Activation of complement by therapeutic liposomes and other lipid excipient-based therapeutic products: Prediction and prevention

Advanced Drug Delivery Reviews

Volumn 63, Issue 12, 2011, Pages 1020-1030

  Szebeni, Janos ^a   Muggia, Franco ^b   Gabizon, Alberto ^c   Barenholz, Yechezkel ^d  

^a BAY ZOLTÁN NONPROFIT LTD FOR APPLIED RESEARCH   (Hungary)

^b NEW YORK UNIVERSITY   (United States)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Adverse drug effects; Allergy; Cancer chemotherapy; CARPA; Hypersensitivity reactions; Immune toxicity; Nanomedicines

Indexed keywords

CANCER CHEMOTHERAPY; CARPA; DRUG EFFECTS; HYPERSENSITIVITY REACTION; IMMUNE TOXICITY; NANOMEDICINES;

ALLERGIES; CHEMOTHERAPY; DRUG INTERACTIONS; DRUG PRODUCTS; LIPOSOMES; MEDICAL NANOTECHNOLOGY; SIGNAL TRANSDUCTION;

PHOSPHOLIPIDS;

ADRENALIN; ALBUMIN; AMPHOCYL; AMPHOTERICIN B CHOLESTEROL SULFATE; AMPHOTERICIN B LIPID COMPLEX; ANTIHISTAMINIC AGENT; ANTINEOPLASTIC AGENT; CARBOPLATIN; CISPLATIN; COMPLEMENT; CORTICOSTEROID; CREMOPHOR; DAUNORUBICIN; DIPALMITOYLPHOSPHATIDYLCHOLINE; DOXORUBICIN; EXCIPIENT; INDOMETACIN; LIPID; LIPOSOME; NANOPARTICLE; OXALIPLATIN; PACLITAXEL; UNCLASSIFIED DRUG; VERTEPORFIN;

ALLERGY; BREAST CANCER; C COMPLEMENT RELATED PSEUDOALLERGY; CANCER COMBINATION CHEMOTHERAPY; CARDIOPULMONARY INSUFFICIENCY; CLINICAL FEATURE; CLINICAL OBSERVATION; COMPLEMENT ACTIVATION; DISEASE COURSE; DISEASE SEVERITY; DRUG CROSS REACTIVITY; DRUG DELIVERY SYSTEM; DRUG HYPERSENSITIVITY; DRUG SAFETY; EFFECTOR CELL; HUMAN; IMMUNE DEFICIENCY; IMMUNOGENICITY; IMMUNOPATHOGENESIS; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; KAPOSI SARCOMA; MALIGNANT NEOPLASTIC DISEASE; MICELLE; MULTIPLE MYELOMA; MYCOSIS; NANOMEDICINE; NONHUMAN; OVARY CANCER; PATIENT SAFETY; PREDICTION; PREMEDICATION; PRIORITY JOURNAL; RETINA MACULA AGE RELATED DEGENERATION; REVIEW; SIDE EFFECT; SIGNAL TRANSDUCTION; SYMPTOM;

ANIMALS; ANTINEOPLASTIC AGENTS; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; DRUG HYPERSENSITIVITY; EXCIPIENTS; HUMANS; LIPIDS; LIPOSOMES;

EID: 80052174164     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2011.06.017     Document Type: Review

References (105)

