Ouabain, a Cardiac Glycoside, Inhibits the Fanconi Anemia/BRCA Pathway Activated by DNA Interstrand Cross-Linking Agents

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Wha Jun, Dong ^a   Hwang, Mihwa ^a   Kim, Hyun Jung ^a   Hwang, Soo Kyung ^a   Kim, Sunshin ^a   Lee, Chang Hun ^a  

^a National Cancer Center   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; ANTINEOPLASTIC AGENT; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CALCIUM ION; CARDIAC GLYCOSIDE; CISPLATIN; CURCUMIN; DIGITOXIN; DIGOXIN; FANC1 PROTEIN; FANCONI ANEMIA GROUP D2 PROTEIN; FANCONI ANEMIA PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOMYCIN; OUABAIN; UNCLASSIFIED DRUG;

ARTICLE; CANCER RESISTANCE; CELL CYCLE ARREST; CHEMOSENSITIZATION; CONTROLLED STUDY; DNA DAMAGE; DNA INTERSTRAND CROSS LINK; DNA REPAIR; DRUG BINDING; DRUG CYTOTOXICITY; DRUG STRUCTURE; DRUG TARGETING; ENZYME BINDING; FANCONI ANEMIA; GENE CONTROL; HEART DISEASE; HUMAN; HUMAN CELL; MOLECULAR LIBRARY; SCREENING; TUMOR CELL; UBIQUITINATION;

BLOTTING, WESTERN; CELL CYCLE; CELL LINE, TUMOR; CELL SURVIVAL; CISPLATIN; FANCONI ANEMIA; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MITOMYCIN; OUABAIN; SIGNAL TRANSDUCTION; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84885072141     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075905     Document Type: Article

References (38)

