The accelerated blood clearance (ABC) phenomenon: Clinical challenge and approaches to manage

Journal of Controlled Release

Volumn 172, Issue 1, 2013, Pages 38-47

  Abu Lila, Amr S ^a,b   Kiwada, Hiroshi ^a   Ishida, Tatsuhiro ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b Zagazig University   (Egypt)

Author keywords

Accelerated blood clearance (ABC); Anti PEG IgM; phenomenon; Polyethylene glycol(PEG); Repeated administration; Splenic B cells

Indexed keywords

ACCELERATED BLOOD CLEARANCES; ANTI-PEG IGM; B CELLS; PHENOMENON; POLYETHYLENE GLYCOL (PEG);

LIPOSOMES; POLYETHYLENE GLYCOLS;

BLOOD;

COMPLEMENT RECEPTOR; CYTOTOXIC AGENT; DOXORUBICIN; EPIRUBICIN; IMMUNOGLOBULIN M; LIPOSOME; MACROGOL; NANOCARRIER; NANOPARTICLE; NUCLEIC ACID; OXALIPLATIN; POLYMER; SMALL INTERFERING RNA; SOLID LIPID NANOPARTICLE;

ACCELERATED BLOOD CLEARANCE; CANCER CHEMOTHERAPY; COMPLEMENT ACTIVATION; DENSITY; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG PENETRATION; DRUG RETENTION; ENCAPSULATION; HUMAN; KUPFFER CELL; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MICELLE; NONHUMAN; PHAGOCYTOSIS; PHYSICAL CHEMISTRY; PLASMA CLEARANCE; PRIORITY JOURNAL; REVIEW; SPLENECTOMY; SURFACE CHARGE;

ACCELERATED BLOOD CLEARANCE (ABC) PHENOMENON; ANTI-PEG IGM; POLYETHYLENE GLYCOL(PEG); REPEATED ADMINISTRATION; SPLENIC B CELLS;

ANIMALS; COMPLEMENT ACTIVATION; DRUG CARRIERS; HUMANS; IMMUNOGLOBULIN M; LIPOSOMES; POLYETHYLENE GLYCOLS; SPLEEN;

EID: 84883504398     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.07.026     Document Type: Review

References (90)

