang, X., Choi, A.M. Mechanisms of cell death in oxidative stress. Antioxid. Redox. Signal., 2007, 9(1), 49-89.
149. 2, a Necessary Evil for Cell Signaling. Science, 2006, 312(5782), 1882-1883.
150. Gugger, M., Waser, B., Kappeler, A., Schonbrunn, A., Reubi, J.C. Cellular detection of sst2A receptors in human gastrointestinal tissue. Gut, 2004, 53(10):1431-1436.