Evidence for dual mode of action of a thiosemicarbazone, NSC73306: A potent substrate of the multidrug resistance-linked ABCG2 transporter

Molecular Cancer Therapeutics

Volumn 6, Issue 12, 2007, Pages 3287-3296

  Wu, Chung Pu ^a   Shukla, Suneet ^a   Calcagno, Anna Maria ^a   Hall, Matthew D ^a   Gottesman, Michael M ^a   Ambudkar, Suresh V ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BREAST CANCER RESISTANCE PROTEIN; GLYCOPROTEIN P; IODINE 125; MITOXANTRONE; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 4; MULTIDRUG RESISTANCE PROTEIN 5; NSC 73306; PRAZOSIN; THIOSEMICARBAZONE DERIVATIVE; TOPOTECAN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CANCER CELL; CONTROLLED STUDY; CYTOTOXICITY; DRUG ACCUMULATION; DRUG MECHANISM; DRUG PROTEIN BINDING; EMBRYO; ENZYME ACTIVATION; HUMAN; HUMAN CELL; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN TRANSPORT;

ATP-BINDING CASSETTE TRANSPORTERS; BLOTTING, WESTERN; CELL LINE, TUMOR; DRUG RESISTANCE, MULTIPLE; HUMANS; INDOLES; MITOXANTRONE; NEOPLASM PROTEINS; PHOTOAFFINITY LABELS;

EID: 37549027669     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-07-2005     Document Type: Article

References (49)

