Targeting cancer cell mitochondria as a therapeutic approach

Future Medicinal Chemistry

Volumn 5, Issue 1, 2013, Pages 53-67

  Wen, Shijun ^a,b   Zhu, Daqian ^a,b   Huang, Peng ^a,c  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,5 DIAZIRIDINYL 3 (HYDROXYMETHYL) 6 METHYL 1,4 BENZOQUINONE; ACETYLSALICYLIC ACID; ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENT; ARSENIC TRIOXIDE; BERBERINE; CELASTROL; CERULENIN; CURCUMIN; EDELFOSINE; ELLIPTICINE; GAMITRINIB; HEMIDESMUS INDICUS EXTRACT; METFORMIN; MITOCHONDRIAL DNA; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; NAPHTHYRIDINE DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PANCRASTISTATIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RESVERATROL; RH 1; RHODAMINE 123; RUTHENIUM COMPLEX; SILVER CARBENE; SODIUM SELENITE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VOLTAGE DEPENDENT ANION CHANNEL;

ANTINEOPLASTIC ACTIVITY; CALCIUM HOMEOSTASIS; CANCER CELL; CELL CYCLE ARREST; CELL FATE; CELL METABOLISM; CELL VIABILITY; DRUG TARGETING; ENERGY METABOLISM; GENE MUTATION; GLYCOLYSIS; HUMAN; MACROMOLECULE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; RESPIRATORY CHAIN; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION;

HOMEOSTASIS; HUMANS; MITOCHONDRIA; NADPH OXIDASE; NEOPLASMS; OXIDATIVE PHOSPHORYLATION;

EID: 84871604292     PISSN: 17568919     EISSN: 17568927     Source Type: Journal    
DOI: 10.4155/fmc.12.190     Document Type: Review

References (93)

1. Trachootham D, Zhang H, Zhang W et al. Effective elimination of fludarabine-resistant CLL cells by PEITC through a redox-mediated mechanism. Blood 112(5), 1912-1922 (2008).
2. Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS-mediated mechanisms. a radical therapeutic approach? Nat. Rev. Drug Discov. 8(7), 579-591 (2009).
3. Lu W, Ogasawara MA, Huang P. Models of reactive oxygen species in cancer, Drug Discov. Today Dis. Models 4(2), 67-73 (2008).
4. Hara K, Kasahara E, Takahashi, N et al. Mitochondria determine the efficacy of anticancer agents that interact with DNA but not the cytoskeleton. J. Pharmacol. Exp. Ther. 337(3), 838-845 (2011).
5. Kim KH, Park JY, Jung HJ, Kwon HJ. Identification and biological activities of a new antiangiogenic small molecule that suppresses mitochondrial reactive oxygen species. Biochem. Biophy. Res. Commun. 404(1), 541-545 (2011).
6. Jeong NY, Yoo YH. Cerulenin-induced apoptosis is mediated by disrupting the interaction between AIF and hexokinase II. Int. J. Oncol. 40(6), 1949-1956 (2012).
7. Chen Z, Zhang H, Lu W, Huang P. Role of mitochondria-Associated hexokinase II in cancer cell death induced by 3-bromopyruvate. Biochim. Biophys. Acta 1787, 553-560 (2009).
8. Tang Z, Yuan S, Hu Y et al. Over-expression of GAPDH in human colorectal carcinoma as a preferred target of 3-bromopyruvate propyl ester. J. Bioenerg. Biomembr. 44(1), 117-125 (2012).
9. Fulda S, Kroemer G. Mitochondria as therapeutic targets for the treatment of malignant disease. Antioxid. Redox Sign. 15(12), 2937-2949 (2011).
10. Chen G, Wang F, Trachootham D, Huang P. Preferential killing of cancer cells with mitochondrial dysfunction by natural compounds. Mitochondrion 10, 614-625 (2010).
