Nuclear delivery of doxorubicin via folate-targeted liposomes with bypass of multidrug-resistance efflux pump

Clinical Cancer Research

Volumn 6, Issue 5, 2000, Pages 1949-1957

  Goren, Dorit ^a   Horowitz, Aviva T ^a   Tzemach, Dina ^a   Tarshish, Mark ^a   Zalipsky, Samuel ^b   Gabizon, Alberto ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b ALZA CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; FOLIC ACID; GLYCOPROTEIN P; LIPOSOME; MACROGOL; PHOSPHATIDYLETHANOLAMINE; VERAPAMIL;

ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; DRUG DELIVERY SYSTEM; FLOW CYTOMETRY; LUNG CARCINOMA; MOUSE; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH;

ANIMALS; ANTINEOPLASTIC AGENTS; BINDING, COMPETITIVE; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL DIVISION; CELL NUCLEUS; DOXORUBICIN; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; FEMALE; FLOW CYTOMETRY; LIPOSOMES; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; NEOPLASMS, EXPERIMENTAL; RECEPTORS, CELL SURFACE; TUMOR CELLS, CULTURED;

EID: 0034031080     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (30)

1. Rothberg, K. G., Ying Y. S., Kolhouse, F. J., Kamen, B. A., and Anderson, R. G. W. The glycophospholipid-linked folate receptor internalizes folate without entering the clathrin-coated pit endocytotic pathway. J. Cell Biol., 110: 637-649, 1990.
2. Gates, S. B., Mendelsohn, L. G., Shackelford, K. A., Habeck, L. L., Kursar, J. D., Gossett, L. S., Worzalla, J. F., Shih, C., and Grindey, G. B. Characterization of folate receptor from normal and neoplastic murine tissue: influence of dietary folate on folate receptor expression. Clin. Cancer Res., 2: 1135-1141, 1996.
3. Weitman, S. D., Lark, R. H., Coney, L. R., Fort, D. W., Frasca, V., Zurawski, V. R., Jr., and Kamne, B. A. Distribution of the folate receptor GP38 in normal and malignant cell lines and tissues. Cancer Res., 52: 3396-3401, 1992.
4. Ross, J. F., Chaudhuri, P. K., and Ratnam, M. Differential regulation of folate receptor isoforms in normal and malignant tissues in vivo and in established cell lines. Cancer (Phila.), 73: 2432-2443, 1994.
5. Mantovani, L. T., Miotti, S., and Menard, S. Folate binding protein distribution in normal tissues and biological fluids from ovarian carcinoma patients as detected by the monoclonal antibodies MOv 18 and M0v19. Eur. J. Cancer, 30A: 363-369, 1994.
6. Anderson, R. G. W., Kamen, B. A., Rothberg, K. G., and Lacy, S. W. Potocytosis sequestration and transport of small molecules. Science (Washington DC), 255: 410-411, 1992.
7. Wang, S., and Low, P. S. Folate mediated targeting of anti-neoplastic drugs, imaging agents, and nucleic acids to cancer cells. J. Controlled Release, 53: 39-48, 1998.
8. Kranz, D. M., Patrick, T. A., Brigle, K. E., Sprinella, M. J., and Roy, E. J. Conjugates of folates and anti-T-cell receptor antibodies specifically target folate-receptor-positive tumor cells for lysis. Proc. Natl. Acad. Sci. USA, 92: 9057-9061, 1995.
9. Leamon, P. C., and Low, S. P. Delivery of macromolecules into living cells: a method that exploits folate receptor endocytosis. Proc. Natl. Acad. Sci. USA, 88: 5527-5576, 1991.
10. Lee, R. J., and Low, P. S. Delivery of liposomes into cultured KB cells via folate receptor-mediated endocytosis. J. Biol. Chem., 269: 3198-3204, 1994.
11. Lee, R. J., and Low, P. S. Folate-mediated tumor cell targeting of liposome-entrapped doxorubicin in vitro. Biochim. Biophys. Acta, 1233: 134-144, 1995.
12. Gottesman, M. M., Pastan, I., and Ambudkar, S. V. P-glycoprotein and multi drug resistance. Curr. Opin. Genet. Dev., 6: 610-617, 1996.