1. Gottesman MM, Pastan I, Ambudkar SV. P-glycoprotein and multidrug resistance. Curr Opin Genet Dev 1996;6:610-7.
2. Gottesman M, Ambudkar SV. Overview: ABC transporters and human disease. J Bioenerg Biomembr 2001;33:453-8.
3. Allen JD, Brinkhuis RF, van Deemter L, Wijnholds J, Schinkel AH. Extensive contribution of the multidrug transporters P-glycoprotein and Mrp1 to basal drug resistance. Cancer Res 2000;60:5761-6.
4. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002;2:48-58.
5. Henriksen U, Gether U, Litman T. Effect of Walker A mutation (K86M) on oligomerization and surface targeting of the multidrug resistance transporter ABCG2. J Cell Sci 2005;118:1417-26.
6. Xu J, Peng H, Chen Q, Liu Y, Dong Z, Zhang JT. Oligomerization domain of the multidrug resistance-associated transporter ABCG2 and its dominant inhibitory activity. Cancer Res 2007;67:4373-81.
7. Bates SE, Medina-Perez WY, Kohlhagen G, et al. ABCG2 mediates differential resistance to SN-38 (7-ethyl-10-hydroxycamptothecin) and homocamptothecins. J Pharmacol Exp Ther 2004;310:836-42.
8. Miyake K, Mickley L, Litman T, et al. Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res 1999;59:8-13.
9. Yoshikawa M, Ikegami Y, Sano K, et al. Transport of SN-38 by the wild type of human ABC transporter ABCG2 and its inhibition by quercetin, a natural flavonoid. J Exp Ther Oncol 2004;4:25-35.
10. Maliepaard M, van Gastelen MA, de Jong LA, et al. Overexpression of the BCRP/MXR/ABCP gene in a topotecan-selected ovarian tumor cell line. Cancer Res 1999;59:4559-63.
11. Scheffer GL, Maliepaard M, Pijnenborg AC, et al. Breast cancer resistance protein is localized at the plasma membrane in mitoxantrone- and topotecan-resistant cell lines. Cancer Res 2000;60:2589-93.
12. Kim M, Turnquist H, Jackson J, et al. The multidrug resistance transporter ABCG2 (breast cancer resistance protein 1) effluxes Hoechst 33342 and is overexpressed in hematopoietic stem cells. Clin Cancer Res 2002;8:22-8.
13. van Herwaarden AE, Schinkel AH. The function of breast cancer resistance protein in epithelial barriers, stem cells and milk secretion of drugs and xenotoxins. Trends Pharmacol Sci 2006;27:10-6.
14. Robey RW, Polgar O, Deeken J, To KW, Bates SE. ABCG2: determining its relevance in clinical drug resistance. Cancer Metastasis Rev 2007;26:39-57.
15. Jonker JW, Smit JW, Brinkhuis RF, et al. Role of breast cancer resistance protein in the bioavailability and fetal penetration of topotecan. J Natl Cancer Inst 2000;92:1651-6.
16. Sarkadi B, Homolya L, Szakacs G, Varadi A. Human multidrug resistance ABCB and ABCG transporters: participation in a chemoimmunity defense system. Physiol Rev 2006;86:1179-236.
17. Tsuruo T, Iida H, Tsukagoshi S, Sakurai Y. Overcoming of vincristine resistance in P388 leukemia in vivo and in vitro through enhanced cytotoxicity of vincristine and vinblastine by verapamil. Cancer Res 1981;41:1967-72.
18. Szakacs G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM. Targeting multidrug resistance in cancer. Nat Rev Drug Discov 2006;5:219-34.
19. Ludwig JA, Szakacs G, Martin SE, et al. Selective toxicity of NSC73306 in MDR1-positive cells as a new strategy to circumvent multidrug resistance in cancer. Cancer Res 2006;66:4808-15.
20. Szakacs G, Annereau JP, Lababidi S, et al. Predicting drug sensitivity and resistance: profiling ABC transporter genes in cancer cells. Cancer Cell 2004;6:129-37.
21. Chen ZS, Robey RW, Belinsky MG, et al. Transport of methotrexate, methotrexate polyglutamates, and 17β-estradiol 17-(β-D-glucuronide) by ABCG2: effects of acquired mutations at R482 on methotrexate transport. Cancer Res 2003;63:4048-54.
22. Honjo Y, Hrycyna CA, Yan QW, et al. Acquired mutations in the MXR/BCRP/ABCP gene alter substrate specificity in MXR/BCRP/ABCP-overexpressing cells. Cancer Res 2001;61:6635-9.
23. Miwa M, Tsukahara S, Ishikawa E, Asada S, Imai Y, Sugimoto Y. Single amino acid substitutions in the transmembrane domains of breast cancer resistance protein (BCRP) alter cross resistance patterns in transfectants. Int J Cancer 2003;107:757-63.
24. Ozvegy-Laczka C, Koblos G, Sarkadi B, Varadi A. Single amino acid (482) variants of the ABCG2 multidrug transporter: major differences in transport capacity and substrate recognition. Biochim Biophys Acta 2005;1668:53-63.
25. Robey RW, Honjo Y, Morisaki K, et al. Mutations at amino-acid 482 in the ABCG2 gene affect substrate and antagonist specificity. Br J Cancer 2003;89:1971-8.
