Antibody-targeted immunoliposomes for cancer treatment

Mini-Reviews in Medicinal Chemistry

Volumn 13, Issue 14, 2013, Pages 2026-2035

  Gao, Jie ^a,c   Chen, Huaiwen ^a   Song, Hao ^b   Su, Xiao ^a   Niu, Fangfang ^a   Li, Wei ^a   Li, Bohua ^a,c   Dai, Jianxin ^a,c   Wang, Hao ^a,c   Guo, Yajun ^a,b,c,d  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b LIAOCHENG UNIVERSITY   (China)

^c National Engineering Research Center for Antibody Medicine   (China)

^d CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

Antibodies conjugation; Antibody engineering; Cancer; Chemotherapy; Gene therapy; Immunoliposomes

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; ANTI DISIALOGANGLIOSIDE; ANTINEOPLASTIC AGENT; BEVACIZUMAB; BIOTIN; CAMPTOTHECIN; CETUXIMAB; DIOLEOYLPHOSPHATIDYL ETHANOLAMINE; DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR; IMMUNOLIPOSOME; NAVELBINE; NSC 701315; PACLITAXEL; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MDM2; STREPTAVIDIN; TOPOTECAN; TRANSFERRIN; TRASTUZUMAB; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN RECOGNITION; ANTINEOPLASTIC ACTIVITY; BINDING AFFINITY; CANCER THERAPY; CHEMOTHERAPY; COMPLEMENT DEPENDENT CYTOTOXICITY; CONJUGATION; CROSS LINKING; DRUG DELIVERY SYSTEM; HUMAN; HYDROPHILICITY; IMMUNE RESPONSE; IMMUNOGENICITY; NEOPLASM; NONHUMAN; OVERALL SURVIVAL; PHASE 2 CLINICAL TRIAL (TOPIC); PROTEIN ENGINEERING; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW;

ANIMALS; ANTIBODIES; ANTIBODIES, IMMOBILIZED; ANTINEOPLASTIC AGENTS; DRUG CARRIERS; HUMANS; HYDRAZONES; LIPOSOMES; NEOPLASMS; NUCLEIC ACIDS; SULFHYDRYL COMPOUNDS;

EID: 84893019822     PISSN: 13895575     EISSN: 18755607     Source Type: Journal    
DOI: 10.2174/1389557513666131119202717     Document Type: Review

References (116)

1. Ferlay, J.; Shin, H. R.; Bray, F.; Forman, D.; Mathers, C.; Parkin, D. M. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer, 2010, 127, 2893-917.
2. van der Bosch, J.; Zirvi, K. A. Growth state-specific responsiveness of primary cultures of a nude mouse-xenografted human colon carcinoma to 4'-deoxydoxorubicin and a crude human leukocyte alpha-interferon preparation. Cancer Res., 1982, 42, 3789-92.
3. Gogvadze, V.; Orrenius, S.; Zhivotovsky, B. Mitochondria in cancer cells: what is so special about them? Trends Cell Biol., 2008, 18, 165-73.
4. Block, K. I.; Koch, A. C.; Mead, M. N.; Tothy, P. K.; Newman, R. A.; Gyllenhaal, C. Impact of antioxidant supplementation on chemotherapeutic toxicity: a systematic review of the evidence from randomized controlled trials. Int. J. Cancer, 2008, 123, 1227-39.
5. Wang, J.; Huang, Y. Pharmacogenomics of sex difference in chemotherapeutic toxicity. Curr. Drug Discov. Technol., 2007, 4, 59-68.
6. Fan, C.; Foster, B. K.; Wallace, W. H.; Xian, C. J. Pathobiology and prevention of cancer chemotherapy-induced bone growth arrest, bone loss, and osteonecrosis. Curr. Mol. Med., 2011, 11, 140-51.
7. Kneuertz, P. J.; Maithel, S. K.; Staley, C. A.; Kooby, D. A. Chemotherapy-associated liver injury: impact on surgical management of colorectal cancer liver metastases. Ann. Surg. Oncol., 2011, 18, 181-90.
8. Rinaldi, M.; Cauchi, C.; Gridelli, C. First line chemotherapy in advanced or metastatic NSCLC. Ann. Oncol., 2006, 17 Suppl 5, v64-7.
