Marine sponge-derived sipholane triterpenoids reverse P-glycoprotein (ABCB1)-mediated multidrug resistance in cancer cells

Biochemical Pharmacology

Volumn 80, Issue 10, 2010, Pages 1497-1506

  Abraham, Ioana ^a   Jain, Sandeep ^b   Wu, Chung Pu ^c   Khanfar, Mohammad A ^b   Kuang, Yehong ^a,d   Dai, Chun Ling ^a,e   Shi, Zhi ^a,e   Chen, Xiang ^d   Fu, Liwu ^e   Ambudkar, Suresh V ^c   Sayed, Khalid El ^b   Chen, Zhe Sheng ^a  

^a ST JOHN'S UNIVERSITY   (United States)

^b UNIVERSITY OF LOUISIANA AT MONROE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d CENTRAL SOUTH UNIVERSITY   (China)

^e SUN YAT SEN UNIVERSITY   (China)

Author keywords

ABC transporter; Chemosensitivity; Multidrug resistance; P glycoprotein; Sipholane triterpenoid

Indexed keywords

ANTINEOPLASTIC AGENT; CALLYSPONGIA SIPHONELLA EXTRACT; GLYCOPROTEIN P; MITOXANTRONE; MULTIDRUG RESISTANCE PROTEIN 1; PACLITAXEL; SIPHOLENONE E; SIPHOLENONE L; SIPHONELLINOL D; TRITERPENOID; UNCLASSIFIED DRUG; VINBLASTINE; ABCB1 PROTEIN, HUMAN; LIGAND; MULTIDRUG RESISTANCE PROTEIN; PROTEIN BINDING;

ARTICLE; CALLYSPONGIA; CANCER CELL CULTURE; CHEMOSENSITIVITY; CYTOTOXICITY; DRUG EFFECT; DRUG INHIBITION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IC 50; LIGAND BINDING; MOLECULAR DOCKING; MULTIDRUG RESISTANCE; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; SQUAMOUS CELL CARCINOMA; WESTERN BLOTTING; ANIMAL; BINDING SITE; BIOSYNTHESIS; CELL SURVIVAL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; DRUG RESISTANCE; IMMUNOBLOTTING; ISOLATION AND PURIFICATION; METABOLISM; POLYACRYLAMIDE GEL ELECTROPHORESIS; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; BINDING SITES; CALLYSPONGIA; CELL LINE, TUMOR; CELL SURVIVAL; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HUMANS; IMMUNOBLOTTING; LIGANDS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; P-GLYCOPROTEIN; PROTEIN BINDING; P-GLYCOPROTEINS;

EID: 77957020543     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.08.001     Document Type: Article

References (52)

