Effect of transferrin receptor-targeted liposomal doxorubicin in P-glycoprotein-mediated drug resistant tumor cells

International Journal of Pharmaceutics

Volumn 329, Issue 1-2, 2007, Pages 94-102

  Kobayashi, Tomotaka ^a   Ishida, Tatsuhiro ^a   Okada, Yurie ^a   Ise, Saori ^a   Harashima, Hideyoshi ^b   Kiwada, Hiroshi ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Liposome; Multidrug resistance (MDR); P glycoprotein (P gp); Targeting; Transferrin

Indexed keywords

DOXORUBICIN; GLYCOPROTEIN P; LIPOSOME; PHOSPHATIDYLCHOLINE; TRANSFERRIN RECEPTOR;

ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DRUG ACCUMULATION; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG RELEASE; DRUG SENSITIVITY; DRUG TARGETING; ENCAPSULATION; ENDOCYTOSIS; HUMAN; HUMAN CELL; MULTIDRUG RESISTANCE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL;

ANTIBIOTICS, ANTINEOPLASTIC; CELL LINE, TUMOR; DOXORUBICIN; DRUG DELIVERY SYSTEMS; DRUG RESISTANCE, NEOPLASM; HUMANS; LIPOSOMES; NEOPLASMS; P-GLYCOPROTEIN; RECEPTORS, TRANSFERRIN;

EID: 33845595490     PISSN: 03785173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2006.08.039     Document Type: Article

References (55)

