Alkylated derivatives of poly(ethylacrylic acid) can be inserted into preformed liposomes and trigger pH-dependent intracellular delivery of liposomal contents

Molecular Membrane Biology

Volumn 21, Issue 6, 2004, Pages 385-393

  Chen, Tao ^a,d   McIntosh, Deirdre ^a,e   He, Yuehua ^b   Kim, Jyngsoo ^c   Tirrell, David A ^c   Schenrer, Peter ^a   Fenske, David B ^a   Sandhu, Ammen P ^a   Cullis, Pieter R ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Inex Pharmaceuticals Corporation   (Canada)

^c California Institute of Technology   (United States)

^d Lipont Liposomes Research Institute   (China)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Intracellular delivery; Liposomes; PH dependent membrane fusion; PH sensitive polymers; Poly(ethylacrylic acid)

Indexed keywords

ACRYLIC ACID DERIVATIVE; ALIPHATIC AMINE; BAFILOMYCIN; CALCEIN; CARBOXYL GROUP; CHLOROQUINE; LIPOSOME; POLY(ETHYL ACRYLIC ACID); POLYMER; UNCLASSIFIED DRUG;

ALKYLATION; ARTICLE; CELL STRAIN COS7; CELL VACUOLE; CELLULAR DISTRIBUTION; CYTOPLASM; ENDOSOME; FLUORESCENCE; PH; PRIORITY JOURNAL;

ACRYLATES; ALKYLATION; ANIMALS; CERCOPITHECUS AETHIOPS; CHROMATOGRAPHY; COS CELLS; DRUG DELIVERY SYSTEMS; ENDOCYTOSIS; FLUORESCEINS; HYDROGEN-ION CONCENTRATION; KINETICS; LIPIDS; LIPOSOMES; MOLECULAR STRUCTURE;

EID: 11144327500     PISSN: 09687688     EISSN: None     Source Type: Journal    
DOI: 10.1080/09687860400010516     Document Type: Article

References (73)