1. Ambudkar S.V., Kimchi-Sarfaty C., Sauna Z.E., Gottesman M.M. P-glycoprotein: from genomics to mechanism. Oncogene 2003, 22:7468-7485.
2. Gottesman M.M. Mechanisms of cancer drug resistance. Annu Rev Med 2002, 53:615-627.
3. Ambudkar S.V., Dey S., Hrycyna C.A., Ramachandra M., Pastan I., Gottesman M.M. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu Rev Pharmacol Toxicol 1999, 39:361-398.
4. Szakacs G., Paterson J.K., Ludwig J.A., Booth-Genthe C., Gottesman M.M. Targeting multidrug resistance in cancer. Nat Rev Drug Discov 2006, 5:219-234.
5. Robert J., Jarry C. Multidrug resistance reversal agents. J Med Chem 2003, 46:4805-4817.
6. Tan B., Piwnica-Worms D., Ratner L. Multidrug resistance transporters and modulation. Curr Opin Oncol 2000, 12:450-458.
7. Dantzig A.H., de Alwis D.P., Burgess M. Considerations in the design and development of transport inhibitors as adjuncts to drug therapy. Adv Drug Deliv Rev 2003, 55:133-150.
8. Teodori E., Dei S., Martelli C., Scapecchi S., Gualtieri F. The functions and structure of ABC transporters: implications for the design of new inhibitors of Pgp and MRP1 to control multidrug resistance (MDR). Curr Drug Targets 2006, 7:893-909.
9. Daenen S., van der Holt B., Verhoef G.E., Lowenberg B., Wijermans P.W., Huijgens P.C., et al. Addition of cyclosporin A to the combination of mitoxantrone and etoposide to overcome resistance to chemotherapy in refractory or relapsing acute myeloid leukaemia: a randomised phase II trial from HOVON, the Dutch-Belgian Haemato-Oncology Working Group for adults. Leuk Res 2004, 28:1057-1067.
10. Baer M.R., George S.L., Dodge R.K., O'Loughlin K.L., Minderman H., Caligiuri M.A., et al. Phase 3 study of the multidrug resistance modulator PSC-833 in previously untreated patients 60 years of age and older with acute myeloid leukemia: Cancer and Leukemia Group B Study 9720. Blood 2002, 100:1224-1232.
11. Nobili S., Landini I., Giglioni B., Mini E. Pharmacological strategies for overcoming multidrug resistance. Curr Drug Targets 2006, 7:861-879.
12. Fox E., Bates S.E. Tariquidar (XR9576): a P-glycoprotein drug efflux pump inhibitor. Expert Rev Anticancer Ther 2007, 7:447-459.
13. Pusztai L., Wagner P., Ibrahim N., Rivera E., Theriault R., Booser D., et al. Phase II study of tariquidar, a selective P-glycoprotein inhibitor, in patients with chemotherapy-resistant, advanced breast carcinoma. Cancer 2005, 104:682-691.
14. Sandler A., Gordon M., De Alwis D.P., Pouliquen I., Green L., Marder P., et al. A Phase I trial of a potent P-glycoprotein inhibitor, zosuquidar trihydrochloride (LY335979), administered intravenously in combination with doxorubicin in patients with advanced malignancy. Clin Cancer Res 2004, 10:3265-3272.
15. Tang R., Faussat A.M., Perrot J.Y., Marjanovic Z., Cohen S., Storme T., et al. Zosuquidar restores drug sensitivity in P-glycoprotein expressing acute myeloid leukemia (AML). BMC Cancer 2008, 8:51.
16. van Zuylen L., Sparreboom A., van der Gaast A., Nooter K., Eskens F.A., Brouwer E., et al. Disposition of docetaxel in the presence of P-glycoprotein inhibition by intravenous administration of R101933. Eur J Cancer 2002, 38:1090-1099.
17. Chi K.N., Chia S.K., Dixon R., Newman M.J., Wacher V.J., Sikic B., et al. A phase I pharmacokinetic study of the P-glycoprotein inhibitor, ONT-093, in combination with paclitaxel in patients with advanced cancer. Invest New Drugs 2005, 23:311-315.
18. Newman M.J., Rodarte J.C., Benbatoul K.D., Romano S.J., Zhang C., Krane S., et al. Discovery and characterization of OC144-093, a novel inhibitor of P-glycoprotein-mediated multidrug resistance. Cancer Res 2000, 60:2964-2972.
