Liposome clearance

Bioscience Reports

Volumn 22, Issue 2, 2002, Pages 197-224

  Ishida, Tatsuhiro ^a   Harashima, Hideyoshi ^b   Kiwada, Hiroshi ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Clearance; Liposomes; Mononuclear phagocyte system; Opsonins; Serum protein

Indexed keywords

COMPLEMENT MEMBRANE ATTACK COMPLEX; LIPOSOME; MACROGOL; OPSONIN; PHOSPHOLIPID; PLASMA PROTEIN;

ANIMAL EXPERIMENT; CHEMICAL MODIFICATION; CONTROLLED STUDY; DRUG CLEARANCE; DRUG PROTEIN BINDING; HUMAN; MONONUCLEAR PHAGOCYTE; NONHUMAN; SHORT SURVEY; STEREOCHEMISTRY; SURFACE PROPERTY;

ANIMALS; BETA 2-GLYCOPROTEIN I; CATTLE; COMPLEMENT ACTIVATION; DRUG COMPOUNDING; GLYCOPROTEINS; GUINEA PIGS; HUMANS; IMMUNOGLOBULINS; INJECTIONS, INTRAVENOUS; LIPOSOMES; LIVER; MEMBRANE LIPIDS; MEMBRANE PROTEINS; METABOLIC CLEARANCE RATE; MICE; OPSONIN PROTEINS; PARTICLE SIZE; PHAGOCYTOSIS; POLYETHYLENE GLYCOLS; PROTEIN BINDING; RATS; RECEPTORS, CELL SURFACE; RECEPTORS, IMMUNOLOGIC; RECEPTORS, LIPOPROTEIN; RECEPTORS, SCAVENGER; SCAVENGER RECEPTORS, CLASS B; SPECIES SPECIFICITY; TISSUE DISTRIBUTION;

ANIMALIA;

EID: 0036555035     PISSN: 01448463     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1020134521778     Document Type: Short Survey

References (120)

1. Patel, H. M. (1992) Serum opsonins and liposomes: Their interaction and opsonophagocytosis. Crit. Rev. Ther. Drug Carrier Syst. 9:39-90.
2. Devine, D. V. and Marjan, J. M. (1997) The role of immunoproteins in the survival of liposomes in the circulation. Crit. Rev. Ther. Drug. Carrier Syst. 14:105-131.
3. Moghimi, S. M. and Patel, H. M. (1998) Serum mediated recognition of liposomes by phagocytic cells of the reticuloendotherial system: The concept of tissue specificity. Adv. Drug Deliv. Rev. 32:45-60.
4. Rodrigueza, W. V., Phillips, M. C., and Williams, K. J. (1998) Structural and metabolic consequences of liposome-lipoprotein interactions. Adv. Drug Deliv. Rev. 32.
5. Senior, J. H. (1987) Fate and behavior of liposomes in vivo: A review of controlling factors. Crit. Rev. Ther. Drug Carrier Syst. 3:123-193.
6. M1-containing liposomes. Biochim. Biophys. Acta 1104:95-101.
7. Kimberly, R. P. (1983) Phagocytosis by the mononuclear phagocytes system and immune diseases. Am. J. Med. 74:481-493.
8. Absolom, D. R. (1986) Opsonins and dysopsonins: An overview. Methods Enzymol. 132:281-318.
9. Senior, J. H. (1987) Fate and behavior of liposomes in vivo: A review of controlling factors. Crit. Rev. Ther. Drug Carrier Syst. 3:123-193.
10. Black, C. D. and Gregoriadis, G. (1976) Interactions of liposomes with blood plasma proteins. Biochem. Soc. Trans. 4:253-256.
11. Bonte, F. and Juliano, R. L. (1986) Interactions of liposomes with serum proteins. Chem. Phys. Lipids 40:359-372.
12. Alving, C. R., Richards, R. L., and Guirguis, A. A. (1977) Cholesterol-dependent human complement activation resulting in damage to liposomal model membrane. J. Immunol. 118:342-347.
