Lipid raft modulation by Rp1 reverses multidrug resistance via inactivating MDR-1 and Src inhibition

Biochemical Pharmacology

Volumn 85, Issue 10, 2013, Pages 1441-1453

  Yun, Un Jung ^a   Lee, Ji Hye ^a   Koo, Kyung Hee ^a   Ye, Sang Kyu ^b   Kim, Soo Youl ^a   Lee, Chang Hun ^a   Kim, Yong Nyun ^a  

^a National Cancer Center   (South Korea)

^b Seoul National University College of Medicine   (South Korea)

Author keywords

Actinomycin D; Ginsenosides; Lipid rafts; MDR 1; Src

Indexed keywords

CHOLESTEROL; DACTINOMYCIN; DOXORUBICIN; GINSENOSIDE; GINSENOSIDE RP 1; MULTIDRUG RESISTANCE PROTEIN 1; PROTEIN TYROSINE KINASE; RHODAMINE 123; UNCLASSIFIED DRUG;

ARTICLE; ATTENUATION; CONTROLLED STUDY; DOWN REGULATION; DRUG ACCUMULATION; DRUG POTENTIATION; DRUG SENSITIZATION; FEMALE; HUMAN; HUMAN CELL; INHIBITION KINETICS; LIPID RAFT; MULTIDRUG RESISTANCE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANTINEOPLASTIC AGENTS; CELL DEATH; CELL LINE, TUMOR; CHOLESTEROL; DACTINOMYCIN; DOXORUBICIN; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GINSENOSIDES; HUMANS; MEMBRANE MICRODOMAINS; ONCOGENE PROTEIN PP60(V-SRC); OVARIAN NEOPLASMS; P-GLYCOPROTEIN; RHODAMINE 123; SIGNAL TRANSDUCTION;

EID: 84876695004     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2013.02.025     Document Type: Article

References (53)

