Data mining of NCI's anticancer screening database reveals mitochondrial complex I inhibitors cytotoxic to leukemia cell lines

Biochemical Pharmacology

Volumn 73, Issue 3, 2007, Pages 331-340

  Glover, Constance J ^a   Rabow, Alfred A ^b   Isgor, Yasemin G ^a   Shoemaker, Robert H ^a   Covell, David G ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

Author keywords

Apoptosis; Drug discovery; Enzyme inhibition; K562 leukemia cells; Mitochondria; NADH: Coenzyme Q oxidoreductase; Self organized maps

Indexed keywords

ANTILEUKEMIC AGENT; ANTIMYCIN A1; ANTINEOPLASTIC AGENT; DIMETHYL SULFOXIDE; ENZYME INHIBITOR; GLUTAMIC ACID; MALIC ACID; NSC 618296; NSC 619195; NSC 619196; NSC 622637; NSC 645376; NSC 665111; NSC 668602; NSC 673301; NSC 692595; NSC 929621; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE) INHIBITOR; ROTENONE; SUCCINIC ACID;

ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER SCREENING; CELL PERMEABILIZATION; CELL STRAIN K 562; CONTROLLED STUDY; COW; DATA ANALYSIS; DATA BASE; DRUG CYTOTOXICITY; DRUG POTENCY; DRUG RESEARCH; DRUG TARGETING; ENZYME ACTIVITY; ENZYME INHIBITION; HEALTH CARE ORGANIZATION; HEART MITOCHONDRION; HUMAN; HUMAN CELL; IC 50; LEUKEMIA; LEUKEMIA CELL LINE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RESPIRATORY CHAIN; SUBMITOCHONDRIAL PARTICLE;

ANIMALS; ANTINEOPLASTIC AGENTS; CATTLE; CELL LINE, TUMOR; DATABASES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SCREENING ASSAYS, ANTITUMOR; ELECTRON TRANSPORT COMPLEX I; ENZYME INHIBITORS; LEUKEMIA; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 33845605490     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2006.10.005     Document Type: Article

References (75)