11. Wang F, Ogasawara MA, Huang P. Small mitochondria-targeting molecules as anti-cancer agents. Mol. Aspects Med. 31, 75-92 (2010).
12. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase. role in cardiovascular biology and disease. Circ. Res. 86, 494-501 (2000).
13. Lu W, Hu Y, Chen G et al. Novel role of NOX in supporting aerobic glycolysis in cancer cells with mitochondrial dysfunction and as a potential target for cancer therapy. PLoS Biol. 10(5), e1001326 (2012).
14. Rupprecht R, Papadopoulos V, Rammes G, Baghai TC et al. Translocator protein (18 kDa) (TSPO) as a therapeutic target for neurological and psychiatric disorders. Nat. Rev. Drug. Discov. 9(12), 971-988 (2010).
15. Ostuni MA, Ducroc R, Péranzi G et al. Translocator protein (18 kDa) ligand PK 11195 induces transient mitochondrial Ca2+ release leading to transepithelial Cl- secretion in HT-29 human colon cancer cells. Biol. Cell 99(11), 639-647 (2007).
16. Bai M, Rone MB, Papadopoulos V, Bornhop DJ. A novel functional translocator protein ligand for cancer imaging. Bioconjug. Chem. 18(6), 2018-2023 (2007).
17. Veenman L, Shandalov Y, Gavish M. VDAC activation by the 18 kDa translocator protein (TSPO), implications for apoptosis. J. Bioenerg. Biomembr. 40(3), 199-205 (2008).
18. Zheng J, Boisgard R, Siquier-Pernet K, Decaudin D, Dollé F, Tavitian B. Differential expression of the 18 kDa translocator protein (TSPO) by neoplastic and inflammatory cells in mouse tumors of breast cancer. Mol. Pharm. 8(3), 823-832. (2011).
19. Mukherjee S, Das SK. Translocator protein (TSPO) in breast cancer. Curr. Mol. Med. 12(4), 443-457 (2012).
20. Itahana K, Zhang Y. Mitochondrial p32 is a critical mediator of ARF-induced apoptosis. Cancer Cell 13(6), 542-553 (2008).
21. Itahana K, Clegg HV, Zhang Y. ARF in the mitochondria. the last frontier? Cell Cycle 7(23), 3641-3646 (2008).
22. McGee AM, Baines CP. Complement 1q-binding protein inhibits the mitochondrial permeability transition pore and protects against oxidative stress-induced death. Biochem. J. 433(1), 119-125 (2011).
23. Fogal V, Richardson AD, Karmali PP et al. Mitochondrial p32 protein is a critical regulator of tumor metabolism via maintenance of oxidative phosphorylation. Mol. Cell Biol. 30(6), 1303-1318 (2010).
24. Amamoto R, Yagi M, Song Y et al. Mitochondrial p32/C1QBP is highly expressed in prostate cancer and is associated with shorter prostate-specific antigen relapse time after radical prostatectomy. Cancer Sci. 102(3), 639-647 (2011).
25. McGee AM, Douglas DL, Liang Y, Hyder SM, Baines CP. The mitochondrial protein C1qbp promotes cell proliferation, migration and resistance to cell death. Cell Cycle 10(23), 4119-4127 (2011).
26. Luciakova K, Barath P, Poliakova D, Persson A, Nelson BD. Repression of the human adenine nucleotide translocase-2 gene in growth-Arrested human diploid cells. the role of nuclear factor-1. J. Biol. Chem. 278(33), 30624-30633 (2003).
27. Chevrollier A, Loiseau D, Reynier P, Stepien G. Adenine nucleotide translocase 2 is a key mitochondrial protein in cancer metabolism. Biochim. Biophys. Acta 1807(6), 562-567 (2011).
28. Le Bras M, Borgne-Sanchez A, Touat Z et al. Chemosensitization by knockdown of adenine nucleotide translocase-2. Cancer Res. 66(18), 9143-9152 (2006).
