In Vitro and in Vivo Characterization of Doxorubicin and Vincristine Coencapsulated within Liposomes through Use of Transition Metal Ion Complexation and pH Gradient Loading

Clinical Cancer Research

Volumn 10, Issue 2, 2004, Pages 728-738

  Abraham, Sheela A ^a,b   McKenzie, Cheryl ^a   Masin, Dana ^a   Ng, Rebecca ^a   Harasym, Troy O ^c   Mayer, Lawrence D ^a,b,c   Bally, Marcel B ^a,b,c  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c Celator Technologies Inc   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIMYCIN; DOXORUBICIN; DOXORUBICIN PLUS VINCRISTINE; LIPOSOME; MANGANESE; UNCLASSIFIED DRUG; VINCRISTINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG ELIMINATION; DRUG FORMULATION; DRUG MANUFACTURE; DRUG RELEASE; DRUG SCREENING; ENCAPSULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MAXIMUM TOLERATED DOSE; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ANTINEOPLASTIC AGENTS, PHYTOGENIC; BREAST NEOPLASMS; CALCIMYCIN; CELL LINE, TUMOR; COLORING AGENTS; DOXORUBICIN; HUMANS; HYDROGEN-ION CONCENTRATION; INHIBITORY CONCENTRATION 50; IONOPHORES; IONS; LIPID METABOLISM; LIPOSOMES; MANGANESE; MANGANESE COMPOUNDS; MICE; MICE, SCID; NEOPLASM TRANSPLANTATION; PROTONS; SULFATES; TETRAZOLIUM SALTS; THIAZOLES; TIME FACTORS; VINCRISTINE;

EID: 0842333135     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-1131-03     Document Type: Article

References (53)

1. Goldie, J. H. Drug resistance in cancer: a perspective. Cancer Metastisis Rev., 20: 63-68, 2001.
2. Hobbs, S. K., Monsky, W. L., Yuan, F., Roberts, W. G., Griffith, L., Torchilin, V. P., and Jain, R. K. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc. Natl. Acad. Sci. USA, 95: 4607-4612, 1998.
3. Rahman, A., Kessler, A., More, N., Sikic, B., Rowden, G., Woolley, P., and Schein, P. S. Liposomal protection of adriamycin-induced cardiotoxicity in mice. Cancer Res., 40: 1532-1537, 1980.
4. Mayer, L. D., Bally, M. B., Loughrey, H., Masin, D., and Cullis, P. R. Liposomal vincristine preparations which exhibit decreased drug toxicity and increased activity against murine L1210 and P388 tumors. Cancer Res., 50: 575-579, 1990.
5. Burke, T. G., and Gao, X. Stabilization of topotecan in low pH liposomes composed of distearoylphosphatidylcholine. J. Pharm. Sci., 83: 967-969, 1994.
6. Rihova, B. Immunomodulating activities of soluble synthetic polymer-bound drugs. Adv. Drug Deliv. Rev., 54: 653-674, 2002.
7. Alakhov, V., Klinski, E., Lemieux, P., Pietrzynski, G., and Kabanov, A. Block copolymeric biotransport carriers as versatile vehicles for drug delivery. Exp. Opin. Biol. Ther., 1: 583-602, 2001.
8. Gariepy, J., and Kawamura, K. Vectorial delivery of macromolecules into cells using peptide-based vehicles. Trends Biotechnol., 19: 21-28, 2001.
9. Newell, M., Milliken, S., Goldstein, D., Lewis, C., Boyle, M., Dolan, G., Ryan, S., and Cooper, D. A. A phase II study of liposomal doxorubicin in the treatment of HIV-related Kaposi's sarcoma. Aust. N. Z. J. Med., 28: 777-783, 1998.
10. Tejada-Berges, T., Granai, C. O., Gordinier, M., and Gajewski, W. Caelyx/Doxil for the treatment of metastatic ovarian and breast cancer. Exp. Rev. Anticancer Ther., 2: 143-150, 2002.
