Accumulation and toxicity of antibody-targeted doxorubicin-loaded PEG-PE micelles in ovarian cancer cell spheroid model

Journal of Controlled Release

Volumn 164, Issue 1, 2012, Pages 95-102

  Perche, Federico ^a   Patel, Niravkumar R ^a   Torchilin, Vladimir P ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Cancer cell spheroids; Doxorubicin; Immunomicelles; Targeting

Indexed keywords

CANCER CELLS; DOXORUBICIN; END-LABELING; ETHANOLAMINES; IMMUNOMICELLES; LACTATE DEHYDROGENASE; OVARIAN CANCER CELLS; OVARIAN CANCERS; OVARIAN CARCINOMA; TARGETED DRUG DELIVERY; TARGETING;

ANTIBODIES; CELLS; CONFOCAL MICROSCOPY; DISEASES; DRUG DELIVERY; FLOW CYTOMETRY; PATIENT TREATMENT; POLYETHYLENE GLYCOLS; TOXICITY;

MICELLES;

DOXORUBICIN; MACROGOL; MONOCLONAL ANTIBODY 2C5 DOXORUBICIN POLYETHYLENEGLYCOL PHOSPHATIDYLETHANOLAMINE IMMUNOMICELLE; PHOSPHATIDYLETHANOLAMINE; UNCLASSIFIED DRUG;

ARTICLE; DRUG CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG FORMULATION; DRUG TARGETING; DRUG UPTAKE; MICELLE; OVARY CANCER; PRIORITY JOURNAL; SPHEROID CELL;

ANTIBIOTICS, ANTINEOPLASTIC; ANTIBODIES, MONOCLONAL; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; DOXORUBICIN; DRUG CARRIERS; FEMALE; FLOW CYTOMETRY; HUMANS; IN SITU NICK-END LABELING; MICELLES; MICROSCOPY, CONFOCAL; OVARIAN NEOPLASMS; PHOSPHATIDYLETHANOLAMINES; POLYETHYLENE GLYCOLS; PROTO-ONCOGENE PROTEINS C-BCL-2; SPHEROIDS, CELLULAR;

EID: 84869498365     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2012.09.003     Document Type: Article

References (72)

