The challenges facing block copolymer micelles for cancer therapy: In vivo barriers and clinical translation

Advanced Drug Delivery Reviews

Volumn 91, Issue , 2015, Pages 7-22

  Eetezadi, Sina ^a   Ekdawi, Sandra N ^a   Allen, Christine ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Cancer heterogeneity; EPR; Experimental models; Nano drug delivery systems; Nanoformulation; Nanomedicines; Tumor drug bioavailability; Tumor penetration

Indexed keywords

BIOCHEMISTRY; BLOCK COPOLYMERS; CONTROLLED DRUG DELIVERY; DISEASES; MEDICAL NANOTECHNOLOGY; ONCOLOGY; PARAMAGNETIC RESONANCE; TARGETED DRUG DELIVERY; TUMORS;

CANCER HETEROGENEITIES; DRUG DELIVERY SYSTEM; EXPERIMENTAL MODELS; NANOFORMULATION; TUMOR PENETRATION;

MICELLES;

CARCINOEMBRYONIC ANTIBODY; CARCINOEMBRYONIC ANTIBODY A5B7; CISPLATIN; COPOLYMER; DOXORUBICIN; LIPOSOME; MACROGOL; MONOCLONAL ANTIBODY DC101; NK 911; PACLITAXEL; PLATINUM 1,2 DIAMINOCYCLOHEXANE; POLYCAPROLACTONE; POLYLACTIDE; SP 1049C; TRANSFORMING GROWTH FACTOR BETA INHIBITOR; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; MICELLE; POLYMER;

ADVANCED CANCER; ANTINEOPLASTIC ACTIVITY; AREA UNDER THE CURVE; BLOCK COPOLYMER MICELLE; BLOOD COMPONENT; BREAST CANCER; CANCER IMMUNOTHERAPY; CANCER THERAPY; CAPILLARY DENSITY; CLINICAL RESEARCH; COLORECTAL CANCER; COMPARATIVE STUDY; DRUG BIOAVAILABILITY; DRUG CLEARANCE; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG EXPOSURE; DRUG FORMULATION; DRUG HALF LIFE; DRUG RETENTION; DRUG STABILITY; DRUG UPTAKE; ENHANCED PERMEABILITY RETENTION; FLUORESCENCE MICROSCOPY; GLIOBLASTOMA; GLIOMA; HEAD AND NECK CANCER; HUMAN; HYDROPHILICITY; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; INTRAVITAL LASER SCANNING CONFOCAL FLUORESCENCE MICROSCOPY; MICELLE; NONHUMAN; PANCREAS CANCER; PARTICLE SIZE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PHYSICAL CHEMISTRY; PLASMA CLEARANCE; PRIORITY JOURNAL; REVIEW; TUMOR MICROENVIRONMENT; UTERINE CERVIX CANCER; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; DRUG DESIGN; NEOPLASMS; PATHOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; DRUG DELIVERY SYSTEMS; DRUG DESIGN; DRUG STABILITY; HUMANS; MICELLES; MODELS, BIOLOGICAL; NEOPLASMS; POLYMERS;

EID: 84940945089     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2014.10.001     Document Type: Review

References (167)

