Ligand-targeted liposome design: Challenges and fundamental considerations

Trends in Biotechnology

Volumn 32, Issue 1, 2014, Pages 32-45

  Noble, Gavin T ^a   Stefanick, Jared F ^a   Ashley, Jonathan D ^a   Kiziltepe, Tanyel ^a,b   Bilgicer, Basar ^a,b  

^a University of Notre Dame   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

Active targeting; EPR effect; Ligand targeted liposomes; Liposomal drug delivery; Liposome stealth; PEGylation

Indexed keywords

ACTIVE TARGETING; ADVANCED DESIGNS; CLINICAL OUTCOME; DRUG CARRIER; EPR EFFECT; PEGYLATION; SERUM PROTEINS; TUMOR PENETRATION;

BIOCHEMISTRY; DRUG DELIVERY; LIGANDS; LIPOSOMES; MEDICAL NANOTECHNOLOGY;

DESIGN;

ADJUVANT; ANTINEOPLASTIC AGENT; CISPLATIN; CREMOPHOR; DOXORUBICIN; DRUG CARRIER; ENDOTAG 1; GANGLIOSIDE GM1; IMMUNOLIPOSOME; IRINOTECAN; KOLLIPHOR EL; LEP ETU; LIGAND; LIGAND TARGETED LIPOSOME; LIPOSOME; MACROGOL 10000; MACROGOL 2000; MACROGOL 20000; MACROGOL 350; MACROGOL 5000; MACROGOL 550; MACROGOL 750; MITOXANTRONE; MONOCLONAL ANTIBODY; NANOPARTICLE; OXALIPLATIN; PACLITAXEL; PEG 350; PEG 5000; PEG 550; PEG 750; PEPTIDOMIMETIC AGENT; PHOSPHATIDYLINOSITOL; PLASMID DNA; POLYMER; UNCLASSIFIED DRUG; UNINDEXED DRUG; VINCRISTINE SULFATE;

ACTIVE TARGETING; ANAPHYLAXIS; ANTIGENICITY; B CELL LYMPHOMA; BINDING AFFINITY; BREAST CANCER; CANCER CHEMOTHERAPY; COLON CARCINOMA; CONTROLLED DRUG RELEASE; COST; DRUG APPROVAL; DRUG BIOAVAILABILITY; DRUG DELIVERY SYSTEM; DRUG DESIGN; DRUG DOSAGE FORM COMPARISON; DRUG EFFICACY; DRUG FORMULATION; DRUG HALF LIFE; DRUG PROTEIN BINDING; DRUG TARGETING; ENDOCYTOSIS; FOOD AND DRUG ADMINISTRATION; HUMAN; INTERMETHOD COMPARISON; INTERNALIZATION; KAPOSI SARCOMA; LEUKEMIA; LIPID BILAYER; LIPOSOMAL DELIVERY; LIVER CELL CARCINOMA; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; MACROMOLECULE; MATERIAL COATING; MELANOMA; MULTIPLE MYELOMA; NANOMEDICINE; NANOTECHNOLOGY; NONHUMAN; OPSONIZATION; OVARY CANCER; PARTICLE SIZE; PASSIVE TARGETING; PHAGE DISPLAY; PRIORITY JOURNAL; PROSTATE CANCER; REVIEW; THYROID MEDULLARY CARCINOMA; TUMOR CELL;

ACTIVE TARGETING; EPR EFFECT; LIGAND-TARGETED LIPOSOMES; LIPOSOMAL DRUG DELIVERY; LIPOSOME STEALTH; PEGYLATION;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOTECHNOLOGY; CELL LINE, TUMOR; DRUG DELIVERY SYSTEMS; HUMANS; LIGANDS; LIPOSOMES; MICE; NANOMEDICINE;

EID: 84890799193     PISSN: 01677799     EISSN: 18793096     Source Type: Journal    
DOI: 10.1016/j.tibtech.2013.09.007     Document Type: Review

References (127)