1. A.L. Klibanov, K. Maruyama, V.P. Torchilin, and L. Huang Amphipathic polyethyleneglycols effectively prolong the circulation time of liposomes FEBS Lett. 268 1990 235 237 (Pubitemid 20233874)
2. J. Senior, C. Delgado, D. Fisher, C. Tilcock, and G. Gregoriadis Influence of surface hydrophilicity of liposomes on their interaction with plasma protein and clearance from the circulation: studies with poly(ethylene glycol)-coated vesicles Biochim. Biophys. Acta 1062 1991 77 82
3. V.P. Torchilin Polymer-coated long-circulating microparticulate pharmaceuticals J. Microencapsul. 15 1998 1 19 (Pubitemid 28031786)
4. C. Allen, N. Dos Santos, R. Gallagher, G.N. Chiu, Y. Shu, W.M. Li, S.A. Johnstone, A.S. Janoff, L.D. Mayer, M.S. Webb, and M.B. Bally Controlling the physical behavior and biological performance of liposome formulations through use of surface grafted poly(ethylene glycol) Biosci Rep. 22 2002 225 250 (Pubitemid 35222733)
5. D.D. Lasic, F.J. Martin, A. Gabizon, S.K. Huang, and D. Papahadjopoulos Sterically stabilized liposomes: a hypothesis on the molecular origin of the extended circulation times Biochim. Biophys. Acta 1070 1991 187 192
6. 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 (Pubitemid 30136603)
7. 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 (Pubitemid 32673411)
8. T. Ishida, R. Maeda, M. Ichihara, Y. Mukai, Y. Motoki, Y. Manabe, K. Irimura, and H. Kiwada The accelerated clearance on repeated injection of pegylated liposomes in rats: laboratory and histopathological study Cell. Mol. Biol. Lett. 7 2002 286
9. T. Ishida, R. Maeda, M. Ichihara, K. Irimura, and H. Kiwada Accelerated clearance of PEGylated liposomes in rats after repeated injections J. Control. Release 88 2003 35 42 (Pubitemid 36173950)
10. B. Goins, W.T. Phillips, and R. Klipper Repeat injection studies of technetium-99m-labeled peg-liposomes in the same animal J. Liposome Res. 8 1998 265 281 (Pubitemid 28268267)
11. T. Ishida, T. Ichikawa, M. Ichihara, Y. Sadzuka, and H. Kiwada Effect of the physicochemical properties of initially injected liposomes on the clearance of subsequently injected PEGylated liposomes in mice J. Control. Release 95 2004 403 412 (Pubitemid 38340491)
12. M. Joshi, S. Pathak, S. Sharma, and V. Patravale Solid microemulsion preconcentrate (NanOsorb) of artemether for effective treatment of malaria Int. J. Pharm. 362 2008 172 178
13. H. Koide, T. Asai, K. Hatanaka, T. Urakami, T. Ishii, E. Kenjo, M. Nishihara, M. Yokoyama, T. Ishida, H. Kiwada, and N. Oku Particle size-dependent triggering of accelerated blood clearance phenomenon Int. J. Pharm. 362 2008 197 200
14. T. Ishihara, M. Takeda, H. Sakamoto, A. Kimoto, C. Kobayashi, N. Takasaki, K. Yuki, K. Tanaka, M. Takenaga, R. Igarashi, T. Maeda, N. Yamakawa, Y. Okamoto, M. Otsuka, T. Ishida, H. Kiwada, Y. Mizushima, and T. Mizushima Accelerated blood clearance phenomenon upon repeated injection of PEG-modified PLA-nanoparticles Pharm. Res. 26 2009 2270 2279
15. W. Lu, J. Wan, Z. She, and X. Jiang Brain delivery property and accelerated blood clearance of cationic albumin conjugated pegylated nanoparticle J. Control. Release 118 2007 38 53 (Pubitemid 46283096)
16. 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 (Pubitemid 47407760)
17. X. Wang, T. Ishida, and H. Kiwada 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 2007 236 244 (Pubitemid 46759557)
18. T. Ishida, and H. Kiwada Accelerated blood clearance (ABC) phenomenon upon repeated injection of PEGylated liposomes Int. J. Pharm. 354 2008 56 62