1. World Health Organization, Cancer. Fact Sheet # 297, in, 2011.
2. D.M. Parkin, F. Bray, J. Ferlay, and P. Pisani Global cancer statistics, 2002 CA Cancer J. Clin. 55 2005 74 108
3. W.P. McGuire III, and M. Markman Primary ovarian cancer chemotherapy: current standards of care Br. J. Cancer 89 Suppl. 3 2003 S3 S8
4. M.A. Bookman, M.F. Brady, W.P. McGuire, P.G. Harper, D.S. Alberts, M. Friedlander, N. Colombo, J.M. Fowler, P.A. Argenta, K. De Geest, D.G. Mutch, R.A. Burger, A.M. Swart, E.L. Trimble, C. Accario-Winslow, and L.M. Roth Evaluation of new platinum-based treatment regimens in advanced-stage ovarian cancer: a Phase III Trial of the Gynecologic Cancer Intergroup J. Clin. Oncol. 27 2009 1419 1425
5. B.T. Hennessy, R.L. Coleman, and M. Markman Ovarian cancer Lancet 374 2009 1371 1382
6. G. Szakacs, J.K. Paterson, J.A. Ludwig, C. Booth-Genthe, and M.M. Gottesman Targeting multidrug resistance in cancer Nat. Rev. Drug Discov. 5 2006 219 234
7. I. Bozic, B. Allen, and M.A. Nowak Dynamics of targeted cancer therapy Trends Mol. Med. 18 2012 311 316
8. C. Carvalho, R.X. Santos, S. Cardoso, S. Correia, P.J. Oliveira, M.S. Santos, and P.I. Moreira Doxorubicin: the good, the bad and the ugly effect Curr. Med. Chem. 16 2009 3267 3285
9. A. Shapira, Y.D. Livney, H.J. Broxterman, and Y.G. Assaraf Nanomedicine for targeted cancer therapy: towards the overcoming of drug resistance Drug Resist. Updat. 14 2011 150 163
10. W.C. Zamboni, V. Torchilin, A.K. Patri, J. Hrkach, S. Stern, R. Lee, A. Nel, N.J. Panaro, and P. Grodzinski Best practices in cancer nanotechnology: perspective from NCI nanotechnology alliance Clin. Cancer Res. 18 2012 3229 3241
11. C.H. Choi, C.A. Alabi, P. Webster, and M.E. Davis Mechanism of active targeting in solid tumors with transferrin-containing gold nanoparticles Proc. Natl. Acad. Sci. U. S. A. 107 2010 1235 1240
12. D. Kim, Z.G. Gao, E.S. Lee, and Y.H. Bae In vivo evaluation of doxorubicin-loaded polymeric micelles targeting folate receptors and early endosomal pH in drug-resistant ovarian cancer Mol. Pharm. 6 2009 1353 1362
13. S.P. Egusquiaguirre, M. Igartua, R.M. Hernandez, and J.L. Pedraz Nanoparticle delivery systems for cancer therapy: advances in clinical and preclinical research Clin. Transl. Oncol. 14 2012 83 93
14. E.A. Dubikovskaya, S.H. Thorne, T.H. Pillow, C.H. Contag, and P.A. Wender Overcoming multidrug resistance of small-molecule therapeutics through conjugation with releasable octaarginine transporters Proc. Natl. Acad. Sci. U. S. A. 105 2008 12128 12133
15. Y. Matsumura, T. Hamaguchi, T. Ura, K. Muro, Y. Yamada, Y. Shimada, K. Shirao, T. Okusaka, H. Ueno, M. Ikeda, and N. Watanabe Phase I clinical trial and pharmacokinetic evaluation of NK911, a micelle-encapsulated doxorubicin Br. J. Cancer 91 2004 1775 1781
16. Y. Barenholz Doxil(R) - the first FDA-approved nano-drug: lessons learned J. Control. Release 160 2012 117 134
17. E. Pujade-Lauraine, U. Wagner, E. Aavall-Lundqvist, V. Gebski, M. Heywood, P.A. Vasey, B. Volgger, I. Vergote, S. Pignata, A. Ferrero, J. Sehouli, A. Lortholary, G. Kristensen, C. Jackisch, F. Joly, C. Brown, N. Le Fur, and A. du Bois Pegylated liposomal doxorubicin and carboplatin compared with paclitaxel and carboplatin for patients with platinum-sensitive ovarian cancer in late relapse J. Clin. Oncol. 28 2010 3323 3329
18. A.N. Gordon, M. Tonda, S. Sun, and W. Rackoff Long-term survival advantage for women treated with pegylated liposomal doxorubicin compared with topotecan in a phase 3 randomized study of recurrent and refractory epithelial ovarian cancer Gynecol. Oncol. 95 2004 1 8
19. B. Desoize, D. Gimonet, and J.C. Jardillier Multicellular resistance: another mechanisms of pleiotropic resistance? Bull. Cancer 85 1998 785 793