9. Schrama, D.; Reisfeld, R. A.; Becker, J. C. Antibody targeted drugs as cancer therapeutics. Nat. Rev. Drug Discov., 2006, 5, 147-59.
10. Archakov, A. I. Nanobiotechnologies in medicine: nanodiagnostics and nanodrugs. Biochemistry (Moscow), 2010, 4, 2-14.
11. Feng, S. S. New-concept chemotherapy by nanoparticles of biodegradable polymers: where are we now? Nanomedicine (Lond.), 2006, 1, 297-309.
12. Allen, T. M.; Cullis, P. R. Drug delivery systems: entering the mainstream. Science, 2004, 303, 1818-22.
13. Moghimi, S. M.; Hunter, A. C.; Murray, J. C. Nanomedicine: current status and future prospects. FASEB J., 2005, 19, 311-30.
14. Bawarski, W. E.; Chidlowsky, E.; Bharali, D. J.; Mousa, S. A. Emerging nanopharmaceuticals. Nanomedicine, 2008, 4, 273-82.
15. Duncan, R. Polymer conjugates as anticancer nanomedicines. Nat. Rev. Cancer, 2006, 6, 688-701.
16. Gao, J.; Feng, S. S.; Guo, Y. Nanomedicine against multidrug resistance in cancer treatment. Nanomedicine (Lond.), 2012, 7, 465-8.
17. Matsumura, Y. &; Maeda, H. A new concept of macromolecular therapies in cancer chemotherapy: mechanism of tumortropic accumulation of proteins and the antitumor agent SMANCS. Cancer Res., 1986, 6, 6387-92.
18. Davis, M. E.; Chen, Z. G.; Shin, D. M. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat. Rev. Drug Discov. 2008, 7, 771-82.
19. Torchilin, V. P. Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov., 2005, 2, 145-60.
20. Schrama, D.; Reisfeld, R. A.; Becker, J. C. Antibody targeted drugs as cancer therapeutics. Nat. Rev. Drug Discov., 2006, 5, 147-59.
21. Adams, G. P.; Weiner, L. M. Monoclonal antibody therapy of cancer. Nat. Biotechnol., 2005, 23, 1147-57.
22. Zhang, T.; Herlyn, D. Combination of active specific immunotherapy or adoptive antibody or lymphocyte immunotherapy with chemotherapy in the treatment of cancer. Cancer Immunol. Immunother., 2009, 58, 475-92.
23. Beckman, R. A.; Weiner, L. M.; Davis, H. M. Antibody constructs in cancer therapy: protein engineering strategies to improve exposure in solid tumors. Cancer, 2007, 109, 170-79.
24. Kolkman, J. A.; Law, D. A. Nanobodies-from llamas to therapeutic proteins. Drug Discovery Today: Technologies, 2010, 2, 139-46.
25. Lee, R. J.; Low, P. S. Delivery of Liposomes to Cultured KB Cells via Folate Receptor-Mediated Endocytosis. J. Biol. Chem., 1994, 269, 3198-3204.
26. Lopes de Menezes, D. E.; Pilarski, L. M.; Allen, T. M. In vitro and in vivo targeting of immunoliposomal doxorubicin to human B-cell lymphoma. Cancer Res., 1998, 58, 3320-30.
27. Lopes de Menezes, D. E.; Kirchmeier, M. J.; Gagne, J. F.; Pilarski, L. M.; Allen, T. M. Cellular trafficking and cytotoxicity of anti-CD19-targeted liposomal doxorubicin in B lymphoma cells. J. Liposome Res., 1999, 9, 199-228.
28. Singh, M. Transferrin As A targeting ligand for liposomes and anticancer drugs. Curr. Pharm. Design, 1999, 5, 443-51.
29. Sugano, M.; Egilmez, N. K.; Yokota, S. J.; Chen, F. A.; Harding, J.; Huang, S. K.; Bankert, R. B. Antibody targeting of doxorubicinloaded liposomes suppresses the growth and metastatic spread of established human lung tumor xenografts in severe combined immunodeficient mice. Cancer Res., 2000, 60, 6942-49.
30. Abra, R. M.; Bankert, R. B.; Chen, F.; Egilmez, N. K.; Huang, K.; Saville, R.; Slater J. L.; Sugano, M.; Yokota, S. J. The next generation of liposome delivery systems: recent experience with tumor-targeted, sterically-stabilized immunoliposomes and activeloading gradients. J. Liposome Res., 2002, 12, 1-3.