19. T. Tagami, Y. Uehara, N. Moriyoshi, T. Ishida, and H. Kiwada Anti-PEG IgM production by siRNA encapsulated in a PEGylated lipid nanocarrier is dependent on the sequence of the siRNA J. Control. Release 151 2011 149 154
20. 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
21. T. Ishida, M. Ichihara, X. Wang, and H. Kiwada Spleen plays an important role in the induction of accelerated blood clearance of PEGylated liposomes J. Control. Release 115 2006 243 250 (Pubitemid 44634842)
22. 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
23. F. Martin, A.M. Oliver, and J.F. Kearney Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens Immunity 14 2001 617 629 (Pubitemid 32520872)
24. A. Zandvoort, and W. Timens The dual function of the splenic marginal zone: essential for initiation of anti-TI-2 responses but also vital in the general first-line defense against blood-borne antigens Clin. Exp. Immunol. 130 2002 4 11
25. 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 2011 1 11
26. S.C. Semple, T.O. Harasym, K.A. Clow, S.M. Ansell, S.K. Klimuk, and M.J. Hope Immunogenicity and rapid blood clearance of liposomes containing polyethylene glycol-lipid conjugates and nucleic acid J. Pharmacol. Exp. Ther. 312 2005 1020 1026 (Pubitemid 40293760)
27. Q. Vos, A. Lees, Z.Q. Wu, C.M. Snapper, and J.J. Mond B-cell activation by T-cell-independent type 2 antigens as an integral part of the humoral immune response to pathogenic microorganisms Immunol. Rev. 176 2000 154 170
28. Z. Sha, and R.W. Compans Induction of CD4(+) T-cell-independent immunoglobulin responses by inactivated influenza virus J. Virol. 74 2000 4999 5005 (Pubitemid 30313838)
29. T.L. Cheng, B.M. Chen, J.W. Chern, M.F. Wu, and S.R. Roffler Efficient clearance of poly(ethylene glycol)-modified immunoenzyme with anti-PEG monoclonal antibody for prodrug cancer therapy Bioconjugate Chem. 11 2000 258 266 (Pubitemid 30174492)
30. T.L. Cheng, P.Y. Wu, M.F. Wu, J.W. Chern, and S.R. Roffler Accelerated clearance of polyethylene glycol-modified proteins by anti-polyethylene glycol IgM Bioconjugate Chem. 10 1999 520 528 (Pubitemid 29243337)
31. K.B. Reid, and R.R. Porter The proteolytic activation systems of complement Annu. Rev. Biochem. 50 1981 433 464
32. Y. Zhao, C. Wang, L. Wang, Q. Yang, W. Tang, Z. She, and Y. Deng A frustrating problem: accelerated blood clearance of PEGylated solid lipid nanoparticles following subcutaneous injection in rats Eur. J. Pharm. Biopharm. 81 2012 506 513
33. A.J. Bradley, and D.V. Devine The complement system in liposome clearance: can complement deposition be inhibited? Adv. Drug Deliv. Rev. 32 1998 19 29 (Pubitemid 28277173)
34. 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 (Pubitemid 44634849)
35. K. Taguchi, S. Ogaki, H. Watanabe, D. Kadowaki, H. Sakai, K. Kobayashi, H. Horinouchi, T. Maruyama, and M. Otagiri Fluid resuscitation with hemoglobin vesicles prevents Escherichia coli growth via complement activation in a hemorrhagic shock rat model J. Pharmacol. Exp. Ther. 337 2011 201 208
36. Q. Yang, Y. Ma, Y. Zhao, Z. She, L. Wang, J. Li, C. Wang, and Y. Deng Accelerated drug release and clearance of PEGylated epirubicin liposomes following repeated injections: a new challenge for sequential low-dose chemotherapy Int. J. Nanomedicine 8 2013 1257 1268
37. T. Ishida, S. Kashima, and H. Kiwada The contribution of phagocytic activity of liver macrophages to the accelerated blood clearance (ABC) phenomenon of PEGylated liposomes in rats J. Control. Release 126 2008 162 165
38. A.H. Brouwers, D.J. De Jong, E.T. Dams, W.J. Oyen, O.C. Boerman, P. Laverman, T.H. Naber, G. Storm, and F.H. Corstens Tc-99m-PEG-liposomes for the evaluation of colitis in Crohn's disease J. Drug Target. 8 2000 225 233