20. T.T. Goodman, C.P. Ng, and S.H. Pun 3-D tissue culture systems for the evaluation and optimization of nanoparticle-based drug carriers Bioconjug. Chem. 19 2008 1951 1959
21. D. Khaitan, and B.S. Dwarakanath Multicellular spheroids as an in vitro model in experimental oncology: applications in translational medicine Expert Opin. Drug Discovery 1 2006 663 675
22. G. Mehta, A.Y. Hsiao, M. Ingram, G.D. Luker, and S. Takayama Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy J. Control. Release 2012 (Electronic publication ahead of print)
23. F. Pampaloni, E.G. Reynaud, and E.H. Stelzer The third dimension bridges the gap between cell culture and live tissue Nat. Rev. Mol. Cell Biol. 8 2007 839 845
24. F. Perche, and V.P. Torchilin Cancer cell spheroids as a model to evaluate chemotherapy protocols Cancer Biol. Ther. 13 2012
25. H. Karlsson, M. Fryknas, R. Larsson, and P. Nygren Loss of cancer drug activity in colon cancer HCT-116 cells during spheroid formation in a new 3-D spheroid cell culture system Exp. Cell Res. 318 2012 1577 1585
26. J. Ou, W. Luan, J. Deng, R. Sa, and H. Liang alphaV integrin induces multicellular radioresistance in human nasopharyngeal carcinoma via activating SAPK/JNK pathway PLoS One 7 2012 e38737
27. S.H. Jang, M.G. Wientjes, D. Lu, and J.L. Au Drug delivery and transport to solid tumors Pharm. Res. 20 2003 1337 1350
28. R.E. Durand Slow penetration of anthracyclines into spheroids and tumors: a therapeutic advantage? Cancer Chemother. Pharmacol. 26 1990 198 204
29. T.M. Yang, D. Barbone, D.A. Fennell, and V.C. Broaddus Bcl-2 family proteins contribute to apoptotic resistance in lung cancer multicellular spheroids Am. J. Respir. Cell Mol. Biol. 41 2009 14 23
30. P.A. Kenny, G.Y. Lee, C.A. Myers, R.M. Neve, J.R. Semeiks, P.T. Spellman, K. Lorenz, E.H. Lee, M.H. Barcellos-Hoff, O.W. Petersen, J.W. Gray, and M.J. Bissell The morphologies of breast cancer cell lines in three-dimensional assays correlate with their profiles of gene expression Mol. Oncol. 1 2007 84 96
31. N. Howlader, A.M. Noone, M. Krapcho, N. Neyman, R. Aminou, S.F. Altekruse, C.L. Kosary, J. Ruhl, Z. Tatalovich, H. Cho, A. Mariotto, M.P. Eisner, D.R. Lewis, H.S. Chen, E.J. Feuer, K.A. Cronin, (eds), in, SEER Cancer Statistics Review, 1975-2009 (Vintage 2009 Populations), National Cancer Institute. Bethesda, MD, http://seer.cancer.gov/csr/1975-2009-pops09/, based on November 2011 SEER data submission, posted to the SEER web site, 2012.
32. R.A. Davidowitz, M.P. Iwanicki, and J.S. Brugge In vitro mesothelial clearance assay that models the early steps of ovarian cancer metastasis J. Vis. Exp. 60 2012 pii: 3888
33. K. Shield, M.L. Ackland, N. Ahmed, and G.E. Rice Multicellular spheroids in ovarian cancer metastases: biology and pathology Gynecol. Oncol. 113 2009 143 148
34. Z. Gao, A.N. Lukyanov, A.R. Chakilam, and V.P. Torchilin PEG-PE/phosphatidylcholine mixed immunomicelles specifically deliver encapsulated taxol to tumor cells of different origin and promote their efficient killing J. Drug Target. 11 2003 87 92
35. A. Roby, S. Erdogan, and V.P. Torchilin Enhanced in vivo antitumor efficacy of poorly soluble PDT agent, meso-tetraphenylporphine, in PEG-PE-based tumor-targeted immunomicelles Cancer Biol. Ther. 6 2007 1136 1142
36. R.R. Sawant, R.M. Sawant, and V.P. Torchilin Mixed PEG-PE/vitamin E tumor-targeted immunomicelles as carriers for poorly soluble anti-cancer drugs: improved drug solubilization and enhanced in vitro cytotoxicity Eur. J. Pharm. Biopharm. 70 2008 51 57
37. T.A. ElBayoumi, and V.P. Torchilin Tumor-targeted nanomedicines: enhanced antitumor efficacy in vivo of doxorubicin-loaded, long-circulating liposomes modified with cancer-specific monoclonal antibody Clin. Cancer Res. 15 2009 1973 1980
38. B. Gupta, T.S. Levchenko, D.A. Mongayt, and V.P. Torchilin Monoclonal antibody 2C5-mediated binding of liposomes to brain tumor cells in vitro and in subcutaneous tumor model in vivo J. Drug Target. 13 2005 337 343
