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Journal of Oncology
Volume 2010, Article ID 723798, 8 pages
http://dx.doi.org/10.1155/2010/723798
Review Article

Peptide-Mediated Liposomal Drug Delivery System Targeting Tumor Blood Vessels in Anticancer Therapy

Institute of Cellular and Organismic Biology, Academia Sinica, Taipei 11529, Taiwan

Received 3 November 2009; Revised 13 January 2010; Accepted 3 March 2010

Academic Editor: Arkadiusz Dudek

Copyright © 2010 Han-Chung Wu and De-Kuan Chang. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. Bosslet, R. Straub, M. Blumrich et al., “Elucidation of the mechanism enabling tumor selective prodrug monotherapy,” Cancer Research, vol. 58, no. 6, pp. 1195–1201, 1998. View at Google Scholar · View at Scopus
  2. D. E. K. Chang, C. T. Lin, C. H. Wu, and H. A. N. C. Wu, “A novel peptide enhances therapeutic efficacy of liposomal anti-cancer drugs in mice models of human lung cancer,” PLoS ONE, vol. 4, no. 1, article e4171, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. R. K. Jain, “Transport of molecules in the tumor interstitium: a review,” Cancer Research, vol. 47, no. 12, pp. 3039–3051, 1987. View at Google Scholar · View at Scopus
  4. C. H. Heldin, K. Rubin, K. Pietras, and A. Ostman, “High interstitial fluid pressure—an obstacle in cancer therapy,” Nature Reviews Cancer, vol. 4, no. 10, pp. 806–813, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. H. C. Wu, D. K. Chang, and C. T. Huang, “Targeted-therapy for cancer,” Journal of Cancer Molecules, vol. 2, pp. 57–66, 2006. View at Google Scholar
  6. T. M. Allen and P. R. Cullis, “Drug delivery systems: entering the mainstream,” Science, vol. 303, no. 5665, pp. 1818–1822, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. D. A. Sipkins, D. A. Cheresh, M. R. Kazemi, L. M. Nevin, M. D. Bednarski, and K. C. P. Li, “Detection of tumor angiogenesis in vivo by alphaVbeta-targeted magnetic resonance imaging,” Nature Medicine, vol. 4, no. 5, pp. 623–626, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. A. G. Niethammer, R. Xiang, J. C. Becker et al., “A DNA vaccine against VEGF receptor 2 prevents effective angiogenesis and inhibits tumor growth,” Nature Medicine, vol. 8, no. 12, pp. 1369–1375, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. J. D. Hood, M. Bednarski, R. Frausto et al., “Tumor regression by targeted gene delivery to the neovasculature,” Science, vol. 296, no. 5577, pp. 2404–2407, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. K. Cho, X. U. Wang, S. Nie, Z. Chen, and D. M. Shin, “Therapeutic nanoparticles for drug delivery in cancer,” Clinical Cancer Research, vol. 14, no. 5, pp. 1310–1316, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. T. M. Allen, “Ligand-targeted therapeutics in anticancer therapy,” Nature Reviews Cancer, vol. 2, no. 10, pp. 750–763, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Pastorino, C. Brignole, D. Marimpietri et al., “Vascular damage and anti-angiogenic effects of tumor vessel-targeted liposomal chemotherapy,” Cancer Research, vol. 63, no. 21, pp. 7400–7409, 2003. View at Google Scholar · View at Scopus
  13. T. Y. Lee, C. T. Lin, S. Z. U. Y. Kuo, D. E. K. Chang, and H. A. N. C. Wu, “Peptide-mediated targeting to tumor blood vessels of lung cancer for drug delivery,” Cancer Research, vol. 67, no. 22, pp. 10959–10965, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Y. Lee, H. A. N. C. Wu, Y. U. N. L. Tseng, and C. T. Lin, “A novel peptide specifically binding to nasopharyngeal carcinoma for targeted drug delivery,” Cancer Research, vol. 64, no. 21, pp. 8002–8008, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Sapra and T. M. Allen, “Internalizing antibodies are necessary for improved therapeutic efficacy of antibody-targeted liposomal drugs,” Cancer Research, vol. 62, no. 24, pp. 7190–7194, 2002. View at Google Scholar · View at Scopus
