Challenges in development of targeted liposomal therapeutics

AAPS Journal

Volumn 14, Issue 2, 2012, Pages 303-315

  Sawant, Rupa R ^a   Torchilin, Vladimir P ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Active targeting; Immunoliposomes; Passive targeting; Stimuli sensitive; Targeted liposomes

Indexed keywords

ANTIBODY; CISPLATIN; CYTARABINE; DOXORUBICIN; EPIRUBICIN; FOLIC ACID; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOLIPOSOME; LIPOSOME; MACROGOL DERIVATIVE; MONOCLONAL ANTIBODY; NANOCARRIER; NAVELBINE; NUCLEIC ACID; PACLITAXEL; PEPTIDE; PHOSPHOLIPID; POLYMER; TRANSFERRIN; TRASTUZUMAB; VINCRISTINE;

ANTIBODY SPECIFICITY; BIOACCUMULATION; BIOCOMPATIBILITY; BIODEGRADABILITY; BIOLOGICAL ACTIVITY; BRAIN TUMOR; CANCER CELL; CANCER RESISTANCE; CHEMICAL MODIFICATION; CHEMOSENSITIVITY; DERIVATIZATION; DRUG BIOAVAILABILITY; DRUG CHOICE; DRUG CLEARANCE; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG DEVELOPMENT; DRUG DISTRIBUTION; DRUG FORMULATION; DRUG TARGETING; ENCAPSULATION; HUMAN; HYDROPHOBICITY; LIPID COMPOSITION; MULTIDRUG RESISTANCE; NONHUMAN; PHYSICAL CHEMISTRY; REVIEW; SURFACE PROPERTY; TARGET CELL;

ANIMALS; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; DRUG DISCOVERY; HUMANS; LIPOSOMES; PHARMACEUTICAL PREPARATIONS;

EID: 84860774962     PISSN: 15507416     EISSN: None     Source Type: Journal    
DOI: 10.1208/s12248-012-9330-0     Document Type: Review

References (149)

1. Torchilin VP. Drug targeting. Eur J Pharm Sci. 2000;11 Suppl 2: S81-91.
2. Lasic DD. Liposomes: from physics to applications. Amsterdam: Elsevier; 1993.
3. Klibanov AL, Maruyama K, Torchilin VP, Huang L. Amphi-pathic polyethyleneglycols effectively prolong the circulation time of liposomes. FEBS Lett. 1990;268(1):235-7. (Pubitemid 20233874)
4. Maeda H, Wu J, Sawa T, Matsumura Y, Hori K. Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Control Release. 2000;65(1-2):271-84. (Pubitemid 30122932)
5. Maeda H. Enhanced permeability and retention (EPR) effect: basis for drug targeting to tumors. In: Muzykantov V, Torchilin VP, editors. Biomedical aspects of drug targeting. Boston, MA: Kluwer; 2003. p. 211-28.
6. Torchilin V. Tumor delivery of macromolecular drugs based on the EPR effect. Adv Drug Deliv Rev. 2011;63(3):131-5.
7. Blume G, Cevc G. Molecular mechanism of the lipid vesicle longevity in vivo. Biochim Biophys Acta. 1993;1146(2):157-68. (Pubitemid 23084758)
8. Connor J, Huang L. pH-sensitive immunoliposomes as an efficient and target-specific carrier for antitumor drugs. Cancer Res. 1986;46(7):3431-5. (Pubitemid 16096885)
9. Torchilin VP, Klibanov AL, Huang L, O'Donnell S, Nossiff ND, Khaw BA. Targeted accumulation of polyethylene glycol-coated immunoliposomes in infarcted rabbit myocardium. FASEB J. 1992;6(9):2716-9.
10. Abra RM, Bankert RB, Chen F, Egilmez NK, Huang K, Saville R, et al. The next generation of liposome delivery systems: recent experience with tumor-targeted, sterically-stabilized immunoliposomes and active-loading gradients. J Liposome Res. 2002;12(1-2):1-3. (Pubitemid 34846950)
11. Ishida T, Kirchmeier MJ, Moase EH, Zalipsky S, Allen TM. Targeted delivery and triggered release of liposomal doxorubicin enhances cytotoxicity against human B lymphoma cells. Biochim Biophys Acta. 2001;1515(2):144-58. (Pubitemid 33086831)
12. Kale AA, Torchilin VP. Enhanced transfection of tumor cells in vivo using "Smart" pH-sensitive TAT-modified pegylated liposomes. J Drug Target. 2007;15(7-8):538-45. (Pubitemid 47209054)
13. Drummond DC, Zignani M, Leroux J. Current status of pH-sensitive liposomes in drug delivery. Prog Lipid Res. 2000;39 (5):409-60.
