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Research Article

Liposome triggering of innate immune responses: A perspective on benefits and adverse reactions

Biological recognition and interactions of liposomes

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Pages 85-90 | Accepted 03 Feb 2009, Published online: 01 Jun 2009

References

  • Allen TM, Cullis PR. Drug delivery systems: entering the mainstream. Science 2004;303:1818–1822.
  • Alving CR, Rao M. Lipid A and liposomes containing lipid A as antigens and adjuvants. Vaccine 2008;26:3036–3045.
  • Alving CR, Swartz GM, Jr. Antibodies to cholesterol, cholesterol conjugates, and liposomes: implications for atherosclerosis and autoimmunity. CRC Crit Rev Immunol 1991;10:441–453.
  • Amselem S, Gabizon A, Barenholz Y. Optimization and upscaling of doxorubicin-containing liposomes for clinical use. J Pharm Sci 2006;79:1045–1052.
  • 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 2007;110:103–111.
  • Bradley AJ, Brooks DE, Norris-Jones R, Devine DV. C1q binding to liposomes is charge dependent and is inhibited by peptides consisting of residues 14–26 of the human C1qA chain in a sequence-independent manner. Biochim Biophys Acta 1999;1418:19–30.
  • Bradley AJ, Devine DV, Ansell SM, Janzen J, Brooks DE. Inhibition of liposome-induced complement activation by incorporated poly(ethylene glycol)-lipids. Arch Biochem Biophys 1998;357:185–194.
  • Chanan-Khan A, Szebeni J, Savay S, Liebes L, Rafique NM, Alving CR, Muggia F. Complement activation following first exposure to pegylated liposomal doxorubicin (Doxil): possible role in hypersensitivity reactions. Ann Oncol 2003;14:1430–1437.
  • Chonn A, Cullis P, Devine DA. The role of surface charge in the activation of the classical and alternative pathways of complement by liposomes. J Immunol 1991;146:4234–4241.
  • Csomor E, Bajtaya Z, Sandora N, Kristofa K, Arlaudc GJ, Thield S, et al. Complement protein C1q induces maturation of human dendritic cells. Mol Immunol 2007;44:3389–3397.
  • Daemen T, Hofstede G, Kate MTT, Bakker-Woudenberg IAJM, Scherphof G. Liposomal doxorubicin-induced toxicity: depletion and impairment of phagocytic activity of liver macrophages. Int J Cancer 1995;61:716–721.
  • Dams ET, Laverman P, Oyen WJ, Storm G, Scherphof GL, van Der Meer JW, et al. Accelerated blood clearance and altered biodistribution of repeated injections of sterically stabilized liposomes. J Pharmacol Exp Ther 2000a;292:1071–1079.
  • Dams ET, Oyen WJ, Boerman OC, Storm G, Laverman P, Kok PJ, et al. 99mTc-PEG liposomes for the scintigraphic detection of infection and inflammation: clinical evaluation. J Nucl Med 2000b;41:622–630.
  • Dempsey PW, Allison ME, Akkaraju S, Goodnow CC, Fearon DF. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 1996;271:348–350.
  • Devine DV, Marjan JMJ. The role of immunoproteins in the survival of liposomes in the circulation. Crit Rev Ther Drug Carrier Syst 1997;14:105–131.
  • Dos Santos N, Allen C, Doppen AM, Cox KAK, Gallegher RC, Karlsson G, et al. Influence of poly(ethylene glycol) grafting density and polymer length on liposomes: relating plasma circulation lifetimes to protein binding. Biochim Biophys Acta 2007;1768:1367–1377.
  • Dow SW. Liposome-nucleic acid immunotherapeutics. Exp Opin Drug Deliv 2008;5:11–24.
  • Erdmann SM, Heussen N, Moll-Slodowy S, Merk HF, Sachs B. CD63 expression on basophils as a tool for the diagnosis of pollen-associated food allergy: sensitivity and specificity. Clin Exp Allergy 2003;33:607–614.