1. Davis M.E., et al. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat. Rev. Drug Discov. 2008, 7:771-782.
2. Petros R.A., DeSimone J.M. Strategies in the design of nanoparticles for therapeutic applications. Nat. Rev. Drug Discov. 2010, 9:615-627.
3. Wang A.Z., et al. Nanoparticle delivery of cancer drugs. Annu. Rev. Med. 2012, 63:185-198.
4. Allen T.M., Cullis P.R. Liposomal drug delivery systems: From concept to clinical applications. Adv. Drug Deliv. Rev. 2013, 65:36-48.
5. Maeda H. Macromolecular therapeutics in cancer treatment: the EPR effect and beyond. J. Control. Release 2012, 164:138-144.
6. Egusquiaguirre S.P., et al. Nanoparticle delivery systems for cancer therapy: advances in clinical and preclinical research. Clin. Transl. Oncol. 2012, 14:83-93.
7. Longmire M., et al. Clearance properties of nano-sized particles and molecules as imaging agents: considerations and caveats. Nanomedicine 2008, 3:703-717.
8. Banerjee D., Sengupta S. Nanoparticles in cancer chemotherapy. Prog. Mol. Biol. Transl. Sci. 2011, 104:489-507.
9. Barenholz Y.(Chezy) Doxil® - The first FDA-approved nano-drug: lessons learned. J. Control. Release 2012, 160:117-134.
10. Solomon R., Gabizon A. Clinical pharmacology of liposomal anthracyclines: focus on pegylated liposomal doxorubicin. Clin. Lymphoma Myelom 2008, 8:21-32.
11. Moore A., Pinkerton R. Vincristine: can its therapeutic index be enhanced?. Pediatr. Blood Cancer 2009, 53:1180-1187.
12. Silverman J.A., Deitcher S.R. Marqibo® (vincristine sulfate liposome injection) improves the pharmacokinetics and pharmacodynamics of vincristine. Cancer Chemother. Pharmacol. 2013, 71:555-564.
13. Chang H-I., Yeh M-K. Clinical development of liposome-based drugs: formulation, characterization, and therapeutic efficacy. Int. J. Nanomed. 2012, 7:49-60.
14. Koudelka S., Turánek J. Liposomal paclitaxel formulations. J. Control. Release 2012, 163:322-334.
15. Andresen T.L., et al. Advanced strategies in liposomal cancer therapy: problems and prospects of active and tumor specific drug release. Prog. Lipid Res. 2005, 44:68-97.
16. Malam Y., et al. Liposomes and nanoparticles: nanosized vehicles for drug delivery in cancer. Trends Pharmacol. Sci. 2009, 30:592-599.
17. Barenholz Y. Liposome application: problems and prospects. Curr. Opin. Colloid Interface Sci. 2001, 6:66-77.
18. Bandak S., et al. Pharmacological studies of cisplatin encapsulated in long-circulating liposomes in mouse tumor models. Anticancer Drugs 1999, 10:911-920.
19. Andresen T.L., et al. Enzyme-triggered nanomedicine: drug release strategies in cancer therapy. Mol. Membr. Biol. 2010, 27:353-363.
20. Ganta S., et al. A review of stimuli-responsive nanocarriers for drug and gene delivery. J. Control. Release 2008, 126:187-204.
21. Shum P., et al. Phototriggering of liposomal drug delivery systems. Adv. Drug Deliv. Rev. 2001, 53:273-284.
22. May J.P., Li S-D. Hyperthermia-induced drug targeting. Expert Opin. Drug Deliv. 2013, 10:511-527.
23. Li L., et al. Mild hyperthermia triggered doxorubicin release from optimized stealth thermosensitive liposomes improves intratumoral drug delivery and efficacy. J. Control. Release 2013, 168:142-150.
24. Ponce A.M., et al. Hyperthermia mediated liposomal drug delivery. Int. J. Hyperthermia 2006, 22:205-213.
25. Schroeder A., et al. Ultrasound triggered release of cisplatin from liposomes in murine tumors. J. Control. Release 2009, 137:63-68.
26. Schroeder A., et al. Ultrasound, liposomes, and drug delivery: principles for using ultrasound to control the release of drugs from liposomes. Chem. Phys. Lipids 2009, 162:1-16.
27. Sapra P., Allen T.M. Ligand-targeted liposomal anticancer drugs. Prog. Lipid Res. 2003, 42:439-462.
28. Ruoslahti E. Peptides as targeting elements and tissue penetration devices for nanoparticles. Adv. Mater. 2012, 24:3747-3756.