14. Ponce AM, Vujaskovic Z, Yuan F, Needham D, Dewhirst MW. Hyperthermia mediated liposomal drug delivery. Int J Hyperthermia. 2006;22(3):205-13. (Pubitemid 43878680)
15. Yatvin MB, Weinstein JN, Dennis WH, Blumenthal R. Design of liposomes for enhanced local release of drugs by hyperthermia. Science. 1978;202(4374):1290- 3. (Pubitemid 9154441)
16. Sabate R, Barnadas-Rodriguez R, Callejas-Fernandez J, Hidalgo-Alvarez R, Estelrich J. Preparation and characterization of extruded magnetoliposomes. Int J Pharm. 2008;347(1-2):156-62. (Pubitemid 350180325)
17. Fortin-Ripoche JP, Martina MS, Gazeau F, Menager C, Wilhelm C, Bacri JC, et al. Magnetic targeting of magnetoliposomes to solid tumors with MR imaging monitoring in mice: feasibility. Radiology. 2006;239(2):415-24.
18. West KR, Otto S. Reversible covalent chemistry in drug delivery. Curr Drug Discov Technol. 2005;2(3):123-60. (Pubitemid 41242960)
19. Hobbs SK, Monsky WL, Yuan F, Roberts WG, Griffith L, Torchilin VP, et al. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc Natl Acad Sci USA. 1998;95(8):4607-12. (Pubitemid 28207960)
20. Jain RK. Transport of molecules, particles, and cells in solid tumors. Annu Rev Biomed Eng. 1999;1:241-63. (Pubitemid 129740012)
21. Huang SK, Mayhew E, Gilani S, Lasic DD, Martin FJ, Papahadjopoulos D. Pharmacokinetics and therapeutics of sterically stabilized liposomes in mice bearing C-26 colon carcinoma. Cancer Res. 1992;52(24):6774-81. (Pubitemid 23006277)
22. Yuan F, Leunig M, Huang SK, Berk DA, Papahadjopoulos D, Jain RK. Microvascular permeability and interstitial penetration of sterically stabilized (stealth) liposomes in a human tumor xenograft. Cancer Res. 1994;54(13):3352-6. (Pubitemid 24225946)
23. Jain RK. Delivery of novel therapeutic agents in tumors: physiological barriers and strategies. J Natl Cancer Inst. 1989;81(8):570-6. (Pubitemid 19104487)
24. Gabizon A, Chemla M, Tzemach D, Horowitz AT, Goren D. Liposome longevity and stability in circulation: effects on the in vivo delivery to tumors and therapeutic efficacy of encapsulated anthracyclines. J Drug Target. 1996;3(5):391-8. (Pubitemid 26059827)
25. Yuan F, Dellian M, Fukumura D, Leunig M, Berk DA, Torchilin VP, et al. Vascular permeability in a human tumor xenograft: molecular size dependence and cutoff size. Cancer Res. 1995;55 (17):3752-6.
26. Torchilin VP. Recent advances with liposomes as pharmaceutical carriers. Nat Rev Drug Discov. 2005;4(2):145-60. (Pubitemid 40282557)
27. Gabizon A, Dagan A, Goren D, Barenholz Y, Fuks Z. Liposomes as in vivo carriers of adriamycin: reduced cardiac uptake and preserved antitumor activity in mice. Cancer Res. 1982;42(11):4734-9. (Pubitemid 13205982)
28. Gabizon AA. Liposomal anthracyclines. Hematol Oncol Clin North Am. 1994;8(2):431-50. (Pubitemid 24126182)
29. Gabizon A, Chisin R, Amselem S, Druckmann S, Cohen R, Goren D, et al. Pharmacokinetic and imaging studies in patients receiving a formulation of liposome-associated adriamycin. Br J Cancer. 1991;64(6):1125-32.
30. Liu D, Hu Q, Song YK. Liposome clearance from blood: different animal species have different mechanisms. Biochim Biophys Acta. 1995;1240(2):277-84. (Pubitemid 26004752)
31. Proffitt RT, Williams LE, Presant CA, Tin GW, Uliana JA, Gamble RC, et al. Tumor-imaging potential of liposomes loaded with In-111-NTA: biodistribution in mice. J Nucl Med. 1983;24 (1):45-51. (Pubitemid 13189999)
32. Gill PS, Wernz J, Scadden DT, Cohen P, Mukwaya GM, von Roenn JH, et al. Randomized phase III trial of liposomal daunorubicin versus doxorubicin, bleomycin, and vincristine in AIDS-related Kaposi's sarcoma. J Clin Oncol. 1996;14(8):2353-64. (Pubitemid 26264888)
33. Gabizon A, Papahadjopoulos D. Liposome formulations with prolonged circulation time in blood and enhanced uptake by tumors. Proc Natl Acad Sci USA. 1988;85(18):6949-53.
34. Torchilin VP, Trubetskoy VS. Which polymers can make nano-particulate drug carriers long-circulating? Adv Drug Deliv Rev. 1995;16:141-55.