1. Allen T.M., and Everest J.M. Effect of liposome size and drug release properties on pharmacokinetics of encapsulated drug in rats. J. Pharmacol. Exp. Ther. 226 (1983) 539-544
2. Allen T.M., Hansen C., Martin F., Redemann C., and Yau-Young A. Liposomes containing synthetic lipid derivatives of poly(ethylene glycol) show prolonged circulation half-lives in vivo. Biochim. Biophys. Acta 1066 (1991) 29-36
3. Allen T.M. Long-circulating (sterically stabilized) liposomes for targeted drug delivery. Trends Pharmacol. Sci. 15 (1994) 215-220
4. Allen T.M., Mumbengegwi D.R., and Charrois G.J. Anti-CD19-targeted liposomal doxorubicin improves the therapeutic efficacy in murine B-cell lymphoma and ameliorates the toxicity of liposomes with varying drug release rates. Clin. Cancer Res. 11 (2005) 3567-3573
5. Bartlett G.R. Phosphorus assay in column chromatography. J. Biol. Chem. 234 (1959) 466-468
6. Dalton W.S. Mechanisms of drug resistance in hematologic malignancies. Semin. Hematol. 34 (1997) 3-8
7. Dalton W.S., and Jove R. Drug resistance in multiple myeloma: approaches to circumvention. Semin. Oncol. 26 (1999) 23-27
8. Del Poeta G., Venditti A., Aronica G., Stasi R., Cox M.C., Buccisano F., Bruno A., Tamburini F., Suppo G., Simone M.D., Epiceno A.M., Del Moro B., Masi M., Papa G., and Amadori S. P-glycoprotein expression in de novo acute myeloid leukemia. Leuk. Lymphoma 27 (1997) 257-274
9. Derycke A.S., Kamuhabwa A., Gijsens A., Roskams T., De Vos D., Kasran A., Huwyler J., Missiaen L., and de Witte P.A. Transferrin-conjugated liposome targeting of photosensitizer AlPcS4 to rat bladder carcinoma cells. J. Natl. Cancer Inst. 96 (2004) 1620-1630
10. Elliott R.L., Elliott M.C., Wang F., and Head J.F. Breast carcinoma and the role of iron metabolism. A cytochemical, tissue culture, and ultrastructural study. Ann. NY Acad. Sci. 698 (1993) 159-166
11. Forssen E.A., Male-Brune R., Adler-Moore J.P., Lee M.J., Schmidt P.G., Krasieva T.B., Shimizu S., and Tromberg B.J. Fluorescence imaging studies for the disposition of daunorubicin liposomes (DaunoXome) within tumor tissue. Cancer Res. 56 (1996) 2066-2075
12. Gabizon A.A. Selective tumor localization and improved therapeutic index of anthracyclines encapsulated in long-circulating liposomes. Cancer Res. 52 (1992) 891-896
13. Gijsens A., Derycke A., Missiaen L., De Vos D., Huwyler J., Eberle A., and de Witte P. Targeting of the photocytotoxic compound AlPcS4 to Hela cells by transferrin conjugated PEG-liposomes. Int. J. Cancer 101 (2002) 78-85
14. Goasguen J.E., Lamy T., Bergeron C., Ly Sunaram B., Mordelet E., Gorre G., Dossot J.M., Le Gall E., Grosbois B., Le Prise P.Y., and Fauchet R. Multifactorial drug-resistance phenomenon in acute leukemias: impact of P170-MDR1, LRP56 protein, glutathione-transferases and metallothionein systems on clinical outcome. Leuk. Lymphoma 23 (1996) 567-576
15. Goebel F.D., Goldstein D., Goos M., Jablonowski H., and Stewart J.S. Efficacy and safety of Stealth liposomal doxorubicin in AIDS-related Kaposi's sarcoma. The international SL-DOX study group. Brit. J. Cancer 73 (1996) 989-994
16. Goren D., Horowitz A.T., Tzemach D., Tarshish M., Zalipsky S., and Gabizon A. Nuclear delivery of doxorubicin via Folate-targeted liposomes with bypass of multidrug-resistance efflux pump. Clin. Cancer Res. 6 (2000) 1949-1957
17. Gottesman M.M., and Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem. 62 (1993) 385-427
18. Hamada H., and Tsuruo T. Purification of the 170 to 180-kilodalton membrane glycoprotein associated with multidrug resistance. 170 to 180-kilodalton membrane glycoprotein is an ATPase. J. Biol. Chem. 263 (1988) 1454-1458
19. Haran G., Cohen R., Bar L.K., and Barenholz Y. Transmembrane ammonium sulfate gradients in liposomes produce efficient and stable entrapment of amphipathic weak bases. Biochim. Biophys. Acta 1151 (1993) 201-215