39. L. Iakoubov, O. Rokhlin, and V. Torchilin Anti-nuclear autoantibodies of the aged reactive against the surface of tumor but not normal cells Immunol. Lett. 47 1995 147 149
40. T.A. Elbayoumi, and V.P. Torchilin Enhanced accumulation of long-circulating liposomes modified with the nucleosome-specific monoclonal antibody 2C5 in various tumours in mice: gamma-imaging studies Eur. J. Nucl. Med. Mol. Imaging 33 2006 1196 1205
41. J. Lankelma, H. Dekker, F.R. Luque, S. Luykx, K. Hoekman, P. van der Valk, P.J. van Diest, and H.M. Pinedo Doxorubicin gradients in human breast cancer Clin. Cancer Res. 5 1999 1703 1707
42. H. Cabral, Y. Matsumoto, K. Mizuno, Q. Chen, M. Murakami, M. Kimura, Y. Terada, M.R. Kano, K. Miyazono, M. Uesaka, N. Nishiyama, and K. Kataoka Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size Nat. Nanotechnol. 6 2011 815 823
43. A.L. Klibanov, K. Maruyama, V.P. Torchilin, and L. Huang Amphipathic polyethyleneglycols effectively prolong the circulation time of liposomes FEBS Lett. 268 1990 235 237
44. V.P. Torchilin, A.N. Lukyanov, Z. Gao, and B. Papahadjopoulos-Sternberg Immunomicelles: targeted pharmaceutical carriers for poorly soluble drugs Proc. Natl. Acad. Sci. U. S. A. 100 2003 6039 6044
45. A.N. Lukyanov, Z. Gao, L. Mazzola, and V.P. Torchilin Polyethylene glycol-diacyllipid micelles demonstrate increased accumulation in subcutaneous tumors in mice Pharm. Res. 19 2002 1424 1429
46. X. Shuai, H. Ai, N. Nasongkla, S. Kim, and J. Gao Micellar carriers based on block copolymers of poly(epsilon-caprolactone) and poly(ethylene glycol) for doxorubicin delivery J. Control. Release 98 2004 415 426
47. N. Tang, G. Du, N. Wang, C. Liu, H. Hang, and W. Liang Improving penetration in tumors with nanoassemblies of phospholipids and doxorubicin J. Natl. Cancer Inst. 99 2007 1004 1015
48. V.P. Torchilin, T.S. Levchenko, A.N. Lukyanov, B.A. Khaw, A.L. Klibanov, R. Rammohan, G.P. Samokhin, and K.R. Whiteman p-Nitrophenylcarbonyl-PEG-PE- liposomes: fast and simple attachment of specific ligands, including monoclonal antibodies, to distal ends of PEG chains via p-nitrophenylcarbonyl groups Biochim. Biophys. Acta 1511 2001 397 411
49. H.R. Mellor, and R. Callaghan Accumulation and distribution of doxorubicin in tumour spheroids: the influence of acidity and expression of P-glycoprotein Cancer Chemother. Pharmacol. 68 2011 1179 1190
50. A.L. Howes, G.G. Chiang, E.S. Lang, C.B. Ho, G. Powis, K. Vuori, and R.T. Abraham The phosphatidylinositol 3-kinase inhibitor, PX-866, is a potent inhibitor of cancer cell motility and growth in three-dimensional cultures Mol. Cancer Ther. 6 2007 2505 2514
51. T. Musacchio, V. Laquintana, A. Latrofa, G. Trapani, and V.P. Torchilin PEG-PE micelles loaded with paclitaxel and surface-modified by a PBR-ligand: synergistic anticancer effect Mol. Pharm. 6 2009 468 479
52. T.H. Kim, C.W. Mount, W.R. Gombotz, and S.H. Pun The delivery of doxorubicin to 3-D multicellular spheroids and tumors in a murine xenograft model using tumor-penetrating triblock polymeric micelles Biomaterials 31 2010 7386 7397
53. E. Koren, A. Apte, A. Jani, and V.P. Torchilin Multifunctional PEGylated 2C5-immunoliposomes containing pH-sensitive bonds and TAT peptide for enhanced tumor cell internalization and cytotoxicity J. Control. Release 160 2012 264 273
54. Y. Tsukioka, Y. Matsumura, T. Hamaguchi, H. Koike, F. Moriyasu, and T. Kakizoe Pharmaceutical and biomedical differences between micellar doxorubicin (NK911) and liposomal doxorubicin (Doxil) Jpn. J. Cancer Res. 93 2002 1145 1153
55. M. Wartenberg, C. Frey, H. Diedershagen, J. Ritgen, J. Hescheler, and H. Sauer Development of an intrinsic P-glycoprotein-mediated doxorubicin resistance in quiescent cell layers of large, multicellular prostate tumor spheroids Int. J. Cancer 75 1998 855 863