11. Batist, G., Barton, J., Chaikin, P., Swenson, C., and Welles, L. Myocet (liposome-encapsulated doxorubicin citrate): a new approach in breast cancer therapy. Exp. Opin. Pharmacother., 3: 1739-1751, 2002.
12. Sharpe, M., Easthope, S. E., Keating, G. M., and Lamb, H. M. Polyethylene glycol-liposomal doxorubicin: a review of its use in the management of solid and haematological malignancies and AIDS-related Kaposi's sarcoma. Drugs, 62: 2089-2126, 2002.
13. Christou, L., Hatzimichael, E., Chaidos, A., Tsiara, S., and Bourantas, K. L. Treatment of plasma cell leukemia with vincristine, liposomal doxorubicin and dexamethasone. Eur. J. Haematol., 67: 51-53, 2001.
14. Hussein, M. A., Wood, L., Hsi, E., Srkalovic, G., Karam, M., Elson, P., and Bukowski, R. M. A Phase II trial of pegylated liposomal doxorubicin, vincristine, and reduced-dose dexamethasone combination therapy in newly diagnosed multiple myeloma patients. Cancer (Phila.), 95: 2160-2168, 2002.
15. Tsavaris, N., Kosmas, C., Vadiaka, M., Giannouli, S., Siakantaris, M. P., Vassilakopoulos, T., and Pangalis, G. A. Pegylated liposomal doxorubicin in the CHOP regimen for older patients with aggressive (stages III/IV) non-Hodgkin's lymphoma. Anticancer Res., 22: 1845-1848, 2002.
16. Sarris, A. H., Hagemeister, F., Romaguera, J., Rodriguez, M. A., McLaughlin, P., Tsimberidou, A. M., Medeiros, L. J., Samuels, B., Pate, O., Oholendt, M., Kantarjian, H., Burge, C., and Cabanillas, F. Liposomal vincristine in relapsed non-Hodgkin's lymphomas: early results of an ongoing phase II trial. Ann. Oncol., 11: 69-72, 2000.
17. Swenson, C. E., Bolcsak, L. E., Batist, G., Guthrie, T. H., Jr., Tkaczuk, K. H., Boxenbaum, H., Welles, L., Chow, S. C., Bhamra, R., and Chaikin, P. Pharmacokinetics of doxorubicin administered i. v. as Myocet (TLC D-99; liposome-encapsulated doxorubicin citrate) compared with conventional doxorubicin when given in combination with cyclophosphamide in patients with metastatic breast cancer. Anticancer Drugs, 14: 239-246, 2003.
18. Valero, V., Buzdar, A. U., Theriault, R. L., Azamia, N., Fonseca, G. A., Willey, J., Ewer, M., Walters, R. S., Mackay, B., Podoloff, D., Booser, D., Lee, L. W., and Hortobagyi, G. N. Phase II trial of liposome-encapsulated doxorubicin, cyclophosphamide, and fluorouracil as first-line therapy in patients with metastatic breast cancer. J. Clin. Oncol., 17: 1425-1434, 1999.
19. Gianni, L. The future of targeted therapy: combining novel agents. Oncology, 63: 47-56, 2002.
20. Winer, E. P., and Burstein, H. J. New combinations with Herceptin in metastatic breast cancer. Oncology, 61: 50-57, 2001.
21. Saxon, D., Mayer, L., and Bally, M. Liposomal anticancer drugs as agents to be used in combination with other anticancer agents: studies on a liposomal formulation with two encapsulated drugs. J. Liposome Res., 9: 507-522, 1999.
22. Mayer, L. D., Hope, M. J., Cullis, P. R., and Janoff, A. S. Solute distributions and trapping efficiencies observed in freeze-thawed multilamellar vesicles. Biochim. Biophys. Acta, 817: 193-196, 1985.