13. Dey, S., Ramachandra, M., Pastan, I., Gottesman, M. M., and Ambudkar, S. V. Evidence of two nonidentical drug resistance sites in the human P-glycoprotein. Proc. Natl. Acad. Sci. USA, 97: 10594-10599, 1997.
14. Gabizon, A., Horowitz, A. T., Goren, D., Tzemach, D., Mandelbaum-Shavit, F., Qazen, M. M., and Zalipsky, S. Targeting folate receptor with folate linked to the extremities of poly(ethylene glycol)-grafted liposomes: in vitro studies. Bioconjugate Chem., 10: 289-298, 1999.
15. 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: 201-215, 1993.
16. Working, P. K., and Dayan, A. D. Pharmacological-toxicological expert report. Caelyx. Hum. Exp. Toxicol., 15: 751-785, 1996.
17. Goren, D., Horowitz, A. T., Zalipsky, S., Woodle, M. C., Yarden, Y., and Gabizon, A. Targeting of stealth liposomes to erbB-2 (Her/2) receptor: in vitro and in vivo studies. Br. J. Cancer, 74: 1749-1756, 1996.
18. Horowitz, A. T., Barenholz, Y., and Gabizon, A. In vitro cytotoxicity of liposome-encapsulated doxorubicin: dependence on liposome composition and drug release. Biochim. Biophys. Acta, 1109: 203-209, 1992.
19. Lamy, T., Drenou, B., Grulois, I., Fardel, O., Jacquelinet, C., Goasguen, J., Dauriac, C., Amiot, L., Bernard, M., and Fauchet, R. Multi-drug resistance (MDR) activity in acute leukemia determined by rhodamine 123 efflux assay. Leukemia (Baltimore), 9: 1549-1555, 1995.
20. Webb, M., Raphael, C. L., Asbahr, H., Erber, W. N., and Meyer, B. F. The detection of rhodamine 123 efflux at low levels of drug resistance. Br. J. Haematol, 93: 650-655, 1996.
21. Wang, S., Lee, R. J., Cauchon, G., Gorenstein, D. G., and Low, P. S. Delivery of antisense oligonucleotides against the human epidermal growth factor receptor into cultured KB cells with liposomes conjugated to folate via polyethyleneglycol. Proc. Natl. Acad. Sci. USA, 92: 3318-3322, 1995.
22. Lee, R. J., Wang, S., and Low, P. S. Measurement of endosome pH following folate receptor-mediated endocytosis. Biochim. Biophys. Acta, 1312: 237-242, 1996.
23. Barenholz, Y., Amselem, S., Cohen, R., Gelvan, D., Samuni, A., Golden, E. B., and Gabizon, A. Stability of liposomal doxorubicin formulations: problems and prospects. Med. Res. Rev., 13: 449-491, 1993.
24. Baldini, N., Scotlandi, K., Serra, M., Shikita, T., Zini, N., Ognibene, A., Santi, S., Ferracini, R., and Maraldi, N. M. Nuclear immunolocalization of P-glycoprotein in multidrug-resistant cell lines showing similar mechanism of doxorubicin distribution. Eur. J. Cell Biol., 68: 226-239, 1995.
25. Molinari, A., Calcabrini, A., Meschini, S., Stringaro, A., Del Bufalo, D., Cianfriglia, M., and Arancia, G. Detection of P-glycoprotein in the Golgi apparatus of drug-untreated human melanoma cells. Int. J. Cancer, 75: 885-893, 1998.
26. Bradshaw, D. M., and Arceci, R. J. Clinical relevance of transmembrane drug efflux as a mechanism of multidrug resistance. J. Clin. Oncol., 16: 3674-3690, 1998.
27. Lasic, D. D., Fredrik, P. M., Stuart, M. C. A., Barenholz, Y., and McIntosh, T. J. Gelation of liposome interior: a novel method for drug encapsulation. FEBS Lett., 312: 255-258, 1992.
28. Li, X., Hirsh, D. J., Cabral-Lilly, D., Zirkel, A., Gruner, S. M., Janoff, A. S., and Perkins, W. R. Doxorubicin physical state in solution and inside liposomes loaded via a pH gradient. Biochim. Biophys. Acta, 1415: 23-40, 1998.
29. Eksborg, S. Extraction of daunorubicin and doxorubicin and their hydroxyl metabolites: self-association in aqueous solution. J. Pharm. Sci., 67: 782-785, 1978.
30. Mennozi, M., Valentini, L., Vannini E., and Arcamone, F. Self-association of doxorubicin and related compounds in aqueous solution. J. Pharm. Sci., 73: 766-770, 1984.