Liposome transport of hydrophobic drugs: Gel phase lipid bilayer permeability and partitioning of the lactone form of a hydrophobic camptothecin, DB-67

Journal of Pharmaceutical Sciences

Volumn 97, Issue 1, 2008, Pages 400-420

  Joguparthi, Vijay ^a   Xiang, Tian Xiang ^a   Anderson, Bradley D ^a  

^a University of Kentucky   (United States)

Author keywords

Bilayer; Cancer chemotherapy; Encapsulation; Kinetics; Liposomes; Mathematical model; Membrane transport; Passive diffusion transport; Permeability

Indexed keywords

CAMPTOTHECIN;

ARTICLE; BINDING AFFINITY; CHEMICAL STRUCTURE; DRUG PENETRATION; DRUG RETENTION; DRUG TRANSPORT; HYDROLYSIS; KINETICS; NONHUMAN; PARTITION COEFFICIENT; RAT;

EID: 38349161151     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.21125     Document Type: Article

References (68)

1. Bom D, Curran DP, Kruszewski S, Zimmer SG, Thompson Strode J, Kohlhagen G, Du W, Chavan AJ, Fraley KA, Bingcang AL, Latus LJ, Pommier Y, Burke TG. 2000. The novel silatecan 7-tert-butyldimethylsilyl-10-hydroxycamptothecin displays high lipophilicity, improved human blood stability, and potent anticancer activity. J Med Chem 43: 3970-3980.
2. Pollack IF, Erff M, Bom D, Burke TG, Strode JT, Curran DP. 1999. Potent topoisomerase I inhibition by novel silatecans eliminates glioma proliferation in vitro and in vivo. Cancer Res 59:4898-4905.
3. Investigational new drug application to the FDA. Application # 74959.
4. Hertzberg RP, Caranfa MJ, Hecht SM. 1989. On the mechanism of topoisomerase I inhibition by camptothecin: Evidence for binding to an enzyme-DNA complex. Biochemistry 28:4629-4638.
5. Hertzberg RP, Caranfa MJ, Holden KG, Jakas DR, Gallagher G, Mattern MR, Mong SM, Bartus JO, Johnson RK, Kingsbury WD. 1989. Modification of the hydroxy lactone ring of camptothecin: Inhibition of mammalian topoisomerase I and biological activity. J Med Chem 32:715-720.
6. Fassberg J, Stella VJ. 1992. A kinetic and mechanistic study of the hydrolysis of camptothecin and some analogues. J Pharm Sci 81:676-684.
7. Burke TG, Mi Z. 1993. Preferential binding of the carboxylate form of camptothecin by human serum albumin. Anal Biochem 212:285-287.
8. Burke TG, Mi Z. 1994. The structural basis of camptothecin interactions with human serum albumin: Impact on drug stability. J Med Chem 37:40-46.
9. Burke TG, Munshi CB, Mi Z, Jiang Y. 1995. The important role of albumin in determining the relative human blood stabilities of the camptothecin anticancer drugs. J Pharm Sci 84:518-519.
10. Mi Z, Burke TG. 1994. Marked interspecies variations concerning the interactions of camptothecin with serum albumins: A frequency-domain fluorescence spectroscopic study. Biochemistry 33:12540-12545.
11. Mi Z, Burke TG. 1994. Differential interactions of camptothecin lactone and carboxylate forms with human blood components. Biochemistry 33:10325-10336.
12. Bom D, Curran DP, Chavan AJ, Kruszewski S, Zimmer SG, Fraley KA, Burke TG. 1999. Novel A,B,E-ring-modified camptothecins displaying high lipophilicity and markedly improved human blood stabilities. J Med Chem 42:3018-3022.
13. Keir ST, Hausheer F, Lawless AA, Bigner DD, Friedman HS. 2001. Therapeutic activity of 7-[(2-trimethylsilyl)ethyl)]-20 (S)-camptothecin against central nervous system tumor-derived xenografts in athymic mice. Cancer Chemother Pharmacol 48:83-87.
14. Pratesi G, Beretta GL, Zunino F. 2004. Gimatecan, a novel camptothecin with a promising preclinical profile. Anticancer Drugs 15:545-552.