56. J.H. Zheng, C.T. Chen, J.L. Au, and M.G. Wientjes Time- and concentration-dependent penetration of doxorubicin in prostate tumors AAPS PharmSci 3 2001 E15
57. G. Haslam, D. Wyatt, and P.A. Kitos Estimating the number of viable animal cells in multi-well cultures based on their lactate dehydrogenase activities Cytotechnology 32 2000 63 75
58. H. Gao, J. Qian, Z. Yang, Z. Pang, Z. Xi, S. Cao, Y. Wang, S. Pan, S. Zhang, W. Wang, X. Jiang, and Q. Zhang Whole-cell SELEX aptamer-functionalised poly(ethyleneglycol)-poly(epsilon-caprolactone) nanoparticles for enhanced targeted glioblastoma therapy Biomaterials 33 2012 6264 6272
59. C. Mamot, R. Ritschard, A. Wicki, W. Kung, J. Schuller, R. Herrmann, and C. Rochlitz Immunoliposomal delivery of doxorubicin can overcome multidrug resistance mechanisms in EGFR-overexpressing tumor cells J. Drug Target. 20 2012 422 432
60. T. Wang, V.A. Petrenko, and V.P. Torchilin Paclitaxel-loaded polymeric micelles modified with MCF-7 cell-specific phage protein: enhanced binding to target cancer cells and increased cytotoxicity Mol. Pharm. 7 2010 1007 1014
61. H.S. Yoo, and T.G. Park Folate receptor targeted biodegradable polymeric doxorubicin micelles J. Control. Release 96 2004 273 283
62. P.K. Jayanna, D. Bedi, J.W. Gillespie, P. DeInnocentes, T. Wang, V.P. Torchilin, R.C. Bird, and V.A. Petrenko Landscape phage fusion protein-mediated targeting of nanomedicines enhances their prostate tumor cell association and cytotoxic efficiency Nanomedicine 6 2010 538 546
63. X.B. Xiong, and A. Lavasanifar Traceable multifunctional micellar nanocarriers for cancer-targeted co-delivery of MDR-1 siRNA and doxorubicin ACS Nano 5 2011 5202 5213
64. Y.L. Tseng, J.J. Liu, and R.L. Hong Translocation of liposomes into cancer cells by cell-penetrating peptides penetratin and tat: a kinetic and efficacy study Mol. Pharmacol. 62 2002 864 872
65. A.M. Chen, M. Zhang, D. Wei, D. Stueber, O. Taratula, T. Minko, and H. He Co-delivery of doxorubicin and Bcl-2 siRNA by mesoporous silica nanoparticles enhances the efficacy of chemotherapy in multidrug-resistant cancer cells Small 5 2009 2673 2677
66. R.K. Srivastava, C.Y. Sasaki, J.M. Hardwick, and D.L. Longo Bcl-2-mediated drug resistance: inhibition of apoptosis by blocking nuclear factor of activated T lymphocytes (NFAT)-induced Fas ligand transcription J. Exp. Med. 190 1999 253 265
67. D. Del Bufalo, A. Biroccio, C. Leonetti, and G. Zupi Bcl-2 overexpression enhances the metastatic potential of a human breast cancer line FASEB J. 11 1997 947 953
68. J.M. Davis, P.M. Navolanic, C.R. Weinstein-Oppenheimer, L.S. Steelman, W. Hu, M. Konopleva, M.V. Blagosklonny, and J.A. McCubrey Raf-1 and Bcl-2 induce distinct and common pathways that contribute to breast cancer drug resistance Clin. Cancer Res. 9 2003 1161 1170
69. T.A. Elbayoumi, and V.P. Torchilin Tumor-specific antibody-mediated targeted delivery of Doxil reduces the manifestation of auricular erythema side effect in mice Int. J. Pharm. 357 2008 272 279
70. P. Parhi, C. Mohanty, and S.K. Sahoo Nanotechnology-based combinational drug delivery: an emerging approach for cancer therapy Drug Discov. Today 2012
71. R.C. Casey, K.M. Burleson, K.M. Skubitz, S.E. Pambuccian, T.R. Oegema Jr., L.E. Ruff, and A.P. Skubitz Beta 1-integrins regulate the formation and adhesion of ovarian carcinoma multicellular spheroids Am. J. Pathol. 159 2001 2071 2080
72. M. Kumagai, S. Shimoda, R. Wakabayashi, Y. Kunisawa, T. Ishii, K. Osada, K. Itaka, N. Nishiyama, K. Kataoka, and K. Nakano Effective transgene expression without toxicity by intraperitoneal administration of PEG-detachable polyplex micelles in mice with peritoneal dissemination J. Control. Release 160 2012 542 551