35. Allen TM, Chonn A. Large unilamellar liposomes with low uptake into the reticuloendothelial system. FEBS Lett. 1987;223 (1):42-6.
36. Papahadjopoulos D, Allen TM, Gabizon A, Mayhew E, Matthay K, Huang SK, et al. Sterically stabilized liposomes: improvements in pharmacokinetics and antitumor therapeutic efficacy. Proc Natl Acad Sci USA. 1991;88(24):11460-4. (Pubitemid 21916061)
37. Woodle MC, Lasic DD. Sterically stabilized liposomes. Biochim Biophys Acta. 1992;1113(2):171-99.
38. Allen TM, Hansen C, Martin F, Redemann C, Yau-Young A. Liposomes containing synthetic lipid derivatives of poly(ethylene glycol) show prolonged circulation half-lives in vivo. Biochim Biophys Acta. 1991;1066(1):29-36.
39. 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. 1991;1070(1):187-92.
40. Needham D, Hristova K, McIntosh TJ, Dewhirst MW, Lasic DD. Polymer grafted liposomes: physical basis for the "stealth" property. J Liposome Res. 1992;2:411-30. (Pubitemid 23005614)
41. Lasic DD, Martin F. Stealth liposomes. Boca Raton, FL: CRC; 1995.
42. Allen TM. The use of glycolipids and hydrophilic polymers in avoiding rapid uptake of liposomes by the mononuclear phagocyte system. Adv Drug Deliv Rev. 1994;13:285-309. (Pubitemid 24065267)
43. Chonn A, Semple SC, Cullis PR. Separation of large unilamellar liposomes from blood components by a spin column procedure: towards identifying plasma proteins which mediate liposome clearance in vivo. Biochim Biophys Acta. 1991;1070(1):215-22.
44. Senior J, Delgado C, Fisher D, Tilcock C, Gregoriadis G. 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. 1991;1062(1):77-82.
45. Woodle MC. Surface-modified liposomes: assessment and characterization for increased stability and prolonged blood circulation. Chem Phys Lipids. 1993;64(1-3):249-62. (Pubitemid 23290877)
46. Senior JH. Fate and behavior of liposomes in vivo: a review of controlling factors. Crit Rev Ther Drug Carrier Syst. 1987;3 (2):123-93. (Pubitemid 17219201)
47. Huang SK, Stauffer PR, Hong K, Guo JW, Phillips TL, Huang A, et al. Liposomes and hyperthermia in mice: increased tumor uptake and therapeutic efficacy of doxorubicin in sterically stabilized liposomes. Cancer Res. 1994;54(8):2186-91. (Pubitemid 24138693)
48. 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(4):987-92. (Pubitemid 24085451)
49. Boman NL, Masin D, Mayer LD, Cullis PR, Bally MB. Liposomal vincristine which exhibits increased drug retention and increased circulation longevity cures mice bearing P388 tumors. Cancer Res. 1994;54(11):2830-3. (Pubitemid 24187755)
50. Allen TM, Mehra T, Hansen C, Chin YC. Stealth liposomes: an improved sustained release system for 1-beta-D-arabinofurano-sylcytosine. Cancer Res. 1992;52(9):2431-9.
51. Kim ES, Lu C, Khuri FR, Tonda M, Glisson BS, Liu D, et al. A phase II study of STEALTH cisplatin (SPI-77) in patients with advanced non-small cell lung cancer. Lung cancer (Amsterdam, Netherlands). 2001;34(3):427-32. (Pubitemid 33041478)
52. Gabizon AA. Liposome circulation time and tumor targeting: implications for cancer chemotherapy. Adv Drug Deliv Rev. 1995;16:285-94.
53. Gabizon AA. Pegylated liposomal doxorubicin: metamorphosis of an old drug into a new form of chemotherapy. Cancer Invest. 2001;19(4):424-36. (Pubitemid 32525189)
54. Whiteman KR, Subr V, Ulbrich K, Torchilin VP. Poly(Hpma)-coated liposomes demonstrate prolonged circulation in mice. J Liposome Res. 2001;11(2-3):153-64. (Pubitemid 33096375)
55. Torchilin VP, Levchenko TS, Whiteman KR, Yaroslavov AA, Tsatsakis AM, Rizos AK, et al. Amphiphilic poly-N-vinylpyrro-lidones: synthesis, properties and liposome surface modification. Biomaterials. 2001;22(22):3035-44. (Pubitemid 32768711)
56. Metselaar JM, Bruin P, de Boer LW, de Vringer T, Snel C, Oussoren C, et al. A novel family of L-amino acid-based biodegradable polymer-lipid conjugates for the development of long-circulating liposomes with effective drug-targeting capacity. Bioconjug Chem. 2003;14(6):1156-64. (Pubitemid 37449043)
57. Takeuchi H, Kojima H, Yamamoto H, Kawashima Y. Evaluation of circulation profiles of liposomes coated with hydrophilic polymers having different molecular weights in rats. J Control Release. 2001;75(1-2):83-91. (Pubitemid 32635199)
58. Moein Moghimi S, Hamad I, Bunger R, Andresen TL, Jorgensen K, Hunter AC, et al. Activation of the human complement system by cholesterol-rich and PEGylated liposomes-modulation of cholesterol-rich liposome-mediated complement activation by elevated serum LDL and HDL levels. J Liposome Res. 2006;16 (3):167-74. (Pubitemid 44358990)
59. Holland JW, Hui C, Cullis PR, Madden TD. Poly(ethylene glycol)-lipid conjugates regulate the calcium-induced fusion of liposomes composed of phosphatidylethanolamine and phospha-tidylserine. Biochemistry. 1996;35(8):2618-24.