15. Burke TG, Mishra AK, Wani MC, Wall ME. 1993. Lipid bilayer partitioning and stability of camptothecin drugs. Biochemistry 32:5352-5364.
16. Xiang TX, Anderson BD. 2002. Stable supersaturated aqueous solutions of silatecan 7-t-butyldimethylsilyl-10-hydroxycamptothecin via chemical conversion in the presence of a chemically modified beta-cyclodextrin. Pharm Res 19: 1215-1222.
17. Xiang TX, Jiang ZQ, Song L, Anderson BD. 2006. Molecular dynamics simulations and experimental studies of binding and mobility of 7-tert-butyldimethylsilyl-10-hydroxycamptothecin and its 20(S)-4-aminobutyrate ester in DMPC membranes. Mol Pharm 3:589-600.
18. Drummond DC, Meyer O, Hong K, Kirpotin DB, Papahadjopoulos D. 1999. Optimizing liposomes for delivery of chemotherapeutic agents to solid tumors. Pharmacol Rev 51:691-743.
19. Colbern GT, Dykes DJ, Engbers C, Musterer R, Hiller A, Pegg E, Saville R, Weng S, Luzzio M, Uster P, Amantea M, Working PK. 1998. Encapsulation of the topoisomerase I inhibitor GL147211C in pegylated (STEALTH) liposomes: Pharmacokinetics and antitumor activity in HT29 colon tumor xenografts. Clin Cancer Res 4:3077-3082.
20. Emerson DL, Bendele R, Brown E, Chiang S, Desjardins JP, Dihel LC, Gill SC, Hamilton M, LeRay JD, Moon-McDermott L, Moynihan K, Richardson FC, Tomkinson B, Luzzio MJ, Baccanari D. 2000. Antitumor efficacy, pharmacokinetics, and biodistribution of NX 211: A low-clearance liposomal formulation of lurtotecan. Clin Cancer Res 6:2903-2912.
21. Messerer CL, Ramsay EC, Waterhouse D, Ng R, Simms EM, Harasym N, Tardi P, Mayer LD, Bally MB. 2004. Liposomal irinotecan: Formulation development and therapeutic assessment in murine xenograft models of colorectal cancer. Clin Cancer Res 10:6638-6649.
22. Pal A, Khan S, Wang YF, Kamath N, Sarkar AK, Ahmad A, Sheikh S, Ali S, Carbonaro D, Zhang A, Ahmad I. 2005. Preclinical safety, pharmacokinetics and antitumor efficacy profile of liposome-entrapped SN-38 formulation. Anticancer Res 25: 331-341.
23. Tardi P, Choice E, Masin D, Redelmeier T, Bally M, Madden TD. 2000. Liposomal encapsulation of topotecan enhances anticancer efficacy in murine and human xenograft models. Cancer Res 60:3389-3393.
24. Burke TG, Gao X. 1994. Stabilization of topotecan in low pH liposomes composed of distearoylphosphatidylcholine. J Pharm Sci 83:967-969.
25. Peikov V, Ugwu S, Parmar M, Zhang A, Ahmad I, 2005. pH-dependent association of SN-38 with lipid bilayers of a novel liposomal formulation. Int J Pharm 299:92-99.
26. Abraham SA, Edwards K, Karlsson G, Hudon N, Mayer LD, Bally MB. 2004. An evaluation of transmembrane ion gradient-mediated encapsulation of topotecan within liposomes. J Control Release 96: 449-461.
27. Abraham SA, Edwards K, Karlsson G, MacIntosh S, Mayer LD, McKenzie C, Bally MB. 2002. Formation of transition metal-doxorubicin complexes inside liposomes. Biochim Biophys Acta 1565:41-54.
28. Drummond DC, Noble CO, Guo Z, Hong K, Park JW, Kirpotin DB. 2006. Development of a highly active nanoliposomal irinotecan using a novel intraliposomal stabilization strategy. Cancer Res 66: 3271-3277.
29. Zhigaltsev IV, Maurer N, Edwards K, Karlsson G, Cullis PR. 2006. Formation of drug-arylsulfonate complexes inside liposomes: A novel approach to improve drug retention. J Control Release 110:378-386.
30. Mayer PT, Xiang TX, Anderson BD. 2000. Independence of substituent contributions to the transport of small molecule permeants in lipid bilayers. AAPS Pharm Sci 2:E14.
31. Xiang T, Xu Y, Anderson BD. 1998. The barrier domain for solute permeation varies with lipid bilayer phase structure. J Membr Biol 165:77-90.
32. Xiang TX, Anderson BD. 1994. Substituent contributions to the transport of substituted p-toluic acids across lipid bilayer membranes. J Pharm Sci 83: 1511-1518.
33. Xiang TX, Anderson BD. 1994. The relationship between permeant size and permeability in lipid bilayer membranes. J Membr Biol 140:111-122.
34. Yan X, Scherphof GL, Kamps JA. 2005. Liposome opsonization. J Liposome Res 15:109-139.
35. Høeg-Møller C. 2003. Preformulation studies of the gamma-aminobutyric acid ester prodrug of DB-67 MS Thesis The Danish University of Pharmaceutical Sciences. Copenhagen, Denmark.
36. Xiang TX, Anderson BD. 1997. Permeability of acetic acid across gel and liquid-crystalline lipid bilayers conforms to free-surface-area theory. Biophys J 72:223-237.
37. Huang C, Mason JT. 1978. Geometric packing constraints in egg phosphatidylcholine vesicles. Proc Natl Acad Sci USA 75:308-310.
38. Mayer LD, Reamer J, Bally MB. 1999. Intravenous pretreatment with empty pH gradient liposomes alters the pharmacokinetics and toxicity of doxorubicin through in vivo active drug encapsulation. J Pharm Sci 88:96-102.
39. Scott DO, Bindra DS, Stella VJ. 1993. Plasma pharmacokinetics of lactone and carboxylate forms of 20(S)-camptothecin in anesthetized rats. Pharm Res 10:1451-1457.
40. Gabizon A, Catane R, Uziely B, Kaufman B, Safra T, Cohen R, Martin F, Huang A, Barenholz Y. 1994. Prolonged circulation time and enhanced accumulation in malignant exudates of doxorubicin encapsulated in polyethylene-glycol coated liposomes. Cancer Res 54:987-992.
41. Gabizon AA. 2001. Stealth liposomes and tumor targeting: One step further in the quest for the magic bullet. Clin Cancer Res 7:223-225.
42. Gabizon AA. 2002. Liposomal drug carrier systems in cancer chemotherapy: Current status and future prospects. J Drug Target 10:535-538.
43. Bally MB, Nayar R, Masin D, Hope MJ, Cullis PR, Mayer LD. 1990. Liposomes with entrapped doxorubicin exhibit extended blood residence times. Biochim Biophys Acta 1023:133-139.
44. Cheung BC, Sun TH, Leenhouts JM, Cullis PR. 1998. Loading of doxorubicin into liposomes by forming Mn2+-drug complexes. Biochim Biophys Acta 1414:205-216.
45. Cullis PR, Hope MJ, Bally MB, Madden TD, Mayer LD, Fenske DB. 1997. Influence of pH gradients on the transbilayer transport of drugs, lipids, peptides and metal ions into large unilamellar vesicles. Biochim Biophys Acta 1331:187-211.
46. Lasic DD, Ceh B, Stuart MC, Guo L, Frederik PM, Barenholz Y. 1995. Transmembrane gradient driven phase transitions within vesicles: Lessons for drug delivery. Biochim Biophys Acta 1239:145-156.
47. Maurer N, Wong KF, Hope MJ, Cullis PR. 1998. Anomalous solubility behavior of the antibiotic ciprofloxacin encapsulated in liposomes: A 1H-NMR study. Biochim Biophys Acta 1374:9-20.
48. Fatouros DG, Hatzidimitriou K, Antimisiaris SG. 2001. Liposomes encapsulating prednisolone and prednisolone-cyclodextrin complexes: Comparison of membrane integrity and drug release. Eur J Pharm Sci 13:287-296.
49. McCormack B, Gregoriadis G. 1994. Entrapment of cyclodextrin-drug complexes into liposomes: Potential advantages in drug delivery. J Drug Target 2: 449-454.
50. McCormack B, Gregoriadis G. 1996. Comparative studies of the fate of free and liposome-entrapped hydroxypropyl-beta-cyclodextrin/drug complexes after intravenous injection into rats: Implications in drug delivery. Biochim Biophys Acta 1291:237-244.
51. Clerc S, Barenholz Y. 1995. Loading of amphipathic weak acids into liposomes in response to transmembrane calcium acetate gradients. Biochim Biophys Acta 1240:257-265.
52. Hatzi P, Mourtas S, Klepetsanis PG, Antimisiaris SG. 2007. Integrity of liposomes in presence of cyclodextrins: Effect of liposome type and lipid composition. Int J Pharm 333:167-176.
53. Nishijo J, Shiota S, Mazima K, Inoue Y, Mizuno H, Yoshida J. 2000. Interactions of cyclodextrins with dipalmitoyl, distearoyl, and dimyristoyl phosphatidyl choline liposomes. A study by leakage of carboxyfluorescein in inner aqueous phase of unilamellar liposomes. Chem Pharm Bull (Tokyo) 48:48-52.
54. Mayer PT, Anderson BD. 2002. Transport across 1,9-decadiene precisely mimics the chemical selectivity of the barrier domain in egg lecithin bilayers. J Pharm Sci 91:640-646.
55. Diamond JM, Katz Y. 1974. Interpretation of nonelectrolyte partition coefficients between dimyristoyl lecithin and water. J Membr Biol 17:121-154.
56. Xiang TX, Anderson BD. 1998. Influence of chain ordering on the selectivity of dipalmitoylphosphatidylcholine bilayer membranes for permeant size and shape. Biophys J 75:2658-2671.
57. Xiang TX, Anderson BD. 1998. Phase structures of binary lipid bilayers as revealed by permeability of small molecules. Biochim Biophys Acta 1370: 64-76.
58. Hayduk W, Loakimidis S. 1976. Liquid diffusivities in normal paraffin solutions. J Chem Eng Data 21: 255-260.
59. Edward J. 1970. Molecular volumes and the Stokes-Einstein equation. J Chem Educ 47:261-270.
60. Zhang JA, Xuan T, Parmar M, Ma L, Ugwu S, Ali S, Ahmad I. 2004. Development and characterization of a novel liposome-based formulation of SN-38. Int J Pharm 270:93-107.
61. Peschka R, Dennehy C, Szoka FC Jr. 1998. A simple in vitro model to study the release kinetics of liposome encapsulated material. J Control Release 56:41-51.
62. Ugwu S, Zhang A, Parmar M, Miller B, Sardone T, Peikov V, Ahmad I. 2005. Preparation, characterization, and stability of liposome-based formulations of mitoxantrone. Drug Dev Ind Pharm 31: 223-229.
63. Ahmad A, Wang YF, Ahmad I, 2005. Separation of liposome-entrapped mitoxantrone from nonliposomal mitoxantrone in plasma: Pharmacokinetics in mice. Methods Enzymol 391:176-185.
64. Bellott R, Pouna P, Robert J. 2001. Separation and determination of liposomal and non-liposomal daunorubicin from the plasma of patients treated with Daunoxome. J Chromatogr B Biomed Sci Appl 757:257-267.
65. Druckmann S, Gabizon A, Barenholz Y. 1989. Separation of liposome-associated doxorubicin from non-liposome-associated doxorubicin in human plasma: Implications for pharmacokinetic studies. Biochim Biophys Acta 980:381-384.
66. Mayer LD, St-Onge G. 1995. Determination of free and liposome-associated doxorubicin and vincristine levels in plasma under equilibrium conditions employing ultrafiltration techniques. Anal Biochem 232:149-157.
67. Thies RL, Cowens DW, Cullis PR, Bally MB, Mayer LD. 1990. Method for rapid separation of liposome-associated doxorubicin from free doxorubicin in plasma. Anal Biochem 188:65-71.
68. Tejwani R, Anderson BD. 2007. Influence of intravesicular pH drift and membrane binding on the liposomal release of a model amine-containing permeant. J Pharm Sci (this issue).