31. Gao, J.; Kou, G.; Wang, H.; Chen, H. W.; Li, B. H.; Lu Y.; Zhang D. P.; Wang, S. H.; Hou, S.; Qian, W. Z.; Dai, J. X.; Zhao, J.; Zhong, Y. Q.; Guo, Y. PE38KDELloaded anti-HER2 nanoparticles inhibit breast tumor progression with reduced toxicity and immunogenicity. Breast Cancer Res. Treat., 2009, 115, 29-41.
32. Gao, J.; Kou, G.; Chen, H. W.; Wang H; Li, B. H.; Lu, Y.; Zhang, D. P.; Wang, S. H.; Hou, S.; Qian, W. Z.; Dai, J. X.; Zhao, J.; Zhong, Y. Q.; Guo, Y. Treatment of hepatocellular carcinoma in mice with PE38KDEL type I mutant-loaded poly(lactic-co-glycolic acid) nanoparticles conjugated with humanized SM5-1 F(ab') fragments. Mol. Cancer Ther., 2008, 7, 3399-407.
33. Gao, J.; Sun, J.; Li, H.; Liu, W.; Zhang, Y.; Li, B.; Qian, W.; Wang, H.; Chen, J.; Guo, Y. Lyophilized HER2-specific PEGylated immunoliposomes for active siRNA gene silencing. Biomaterials, 2010, 31, 2655-64.
34. Gao, J.; Feng, S. S.; Guo, Y. Antibody engineering promotes nanomedicine for cancer treatment. Nanomedicine (Lond), 2010, 5, 1141-5.
35. Kou, G.; Gao, J.; Wang, H.; Chen, H. W.; Li, B. H.; Zhang D. P.; Wang, S. H.; Hou, S.; Qian, W. Z.; Dai, J. X.; Zhong, Y. Q.; Guo, Y. Preparation and characterization of paclitaxel-loaded PLGA nanoparticles coated with cationic SM5-1 single-chain antibody. J. Biochem. Mol. Biol., 2007, 40, 731-39.
36. Sapra, P.; Tyagi, P.; Allen, T. M. Ligand-Targeted Liposomes for Cancer Treatment. Curr. Drug Delivery, 2005, 2, 369-381.
37. Dai, J.; Jin, J.; Li, B.; Wang, H.; Hou, S.; Qian, W.; Kou, G.; Zhang, D.; Li, J.; Tan, M.; Ma, J.; Guo, Y. A chimeric SM5-1 antibody inhibits hepatocellular carcinoma cell growth and induces caspase-dependent apoptosis. Cancer Lett., 2007, 258, 208-14.
38. Wu, L.; Wang, C.; Zhang, D.; Zhang, X.; Qian, W.; Zhao, L.; Wang, H.; Li, B.; Guo, Y. Characterization of a humanized anti-CD20 antibody with potent antitumor activity against B-cell lymphoma. Cancer Lett., 2010, 292, 208-14.
39. Li, B.; Wang, H.; Zhang, D.; Qian, W.; Hou, S.; Shi, S.; Zhao, L.; Kou, G.; Cao, Z.; Dai, J.; Guo, Y. Construction and characterization of a high-affinity humanized SM5-1 monoclonal antibody. Biochem. Biophys. Res. Commun., 2007, 357, 951-56.
40. Lonberg, N. Human antibodies from transgenic animals. Nat. Biotechnol., 2005, 23, 1117-25.
41. Jain, R. K.; Duda, D. G.; Clark, J. W.; Loeffler, J. S. Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nat. Clin. Pract. Oncol., 2006, 3, 24-40.
42. Cunningham, D.; Humblet, Y.; Siena, S.; Khayat, D.; Bleiberg, H.; Santoro, A.; Bets, D.; Mueser, M.; Harstrick, A.; Verslype, C.; Chau, I.; Van Cutsem, E. Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer. N. Engl. J. Med., 2004, 351, 337-45.
43. Hortobagyi, G. N. Treatment of breast cancer. N. Engl. J. Med., 1998, 339, 974-84.
44. Li, B.; Shi, S.; Qian, W.; Zhao, L.; Zhang, D.; Hou, S.; Zheng, L.; Dai, J.; Zhao, J.; Wang. H.; Guo, Y. Development of novel tetravalent anti-CD20 antibodies with potent antitumor activity. Cancer Res., 2008, 68, 2400-08.