1. Birrenbach G., Speiser P.P. Polymerized micelles and their use as adjuvants in immunology. J. Pharm. Sci. 1976, 65:1763-1766.
2. Kreuter J. Nanoparticles - a historical perspective. Int. J. Pharm. 2007, 331:1-10.
3. Bader H., Ringsdorf H., Schmidt B. Watersoluble polymers in medicine. Angew. Makromol. Chem. 1984, 123:457-485.
4. Alakhov V., Klinski E., Li S.M., Pietrzynski G., Venne A., Batrakova E., Bronitch T., Kabanov A. Block copolymer-based formulation of doxorubicin. From cell screen to clinical trials. Colloids Surf. B 1999, 16:113-134.
5. Matsumura Y. The drug discovery by nanomedicine and its clinical experience. Jpn. J. Clin. Oncol. 2014, 44:515-525.
6. Cabral H., Kataoka K. Progress of drug-loaded polymeric micelles into clinical studies. J. Control. Release 2014, 190:465-476.
7. Mikhail A.S., Allen C. Block copolymer micelles for delivery of cancer therapy: transport at the whole body, tissue and cellular levels. J. Control. Release 2009, 138:214-223.
8. Owen S.C., Chan D.P.Y., Shoichet M.S. Polymeric micelle stability. Nano Today 2012, 7:53-65.
9. Cabral H., Matsumoto Y., Mizuno K., Chen Q., Murakami M., Kimura M., Terada Y., Kano M.R., Miyazono K., Uesaka M., Nishiyama N., Kataoka K. Accumulation of sub-100nm polymeric micelles in poorly permeable tumours depends on size. Nat. Nanotechnol. 2011, 6:815-823.
10. Murakami M., Cabral H., Matsumoto Y., Wu S.R., Kano M.R., Yamori T., Nishiyama N., Kataoka K. Improving drug potency and efficacy by nanocarrier-mediated subcellular targeting. Sci. Transl. Med. 2011, 3.
11. Torchilin V.P. Micellar nanocarriers: pharmaceutical perspectives. Pharm. Res. 2007, 24:1-16.
12. Zhang L., Gu F.X., Chan J.M., Wang A.Z., Langer R.S., Farokhzad O.C. Nanoparticles in medicine: therapeutic applications and developments. Clin. Pharmacol. Ther. 2008, 83:761-769.
13. Kwon G.S., Kataoka K. Block-copolymer micelles as long-circulating drug vehicles. Adv. Drug Deliv. Rev. 1995, 16:295-309.
14. Allen C., Maysinger D., Eisenberg A. Nano-engineering block copolymer aggregates for drug delivery. Colloids Surf. B 1999, 16:3-27.
15. Nicolas J., Mura S., Brambilla D., Mackiewicz N., Couvreur P. Design, functionalization strategies and biomedical applications of targeted biodegradable/biocompatible polymer-based nanocarriers for drug delivery. Chem. Soc. Rev. 2013, 42:1147-1235.
16. Jones M.C., Leroux J.C. Polymeric micelles - a new generation of colloidal drug carriers. Eur. J. Pharm. Biopharm. 1999, 48:101-111.
17. Rapoport N. Physical stimuli-responsive polymeric micelles for anti-cancer drug delivery. Prog. Polym. Sci. 2007, 32:962-990.
18. Mikhail A.S., Allen C. Poly(ethylene glycol)-b-poly(epsilon-caprolactone) micelles containing chemically conjugated and physically entrapped docetaxel: synthesis, characterization, and the influence of the drug on micelle morphology. Biomacromolecules 2010, 11:1273-1280.
19. Mochida Y., Cabral H., Miura Y., Albertini F., Fukushima S., Osada K., Nishiyama N., Kataoka K. Bundled assembly of helical nanostructures in polymeric micelles loaded with platinum drugs enhancing therapeutic efficiency against pancreatic tumor. ACS Nano 2014, 8:6724-6738.
20. Baba M., Matsumoto Y., Kashio A., Cabral H., Nishiyama N., Kataoka K., Yamasoba T. Micellization of cisplatin (NC-6004) reduces its ototoxicity in guinea pigs. J. Control. Release 2012, 157:112-117.
21. Lammers T. SMART drug delivery systems: back to the future vs. clinical reality. Int. J. Pharm. 2013, 454:527-529.
22. Park K. Facing the truth about nanotechnology in drug delivery. ACS Nano 2013, 7:7442-7447.
23. Ruenraroengsak P., Cook J.M., Florence A.T. Nanosystem drug targeting: facing up to complex realities. J. Control. Release 2010, 141:265-276.
24. Crommelin D.J., Florence A.T. Towards more effective advanced drug delivery systems. Int. J. Pharm. 2013, 454:496-511.
25. Bae Y.H., Mrsny R.J., Park K. Cancer Targeted Drug Delivery An Elusive Dream 2013, Springer, New York, [S.l.].