1. Wagner V., Dullaart A., Bock A.-K., Zweck A. The emerging nanomedicine landscape. Nat. Biotechnol. 2006, 24:1211-1217.
2. Marcato P.D., Duran N. New aspects of nanopharmaceutical delivery systems. J. Nanosci. Nanotechnol. 2008, 8:1-14.
3. Venkatraman S.S., Ma L.L., Natarajan J.V., Chattopadhyay S. Polymer- and liposome-based nanoparticles in targeted drug delivery. Front. Biosci. (Schol. Ed.) 2010, 2:801-814.
4. Bangham A.D., Horne R.W. Negative staining of phospholipids and their structural modification by surface active agents as observed in the electron microscope. J. Mol. Biol. 1964, 8:660-668.
5. Haxby J.A., Kinsky C.B., Kinsky S.C. Immune response of a liposomal model membrane. Proc. Natl. Acad. Sci. USA 1968, 61:300-307.
6. Haxby J.A., Gotze O., Muller-Eberhard H.J., Kinsky S.C. Release of trapped marker from liposomes by the action of purified complement components. Proc. Natl. Acad. Sci. USA 1969, 64:290-295.
7. Kinsky S.C., Haxby J.A., Zopf D.A., Alving C.R., Kinsky C.B. Complement-dependent damage to liposomes prepared from pure lipids and Forssman hapten. Biochemistry 1969, 8:4149-4158.
8. Alving C.R., Kinsky S.C., Haxby J.A., Kinsky C.B. Antibody binding and complement fixation by a liposomal model membrane. Biochemistry 1969, 8:1582-1587.
9. Gregoriadis G., Allison A.C. Entrapment of proteins in liposomes prevents allergic reactions in pre-immunised mice. FEBS Lett. 1974, 45:71-74.
10. Alving C.R. Liposomal vaccines: clinical status and immunological presentation for humoral and cellular immunity. Ann. N. Y. Acad. Sci. 1995, 754:143-152.
11. Szebeni J., Fontana J.L., Wassef N.M., Mongan P.D., Morse D.S., Dobbins D.E., Stahl G.L., Bünger R., Alving C.R. Hemodynamic changes induced by liposomes and liposome-encapsulated hemoglobin in pigs: a model for pseudo-allergic cardiopulmonary reactions to liposomes. Role of complement and inhibition by soluble CR1 and anti-C5a antibody. Circulation 1999, 99:2302-2309.
12. Szebeni J. Complement activation-related pseudoallergy: a new class of drug-induced immune toxicity. Toxicology 2005, 216:106-121.
13. Szebeni J., Muggia F.M., Alving C.R. Complement activation by Cremophor EL as a possible contributor to hypersensitivity to paclitaxel: an in vitro study. J. Natl. Cancer Inst. 1998, 90:300-306.
14. Szebeni J., Alving C.R., Savay S., Barenholz Y., Priev A., Danino D., Talmon Y. Formation of complement-activating particles in aqueous solutions of Taxol: possible role in hypersensitivity reactions. Int. Immunopharm. 2001, 1:721-735.
15. Moghimi S.M., Hunter C., Dadswell C.M., Savay S., Alving C., Szebeni J. Causative factors behind poloxamer 188 (Pluronic F68, Flocor trade mark)-induced complement activation in human sera; A protective role against poloxamer-mediated complement activation by elevated serum lipoprotein levels. Biochim. Biophys Acta 2004, 1689:103-113.
16. Hamad I., Hunter A.C., Szebeni J., Moghimi S.M. Poly(ethylene glycol)s generate complement activation products in human serum through increased alternative pathway turnover and a MASP-2-dependent process. Mol. Immunol. 2008, 46:225-232.
17. Hamad I., Al-Hanbali O., Hunter A.C., Rutt K.J., Andresen T.L., Moghimi S.M. Distinct polymer architecture mediates switching of complement activation pathways at the nanosphere-serum interface: implications for stealth nanoparticle engineering. ACS Nano 2010, 4:6629-6638.
18. Moghimi S.M., Andersen A.J., Hashem S.H., Lettiero B., Ahmadvand D., Hunter A.C., Andresen T.L., Hamad I., Szebeni J. Complement activation cascade triggered by PEG-PL engineered nanomedicines and carbon nanotubes: the challenges ahead. J. Control. Release 2010, 146:175-181.