1. M.M. Gottesman, T. Fojo, and S.E. Bates Multidrug resistance in cancer: role of ATP-dependent transporters Nat Rev Cancer 2 2002 48 58
2. J.I. Fletcher, M. Haber, M.J. Henderson, and M.D. Norris ABC transporters in cancer: more than just drug efflux pumps Nat Rev Cancer 10 2010 147 156
3. J.M. Yang, Z. Xu, H. Wu, H. Zhu, X. Wu, and W.N. Hait Overexpression of extracellular matrix metalloproteinase inducer in multidrug resistant cancer cells Mol Cancer Res 1 2003 420 427
4. Q.Q. Li, J.D. Xu, W.J. Wang, X.X. Cao, Q. Chen, and F. Tang Twist1-mediated adriamycin-induced epithelial-mesenchymal transition relates to multidrug resistance and invasive potential in breast cancer cells Clin Cancer Res 15 2009 2657 2665
5. A. Abolhoda, A.E. Wilson, H. Ross, P.V. Danenberg, M. Burt, and K.W. Scotto Rapid activation of MDR1 gene expression in human metastatic sarcoma after in vivo exposure to doxorubicin Clin Cancer Res 5 1999 3352 3356
6. S.K. Patra Dissecting lipid raft facilitated cell signaling pathways in cancer Biochim Biophys Acta 1785 2008 182 206
7. E.K. Park, E.J. Lee, S.H. Lee, K.H. Koo, J.Y. Sung, and E.H. Hwang Induction of apoptosis by the ginsenoside Rh2 by internalization of lipid rafts and caveolae and inactivation of Akt Br J Pharmacol 160 2010 1212 1223
8. E.K. Park, M.J. Park, S.H. Lee, Y.C. Li, J. Kim, and J.S. Lee Cholesterol depletion induces anoikis-like apoptosis via FAK down-regulation and caveolae internalization J Pathol 218 2009 337 349
9. Y.C. Li, M.J. Park, S.K. Ye, C.W. Kim, and Y.N. Kim Elevated levels of cholesterol-rich lipid rafts in cancer cells are correlated with apoptosis sensitivity induced by cholesterol-depleting agents Am J Pathol 168 2006 1107 1118 quiz 404-5
10. S. Staubach, and F.G. Hanisch Lipid rafts: signaling and sorting platforms of cells and their roles in cancer Expert Rev Proteomics 8 2011 263 277
11. K.S. George, and S. Wu Lipid raft: a floating island of death or survival Toxicol Appl Pharmacol 259 2012 311 319
12. P. Lajoie, and I.R. Nabi Lipid rafts, caveolae, and their endocytosis Int Rev Cell Mol Biol 282 2010 135 163
13. L.J. Pike Growth factor receptors lipid rafts and caveolae: an evolving story Biochim Biophys Acta 1746 2005 260 273
14. S. Orlowski, S. Martin, and A. Escargueil P-glycoprotein and 'lipid rafts': some ambiguous mutual relationships (floating on them, building them or meeting them by chance?) Cell Mol Life Sci 63 2006 1038 1059
15. F. Fenyvesi, E. Fenyvesi, L. Szente, K. Goda, Z. Bacso, and I. Bacskay P-glycoprotein inhibition by membrane cholesterol modulation Eur J Pharm Sci 34 2008 236 242
16. Y. Lavie, G. Fiucci, and M. Liscovitch Up-regulation of caveolae and caveolar constituents in multidrug-resistant cancer cells J Biol Chem 273 1998 32380 32383
17. H.R. Shin, J.Y. Kim, T.K. Yun, G. Morgan, and H. Vainio The cancer-preventive potential of Panax ginseng: a review of human and experimental evidence Cancer Causes Control 11 2000 565 576
18. P.Y. Yue, N.K. Mak, Y.K. Cheng, K.W. Leung, T.B. Ng, and D.T. Fan Pharmacogenomics and the Yin/Yang actions of ginseng: anti-tumor, angiomodulating and steroid-like activities of ginsenosides Chin Med 2 2007 6
19. H.Y. Kwon, E.H. Kim, S.W. Kim, S.N. Kim, J.D. Park, and D.K. Rhee Selective toxicity of ginsenoside Rg3 on multidrug resistant cells by membrane fluidity modulation Arch Pharmacal Res 31 2008 171 177
20. J. Zhang, F. Zhou, X. Wu, X. Zhang, Y. Chen, and B.S. Zha Cellular pharmacokinetic mechanisms of adriamycin resistance and its modulation by 20(S)-ginsenoside Rh2 in MCF-7/Adr cells Br J Pharmacol 165 2012 120 134
21. Y. Kikuchi, H. Sasa, T. Kita, J. Hirata, T. Tode, and I. Nagata Inhibition of human ovarian cancer cell proliferation in vitro by ginsenoside Rh2 and adjuvant effects to cisplatin in vivo Anticancer Drugs 2 1991 63 67
22. T.Y. Park, M.H. Park, W.C. Shin, M.H. Rhee, D.W. Seo, and J.Y. Cho Anti-metastatic potential of ginsenoside Rp1, a novel ginsenoside derivative Biol Pharm Bull 31 2008 1802 1805
23. A. Kumar, M. Kumar, T.Y. Park, M.H. Park, T. Takemoto, and T. Terado Molecular mechanisms of ginsenoside Rp1-mediated growth arrest and apoptosis Int J Mol Med 24 2009 381 386
24. Y.N. Kim, G.J. Wiepz, A.G. Guadarrama, and P.J. Bertics Epidermal growth factor-stimulated tyrosine phosphorylation of caveolin-1 Enhanced caveolin-1 tyrosine phosphorylation following aberrant epidermal growth factor receptor status J Biol Chem 275 2000 7481 7491
25. M.A. Ghetie, R. Marches, S. Kufert, and E.S. Vitetta An anti-CD19 antibody inhibits the interaction between P-glycoprotein (P-gp) and CD19, causes P-gp to translocate out of lipid rafts, and chemosensitizes a multidrug-resistant (MDR) lymphoma cell line Blood 104 2004 178 183
26. G. Szakacs, J.K. Paterson, J.A. Ludwig, C. Booth-Genthe, and M.M. Gottesman Targeting multidrug resistance in cancer Nat Rev Drug Discov 5 2006 219 234
27. H.E. Mischo, P. Hemmerich, F. Grosse, and S. Zhang Actinomycin D induces histone gamma-H2AX foci and complex formation of gamma-H2AX with Ku70 and nuclear DNA helicase II J Biol Chem 280 2005 9586 9594
28. K. Simons, and D. Toomre Lipid rafts and signal transduction Nat Rev Mol Cell Biol 1 2000 31 39