26. Lammers T., Kiessling F., Hennink W.E., Storm G. Drug targeting to tumors: principles, pitfalls and (pre-) clinical progress. J. Control. Release 2012, 161:175-187.
27. Jain R.K., Stylianopoulos T. Delivering nanomedicine to solid tumors. Nat. Rev. Clin. Oncol. 2010, 7:653-664.
28. Seymour L.W., Miyamoto Y., Maeda H., Brereton M., Strohalm J., Ulbrich K., Duncan R. Influence of molecular weight on passive tumour accumulation of a soluble macromolecular drug carrier. Eur. J. Cancer 1995, 31A:766-770.
29. Li S.D., Huang L. Pharmacokinetics and biodistribution of nanoparticles. Mol. Pharm. 2008, 5:496-504.
30. Choi H.S., Liu W., Misra P., Tanaka E., Zimmer J.P., Itty Ipe B., Bawendi M.G., Frangioni J.V. Renal clearance of quantum dots. Nat. Biotechnol. 2007, 25:1165-1170.
31. Matsumura Y., Maeda H. A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res. 1986, 46:6387-6392.
32. Fang J., Nakamura H., Maeda H. The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv. Drug Deliv. Rev. 2011, 63:136-151.
33. Alexis F., Pridgen E., Molnar L.K., Farokhzad O.C. Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol. Pharm. 2008, 5:505-515.
34. Moghimi S.M., Hedeman H., Muir I.S., Illum L., Davis S.S. An investigation of the filtration capacity and the fate of large filtered sterically-stabilized microspheres in rat spleen. Biochim. Biophys. Acta 1993, 1157:233-240.
35. Moghimi S.M., Hunter A.C., Murray J.C. Long-circulating and target-specific nanoparticles: theory to practice. Pharmacol. Rev. 2001, 53:283-318.
36. Owens D.E., Peppas N.A. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int. J. Pharm. 2006, 307:93-102.
37. Moghimi S.M., Hunter A.C., Andresen T.L. Factors controlling nanoparticle pharmacokinetics: an integrated analysis and perspective. Annu. Rev. Pharmacol. Toxicol. 2012, 52:481-503.
38. Chrastina A., Massey K.A., Schnitzer J.E. Overcoming in vivo barriers to targeted nanodelivery. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2011, 3:421-437.
39. Kwon G.S., Yokoyama M., Okano T., Sakurai Y., Kataoka K. Biodistribution of micelle-forming polymer-drug conjugates. Pharm. Res. 1993, 10:970-974.
40. Verhoef J.J.F. Questioning the use of PEGylation for drug delivery. Drug Deliv. Transl. Res. 2013, 3.
41. Shiraishi K., Yokoyama M. Polymeric micelles possessing polyethyleneglycol as outer shell and their unique behaviors in accelerated blood clearance phenomenon. Biol. Pharm. Bull. 2013, 36:878-882.
42. Barz M., Luxenhofer R., Zentel R., Vicent M.J. Overcoming the PEG-addiction: well-defined alternatives to PEG, from structure-property relationships to better defined therapeutics. Polym. Chem. U. K. 2011, 2:1900-1918.
43. Knop K., Hoogenboom R., Fischer D., Schubert U.S. Poly(ethylene glycol) in drug delivery: pros and cons as well as potential alternatives. Angew. Chem. Int. Ed. 2010, 49:6288-6308.
44. Hunter A.C., Moghimi S.M. Therapeutic synthetic polymers: a game of Russian roulette?. Drug Discov. Today 2002, 7:998-1001.
45. Yamamoto Y., Nagasaki Y., Kato Y., Sugiyama Y., Kataoka K. Long-circulating poly(ethylene glycol)-poly(D,L-lactide) block copolymer micelles with modulated surface charge. J. Control. Release 2001, 77:27-38.
46. Lee H., Fonge H., Hoang B., Reilly R.M., Allen C. The effects of particle size and molecular targeting on the intratumoral and subcellular distribution of polymeric nanoparticles. Mol. Pharm. 2010, 7:1195-1208.
47. Fonge H., Huang H., Scollard D., Reilly R.M., Allen C. Influence of formulation variables on the biodistribution of multifunctional block copolymer micelles. J. Control. Release 2012, 157:366-374.
48. Hoang B., Ekdawi S.N., Reilly R.M., Allen C. Active targeting of block copolymer micelles with trastuzumab Fab fragments and nuclear localization signal leads to increased tumor uptake and nuclear localization in HER2-overexpressing xenografts. Mol. Pharm. 2013, 10:4229-4241.