19. Deamer D.W. Origins of life: how leaky were primitive cells?. Nature 2008, 454(7200):37-38.
20. Deamer D.W. On the origin of systems. Systems biology, synthetic biology and the origin of life. EMBO Rep. 2009, 10(Suppl. 1):S1-S4.
21. Ciftcioglu N., McKay D.S., Mathew G., Kajander E.O. Nanobacteria: fact or fiction? Characteristics, detection, and medical importance of novel self-replicating, calcifying nanoparticles. J Invest. Med. 2006, 2(54):385-394.
22. Sculier J.P., Coune A., Brassinne C., Laduron C., Atassi G., Ruysschaert J.M., Fruhling J. Intravenous infusion of high doses of liposomes containing NSC 251635, a water-insoluble cytostatic agent. A pilot study with pharmacokinetic data. J. Clin. Oncol. 1986, 4:789-797.
23. de Marie S. Liposomal and lipid-based formulations of amphotericin B. Leukemia 1996, 10(Suppl. 2):S93-S96.
24. Cabriales S., Bresnahan J., Testa D., Espina B.M., Scadden D.T., Ross M., Gill P.S. Extravasation of liposomal daunorubicin in patients with AIDS-associated Kaposi's sarcoma: a report of four cases [see comments]. Oncol. Nurs. Forum 1998, 25:67-70.
25. Eckardt J.R., Campbell E., Burris H.A., Weiss G.R., Rodriguez G.I., Fields S.M., Thurman A.M., Peacock N.W., Cobb P., Rothenberg M.L., et al. A phase II trial of DaunoXome, liposome-encapsulated daunorubicin, in patients with metastatic adenocarcinoma of the colon. Am. J. Clin. Oncol. 1994, 17:498-501.
26. Fossa S.D., Aass N., Paro G. A phase II study of DaunoXome in advanced urothelial transitional cell carcinoma. Eur. J. Cancer 1998, 34:1131-1132.
27. Gill P.S., Espina B.M., Muggia F., Cabriales S., Tulpule A., Esplin J.A., Liebman H.A., Forssen E., Ross M.E., Levine A.M. Phase I/II clinical and pharmacokinetic evaluation of liposomal daunorubicin. J. Clin. Oncol. 1995, 13:996-1003.
28. Gill P.S., Wernz J., Scadden D.T., Cohen P., Mukwaya G.M., von Roenn J.H., Jacobs M., Kempin S., Silverberg I., Gonzales G., Rarick M.U., Myers A.M., Shepherd F., Sawka C., Pike M.C., Ross M.E. Randomized phase III trial of liposomal daunorubicin versus doxorubicin, bleomycin, and vincristine in AIDS-related Kaposi's sarcoma. J. Clin. Oncol. 1996, 14:2353-2364.
29. Girard P.M., Bouchaud O., Goetschel A., Mukwaya G., Eestermans G., Ross M., Rozenbaum W., Saimot A.G. Phase II study of liposomal encapsulated daunorubicin in the treatment of AIDS-associated mucocutaneous Kaposi's sarcoma. AIDS 1996, 10:753-757.
30. Guaglianone P., Chan K., DelaFlor-Weiss E., Hanisch R., Jeffers S., Sharma D., Muggia F. Phase I and pharmacologic study of liposomal daunorubicin (DaunoXome). Invest. New Drugs 1994, 12:103-110.
31. Money-Kyrle J.F., Bates F., Ready J., Gazzard B.G., Phillips R.H., Boag F.C. Liposomal daunorubicin in advanced Kaposi's sarcoma: a phase II study. Clin. Oncol. (R. Coll. Radiol.) 1993, 5:367-371.
32. Richardson D.S., Kelsey S.M., Johnson S.A., Tighe M., Cavenagh J.D., Newland A.C. Early evaluation of liposomal daunorubicin (DaunoXome, Nexstar) in the treatment of relapsed and refractory lymphoma. Invest. New Drugs 1997, 15:247-253.
33. O'Dwyer P.J., Weiss R. Hypersensitivity reactions induced by etoposide. Cancer Treat. Rep. 1984, 68:959-961.
34. Greenberger P.A. Contrast media reactions. J Allergy Clin. Immunol. 1984, 74:600-605.
35. Frick O.L. Immediate hypersensitivity. Basic & Clinical Immunology 1987, 197-228. Appleton & Lange, Norwalk, CT. D.P. Stites, J.D. Stobo, J.W. Wells (Eds.).
36. Donehower R.C., Rowinsky E.K., Grochow L.B., Longnecker S.M., Ettinger D.S. Phase I trial of taxol in patients with advanced cancer. Cancer Treat. Rep. 1987, 71:1171-1177.