13. Chonn, A., Cullis, P. R., and Devine, D. V. (1991) The role of surface charge in the activation of the classical and alternative pathways of complement by liposomes. J. Immunol. 146:4234-4241.
14. Chonn, A., Semple, S. C., and Cullis, P. R. (1992) Association of blood proteins with large unilamellar liposomes in vivo. Relation to circulation lifetimes. J. Biol. Chem. 267:18759-18765.
15. Funato, K., Yoda, R. and Kiwada, H. (1992) Contribution of complement system on destabilization of liposomes composed of hydrogenated egg phosphatidylcholine in rat fresh plasma. Biochim. Biophys. Acta 1103:198-204.
16. Derksen, J. T. P., Morselt, H. W. M., Kalicharan, D., Hulstaert, C. E., and Scherphof, G. L. (1987) Interaction of immunoglobulin-coated liposomes with rat liver macrophages in vitro. Exp. Cell Res. 168:105-115.
17. Lee, K. D., Hong, K., and Papahadjopoulos, D. (1992) Recognition of liposomes by cells: In vitro binding and endocytosis mediated by specific lipid headgroups and surface charge density. Biochim. Biophys. Acta 1103:185-197.
18. Moghimi, S. M. and Patel, H. M. (1988) Tissue specific opsonins for phagocytic cells and their different affinity for cholesterol-rich liposomes. FEBS Lett. 233:143-147.
19. Lee, K. D., Nir, S., and Papahadjopoulos, D. (1993) Quantitative analysis of liposome-cell interactions in vitro: Rate constants of binding and endocytosis with suspension and adherent J774 cells and human monocytes. Biochemistry 32:889-899.
20. Tyrell, D. A., Richardson, V. J., and Ryman, B. E. (1977) The effect of serum protein fractions on liposome-cell interactions in cultured cells and the perfused rat liver. Biochim. Biophys. Acta 497:469-480.
21. Kiwada, H., Miyajima, Y., and Kalto, Y. (1987) Studies on the uptake of mechanism of liposomes by perfused rat liver. II. An indispensable factor for liver uptake in serum. Chem. Pharm. Bull. 35:1189-1195.
22. Harashima, H., Sakata, K., Funato, K., and Kiwada, H. (1994) Enhanced hepatic uptake of liposomes through complement activation depending on the size of liposomes. Pharm. Res. 11:402-406.
23. Matsuo, H., Funato, K., Harashima, H., and Kiwada, H. (1994) The complement- but not mannose receptor-mediated phagocytosis is involved in hepatic uptake of cetylmannoside-modified liposomes in situ. J. Drug. Target. 2:141-146.
24. Liu, D., Hu, Q. G., and Song, Y. K. (1995) Liposome clearance from blood: Different animal species have different mechanisms. Biochim. Biophys. Acta 124:277-284.
25. M1. Pharm. Res. 12:1775-1780.
26. Harashima, H., Ohnishi, Y., and Kiwada, H. (1992) In vivo evaluation on the effect of the size and opsonization on the hepatic extraction of liposomes in rats: An application of Oldendorf method. Biopharm. Drug Disposit. 13:549-553.
27. Chonn, A., Semple, S. C., and Cullis, P. R. (1995) β2-glycoprotein I is a major protein associated with very rapidly cleared liposomes in vivo, suggesting a significant role in the immune clearance of "non-self" particles. J. Biol. Chem. 270:25845-25849.
28. Semple, A., Chonn, A., and Cullis, P. R. (1998) Interaction of liposomes and lipid-based carrier systems with blood proteins: Relation to clearance behavior in vivo. Adv. Drug Deliv. Rev. 32:3-13.
29. Nishikawa, K., Arai, H., and Inoue, K. (1990) Scavenger receptor-mediated uptake and metabolism of lipid vesicles containing acidic phospholipids by mouse peritoneal macrophages. J. Biol. Chem. 265:5226-5231.