39. J. Szebeni, L. Baranyi, S. Savay, M. Bodo, D.S. Morse, M. Basta, G.L. Stahl, R. Bunger, and C.R. Alving Liposome-induced pulmonary hypertension: properties and mechanism of a complement-mediated pseudoallergic reaction Am. J. Physiol. Heart Circ. Physiol. 279 2000 H1319 H1328
40. A. Chanan-Khan, J. Szebeni, S. Savay, L. Liebes, N.M. Rafique, C.R. Alving, and F.M. Muggia Complement activation following first exposure to pegylated liposomal doxorubicin (Doxil): possible role in hypersensitivity reactions Ann. Oncol. 14 2003 1430 1437 (Pubitemid 37185291)
41. Y. Liu, H. Reidler, J. Pan, D. Milunic, D. Qin, D. Chen, Y.R. Vallejo, and R. Yin A double antigen bridging immunogenicity ELISA for the detection of antibodies to polyethylene glycol polymers J. Pharmacol. Toxicol. Methods 64 2011 238 245
42. J.K. Armstrong, G. Hempel, S. Koling, L.S. Chan, T. Fisher, H.J. Meiselman, and G. Garratty Antibody against poly(ethylene glycol) adversely affects PEG-asparaginase therapy in acute lymphoblastic leukemia patients Cancer 110 2007 103 111 (Pubitemid 46986423)
43. A.W. Richter, and E. Akerblom Antibodies against polyethylene glycol produced in animals by immunization with monomethoxy polyethylene glycol modified proteins Int. Arch. Allergy Appl. Immunol. 70 1983 124 131 (Pubitemid 13171427)
44. C. Oussoren, and G. Storm Effect of repeated intravenous administration on circulation kinetics of poly(ethyleneglycol) liposomes in rats J. Liposome Res. 9 1999 349 355 (Pubitemid 29439400)
45. 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 (Pubitemid 40941995)
46. R. Saadati, S. Dadashzadeh, Z. Abbasian, and H. Soleimanjahi Accelerated blood clearance of PEGylated PLGA nanoparticles following repeated injections: effects of polymer dose, PEG coating, and encapsulated anticancer drug Pharm. Res. 30 2013 985 995
47. T. Ishihara, T. Maeda, H. Sakamoto, N. Takasaki, M. Shigyo, T. Ishida, H. Kiwada, Y. Mizushima, and T. Mizushima Evasion of the accelerated blood clearance phenomenon by coating of nanoparticles with various hydrophilic polymers Biomacromolecules 11 2010 2700 2706
48. 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
49. 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
50. 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
51. Y. Zhao, L. Wang, M. Yan, Y. Ma, G. Zang, Z. She, and Y. Deng Repeated injection of PEGylated solid lipid nanoparticles induces accelerated blood clearance in mice and beagles Int. J. Nanomedicine 7 2012 2891 2900
52. O. Lyass, B. Uziely, R. Ben-Yosef, D. Tzemach, N.I. Heshing, M. Lotem, G. Brufman, and A. Gabizon Correlation of toxicity with pharmacokinetics of pegylated liposomal doxorubicin (Doxil) in metastatic breast carcinoma Cancer 89 2000 1037 1047
53. A. Gabizon, A. Dagan, D. Goren, Y. Barenholz, and Z. Fuks Liposomes as in vivo carriers of adriamycin: reduced cardiac uptake and preserved antitumor activity in mice Cancer Res. 42 1982 4734 4739 (Pubitemid 13205982)
54. Y. Matsumura, and H. Maeda A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs Cancer Res. 46 1986 6387 6392 (Pubitemid 17221789)
55. A. Chonn, and P.R. Cullis Recent advances in liposomal drug-delivery systems Curr. Opin. Biotechnol. 6 1995 698 708
56. T.M. Allen, and P.R. Cullis Drug delivery systems: entering the mainstream Science 303 2004 1818 1822 (Pubitemid 38374867)
57. 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
58. 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