45. Wu, C.; Ying, H.; Grinnell, C.; Bryant, S.; Miller, R.; Clabbers, A.; Bose, S.; McCarthy, D.; Zhu, R. R.; Santora, L.; Davis-Taber, R.; Kunes, Y.; Fung, E.; Schwartz, A.; Sakorafas, P.; Gu J.; Tarcsa, E.; Murtaza, A.; Ghayur, T. Simultaneous targeting of multiple disease mediators by a dual-variable-domain immunoglobulin. Nat. Biotechnol., 2007, 25, 1290-97.
46. Hudson, P. J.; Kortt, A. A. High avidity scFv multimers; diabodies and triabodies. J. Immunol. Methods, 1999, 231, 177-189.
47. Holt, L. J.; Herring, C.; Jespers, L. S.; Woolven, B. P.; Tomlinson, I. M. Tomlinson Domain antibodies: proteins for therapy. Trends Biotechnol., 2003, 21, 484-90.
48. Qiu, X. Q.; Wang, H.; Cai, B.; Wang, L. L.; Yue, S. T. Small antibody mimetics comprising two complementarity-determining regions and a framework region for tumor targeting. Nature biotechnology. Nat Biotechnol., 2007, 25, 921-29.
49. Traut, R. R.; Bollen, A.; Sun, R. R.; Hershey, J. W.; Sundberg, B. J.; Pierce, L. R. Methyl 4-mercaptobutyrimidate as a cleavable crosslinking reagent and its application to the Escherichia coli 30s ribosome. Biochemistry, 1973, 12, 3266-73.
50. Carlsson, J.; Drevin, H.; Axen, R. Protein thiolation and reversible protein-protein conjugation. N-Succinimidyl 3(2-pyridyldithio) propionate, a new heterobifunctional reagent. Biochem. J., 1978, 173, 723-37.
51. Thorpe, P. E.; Wallace, P. M.; Knowles, P. P.; Relf, M. G.; Brown, A. N.; Watson, G. J.; Knyba, R. E.; Wawrzynczak, E. J.; Blakey, D. C. New coupling agents for the synthesis of immunotoxins containing a hindered disulfide bond with improved stability in vivo. Cancer Res., 1987, 47, 5924-31.
52. Duncan, R. J.; Weston, P. D.; Wrigglesworth, R. A new reagent which may be used to introduce sulfhydryl groups into proteins, and its use in the preparation of conjugates for immunoassay. Anal. Biochem., 1983, 132, 68-73.
53. Klotz, I. M.; Heiney, R. E. Introduction of sulfhydryl groups into proteins using acetylmercaptosuccinic anhydride. Arch. Biochem. Biophys., 1962, 96, 605-12.
54. Wegner, G. J.; Lee, H. J.; Marriott, G.; Corn, R. M. Fabrication of histidine-tagged fusion protein arrays for surface plasmon resonance imaging studies of protein-protein and protein-DNA interactions. Anal. Chem., 2005, 75, 4740-6.
55. Martin, F. J.; Hubbell, W. L.; Papahadjopoulos, D. Immunospecific targeting of liposomes to cells: a novel and efficient method forcovalent attachment of Fab' fragments via disulfide bonds. Biochemistry, 1981, 20, 4229-38.
56. Ivanov, V. O.; Preobrazhensky, S. N.; Tsibulsky, V. P.; Babaev, V. R.; Repin, V. S.; Smirnov, V. N. Liposome uptake by cultured macrophages mediated by modified low-density lipoproteins. Biochim. Biophys. Acta., 1985, 846, 76-84.
57. Leserman, L. D.; Barbet, J.; Kourilsky, F.; Weinstein, J. N. Targeting to cells of fluorescent liposomes covalently coupled with monoclonal antibody or protein A. Nature, 1980, 288, 602-4.
58. Suzuki, R.; Takizawa, T.; Kuwata, Y.; Mutoh, M.; Ishiguro, N.; Utoguchi, N.; Shinohara, A.; Eriguchi, M.; Yanagie, H.; Maruyama, K. Effective anti-tumor activity of oxaliplatin encapsulated in transferrin-PEG-liposome. Int. J. Pharm., 2008, 346, 43-50.