19. Le Cesne A., Blay J.Y., Judson I., Van Oosterom A., Verweij J., Radford J., et al. Phase II study of ET-743 in advanced soft tissue sarcomas: a European Organisation for the Research and Treatment of Cancer (EORTC) soft tissue and bone sarcoma group trial. J Clin Oncol 2005, 23:576-584.
20. Garcia-Carbonero R., Supko J.G., Maki R.G., Manola J., Ryan D.P., Harmon D., et al. Ecteinascidin-743 (ET-743) for chemotherapy-naive patients with advanced soft tissue sarcomas: multicenter phase II and pharmacokinetic study. J Clin Oncol 2005, 23:5484-5492.
21. Demetri G.D., Chawla S.P., von Mehren M., Ritch P., Baker L.H., Blay J.Y., et al. Efficacy and safety of trabectedin in patients with advanced or metastatic liposarcoma or leiomyosarcoma after failure of prior anthracyclines and ifosfamide: results of a randomized phase II study of two different schedules. J Clin Oncol 2009, 27:4188-4196.
22. Mita A.C., Hammond L.A., Bonate P.L., Weiss G., McCreery H., Syed S., et al. Phase I and pharmacokinetic study of tasidotin hydrochloride (ILX651), a third-generation dolastatin-15 analogue, administered weekly for 3 weeks every 28 days in patients with advanced solid tumors. Clin Cancer Res 2006, 12:5207-5215.
23. Bai R., Edler M.C., Bonate P.L., Copeland T.D., Pettit G.R., Luduena R.F., et al. Intracellular activation and deactivation of tasidotin, an analog of dolastatin 15: correlation with cytotoxicity. Mol Pharmacol 2009, 75:218-226.
24. El-Rayes B.F., Ali S., Philip P.A., Sarkar F.H. Protein kinase C: a target for therapy in pancreatic cancer. Pancreas 2008, 36:346-352.
25. Barr P.M., Lazarus H.M., Cooper B.W., Schluchter M.D., Panneerselvam A., Jacobberger J.W., et al. Phase II study of bryostatin 1 and vincristine for aggressive non-Hodgkin lymphoma relapsing after an autologous stem cell transplant. Am J Hematol 2009, 84:484-487.
26. Jimenez J.C., Lopez-Macia A., Gracia C., Varon S., Carrascal M., Caba J.M., et al. Structure-activity relationship of kahalalide F synthetic analogues. J Med Chem 2008, 51:4920-4931.
27. Martin-Algarra S., Espinosa E., Rubio J., Lopez Lopez J.J., Manzano J.L., Carrion L.A., et al. Phase II study of weekly Kahalalide F in patients with advanced malignant melanoma. Eur J Cancer 2009, 45:732-735.
28. Shi Z., Jain S., Kim I.W., Peng X.X., Abraham I., Youssef D.T., et al. Sipholenol A, a marine-derived sipholane triterpene, potently reverses P-glycoprotein (ABCB1)-mediated multidrug resistance in cancer cells. Cancer Sci 2007, 98:1373-1380.
29. Jain S., Laphookhieo S., Shi Z., Fu L.W., Akiyama S., Chen Z.S., et al. Reversal of P-glycoprotein-mediated multidrug resistance by sipholane triterpenoids. J Nat Prod 2007, 70:928-931.
30. Jain S., Abraham I., Carvalho P., Kuang Y.H., Shaala L.A., Youssef D.T., et al. Sipholane triterpenoids: chemistry, reversal of ABCB1/P-glycoprotein-mediated multidrug resistance, and pharmacophore modeling. J Nat Prod 2009, 72:1291-1298.
31. Akiyama S., Fojo A., Hanover J.A., Pastan I., Gottesman M.M. Isolation and genetic characterization of human KB cell lines resistant to multiple drugs. Somat Cell Mol Genet 1985, 11:117-126.
32. Chen Z.S., Hopper-Borge E., Belinsky M.G., Shchaveleva I., Kotova E., Kruh G.D. Characterization of the transport properties of human multidrug resistance protein 7 (MRP7, ABCC10). Mol Pharmacol 2003, 63:351-358.
33. Robey R.W., Honjo Y., Morisaki K., Nadjem T.A., Runge S., Risbood M., et al. Mutations at amino-acid 482 in the ABCG2 gene affect substrate and antagonist specificity. Br J Cancer 2003, 89:1971-1978.