60. Hong RL, Huang CJ, Tseng YL, Pang VF, Chen ST, Liu JJ, et al. Direct comparison of liposomal doxorubicin with or without polyethylene glycol coating in C-26 tumor-bearing mice: is surface coating with polyethylene glycol beneficial? Clin Cancer Res. 1999;5(11):3645-52.
61. Erbacher P, Bettinger T, Belguise-Valladier P, Zou S, Coll JL, Behr JP, et al. Transfection and physical properties of various saccharide, poly(ethylene glycol), and antibody-derivatized polyethylenimines (PEI). J Gene Med. 1999;1(3):210-22. (Pubitemid 129631076)
62. Boomer JA, Qualls MM, Inerowicz HD, Haynes RH, Patri VS, Kim JM, et al. Cytoplasmic delivery of liposomal contents mediated by an acid-labile cholesterol-vinyl ether-PEG conjugate. Bioconjug Chem. 2009;20(1):47-59.
63. Guo X, Szoka Jr FC. Steric stabilization of fusogenic liposomes by a low-pH sensitive PEG-diortho ester-lipid conjugate. Bioconjug Chem. 2001;12(2):291-300. (Pubitemid 32235482)
64. Li W, Huang Z, MacKay JA, Grube S, Szoka Jr FC. Low-pH-sensitive poly(ethylene glycol) (PEG)-stabilized plasmid nano-lipoparticles: effects of PEG chain length, lipid composition and assembly conditions on gene delivery. J Gene Med. 2005;7 (1):67-79.
65. Sawant RM, Hurley JP, Salmaso S, Kale A, Tolcheva E, Levchenko TS, et al. "SMART" drug delivery systems: double-targeted pH-responsive pharmaceutical nanocarriers. Bioconjug Chem. 2006;17(4):943-9. (Pubitemid 44162612)
66. Boomer JA, Inerowicz HD, Zhang Z-Y, Bergstrand N, Edwards K, Kim J-M, et al. Acid triggered release from sterically-stabilized fusogenic vesicles via a hydrolytic dePEGylation strategy. Langmuir. 2003;19:6408-15.
67. Zalipsky S, Qazen M, Walker 2nd JA, Mullah N, Quinn YP, Huang SK. New detachable poly(ethylene glycol) conjugates: cysteine-cleavable lipopolymers regenerating natural phospho-lipid, diacyl phosphatidylethanolamine. Bioconjug Chem. 1999;10(5):703-7. (Pubitemid 29456355)
68. Barenholz Y. Design of liposome-based drug carriers: from basic research to application as approved drugs. In: Lasic DD, Papahadjopoulos D, editors. Medical applications of liposomes. New York: Elsevier; 1998. p. 545-65.
69. Papahadjopoulos D, Jacobson K, Nir S, Isac T. Phase transitions in phospholipid vesicles. Fluorescence polarization and permeability measurements concerning the effect of temperature and cholesterol. Biochim Biophys Acta. 1973;311(3):330-48.
70. Gregoriadis G, Davis C. Stability of liposomes in vivo and in vitro is promoted by their cholesterol content and the presence of blood cells. Biochem Biophys Res Commun. 1979;89(4):1287-93.
71. Senior J, Gregoriadis G. Stability of small unilamellar liposomes in serum and clearance from the circulation: the effect of the phospholipid and cholesterol components. Life Sci. 1982;30 (24):2123-36. (Pubitemid 12066826)
72. Drummond DC, MeyerO, HongK, KirpotinDB, Papahadjopoulos D. Optimizing liposomes for delivery of chemotherapeutic agents to solid tumors. Pharmacol Rev. 1999;51(4):691-743.
73. Abra RM, Hunt CA. Liposome disposition in vivo. III. Dose and vesicle-size effects. Biochim Biophys Acta. 1981;666(3):493-503. (Pubitemid 12144883)
74. Senior J, Crawley JC, Gregoriadis G. Tissue distribution of liposomes exhibiting long half-lives in the circulation after intravenous injection. Biochim Biophys Acta. 1985;839(1):1-8. (Pubitemid 15085295)
75. Allen TM, Hansen C, Rutledge J. Liposomes with prolonged circulation times: factors affecting uptake by reticuloendothelial and other tissues. Biochim Biophys Acta. 1989;981(1):27-35. (Pubitemid 19127766)
76. Gabizon A, Papahadjopoulos D. The role of surface charge and hydrophilic groups on liposome clearance in vivo. Biochim Biophys Acta. 1992;1103(1):94-100.