59. Ying, X.; Wen, H.; Lu, W. L.; Du, J.; Guo, J.; Tian, W.; Men, Y.; Zhang, Y.; Li, R. J.; Yang, T. Y.; Shang, D. W.; Lou, J. N.; Zhang, L. R.; Zhang, Q. Dual-targeting daunorubicin liposomes improve the therapeutic efficacy of brain glioma in animals. J. Control. Release, 2010, 141, 183-92.
60. Koning, G. A.; Kamps, J. A.; Scherphof, G. L. Efficient intracellular delivery of 5-fluorodeoxyuridine into colon cancer cells by targeted immunoliposomes. Cancer Detect. Prev., 2002, 26, 299-307.
61. Harding, J. A.; Engbers, C. M.; Newman, M. S.; Goldstein, N. I.; Zalipsky, S. Immunogenicity and pharmacokinetic attributes of poly(ethylene glycol)-grafted immunoliposomes. Biochim. Biophys. Acta., 1997, 1327, 181-92.
62. Torchilin, V. P.; Khaw, B. A.; Smirnov, V. N.; Haber, E. Preservation of antimyosin antibody activity after covalent coupling to liposomes. Biochem. Biophys. Res. Commun., 1979, 89, 1114-9.
63. Torchilin, V. P.; Goldmacher, V. S.; Smirnov, V. N. Comparative studies on covalent and noncovalent immobilization of protein molecules on the surface of liposomes. Biochem. Biophys. Res. Commun., 1978, 85, 983-90.
64. Huang, L.; Kennel, S. J. Binding of immunoglobulin G to phospholipid vesicles by sonication. Biochemistry, 1979, 18, 1702-7.
65. Ko. Y. T.; Bhattacharya, R.; Bickel, U. Liposome encapsulated polyethylenimine/ODN polyplexes for brain targeting. J. Control. Release, 2009, 133, 230-7.
66. Xiao, Z.; McQuarrie, S. A.; Suresh, M. R.; Mercer, J. R.; Gupta, S.; Miller, G. G. A three-step strategy for targeting drug carriers to human ovarian carcinoma cells in vitro. J. Biotechnol., 2002, 94, 171-84.
67. Schnyder, A.; Krähenbühl, S.; Török, M.; Drewe, J.; Huwyler, J. Targeting of skeletal muscle in vitro using biotinylated immunoliposomes. Biochem. J., 2004, 377, 61-67.
68. Sapra, P.; Allen, T. M. Ligand-targeted liposomal anticancer drugs. Prog. Lipid Res., 2003, 42, 439-62.
69. Park, J. W.; Hong, K.; Kirpotin, D. B.; Colbern, G.; Shalaby, R.; Baselga, J.; Shao, Y.; Nielsen, U. B.; Marks, J. D.; Moore, D.; Papahadjopoulos, D.; Benz, C. C. Anti-HER2 immunoliposomes: enhanced efficacy attributable to targeted delivery. Clin. Cancer Res., 2002, 8, 1172-81.
70. 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, 517-25.
71. Chen, H.; Gao, J.; Lu, Y.; Kou, G.; Zhang, H.; Fan, L.; Sun, Z.; Guo, Y.; Zhong, Y. Preparation and characterization of PE38KDEL-loaded anti-HER2 nanoparticles for targeted cancer therapy. J. Control. Release, 2008, 128, 209-16.
72. Gao, J.; Zhong, W.; He, J.; Li, H.; Zhang, H.; Zhou, G.; Li, B.; Lu, Y.; Zou, H.; Kou, G.; Zhang, D.; Wang, H.; Guo, Y.; Zhong, Y. Tumor-targeted PE38KDEL delivery via PEGylated anti-HER2 immunoliposomes. Int. J. Pharm., 2009, 374, 145-52.
73. Provoda, C. J.; Stier, E. M.; Lee, K. D. Tumor cell killing enabled by listeriolysin O-liposome-mediated delivery of the protein toxin gelonin. J. Biol. Chem., 2003, 278, 35102-8.
74. Pazo Cid, R. A.; Lao, J.; Lanzuela, M. Doxorubicin plus sorafenib in treatment of advanced hepatocellular carcinoma. JAMA., 2011, 305, 781.
75. Park, J. W.; Benz, C. C.; Martin, F. J. Future directions of liposomeand immunoliposome-based cancer therapeutics. Semin. Oncol., 2004, 31, 196-205.