37. Weiss R.B., Baker J.R.J. Hypersensitivity reactions from antineoplastic agents. Cancer Metastasis Rev. 1987, 6:413-432.
38. Simpson J.K., Miller R.F., Spittle M.F. Liposomal doxorubicin for treatment of AIDS-related Kaposi's sarcoma. Clin. Oncol. (R. Coll. Radiol.) 1993, 5:372-374.
39. Gabizon A., Isacson R., Libson E., Kaufman B., Uziely B., Catane R., Ben-Dor C.G., Rabello E., Cass Y., Peretz T., et al. Clinical studies of liposome-encapsulated doxorubicin. Acta Oncol. 1994, 33:779-786.
40. Uziely B., Jeffers S., Isacson R., Kutsch K., Wei-Tsao D., Yehoshua Z., Libson E., Muggia F.M., Gabizon A. Liposomal doxorubicin: antitumor activity and unique toxicities during two complementary phase I studies. J. Clin. Oncol. 1995, 13:1777-1785.
41. Dezube B.J. Safety assessment: DoxilR (Doxorubicin HCl liposome injection) in refractory AIDS-related Kaposi's sarcoma. Doxil Clinical Series 1996, 1-8. Gardiner-Caldwell SynerMed, Califon, NJ.
42. Skubitz K.M., Skubitz A.P. Mechanism of transient dyspnea induced by pegylated-liposomal doxorubicin (Doxil). Anticancer Drugs 1998, 9:45-50.
43. Lyass O., Hubert A., Gabizon A.A. Phase I study of doxil-cisplatin combination chemotherapy in patients with advanced malignancies. Clin. Cancer Res. 2001, 7:3040-3046.
44. Onetto N., Canetta R., Winograd B., Catane R., Dougan M., Grechko J., Burroughs J., Rozencweig M. Overview of Taxol safety. J. Natl. Cancer Inst. Monogr. 1993, 131-139.
45. Guchelaar H.J., ten Napel C.H., de Vries E.G., Mulder N.H. Clinical, toxicological and pharmaceutical aspects of the antineoplastic drug taxol: a review. Clin. Oncol. 1994, 6:40-48.
46. Olson J., Sood A., Sorosky J., Anderson B., Buller R.E. Taxol hypersensitivity: rapid retreatment is safe and cost effective. Gynecol. Oncol. 1998, 68:25-28.
47. Szebeni J., Baranyi L., Sávay S., Bodó M., Milosevits J., Alving C.R., Bünger R. 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. 2006, 290:H1050-H1058.
48. Szebeni J. The interaction of liposomes with the complement system. Crit. Rev. Ther. Drug Carrier Syst. 1998, 15:57-88.
49. Szebeni J. Complement activation-related pseudoallergy caused by liposomes, micellar carriers of intravenous drugs and radiocontrast agents. Crit. Rev. Ther. Drug Carrier Syst. 2001, 18:567-606.
50. Szebeni J. Complement activation-related pseudoallergy: mechanism of anaphylactoid reactions to drug carriers and radiocontrast agents. The Complement System: Novel Roles in Health and Disease 2004, 399-440. Kluwer, Boston, pp. 399-440. J. Szebeni (Ed.).
51. Ozato K., Ziegler H.K., Henney C.S. Liposomes as model membrane systems for immune attack. II. The interaction of complement and K cell populations with immobilized liposomes. J. Immunol. 1978, 121:1383-1388.
52. Cunningham C.M., Kingzette M., Richards R.L., Alving C.R., Lint T.F., Gewurz H. Activation of human complement by liposomes: a model for membrane activation of the alternative pathway. J. Immunol. 1979, 122:1237-1242.
53. Alving C.R., Urban K.A., Richards R.L. Influence of temperature on complement-dependent immune damage to liposomes. Biochim. Biophys. Acta 1980, 600:117-125.
54. Mold C., Gewurz H. Activation of human complement by liposomes: serum factor requirement for alternative pathway activation. J. Immunol. 1980, 5:696-700.
55. Hashimoto Y., Sugawara M., Endoh H. Coating of liposomes with subunits of monoclonal IgM antibody and targeting of the liposomes. J. Immunol. Methods 1983, 62:155-162.
56. Okada N., Yasuda T., Tsumita T., Okada H. Membrane sialoglycolipids regulate the activation of alternative complement pathway by liposomes containing trinitrophenylaminocaproyldipalmitoylphosphatidylethaolamine. Immunology 1983, 48:129-140.