34. Carmichael J., DeGraff W.G., Gazdar A.F., Minna J.D., Mitchell J.B. Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res 1987, 47:936-942.
35. Shi Z., Liang Y.J., Chen Z.S., Wang X.W., Wang X.H., Ding Y., et al. Reversal of MDR1/P-glycoprotein-mediated multidrug resistance by vector-based RNA interference in vitro and in vivo. Cancer Biol Ther 2006, 5:39-47.
36. Aoki S., Chen Z.S., Higasiyama K., Setiawan A., Akiyama A., Kobayashi M. Reversing effect of agosterol A, a spongean sterol acetate, on multidrug resistance in human carcinoma cells. Jpn J Cancer Res 2001, 92:886-895.
37. Shi Z., Tiwari A.K., Shukla S., Robey R.W., Kim I.W., Parmar S., et al. Inhibiting the function of ABCB1 and ABCG2 by the EGFR tyrosine kinase inhibitor AG1478. Biochem Pharmacol 2009, 77:781-793.
38. Tiberghien F., Loor F. Ranking of P-glycoprotein substrates and inhibitors by a calcein-AM fluorometry screening assay. Anticancer Drugs 1996, 7:568-578.
39. Schwab D., Fischer H., Tabatabaei A., Poli S., Huwyler J. Comparison of in vitro P-glycoprotein screening assays: recommendations for their use in drug discovery. J Med Chem 2003, 46:1716-1725.
40. Ambudkar S.V. Drug-stimulatable ATPase activity in crude membranes of human MDR1-transfected mammalian cells. Meth Enzymol 1998, 292:504-514.
41. Hrycyna C.A., Ramachandra M., Ambudkar S.V., Ko Y.H., Pedersen P.L., Pastan I., et al. Mechanism of action of human P-glycoprotein ATPase activity. Photochemical cleavage during a catalytic transition state using orthovanadate reveals cross-talk between the two ATP sites. J Biol Chem 1998, 273:16631-16634.
42. Sauna Z.E., Muller M., Peng X.H., Ambudkar S.V. 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, 41:13989-14000.
43. Sauna Z.E., Ambudkar S.V. Evidence for a requirement for ATP hydrolysis at two distinct steps during a single turnover of the catalytic cycle of human P-glycoprotein. Proc Natl Acad Sci USA 2000, 97:2515-2520.
44. Tripos Associates. SYBYL Molecular Modeling Software, version 8.0; Tripos Associates: St. Louis, MO, 2007; , accessed on 05/27/2010. http://www.tripos.com/.
45. Jain A.N. Surflex-Dock 2.1: Robust performance from ligand energetic modeling, ring flexibility, and knowledge-based search. J Comput Aided Mol Des 2007, 21:281-306.
46. Renes J., de Vries E.G., Nienhuis E.F., Jansen P.L., Muller M. ATP- and glutathione-dependent transport of chemotherapeutic drugs by the multidrug resistance protein MRP1. Br J Pharmacol 1999, 126:681-688.
47. Zhou Y., Hopper-Borge E., Shen T., Huang X.C., Shi Z., Kuang Y.H., et al. Cepharanthine is a potent reversal agent for MRP7(ABCC10)-mediated multidrug resistance. Biochem Pharmacol 2009, 77:993-1001.
48. Rabindran S.K., Ross D.D., Doyle L.A., Yang W., Greenberger L.M. Fumitremorgin C reverses multidrug resistance in cells transfected with the breast cancer resistance protein. Cancer Res 2000, 60:47-50.
49. Aller S.G., Yu J., Ward A., Weng Y., Chittaboina S., Zhuo R., et al. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 2009, 323:1718-1722.
50. Carson S.W., Ousmanou A.D., Hoyler S.L. Emerging significance of P-glycoprotein in understanding drug disposition and drug interactions in psychopharmacology. Psychopharmacol Bull 2002, 36:67-81.
51. Greenberger L.M. Major photoaffinity drug labeling sites for iodoaryl azidoprazosin in P-glycoprotein are within, or immediately C-terminal to, transmembrane domains 6 and 12. J Biol Chem 1993, 268:11417-11425.
52. Isenberg B., Thole H., Tummler B., Demmer A. Identification and localization of three photobinding sites of iodoarylazidoprazosin in hamster P-glycoprotein. Eur J Biochem 2001, 268:2629-2634.