29. Jang JY, Choi Y, Jeon YK, Kim CW. Suppression of adenine nucleotide translocase-2 by vector-based siRNA in human breast cancer cells induces apoptosis and inhibits tumor growth in vitro and in vivo. Breast Cancer Res. 10(1), R11 (2008).
30. Jang JY, Jeon YK, Kim CW. Degradation of HER2/neu by ANT2 shRNA suppresses migration and invasiveness of breast cancer cells. BMC Cancer 10, 391 (2010).
31. Jang JY, Jeon YK, Choi Y, Kim CW. Short-hairpin RNA-induced suppression of adenine nucleotide translocase-2 in breast cancer cells restores their susceptibility to TRAIL-induced apoptosis by activating JNK and modulating TRAIL receptor expression. Mol. Cancer 9, 262 (2010).
32. Sharaf el dein O, Mayola E, Chopineau J, Brenner C. The adenine nucleotide translocase 2, a mitochondrial target for anticancer biotherapy. Curr. Drug Targets 12(6), 894-901 (2011).
33. Lin RY, Ver JC, Chaganti RSK, Golde DW. Human monocarboxylate transporter 2 (MCT2) is a high affinity pyruvate transporter. J. Biol. Chem. 273(44), 28959-28965 (1998).
34. Gallagher SM, Castorino JJ, Wang D, Philp NJ. Monocarboxylate transporter 4 egulates maturation and trafficking of CD147 to the plasma membrane in the metastatic breast cancer cell line MDA-MB-231. Cancer Res. 67, 4182-4189 (2007).
35. Vegran F, Boidot B, Michiels C, Sonveaux P, Feron O. Lactate influx through the endothelial cell monocarboxylate transporter MCT1 supports an NF-kB/IL-8 pathway that drives tumor angiogenesis. Cancer Res. 71, 2550-2560 (2011).
36. Diers AR, Broniowska KA, Chang CF, Hogg N. Pyruvate fuels mitochondrial respiration and proliferation of breast cancer cells. Effect of monocarboxylate transporter inhibition. Biochem. J. 444(3), 561-571 (2012).
37. Griffin C, Karnik A, McNulty J, Pandey S. Pancratistatin selectively targets cancer cell mitochondria and reduces growth of human colon tumor xenografts. Mol. Cancer Ther. 10(1), 57-68 (2011).
38. Eloy L, Jarrousse AS, Teyssot ML et al. Anticancer activity of silver-N-heterocyclic carbene complexes. Caspase-independent induction of apoptosis via mitochondrial apoptosis-inducing factor (AIF). ChemMedChem 7(5), 805-814 (2012).
39. Summerhayes IC, Lampidis TJ, Bernal SD et al. Unusual retention of rhodamine 123 by mitochondria in muscle and carcinoma cells. Proc. Natl Acad. Sci. USA 79, 5292-5296 (1982).
40. Bernal SD, Lampidis TJ, Summerhayes IC, Chen LB. Rhodamine-123 selectively reduces clonal growth of carcinoma cells in vitro. Science 218, 1117-1119 (1982).
41. Biswas S, Dodwadkar NS, Sawant RR, Koshkaryev A, Torchilin VP. Surface modification of liposomes with rhodamine- 123-conjugated polymer results in enhanced mitochondrial targeting. J. Drug Target. 19(7), 552-561 (2011).
42. Capozzi A, Mantuano E, Matarrese P et al. A new 4-phenyl-1,8- naphthyridine derivative affects carcinoma cell proliferation by impairing cell cycle progression and inducing apoptosis. Anticancer Agents Med. Chem. 12(6), 653-662 (2012).
43. Park MT, Song MJ, Oh ET et al. The anti-tumour compound, RH1, causes mitochondria-mediated apoptosis by activating c-Jun N-terminal kinase. Br. J. Pharmacol.163(3), 567-585 (2011).