77. Bae YH. Drug targeting and tumor heterogeneity. J Control Release. 2009;133(1):2-3.
78. Heldin CH, Rubin K, Pietras K, Ostman A. High interstitial fluid pressure-an obstacle in cancer therapy. Nat Rev Cancer. 2004;4 (10):806-13. (Pubitemid 39331152)
79. Allen TM, Cullis PR. Drug delivery systems: entering the mainstream. Science. 2004;303(5665):1818-22. (Pubitemid 38374867)
80. Ferrari M. Cancer nanotechnology: opportunities and challenges. Nat Rev Cancer. 2005;5(3):161-71. (Pubitemid 40314948)
81. Kirpotin D, Park JW, Hong K, Zalipsky S, Li WL, Carter P, et al. Sterically stabilized anti-HER2 immunoliposomes: design and targeting to human breast cancer cells in vitro. Biochemistry. 1997;36(1):66-75. (Pubitemid 27024679)
82. Park JW, Hong K, Carter P, Asgari H, Guo LY, Keller GA, et al. Development of anti-p185HER2 immunoliposomes for cancer therapy. Proc Natl Acad Sci USA. 1995;92(5):1327-31.
83. Sapra P, Allen TM. Internalizing antibodies are necessary for improved therapeutic efficacy of antibody-targeted liposomal drugs. Cancer Res. 2002;62(24):7190-4. (Pubitemid 36025236)
84. Liebert M, Wedemeyer GA, Stein JA, Washington Jr RW, Flint A, Ren LQ, et al. Identification by monoclonal antibodies of an antigen shed by human bladder cancer cells. Cancer Res. 1989;49 (23):6720-6. (Pubitemid 20008813)
85. Lopes de Menezes DE, Pilarski LM, Allen TM. In vitro and in vivo targeting of immunoliposomal doxorubicin to human B-cell lymphoma. Cancer Res. 1998;58(15):3320-30. (Pubitemid 28371072)
86. Park JW, Hong K, Kirpotin DB, Colbern G, Shalaby R, Baselga J, et al. Anti-HER2 immunoliposomes: enhanced efficacy attributable to targeted delivery. Clin Cancer Res. 2002;8(4):1172-81. (Pubitemid 35177372)
87. Goren D, Horowitz AT, Zalipsky S, Woodle MC, Yarden Y, Gabizon A. Targeting of stealth liposomes to erbB-2 (Her/2) receptor: in vitro and in vivo studies. Br J Cancer. 1996;74 (11):1749-56. (Pubitemid 26401894)
88. Torchilin VP. Liposomes as targetable drug carriers. Crit Rev Ther Drug Carrier Syst. 1985;2(1):65-115. (Pubitemid 16099051)
89. Mamot C, Drummond DC, Noble CO, Kallab V, Guo Z, Hong K, et al. Epidermal growth factor receptor-targeted immunolipo-somes significantly enhance the efficacy of multiple anticancer drugs in vivo. Cancer Res. 2005;65(24):11631-8. (Pubitemid 41821723)
90. Maruyama K. PEG-immunoliposome. Biosci Rep. 2002;22 (2):251-66. (Pubitemid 35222734)
91. Lee RJ, Low PS. Delivery of liposomes into cultured KB cells via folate receptor-mediated endocytosis. J Biol Chem. 1994;269 (5):3198-204. (Pubitemid 24237629)
92. Blume G, Cevc G, Crommelin MD, Bakker-Woudenberg IA, Kluft C, Storm G. Specific targeting with poly(ethylene glycol)-modified liposomes: coupling of homing devices to the ends of the polymeric chains combines effective target binding with long circulation times. Biochim Biophys Acta. 1993;1149 (1):180-4. (Pubitemid 23186318)
93. Maruyama K, Takizawa T, Yuda T, Kennel SJ, Huang L, Iwatsuru M. Targetability of novel immunoliposomes modified with amphipathic poly(ethylene glycol)s conjugated at their distal terminals to monoclonal antibodies. Biochim Biophys Acta. 1995;1234(1):74-80.