1. Helleday T, Petermann E, Lundin C, Hodgson B, Sharma RA, (2008) DNA repair pathways as targets for cancer therapy. Nat Rev Cancer 8: 193-204. doi:10.1038/nri2275. PubMed: 18256616.
2. Lord CJ, Garrett MD, Ashworth A, (2006) Targeting the double-strand DNA break repair pathway as a therapeutic strategy. Clin Cancer Res 12: 4463-4468. doi:10.1158/1078-0432.CCR-06-1269. PubMed: 16899589.
3. Madhusudan S, Hickson ID, (2005) DNA repair inhibition: a selective tumour targeting strategy. Trends Mol Med 11: 503-511. doi:10.1016/j.molmed.2005.09.004. PubMed: 16214418.
4. Furgason JM, Bahassi EM, (2013) Targeting DNA repair mechanisms in cancer. Pharmacol Therapeutics 137: 298-308. doi:10.1016/j.pharmthera.2012.10.009. PubMed: 23107892.
5. Musto P, D'Auria F, (2007) Melphalan: old and new uses of a still master drug for multiple myeloma. Expert Opin Invest Drugs 16: 1467-1487. doi:10.1517/13543784.16.9.1467. PubMed: 17714032.
6. Abu-Surrah AS, Kettunen M, (2006) Platinum group antitumor chemistry: design and development of new anticancer drugs complementary to cisplatin. Curr Med Chem 13: 1337-1357. doi:10.2174/092986706776872970. PubMed: 16712474.
7. Smith IE, Talbot DC, (1992) Cisplatin and its analogues in the treatment of advanced breast cancer: a review. Br J Cancer 65: 787-793. doi:10.1038/bjc.1992.169. PubMed: 1616849.
8. Taniguchi T, Tischkowitz M, Ameziane N, Hodgson SV, Mathew CG, et al. (2003) Disruption of the Fanconi anemia-BRCA pathway in cisplatin-sensitive ovarian tumors. Nat Med 9: 568-574. doi:10.1038/nm852. PubMed: 12692539.
9. Chen CC, Taniguchi T, D'Andrea A, (2007) The Fanconi anemia (FA) pathway confers glioma resistance to DNA alkylating agents. J Mol Med 85: 497-509. doi:10.1007/s00109-006-0153-2. PubMed: 17221219.
10. Chen Q, Van der Sluis PC, Boulware D, Hazlehurst LA, Dalton WS, (2005) The FA/BRCA pathway is involved in melphalan-induced DNA interstrand cross-link repair and accounts for melphalan resistance in multiple myeloma cells. Blood 106: 698-705. doi:10.1182/blood-2004-11-4286. PubMed: 15802532.
11. Chirnomas D, Taniguchi T, de la Vega M, Vaidya AP, Vasserman M, et al. (2006) Chemosensitization to cisplatin by inhibitors of the Fanconi anemia/BRCA pathway. Mol Cancer Ther 5: 952-961. doi:10.1158/1535-7163.MCT-05-0493. PubMed: 16648566.
12. Landais I, Sobeck A, Stone S, LaChapelle A, Hoatlin ME, (2009) A novel cell-free screen identifies a potent inhibitor of the Fanconi anemia pathway. Int J Cancer 124: 783-792. doi:10.1002/ijc.24039. PubMed: 19048618.
13. Taniguchi T, Garcia-Higuera I, Andreassen PR, Gregory RC, Grompe M, et al. (2002) S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 100: 2414-2420. doi:10.1182/blood-2002-01-0278. PubMed: 12239151.
14. Garcia-Higuera I, Taniguchi T, Ganesan S, Meyn MS, Timmers C, et al. (2001) Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 7: 249-262. doi:10.1016/S1097-2765(01)00173-3. PubMed: 11239454.
15. Kennedy RD, D'Andrea AD, (2005) The Fanconi Anemia/BRCA pathway: new faces in the crowd. Genes Dev 19: 2925-2940. doi:10.1101/gad.1370505. PubMed: 16357213.
16. Kim S, Jun DH, Kim HJ, Jeong KC, Lee CH, (2011) Development of a high-content screening method for chemicals modulating DNA damage response. J Biomol Screen 16: 259-265. doi:10.1177/1087057110392993. PubMed: 21233308.
17. Jun DW, Jeong YS, Kim HJ, Jeong KC, Kim S, et al. (2012) Characterization of DDRI-18 (3, 3'-(1H, 3'H-5, 5'-bibenzo [d] imidazole-2, 2'-diyl) dianiline), a novel small molecule inhibitor modulating the DNA damage response. Br J Pharmacol 167: 141-150. doi:10.1111/j.1476-5381.2012.01977.x. PubMed: 22519567.
18. Zhang JH, Chung TD, Oldenburg KR, (1999) A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. J Biomol Screen 4: 67-73. doi:10.1177/108705719900400206. PubMed: 10838414.
19. Prassas I, Diamandis EP, (2008) Novel therapeutic applications of cardiac glycosides. Nat Rev Drug Discov 7: 926-935. doi:10.1038/nrd2682. PubMed: 18948999.
20. Aperia A, (2007) New roles for an old enzyme: Na, K-ATPase emerges as an interesting drug target. J Intern Med 261: 44-52. doi:10.1111/j.1365-2796.2006.01745.x. PubMed: 17222167.