57. Richards R.L., Habbersett R.C., Scher I., Janoff A.S., Schieren H.P., Mayer L.D., Cullis P.R., Alving C.R. Influence of vesicle size on complement-dependent immune damage to liposomes. Biochim. Biophys. Acta 1986, 855:223-230.
58. Bonte F., Juliano R.L. Interactions of liposomes with serum proteins. Chem. Phys. Lipids 1986, 40:359-372.
59. Masaki T., Okada N., Yasuda R., Okada H. Assay of complement activity in human serum using large unilamellar liposomes. J. Immunol. Methods 1989, 123:19-24.
60. Chonn A., Cullis P.R., Devine D.V. The role of surface charge in the activation of the classical and alternative pathways of complement by liposomes. J. Immunol. 1991, 146:4234-4241.
61. Funato K., Yoda R., Kiwada H. Contribution of complement system on destabilization of liposomes composed of hydrogenated egg phosphatidylcholine in rat fresh plasma. Biochim. Biophys. Acta 1992, 1103:198-204.
62. Harashima H., Sakata K., Funato K., Kiwada H. Enhanced hepatic uptake of liposomes through complement activation depending on the size of liposomes. Pharm. Res. 1994, 11:402-406.
63. Szebeni J., Wassef N.M., Hartman K.R., Rudolph A.S., Alving C.R. Complement activation in vitro by the red blood cell substitute, liposome-encapsulated hemoglobin: mechanism of activation and inhibition by soluble complement receptor type 1. Transfusion 1997, 37:150-159.
64. Szebeni J., Baranyi B., Savay S., Bodo M., Morse D.S., Basta M., Stahl G.L., Bunger R., Alving C.R. Liposome-induced pulmonary hypertension: properties and mechanism of a complement-mediated pseudoallergic reaction. Am. J. Physiol. 2000, 279:H1319-H1328.
65. Szebeni J., Bunger R., Baranyi L., Bedocs P., Toth M., Rosivall L., Barenholz Y., Alving C.R. Animal models of complement-mediated hypersensitivity reactions to liposomes and other lipid-based nanoparticles. J. Liposome Res. 2007, 17:107-117.
66. Matsumura Y., Gotoh M., Muro K., Yamada Y., Shirao K., Shimada Y., Okuwa M., Matsumoto S., Miyata Y., Ohkura H., Chin K., Baba S., Yamao T., Kannami A., Takamatsu Y., Ito K., Takahashi K. Phase I and pharmacokinetic study of MCC-465, a doxorubicin (DXR) encapsulated in PEG immunoliposome, in patients with metastatic stomach cancer. Ann. Oncol. 2004, 15:517-525.
67. Szebeni J., Baranyi L., Savay S., Milosevits J., Bodo M., Bunger R., Alving C.R. The interaction of liposomes with the complement system: in vitro and in vivo assays. Methods Enzymol. 2003, 373:136-154.
68. Moghimi S.M., Hamad I., Andresen T.L., Jörgensen 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.
69. Sou K., Tsuchida E. Electrostatic interactions and complement activation on the surface of phospholipid vesicle containing acidic lipids: effect of the structure of acidic groups. Biochim. Biophys. Acta 2008, 1778:1035-1041.
70. J. Szebeni, P. Bedocs, Z. Rozsnyay, Z. Weiszhár, L. Rosivall, R. Cohen, O. Garbuzenko, G. Báthori, M. Tóth, R. Bünger, and Y. Barenholz, Liposome-induced complement activation and related cardiopulmonary distress in pigs: factors promoting reactogenicity of Doxil and Ambisome. Nanomedicine: Nanotechnol, Biol, Med. in press.
71. Pedersen M.B., Zhou X., Larsen E.K.U., Sorensen U.S., Kjems J., Nygaard J.V., Nyengaard J.R., Meyer R.L., Boesen T., Vorup-Jensen T. Curvature of synthetic and natural surfaces is an important target feature in classical pathway complement activation. J. Immunol. 2010, 184:1931-1945.
72. Kopf M., Herren S., Wiles M.V., Pepys M.B., Kosco-Vilbois M.H. Interleukin 6 influences germinal center development and antibody production via a contribution of C3 complement component. J. Exp. Med. 1998, 188:1895-1906.