94. Medina OP, Zhu Y, Kairemo K. Targeted liposomal drug delivery in cancer. Curr Pharm Des. 2004;10(24):2981-9. (Pubitemid 39214006)
95. Lopes De Menezes DE, Kirchmeier MJ, Gagne J-F, Pilarski LM, Allen TM. Cellular trafficking and cytotoxicity of anti-Cd19-targeted liposomal doxorubicin in B lymphoma cells. J Liposome Res. 1999;9:199-228. (Pubitemid 29289785)
96. Sapra P, Allen TM. Ligand-targeted liposomal anticancer drugs. Prog Lipid Res. 2003;42(5):439-62. (Pubitemid 36700404)
97. Torchilin VP, Levchenko TS, Lukyanov AN, Khaw BA, Klibanov AL, Rammohan R, et al. p-Nitrophenylcarbonyl-PEG-PE-lip-osomes: fast and simple attachment of specific ligands, including monoclonal antibodies, to distal ends of PEG chains via p-nitrophenylcarbonyl groups. Biochim Biophys Acta. 2001;1511 (2):397-411. (Pubitemid 32250227)
98. Torchilin VP, Rammohan R, Weissig V, Khaw BA, Klibanov A, Samokhin GP, editors. PEG-Immunoliposomes: attachment of monoclonal antibody to distal ends of PEG chains via p-nitrophenylcarbonyl groups. 27th International Symposium on Controlled Release of Bioactive Materials; 2000; Paris: Controlled Release Society, Inc
99. Torchilin VP, Weissig V, Martin FJ, Heath TD, New RRC. Surface modifications of liposomes. In: Torchilin VP, Weissig V, editors. Liposomes: a practical approach. 2nd ed. Oxford: Oxford University Press; 2003. p. 193-229.
100. Hansen CB, Kao GY, Moase EH, Zalipsky S, Allen TM. Attachment of antibodies to sterically stabilized liposomes: evaluation, comparison and optimization of coupling procedures. Biochim Biophys Acta. 1995;1239(2):133-44.
101. Ishida T, Iden DL, Allen TM. A combinatorial approach to producing sterically stabilized (stealth) immunoliposomal drugs. FEBS Lett. 1999;460(1):129-33. (Pubitemid 29479257)
102. Sofou S, Sgouros G. Antibody-targeted liposomes in cancer therapy and imaging. Expert Opin Drug Deliv. 2008;5(2):189-204. (Pubitemid 351308311)
103. Torchilin V. Antibody-modified liposomes for cancer chemotherapy. Expert Opin Drug Deliv. 2008;5(9):1003-25.
104. Martin FJ, Papahadjopoulos D. Irreversible coupling of immu-noglobulin fragments to preformed vesicles. An improved method for liposome targeting. J Biol Chem. 1982;257(1):286-8. (Pubitemid 12109779)
105. Moreira JN, Ishida T, Gaspar R, Allen TM. Use of the postinsertion technique to insert peptide ligands into pre-formed stealth liposomes with retention of binding activity and cytotoxicity. Pharm Res. 2002;19(3):265-9. (Pubitemid 34211842)
106. Elbayoumi TA, Torchilin VP. Tumor-specific anti-nucleosome antibody improves therapeutic efficacy of doxorubicin-loaded long-circulating liposomes against primary and metastatic tumor in mice. Mol Pharm. 2009;6(1):246-54.
107. Kirpotin DB, Drummond DC, Shao Y, Shalaby MR, Hong K, Nielsen UB, et al. Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models. Cancer Res. 2006;66 (13):6732-40. (Pubitemid 44085631)
108. Xiong XB, Huang Y, Lu WL, Zhang H, Zhang X, Zhang Q. Enhanced intracellular uptake of sterically stabilized liposomal doxorubicin in vitro resulting in improved antitumor activity in vivo. Pharm Res. 2005;22(6):933-9. (Pubitemid 40898103)
109. Xiong XB, Huang Y, Lu WL, Zhang X, Zhang H, Nagai T, et al. Intracellular delivery of doxorubicin with RGD-modified steri-cally stabilized liposomes for an improved antitumor efficacy: in vitro and in vivo. J Pharm Sci. 2005;94(8):1782-93. (Pubitemid 41360872)
110. Allen TM, Ahmad I, Lopes de Menezes DE, Moase EH. Immunoliposome-mediated targeting of anti-cancer drugs in vivo. Biochem Soc Trans. 1995;23(4):1073-9.
111. Vingerhoeds MH, Steerenberg PA, Hendriks JJ, Dekker LC, Van Hoesel QG, Crommelin DJ, et al. Immunoliposome-mediated targeting of doxorubicin to human ovarian carcinoma and in vivo. Br J Cancer. 1996;74(7):1023-9. (Pubitemid 26333901)
112. Moase EH, Qi W, Ishida T, Gabos Z, Longenecker BM, Zimmermann GL, et al. Anti-MUC-1 immunoliposomal doxo-rubicin in the treatment of murine models of metastatic breast cancer. Biochim Biophys Acta. 2001;1510(1-2):43-55. (Pubitemid 32149884)
113. Lukyanov AN, Elbayoumi TA, Chakilam AR, Torchilin VP. Tumor-targeted liposomes: doxorubicin-loaded long-circulating liposomes modified with anti-cancer antibody. J Control Release. 2004;100(1):135-44. (Pubitemid 39445991)
114. Gupta B, Torchilin VP. Monoclonal antibody 2 C5-modified doxorubicin-loaded liposomes with significantly enhanced therapeutic activity against intracranial human brain U-87 MG tumor xenografts in nude mice. Cancer Immunol Immunother. 2007;56(8):1215-23. (Pubitemid 46763936)
115. Park JW, Kirpotin DB, Hong K, Shalaby R, Shao Y, Nielsen UB, et al. Tumor targeting using anti-her2 immunoliposomes. J Control Release. 2001;74(1-3):95-113. (Pubitemid 32727613)
116. Shmeeda H, Tzemach D, Mak L, Gabizon A. Her2-targeted pegylated liposomal doxorubicin: retention of target-specific binding and cytotoxicity after in vivo passage. J Control Release. 2009;136(2):155-60.