1. Ferreira C.G., Epping M., Kruyt F.A.E., and Giaccone G. Apoptosis: target of cancer therapy. Clin Cancer Res 8 (2002) 2024-2034
2. Makin G. Targeting apoptosis in cancer chemotherapy. Exp Opin Ther Targets 6 (2002) 73-84
3. Kaufman S.H., and Earnshaw W.C. Induction of apoptosis by cancer chemotherapy. Exp Cell Res 256 (2000) 42-49
4. Green D.R., and Kroemer G. The pathophysiology of mitochondrial cell death. Science 305 (2004) 626-629
5. Yano T. The energy-transducing NADH: quinone oxidoreductase, complex I. Mol Aspects Med 23 (2002) 345-368
6. Ricci J., Muñoz-Pinedo C., Fitzgerald P., Bailly-Maitre B., Perkins G.A., Yadava N., et al. Disruption of mitochondrial function during apoptosis is mediated by caspase cleavage of the p75 subunit of complex I of the electron transport chain. Cell 117 (2004) 773-786
7. Kushnareva Y., Murphy A.N., and Andreyev A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation-reduction state. Biochem J 368 (2002) 545-553
8. Cai Y., and Jones D.J. Superoxide in apoptosis. J Biol Chem 273 (1998) 11401-11404
9. Genova M.L., Ventura B., Giuliano G., Bovina C., Formiggini G., Castelli G.P., et al. The site of production of superoxide radical in mitochondrial complex I is not a bound ubisemiquinone but presumably iron-sulfur cluster N2. FEBS Lett 505 (2001) 364-368
10. Ricci J., Gottlieb R.A., and Green D.R. Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J Cell Biol 160 (2003) 65-75
11. Ricci J., Waterhouse N., and Green D.R. Mitochondrial functions during cell death, a complex (I-V) dilemma. Cell Death Differ 10 (2003) 488-492
12. Degli Esposti M., Ngo A., Ghelli A., Benelli B., Carelli V., McLennan H., et al. The interaction of Q analogs, particularly hydroxydecyl benzoquinone (Idebenone), with the respiratory complexes of heart mitochondria. Arch Biochem Biophys 330 (1996) 395-400
13. Dröge W. Free radicals in the physiological control of cell function. Physiol Rev 82 (2002) 47-95
14. Clayton R., Clark J.B., and Sharpe M. Cytochrome c release from rat brain mitochondria is proportional to the mitochondrial functional deficit: implications for apoptosis and neurodegenerative disease. J Neurochem 92 (2005) 840-849
15. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J.A., et al. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species. J Biol Chem 278 (2003) 8516-8525
16. Brill L.B., and Bennett J.P.J. Dependence on electron transport chain function and intracellular signaling of genomic responses in SH-SY5Y cells to the mitochondrial neurotoxin MPP+. Exp Neurol 181 (2003) 25-38
17. Yuan S.F., Chang H., Chen H., Yeh Y., Kao Y., Lin K., et al. Annonacin, a mono-tetrahydrofuran acetogenin, arrests cancer cells at the G1 phase and causes cytotoxicity in a Bax- and caspase-3-related pathway. Life Sci 72 (2003) 2853-2861
18. Zhu X., Liu Z., Xie B., Li Z., Feng G., Xie H., et al. Involvement of caspase-3 activation in squamocin-induced apoptosis in leukemia cell line HL-60. Life Sci 70 (2002) 1259-1269
19. Chih H., Chiu H., Tang K., Chang F., and Wu Y. Bullatacin, a potent antitumor annonaceous acetogenin, inhibits proliferation of human hepatocarcinoma cell line 2. 2. 15 by apoptosis induction. Life Sci 69 (2001) 1321-1331
20. Kallio A, Zheng A, Dahllund J, Heiskanen KM, Härkönen P. Role of mitochondria in tamoxifen-induced rapid death of MCF-7 breast cancer cells. Apoptosis 2005; October 3, 2005 [e-pub ahead of print].
21. Moreira PI, Custódio J, Moreno A, Oliveira CR, Santos MS. Tamoxifen and estradiol interact with the flavin mononucleotide site of complex I leading to mitochondrial failure. J Biol Chem, 2006 [e-pub Jan 12].
22. Carroll J., Fearnley I.M., Shannon R.J., Hirst J., and Walker J.E. Analysis of the subunit composition of complex I from bovine heart mitochondria. Mol Cell Proteomics 2 (2003) 117-126
23. Grigorieff N. Three-dimensional structure of bovine NADH:ubiquinone oxidoreductase (complex I) at 22 Å in ice. J Mol Biol 277 (1998) 1033-1046
24. Yagi T., and Matsuno-Yagi A. The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. Biochemistry 42 (2003) 2266-2274
25. Tormo J.R., Gonzalez M.C., Cortes D., and Estornell E. Kinetic characterization of mitochondrial complex I inhibitors using annonaceous acetogenins. Arch Biochem Biophys 369 (1999) 119-126
26. Degli Esposti M. Inhibitors of NADH-ubiquuinone reductase: an overview. Biochim Biophys Acta 1364 (1998) 222-235
27. Miyoshi H. Probing the ubiquinone reduction site in bovine mitochondrial complex I using a series of synthetic ubiquinones and inhibitors. J Bioenerg Biomembr 33 (2001) 223-231