76. Nielsen, U. B.; Kirpotin, D. B.; Pickering, E. M.; Hong, K.; Park, J. W.; Refaat, Shalaby M.; Shao, Y.; Benz, C. C.; Marks, J. D. Therapeutic efficacy of anti-ErbB2 immunoliposomes targeted by a phage antibody selected for cellular endocytosis. Biochim. Biophys. Acta., 2002, 1591, 109-18.
77. Park, J. W.; Kirpotin, D. B.; Hong, K.; Shalaby, R.; Shao, Y.; Nielsen, U. B.; Marks, J. D.; Papahadjopoulos, D.; Benz, C. C. Tumor targeting using anti-her2 immunoliposomes. J. Control. Release, 2001, 74, 95-113.
78. Anhorn, M. G.; Wagner, S.; Kreuter, J.; Langer, K.; von Briesen, H. Specific targeting of HER2 overexpressing breast cancer cells with doxorubicin-loaded trastuzumab-modified human serum albumin nanoparticles. Bioconjug. Chem., 2008, 19, 2321-31.
79. Laginha, K. M,; Moase, E. H.; Yu, N.; Huang, A.; Allen, T. M. Bioavailability and therapeutic efficacy of HER2 scFv-targeted liposomal doxorubicin in a murine model of HER2-overexpressing breast cancer. J. Drug Target, 2008, 16, 605-10.
80. Park, J. W.; Benz, C. C.; Martin, F. J. Future directions of liposomeand immunoliposome-based cancer therapeutics. Semin. Oncol., 2004, 31, 196-205.
81. Pastorino, F.; Brignole, C.; Marimpietri, D.; Sapra, P.; Moase, E. H.; Allen, T. M.; Ponzoni, M. Doxorubicin-loaded Fab' fragments of anti-disialoganglioside immunoliposomes selectively inhibit the growth and dissemination of human neuroblastoma in nude mice. Cancer Res., 2003, 63, 86-92.
82. Wani, M. C.; Taylor, H. L.; Wall, M. E.; Coggon, P.; McPhail, A. T. Plant antitumor agents. VI. The isolation and structure of taxol, a novelantileukemic and antitumor agent from Taxus brevifolia. J. Am. Chem. Soc., 1971, 93, 2325-7.
83. Yang, T.; Choi, M. K.; Cui, F. D.; Kim, J. S.; Chung, S. J.; Shim, C. K.; Kim, D. D. Preparation and evaluation of paclitaxel-loaded PEGylated immunoliposome. J. Control. Release, 2007, 120, 169-77.
84. Yang, T.; Choi, M. K.; Cui, F. D.; Lee, S. J.; Chung, S. J.; Shim, C. K.; Kim, D. D. Antitumor effect of paclitaxel-loaded PEGylated immunoliposomes against human breast cancer cells. Pharm. Res., 2007, 24, 2402-11.
85. Mamot, C.; Drummond, D. C.; Noble, C. O.; Kallab, V.; Guo, Z.; Hong, K.; Kirpotin, D. B.; Park, J. W. Epidermal growth factor receptor-targeted immunoliposomes significantly enhance the efficacy of multiple anticancer drugs in vivo. Cancer Res., 2005, 65, 11631-8.
86. Drummond, D. C.; Noble, C. O.; Guo, Z.; Hayes, M. E.; Connolly-Ingram, C.; Gabriel, B. S.; Hann, B.; Liu, B.; Park, J. W.; Hong, K.; Benz, C. C.; Marks, J. D.; Kirpotin, D. B. Development of a highly stable and targetable nanoliposomal formulation of topotecan. J. Control. Release, 2010, 141, 13-21.
87. Modak, S.; Cheung, N. K. Neuroblastoma: Therapeutic strategies for a clinical enigma. Cancer Treat. Rev., 2010, 36, 307-17.
88. Children's Oncology Group (CCG 09709), Villablanca, J. G.; Krailo, M. D.; Ames, M. M.; Reid, J. M.; Reaman, G. H.; Reynolds, C. P. Phase I trial of oral fenretinide in children with high-risk solid tumors: a report from the Children's Oncology Group (CCG 09709). J. Clin. Oncol., 2006, 24, 3423-30.