117. Kamps JA, Koning GA, Velinova MJ, Morselt HW, Wilkens M, Gorter A, et al. Uptake of long-circulating immunoliposomes, directed against colon adenocarcinoma cells, by liver metastases of colon cancer. J Drug Target. 2000;8(4):235-45.
118. Mamot C, Drummond DC, Greiser U, Hong K, Kirpotin DB, Marks JD, et al. Epidermal growth factor receptor (EGFR)-targeted immunoliposomes mediate specific and efficient drug delivery to EGFR- and EGFRvIII-overexpressing tumor cells. Cancer Res. 2003;63(12):3154-61. (Pubitemid 36735867)
119. Gabizon A, Horowitz AT, Goren D, Tzemach D, Shmeeda H, Zalipsky S. In vivo fate of folate-targeted polyethylene-glycol liposomes in tumor-bearing mice. Clin Cancer Res. 2003;9 (17):6551-9. (Pubitemid 38031844)
120. Yokota T, Milenic DE, Whitlow M, Schlom J. Rapid tumor penetration of a single-chain Fv and comparison with other immunoglobulin forms. Cancer Res. 1992;52(12):3402-8.
121. Lee RJ, Low PS. Folate-mediated tumor cell targeting of liposome-entrapped doxorubicin in vitro. Biochim Biophys Acta. 1995;1233(2):134-44.
122. Park JW, Hong K, Kirpotin DB, Papahadjopoulos D, Benz CC. Immunoliposomes for cancer treatment. Adv Pharmacol. 1997;40:399-435.
123. Storm G, Steerenberg PA, Emmen F, van Borssum Waalkes M, Crommelin DJ. Release of doxorubicin from peritoneal macrophages exposed in vivo to doxorubicin-containing liposomes. Biochim Biophys Acta. 1988;965(2-3):136-45.
124. Chu CJ, Dijkstra J, Lai MZ, Hong K, Szoka FC. Efficiency of cytoplasmic delivery by pH-sensitive liposomes to cells in culture. Pharm Res. 1990;7(8):824-34. (Pubitemid 20332534)
125. Trubetskaya OV, Trubetskoy VS, Domogatsky SP, Rudin AV, Popov NV, Danilov SM, et al. Monoclonal antibody to human endothelial cell surface internalization and liposome delivery in cell culture. FEBS Lett. 1988;228(1):131-4. (Pubitemid 18039482)
126. Allen TM, Hansen C, Stuart DD. Targeted stericalliy stabilized liposomal drug delivery. In: Lasic DD, Papahadjopoulos D, editors. Medical applications of liposomes. New York: Elsevier; 1998. p. 545-65.
127. Zhou Y, Drummond DC, Zou H, Hayes ME, Adams GP, Kirpotin DB, et al. Impact of single-chain Fv antibody fragment affinity on nanoparticle targeting of epidermal growth factor receptor-expressing tumor cells. J Mol Biol. 2007;371(4):934-47. (Pubitemid 47103290)
128. Sapra P, Allen TM. Improved outcome when B-cell lymphoma is treated with combinations of immunoliposomal anticancer drugs targeted to both the CD19 and CD20 epitopes. Clin Cancer Res. 2004;10(7):2530-7. (Pubitemid 38445715)
129. Allen TM, Mumbengegwi DR, Charrois GJ. Anti-CD19-targeted liposomal doxorubicin improves the therapeutic efficacy in murine B-cell lymphoma and ameliorates the toxicity of liposomes with varying drug release rates. Clin Cancer Res. 2005;11(9):3567-73. (Pubitemid 40627913)
130. Hosokawa S, Tagawa T, Niki H, Hirakawa Y, Nohga K, Nagaike K. Efficacy of immunoliposomes on cancer models in a cell-surface-antigen-density-dependent manner. Br J Cancer. 2003;89(8):1545-51. (Pubitemid 37386613)
131. Emanuel N, Kedar E, Bolotin EM, Smorodinsky NI, Barenholz Y. Targeted delivery of doxorubicin via sterically stabilized immunoliposomes: pharmacokinetics and biodistribution in tumor-bearing mice. Pharm Res. 1996;13(6):861-8. (Pubitemid 26227743)
132. Allen TM, Brandeis E, Hansen CB, Kao GY, Zalipsky S. A new strategy for attachment of antibodies to sterically stabilized liposomes resulting in efficient targeting to cancer cells. Biochim Biophys Acta. 1995;1237(2):99-108.