30. Dijkstra, J., Van Galen, M., and Scherphof, G. L. (1984) Effects of ammonium chloride and chloroquine on endocytic uptake of liposomes by Kupffer cells in vitro. Biochem. Biophys. Acta 804:58-67.
31. Romero, E. L., Morilla, M. J., Regts, J., Koning, G. A., and Scherphof, G. L. (1999) On the mechanism of hepatic transendothelial passage of large liposomes. FEBS Lett. 448:193-196.
32. Scherphof, G. L., Daemen, T., Romero, E. L., and Kamps, J. A. A. M. (2000) Liposome elimination by non-phagocytic cells of the liver. J. Liposome Res. 10:431-442.
33. Allen, T. M. (1981) A study of phospholipid interactions between high-density lipoproteins and small unilamellar vesicles. Biochim. Biophys. Acta 640:385-397.
34. Senior, J., Gregoriadis, G., and Mitropoulos, K. (1983) Stability and clearance of small unilamellar liposomes: Studies with normal and lipoprotein-deficient mice. Biochim. Biophys. Acta 760:111-118.
35. Patel, H. M., Tuzel, N. S., and Ryman, B. E. (1983) Inhibitory effect of cholesterol on the uptake of liposomes by liver and spleen. Biochim. Biophys. Acta 761:142-151.
36. Wetterau, J. R. and Jonas, A. (1983) Factors affecting the size of complexes of dipalmitoylphosphatidylcholine with human apolipoprotein A-1. J. Biol. Chem. 258:2637-2643.
37. Klausner, R. D., Blumenthal, R., Innnerarity, T., and Weistein, J. N. The interaction of apolipoprotein A-1 with small unilamellar vesicles of L-alpha-dipalmitoylphosphatidylcholine. J. Biol. Chem. 260:13719-13727.
38. 14C]phosphatidylcholine between liposomes and human plasma high density lipoprotein: Partial purification of a transfer stimulating factor using a rapid transfer assay. Biochim. Biophys. Acta 712:444-452.
39. Damen, J., Dijkstra, J., Regts, J., and Scherphof, G. (1980) Effect of lipoprotein-free plasma on the interaction of human plasma high density lipoprotein with egg yolk phosphatidylcholine liposomes. Biochim. Biophys. Acta 620:90-99.
40. Scherphof, G. L. and Morselt, H. (1984) On the size-dependent disintegration of small unilamellar phosphatidylcholine vesicles in rat plasma: Evidence of complete loss of vesicle structure. Biochem. J. 221:423-429.
41. Shahrokh, Z. and Nichols, A. V. (1982) Particle size interconversion of human low-density lipoproteins during incubation of plasma with phosphatidylcholine vesicles. Biochim. Biophys. Res. Commun. 108:888-895.
42. Comiskey, S. J. and Heath, T. D. (1990) Serum-induced leakage of negatively charged liposomes at nanomolar lipid concentrations. Biochemistry 29:3626-3631.
43. Muller-Eberhard, H. J. (1986) The membrane attack complex of complement. Annu. Rev. Immunol. 4:503-528.
44. Malinsky, J. A. and Nelsestuen, G. L. (1989) Membrane permeability to macromolecules mediated by the membrane attack complex. Biochemistry 28:61-70.
45. Damen, J., Regts, J. and Scherphof, G. L. (1981) Transfer and exchange of phospholipid between small unilamellar liposomes and rat plasma high density lipoproteins: Dependence on cholesterol and phospholipid composition. Biochim. Biophys. Acta 665:538-545.
46. Hunt, C. A. (1982) Liposomes disposition in vivo. V. Liposomes stability in plasma and implications for drug carrier function. Biochim. Biophys. Acta 719:450-463.
47. Senior, J. and Gregoriadis, G. (1982) Is half-life of circulating liposomes determined by changes in their permeability? FEBS Lett. 145:109-114.