  16. D.-K. Chang, C.-Y. Chiu, S.-Y. Kuo et al., “Antiangiogenic targeting liposomes increase therapeutic efficacy for solid tumors,” Journal of Biological Chemistry, vol. 284, no. 19, pp. 12905–12916, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. F. Pastorino, D. D. Paolo, F. Piccardi et al., “Enhanced antitumor efficacy of clinical-grade vasculature-targeted liposomal doxorubicin,” Clinical Cancer Research, vol. 14, no. 22, pp. 7320–7329, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. G. Bocci, K. C. Nicolaou, and R. S. Kerbel, “Protracted low-dose effects on human endothelial cell proliferation and survival in vitro reveal a selective antiangiogenic window for various chemotherapeutic drugs,” Cancer Research, vol. 62, no. 23, pp. 6938–6943, 2002. View at Google Scholar · View at Scopus
  19. T. Browder, C. E. Butterfield, B. M. Kräling et al., “Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer,” Cancer Research, vol. 60, no. 7, pp. 1878–1886, 2000. View at Google Scholar · View at Scopus
  20. D. Hanahan, G. Bergers, and E. Bergsland, “Less is, more, regularly: metronomic dosing of cytotoxic drugs can target tumor angiogenesis in mice,” The Journal of Clinical Investigation, vol. 105, no. 8, pp. 1045–1047, 2000. View at Google Scholar · View at Scopus
  21. G. Klement, S. Baruchel, J. Rak et al., “Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity,” The Journal of Clinical Investigation, vol. 105, no. 8, pp. 15–24, 2000. View at Google Scholar · View at Scopus
  22. H. Hurwitz, L. Fehrenbacher, W. Novotny et al., “Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer,” The New England Journal of Medicine, vol. 350, no. 23, pp. 2335–2342, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. R. J. Motzer, T. E. Hutson, P. Tomczak et al., “Sunitinib versus interferon alfa in metastatic renal-cell carcinoma,” The New England Journal of Medicine, vol. 356, no. 2, pp. 115–124, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. M. J. Ratain, T. I. M. Eisen, W. M. Stadler et al., “Phase II placebo-controlled randomized discontinuation trial of sorafenib in patients with metastatic renal cell carcinoma,” Journal of Clinical Oncology, vol. 24, no. 16, pp. 2505–2512, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Akino, K. Hida, Y. Hida et al., “Cytogenetic abnormalities of tumor-associated endothelial cells in human malignant tumors,” The American Journal of Pathology, vol. 175, no. 6, pp. 2657–2667, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. K. Hida, Y. Hida, D. N. Amin et al., “Tumor-associated endothelial cells with cytogenetic abnormalities,” Cancer Research, vol. 64, no. 22, pp. 8249–8255, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Denekamp, “Angiogenesis, neovascular proliferation and vascular pathophysiology as targets for cancer therapy,” The British Journal of Radiology, vol. 66, no. 783, pp. 181–196, 1993. View at Google Scholar · View at Scopus
  28. H. A. N. C. Wu and P. I. C. Li, “Proteins expressed on tumor endothelial cells as potential targets for anti-angiogenic therapy,” Journal of Cancer Molecules, vol. 4, no. 1, pp. 17–22, 2008. View at Google Scholar · View at Scopus