1. Hong, M. S., Lim, S. J., Lee, M. K., Kim, Y. B. and Kim, C. K., 2001, Prolonged blood circulation of methotrexate by modulation of liposomal composition. Drug Deliv., 8, 231-237.
2. Arndt, D., Zeisig, R., Bechtel, D. and Fichtner, I., 2001, Liposomal bleomycin: increased therapeutic activity and decreased pulmonary toxicity in mice. Drug Deliv., 8, 1-7.
3. Cervetti, G., Caracciolo, F., Cecconi, N., Azzara, A. and Petrini, M., 2003, Efficacy and toxicity of liposomal daunorubicin included in PVABEC regimen for aggressive NHL of the elderly. Leuk Lymphoma, 44, 465-469.
4. Gabizon, A., Tzemach, D., Mak, L., Bronstein, M. and Horowitz, A. T., 2002, Dose dependency of pharmacokinetics and therapeutic efficacy of pegylated liposomal doxorubicin (DOXIL) in murine models. J Drug Target, 10, 539-548.
5. Wollina, U., Hohaus, K., Schonlebe, J., Haroske, E. and Kostler, E., 2003, Liposomal daunorubicin in tumor stage cutaneous T-cell lymphoma: report of three cases. J. Cancer Res. Clin. Oncol., 129, 65-69.
6. Abra, R. M., Bankert, R. B., Chen, F., Egilmez, N. K., Huang, K., Seville, R., Slater, J. L., Sugano, M. and Yokota, S. J., 2002, The next generation of liposome delivery systems: recent experience with tumor-targeted, sterically-stabilized immunoliposomes and active-loading gradients. J. Liposome Res., 12, 1-3.
7. Sapra, P. and Allen, T. M., 2002, Internalizing antibodies are necessary for improved therapeutic efficacy of antibody-targeted liposomal drugs. Cancer Res., 62, 7190-7194.
8. Guthlein, F., Burger, A. M., Brandi, M., Fiebig, H. H., Schubert, R., Unger, C. and Massing, U., 2002, Pharmacokinetics and antitumor activity of vincristine entrapped in vesicular phospholipid gels. Anticancer Drugs, 13, 797-805.
9. Kanaoka, E., Takahashi, K., Yoshikawa, T., Jizomoto, H., Nishihara, Y., Uchida, N., Maekawa, R. and Hirano, K., 2002, A significant enhancement of therapeutic effect against hepatic metastases of M5076 in mice by a liposomal interleukin-2 (mixture). J. Control Release, 82, 183-187.
10. Johnson, P. C., Wheat, L. J., Cloud, G. A., Goldman, M., Lancaster, D., Bamberger, D. M., Powderly, W. G., Hafner, R., Kauffman, C. A. and Dismukes, W. E., 2002, Safety and efficacy of liposomal amphotericin B compared with conventional amphotericin B for induction therapy of histoplasmosis in patients with AIDS. Ann. Intern. Med., 137, 105-109.
11. 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., 2002, Anti-HER2 immunoliposomes: enhanced efficacy attributable to targeted delivery. Clin. Cancer Res., 8, 1172-1181.
12. Gokhale, P. C., Pei, J., Zhang, C., Ahmad, I., Rahman, A. and Kasid, U., 2001, Improved safety pharmacokinetics and therapeutic efficacy profiles of a novel liposomal formulation of mitoxantrone. Anticancer Res., 21, 3313-3321.
13. Passas, A., Buffels, R., Anagnostopoulos, A., Gacos, E., Vadikolia, C., Haloudis, P. and Kaloyannidis, P., 2002, Safety and early efficacy assessment of liposomal daunorubicin (DaunoXome) in adults with refractory or relapsed acute myeloblastic leukaemia: a phase I-II study. Br. J. Haematol., 116, 308-315.
14. Chonn, A. and Cullis, P. R., 1995, Recent advances in liposomal drug-delivery systems. Curr. Opin. Biotechnol., 6, 698-708.
15. Jain, R. K., 1999, Transport of molecules, particles and cells in solid tumors. Annu. Rev. Biomed. Eng., 1, 241-263.
16. Jain, R. K. and Carmeliet, P., 2002, Tumor angiogenesis and accessibility: role of vascular endothelial growth factor. Semin. Oncol., 29, 3-9.
17. Carmeliet, P. and Jain, R. K., 2000, Angiogenesis in cancer and other diseases. Nature, 407, 249-257.
18. Woodle, M. C. and Lasic, D. D., 1992, Sterically stabilized liposomes. Biochim. Biophys. Acta, 1113, 171-199.