44. Broadley K, Larsen L, Herst PM, Smith RAJ, Berridge MV, McConnell MJ. The novel phloroglucinol PMT7 kills glycolytic cancer cells by blocking autophagy and sensitizing to nutrient stress. J. Cell. Biochem. 112(7), 1869-1879 (2011).
45. Freitas M, Alves V, Sarmento-Ribeiro AB, Mota-Pinto A. Combined effect of sodium selenite and docetaxel on PC3 metastatic prostate cancer cell line. Biochem. Biophys. Res. Commun. 408(4), 713-719 (2011).
46. Mollinedo F, Fernandez M, Hornillos V et al. Involvement of lipid rafts in the localization and dysfunction effect of the anti-tumor ether phospholipid edelfosine in mitochondria. Cell Death Dis. 2(5), e158 (2011).
47. Dong LF, Low P, Dyason JC et al a-tocopheryl succinate induces apoptosis by targeting ubiquinone-binding sites in mitochondrial respiratory complex II. Oncogene 27(31), 4324-4335 (2008).
48. Dong LF, Jameson VJA, Tilly D et al. Mitochondrial targeting of vitamin E succinate enhances its pro-Apoptotic and anti-cancer activity via mitochondrial complex II. J. Biol. Chem. 286(5), 3717-3728 (2011).
49. Dong LF, Jameson, VJA, Tilly D et al. Mitochondrial targeting of a-tocopheryl succinate enhances its pro-Apoptotic efficacy. A new paradigm for effective cancer therapy. Free Radical Biol. Med. 50(11), 1546-1555 (2011).
50. Shen ZX, Chen GQ, Ni JH et al. Use of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia (APL). II. Clinical efficacy and pharmacokinetics in relapsed patients. Blood 89, 3354-3360 (1997).
51. Chen, YC, Lin-Shiau, SY, Lin JK. Involvement of reactive oxygen species and caspase 3 activation in arsenite-induced apoptosis. J. Cell Physiol. 177, 324-333 (1998).
52. Wang TS, Kuo CF, Jan KY, Huang H. Arsenite induces apoptosis in Chinese hamster ovary cells by generation of reactive oxygen species. J. Cell Physiol. 169, 256-268 (1996).
53. Pelicano H, Feng L, Zhou Y et al. Inhibition of mitochondrial respiration. a novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism. J. Biol. Chem. 278, 37832-37839 (2003).
54. Sun RC, Board PG, Blackburn AC.Targeting metabolism with arsenic trioxide and dichloroacetate in breast cancer cells. Mol. Cancer 10, 142 (2011).
55. Zhao H, Xing D, Chen Q. New insights of mitochondria reactive oxygen species generation and cell apoptosis induced by low dose photodynamic therapy. Eur. J. Cancer 47(18), 2750-2761(2011).
56. El-Sikhry HE, Miller GG, Madiyalakan MR, Seubert JM. Sonodynamic and photodynamic mechanisms of action of the novel hypocrellin sonosensitizer, SL017. Mitochondrial cell death is attenuated by 11, 12- epoxyeicosatrienoic acid. Invest. New Drugs, 29(6), 1328-1336 (2011).
57. Fedeles BI, Zhu AY, Young KS et al. Chemical genetics analysis of an aniline mustard anticancer agent reveals complex I of the electron transport chain as a target. J. Biol. Chem. 286(39), 33910-33920 (2011).
58. Raza H, John A, Benedict S. Acetylsalicylic acid-induced oxidative stress, cell cycle arrest, apoptosis and mitochondrial dysfunction in human hepatoma HepG2 cells. Eur. J. Pharmacol. 668(1-2), 15-24 (2011).
59. Kuznetsov AV, Margreiter R, Amberger A, Saks V, Grimm M. Changes in mitochondrial redox state, membrane potential and calcium precede mitochondrial dysfunction in doxorubicin-induced cell death. Biochim. Biophys. Acta 1813(6), 1144-1152 (2011).