48. Gregoriadis, G. and Senior, J. (1980) The phospholipid component of small unilamellar liposomes controls the rate of clearance of entrapped solutes from the circulation. FEBS Lett. 119:43-46.
49. Kirby, J. and Gregoriadis, G. (1981) Plasma-induced release of solutes from small unilamellar liposomes is associated with pore formation in the bilayers. Biochem. J. 119:251-254.
50. Marjan, J., Xie, Z., and Devine, D. (1994) Liposome-induced activation of the classical complement pathway does not require immunoglobulin. Biochim. Biophys. Acta 1192:35-44.
51. Devine, D. V., Wong, K., Serrano, K., Chonn, A., and Cullis, P. R. (1994) Liposome-complement interactions in rat serum: Implications for liposome survival studies. Biochim. Biophys. Acta 1191:43-51.
52. Harashima, H., Huong, T. M., Ishida, T., Manabe, Y., Matsuo, H., and Kiwada, H. (1996) Synergistic effect between size and cholesterol content in the enhanced hepatic uptake clearance of liposomes through complement activation in rats. Pharm. Res. 13:1704-1709.
53. Dijkstra, J., Van Galen, W. J. M., Hulstaert, C. E., Kalicharan, D., Roedink, F. H., and Scherphof, G. L. (1984) Interaction of liposomes with Kupffer cells in vitro. Exp. Cell Res., 150:161-176.
54. Dijkstra, J., Van Galen, M., Regts, D., and Scherphof, G. (1985) Uptake and processing of liposomal phospholipids by Kupffer cells in vitro. Eur. J. Biochem. 148:391-397.
55. Huong, T. M., Harashima, H., and Kiwada, H. (1998) Complement dependent and independent liposome uptake be peritoneal macrophages: Cholesterol content dependency. Biol. Pharm. Bull. 21:969-973.
56. Harashima, H. and Kiwada, H. (1996) Studies on the mechanism of uptake of liposomes using an isolated perfused liver system. J. Liposome Res. 6:61-75.
57. Harashima, H., Matsuo, H., and Kiwada, H. (1998) Identification of proteins mediating clearance of liposomes using a liver perfusion system. Adv. Drug Deliv. 32:61-79.
58. Liu, D., Liu, F., and Song, Y. K. (1995) Recognition and clearance of liposomes containing phosphatidylserine are mediated by serum opsonin. Biochim. Biophys. Acta 1235:140-146.
59. Liu, F. and Liu, D. X. (1996) Serum independent liposome uptake by mouse liver. Biochim. Biophys. Acta 127:5-11.
60. Oja, C. D., Semple, S. C., Chonn, A., and Cullis, P. R. (1996) Influence of dose on liposome clearance: Critical role of blood proteins. Biochim. Biophys. Acta 1281:31-37.
61. Ishida, T., Funato, K., Kojima, S., Yoda, R., and Kiwada, H. (1997) Enhancing effect of cholesterol on the elimination of liposomes from circulation is mediated by complement activation. Int. J. Pharm. 156:27-37.
62. Ishida, T., Kojima, H., Harashima, H., and Kiwada, H. (2000) Biodistribution of liposomes and C3 fragments associated with liposomes: Evaluation of their relationship. Int. J. Pharm. 205:183-193.
63. Ishida, T., Yasukawa, K., Kojima, H., Harashima, H., and Kiwada, H. (2001) Effect of cholesterol content in activation of the classical versus the alternative pathway of rat complement system induced by hydrogenated egg phosphatidylcholine-based liposomes. Int. J. Pharm. 224:69-79.
64. Huong, T. M., Harashima, H., and Kiwada, H. (1999) In vivo studies on the role of complement in the clearance of liposomes in rats and guinea pigs. Biol. Pharm. Bull. 22:515-520.
65. Huong, T. M., Ishida, T., Harashima, H., and Kiwada, H. (2001) The complement system enhances the clearance of phosphatidylserine (PS)-liposomes in rat and guinea pig. Int. J. Pharm. 215:197-205.