73. Krohn C.D., Reiker s O., Mollnes T.E., Aasen A.O. Complement activation and release of interleukin-6 and tumour necrosis factor-alpha in drained and systemic blood after major orthopaedic surgery. Eur. J. Surg. 1998, 164:103-108.
74. Szebeni J., Baranyi B., Savay S., Lutz L.U., Jelezarova E., Bunger R., Alving C.R. The role of complement activation in hypersensitivity to pegylated liposomal doxorubicin (Doxil®). J. Liposome Res. 2000, 10:347-361.
75. Small P., Satin R., Palayew M.J., Hyams B. Prophylactic antihistamines in the management of radiographic contrast reactions. Clin. Allergy 1982, 12:289-294.
76. Chanan-Khan A., Szebeni J., Savay S., Liebes L., Rafique N.M., Alving C.R., Muggia F.M. Complement activation following first exposure to PEGylated liposomal doxorubicin (Doxil): possible role in hypersensitivity reactions. Ann. Oncol. 2003, 14:1430-1437.
77. Walsh T.J., Finberg R.W., Arndt C., Hiemenz J., Schwartz C., Bodensteiner D., Pappas P., Seibel N., Greenberg R.N., Dummer S., Schuster M., Holcenberg J.S. Liposomal amphotericin B for empirical therapy in patients with persistent fever and neutropenia. N. Engl. J. Med. 1999, 340:764-771.
78. Savay S., Szebeni J., Baranyi L., Alving C.R. Potentiation of liposome-induced complement activation by surface-bound albumin. Biochim. Biophys. Acta 2002, 1559:79-86.
79. Buyon J.P., Tamerius J., Belmont H.M., Abramson S.B. Assessment of disease activity and impending flare in patients with systemic lupus erythematosus. Comparison of the use of complement split products and conventional measurements of complement. Arthritis Rheum. 1992, 35:1028-1037.
80. Gabizon A.A., Muggia F.M. Initial clinical evaluation of PEGylated liposomal doxorubicin in solid tumors. Long-Circulating Liposomes: Old Drugs, New Therapeutics 1998, 155-174. Landes Bioscience, Austin, TX. M.C. Woodle, S. G. (Eds.).
81. Lenz H.J. Management and preparedness for infusion and hypersensitivity reactions. Oncologist 2007, 12:601-609.
82. Peereboom D.M., Donehower R.C., Eisenhauer E.A., McGuire W.P., Onetto N., Hubbard J.L., Piccart M., Gianni L., Rowinsky E.K. Successful re-treatment with Taxol after major hypersensitivity reactions. J. Clin. Oncol. 1993, 11:885-890.
83. Arbuck S.G., Christian M.C., Fisherman J.S., Cazenave L.A., Sarosy G., Suffness M., Adams J., Canetta R., Cole K.E., Friedman M.A. Clinical development of Taxol. J. Natl. Cancer Inst. Monogr. 1993, 11-24.
84. Rowinsky E.K., Eisenhauer E.A., Chaudhry V., Arbuck S.G., Donehower R.C. Clinical toxicities encountered with paclitaxel (Taxol). Semin. Oncol. 1993, 20:1-15.
85. Spriggs D.R., Tondini C. Taxol administered as a 120 hour infusion. Invest. New Drugs 1992, 10:275-278.
86. Weiss R.B., Donehower R.C., Wiernik P.H., Ohnuma T., Gralla R.J., Trump D.L., Baker J.R., VanEcho D.A., VonHoff D.D., Leyland-Jones B. Hypersensitivity reactions from Taxol. J. Clin. Oncol. 1990, 8:1263-1268.
87. Rosell R., Gonzlez-Larriba J.L., Alberola V., Molina F., Monz ̌ M., Benito D., P,rez J.M., de Anta J.M. Single-agent paclitaxel by 3-hour infusion in the treatment of non-small cell lung cancer: links between p53 and K-ras gene status and chemosensitivity. Semin. Oncol. 1995, 22:12-18.
88. Kris M.G., O'Connell J.P., Gralla R.J. A phase I trial of Taxol given as 3-hour infusions every 21days. Cancer Treat. Rep. 1986, 70:605-607.
89. Schiller J.H., Storer B., Tutsch K., Arzoomanian R., Alberti D., Feierabend C., Spriggs D. A phase I trial of 3-hour infusions of paclitaxel (Taxol) with or without granulocyte colony-stimulating factor. Semin. Oncol. 1994, 21:9-14.