  29. R. K. Jain, “Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy,” Science, vol. 307, no. 5706, pp. 58–62, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. K. Pietras, K. Rubin, T. Sjoblom et al., “Inhibition of PDGF receptor signaling in tumor stroma enhances antitumor effect of chemotherapy,” Cancer Research, vol. 62, no. 19, pp. 5476–5484, 2002. View at Google Scholar · View at Scopus
  31. H. Wildiers, G. Guetens, G. De Boeck et al., “Effect of antivascular endothelial growth factor treatment on the intratumoral uptake of CPT-11,” British Journal of Cancer, vol. 88, no. 12, pp. 1979–1986, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. C. G. Willett, Y. Boucher, E. di Tomaso et al., “Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer,” Nature Medicine, vol. 10, no. 2, pp. 145–147, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. R. K. Jain, “Antiangiogenic therapy for cancer: current and emerging concepts,” Oncology, vol. 19, no. 4, supplement 3, pp. 7–16, 2005. View at Google Scholar · View at Scopus
  34. W. Arap, M. G. Kolonin, M. Trepel et al., “Steps toward mapping the human vasculature by phage display,” Nature Medicine, vol. 8, no. 2, pp. 121–127, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. M. L. Balestrieri and C. Napoli, “Novel challenges in exploring peptide ligands and corresponding tissue-specific endothelial receptors,” European Journal of Cancer, vol. 43, no. 8, pp. 1242–1250, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. W. Arap, R. Pasqualini, and E. Ruoslahti, “Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model,” Science, vol. 279, no. 5349, pp. 377–380, 1998. View at Publisher · View at Google Scholar · View at Scopus
  37. R. Pasqualini, E. Koivunen, R. Kain et al., “Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis,” Cancer Research, vol. 60, no. 3, pp. 722–727, 2000. View at Google Scholar · View at Scopus
  38. H. C. Wu, Y. L. Huang, T. T. Chao et al., “Identification of B-cell epitope of dengue virus type 1 and its application in diagnosis of patients,” Journal of Clinical Microbiology, vol. 39, no. 3, pp. 977–982, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. H. A. N. C. Wu, M. E. I. Y. Jung, C. Y. Chiu et al., “Identification of a dengue virus type 2 (DEN-2) serotype-specific B-cell epitope and detection of DEN-2-immunized animal serum samples using an epitope-based peptide antigen,” The Journal of General Virology, vol. 84, no. 10, pp. 2771–2779, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. U. N. C. Chen, H. N. Huang, C. T. Lin, Y. I. F. Chen, C. C. King, and H. A. N. C. Wu, “Generation and characterization of monoclonal antibodies against dengue virus type 1 for epitope mapping and serological detection by epitope-based peptide antigens,” Clinical and Vaccine Immunology, vol. 14, no. 4, pp. 404–411, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Atwell, M. Ultsch, A. M. De Vos, and J. A. Wells, “Structural plasticity in a remodeled protein-protein interface,” Science, vol. 278, no. 5340, pp. 1125–1128, 1997. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Nord, E. Gunneriusson, J. Ringdahl, S. Stahl, M. Uhlén, and P. E. R. A. Nygren, “Binding proteins selected from combinatorial libraries of an α-helical bacterial receptor domain,” Nature Biotechnology, vol. 15, no. 8, pp. 772–777, 1997. View at Google Scholar · View at Scopus
  43. B. Li, J. Y. K. Tom, D. Oare et al., “Minimization of a polypeptide hormone,” Science, vol. 270, no. 5242, pp. 1657–1660, 1995. View at Google Scholar · View at Scopus
  44. K. N. Sugahara, T. Teesalu, P. P. Karmali et al., “Tissue-penetrating delivery of compounds and nanoparticles into tumors,” Cancer Cell, vol. 16, no. 6, pp. 510–520, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. A. R. Castano, S. Tangri, J. E. W. Miller et al., “Peptide binding and presentation by mouse CD1,” Science, vol. 269, no. 5221, pp. 223–226, 1995. View at Google Scholar · View at Scopus