89. Raffaghello, L.; Pagnan, G.; Pastorino, F.; Cosimo, E.; Brignole, C.; Marimpietri, D.; Montaldo, P. G.; Gambini, C.; Allen, T. M.; Bogenmann, E.; Ponzoni, M. In vitro and in vivo antitumor activity of liposomal Fenretinide targeted to human neuroblastoma. Int. J. Cancer, 2003, 104, 559-67.
90. Devi, G. R. siRNA-based approaches in cancer therapy. Cancer Gene Ther., 2006, 13, 819-29.
91. Hussain, S.; Plückthun, A.; Allen, T. M.; Zangemeister-Wittke, U. Chemosensitization of carcinoma cells using epithelial cell adhesion molecule-targeted liposomal antisense against bcl-2/bclxL. Mol. Cancer Ther., 2006, 5, 3170-80.
92. Stuart, D. D.; Kao, G. Y.; Allen, T. M. A novel, long-circulating, and functional liposomal formulation of antisense oligodeoxynucleotides targeted against MDR1. Cancer Gene Ther., 2000, 7, 466-75.
93. Stuart, D. D.; Allen, T. M. A new liposomal formulation for antisense oligodeoxynucleotides with small size, high incorporation efficiency and good stability. Biochim. Biophys. Acta., 2000, 1463, 219-29.
94. Xu, L.; Pirollo, K. F.; Chang, E. H. Tumor-targeted p53-gene therapy enhances the efficacy of conventionalchemo/radiotherapy. J. Control Release, 2001, 74, 115-28.
95. Xu, L.; Huang, C. C.; Huang, W.; Tang, W. H.; Rait, A.; Yin, Y. Z.; Cruz, I.; Xiang, L. M.; Pirollo, K. F.; Chang, E. H. Systemic tumortargeted gene delivery by anti-transferrin receptor scFvimmunoliposomes. Mol. Cancer Ther., 2002, 1, 337-46.
96. Pirollo, K. F.; Rait, A.; Zhou, Q.; Zhang, X. Q.; Zhou, J.; Kim, C. S.; Benedict, W. F.; Chang, E. H. Tumor-targeting nanocomplex delivery of novel tumor suppressor RB94 chemosensitizes bladder carcinoma cells in vitro and in vivo. Clin. Cancer Res., 2008, 14, 2190-8.
97. Pirollo, K. F.; Zon, G.; Rait, A.; Zhou, Q.; Yu, W.; Hogrefe, R.; Chang, E. H. Tumor-targeting nanoimmunoliposome complex for short interfering RNA delivery. Hum. Gene Ther., 2006, 17, 117-24.
98. Pirollo, K. F.; Rait, A.; Zhou, Q.; Hwang, S. H.; Dagata, J. A.; Zon, G.; Hogrefe, R. I.; Palchik, G.; Chang, E. H. Materializing the potential of small interfering RNA via a tumor-targeting nanodelivery system. Cancer Res., 2007, 67, 2938-43.
99. Shi, N.; Pardridge, W. M. Noninvasive gene targeting to the brain. Proc. Natl. Acad. Sci. U S A, 2000, 97, 7567-72.
100. Shi, N.; Zhang, Y.; Zhu, C.; Boado, R. J.; Pardridge, W. M. Brainspecific expression of an exogenous gene after i. v. administration. Proc. Natl. Acad. Sci. U S A, 2001, 98, 12754-9.
101. Shi, N.; Boado, R. J.; Pardridge, W. M. Receptor-mediated gene targeting to tissues in vivo following intravenous administration of pegylated immunoliposomes. Pharm. Res., 2001, 18, 1091-5.
102. Zhang, Y.; Zhang, Y. F.; Bryant, J.; Charles, A.; Boado, R. J.; Pardridge, W. M. Intravenous RNA interference gene therapy targeting the human epidermal growth factor receptor prolongs survival in intracranial brain cancer. Clin. Cancer Res., 2004, 10, 3667-77.
103. Peer, D.; Park, E. J.; Morishita, Y.; Carman, C. V.; Shimaoka, M. Systemic leukocyte-directed siRNA delivery revealing cyclin D1 as an anti-inflammatory target. Science, 2008, 319, 627-30.
104. Pagnan, G.; Stuart, D. D.; Pastorino, F.; Raffaghello, L.; Montaldo, P. G.; Allen, T. M.; Calabretta, B.; Ponzoni, M. Delivery of c-myb antisense oligodeoxynucleotides to human neuroblastoma cells via disialoganglioside GD(2)-targeted immunoliposomes: antitumor effects. J. Natl. Cancer Inst., 2000, 92, 253-61.
