Relationship between the concentration of anti-polyethylene glycol (PEG) immunoglobulin M (IgM) and the intensity of the accelerated blood clearance (ABC) phenomenon against PEGylated liposomes in mice

Biological and Pharmaceutical Bulletin

Volumn 38, Issue 3, 2015, Pages 417-424

  Hashimoto, Yosuke ^a   Shimizu, Taro ^a   Lila, Amr Selim Abu ^a,b   Ishida, Tatsuhiro ^a   Kiwada, Hiroshi ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b Zagazig University   (Egypt)

Author keywords

Accelerated blood clearance (ABC) phenomenon; Anti polyethylene glycol (PEG); Complement activation; Immunoglobulin M (IgM); PEGylated liposome (SL)

Indexed keywords

IMMUNOGLOBULIN M; LIPOSOME; MACROGOL; COMPLEMENT; DOXORUBICIN; DRUG CARRIER; MACROGOL DERIVATIVE; NANOPARTICLE;

ACCELERATED BLOOD CLEARANCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG DISTRIBUTION; DRUG UPTAKE; MALE; MOUSE; NONHUMAN; PLASMA CLEARANCE; ANALOGS AND DERIVATIVES; ANIMAL; BAGG ALBINO MOUSE; BLOOD; IMMUNOLOGY; INTRAVENOUS DRUG ADMINISTRATION; LIVER; METABOLISM;

ANIMALS; COMPLEMENT SYSTEM PROTEINS; DOXORUBICIN; DRUG CARRIERS; IMMUNOGLOBULIN M; INJECTIONS, INTRAVENOUS; LIPOSOMES; LIVER; MALE; MICE, INBRED BALB C; NANOPARTICLES; POLYETHYLENE GLYCOLS;

EID: 84937217183     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.b14-00653     Document Type: Article

References (39)