  46. J. Mai, S. Song, M. Rui et al., “A synthetic peptide mediated active targeting of cisplatin liposomes to Tie2 expressing cells,” Journal of Controlled Release, vol. 139, no. 3, pp. 174–181, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Folgori, R. Tafi, A. Meola et al., “A general strategy to identify mimotopes of pathological antigens using only random peptide libraries and human sera,” EMBO Journal, vol. 13, no. 9, pp. 2236–2243, 1994. View at Google Scholar · View at Scopus
  48. I. J. Liu, P. O. R. Hsueh, C. T. Lin et al., “Disease-specific B cell epitopes for serum antibodies from patients with severe acute respiratory syndrome (SARS) and serologic detection of SARS antibodies by epitope-based peptide antigens,” The Journal of Infectious Diseases, vol. 190, no. 4, pp. 797–809, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. L. Mazzucchelli, J. B. Burritt, A. J. Jesaitis et al., “Cell-specific peptide binding by human neutrophils,” Blood, vol. 93, no. 5, pp. 1738–1748, 1999. View at Google Scholar · View at Scopus
  50. A. Lo, C. T. Lin, and H. A. N. C. Wu, “Hepatocellular carcinoma cell-specific peptide ligand for targeted drug delivery,” Molecular Cancer Therapeutics, vol. 7, no. 3, pp. 579–589, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. A. F. S. A. Habeeb, “Determination of free amino groups in proteins by trinitrobenzenesulfonic acid,” Analytical Biochemistry, vol. 14, no. 3, pp. 328–336, 1966. View at Google Scholar · View at Scopus
  52. S. Zalipsky, N. Mullah, J. A. Harding, J. Gittelman, L. Guo, and S. A. DeFrees, “Poly(ethylene glycol)-grafted liposomes with oligopeptide or oligosaccharide ligands appended to the termini of the polymer chains,” Bioconjugate Chemistry, vol. 8, no. 2, pp. 111–118, 1997. View at Publisher · View at Google Scholar · View at Scopus
  53. D. Kirpotin, J. W. Park, K. Hong et al., “Sterically stabilized anti-HER2 immunoliposomes: design and targeting to human breast cancer cells in vitro,” Biochemistry, vol. 36, no. 1, pp. 66–75, 1997. View at Publisher · View at Google Scholar · View at Scopus
  54. F. Curnis, G. Arrigoni, A. Sacchi et al., “Differential binding of drugs containing the NGR motif to CD13 isoforms in tumor vessels, epithelia, and myeloid cells,” Cancer Research, vol. 62, no. 3, pp. 867–874, 2002. View at Google Scholar · View at Scopus
  55. L. Brannon-Peppas and J. O. Blanchette, “Nanoparticle and targeted systems for cancer therapy,” Advanced Drug Delivery Reviews, vol. 56, no. 11, pp. 1649–1659, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Duncan, “Polymer conjugates as anticancer nanomedicines,” Nature Reviews Cancer, vol. 6, no. 9, pp. 688–701, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. F. Muggia and A. Hamilton, “Phase III data on Caelyx in ovarian cancer,” European Journal of Cancer, vol. 37, supplement 9, pp. 15–18, 2001. View at Google Scholar · View at Scopus
  58. D. Papahadjopoulos, T. M. Allen, A. Gabizon et al., “Sterically stabilized liposomes: improvements in pharmacokinetics and antitumor therapeutic efficacy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 24, pp. 11460–11464, 1991. View at Google Scholar · View at Scopus
  59. G. T. Colbern, A. J. Hiller, R. S. Musterer, E. Pegg, I. C. Henderson, and P. K. Working, “Significant increase in antitumor potency of doxorubicin HCl by its encapsulation in pegylated liposomes,” Journal of Liposome Research, vol. 9, no. 4, pp. 523–538, 1999. View at Google Scholar · View at Scopus