66. Szebeni, J., Wassef, N. M., Spielberg, H., Rudolph, A. S., and Alving, C. R. (1994) Complement activation in rats by liposomes and liposomes-encapsulated hemoglobin: Evidence for anti-lipid antibodies and alternative pathway activation. Biochem. Biophys. Res. Commun. 205:255-263.
67. Cunningham, C. M., Kingzette, M., Richards, R. L., Alving, C. R., Lint, T. F., and Gewurz, H. (1979) Activation of human complement by liposomes: A model for membrane activation of the alternative pathway. J. Immunol. 122:1237-1242.
68. Volanakis, J. E. and Narkates, A. J. (1981) Interaction of C-reactive protein with artificial phosphatidylcholine bilayers and complement. J. Immunol. 126:1820-1825.
69. Richards, G. L., Gewurz, H., Siegel, J., and Alving, C. R. (1979) Interaction of CRP and complement with liposomes, II. Influence of membrane composition. J. Immunol. 122:1185-1189.
70. Scieszka, J. F., Maggiora, L. L., Wright, S. D., and Cho, M. J. (1991) Role of complements C3 and C5 in the phagocytosis of liposomes by human neutrophils. Pharm. Res. 8:65-69.
71. Wright, S. D. and Silverstwin, S. C. (1982) Tumor-promoting phorbol esters stimulate C3b and C3bi receptor-mediated phagocytosis in cultured human monocytes. J. Exp. Med. 156:1149-1164.
72. Matsuo, H., Yamashita, C., Akiyama, K., and Kiwada, H. (1995) Effect of cetylmannoside modification on the alternative complement pathway activation in rat serum. Biol. Pharm. Bull. 18:581-585.
73. M1 shortens the blood circulation time in rats. Pharm. Res. 12:508-512.
74. Allen, T. M. and Chonn, A. (1987) Large unilamellar liposomes with low uptake into the reticuloendothelial system. FEBS Lett. 223:42-46.
75. Harashima, H., Hiraiwa, T., Ochi, Y., and Kiwada, H. (1995) Size dependent liposome degradation in blood: In vivo/in vitro correlation by kinetic modeling. J. Drug Targeting 3:253-261.
76. Morgan, B. P. (1990) In: The Complement System. Academic Press, London, pp. 10-11.
77. Metzger, H. (1991) Fc receptors and membrane immunoglobulin. Curr. Opin. Immunol. 3:40-46.
78. Rossi, J. D. and Wallace, B. A. (1983) Binding of fibronectin to phospholipid vesicles. J. Biol. Chem. 258:3327-3331.
79. Water, L. D. V., Destree, A. T., and Hynes, R. O. (1983) Fibronectin binds to some bacteria but does not promote their uptake by phagocytic cells. Science 220:201-204.
80. Falcone, D. J. (1986) Fluorescent opsonization assay: Binding of plasma fibronectin to fibrinderivatized fluorescent particles does not change their uptake by macrophages. J. Leukocyte Biol. 39:1-12.
81. Murai, M., Aramki, Y., and Tsuchiya, S. (1995) Identification of the serum factor required for liposome primed activation of mouse peritoneal macrophages: Modified α2-macroglobulin enhances Fc gamma receptor mediated phagocytosis of opsonized sheep red blood cells. Immunology 86:64-70.
82. Reid, K. B. M. (1986) Activation and control of the complement system. Essays Biochem. 22:27-68.
83. Van de Winkel, J. G. J., and Capel, J. A. Overview: Fc receptors. Human IgG Fc receptor heterogeneity: Molecular aspects and clinical implications. Immunol. Today 14:215-221.
84. Yokota, A., et al. (1992) Two forms of the low-affinity Fc receptor for IgE differentially mediate endocytosis and phagocytosis: Identification of the critical cytoplasmic domains. Proc. Natl. Acad. Sci. USA 89:5030-5034.
85. Dewer, S. K., Titus, J. A., Delisi, L., and Segal, D. M. (1981) Mechanism of binding of multivalent immune complex to Fc receptors. Biochemistry 20:6335-6340.