21. Smogorzewska A, Matsuoka S, Vinciguerra P, McDonald ER, Hurov KE, et al. (2007) Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 129: 289-301. doi:10.1016/j.cell.2007.03.009. PubMed: 17412408.
22. Deans AJ, West SC, (2011) DNA interstrand crosslink repair and cancer. Nat Rev Cancer 11: 467-480. doi:10.1038/nrc3088. PubMed: 21701511.
23. Zhang L, He M, Zhang Y, Nilubol N, Shen M, et al. (2012) Quantitative high-throughput drug screening identifies novel classes of drugs with anticancer activity in thyroid cancer cells: opportunities for repurposing. J Clin Endocrinol Metab 97: E319-E328. doi:10.1210/jc.2011-2671. PubMed: 22170715.
24. Hiyoshi H, Abdelhady S, Segerström L, Sveinbjörnsson B, Nuriya M, et al. (2012) Quiescence and γH2AX in neuroblastoma are regulated by ouabain/Na, K-ATPase. Br J Cancer 106: 1807-1815. doi:10.1038/bjc.2012.159. PubMed: 22531632.
25. Aizman O, Uhlén P, Lal M, Brismar H, Aperia A, (2001) Ouabain, a steroid hormone that signals with slow calcium oscillations. Proc Natl Acad Sci USA 98: 13420-13424. doi:10.1073/pnas.221315298. PubMed: 11687608.
26. Brouillard F, Tondelier D, Edelman A, Baudouin-Legros M, (2001) Drug resistance induced by ouabain via the stimulation of MDR1 gene expression in human carcinomatous pulmonary cells. Cancer Res 61: 1693-1698. PubMed: 11245485.
27. Xie Z, Cai T, (2003) Na+-K+--ATPase-mediated signal transduction: from protein interaction to cellular function. Mol Interventions 3: 157-168. doi:10.1124/mi.3.3.157.
28. Chou T-C, Talalay P, (1984) Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22: 27-55. doi:10.1016/0065-2571(84)90007-4. PubMed: 6382953.
29. Kennedy RD, Chen CC, Stuckert P, Archila EM, De la Vega MA, et al. (2007) Fanconi anemia pathway-deficient tumor cells are hypersensitive to inhibition of ataxia telangiectasia mutated. J Clin Invest 117: 1440-1449. doi:10.1172/JCI31245. PubMed: 17431503.
30. Lawrence TS, (1988) Ouabain sensitizes tumor cells but not normal cells to radiation. Int J Radiat Oncol Biol Phys 15: 953-958. doi:10.1016/0360-3016(88)90132-0. PubMed: 3182336.
31. Felth J, Rickardson L, Rosén J, Wickström M, Fryknäs M, et al. (2009) Cytotoxic effects of cardiac glycosides in colon cancer cells, alone and in combination with standard chemotherapeutic drugs. J Nat Prod 72: 1969-1974. doi:10.1021/np900210m. PubMed: 19894733.
32. Platz EA, Yegnasubramanian S, Liu JO, Chong CR, Shim JS, et al. (2011) A novel two-stage, transdisciplinary study identifies digoxin as a possible drug for prostate cancer treatment. Cancer Discov 1: 68-77. doi:10.1158/2159-8274.CD-10-0020 PubMed: 22140654.
33. Mijatovic T, Mathieu V, Gaussin J-F, De Nève N, Ribaucour F, et al. (2006) Cardenolide-induced lysosomal membrane permeabilization demonstrates therapeutic benefits in experimental human non-small cell lung cancers. Neoplasia (New York, NY) 8: 402-412. doi:10.1593/neo.05850. PubMed: 16790089.
34. Miyakawa-Naito A, Uhlén P, Lal M, Aizman O, Mikoshiba K, et al. (2003) Cell Signaling Microdomain with Na, K-ATPase and Inositol 1,4,5-Trisphosphate Receptor Generates Calcium Oscillations. J Biol Chem 278: 50355-50361. doi:10.1074/jbc.M305378200. PubMed: 12947118.
35. McConkey DJ, Lin Y, Nutt LK, Ozel HZ, Newman RA, (2000) Cardiac glycosides stimulate Ca2+ increases and apoptosis in androgen-independent, metastatic human prostate adenocarcinoma cells. Cancer Res 60: 3807-3812. PubMed: 10919654.
36. Xie C-M, Chan WY, Yu S, Zhao J, Cheng CH, (2011) Bufalin induces autophagy-mediated cell death in human colon cancer cells through reactive oxygen species generation and JNK activation. Free Radic Biol Med 51: 1365-1375. doi:10.1016/j.freeradbiomed.2011.06.016. PubMed: 21763418.
37. Li Y, Zhao L, Sun H, Yu J, Li N, et al. (2012) Gene Silencing of FANCF Potentiates the Sensitivity to Mitoxantrone through Activation of JNK and p38 Signal Pathways in Breast Cancer Cells. PLOS ONE 7: e44254. doi:10.1371/journal.pone.0044254. PubMed: 22952942.
38. Saadatzadeh MR, Bijangi-Vishehsaraei K, Kapur R, Haneline LS, (2009) Distinct roles of stress-activated protein kinases in Fanconi anemia type C-deficient hematopoiesis. Blood 113: 2655-2660. doi:10.1182/blood-2008-09-181420. PubMed: 19168785.