59. A.S. Abu Lila, N.E. Eldin, M. Ichihara, T. Ishida, and H. Kiwada Multiple administration of PEG-coated liposomal oxaliplatin enhances its therapeutic efficacy: a possible mechanism and the potential for clinical application Int. J. Pharm. 438 2012 176 183
60. T. Tagami, K. Nakamura, T. Shimizu, T. Ishida, and H. Kiwada Effect of siRNA in PEG-coated siRNA-lipoplex on anti-PEG IgM production J. Control. Release 137 2009 234 240
61. Y. Ma, Q. Yang, L. Wang, X. Zhou, Y. Zhao, and Y. Deng Repeated injections of PEGylated liposomal topotecan induces accelerated blood clearance phenomenon in rats Eur. J. Pharm. Sci. 45 2012 539 545
62. K. Nakamura, A.S. Abu Lila, M. Matsunaga, Y. Doi, T. Ishida, and H. Kiwada A double-modulation strategy in cancer treatment with a chemotherapeutic agent and siRNA Mol. Ther. 19 2011 2040 2047
63. M. Sainlos, M. Hauchecorne, N. Oudrhiri, S. Zertal-Zidani, A. Aissaoui, J.P. Vigneron, J.M. Lehn, and P. Lehn Kanamycin A-derived cationic lipids as vectors for gene transfection ChemBioChem 6 2005 1023 1033 (Pubitemid 40825343)
64. G.D. Schmidt-Wolf, and I.G. Schmidt-Wolf Non-viral and hybrid vectors in human gene therapy: an update Trends Mol. Med. 9 2003 67 72 (Pubitemid 36313867)
65. A. Judge, K. McClintock, J.R. Phelps, and I. Maclachlan Hypersensitivity and loss of disease site targeting caused by antibody responses to PEGylated liposomes Mol. Ther. 13 2006 328 337 (Pubitemid 43056898)
66. T. Tagami, K. Nakamura, T. Shimizu, N. Yamazaki, T. Ishida, and H. Kiwada CpG motifs in pDNA-sequences increase anti-PEG IgM production induced by PEG-coated pDNA-lipoplexes J. Control. Release 142 2010 160 166
67. H. Hemmi, O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira A toll-like receptor recognizes bacterial DNA Nature 408 2000 740 745 (Pubitemid 32015992)
68. N. Yagi, I. Manabe, T. Tottori, A. Ishihara, F. Ogata, J.H. Kim, S. Nishimura, K. Fujiu, Y. Oishi, K. Itaka, Y. Kato, M. Yamauchi, and R. Nagai A nanoparticle system specifically designed to deliver short interfering RNA inhibits tumor growth in vivo Cancer Res. 69 2009 6531 6538
69. H. Ma, K. Shiraishi, T. Minowa, K. Kawano, M. Yokoyama, Y. Hattori, and Y. Maitani Accelerated blood clearance was not induced for a gadolinium-containing PEG-poly(l-lysine)-based polymeric micelle in mice Pharm. Res. 27 2010 296 302
70. K. Shiraishi, M. Hamano, H. Ma, K. Kawano, Y. Maitani, T. Aoshi, K.J. Ishii, and M. Yokoyama Hydrophobic blocks of PEG-conjugates play a significant role in the accelerated blood clearance (ABC) phenomenon J. Control. Release 165 2013 183 190
71. E. Hara, A. Makino, K. Kurihara, F. Yamamoto, E. Ozeki, and S. Kimura Pharmacokinetic change of nanoparticulate formulation "Lactosome" on multiple administrations Int. Immunopharmacol. 14 2012 261 266
72. E. Formann, W. Jessner, L. Bennett, and P. Ferenci Twice-weekly administration of peginterferon-alpha-2b improves viral kinetics in patients with chronic hepatitis C genotype 1 J. Viral Hepat. 10 2003 271 276 (Pubitemid 36801913)
73. E. Ambegia, S. Ansell, P. Cullis, J. Heyes, L. Palmer, and I. MacLachlan Stabilized plasmid-lipid particles containing PEG-diacylglycerols exhibit extended circulation lifetimes and tumor selective gene expression Biochim. Biophys. Acta 1669 2005 155 163 (Pubitemid 40704733)
74. M.S. Webb, D. Saxon, F.M. Wong, H.J. Lim, Z. Wang, M.B. Bally, L.S. Choi, P.R. Cullis, and L.D. Mayer Comparison of different hydrophobic anchors conjugated to poly(ethylene glycol): effects on the pharmacokinetics of liposomal vincristine Biochim. Biophys. Acta 1372 1998 272 282 (Pubitemid 28451550)