86. Unkeless, J. C. (1989) Functional and heterogeneity of human Fc receptors for immunoglobulin G. J. Clin. Invest. 83:355-361.
87. Clarkson, S. B. et al. (1986) Blockade of clearance of immune complexes by an anti-Fc gamma receptor monoclonal antibody. J. Exp. Med. 164:474-489.
88. McNeil, H. P., Simpson, R. J., Chesterman, C. N., and Krilis, S. A. (1990) Anti-phospholipid antibodies are directed against a complex antigen that includes a lipid-binding inhibitor of coagulation: β2-glycoprotein I (apolipoprotein H). Proc. Natl. Acad. Sci. USA 87:4120-4124.
89. Van Oss, C. J., Gillman, C. F., Bronson, P. M., and Border, J. R. (1974) Phagocytosis-inhibiting properties of human serum α-1 acid glycoprotein. Immunol. Commun. 3:321-328.
90. Moghimi, S. M. and Patel, H. S. (1989) Serum opsonins and phagocytosis of saturated and unsaturated phospholipid liposomes. Biochim. Biophys. Acta 984:384-387.
91. Moghimi, S. M. and Patel, H. M. (1993) Serum factors that regulate phagocytosis of liposomes by Kupffer cells. Biochem. Soc. Trans. 21:128S.
92. Moghimi, S. M. and Patel, H. M. (1990) Calcium as a possible modulator or Kupffer cell phagocytic function by regulating liver-specific opsonic activity. Biochim. Biophys. Acta 1028:304-308.
93. Schwartz, R. S., Tanaka, Y., Fidler, I. J., Chiu, D., Lubin, B., and Schroit, A. J. (1985) Increased adherence of sickled and phosphatidylserine-enriched human erythrocytes to cultured human peripheral blood monocytes. J. Clin. Invest. 75:1965-1972.
94. Op den Kamp, J. A. F. (1979) Lipid asymmetry in membranes. Ann. Rev. Biochem. 48:47-71.
95. Lubin, B., Chiu, D., Bastacky, J., Roelofsen, B., and Van Deenen, L. L. M. (1981) Abnormalities in membrane phospholipid organization in sickled erythrocytes. J. Clin. Invest. 67:1643-1649.
96. Schroit, A. J., Madsen, J. W., and Tanaka, Y. (1985) In vivo recognition and clearance of red blood cells containing phosphatidylserine in their plasma membrane. J. Biol. Chem. 260:5131-5138.
97. Savil, J., Fadok, V., Henson, P., and Haslett, C. (1993) Phagocyte recognition of cells undergoing of cells undergoing apoptosis. Immunol. Today 14:131-136.
98. Tanaka, Y. and Schroit, A. J. (1983) Insertion of fluorescent phosphatidylserine into the plasma membrane of red blood cells: Recognition by autologous macrophages. J. Biol. Chem. 258:11335-11343.
99. Allen, T. M., Austin, G. A., Chonn, A., Lin, L., and Lee, K. C. C. (1991) Uptake of liposomes by cultured mouse bone marrow macrophages: Influence of liposome composition and size. Biochim. Biophys. Acta 1061:56-64.
100. Roerdink, R., Regts, J., Van Leeuwen, B., and Scherphof, G. (1984) Intrahepatic uptake and processing of intravenously injected small unilamellar phospholipid vesicles in rats. Biochim. Biophys. Acta 770:195-202.
101. Spanjer, H. H., Van Galen, M., Roerink, F. H., Regts, J., and Scherphof, G. L. (1986) Intrahepatic distribution of small unilamellar liposomes as a function of liposomal lipid composition. Biochim. Biophys. Acta 863:224-230.
102. Daemen, T. et al. (1997) Different intrahepatic distribution of phosphatidylglycerol and phosphatidylserine liposomes. Hepatology 26:416-423.