29. Canton I., Battaglia G. Endocytosis at the nanoscale. Chem. Soc. Rev. 2012, 41:2718-2739.
30. Albanese A., et al. The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu. Rev. Biomed. Eng. 2012, 14:1-16.
31. He C., et al. Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials 2010, 31:3657-3666.
32. Sawant R.R., Torchilin V.P. Challenges in development of targeted liposomal therapeutics. AAPS J. 2012, 14:303-315.
33. Bae Y.H., Park K. Targeted drug delivery to tumors: myths, reality and possibility. J. Control. Release 2011, 153:198-205.
34. Moghimi S.M., Farhangrazi Z.S. Nanomedicine and the complement paradigm. Nanomedicine 2013, 9:458-460.
35. Li S-D., Huang L. Stealth nanoparticles: high density but sheddable PEG is a key for tumor targeting. J. Control. Release 2010, 145:178-181.
36. Charrois G.J.R., Allen T.M. Multiple injections of pegylated liposomal doxorubicin: pharmacokinetics and therapeutic activity. J. Pharmacol. Exp. Ther. 2003, 306:1058-1067.
37. Tirosh O., et al. Hydration of polyethylene glycol-grafted liposomes. Biophys. J. 1998, 74:1371-1379.
38. Dos Santos N., 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.
39. Maldiney T., et al. Effect of core diameter, surface coating, and PEG chain length on the biodistribution of persistent luminescence nanoparticles in mice. ACS Nano 2011, 5:854-862.
40. Fang C., et al. Effect of MePEG molecular weight and particle size on in vitro release of tumor necrosis factor-α-loaded nanoparticles. Acta Pharmacol. Sin. 2005, 26:242-249.
41. Walkey C.D., et al. Nanoparticle size and surface chemistry determine serum protein adsorption and macrophage uptake. J. Am. Chem. Soc. 2011, 134:2139-2147.
42. Perry J.L., et al. PEGylated PRINT nanoparticles: the impact of PEG density on protein binding, macrophage association, biodistribution, and pharmacokinetics. Nano Lett. 2012, 12:5304-5310.
43. Hong R., 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, 5:3645-3652.
44. Guo X., Szoka F.C. Steric stabilization of fusogenic liposomes by a low-pH sensitive PEG-diortho ester-lipid conjugate. Bioconjug. Chem. 2001, 12:291-300.
45. Kirpotin D., et al. Liposomes with detachable polymer coating: destabilization and fusion of dioleoylphosphatidylethanolamine vesicles triggered by cleavage of surface-grafted poly(ethylene glycol). FEBS Lett. 1996, 388:115-118.
46. Ishida T., et al. Targeted delivery and triggered release of liposomal doxorubicin enhances cytotoxicity against human B lymphoma cells. Biochim. Biophys. Acta 2001, 1515:144-158.
47. Alvarez-Lorenzo C., Concheiro A. Bioinspired drug delivery systems. Curr. Opin. Biotechnol. 2013, 10.1016/j.copbio.2013.02.013.
48. Fang R.H., et al. Nanoparticles disguised as red blood cells to evade the immune system. Expert Opin. Biol. Ther. 2012, 12:385-389.
49. Parodi A., et al. Synthetic nanoparticles functionalized with biomimetic leukocyte membranes possess cell-like functions. Nat. Nanotechnol. 2013, 8:61-68.
50. Furumoto K., et al. Effect of coupling of albumin onto surface of PEG liposome on its in vivo disposition. Int. J. Pharm. 2007, 329:110-116.
51. Piao L., et al. Human serum albumin-coated lipid nanoparticles for delivery of siRNA to breast cancer. Nanomedicine 2013, 9:122-129.
52. Rodriguez P.L., et al. Minimal "self" peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles. Science 2013, 339:971-975.
53. Kirpotin D., et al. Sterically stabilized anti-HER2 immunoliposomes: design and targeting to human breast cancer cells in vitro. Biochemistry 1997, 36:66-75.
54. Kirpotin D.B., et al. Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models. Cancer Res. 2006, 66:6732-6740.
55. Stefanick J.F., et al. A systematic analysis of peptide linker length and liposomal polyethylene glycol coating on cellular uptake of peptide-targeted liposomes. ACS Nano 2013, 7:2935-2947.