1. Jokerst JV, Lobovkina T, Zare RN, Gambhir SS. Nanoparticle PEGylation for imaging and therapy. Nanomedicine, 6, 715-728 (2011).
2. Park K. Mechanistic study on the ABC phenomenon of PEG conjugates. J. Control. Release, 165, 234 (2013).
3. Allen TM, Hansen C. Pharmacokinetics of stealth versus conventional liposomes: effect of dose. Biochim. Biophys. Acta, 1068, 133-141 (1991).
4. Klibanov AL, Maruyama K, Torchilin VP, Huang L. Amphipathic polyethylene glycols effectively prolong the circulation time of liposomes. FEBS Lett., 268, 235-237 (1990).
5. Lasic DD, Martin FJ, Gabizon A, Huang SK, Papahadjopoulos D. Sterically stabilized liposomes: a hypothesis on the molecular origin of the extended circulation times. Biochim. Biophys. Acta, 1070, 187-192 (1991).
6. Allen C, Dos Santos N, Gallagher R, Chiu GNC, Shu Y, Li WM, Johnstone SA, Janoff AS, Mayer LD, Webb MS, Bally MB. Controlling the physical behavior and biological performance of liposome formulations through use of surface grafted poly(ethylene glycol). Biosci. Rep., 22, 225-250 (2002).
7. Torchilin VP, Omelyanenko VG, Papisov MI, Bogdanov AA Jr, Trubetskoy VS, Herron JH, Gentry CA. Polyethylene glycol) on the liposome surface: on the mechanism of polymer-coated liposome longevity. Biochim. Biophys. Acta, 1195, 11-20 (1994).
8. Maeda H. Macromolecular therapeutics in cancer treatment: the EPR effect and beyond. J. Control. Release, 164, 138-144 (2012).
9. Barenholz Y. Doxil®-the first FDA-approved nano-drug: lessons learned. J. Control. Release, 160, 117-134 (2012).
10. Abu Lila AS, Kiwada H, Ishida T. The accelerated blood clearance (ABC) phenomenon: clinical challenge and approaches to manage. J. Control. Release, 172, 38-47 (2013).
11. Dams ET, Laverman P, Oyen WJ, Storm G, Scherphof GL, van Der Meer JW, Corstens FH, Boerman OC Accelerated blood clearance and altered biodistribution of repeated injections of sterically stabilized liposomes. J. Pharmacol. Exp. Ther., 292, 1071-1079 (2000).
12. Wang C, Cheng X, Sui Y, Luo X, Jiang G, Wang Y, Huang Z, She Z, Deng Y A noticeable phenomenon: thiol terminal PEG enhances the immunogenicity of PEGylated emulsions injected intravenously or subcutaneously into rats. Eur. J. Pharm. Biopharm., 85, 744-751 (2013).
13. Zhao Y, Wang L, Yan M, Ma Y, Zang G, She Z, Deng Y Repeated injection of PEGylated solid lipid nanoparticles induces accelerated blood clearance in mice and beagles. Int. J. Nanomedicine, 7, 2891-2900 (2012).
14. Szebeni J, Muggia F, Gabizon A, Barenholz Y Activation of complement by therapeutic liposomes and other lipid excipient-based therapeutic products: prediction and prevention. Adv. Drug Deliv. Rev, 63, 1020-1030 (2011).
15. Ishida T, Harada M, Wang XY, Ichihara M, Irimura K, Kiwada H. 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, 305-317 (2005).
16. Bartlett GR. Colorimetric assay methods for free and phosphory-lated glyceric acids. J. Biol. Chem., 234, 469-471 (1959).
17. Shimizu T, Ichihara M, Yoshioka Y, Ishida T, Nakagawa S, Kiwada H. Intravenous administration of polyethylene glycol-coated (PEGylated) proteins and PEGylated adenovirus elicits an anti-PEG immunoglobulin M response. Biol. Pharm. Bull., 35, 1336-1342 (2012).
18. Hashimoto Y, Shimizu T, Mima Y, Abu Lila AS, Ishida T, Kiwada H. Generation, characterization and In vivo biological activity of two distinct monoclonal anti-PEG IgMs. Toxicol. Appl. Pharmacol., 277, 30-38 (2014).
19. Ishihara T, Takeda M, Sakamoto M, Kimoto A, Kobayashi C, Takasaki N, Yuki K, Tanaka I, Takenaga M, Igarashi R, Maeda T, Yamakawa N, Okamoto Y, Otsuka M, Ishida T, Kiwada H, Mizushima Y, Mizushima T. Accelerated blood clearance phenomenon upon repeated injection of PEG-modified PLA-nanoparticles. Pharm. Res., 26, 2270-2279 (2009).
20. Harashima H, Yamane C, Kume Y, Kiwada H. Kinetic analysis of AUC-dependent saturable clearance of liposomes: mathematical description of AUC dependency. J. Pharmacokinet. Biopharm., 21, 299-308 (1993).
21. Takemoto S, Yamaoka K, Nishikawa M, Takakura Y. Histogram analysis of pharmacokinetic parameters by bootstrap resampling from one-point sampling data in animal experiments. Drug Metab. Pharmacokinet., 21, 458-464 (2006).
22. Wang X, Ishida T, Kiwada H. Anti-PEG IgM elicited by injection of liposomes is involved in the enhanced blood clearance of a subsequent dose of PEGylated liposomes. J. Control. Release, 119, 236-244 (2007).
23. Singh AK, Kilpatrick PK, Carbonell RG. Application of antibody and fluorophore-derivatized liposomes to heterogeneous immunoassays for d-dimer. Biotechnol. Prog., 12, 272-280 (1996).
24. Rus H, Cudrici C, Niculescu F. The role of the complement system in innate immunity. Immunol. Res., 33, 103-112 (2005).
25. Pham CTN, Mitchell LM, Huang JL, Lubniewski CM, Schall OF, Killgore JK, Pan DPJ, Wickline SA, Lanza GM, Hourcade DE. Variable antibody-dependent activation of complement by functionalized phospholipid nanoparticle surfaces. J. Biol. Chem., 286, 123-130 (2011).
26. Ishida T, Kiwada H. Accelerated blood clearance (ABC) phenomenon upon repeated injection of PEGylated liposomes. Int. J. Pharm., 354, 56-62 (2008).
27. Sroda K, Rydlewski J, Langner M, Kozubek A, Grzybek M, Sikorski AF. Repeated injections of PEG-PE liposomes generate anti-PEG antibodies. Cell. Mol. Biol. Lett., 10, 37-47 (2005).
28. Suzuki T, Ichihara M, Hyodo K, Yamamoto E, Ishida T, Kiwada H, Ishihara H, Kikuchi H. Accelerated blood clearance of PEGylated liposomes containing doxorubicin upon repeated administration to dogs. Int. J. Pharm., 436, 636-643 (2012).
29. Li CL, Cao JN, Wang YJ, Zhao X, Deng CX, Wei N, Yang J, Cui JX. Accelerated blood clearance of pegylated liposomal topotecan: influence of polyethylene glycol grafting density and animal species. J. Pharm. Sci., 101, 3864-3876 (2012).
30. Kaminskas LM, Mcleod VM, Porter CJH, Boyd BJ. Differences in colloidal structure of PEGylated nanomaterials dictate the likelihood of accelerated blood clearance. J. Pharm. Sci., 100, 5069-5077 (2011).
31. Dams ETM, Laverman P, Oyen WJG, Storm G, Scherphof GL, Van der Meer JWM, Corstens FHM, Boerman OC. Accelerated blood clearance and altered biodistribution of repeated injections of sterically stabilized liposomes. J. Pharmacol. Exp. Ther., 292, 1071-1079 (2000).
32. Lynch DM, Kay PH, Papadimitriou JM, Grounds MD. Studies on the structure of complement C3 and the stability of C3 derived phagocytic ligands C3b/iC3b in SJL/J and BALB/c mice. Eur. J. Immunogenet., 20, 1-9 (1993).
33. Borsos T, Chapuis RM, Langone JJ. Distinction between fixation of C1 and the activation of complement by natural IgM anti-hapten antibody: effect of cell surface hapten density. Mol. Immunol., 18, 863-868 (1981).
34. Armstrong SJ, Outlaw MC, Dimmock NJ. Morphological studies of the neutralization of influenza virus by IgM. J. Gen. Virol., 71, 2313-2319 (1990).
35. Ochsenbein AF, Zinkernagel RM. Natural antibodies and complement link innate and acquired immunity. Immunol. Today, 21, 624-630 (2000).
36. Jones HE, Taylor PR, McGreal E, Zamze S, Wong SYC. The contribution of naturally occurring IgM antibodies, IgM cross-reactivity and complement dependency in murine humoral responses to pneumococcal capsular polysaccharides. Vaccine, 27, 5806-5815 (2009).
37. Armstrong JK, Hempel G, Koling S, Chan LS, Fisher T, Meiselman HJ, Garratty G. Antibody against poly(ethylene glycol) adversely affects PEG-asparaginase therapy in acute lymphoblastic leukemia patients. Cancer, 110, 103-111 (2007).
38. Liu Y, Reidler H, Pan J, Milunic D, Qin D, Chen D, Vallejo YR, Yin R. A double antigen bridging immunogenicity ELISA for the detection of antibodies to polyethylene glycol polymers. J. Pharmacol. Toxicol. Methods, 64, 238-245 (2011).
39. Richter AW, Akerblom E. Antibodies against polyethylene glycol produced in animals by immunization with monomethoxy polyethylene glycol modified proteins. Int. Arch. Allergy Appl. Immunol., 70, 124-131 (1983).