103. Greaves, D. R., Gough, P. J., and Gordon, S. (1998) Recent progress on defining the role of scavenger receptors in lipid transport, athreosclerosis and host defence. Curr. Opin Lipidol. 9:425-432.
104. Kodama, T., Doi, T., Suzuki, H., Takahashi, K., Wada, Y., and Gordon, S. (1996) Collagenous macrophages scavenger receptors. Curr. Opin. Lipidol. 7:287-291.
105. Krieger, M. and Herz, J. (1994) Structures and functions of multiligand lipoprotein receptors: Macrophage scavenger receptors LDL receptor-related protein (LRP). Annu. Rev. Biochem. 63:601-637.
106. da Silva, R. P., Platt, N., de Villiers, W. J. S., and Gordon, S. (1996) Membrane molecules and macrophage endocytosis: Scavenger receptor and macrosialin as markers of plasma-membrane and vacuolar functions. Biochim. Soc. Trans. 24:220-224.
107. Goldstein, J. L., Ho, Y. K., Basu, S. K., and Brown, M. S. (1979) Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc. Natl. Acad. Sci. USA 76:333-337.
108. Lee, K. D., Pitas, R. E., and Papahadjopoulos, D. (1992) Evidence that the scavenger receptor is not involved in the uptake of negatively charged liposomes by cells. Biochim. Biophys. Acta 1111:1-6.
109. Rigotti, A., Acton, S. L., and Krieger, M. (1995) The class B scavenger SR-B1 and CD-36 are receptors for anionic phospholipids. J. Biol. Chem. 270:16221-16224.
110. Acton, S. L., Scherer, P. E., Lodish, H. F., and Krieger, M. (1994) Expression cloning of SR-B1, a CD36 related class B scavenger receptor. J. Biol. Chem. 269:21003-21009.
111. Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J. J., Bratton, D. L., and Henson, P. M. (1992) Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148:2207-2216.
112. Woodle, M. and Lasic, D. (1992) Sterically stabilized liposomes. Biochim. Biophys. Acta. 1113:171-199.
113. Harashima, H., Komatsu, S., Kojima, S., Yanagi, C., Morioka, Y., Naito, M., and Kiwada, H. (1996) Species difference in the disposition of liposomes among mice, rats, and rabbits: Allomeric relationship and species dependent hepatic uptake mechanism. Pharm. Res. 13:1049-1054.
114. Abra, R. M. and Hunt, C. A. (1981) Liposome disposition in vivo. III. Dose and vesicle-size effects. Biochim. Biophys. Acta 666:493-503.
115. Dams, E. T. M. et al. (2000) Accelerated blood clearance and altered biodistribution of repeated injections of sterically stabilized liposomes. J. Pharm. Exp. Ther. 292:1071-1079.
116. Laverman, P. et al. (2001) Factors affecting the accelerated blood clearance of polyethylene glycolliposomes upon repeated injection. J. Pharm. Exp. Ther. 298:607-612.
117. Laverman, P., Carstens, M. G., Storm, G., and Moghimi, S. M. (2001) Recognition and clearance of methoxypoly(ethyleneglycol) 2000-grafted liposomes by macrophages with enhanced phagocytic capacity. Implications in experimental and clinical oncology. Biochim. Biophys. Acta 1526:227-229.
118. Liu, S., Ishida, T., and Kiwada, H. (1997) Effect of serum components from different species on destabilizing hydrogenated phosphatidylcholine-based liposomes. Biol. Pharm. Bull. 20:874-880.
119. Bradley, A. J., Devine, D. V., Ansell, S. M., Janzen, J., and Brooks, D. E. (1998) Inhibition of liposome-induced complement activation by incorporated poly(ethylene glycol)-lipods. Arch. Biochem. Biophys. 357:185-194.
120. Price, M. E., Cornelius, R. M., and Brash, J. L. (2001) Protein adsorption to polyethylene glycol modified liposomes from fibrinogen solution and from plasma. Biochim. Biophys. Acta 1512:191-205.