56. Wu J., et al. Targeting hepatocytes for drug and gene delivery: emerging novel approaches and applications. Front. Biosci. 2002, 7:717-725.
57. Kawakami S., et al. In vivo gene delivery to the liver using novel galactosylated cationic liposomes. Pharm. Res. 2000, 17:306-313.
58. Sonoke S., et al. Galactose-modified cationic liposomes as a liver-targeting delivery system for small interfering RNA. Biol. Pharm. Bull. 2011, 34:1338-1342.
59. Wang S., et al. Sustained liver targeting and improved antiproliferative effect of doxorubicin liposomes modified with galactosylated lipid and PEG-lipid. AAPS PharmSciTech 2010, 11:870-877.
60. Gabizon A., et al. Targeting folate receptor with folate linked to extremities of poly(ethylene glycol)-grafted liposomes: in vitro studies. Bioconjug. Chem. 1999, 10:289-298.
61. Yamada A., et al. Design of folate-linked liposomal doxorubicin to its antitumor effect in mice. Clin. Cancer Res. 2008, 14:8161-8168.
62. Lee R.J., Low P.S. Delivery of liposomes into cultured KB cells via folate receptor-mediated endocytosis. J. Biol. Chem. 1994, 269:3198-3204.
63. Kiziltepe T., et al. Rationally engineered nanoparticles target multiple myeloma cells, overcome cell-adhesion-mediated drug resistance, and show enhanced efficacy in vivo. Blood Cancer J. 2012, 2:e64.
64. Sapra P., Allen T.M. 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, 10:2530-2537.
65. Cheng W.W.K., Allen T.M. Targeted delivery of anti-CD19 liposomal doxorubicin in B-cell lymphoma: a comparison of whole monoclonal antibody, Fab' fragments and single chain Fv. J. Control. Release 2008, 126:50-58.
66. Lopes de Menezes D.E., et al. In vitro and in vivo targeting of immunoliposomal doxorubicin to human B-cell lymphoma. Cancer Res. 1998, 58:3320-3330.
67. Laginha K., et al. Liposomes targeted via two different antibodies: assay, B-cell binding and cytotoxicity. Biochim. Biophys. Acta 2005, 1711:25-32.
68. Saad M., et al. Receptor targeted polymers, dendrimers, liposomes: which nanocarrier is the most efficient for tumor-specific treatment and imaging?. J. Control. Release 2008, 130:107-114.
69. He Y., et al. Luteinizing hormone-releasing hormone receptor-mediated delivery of mitoxantrone using LHRH analogs modified with PEGylated liposomes. Int. J. Nanomed. 2010, 5:697-705.
70. Forssen E., Willis M. Ligand-targeted liposomes. Adv. Drug Deliv. Rev. 1998, 29:249-271.
71. Emanuel N., et al. Targeted delivery of doxorubicin via stericallystabilized immunoliposomes- pharmacokinetics and biodistribution in tumor-bearing mice. Pharm. Res. 1996, 13:861-868.
72. Vingerhoeds M.H., et al. Immunoliposome-mediated targeting of doxorubicin to human ovarian. Br. J. Cancer 1996, 74:1023-1029.
73. Goren D., et al. Targeting of stealth liposomes to erbB-2 (Her/2) receptor: in vitro and in vivo studies. Br. J. Cancer 1996, 74:1749-1756.
74. Gabizon A., et al. In vivo fate of folate-targeted polyethylene-glycol liposomes in tumor-bearing mice. Clin. Cancer Res. 2003, 9:6551-6559.
75. Stohrer M., et al. Oncotic pressure in solid tumors is elevated oncotic pressure in solid tumors is elevated. Cancer Res. 2000, 60:4251-4255.
76. Yokota T., et al. Rapid tumor penetration of a single-chain fv and comparison with other immunoglobulin forms. Cancer Res. 1992, 52:3402-3408.
77. Mori T. Cancer-specific ligands identified from screening of peptide-display libraries. Curr. Pharm. Des. 2004, 10:2335-2343.
78. Lo A., et al. Hepatocellular carcinoma cell-specific peptide ligand for targeted drug delivery. Mol. Cancer Ther. 2008, 7:579-589.
79. Sugahara K.N., et al. Tissue-penetrating delivery of compounds and nanoparticles into tumors. Cancer Cell 2009, 16:510-520.
80. Laakkonen P., et al. Antitumor activity of a homing peptide that targets tumor lymphatics and tumor cells. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:9381-9396.