49. Mikhail A.S., Eetezadi S., Ekdawi S.N., Stewart J., Allen C. Image-based analysis of the size- and time-dependent penetration of polymeric micelles in multicellular tumor spheroids and tumor xenografts. Int. J. Pharm. 2014, 464:168-177.
50. Lee H., Hoang B., Fonge H., Reilly R.M., Allen C. In vivo distribution of polymeric nanoparticles at the whole-body. Tumor Cell. Levels Pharm. Res. 2010, 27:2343-2355.
51. Geng Y., Dalhaimer P., Cai S., Tsai R., Tewari M., Minko T., Discher D.E. Shape effects of filaments versus spherical particles in flow and drug delivery. Nat. Nanotechnol. 2007, 2:249-255.
52. Christian D.A., Cai S., Garbuzenko O.B., Harada T., Zajac A.L., Minko T., Discher D.E. Flexible filaments for in vivo imaging and delivery: persistent circulation of filomicelles opens the dosage window for sustained tumor shrinkage. Mol. Pharm. 2009, 6:1343-1352.
53. Karmali P.P., Simberg D. Interactions of nanoparticles with plasma proteins: implication on clearance and toxicity of drug delivery systems. Expert Opin. Drug Deliv. 2011, 8:343-357.
54. Valle J.W., Armstrong A., Newman C., Alakhov V., Pietrzynski G., Brewer J., Campbell S., Corrie P., Rowinsky E.K., Ranson M. A phase 2 study of SP1049C, doxorubicin in P-glycoprotein-targeting pluronics, in patients with advanced adenocarcinoma of the esophagus and gastroesophageal junction. Invest. New Drugs 2011, 29:1029-1037.
55. Matsumura Y., Hamaguchi T., Ura T., Muro K., Yamada Y., Shimada Y., Shirao K., Okusaka T., Ueno H., Ikeda M., Watanabe N. Phase I clinical trial and pharmacokinetic evaluation of NK911, a micelle-encapsulated doxorubicin. Br. J. Cancer 2004, 91:1775-1781.
56. Nakanishi T., Fukushima S., Okamoto K., Suzuki M., Matsumura Y., Yokoyama M., Okano T., Sakurai Y., Kataoka K. Development of the polymer micelle carrier system for doxorubicin. J. Control. Release 2001, 74:295-302.
57. Sutton D., Nasongkla N., Blanco E., Gao J.M. Functionalized micellar systems for cancer targeted drug delivery. Pharm. Res. 2007, 24:1029-1046.
58. Burt H.M., Zhang X.C., Toleikis P., Embree L., Hunter W.L. Development of copolymers of poly(D, L-lactide) and methoxypolyethylene glycol as micellar carriers of paclitaxel. Colloids Surf. B 1999, 16:161-171.
59. Hamaguchi T., Matsumura Y., Suzuki M., Shimizu K., Goda R., Nakamura I., Nakatomi I., Yokoyama M., Kataoka K., Kakizoe T. NK105, a paclitaxel-incorporating micellar nanoparticle formulation, can extend in vivo antitumour activity and reduce the neurotoxicity of paclitaxel. Br. J. Cancer 2005, 92:1240-1246.
60. Desale S.S., Cohen S.M., Zhao Y., Kabanov A.V., Bronich T.K. Biodegradable hybrid polymer micelles for combination drug therapy in ovarian cancer. J. Control. Release 2013, 171:339-348.
61. Carmeliet P., Jain R.K. Angiogenesis in cancer and other diseases. Nature 2000, 407:249-257.
62. Folkman J., Watson K., Ingber D., Hanahan D. Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature 1989, 339:58-61.
63. De Bock K., Cauwenberghs S., Carmeliet P. Vessel abnormalization: another hallmark of cancer? Molecular mechanisms and therapeutic implications. Curr. Opin. Genet. Dev. 2011, 21:73-79.
64. Kamoun W.S., Chae S.S., Lacorre D.A., Tyrrell J.A., Mitre M., Gillissen M.A., Fukumura D., Jain R.K., Munn L.L. Simultaneous measurement of RBC velocity, flux, hematocrit and shear rate in vascular networks. Nat. Methods 2010, 7:655-660.
65. Fukumura D., Duda D.G., Munn L.L., Jain R.K. Tumor microvasculature and microenvironment: novel insights through intravital imaging in pre-clinical models. Microcirculation 2010, 17:206-225.
66. Jain R.K. Molecular regulation of vessel maturation. Nat. Med. 2003, 9:685-693.
67. Baluk P., Hashizume H., McDonald D.M. Cellular abnormalities of blood vessels as targets in cancer. Curr. Opin. Genet. Dev. 2005, 15:102-111.
68. Morikawa S., Baluk P., Kaidoh T., Haskell A., Jain R.K., McDonald D.M. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am. J. Pathol. 2002, 160:985-1000.