105. Brignole, C.; Pastorino, F.; Marimpietri, D.; Pagnan, G.; Pistorio, A.; Allen, T. M.; Pistoia, V.; Ponzoni, M. Immune cell-mediated antitumor activities of GD2-targeted liposomal c-myb antisense oligonucleotides containing CpG motifs. J. Natl. Cancer Inst., 2004, 96, 1171-80.
106. Di, Paolo. D.; Brignole, C.; Pastorino, F.; Carosio, R.; Zorzoli, A.; Rossi, M.; Loi, M.; Pagnan, G.; Emionite, L.; Cilli, M.; Bruno, S.; Chiarle, R.; Allen, T. M.; Ponzoni, M.; Perri, P. Neuroblastomatargeted nanoparticles entrapping siRNA specifically knockdown ALK. Mol. Ther., 2011, 19, 1131-40.
107. Di, Paolo. D.; Ambrogio, C.; Pastorino, F.; Brignole, C.; Martinengo, C.; Carosio, R.; Loi, M.; Pagnan, G.; Emionite, L.; Cilli, M.; Ribatti, D.; Allen, T. M.; Chiarle, R.; Ponzoni, M.; Perri, P. Selective therapeutic targeting of the anaplastic lymphoma kinase with liposomal siRNA induces apoptosis and inhibits angiogenesis in neuroblastoma. Mol. Ther., 2011, 19, 2201-12.
108. Li, S. D.; Chono, S.; Huang, L. Efficient gene silencing in metastatic tumor by siRNA formulated in surface-modified nanoparticles. J. Control. Release, 2008, 126, 77-84.
109. Li, S. D.; Chen, Y. C.; Hackett, M. J.; Huang, L. Tumor-targeted delivery of siRNA by self-assembled nanoparticles. Mol. Ther., 2008, 16, 163-9.
110. Chen, Y.; Zhu, X.; Zhang, X.; Liu, B.; Huang, L. Nanoparticles modified with tumor-targeting scFv deliver siRNA and miRNA forcancer therapy. Mol. Ther., 2010, 18, 1650-6.
111. Gao, J.; Liu, W.; Xia, Y.; Li, W.; Sun, J.; Chen, H.; Li, B.; Zhang, D.; Qian, W.; Meng, Y.; Deng, L.; Wang, H.; Chen, J.; Guo, Y. The promotion of siRNA delivery to breast cancer overexpressing epidermal growth factor receptor through anti-EGFR antibody conjugation by immunoliposomes. Biomaterials, 2011, 32, 3459-70.
112. Gao, J.; Yu, Y.; Zhang, Y.; Song, J.; Chen, H.; Li, W.; Qian, W.; Deng, L.; Kou, G.; Chen, J.; Guo, Y. EGFR-specific PEGylated immunoliposomes for active siRNA delivery in hepatocellular carcinoma. Biomaterials, 2012, 33, 270-82.
113. Gao, J.; Chen, H.; Yu, Y.; Song, J.; Song, H.; Su, X.; Li, W.; Tong, X.; Qian, W.; Wang, H.; Dai, J.; Guo, Y. Inhibition of hepatocellular carcinoma growth using immunoliposomes for codelivery of adriamycin and ribonucleotide reductase M2 siRNA. Biomaterials, 2013, 34, 10084-98.
114. Lammers, T.; Kiessling, F.; Hennink, W. E.; Storm, G. Nanotheranostics and image-guided drug delivery: current concepts and future directions. Mol. Pharm., 2010, 7, 1899-912.
115. Cho, H.; Magid, R.; Danila, D. C.; Hunsaker, T.; Pinkhassik, E.; Hasty, K. A. Theranostic immunoliposomes for osteoarthritis. Nanomedicine, 2013, doi: 10. 1016/j. nano. 2013. 09. 004.
116. Deng, L.; Ke, X.; He, Z.; Yang, D.; Gong, H.; Zhang, Y.; Jing, X.; Yao, J.; Chen, J. A MSLN-targeted multifunctional nanoimmunoliposome for MRI and targeting therapy in pancreatic cancer. Int. J. Nanomedicine, 2012, 7, 5053-65.