90. Alberts D.S., Liu P.Y., Wilczynski S.P., Clouser M.C., Lopez M.A., Michelin D.P., Lanzotti V.J., Markman M. Randomized trial of PEGylated liposomal doxorubicin (PLD) plus carboplatin versus carboplatin in platinum-sensitive (PS) patients with recurrent ovarian or peritoneal carcinoma after failure of initial platinum-based chemotherapy (South West Oncology group protocol SO200). Gynecol. Oncol. 2008, 108:90-94.
91. Joly F., Ray-Coquard I., Fabbro M., Donoghoe M., Boman K., Sugimoto A., Vaughan M., Reinthaller A., Vergote I., Ferrandina G., Dell'anna T., Huober J., Pujade-Lauraine E. Gynecol. Oncol. 2011, 122:226-232.
92. Gabizon A., Isacson R., Rosengarten O., Tzemach D., Shmeeda H., Sapir R. An open-label study to evaluate dose and cycle dependence of the pharmacokinetics of pegylated liposomal doxorubicin. Cancer Chemother. Pharmacol. 2008, 61:695-702.
93. Harris C.L., Morgan B.P. The many faces of the membrane regulators of complement. The Complement System: Novel Roles in Health and Disease 2004, Kluwer, Boston. J. Szebeni (Ed.).
94. Szebeni J., Barenholz Y. Complement activation, immunogenicity and immune suppression as potential side effects of liposomes. Harnessing Biomaterials for Nanomedicine: Preparation, Toxicity and Applications 2011, Pan Stanford Publishing Pte Ltd. D. Peer (Ed.).
95. Epstein-Barash H., Gutman D., Markovsky E., Mishan-Eisenberg G., Koroukhov N., Szebeni J., Golomb G. Physicochemical parameters affecting liposomal bisphosphonates bioactivity for restenosis therapy: internalization, cell inhibition, activation of cytokines and complement, and mechanism of cell death. J. Control. Release 2010, 146:182-195.
96. Bergers J.J., Otter W.D., Crommelin J.A. Liposome-based cancer vaccines. J. Liposome Res. 1996, 6:339-355.
97. Altina J.G., Parish C.R. Liposomal vaccines-targeting the delivery of antigen. Methods 2006, 40:39-52.
98. Dams E.T., Laverman P., Oyen W.J., Storm G., Scherphof G.L., van Der Meer J.W., Corstens F.H., Boerman O.C. Accelerated blood clearance and altered biodistribution of repeated injections of sterically stabilized liposomes. J. Pharmacol. Exp. Ther. 2000, 292:1071-1079.
99. Ishida T., Kiwada H. Accelerated blood clearance (ABC) phenomenon upon repeated injection of PEGylated liposomes. Int. J. Pharmacol. 2008, 354:56-62.
100. Koide H., Asai T., Hatanaka K., Akai S., Ishii T., Kenjo E., Ishida T., Kiwada H., Tsukada H., Oku N. T cell-independent B cell response is responsible for ABC phenomenon induced by repeated injection of PEGylated liposomes. Int. J. Pharm. 2010, 392:218-223.
101. Ishihara T., Takeda M., Sakamoto H., Kimoto A., Kobayashi C., Takasaki N., Yuki K., Tanaka K., 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. 2009, 10:2270-2279.
102. Daemen T., Hofstede G., Ten Kate M.T., Bakker-Woudenberg I.A., Scherphof G.L. Liposomal doxorubicin-induced toxicity: depletion and impairment of phagocytic activity of liver macrophages. Int. J. Cancer 1995, 61:716-721.
103. Storm G., ten Kate M.T., Working P.K., Bakker-Woudenberg A. Doxorubicin entrapped in sterically stabilized liposomes: effects on bacterial blood clearance capacity of the mononuclear phagocyte system. Clin. Cancer Res. 1998, 4:111.
104. Romberg B., Metselaar J.M., Baranyi L., Snel C.J., Bunger R., Hennink W.E., Szebeni J., Storm G. Poly (amino acid)s: promising enzymatically degradable stealth coatings for liposomes. Int. J. Pharm. 2007, 331:186-189.
105. van Rooijen N. Liposomes for targeting of antigens and drugs: immunoadjuvant activity and liposome-mediated depletion of macrophages. J. Drug Target 2008, 16:529-534.