  • Gabizon A, Catane R, Uziely B, Kaufman B, Safra T, Cohen R, et al. Prolonged circulation time and enhanced accumulation in malignant exudates of doxorubicin encapsulated in polyethylene-glycol coated liposomes. Cancer Res 1994;54:987–992.
  • Gabizon A, Shmeeda H, Barenholz Y. Pharmacokinetics of PEGylated liposomal doxorubicin: review of animal and human studies. Clin Pharmacokin 2003;42:419–436.
  • Hamad I, Hunter AC, Rutt KR, Liu Z, Dai H, Moghimi SM. Complement activation by PEGylated single-walled carbon nanotubes is independent of C1q and alternative pathway turnover. Mol Immunol 2008a;43:3797–3803.
  • Hamad I, Hunter AC, Szebeni J, Moghimi SM. Poly(ethylene glycol)s generate complement activation products in human serum through increased alternative pathway turnover and a MASP-2-dependent process. Mol Immunol 2008b;46:225–232.
  • Hauswirth AW, Natter S, Ghannadan M, Majlesi Y, Schernthaner G-H, Sperr WR, et al. Recombinant allergens promote expression of CD203c on basophils in sensitized individuals. J Allergy Clin Immunol 2002;110:102–109.
  • Ishida T, Atobe K, Wang X, Kiwada H. Accelerated blood clearance of PEGylated liposomes upon repeated injections: effect of doxorubicin-encapsulation and high-dose first injection. J Contr Rel 2006a;115:251–258.
  • Ishida T, Ichikawa T, Ichihara M, Sadzuka Y, Kiwada H. Effect of the physicochemical properties of initially injected liposomes on the clearance of subsequently injected PEGylated liposomes in mice. J Contr Rel 2004;95:403–412.
  • Ishida T, Ichihara M, Wang X, Kiwada H. Spleen plays an important role in the induction of accelerated blood clearance of PEGylated liposomes. J Contr Rel 2006b;115:243–250.
  • Ishida T, Kashima S, Kiwada H. The contribution of phagocytic activity of liver macrophages to the accelerated blood clearance (ABC) phenomenon of PEGylated liposomes in rats. J Contr Rel 2008;126:162–165.
  • Ishida T, Wang X, Shimizu T, Nawata K, Kiwada H. PEGylated liposomes elicit an anti-PEG IgM response in a T-cell-independent manner. J Contr Rel 2007;122:349–355.
  • Janssen BJC, Christodoulidou A, McCarthy A, Lambris JD, Gros P. Structure of C3b reveals conformational changes that underlie complement activity. Nature 2006;444:213–216.
  • Karasavvas N, Beck Z, Tong J, Matyas GR, Rao M, McCutchan FE, et al. Antibodies induced by liposomal protein exhibit dual binding to protein and lipid epitopes. Biochem Biophys Res Commun 2008;366:982–987.
  • Laverman P, Carstens MG, Storm G, Moghimi SM. Recognition and clearance of methoxy(polyethyleneglycol)2000-grafted liposomes by macrophages with enhanced phagocytic capcity. Biochim Biophys Acta 2001;1526:227–229.
  • Lenz HJ. Management and preparedness for infusion and hypersensitivity reactions. Oncologist 2007;12:601–619.
  • Milder FJ, Gomes L, Schouten A, Janssen BJC, Huizinga EG, Romijn RA, et al. Factor B structure provides insights into activation of the central protease of the complement system. Nat Struct Mol Biol 2007;14:224–228.
  • Moghimi SM. Exploitation of macrophage clearance functions in vivo. In: Gordon S (Ed.), The Macrophage as Therapeutic Target. Handbook Exp Pharmacol 2003;158:41–54. Berlin: Springer.
  • Moghimi SM, Gray T. A single dose of intravenously injected poloxamine-coated long-circulating particles triggers macrophage clearance of subsequent doses in rats. Clin Sci 1997;93:371–379.
  • Moghimi SM, Hamad I. Liposome-mediated triggering of complement cascade. J Liposome Res 2008;18:195–209.