28. Degli Esposti M., and Ghelli A. The mechanism of proton and electron transport in mitochondrial complex I. Biochim Biophys Acta 1187 (1994) 116-120
29. Friedrich T., Van Heek P., Leif H., Ohnishi T., Forche E., Kunze B., et al. Two binding sites of inhibitors in NADH:ubiquinone oxidoreductase (complex I). Eur J Biochem 219 (1994) 691-698
30. Okun J.G., Lümmen P., and Brandt U. Three classes of inhibitors share a common binding domain in mitochondrial complex I (NADH:ubiquinone oxidoreductase). J Biol Chem 274 (1999) 2625-2630
31. Rabow A.A., Shoemaker R.H., Sausville E.A., and Covell D.G. Mining the National Cancer Institute's tumor-screening database: identification of compounds with similar cellular activities. J Med Chem 45 (2002) 818-840
32. Monks A., Scudiero D., Skehan P., Shoemaker R., Paull K., Vistica D., et al. Feasibility of a high-flux anticancer drug screen using s diverse panel of cultured human tumor cell lines. J Natl Cancer Inst 83 (1991) 757-766
33. Monks A., Scudiero D.A., Johnson G.S., Paull K.D., and Sausville E.A. The NCI anti-cancer drug screen: a smart screen to identify effectors of novel targets. Anticancer Drug Des 12 (1997) 533-541
34. Boyd M.R. The NCI in vitro anticancer drug discovery screen. In: Teicher B.A. (Ed). Anticancer drug development guide: preclinical screening, clinical trials and approval (1995), Humana Press, Totowa, NJ p. 23-41
35. Shoemaker R.H., Scudiero D., Melillo G., Currens M.J., Monks A.P., Rabow A.A., et al. Application of high-throughput, molecular-targeted screening to anticancer drug discovery. Curr Top Med Chem 2 (2002) 229-246
36. Monga M., and Sausville E.A. Developmental therapeutics program at the NCI: molecular target and drug discovery process. Leukemia 16 (2002) 520-526
37. Paull K.D., Shoemaker R.H., Hodes L., Monks A., Scudiero D.A., Rubinstein L., et al. Display and analysis of patterns of differential activity of drugs against human tumor cell lines: development of mean graph and COMPARE algorithm. J Natl Cancer Inst 81 (1989) 1088-1092
38. Shi L.M., Fan Y., Myers T.G., O'Connor P.M., Paull K.D., Friend S.H., et al. Mining the NCI anticancer drug discovery databases: genetic function approximation for the QSAR study of anticancer ellipticine analogues. J Chem Inf Comput Sci 38 (1998) 189-199
39. Shi L.M., Fan Y., Lee J.K., Waltham M., Andrews D.T., Scherf U., et al. Mining and visualizing large anticancer drug discovery databases. J Chem Inf Comput Sci 40 (2000) 367-379
40. Blower P.E., Yang C., Fligner M.A., Verducci J.S., Richman S., and Weinstein J.N. Pharmacogenomic analysis: correlating molecular substructure classes with microarray gene expression data. Pharmacogenom J 2 (2002) 259-271
41. Wallqvist A., Rabow A.A., Shoemaker R.H., Sausville E.A., and Covell D.G. Establishing connections between microarray expression data and chemotherapeutic cancer pharmacology. Mol Cancer Ther 1 (2002) 311-320
42. Wallqvist A., Rabow A.A., Shoemaker R.H., Sausville E.A., and Covell D.G. Linking the growth inhibition response from the National Cancer Institute's anticancer screen to gene expression levels and other molecular target data. Bioinformatics 19 (2003) 2212-2224
43. Kohonen T. Self-organizing maps (1995), Springer Verlag, Berlin, Germany
44. Smith A.L. Preparation, properties, and conditions for assay of mitochondria: slaughterhouse material, small-scale. Meth Enzymol 10 (1967) 81-86
45. Pallotti F., and Lenaz G. Isolation and subfractionation of mitochondria from animal cells and tissue culture lines. Meth Cell Biol 65 (2001) 1-35
46. 1 segment of the respiratory chain. Biochim Biophys Acta 638 (1981) 282-289
47. Santos D.L., Moreno A.J.M., Leino R.L., Froberg M.K., and Wallace K.B. Carvedilol protects against doxorubicin-induced mitochondrial cardiomyopathy. Toxicol Appl Pharm 185 (2002) 218-227
48. Estornell E., Fato R., Pallotti F., and Lenax G. Assay conditions for the mitochondrial NADH:coenzyme Q oxidoreductase. FEBS Lett 332 (1993) 127-131
49. Jewess P.J., and Devonshire A.L. Kinetic microplate-based assays for inhibitors of mitochondrial NADH:ubiquinone oxidoreductase (complex I) and succinate:cytochrome c oxidoreductase. Anal Biochem 272 (1999) 56-63
50. Birch-Machin M.A., and Turnbull D.M. Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues. Meth Cell Biol 65 (2001) 97-117
51. Lenaz G., Fato R., Baracca A., and Genova M.L. Mitochondrial quinone reductases: complex I. Meth Enzymol 382 (2004) 3-20