23. Fenske, D. B., Wong, K. F., Maurer, E., Maurer, N., Leenhouts, J. M., Boman, N., Amankwa, L., and Cullis, P. R. Ionophore-mediated uptake of ciprofloxacin and vincristine into large unilamellar vesicles exhibiting transmembrane ion gradients. Biochim. Biophys. Acta, 1414: 188-204, 1998.
24. Abraham, S. A., Edwards, K., Karlsson, G., MacIntosh, S., Mayer, L. D., McKenzie, C., and Bally, M. Formation of transition metal-doxorubicin complexes inside liposomes. Biochim. Biophys. Acta, 1565: 41-54, 2002.
25. Wang, E., Taylor, R. W., and Pfeiffer, D. R. Mechanism and specificity of lanthanide series cation transport by ionophores A23187, 4-BrA23187 and ionomycin. Biophysical J., 75: 1244-1254, 1998.
26. Pool, G. L., French, M. E., Edwards, R. A., Huang, L., and Lumb, R. H. Use of radiolabeled hexadecyl cholesteryl ether as a liposome marker. Lipids, 17: 448-452, 1982.
27. Chou, T. C., and Talalay, P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul., 22: 27-55, 1984.
28. Cheung, B. C., Sun, T. H., Leenhouts, J. M., and Cullis, P. R. Loading of doxorubicin into liposomes by forming Mn2+-drug complexes. Biochim. Biophys. Acta, 1414: 205-216, 1998.
29. Mayer, L. D., Tai, L. C., Ko, D. S., Masin, D., Ginsberg, R. S., Cullis, P. R., and Bally, M. B. Influence of vesicle size, lipid composition, and drug-to-lipid ratio on the biological activity of liposomal doxorubicin in mice. Cancer Res., 49: 5922-5930, 1989.
30. Mayer, L. D., Nayar, R., Thies, R. L., Boman, N. L., Cullis, P. R., and Bally, M. B. Identification of vesicle properties that enhance the antitumour activity of liposomal vincristine against murine L1210 leukemia. Cancer Chemother. Pharmacol., 33: 17-24, 1993.
31. Boman, N. L., Mayer, L. D., and Cullis, P. R. Optimization of the retention properties of vincristine in liposomal systems. Biochim. Biophys. Acta, 1152: 253-258, 1993.
32. Deleers, M., and Malaisse, W. J. Ionophore-mediated calcium exchange diffusion in liposomes. Biochem. Biophys. Res. Commun., 95: 650-657, 1980.
33. Bouma, J., Beijnen, J. H., Bult, A., and Underberg, W. J. Anthra-cycline antitumour agents. A review of physicochemical, analytical and stability properties. Pharm. Weekbl. Sci., 8: 109-133, 1986.
34. Harrigan, P. R., Hope, M. J., Redelmeier, T. E., and Cullis, P. R. Determination of transmembrane pH gradients and membrane potentials in liposomes. Biophys. J., 63: 1336-1345, 1992.
35. Bally, M. B., Nayar, R., Masin, D., Hope, M. J., Cullis, P. R., and Mayer, L. D. Liposomes with entrapped doxorubicin exhibit extended blood residence times. Biochim. Biophys. Acta, 1023: 133-139, 1990.
36. Mayer, L. D., Tai, L. C., Bally, M. B., Mitilenes, G. N., Ginsberg, R. S., and Cullis, P. R. Characterization of liposomal systems containing doxorubicin entrapped in response to pH gradients. Biochim. Biophys. Acta, 1025: 143-151, 1990.
37. Vaage, J., Donovan, D., Mayhew, E., Uster, P., and Woodle, M. Therapy of mouse mammary carcinomas with vincristine and doxorubicin encapsulated in sterically stabilized liposomes. Int. J. Cancer, 54: 959-964, 1993.