19. Park, J. W., Hong, K., Carter, P., Asgari, H., Guo, L. Y., Keller, G. A., Wirth, C., Shalaby, R., Kotts, C., Wood, W. I., et al., 1995, Development of anti-p185HER2 immunoliposomes for cancer therapy. Proc. Natl. Acad. Sci. USA, 92, 1327-1331.
20. Jones, M. N., 1994, Carbohydrate-mediated liposomal targeting and drug delivery. Adv. Drug Del. Rev., 13, 215-249.
21. Lee, R. J. and Low, P. S., 1994, Delivery of liposomes into cultured KB cells via folate receptor-mediated endocytosis. J. Biol. Chem., 269, 3198-3204.
22. Lee, R. J. and Low, P. S., 1995, Folate-mediated tumor cell targeting of liposome-entrapped doxorubicin in vitro. Biochim. Biophys. Acta, 1233, 134-144.
23. Viani, P., Cervato, G., Gatti, P. and Cestaro, B., 1993, Plasma dependent pH sensitivity of liposomes containing sulfatide. Biochim. Biophys. Acta, 1147, 73-80.
24. Straubinger, R. M., Duzgunes, N. and Papahadjopoulos, D., 1985, pH-sensitive liposomes mediate cytoplasmic delivery of encapsulated macromolecules. FEBS Lett., 179, 148-154.
25. Yatvin, M. B., Kreutz, W., Horwitz, B. A. and Shinitzky, M., 1980, pH-sensitive liposomes: possible clinical implications. Science, 210, 1253-1255.
26. Kono, K., Nishii, H. and Takagishi, T., 1993, Fusion activity of an amphiphilic polypeptide having acidic amino acid residues: generation of fusion activity by alpha-helix formation and charge neutralization. Biochim. Biophys. Acta, 1164, 81-90.
27. Kono, K., Zenitani, K. and Takagishi, T., 1994, Novel pH-sensitive liposomes: liposomes bearing a poly(ethylene glycol) derivative with carboxyl groups. Biochim. Biophys. Acta, 1193, 1-9.
28. Kono, K., Igawa, T. and Takagishi, T., 1997, Cytoplasmic delivery of calcein mediated by liposomes modified with a pH-sensitive poly(ethylene glycol) derivative. Biochim. Biophys. Acta, 1325, 143-154.
29. Chen, T., He, Y., Cullis, P., Madden, T., Scherrer, P., Kim, J. S., Tirrell, D. and Joshi, P., 1999, Polyanionic polymers which enhance fusogenicity.
30. Maeda, M., Kumano, A. and Tirrell, D. A., 1988, H+-induced release of contents of phosphatidylcholine vesicles bearing surface-bound polyelectrolyte chains. J. Amer. Chem. Soc., 110, 7455-7459.
31. Meyer, O., Papahadjopoulos, D. and Leroux, J. C., 1998, Copolymers of N-isopropylacrylamide can trigger pH sensitivity to stable liposomes. FEBS Lett., 421, 61-64.
32. Murata, M., Takahashi, S., Kagiwada, S., Suzuki, A. and Ohnishi, S., 1992, pH-dependent membrane fusion and vesiculation of phospholipid large unilamellar vesicles induced by amphiphilic anionic and cationic peptides. Biochemistry, 31, 1986-1992.
33. Parente, R. A., Nir, S. and Szoka, F. C., Jr., 1988, pH-dependent fusion of phosphatidylcholine small vesicles. Induction by a synthetic amphipathic peptide. J. Biol. Chem., 263, 4724-4730.
34. Bailey, A. L., Monck, M. A. and Cullis, P. R., 1997, pH-induced destabilization of lipid bilayers by a lipopeptide derived from influenza hemagglutinin. Biochim. Biophys. Acta, 1324, 232-244.
35. Leventis, R., Diacovo, T. and Silvius, J. R., 1987, pH-dependent stability and fusion of liposomes combining protonatable double-chain amphiphiles with phosphatidylethanolamine. Biochemistry, 26, 3267-3276.
36. Liu, D. and Huang, L., 1990, pH-sensitive, plasma-stable liposomes with relatively prolonged residence in circulation. Biochim. Biophys. Acta, 1022, 348-54.
37. Nayar, R. and Schroit, A. J., 1985, Generation of pH-sensitive liposomes: use of large unilamellar vesicles containing N- succinyldioleoylphosphatidylethanolamine. Biochemistry, 24, 5967-5971.
38. Ellens, H., Bentz, J. and Szoka, F. C., 1984, pH-induced destabilization of phosphatidylethanolamine-containing liposomes: role of bilayer contact. Biochemistry, 23, 1532-1538.