52. Hofhaus G., Shakeley R.M., and Attardi G. Use of polarography to detect respiration defects in cell cultures. Meth Enzymol 264 (1996) 476-483
53. Chretien D., Bénit P., Chol M., Lebon S., Rötig A., Munnich A., et al. Assay of mitochondrial respiratory chain complex I in human lymphocytes and cultured skin fibroblasts. Biochem Biophys Res Commun 301 (2003) 222-224
54. Nakashima Y., Shinzawa-Itoh K., Watanabe K., Naoki K., Hano N., and Yoshikawa S. Steady-state kinetics of NADH:coenzyme Q oxidoreductase isolated from bovine heart mitochondria. J Bioenerg Biomembr 34 (2002) 11-19
55. Andreani A., Rambaldi M., Leoni A., Locatelli A., Ghelli A., Ratta M., et al. Thienylimidazo[2. 1-b]thiazoles as inhibitors of mitochondrial NADH dehyrogenase. J Med Chem 38 (1995) 1090-1097
56. Andreani A., Rambaldi M., Locatelli A., Leoni A., Ghelli A., and Degli Esposti M. Thienylvinylindoles as inhibitors of mitochondrial NADH dehydrogenase. Pharm Acta Helv 69 (1994) 15-20
57. Majander A., Huoponen K., Savontaus M., Nikoskelainen E., and Wikström M. Electron transfer properties of NADH:ubiquinone reductase in the ND1/3450 and the ND4/11778 mutations of the Leber hereditary optic neuroretinopathy (LHON). FEBS Lett 292 (1991) 289-292
58. Degli Esposti M., Ghelli A., Crimi M., Estornell E., Fato R., and Lenaz G. Complex I and complex III of mitochondria have common inhibitors acting as ubiquinone antagonists. Biochem Biophys Res Commun 190 (1993) 1090-1096
59. Lambert A.J., and Brand M.D. Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Biol Chem 279 (2004) 39414-39420
60. Willett P., Barnard J.M., and Downs G.M. Chemical similarity searching. J Chem Inf Comput Sci 38 (1998) 983-996
61. Martin Y.C., Kofron J.L., and Traphagen L.M. Do structurally similar molecules have similar biological activity?. J Med Chem 45 (2002) 4350-4358
62. Anderton M.J., Manson M.M., Verschoyle R.D., Gescher A., Lamb J.H., Farmer P.B., et al. Pharmacokinetics and tissue disposition of indole-3-carbinol and its acid condensation products after oral administration to mice. Clin Cancer Res 10 (2004) 5233-5241
63. Staub R.E., Feng C., Onisko B., Bailey G.S., Firestone G.L., and Bjeldanes L.F. Fate of Indole-3-carbinol in cultured human breast tumor cells. Chem Res Toxicol 15 (2002) 101-109
64. Miyoshi H., Ohshima M., Shimada H., Akagi T., Iwamura H., and McLaughlin J.L. Essential structural factors of annonaceous acetogenins as potent inhibitors of mitochondrial complex I. Biochim Biophys Acta 1365 (1998) 443-452
65. Alali F.Q., Liu X., and McLaughlin J.L. Annonaceous acetogenins: recent progress. J Nat Prod 62 (1999) 504-540
66. González-Coloma A., Guadaño A., de Inés C., Martínez-Díaz R., and Cortes D. Selective action of acetogenin mitochondrial complex I inhibitors. Z Naturforsch 57c (2002) 1028-1034
67. Shimada H., Grutzner J.B., Kozlowski J.F., and McLaughlin J.L. Membrane conformations and their relation to cytotoxicity of asimicin and its analogues. Biochemistry 37 (1998) 854-866
68. Motoyama T., Yabunaka H., and Miyoshi H. Essential structural factors of acetogenins, potent inhibitors of mitochondrial complex I. Bioorg Med Chem 12 (2002) 2089-2092
69. Kuwabara K., Takada M., Iwata J., Tatsumoto K., Sakamoto K., Iwamura H., et al. Design syntheses and mitochondrial complex I inhibitory activity of novel acetogenin mimics. Eur J Biochem 267 (2000) 2538-2546
70. Yabunaka H.Y., Abe M., Kenmochi A., Hamada T., Nishioka T., and Miyoshi H. Synthesis and inhibitory activity of ubiquinone-acetogenin hybrid inhibitor with bovine mitochondrial complex I. Bioorg Med Chem Lett 13 (2003) 2385-2388
71. Tormo J.R., and Estornell E. New evidence for the multiplicity of ubiquinone- and inhibitor-binding sites in the mitochondrial complex I. Arch Biochem Biophys 381 (2000) 241-246
72. Esposti M.D., and Ghelli A. Ubiquinone and inhibitor sites in complex I: one, two, or three?. Biochem Soc Trans 27 (1999) 606-609
73. Ohshima M., Miyoshi H., Sakamoto K., Takegami K., Iwata J., Kuwabara K., et al. Characterization of the ubiquinone reduction site of mitochondrial complex I using bulky synthetic ubiquinones. Biochemistry 37 (1998) 6436-6445
74. McGahon A., Bissonnette R., Schmitt M., Cotter K.M., Green D.R., and Cotter T.G. BCR-ABL maintains resistance of chronic myelogenous leukemia cells to apoptotic cell death. Blood 83 (1994) 1179-1187
75. Cao D., Qiao B., Ge Z., and Yuan Y. Comparison of burst of reactive oxygen species and activation of caspase-3 in apoptosis of K562 and HL-60 cells induced by docetaxel. Cancer Lett 214 (2004) 103-113