81. Roth L., et al. Transtumoral targeting enabled by a novel neuropilin-binding peptide. Oncogene 2012, 31:3754-3763.
82. Dietz G.P.H., Bähr M. Delivery of bioactive molecules into the cell: the Trojan horse approach. Mol. Cell. Neurosci. 2004, 27:85-131.
83. Demers M., Wagner D.D. Targeting platelet function to improve drug delivery. Oncoimmunology 2012, 1:100-102.
84. Wang J., Gao W. Nano/microscale motors: biomedical opportunities and challenges. ACS Nano 2012, 6:5745-5751.
85. Maruyama K. PEG-immunoliposome. Biosci. Rep. 2002, 22:251-266.
86. Stefanik J.F., et al. Enhanced cellular uptake of through increased peptide hydrophilicity and optimized ethylene glycol peptide-linker length. ACS Nano 2013, 7:8115-8127.
87. Cheng Z., et al. Multifunctional nanoparticles: cost versus benefit of adding targeting and imaging capabilities. Science 2012, 338:903-910.
88. Salvati A., et al. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat. Nanotechnol. 2013, 8:137-143.
89. McNeeley K.M., et al. Decreased circulation time offsets increased efficacy of PEGylated nanocarriers targeting folate receptors of glioma. Nanotechnology 2007, 18:385101.
90. Bandekar A., et al. Masking and triggered unmasking of targeting ligands on liposomal chemotherapy selectively suppress tumor growth in vivo. Mol. Pharm. 2013, 10:152-160.
91. McNeeley K.M., et al. Masking and triggered unmasking of targeting ligands on nanocarriers to improve drug delivery to brain tumors. Biomaterials 2009, 30:3986-3995.
92. Kuai R., et al. Targeted delivery of cargoes into a murine solid tumor by a cell-penetrating peptide and cleavable poly(ethylene glycol) comodified liposomal delivery system via systemic administration. Mol. Pharm. 2011, 8:2151-2161.
93. Takara K., et al. Size-controlled, dual-ligand modified liposomes that target the tumor vasculature show promise for use in drug-resistant cancer therapy. J. Control. Res. 2012, 162:225-232.
94. Park J.W., et al. Anti-HER2 immunoliposomes: enhanced efficacy attributable to targeted delivery. Clin. Cancer Res. 2002, 8:1172-1181.
95. Nielsen U.B., et al. Therapeutic efficacy of anti-ErbB2 immunoliposomes targeted by a phage antibody selected for cellular endocytosis. Biochim. Biophys. Acta 2002, 1591:109-118.
96. Reynolds J.G., et al. HER2-targeted liposomal doxorubicin displays enhanced anti-tumorigenic effects without associated cardiotoxicity. Toxicol. Appl. Pharmacol. 2012, 262:1-10.
97. Sankhala K., et al. A phase I pharmacokinetic (PK) study of MBP-426, a novel liposome encapsulated oxaliplatin. J. Clin. Oncol. 2009, 27(Suppl.):15S.
98. Sengupta S., Kulkarni A. Design principles for clinical efficacy of cancer nanomedicine: a look into the basics. ACS Nano 2013, 7:2878-2882.
99. Teicher B.A., Chari R.V.J. Antibody conjugate therapeutics: challenges and potential. Clin. Cancer Res. 2011, 17:6389-6397.
100. Zhang Y., et al. Targeted delivery of RGD-modified liposomes encapsulating both combretastatin A-4 and doxorubicin for tumor therapy: in vitro and in vivo studies. Eur. J. Pharm. Biopharm. 2010, 74:467-473.
101. Schiffelers R.M., et al. Anti-tumor efficacy of tumor vasculature-targeted liposomal doxorubicin. J. Control. Release 2003, 91:115-122.
102. Zhao H., et al. RGD-based strategies for improving antitumor activity of paclitaxel-loaded liposomes in nude mice xenografted with human ovarian cancer. J. Drug Target. 2009, 17:10-18.
103. Hölig P., et al. Novel RGD lipopeptides for the targeting of liposomes to integrin-expressing endothelial and melanoma cells. Protein Eng. Des. Sel. 2004, 17:433-441.
104. Li W., et al. RGD-targeted paramagnetic liposomes for early detection of tumor: in vitro and in vivo studies. Eur. J. Radiol. 2011, 80:598-606.
105. Zhou X., et al. Lactosylated liposomes for targeted delivery of doxorubicin to hepatocellular carcinoma. Int. J. Nanomed. 2012, 7:5465-5474.