60. Wang F, Liu J, Robbins D et al. Mutant p53 exhibits trivial effects on mitochondrial functions which can be reactivated by ellipticine in lymphoma cells. Apoptosis 16(3), 301-310 (2011).
61. Gogada R, Amadori M, Zhang H et al. Curcumin induces Apaf-1-dependent, p21- mediated caspase activation and apoptosis. Cell Cycle 10(23), 4128-4137 (2011).
62. Chatterjee SJ, Pandey, S. Chemo-resistant melanoma sensitized by tamoxifen to low dose curcumin treatment through induction of apoptosis and autophagy. Cancer Biol. Ther. 11(2), 216-228 (2011).
63. Gogada R, Prabhu V, Amadori M, Scott R, Hashmi S, Chandra D. Resveratrol induces p53-independent, X-linked inhibitor of apoptosis protein (XIAP)-mediated bax protein oligomerization on mitochondria to initiate cytochrome c release and caspase activation. J. Biol. Chem. 286(33), 28749-28760 (2011).
64. Freeman MR, Kim J, Lisanti MP, Di Vizio D. A metabolic perturbation by U0126 identifies a role for glutamine in resveratrol induced cell death. Cancer Biol. Ther. 12(11), 966-977 (2011).
65. Biasutto L, Mattarei A, Marotta E et al. Development of mitochondria-targeted derivatives of resveratrol. Bioorg. Med. Chem. Lett. 18, 5594-5597(2008).
66. Greathouse GA, Rigler NE. Isolation of the Alkaloids, Berberine and Berbamine, from Mathonia Swaseyi. Plant Physiol. 15(3), 563-564 (1940).
67. Letasiová S, Jantová S, Cipák L, Múcková M. Berberine-Antiproliferative activity in vitro and induction of apoptosis/necrosis of the U937 and B16 cells. Cancer Lett 239(2), 254-262 (2006).
68. Wang L, Liu L, Shi Y et al. Berberine induces caspase-independent cell death in colon tumor cells through activation of apoptosis-inducing factor. PLoS ONE 7(5), e36418 (2012).
69. Arison BH, and Omura S. Revised structure ofcerulenin. J. Antibiot. (Tokyo) 27, 28-30 (1974).
70. Nomura S, Horiuchi T, Omura S, Hata T. The action mechanism of cerulenin. I. Effect of cerulenin on sterol and fatty acid biosynthesis in yeast. J. Biochem. 1(5), 783-796 (1972).
71. Heiligtag SJ, Bredehorst R, David KA. Key role of mitochondria in cerulenin-mediated apoptosis. Cell Death Differ. 9(9), 1017-1025 (2002).
72. Fimognari C, Lenzi M, Ferruzzi L et al. Mitochondrial pathway mediates the antileukemic effects of hemidesmus indicus, a promising botanical drug . PLoS ONE 6(6), e21544 (2011).
73. Pandey S, Chatterjee SJ, Ovadje P, Mousa M, Hamm C. The efficacy of dandelion root extract in inducing apoptosis in drug-resistant human melanoma cells. Evid. Based Complement. Alternat. Med. 129045 (2011).
74. Tan C, Hu S, Liu J, Ji L. Synthesis, characterization, antiproliferative and anti-metastatic properties of two ruthenium- DMSO complexes containing 2,2́-biimidazole. Eur. J. Med. Chem. 46(5), 1555-1563 (2011).
75. Chonghaile TN, Sarosiek KA, Vo TT et al. Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy. Science 334(6059), 1129-1133 (2011).
76. Crawford N, Chacko AD, Savage KI et al. Platinum resistant cancer cells conserve sensitivity to BH3 domains and obatoclax induced mitochondrial apoptosis. Apoptosis 16(3), 311-320 (2011).
77. Ko JK, Choi KH, Peng J, He F et al. Amphipathic tail-Anchoring peptide and Bcl- 2 homology domain-3 (BH3) peptides from Bcl-2 family proteins induce apoptosis through different mechanisms. J. Biol. Chem. 286(11), 9038-9048 (2011).