  • Moghimi SM, Hamad I, Andresen TL, Jørgensen K, Szebeni J. Methylation of the phosphate oxygen moiety of phospholipid-methoxy(polyethylene glycol) conjugate prevents PEGylated liposome-mediated complement activation and anaphylatoxin production. FASEB J 2006;20:2591–2593.
  • Moghimi SM, Hunter AC. Recognition by macrophages and liver cells of opsonized phospholipid vesicles and phospholipid headgroups. Pharm Res 2001;18:1–8.
  • Moghimi SM, Hunter AC, Murray JC. Long-circulating and target-specific nanoparticles: theory to practice. Pharmacol Rev 2001;53:283–318.
  • Moghimi SM, Hunter AC, Murray JC. Nanomedicine: current status and future prospects. FASEB J 2005;19:311–330.
  • Moghimi SM, Murray JC. Poloxamer-188 revisited: a potentially valuable immune modulator? J Natl Cancer Inst 1996;88:766–768.
  • Moghimi SM, Patel HM. Modulation of murine Kupffer cell clearance of liposome by diethylstilbestrol. The effect of vesicle surface charge and a role for complement receptor Mac-1 (CD11b/CD18) of the newly recruited macrophages in liposome recognition. J Contr Rel 2002;78:55–65.
  • Moghimi SM, Szebeni J. Stealth liposomes and long circulating nanoparticles: critical issues in pharmacokinetics, opsonization, and protein-binding properties. Prog Lipid Res 2003;42:463–478.
  • Peachman KK, Rao M, Alving CR, Palmer DR, Sun W, Rothwell SW. Human dendritic cells and macrophages exhibit different intracellular processing pathways for soluble and liposome-encapsulated antigens. Immunobiology 2005;210:321–333.
  • Ricklin D, Lambris JD. Complement-targeted therapeutics. Nat Biotechnol 2007;25:1265–1275.
  • Szebeni J. The interaction of liposomes with the complement system. Crit Rev Ther Drug Carrier Syst 1998;15:57–88.
  • Szebeni J. Complement activation-related pseudoallergy: a new class of drug-induced acute immune toxicity. Toxicology 2005;216:106–121.
  • Szebeni J, Alving CR. Method of inhibiting side effects of pharmaceutical compositions containing amphiphilic vehicles or drug carrier molecules. 2008. US patent no. 7,419,683.
  • Szebeni J, Baranji L, Sávay S, Bodó M, Milosevits J, Alving CR, et al. Complement activation-related cardiac anaphylaxis in pigs: role of C5a anaphylatoxin and adenosine in liposome-induced abnormalities in ECG and heart function. Am J Physiol Heart Circ Physiol 2006;290:H1050–H1058.
  • Szebeni J, Baranyi L, Sávay S, Lutz H, Jelezarova E, Bunger R, et al. The role of complement activation in hypersensitivity to Pegylated liposomal doxorubicin (Doxil). J Liposome Res 2000;10:467–481.
  • Szebeni J, Baranyi L, Savay S, Milosevits J, Bodo M, Bunger R, et al. The interaction of liposomes with the complement system: in vitro and in vivo assays. Meth Enzymol 2003;373:136–15.
  • Szebeni J, Fontana JL, Wassef NM, Mongan PD, Morse DS, Dobbins DE, et al. Hemodynamic changes induced by liposomes and liposome-encapsulated hemoglobin in pigs—a model for pseudoallergic cardiopulmonary reactions to liposomes: role of complement and inhibition by soluble CR1 and anti-C5a antibody. Circulation 1999;99:2302–2309.
  • 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 Contr Rel 2007;119:236–244.
  • Webb MS, Saxon D, Wong FMP, Lim HJ, Wang Z, Bally MC, et al. Comparison of different hydrophobic anchors conjugated to poly(ethylene glycol): effects on pharmacokinetics of liposomal vincristine. Biochim Biophys Acta 1998;1372:272–282.
  • Zalipsky S, Barenholz Y. Liposome composition for reduction of liposome-induced complement activation. 2004; PCT Patent Application (WO 2004/078121).

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