38. Leonessa, F., Green, D., Licht, T., Wright, A., Wingate-Legette, K., Lippman, J., Gottesman, M. M., and Clarke, R. MDA435/LCC6 and MDA435/LCC6MDRI: ascites models of human breast cancer. Br. J. Cancer, 73: 154-161, 1996.
39. Chou, T. C., and Hayball, M. P. CalcuSyn. Windows Sorfware for Dose Effect Analysis, pp. 1-56. Cambridge, UK: Biosoft, 1996.
40. Beraldo, H., Garnier-Suillerot, A., Tosi, L., and Lavelle, F. Iro-n(III)-adriamycin and Iron(III)-daunorubicin complexes: physicochemical characteristics, interaction with DNA, and antitumor activity. Biochemistry, 24: 284-289, 1985.
41. Fiallo, M. M., Garnier-Suillerot, A., Matzanke, B., and Kozlowski, H. How Fe3+ binds anthracycline antitumour compounds. The myth and the reality of a chemical sphinx. J. Inorg. Biochem., 75: 105-115, 1999.
42. Kuwahara, J., Suzuki, T., and Sugiura, Y. Studies on antitumor drugs targeting DNA: photosensitive DNA cleavage of copper-camptothecin. Nucleic Acids Symp. Ser., 201-204, 1985.
43. Kuwahara, J., Suzuki, T., Funakoshi, K., and Sugiura, Y. Photosensitive DNA cleavage and phage inactivation by copper(II)-camptothecin. Biochemistry, 25: 1216-1221, 1986.
44. Dabrowiak, J. C., Greenaway, F. T., and Grulich, R. Transition-metal binding site of bleomycin A2. A carbon-I3 nuclear magnetic resonance study of the zinc(II) and copper(II) derivatives Biochemistry, 17: 4090-4096, 1978.
45. Suzuki, T., Kuwahara, J., and Sugiura, Y. DNA cleavages of bleomycin-transition metal complexes induced by reductant, hydrogen peroxide, and ultraviolet light: characteristics and biological implication. Nucleic Acids Symp. Ser., 161-164, 1984.
46. Lim, H. J., Masin, D., Madden, T. D., and Bally, M. B. Influence of drug release characteristics on the therapeutic activity of liposomal mitoxantrone. J. Pharmacol. Exp. Ther., 281: 566-573, 1997.
47. Madden, T. D., Harrigan, P. R., Tai, L. C., Bally, M. B., Mayer, L. D., Redelmeier, T. E., Loughrey, H. C., Tilcock, C. P., Reinish, L. W., and Cullis, P. R. The accumulation of drugs within large unilamellar vesicles exhibiting a proton gradient: a survey. Chem. Phys. Lipids, 53: 37-46, 1990.
48. Barranco, S. C., Gerner, E. W., Burk, K. H., and Humphrey, R. M. Survival and cell kinetics effects of adriamycin on mammalian cells. Cancer Res., 33: 11-16, 1973.
49. Kim, S. H., and Kim, J. H. Lethal effect of adriamycin on the division cycle of HeLa cells. Cancer Res., 32: 323-325, 1972.
50. Hill, B. T., and Whelan, R. D. Comparative cell killing and kinetic effects of vincristine or vindesine in mammalian cell lines. J. Natl. Cancer Inst., 67: 437-443, 1981.
51. Hill, B. T., and Whelan, R. D. Comparative effects of vincristine and vindesine on cell cycle kinetics in vitro. Cancer Treat Rev., 7(Suppl. 1): 5-15, 1980.
52. Friedland, M. L. Combinational Chemotherapy. In: M. C. Perry (ed.), The Chemotherapy Source Book. Baltimore, Maryland: Williams and Wilkins, 1992.
53. Greco, F. A., and Hainsworth, J. D. Etoposide phosphate or etoposide with cisplatin in the treatment of small cell lung cancer: randomized phase II trial. Lung Cancer, 12(Suppl. 3): S85-S95, 1995.