20. Hertz R., and Barenholz Y. Permeability and integrity properties of lecithin-sphingomyelin liposomes. Chem. Phys. Lipids 15 (1975) 138-156
21. Huebers H.A., and Finch C.A. The physiology of transferrin and transferrin receptors. Physiol. Rev. 67 (1987) 520-582
22. Iinuma H., Maruyama K., Okinaga K., Sasaki K., Sekine T., Ishida O., Ogiwara N., Johkura K., and Yonemura Y. Intracellular targeting therapy of cisplatin-encapsulated transferrin-polyethylene glycol liposome on peritoneal dissemination of gastric cancer. Int. J. Cancer 99 (2002) 130-137
23. Ishida O., Maruyama K., Tanahashi H., Iwatsuru M., Sasaki K., Eriguchi M., and Yanagie H. Liposomes bearing polyethyleneglycol-coupled transferrin with intracellular targeting property to the solid tumors in vivo. Pharm. Res. 18 (2001) 1042-1048
24. Ishida T., Kirchmeier M.J., Moase E.H., Zalipsky S., and Allen T.M. Targeted delivery and triggered release of liposomal doxorubicin enhances cytotoxicity against human B lymphoma cells. Biochim. Biophys. Acta 1515 (2001) 144-158
25. Ishida T., Ichikawa T., Ichihara M., Sadzuka Y., and Kiwada H. Effect of the physicochemical properties of initially injected liposomes on the clearance of subsequently injected PEGylated liposomes in mice. J. Control. Release 95 (2004) 403-412
26. Kirpotin D., Hong K., Mullah N., Papahadjopoulos D., and Zalipsky S. Liposomes with detachable polymer coating: destabilization and fusion of dioleoylphosphatidylethanolamine vesicles triggered by cleavage of surface-grafted poly(ethylene glycol). FEBS Lett. 388 (1996) 115-118
27. Lopes de Menezes D.E., Pilarski L.M., and Allen T.M. In vitro and in vivo targeting of immunoliposomal doxorubicin to human B-cell lymphoma. Cancer Res. 58 (1998) 3320-3330
28. Mamot C., Drummond D.C., Hong K., Kirpotin D.B., and Park J.W. Liposome-based approaches to overcome anticancer drug resistance. Drug Resist. Updat. 6 (2003) 271-279
29. Marie J.P., Faussat-Suberville A.M., Zhou D., and Zittoun R. Daunorubicin uptake by leukemic cells: correlations with treatment outcome and MDR1 expression. Leukemia 7 (1993) 825-831
30. Maruyama K., Holmberg E., Kennel S.J., Klibanov A., Torchilin V.P., and Huang L. Characterization of in vivo immunoliposome targeting to pulmonary endothelium. J. Pharm. Sci. 79 (1990) 978-984
31. Matsuo H., Wakasugi M., Takanaga H., Ohtani H., Naito M., Tsuruo T., and Sawada Y. Possibility of the reversal of multidrug resistance and the avoidance of side effects by liposomes modified with MRK-16, a monoclonal antibody to P-glycoprotein. J. Control. Release 77 (2001) 77-86
32. Mayer L.D., Masin D., Nayar R., Boman N.L., and Bally M.B. Pharmacology of liposomal vincristine in mice bearing L1210 ascitic and B16/BL6 solid tumours. Brit. J. Cancer 71 (1995) 482-488
33. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Meth. 65 (1983) 55-63
34. Nagayasu A., Shimooka T., Kinouchi Y., Uchiyama K., Takeichi Y., and Kiwada H. Effects of fluidity and vesicle size on antitumor activity and myelosuppressive activity of liposomes loaded with daunorubicin. Biol. Pharm. Bull. 17 (1994) 935-939
35. Oudard S., Thierry A., Jorgensen T.J., and Rahman A. Sensitization of multidrug-resistant colon cancer cells to doxorubicin encapsulated in liposomes. Cancer Chemother. Pharmacol. 28 (1991) 259-265
36. Pagnan G., Montaldo P.G., Pastorino F., Raffaghello L., Kirchmeier M., Allen T.M., and Ponzoni M. GD2-mediated melanoma cell targeting and cytotoxicity of liposome-entrapped fenretinide. Int. J. Cancer 81 (1999) 268-274
37. Parajuli P., Yano S., Nishioka Y., Nokihara H., Hanibuchi M., Nishimura N., Utsugi T., and Sone S. Therapeutic efficacy of a new topoisomerase I and II inhibitor TAS-103, against both P-glycoprotein-expressing and -nonexpressing drug-resistant human small-cell lung cancer. Oncol. Res. 11 (1999) 219-224