69. Hobbs S.K., Monsky W.L., Yuan F., Roberts W.G., Griffith L., Torchilin V.P., Jain R.K. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:4607-4612.
70. Konerding M.A., Malkusch W., Klapthor B., van Ackern C., Fait E., Hill S.A., Parkins C., Chaplin D.J., Presta M., Denekamp J. Evidence for characteristic vascular patterns in solid tumours: quantitative studies using corrosion casts. Br. J. Cancer 1999, 80:724-732.
71. Vakoc B.J., Lanning R.M., Tyrrell J.A., Padera T.P., Bartlett L.A., Stylianopoulos T., Munn L.L., Tearney G.J., Fukumura D., Jain R.K., Bouma B.E. Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging. Nat. Med. 2009, 15:1219-U1151.
72. Narang A.S., Varia S. Role of tumor vascular architecture in drug delivery. Adv. Drug Deliv. Rev. 2011, 63:640-658.
73. Minchinton A.I., Tannock I.F. Drug penetration in solid tumours. Nat. Rev. Cancer 2006, 6:583-592.
74. Dreher M.R., Liu W., Michelich C.R., Dewhirst M.W., Yuan F., Chilkoti A. Tumor vascular permeability, accumulation, and penetration of macromolecular drug carriers. J. Natl. Cancer Inst. 2006, 98:335-344.
75. Taurin S., Nehoff H., Greish K. Anticancer nanomedicine and tumor vascular permeability; where is the missing link?. J. Control. Release 2012, 164:265-275.
76. Kwon G., Suwa S., Yokoyama M., Okano T., Sakurai Y., Kataoka K. Enhanced tumor accumulation and prolonged circulation times of micelle-forming poly(ethylene oxide-aspartate) block copolymer-adriamycin conjugates. J. Control. Release 1994, 29:17-23.
77. Charrois G.J.R., Allen T.M. Rate of biodistribution of STEALTH((R)) liposomes to tumor and skin: influence of liposome diameter and implications for toxicity and therapeutic activity. BBA Biomembranes 2003, 1609:102-108.
78. Nichols J.W., Bae Y.H. EPR: evidence and fallacy. J. Control. Release 2014, 190:451-464.
79. Bertrand N., Wu J., Xu X., Kamaly N., Farokhzad O.C. Cancer nanotechnology: the impact of passive and active targeting in the era of modern cancer biology. Adv. Drug Deliv. Rev. 2013, 66:2-25.
80. Pirollo K.F., Chang E.H. Does a targeting ligand influence nanoparticle tumor localization or uptake?. Trends Biotechnol. 2008, 26:552-558.
81. Gray B.P., McGuire M.J., Brown K.C. A liposomal drug platform overrides peptide ligand targeting to a cancer biomarker, irrespective of ligand affinity or density. PLoS One 2013, 8:e72938.
82. Cheng Z., Al Zaki A., Hui J.Z., Muzykantov V.R., Tsourkas A. Multifunctional nanoparticles: cost versus benefit of adding targeting and imaging capabilities. Science 2012, 338:903-910.
83. Kirpotin D.B., Drummond D.C., Shao Y., Shalaby M.R., Hong K., Nielsen U.B., Marks J.D., Benz C.C., Park J.W. 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.
84. Lammers T., Hennink W.E., Storm G. Tumour-targeted nanomedicines: principles and practice. Br. J. Cancer 2008, 99:392-397.
85. Slamon D.J., Godolphin W., Jones L.A., Holt J.A., Wong S.G., Keith D.E., Levin W.J., Stuart S.G., Udove J., Ullrich A., et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989, 244:707-712.
86. Wang M., Thanou M. Targeting nanoparticles to cancer. Pharmacol. Res. 2010, 62:90-99.
87. Dunne M., Zheng J., Rosenblat J., Jaffray D.A., Allen C. APN/CD13-targeting as a strategy to alter the tumor accumulation of liposomes. J. Control. Release 2011, 154:298-305.
88. El Emir E., Qureshi U., Dearling J.L., Boxer G.M., Clatworthy I., Folarin A.A., Robson M.P., Nagl S., Konerding M.A., Pedley R.B. Predicting response to radioimmunotherapy from the tumor microenvironment of colorectal carcinomas. Cancer Res. 2007, 67:11896-11905.
89. Blumenthal R.D., Sharkey R.M., Kashi R., Natale A.M., Goldenberg D.M. Physiological factors influencing radioantibody uptake: a study of four human colonic carcinomas. Int. J. Cancer 1992, 51:935-941.
90. Simnick A.J., Amiram M., Liu W., Hanna G., Dewhirst M.W., Kontos C.D., Chilkoti A. In vivo tumor targeting by a NGR-decorated micelle of a recombinant diblock copolypeptide. J. Control. Release 2011, 155:144-151.
91. