Influence of dose and animal species on accelerated blood clearance of PEGylated liposomal doxorubicin

International Journal of Pharmaceutics

Volumn 476, Issue 1, 2014, Pages 205-212

  Suzuki, Takuya ^a   Ichihara, Masako ^c   Hyodo, Kenji ^a   Yamamoto, Eiichi ^a   Ishida, Tatsuhiro ^c   Kiwada, Hiroshi ^c   Kikuchi, Hiroshi ^b   Ishihara, Hiroshi ^a  

^a DDS Research Global Formulation Research Japan Pharmaceutical Science and Technology   (Japan)

^b EISAI CO LTD   (Japan)

^c Institute of Health Biosciences   (Japan)

Author keywords

Accelerated blood clearance phenomenon; Doxil; Doxorubicin; PEGylated liposomes; Polyethylene glycol; Species difference

Indexed keywords

DOXORUBICIN; IMMUNOGLOBULIN M; ANTINEOPLASTIC ANTIBIOTIC; MACROGOL DERIVATIVE;

ACCELERATED BLOOD CLEARANCE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG BLOOD LEVEL; HAPLORHINI; MINIPIG; MOUSE; NONHUMAN; PLASMA CLEARANCE; RAT; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; DOSE RESPONSE; IMMUNOLOGY; MACACA FASCICULARIS; MALE; PIG; SPECIES DIFFERENCE; WISTAR RAT;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; IMMUNOGLOBULIN M; MACACA FASCICULARIS; MALE; MICE; MICE, INBRED BALB C; POLYETHYLENE GLYCOLS; RATS; RATS, WISTAR; SPECIES SPECIFICITY; SWINE; SWINE, MINIATURE;

EID: 84907897464     PISSN: 03785173     EISSN: 18733476     Source Type: Journal    
DOI: 10.1016/j.ijpharm.2014.09.047     Document Type: Article

References (39)

1. A.S. Abu Lila, H. Kiwada, and T. Ishida The accelerated blood clearance (ABC) phenomenon: clinical challenge and approaches to manage J. Control. Release 172 2013 38 47
2. T.M. Allen Long-circulating (sterically stabilized) liposomes for targeted drug delivery Trends Pharmacol. Sci. 15 1994 215 220
3. T.M. Allen, C. Hansen, F. Martin, C. Redemann, and A. Yau-Young Liposomes containing synthetic lipid derivatives of poly(ethylene glycol) show prolonged circulation half-lives in vivo Biochim. Biophys. Acta 1066 1991 29 36
4. M. Amantea, M.S. Newman, T.M. Sullivan, A. Forrest, and P.K. Working Relationship of dose intensity to the induction of palmar-plantar erythrodysesthia by pegylated liposomal doxorubicin in dogs Hum. Exp. Toxicol. 18 1999 17 26
5. Y. Barenholz Doxil(R)?the first FDA-approved nano-drug: lessons learned J. Control. Release 160 2012 117 134
6. L. Bracci, G. Schiavoni, A. Sistigu, and F. Belardelli Immune-based mechanisms of cytotoxic chemotherapy: implications for the design of novel and rationale-based combined treatments against cancer Cell Death Differ. 21 2014 15 25
7. A. Cabanes, D. Tzemach, D. Goren, A.T. Horowitz, and A. Gabizon Comparative study of the antitumor activity of free doxorubicin and polyethylene glycol-coated liposomal doxorubicin in a mouse lymphoma model Clin. Cancer Res. 4 1998 499 505
8. E. Claassen, N. Kors, C.D. Dijkstra, and N. Van Rooijen Marginal zone of the spleen and the development and localization of specific antibody-forming cells against thymus-dependent and thymus-independent type-2 antigens Immunology 57 1986 399 403
9. J. Cui, C. Li, C. Wang, Y. Li, L. Zhang, and H. Yang Repeated injection of pegylated liposomal antitumour drugs induces the disappearance of the rapid distribution phase J. Pharm. Pharmacol. 60 2008 1651 1657
10. E.T. Dams, P. Laverman, W.J. Oyen, G. Storm, G.L. Scherphof, J.W. van Der Meer, F.H. Corstens, and O.C. Boerman Accelerated blood clearance and altered biodistribution of repeated injections of sterically stabilized liposomes J. Pharmacol. Exp. Ther. 292 2000 1071 1079
11. A. Gabizon, H. Shmeeda, and Y. Barenholz Pharmacokinetics of pegylated liposomal doxorubicin: review of animal and human studies Clin. Pharmacokinet. 42 2003 419 436
12. A. Gabizon, H. Shmeeda, and T. Grenader Pharmacological basis of pegylated liposomal doxorubicin: impact on cancer therapy Eur. J. Pharm. Sci. 45 2012 388 398
13. A. Gabizon, D. Tzemach, J. Gorin, L. Mak, Y. Amitay, H. Shmeeda, and S. Zalipsky Improved therapeutic activity of folate-targeted liposomal doxorubicin in folate receptor-expressing tumor models Cancer Chemother. Pharmacol. 66 2010 43 52
14. O. Garraud, G. Borhis, G. Badr, S. Degrelle, B. Pozzetto, F. Cognasse, and Y. Richard Revisiting the B-cell compartment in mouse and humans: more than one B-cell subset exists in the marginal zone and beyond BMC immunology 13 2012 63
15. M. Ichihara, T. Shimizu, A. Imoto, Y. Hashiguchi, Y. Uehara, T. Ishida, and H. Kiwada Anti-PEG IgM response against PEGylated liposomes in mice and rats Pharmaceutics 3 2010 1 11
16. T. Ishida, K. Atobe, X. Wang, and H. Kiwada Accelerated blood clearance of PEGylated liposomes upon repeated injections: effect of doxorubicin-encapsulation and high-dose first injection J. Control. Release 115 2006 251 258
17. T. Ishida, M. Harada, X.Y. Wang, M. Ichihara, K. Irimura, and H. Kiwada Accelerated blood clearance of PEGylated liposomes following preceding liposome injection: effects of lipid dose and PEG surface-density and chain length of the first-dose liposomes J. Control. Release 105 2005 305 317
18. T. Ishida, M. Ichihara, X. Wang, K. Yamamoto, J. Kimura, E. Majima, and H. Kiwada Injection of PEGylated liposomes in rats elicits PEG-specific IgM, which is responsible for rapid elimination of a second dose of PEGylated liposomes J. Control. Release 112 2006 15 25
19. T. Ishida, X. Wang, T. Shimizu, K. Nawata, and H. Kiwada PEGylated liposomes elicit an anti-PEG IgM response in a T cell-independent manner J. Control. Release 122 2007 349 355
20. H. Koide, T. Asai, K. Hatanaka, S. Akai, T. Ishii, E. Kenjo, T. Ishida, H. Kiwada, H. Tsukada, and N. Oku T cell-independent B cell response is responsible for ABC phenomenon induced by repeated injection of PEGylated liposomes Int. J. Pharm. 392 2010 218 223
21. N.M. La-Beck, B.A. Zamboni, A. Gabizon, H. Schmeeda, M. Amantea, P.A. Gehrig, and W.C. Zamboni Factors affecting the pharmacokinetics of pegylated liposomal doxorubicin in patients Cancer Chemother. Pharmacol. 69 2012 43 50
22. P. Laverman, M.G. Carstens, O.C. Boerman, E.T. Dams, W.J. Oyen, N. van Rooijen, F.H. Corstens, and G. Storm Factors affecting the accelerated blood clearance of polyethylene glycol-liposomes upon repeated injection J. Pharmacol. Exp. Ther. 298 2001 607 612
23. C. Li, J. Cao, Y. Wang, X. Zhao, C. Deng, N. Wei, J. Yang, and J. Cui Accelerated blood clearance of pegylated liposomal topotecan: influence of polyethylene glycol grafting density and animal species J. Pharm. Sci. 101 2012 3864 3876
24. C. Li, X. Zhao, Y. Wang, H. Yang, H. Li, W. Tian, J. Yang, and J. Cui Prolongation of time interval between doses could eliminate accelerated blood clearance phenomenon induced by pegylated liposomal topotecan Int. J. Pharm. 443 2013 17 25
25. M. Loeffler, J.A. Kruger, and R.A. Reisfeld Immunostimulatory effects of low-dose cyclophosphamide are controlled by inducible nitric oxide synthase Cancer Res. 65 2005 5027 5030
26. I.C. MacLennan, and Y.J. Liu Marginal zone B cells respond both to polysaccharide antigens and protein antigens. Res Immunol. 142 1991 346 351
27. H. Maeda, G.Y. Bharate, and J. Daruwalla Polymeric drugs for efficient tumor-targeted drug delivery based on EPR-effect Eur. J. Pharm. Biopharm 71 2009 409 419
28. F. Martin, and J.F. Kearney Marginal-zone B cells. Nat. rev Immunology 2 2002 323 335
29. A. Nagao, A.S. Abu Lila, T. Ishida, and H. Kiwada Abrogation of the accelerated blood clearance phenomenon by SOXL regimen: promise for clinical application Int. J. Pharm 441 2013 395 401
30. 2 Ann. Oncol. 11 2000 1029 1033
31. M. Sharpe, S.E. Easthope, G.M. Keating, and H.M. Lamb 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 2002 2089 2126
32. T. Shimizu, T. Ishida, and H. Kiwada Transport of PEGylated liposomes from the splenic marginal zone to the follicle in the induction phase of the accelerated blood clearance phenomenon Immunobiology 218 2013 725 732
33. B. Steiniger, E.M. Timphus, and P.J. Barth The splenic marginal zone in humans and rodents: an enigmatic compartment and its inhabitants Histochem. Cell Biol. 126 2006 641 648
34. C. Suenderhauf, and N. Parrott A physiologically based pharmacokinetic model of the minipig: data compilation and model implementation. Pharm Res. 30 2013 1 15
35. T. Suzuki, M. Ichihara, K. Hyodo, E. Yamamoto, T. Ishida, H. Kiwada, H. Ishihara, and H. Kikuchi Accelerated blood clearance of PEGylated liposomes containing doxorubicin upon repeated administration to dogs Int. J. Pharm. 436 2012 636 643
36. D.M. Vail, R. Chun, D.H. Thamm, L.D. Garrett, A.J. Cooley, and J.E. Obradovich Efficacy of pyridoxine to ameliorate the cutaneous toxicity associated with doxorubicin containing pegylated (stealth) liposomes: a randomized double-blind clinical trial using a canine model Clin. Cancer Res. 4 1998 1567 1571
37. ® as an alternative non-rodent species for immunogenicity testing: a demonstrator study using the IL-1 receptor antagonist anakinra J. Immunotoxicol. 10 2013 96 105
38. P.K. Working, M.S. Newman, T. Sullivan, and J. Yarrington Reduction of the cardiotoxicity of doxorubicin in rabbits and dogs by encapsulation in long-circulating, pegylated liposomes J. Pharmacol. Exp. Ther. 289 1999 1128 1133
39. H. Zhong, B. Han, I.L. Tourkova, A. Lokshin, A. Rosenbloom, M.R. Shurin, and G.V. Shurin Low-dose paclitaxel prior to intratumoral dendritic cell vaccine modulates intratumoral cytokine network and lung cancer growth Clin. Cancer Res. 13 2007 5455 5462