38. Park J.W., Hong K., Kirpotin D.B., Colbern G., Shalaby R., Baselga J., Shao Y., Nielsen U.B., Marks J.D., Moore D., Papahadjopoulos D., and Benz C.C. Anti-HER2 immunoliposomes: enhanced efficacy attributable to targeted delivery. Clin. Cancer Res. 8 (2002) 1172-1181
39. Qian Z.M., Li H., Sun H., and Ho K. Targeted drug delivery via the transferrin receptor-mediated endocytosis pathway. Pharmacol. Rev. 54 (2002) 561-587
40. Rahman A., Husain S.R., Siddiqui J., Verma M., Agresti M., Center M., Safa A.R., and Glazer R.I. Liposome-mediated modulation of multidrug resistance in human HL-60 leukemia cells. J. Natl. Cancer Inst. 84 (1992) 1909-1915
41. Regev R., and Eytan G.D. Flip-flop of doxorubicin across erythrocyte and lipid membranes. Biochem. Pharmacol. 54 (1997) 1151-1158
42. Rensen P.C., Sliedregt L.A., Ferns M., Kieviet E., van Rossenberg S.M., van Leeuwen S.H., van Berkel T.J., and Biessen E.A. Determination of the upper size limit for uptake and processing of ligands by the asialoglycoprotein receptor on hepatocytes in vitro and in vivo. J. Biol. Chem. 276 (2001) 37577-37584
43. Riordan J.R., Deuchars K., Kartner N., Alon N., Trent J., and Ling V. Amplification of P-glycoprotein genes in multidrug-resistant mammalian cell lines. Nature 316 (1985) 817-819
44. Rivera E., Valero V., Esteva F.J., Syrewicz L., Cristofanilli M., Rahman Z., Booser D.J., and Hortobagyi G.N. Lack of activity of stealth liposomal doxorubicin in the treatment of patients with anthracycline-resistant breast cancer. Cancer Chemother. Pharmacol. 49 (2002) 299-302
45. Sapra P., and Allen T.M. Internalizing antibodies are necessary for improved therapeutic efficacy of antibody-targeted liposomal drugs. Cancer Res. 62 (2002) 7190-7194
46. Schadendorf D., Makki A., Stahr C., van Dyck A., Wanner R., Scheffer G.L., Flens M.J., Scheper R., and Henz B.M. Membrane transport proteins associated with drug resistance expressed in human melanoma. Am. J. Pathol. 147 (1995) 1545-1552
47. Shrivastava P., Hanibuchi M., Yano S., Parajuli P., Tsuruo T., and Sone S. Circumvention of multidrug resistance by a quinoline derivative, MS-209, in multidrug-resistant human small-cell lung cancer cells and its synergistic interaction with cyclosporin A or verapamil. Cancer Chemother. Pharmacol. 42 (1998) 483-490
48. Singh M. Transferrin as a targeting ligand for liposomes and anticancer drugs. Curr. Pharm. Des. 5 (1999) 443-451
49. Slovak M.L., Ho J.P., Bhardwaj G., Kurz E.U., Deeley R.G., and Cole S.P. Localization of a novel multidrug resistance-associated gene in the HT1080/DR4 and H69AR human tumor cell lines. Cancer Res. 53 (1993) 3221-3225
50. Spoelstra E.C., Dekker H., Schuurhuis G.J., Broxterman H.J., and Lankelma J. P-glycoprotein drug efflux pump involved in the mechanisms of intrinsic drug resistance in various colon cancer cell lines. Evidence for a saturation of active daunorubicin transport. Biochem. Pharmacol. 41 (1991) 349-359
51. Thierry A.R., Dritschilo A., and Rahman A. Effect of liposomes on P-glycoprotein function in multidrug resistant cells. Biochem. Biophys Res. Commun. 187 (1992) 1098-1105
52. Thierry A.R., Vige D., Coughlin S.S., Belli J.A., Dritschilo A., and Rahman A. Modulation of doxorubicin resistance in multidrug-resistant cells by liposomes. FASEB J. 7 (1993) 572-579
53. Ueda K., Cardarelli C., Gottesman M.M., and Pastan I. Expression of a full-length cDNA for the human "MDR1" gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 3004-3008
54. Warren L., Jardillier J.C., Malarska A., and Akeli M.G. Increased accumulation of drugs in multidrug-resistant cells induced by liposomes. Cancer Res. 52 (1992) 3241-3245
55. Xu L., Pirollo K.F., Tang W.H., Rait A., and Chang E.H. Transferrin-liposome-mediated systemic p53 gene therapy in combination with radiation results in regression of human head and neck cancer xenografts. Hum. Gene. Ther. 10 (1999) 2941-2952