  60. A. S. Abu Lila, Y. Doi, K. Nakamura, T. Ishida, and H. Kiwada, “Sequential administration with oxaliplatin-containing PEG-coated cationic liposomes promotes a significant delivery of subsequent dose into murine solid tumor,” Journal of Controlled Release, vol. 142, no. 2, pp. 167–173, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. R. Z. Orlowski, A. Nagler, P. Sonneveld et al., “Randomized phase III study of pegylated liposomal doxorubicin plus bortezomib compared with bortezomib alone in relapsed or refractory multiple myeloma: combination therapy improves time to progression,” Journal of Clinical Oncology, vol. 25, no. 25, pp. 3892–3901, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Safra, F. Muggia, S. Jeffers et al., “Pegylated liposomal doxorubicin (doxil): reduced clinical cardiotoxicity in patients reaching or exceeding cumulative doses of 500?mg/m2,” Annals of Oncology, vol. 11, no. 8, pp. 1029–1033, 2000. View at Publisher · View at Google Scholar · View at Scopus
  63. K. J. Harrington, S. Mohammadtaghi, P. S. Uster et al., “Effective targeting of solid tumors in patients with locally advanced cancers by radiolabeled pegylated liposomes,” Clinical Cancer Research, vol. 7, no. 2, pp. 243–254, 2001. View at Google Scholar · View at Scopus
  64. N. M. Marina, D. Cochrane, E. Harney et al., “Dose escalation and pharmacokinetics of pegylated liposomal doxorubicin (Doxil) in children with solid tumors: a pediatric oncology group study,” Clinical Cancer Research, vol. 8, no. 2, pp. 413–418, 2002. View at Google Scholar · View at Scopus
  65. G. Batist, “Cardiac safety of liposomal anthracyclines,” Cardiovascular Toxicology, vol. 7, no. 2, pp. 72–74, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. H. Hashizume, P. Baluk, S. Morikawa et al., “Openings between defective endothelial cells explain tumor vessel leakiness,” American Journal of Pathology, vol. 156, no. 4, pp. 1363–1380, 2000. View at Google Scholar · View at Scopus
  67. D. C. Drummond, O. Meyer, K. Hong, D. B. Kirpotin, and D. Papahadjopoulos, “Optimizing liposomes for delivery of chemotherapeutic agents to solid tumors,” Pharmacological Reviews, vol. 51, no. 4, pp. 691–743, 1999. View at Google Scholar · View at Scopus
  68. Y. Matsumura and H. Maeda, “A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs,” Cancer Research, vol. 46, no. 12, pp. 6387–6392, 1986. View at Google Scholar · View at Scopus
  69. H. Maeda, J. Wu, T. Sawa, Y. Matsumura, and K. Hori, “Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review,” Journal of Controlled Release, vol. 65, no. 1-2, pp. 271–284, 2000. View at Publisher · View at Google Scholar · View at Scopus
  70. D. W. Northfelt, F. J. Martin, P. Working et al., “Doxorubicin encapsulated in liposomes containing surface-bound polyethylene glycol: pharmacokinetics, tumor localization, and safety in patients with AIDS-related Kaposi's sarcoma,” Journal of Clinical Pharmacology, vol. 36, no. 1, pp. 55–63, 1996. View at Google Scholar · View at Scopus
  71. B. Uziely, S. Jeffers, R. Isacson et al., “Liposomal doxorubicin: antitumor activity and unique toxicities during two complementary phase I studies,” Journal of Clinical Oncology, vol. 13, no. 7, pp. 1777–1785, 1995. View at Google Scholar · View at Scopus
  72. K. B. Gordon, A. Tajuddin, J. Guitart, T. M. Kuzel, L. R. Eramo, and J. VonRoenn, “Hand-foot syndrome associated with liposome-encapsulated doxorubicin therapy,” Cancer, vol. 75, no. 8, pp. 2169–2173, 1995. View at Publisher · View at Google Scholar · View at Scopus