78. Valero JG, Sancey L, Kucharczak J et al. Bax-derived membrane-Active peptides act as potent and direct inducers of apoptosis in cancer cells. J. Cell Sci. 124(4), 556-564 (2011).
79. Kang BH, Tavecchio M, Goel HL et al. Targeted inhibition of mitochondrial Hsp90 suppresses localised and metastatic prostate cancer growth in a genetic mouse model of disease. Br. J. Cancer 104(4), 629-634 (2011).
80. Peng B, Xu L, Cao F et al. HSP90 inhibitor, celastrol, arrests human monocytic leukemia cell U937 at G0/G1 in thiol-containing agents reversible way. Mol. Cancer 9, 79 (2010).
81. Dai Y, DeSano J, Tang W et al. Natural proteasome inhibitor celastrol suppresses androgen-independent prostate cancer progression by modulating apoptotic proteins and NF-kappaB. PLoS ONE 5(12), e14153 (2010).
82. Chen G, Zhang X, Zhao M et al. Celastrol targets mitochondrial respiratory chain complex I to induce reactive oxygen species-dependent cytotoxicity in tumor cells. BMC Cancer 11, 170 (2011).
83. Duque JE, Velez J, Samudio I, Lai E. Metformin as a novel component of metronomic chemotherapeutic use. a hypothesis. J. Exp. Clin. Med. 4(3), 140-144 (2012).
84. Lee KH, Hsu EC, Guh JH et al. Targeting energy metabolic and oncogenic signaling pathways in triple-negative breast cancer by a novel adenosine monophosphate-Activated protein kinase (AMPK) activator. J. Biol. Chem. 286(45), 39247-39258 (2011).
85. Zachar Z, Marecek J, Maturo C et al. Non-redox-Active lipoate derivates disrupt cancer cell mitochondrial metabolism and are potent anticancer agents in vivo. J. Mol. Med. 89(11), 1137-1148 (2011).
86. Betriu C, Rodríguez-Avial I, Sánchez BA et al. In vitro activities of tigecycline (GAR- 936) against recently isolated clinical bacteria in Spain. Antimicrob. Agents Chemother. 46(3), 892-895 (2002).
87. Škrtić M, Sriskanthadevan S, Jhas B et al. Inhibition of mitochondrial translation as a therapeutic strategy for human acute myeloid leukemia. Cancer Cell 20(5), 674-688 (2011).
88. Zhang X, Zheng Y, Fried LE et al. Disruption of the mitochondrial thioredoxin system as a cell death mechanism of cationic triphenylmethanes. Free Radical Biol. Med. 7, 811-820 (2011).
89. Neuzil J, Dong LF, Rohlena J, Truksa J, Ralph SJ. Classification of mitocans, anti-cancer drugs acting on mitochondria. Mitochondrion doi:10.1016/j.mito.2012.07.112 (2012) (Epub ahead of print).
90. Neuzil J, Wang XF, Dong LF, Low P, Ralph SJ. Molecular mechanism of 'mitocan'- induced apoptosis in cancer cells epitomizes the multiple roles of reactive oxygen species and Bcl-2 family proteins. FEBS Lett. 580(22), 5125-5129 (2006).
91. Trachootham D, Zhou Y, Zhang H et al. Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell 10(3), 241-252 (2006).
92. Chen G, Chen Z, Hu Y, Huang P. Inhibition of mitochondrial respiration and rapid depletion of mitochondrial glutathione by β-phenethyl isothiocyanate. mechanisms for anti-leukemia activity. Antioxid. Redox Signal. 15(12), 2911-2921 (2011).
93. Hammoudi N, Ahmed KB, Garcia-Prieto C, Huang P. Metabolic alterations in cancer cells and therapeutic implications. Chin. J. Cancer 30(8), 508-525 (2011).