75. H. Xu, Y. Deng, D. Chen, W. Hong, Y. Lu, and X. Dong Esterase-catalyzed dePEGylation of pH-sensitive vesicles modified with cleavable PEG-lipid derivatives J. Control. Release 130 2008 238 245
76. H. Xu, K.Q. Wang, Y.H. Deng, and W. Chen da Effects of cleavable PEG-cholesterol derivatives on the accelerated blood clearance of PEGylated liposomes Biomaterials 31 2010 4757 4763
77. D. Chen, W. Liu, Y. Shen, H. Mu, Y. Zhang, R. Liang, A. Wang, K. Sun, and F. Fu Effects of a novel pH-sensitive liposome with cleavable esterase-catalyzed and pH-responsive double smart mPEG lipid derivative on ABC phenomenon Int. J. Nanomedicine 6 2011 2053 2061
78. B. Romberg, C. Oussoren, C.J. Snel, M.G. Carstens, W.E. Hennink, and G. Storm Pharmacokinetics of poly(hydroxyethyl-l-asparagine)-coated liposomes is superior over that of PEG-coated liposomes at low lipid dose and upon repeated administration Biochim. Biophys. Acta 1768 2007 737 743 (Pubitemid 46275604)
79. K. Taguchi, Y. Urata, M. Anraku, H. Watanabe, D. Kadowaki, H. Sakai, H. Horinouchi, K. Kobayashi, E. Tsuchida, T. Maruyama, and M. Otagiri Hemoglobin vesicles, polyethylene glycol (PEG)ylated liposomes developed as a red blood cell substitute, do not induce the accelerated blood clearance phenomenon in mice Drug Metab. Dispos. 37 2009 2197 2203
80. 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
81. P.G. Tardi, E.N. Swartz, T.O. Harasym, P.R. Cullis, and M.B. Bally An immune response to ovalbumin covalently coupled to liposomes is prevented when the liposomes used contain doxorubicin J. Immunol. Methods 210 1997 137 148 (Pubitemid 28266558)
82. H. Koo, M.S. Huh, I.C. Sun, S.H. Yuk, K. Choi, K. Kim, and I.C. Kwon In vivo targeted delivery of nanoparticles for theranosis Acc. Chem. Res. 44 2011 1018 1028
83. M. Kumagai, M.R. Kano, Y. Morishita, M. Ota, Y. Imai, N. Nishiyama, M. Sekino, S. Ueno, K. Miyazono, and K. Kataoka Enhanced magnetic resonance imaging of experimental pancreatic tumor in vivo by block copolymer-coated magnetite nanoparticles with TGF-beta inhibitor J. Control. Release 140 2009 306 311
84. H. Cabral, N. Nishiyama, and K. Kataoka Supramolecular nanodevices: from design validation to theranostic nanomedicine Acc. Chem. Res. 44 2011 999 1008
85. A. Abuchowski, J.R. McCoy, N.C. Palczuk, T. van Es, and F.F. Davis Effect of covalent attachment of polyethylene glycol on immunogenicity and circulating life of bovine liver catalase J. Biol. Chem. 252 1977 3582 3586 (Pubitemid 8116088)
86. A. Abuchowski, T. van Es, N.C. Palczuk, and F.F. Davis Alteration of immunological properties of bovine serum albumin by covalent attachment of polyethylene glycol J. Biol. Chem. 252 1977 3578 3581 (Pubitemid 8116087)
87. W. Sun, W. Zou, G. Huang, A. Li, and N. Zhang Pharmacokinetics and targeting property of TFu-loaded liposomes with different sizes after intravenous and oral administration J. Drug Target. 16 2008 357 365 (Pubitemid 351935733)
88. S. Hussain, A. Pluckthun, T.M. Allen, and U. Zangemeister-Wittke Antitumor activity of an epithelial cell adhesion molecule targeted nanovesicular drug delivery system Mol. Cancer Ther. 6 2007 3019 3027 (Pubitemid 350206780)
89. G. Knop, and R. Margaria Cardiac pheochromocytoma: a new case reported J. Thorac. Cardiovasc. Surg. 132 2006 1230 1231 (Pubitemid 44584987)
90. N.J. Ganson, S.J. Kelly, E. Scarlett, J.S. Sundy, and M.S. Hershfield Control of hyperuricemia in subjects with refractory gout, and induction of antibody against poly(ethylene glycol) (PEG), in a phase I trial of subcutaneous PEGylated urate oxidase Arthritis Res. Ther. 8 2006 R12