29. P.Y. Grosse, F. Bressolle, and F. Pinguet Methyl-beta-cyclodextrin in HL-60 parental and multidrug-resistant cancer cell lines: effect on the cytotoxic activity and intracellular accumulation of doxorubicin Cancer Chemother Pharmacol 40 1997 489 494
30. S.W. Kamau, S.D. Kramer, M. Gunthert, and H. Wunderli-Allenspach Effect of the modulation of the membrane lipid composition on the localization and function of P-glycoprotein in MDR1-MDCK cells In Vitro Cell Dev Biol Anim 41 2005 207 216
31. J. Troost, H. Lindenmaier, W.E. Haefeli, and J. Weiss Modulation of cellular cholesterol alters P-glycoprotein activity in multidrug-resistant cells Mol Pharmacol 66 2004 1332 1339
32. L.W. Qi, C.Z. Wang, and C.S. Yuan American ginseng: potential structure-function relationship in cancer chemoprevention Biochem Pharmacol 80 2010 947 954
33. S.A. Nag, J.J. Qin, W. Wang, M.H. Wang, H. Wang, and R. Zhang Ginsenosides as anticancer agents: in vitro and in vivo activities, structure-activity relationships, and molecular mechanisms of action Front Pharmacol 3 2012 25
34. J. Zhang, F. Zhou, X. Wu, Y. Gu, H. Ai, and Zheng Y et al., 20(S)-ginsenoside Rh2 noncompetitively inhibits P-glycoprotein in vitro and in vivo: a case for herb-drug interactions Drug Metab Dispos 38 2010 2179 2187
35. M. Ehrlichova, R. Vaclavikova, I. Ojima, A. Pepe, L.V. Kuznetsova, and J. Chen Transport and cytotoxicity of paclitaxel, docetaxel, and novel taxanes in human breast cancer cells Naunyn-Schmiedeberg's Arch Pharmacol 372 2005 95 105
36. M. Liscovitch, and D. Ravid A case study in misidentification of cancer cell lines: MCF-7/AdrR cells (re-designated NCI/ADR-RES) are derived from OVCAR-8 human ovarian carcinoma cells Cancer Lett 245 2007 350 352
37. Y. Lavie, and M. Liscovitch Changes in lipid and protein constituents of rafts and caveolae in multidrug resistant cancer cells and their functional consequences Glycoconj J 17 2000 253 259
38. L.J. Mah, A. El-Osta, and T.C. Karagiannis gammaH2AX: a sensitive molecular marker of DNA damage and repair Leukemia 24 2010 679 686
39. D. Sooryakumar, T.S. Dexheimer, B.A. Teicher, and Y. Pommier Molecular and cellular pharmacology of the novel noncamptothecin topoisomerase I inhibitor Genz-644282 Mol Cancer Ther 10 2011 1490 1499
40. Z. Korade, and A.K. Kenworthy Lipid rafts, cholesterol, and the brain Neuropharmacology 55 2008 1265 1273
41. S. Meyer dos Santos, C.C. Weber, C. Franke, W.E. Muller, G.P. Eckert, and Cholesterol: Coupling between membrane microenvironment and ABC transporter activity Biochem Biophys Res Commun 354 2007 216 221
42. M.A. Ghetie, M. Crank, S. Kufert, I. Pop, and E. Vitetta Rituximab but not other anti-CD20 antibodies reverses multidrug resistance in 2 B lymphoma cell lines, blocks the activity of P-glycoprotein (P-gp), and induces P-gp to translocate out of lipid rafts J Immunother 29 2006 536 544
43. A. Aleshin, and R.S. Finn SRC a century of science brought to the clinic Neoplasia 12 2010 599 607
44. T. Hitosugi, M. Sato, K. Sasaki, and Y. Umezawa Lipid raft specific knockdown of SRC family kinase activity inhibits cell adhesion and cell cycle progression of breast cancer cells Cancer Res 67 2007 8139 8148
45. J.A. George, T. Chen, and C.C. Taylor SRC tyrosine kinase and multidrug resistance protein-1 inhibitions act independently but cooperatively to restore paclitaxel sensitivity to paclitaxel-resistant ovarian cancer cells Cancer Res 65 2005 10381 10388
46. Y. Pengetnze, M. Steed, K.F. Roby, P.F. Terranova, and C.C. Taylor Src tyrosine kinase promotes survival and resistance to chemotherapeutics in a mouse ovarian cancer cell line Biochem Biophys Res Commun 309 2003 377 383
47. K. Klappe, J.W. Hinrichs, B.J. Kroesen, H. Sietsma, and J.W. Kok MRP1 and glucosylceramide are coordinately over expressed and enriched in rafts during multidrug resistance acquisition in colon cancer cells Int J Cancer 110 2004 511 522
48. Y.Y. Liu, V. Gupta, G.A. Patwardhan, K. Bhinge, Y. Zhao, and J. Bao Glucosylceramide synthase upregulates MDR1 expression in the regulation of cancer drug resistance through cSrc and beta-catenin signaling Mol Cancer 9 2010 145
49. F.X. Mahon, S. Hayette, V. Lagarde, F. Belloc, B. Turcq, and F. Nicolini Evidence that resistance to nilotinib may be due to BCR-ABL, Pgp, or Src kinase overexpression Cancer Res 68 2008 9809 9816
50. K.J. Liu, J.H. He, X.D. Su, H.M. Sim, J.D. Xie, and X.G. Chen Saracatinib (AZD0530) is a potent modulator of ABCB1-mediated multidrug resistance in vitro and in vivo Int J Cancer 132 2012 224 235
51. K.M. Tainton, M.J. Smyth, J.T. Jackson, J.E. Tanner, L. Cerruti, and S.M. Jane Mutational analysis of P-glycoprotein: suppression of caspase activation in the absence of ATP-dependent drug efflux Cell Death Differ 11 2004 1028 1037
52. F. Greco, and M.J. Vicent Combination therapy: opportunities and challenges for polymer-drug conjugates as anticancer nanomedicines Adv Drug Delivery Rev 61 2009 1203 1213
53. H.J. Broxterman, and N.H. Georgopapadakou Anticancer therapeutics: "Addictive" targets, multi-targeted drugs, new drug combinations Drug Resist Updat 8 2005 183 197