26. Barrand MA, Heppell-Parton AC, Wright KA, Rabbitts PH, Twentyman PR. A 190-kilodalton protein overexpressed in non-P-glycoprotein-containing multidrug-resistant cells and its relationship to the MRP gene. J Natl Cancer Inst 1994;86:110-7.
27. Wielinga PR, Reid G, Challa EE, et al. Thiopurine metabolism and identification of the thiopurine metabolites transported by MRP4 and MRP5 overexpressed in human embryonic kidney cells. Mol Pharmacol 2002;62:1321-31.
28. Wijnholds J, Mol CA, van Deemter L, et al. Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs. Proc Natl Acad Sci U S A 2000;97:7476-81.
29. Muller M, Yong M, Peng XH, Petre B, Arora S, Ambudkar SV. Evidence for the role of glycosylation in accessibility of the extracellular domains of human MRP1 (ABCC1). Biochemistry 2002;41:10123-32.
30. Robey RW, Medina-Perez WY, Nishiyama K, et al. Overexpression of the ATP-binding cassette half-transporter, ABCG2 (Mxr/BCrp/ABCP1), in flavopiridol-resistant human breast cancer cells. Clin Cancer Res 2001;7:145-52.
31. Ishiyama M, Tominaga H, Shiga M, Sasamoto K, Ohkura Y, Ueno K. A combined assay of cell viability and in vitro cytotoxicity with a highly water-soluble tetrazolium salt, neutral red and crystal violet. Biol Pharm Bull 1996;19:1518-20.
32. Robey RW, Steadman K, Polgar O, et al. Pheophorbide a is a specific probe for ABCG2 function and inhibition. Cancer Res 2004;64:1242-6.
33. Sauna ZE, Muller M, Peng XH, Ambudkar SV. Importance of the conserved Walker B glutamate residues, 556 and 1201, for the completion of the catalytic cycle of ATP hydrolysis by human P-glycoprotein (ABCB1). Biochemistry 2002;41:13989-4000.
34. Shukla S, Robey RW, Bates SE, Ambudkar SV. The calcium channel blockers, 1,4-dihydropyridines, are substrates of the multidrug resistance-linked ABC drug transporter, ABCG2. Biochemistry 2006;45:8940-51.
35. Ambudkar SV. Drug-stimulatable ATPase activity in crude membranes of human MDR1-transfected mammalian cells. Methods Enzymol 1998;292:504-14.
36. Sauna ZE, Nandigama K, Ambudkar SV. Multidrug resistance protein 4 (ABCC4)-mediated ATP hydrolysis: effect of transport substrates and characterization of the post-hydrolysis transition state. J Biol Chem 2004;279:48855-64.
37. Chen YN, Mickley LA, Schwartz AM, Acton EM, Hwang JL, Fojo AT. Characterization of adriamycin-resistant human breast cancer cells which display overexpression of a novel resistance-related membrane protein. J Biol Chem 1990;265:10073-80.
38. Grant CE, Valdimarsson G, Hipfner DR, Almquist KC, Cole SP, Deeley RG. Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res 1994;54:357-61.
39. Wu CP, Calcagno AM, Hladky SB, Ambudkar SV, Barrand MA. Modulatory effects of plant phenols on human multidrug-resistance proteins 1, 4 and 5 (ABCC1, 4 and 5). FEBS J 2005;272:4725-40.
40. Robey RW, Honjo Y, van de Laar A, et al. A functional assay for detection of the mitoxantrone resistance protein, MXR (ABCG2). Biochim Biophys Acta 2001;1512:171-82.
41. Chearwae W, Shukla S, Limtrakul P, Ambudkar SV. Modulation of the function of the multidrug resistance-linked ATP-binding cassette transporter ABCG2 by the cancer chemopreventive agent curcumin. Mol Cancer Ther 2006;5:1995-2006.
42. Pandeya SN, Dimmock JR. Recent evaluations of thiosemicarbazones and semicarbazones and related compounds for antineoplastic and anticonvulsant activities. Pharmazie 1993;48:659-66.
43. Whitnall M, Howard J, Ponka P, Richardson DR. A class of iron chelators with a wide spectrum of potent antitumor activity that overcomes resistance to chemotherapeutics. Proc Natl Acad Sci U S A 2006;103:14901-6.
44. Borst P, Elferink RO. Mammalian ABC transporters in health and disease. Annu Rev Biochem 2002;71:537-92.
45. Kuppens IE, Beijnen J, Schellens JH. Topoisomerase I inhibitors in the treatment of gastrointestinal cancer: from intravenous to oral administration. Clin Colorectal Cancer 2004;4:163-80.
46. Deeley RG, Westlake C, Cole SP. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol Rev 2006;86:849-99.
47. Ambudkar SV, Cardarelli CO, Pashinsky I, Stein WD. Relation between the turnover number for vinblastine transport and for vinblastine-stimulated ATP hydrolysis by human P-glycoprotein. J Biol Chem 1997;272:21160-6.
48. Clark R, Kerr ID, Callaghan R. Multiple drugbinding sites on the R482G isoform of the ABCG2 transporter. Br J Pharmacol 2006;149:506-15.
49. Beraldo H, Gambino D. The wide pharmacological versatility of semicarbazones, thiosemicarba-zones and their metal complexes. Mini Rev Med Chem 2004;4:31-9.