133. Kamps JA, Scherphof GL. Receptor versus non-receptor mediated clearance of liposomes. Adv Drug Deliv Rev. 1998;32(1-2):81-97. (Pubitemid 28277177)
134. Flavell DJ, Noss A, Pulford KA, Ling N, Flavell SU. Systemic therapy with 3BIT, a triple combination cocktail of anti-CD19, -CD22, and -CD38-saporin immunotoxins, is curative of human B-cell lymphoma in severe combined immuno-deficient mice. Cancer Res. 1997;57(21):4824-9. (Pubitemid 27468990)
135. Anabousi S, Bakowsky U, Schneider M, Huwer H, Lehr CM, Ehrhardt C. In vitro assessment of transferrin-conjugated liposomes as drug delivery systems for inhalation therapy of lung cancer. Eur J Pharm Sci. 2006;29(5):367-74. (Pubitemid 44709858)
136. Hatakeyama H, Akita H, Maruyama K, Suhara T, Harashima H. Factors governing the in vivo tissue uptake of transferrin-coupled polyethylene glycol liposomes in vivo. Int J Pharm. 2004;281(1-2):25-33. (Pubitemid 39024260)
137. Li X, Ding L, Xu Y, Wang Y, Ping Q. Targeted delivery of doxorubicin using stealth liposomes modified with transferrin. Int J Pharm. 2009;373(1-2):116-23.
138. Ishida O, Maruyama K, Tanahashi H, Iwatsuru M, Sasaki K, Eriguchi M, et al. Liposomes bearing polyethyleneglycol-coupled transferrin with intracellular targeting property to the solid tumors in vivo. Pharm Res. 2001;18(7):1042-8. (Pubitemid 32799953)
139. Leamon CP, Low PS. Delivery of macromolecules into living cells: a method that exploits folate receptor endocytosis. Proc Natl Acad Sci USA. 1991;88(13):5572-6. (Pubitemid 21914787)
140. Yamada A, Taniguchi Y, Kawano K, Honda T, Hattori Y, Maitani Y. Design of folate-linked liposomal doxorubicin to its antitumor effect in mice. Clin Cancer Res. 2008;14 (24):8161-8.
141. Lu Y, Wu J, Wu J, Gonit M, Yang X, Lee A, et al. Role of formulation composition in folate receptor-targeted liposomal doxorubicin delivery to acute myelogenous leukemia cells. Mol Pharm. 2007;4(5):707-12. (Pubitemid 350004270)
142. Gupta B, Levchenko TS, Torchilin VP. Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides. Adv Drug Deliv Rev. 2005;57(4):637-51. (Pubitemid 40255564)
143. Kale AA, Torchilin VP. Design, synthesis, and characterization of pH-sensitive PEG-PE conjugates for stimuli-sensitive pharmaceutical nanocarriers: the effect of substitutes at the hydrazone linkage on the ph stability of PEG-PE conjugates. Bioconjug Chem. 2007;18(2):363-70. (Pubitemid 46493506)
144. Torchilin V. Multifunctional and stimuli-sensitive pharmaceutical nanocarriers. Eur J Pharm Biopharm. 2009;71(3):431-44.
145. ElBayoumi TA, Torchilin VP. Tumor-targeted nanomedicines: enhanced antitumor efficacy in vivo of doxorubicin-loaded, long-circulating liposomes modified with cancer-specific monoclonal antibody. Clin Cancer Res. 2009;15(6):1973-80.
146. Elbayoumi TA, Torchilin VP. Enhanced cytotoxicity of monoclonal anticancer antibody 2 C5-modified doxorubicin-loaded PEGylated liposomes against various tumor cell lines. Eur J Pharm Sci. 2007;32(3):159-68. (Pubitemid 47532709)
147. Yang T, Choi MK, Cui FD, Lee SJ, Chung SJ, Shim CK, et al. Antitumor effect of paclitaxel-loaded PEGylated immunolipo-somes against human breast cancer cells. Pharm Res. 2007;24 (12):2402-11. (Pubitemid 350060715)
148. Zhao H, Wang JC, Sun QS, Luo CL, Zhang Q. RGD-based strategies for improving antitumor activity of paclitaxel-loaded liposomes in nude mice xenografted with human ovarian cancer. J Drug Target. 2009;17(1):10-8.
149. Hatakeyama H, Akita H, Ishida E, Hashimoto K, Kobayashi H, Aoki T, et al. Tumor targeting of doxorubicin by anti-MT1-MMP antibody-modified PEG liposomes. Int J Pharm. 2007;342 (1-2):194-200. (Pubitemid 47259319)