106. Chiu G.N.C., et al. Modulation of cancer cell survival pathways using multivalent liposomal therapeutic antibody constructs. Mol. Cancer Ther. 2007, 6:844-855.
107. Yu B., et al. Targeted nanoparticle delivery overcomes off-target immunostimulatory effects of oligonucleotides and improves therapeutic efficacy in chronic lymphocytic leukemia. Blood 2013, 121:136-147.
108. Gabizon A., et al. Improved therapeutic activity of folate-targeted liposomal doxorubicin in folate receptor-expressing tumor models. Cancer Chemother. Pharmacol. 2010, 66:43-52.
109. Xie F., et al. Investigation of glucose-modified liposomes using polyethylene glycols with different chain lengths as the linkers for brain targeting. Int. J. Nanomed. 2012, 7:163-175.
110. Accardo A., et al. Peptide-modified liposomes for selective targeting of bombesin receptors overexpressed by cancer cells: a potential theranostic agent. Int. J. Nanomed. 2012, 7:2007-2017.
111. Yang T., et al. Antitumor effect of paclitaxel-loaded PEGylated immunoliposomes against human breast cancer cells. Pharm. Res. 2007, 24:2402-2411.
112. Laginha K.M., et al. Bioavailability and therapeutic efficacy of HER2 scFv-targeted liposomal doxorubicin in a murine model of HER2-overexpressing breast cancer. J. Drug Target. 2008, 16:605-610.
113. Hattori Y., Maitani Y. Enhanced in vitro DNA transfection efficiency by novel folate-linked nanoparticles in human prostate cancer and oral cancer. J. Control. Release 2004, 97:173-183.
114. Sawant R.M., et al. Prostate cancer-specific monoclonal antibody 5D4 significantly enhances the cytotoxicity of doxorubicin-loaded liposomes against target cells in vitro. J. Drug Target. 2008, 16:601-604.
115. Zhang J., et al. A novel octreotide modified lipid vesicle improved the anticancer efficacy of doxorubicin in somatostatin receptor 2 positive tumor models. Mol. Pharm. 2010, 107:1159-1168.
116. Iwase Y., Maitani Y. Octreotide-targeted liposomes loaded with CPT-11 enhanced cytotoxicity for the treatment of medullary thyroid carcinoma. Mol. Pharm. 2011, 8:330-337.
117. Koshkaryev A., et al. Increased apoptosis in cancer cells in vitro and in vivo by ceramides in transferrin-modified liposomes. Cancer Biol. Ther. 2012, 13:50-60.
118. Krieger M.L., et al. Overcoming cisplatin resistance of ovarian cancer cells by targeted liposomes in vitro. Int. J. Pharm. 2010, 389:10-17.
119. Mendonça L.S., et al. Transferrin receptor-targeted liposomes encapsulating anti-BCR-ABL siRNA or asODN for chronic myeloid leukemia treatment. Bioconjug. Chem. 2010, 21:157-168.
120. Li X., et al. Targeted delivery of doxorubicin using stealth liposomes modified with transferrin. Int. J. Pharm. 2009, 373:116-123.
121. Suzuki R., et al. Effective anti-tumor activity of oxaliplatin encapsulated in transferrin-PEG-liposome. Int. J. Pharm. 2008, 346:143-150.
122. Wu J., et al. Reversal of multidrug resistance by liposomes co-encapsulating doxorubicin and verapamil. J. Pharm. Pharm. Sci. 2007, 10:350-357.
123. Kobayashi T., et al. Effect of transferrin receptor-targeted liposomal doxorubicin in P-glycoprotein-mediated drug resistant tumor cells. Int. J. Pharm. 2007, 329:94-102.
124. Xu L., et al. Systemic tumor-targeted gene delivery by anti-transferrin receptor scfv-immunoliposomes. Mol. Cancer Ther. 2002, 1:337-346.
125. Iinuma H., et al. Intracellular targeting therapy of cisplatin-encapsulated transferrin-polyethylene glycol liposome on peritoneal dissemination of gastric cancer. Int. J. Cancer 2002, 99:130-137.
126. Chiu S-J., et al. Efficient delivery of a Bcl-2-specific antisense oligodeoxyribonucleotide (G3139) via transferrin receptor-targeted liposomes. J. Control. Release 2006, 112:199-207.
127. Zhang X., et al. Transferrin receptor targeted lipopolyplexes for delivery of antisense oligonucleotide g3139 in a murine k562 xenograft model. Pharm. Res. 2009, 26:1516-1524.