  73. Y. Matsumura, M. Gotoh, K. Muro et al., “Phase I and pharmacokinetic study of MCC-465, a doxorubicin (DXR) encapsulated in PEG immunoliposome, in patients with metastatic stomach cancer,” Annals of Oncology, vol. 15, no. 3, pp. 517–525, 2004. View at Publisher · View at Google Scholar · View at Scopus
  74. S. E. Al-Batran, J. Bischoff, G. Von Minckwitz et al., “The clinical benefit of pegylated liposomal doxorubicin in patients with metastatic breast cancer previously treated with conventional anthracyclines: a multicentre phase II trial,” British Journal of Cancer, vol. 94, no. 11, pp. 1615–1620, 2006. View at Publisher · View at Google Scholar · View at Scopus
  75. F. Pastorino, C. Brignole, D. Paolo et al., “Targeting liposomal chemotherapy via both tumor cell-specific and tumor vasculature-specific ligands potentiates therapeutic efficacy,” Cancer Research, vol. 66, no. 20, pp. 10073–10082, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. T. R. Shockley, K. Lin, J. A. Nagy, R. G. Tompkins, H. F. Dvorak, and M. L. Yarmush, “Penetration of tumor tissue by antibodies and other immunoproteins,” Annals of the New York Academy of Sciences, vol. 618, pp. 367–382, 1991. View at Google Scholar · View at Scopus
  77. G. P. Adams, R. Schier, A. M. McCall et al., “High affinity restricts the localization and tumor penetration of single-chain Fv antibody molecules,” Cancer Research, vol. 61, no. 12, pp. 4750–4755, 2001. View at Google Scholar · View at Scopus
  78. T. Mori, “Cancer-specific ligands identified from screening of peptide-display libraries,” Current Pharmaceutical Design, vol. 10, no. 19, pp. 2335–2343, 2004. View at Publisher · View at Google Scholar · View at Scopus
  79. E. M. Bolotin, R. Cohen, L. K. Bar et al., “Ammonium sulfate gradients for efficient and stable remote loading of amphipathic weak bases into liposomes and ligandoliposomes,” Journal of Liposome Research, vol. 4, no. 1, pp. 455–479, 1994. View at Google Scholar · View at Scopus
  80. N. L. Boman, D. Masin, L. D. Mayer, P. R. Cullis, and M. B. Bally, “Liposomal vincristine which exhibits increased drug retention and increased circulation longevity cures mice bearing P388 tumors,” Cancer Research, vol. 54, no. 11, pp. 2830–2833, 1994. View at Google Scholar · View at Scopus
  81. A. Gabizon, H. Shmeeda, and Y. Barenholz, “Pharmacokinetics of pegylated liposomal doxorubicin: review of animal and human studies,” Clinical Pharmacokinetics, vol. 42, no. 5, pp. 419–436, 2003. View at Publisher · View at Google Scholar · View at Scopus
  82. M. H. Vingerhoeds, P. A. Steerenberg, J. J. G. W. Hendriks et al., “Immunoliposome-mediated targeting of doxorubicin to human ovarian carcinoma in vitro and in vivo,” British Journal of Cancer, vol. 74, no. 7, pp. 1023–1029, 1996. View at Google Scholar · View at Scopus
  83. D. Goren, A. T. Horowitz, D. Tzemach, M. Tarshish, S. Zalipsky, and A. Gabizon, “Nuclear delivery of doxorubicin via folate-targeted liposomes with bypass of multidrug-resistance efflux pump,” Clinical Cancer Research, vol. 6, no. 5, pp. 1949–1957, 2000. View at Google Scholar · View at Scopus
  84. M. Sugano, N. K. Egilmez, S. J. Yokota et al., “Antibody targeting of doxorubicin-loaded liposomes suppresses the growth and metastatic spread of established human lung tumor xenografts in severe combined immunodeficient mice,” Cancer Research, vol. 60, no. 24, pp. 6942–6949, 2000. View at Google Scholar · View at Scopus
  85. J. W. Park, K. Hong, D. B. Kirpotin et al., “Anti-HER2 immunoliposomes: enhanced efficacy attributable to targeted delivery,” Clinical Cancer Research, vol. 8, no. 4, pp. 1172–1181, 2002. View at Google Scholar · View at Scopus