39. Connor, J., Yatvin, M. B. and Huang, L., 1984, pH-sensitive liposomes: acid-induced liposome fusion. Proc. Natl. Acad. Sci. USA, 81, 1715-1718.
40. Fenske, D. B., Palmer, L. R., Chen, T., Wong, K. F. and Cullis, P. R., 2001, Cationic poly(ethyleneglycol) lipids incorporated into pre-formed vesicles enhance binding and uptake to BHK cells. Biochim. Biophys. Acta, 1512, 259-272.
41. Mellman, I., Fuchs, R. and Helenius, A., 1986, Acidification of the endocytic and exocytic pathways. Annu. Rev. Biochem., 55, 663-700.
42. Ishida, T., Iden, D. L. and Allen, T. M., 1999, A combinatorial approach to producing sterically stabilized (Stealth) immunoliposomal drugs. FEBS Lett., 460, 129-133.
43. Thomas, J. L. and Tirrell, D. A., 1992, Polyelectrolyte-sensitized phospholipid vesicles. Acc. Chem. Res., 25, 336-342.
44. Collins, D., Connor, J., Ting-Beall, H. P. and Huang, L., 1990, Proton and divalent cations induce synergistic but mechanistically different destabilizations of pH-sensitive liposomes composed of dioleoyl phosphatidylethanolamine and oleic acid. Chem. Phys. Lipids, 55, 339-349.
45. Duzgunes, N., Straubinger, R. M., Baldwin, P. A., Friend, D. S. and Papahadjopoulos, D., 1985, Proton-induced fusion of oleic acid- phosphatidylethanolamine liposomes. Biochemistry, 24, 3091-3098.
46. Slepushkin, V. A., Simoes, S., Dazin, P., Newman, M. S., Guo, L. S., Pedroso de Lima, M. C. and Duzgunes, N., 1997, Sterically stabilized pH-sensitive liposomes. Intracellular delivery of aqueous contents and prolonged circulation in vivo. J. Biol. Chem., 272, 2382-2388.
47. Guo, X. and Szoka, F. C., Jr., 2001, Steric stabilization of fusogenic liposomes by a low-pH sensitive PEG-diortho ester-lipid conjugate. Bioconjug. Chem., 12, 291-300.
48. Mandersloot, J. G., Reman, F. C., Van Deenen, L. L. and De Gier, J., 1975, Barrier properties of lecithin/lysolecithin mixtures. Biochim. Biophys. Acta, 382, 22-26.
49. Liang, E. and Hughes, J., 1998, Characterization of a pH-sensitive surfactant, dodecyl-2-(1′-imidazolyl) propionate (DIP), and preliminary studies in liposome mediated gene transfer. Biochim. Biophys. Acta, 1369, 39-50.
50. Chen, F. J., Asokan, A. and Cho, M. J., 2003, Cytosolic delivery of macromolecules: I. Synthesis and characterization of pH-sensitive acyloxyalkylimidazoles. Biochim. Biophys. Acta, 1611, 140-150.
51. Gerasimov, O. V., Schwan, A. and Thompson, D. H., 1997, Acid-catalyzed plasmenylcholine hydrolysis and its effect on bilayer permeability: a quantitative study. Biochim. Biophys. Acta, 1324, 200-214.
52. Plank, C., Oberhauser, B., Mechtler, K., Koch, C. and Wagner, E., 1994, The influence of endosome-disruptive peptides on. gene transfer using synthetic virus-like gene transfer systems. J. Biol. Chem., 269, 12918-12924.
53. Wagner, E., Plank, C., Zatloukal, K., Cotten, M. and Birnstiel, M. L., 1992, Influenza virus hemagglutinin HA-2 N-terminal fusogenic peptides augment gene transfer by transferrin-polylysine-DNA complexes: toward a synthetic virus-like gene-transfer vehicle. Proc. Natl. Acad. Sci. USA, 89, 7934-7938.
54. Subbarao, N. K., Parente, R. A., Szoka, F. C., Jr., Nadasdi, L. and Pongracz, K., 1987, pH-dependent bilayer destabilization by an amphipathic peptide. Biochemistry, 26, 2964-2972.
55. Simoes, S., Slepushkin, V., Gaspar, R., de Lima, M. C. and Duzgunes, N., 1998, Gene delivery by negatively charged ternary complexes of DNA, cationic liposomes and transferrin or fusigenic peptides. Gene Ther., 5, 955-964.
56. Simoes, S., Slepushkin, V., Pires, P., Gaspar, R., de Lima, M. P. and Duzgunes, N., 1999, Mechanisms of gene transfer mediated by lipoplexes associated with targeting ligands or pH-sensitive peptides. Gene Ther., 6, 1798-1807.
57. Haensler, J. and Szoka, F. C., Jr., 1993, Polyamidoamine cascade polymers mediate efficient transfection of cells in culture. Bioconjug. Chem., 4, 372-379.
58. Hahn, K. H. and Kim, H., 1991, Fusion and fragmentation of phospholipid vesicles by apohemoglobin at low pH. J. Biochem. (Tokyo), 110, 635-640.
59. Zhang, F., Andreassen, P., Fender, P., Geissler, E., Hernandez, J. F. and Chroboczek, J., 1999, A transfecting peptide derived from adenovirus fiber protein. Gene Ther., 6, 171-181.
60. da Costa, M. H. and Chaimovich, H., 1997, Structure-activity relationships in the fusion of small unilamellar phosphatidylcholine vesicles induced by a model peptide. Biochimie, 79, 509-516.
61. Horvath, A., Toth, G. K., Gogolak, P., Nagy, Z., Kurucz, I., Pecht, I. and Rajnavolgyi, E., 1998, A hemagglutinin-based multipeptide construct elicits enhanced protective immune response in mice against influenza A virus infection. Immunol. Lett., 60, 127-136.
62. Kalyan, N. K., Lee, S. G., Wilhelm, J., Pisano, M. R., Hum, W. T., Hsiao, C. L., Davis, A. R., Eichberg, J. W., Robert-Guroff, M. and Hung, P. P., 1994. Immunogenicity of recombinant influenza virus haemagglutinin carrying peptides from the envelope protein of human immunodeficiency virus type 1. Vaccine, 12, 753-760.
63. Shinnick, T. M., Sutcliffe, J. G., Green, N. and Lerner, R. A., 1983, Synthetic peptide immunogens as vaccines. Annu. Rev. Microbiol., 37, 425-446.
64. Zignani, M., Drummond, D. C., Meyer, O., Hong, K. and Leroux, J. C., 2000, In vitro characterization of a novel polymeric-based pH-sensitive liposome system. Biochim. Biophys. Acta, 1463, 383-394.
65. Roux, E., Francis, M., Winnik, F. M. and Leroux, J. C., 2002, Polymer based pH-sensitive carriers as a means to improve the cytoplasmic delivery of drugs. Int. J. Pharm., 242, 25-36.
66. Chung, J. C., Gross D. J., Thomas, J. L., Tirrell, D. A., Opsahlong, L. R., 1996, pH-sensitive, cation-selective channels formed by a simple synthetic polyelectrolyte in artificial bilayer membranes. Macromolecules, 29, 4636-4641.
67. Cheung, C. Y., Murthy, N., Stayton, P. S. and Hoffman, A. S., 2001, A pH-sensitive polymer that enhances cationic lipid-mediated gene transfer. Bioconjug. Chem., 12, 906-910.
68. Murthy, N., Robichaud, J. R., Tirrell, D. A., Stayton, P. S. and Huffman, A. S., 1999, The design and synthesis of polymers for eukaryotic membrane disruption. J. Control Release, 61, 137-143.
69. Chonn, A., Semple, S. C. and Cullis, P. R., 1992, Association of blood proteins with large unilamellar liposomes in vivo. Relation to circulation lifetimes. J. Biol. Chem., 267, 18759-18765.
70. Laurema, A., Heikkila, A., Keski-Nisula, L., Heikura, T., Lehtolainen, P., Manninen, H., Tuomisto, T. T., Heinonen, S. and Yla-Herttuala, S., 2003, Transfection of oocytes and other types of ovarian cells in rabbits after direct injection into uterine arteries of adenoviruses and plasmid/liposomes. Gene Ther., 10, 580-584.
71. Nomura, T., Yasuda, K., Yamada, T., Okamoto, S., Mahato, R. I., Watanabe, Y., Takakura, Y. and Hashida, M., 1999, Gene expression and antitumor effects following direct interferon (IFN)-gamma gene transfer with naked plasmid DNA and DC-chol liposome complexes in mice. Gene Ther., 6, 121-129.
72. Hope, M. J., Bally, M. B., Webb, G. and Cullis, P. R., 1985, Production of large unilamellar vesicles by a rapid extrusion procedure. Characterization of size distribution, trapped volume and ability to maintain a membrane potential. Biochim. Biophys. Acta, 812, 55-65.
73. Struck, D. K., Hoekstra, D. and Pagano, R. E., 1981, Use of resonance energy transfer to monitor membrane fusion. Biochemistry, 20, 4093-4099.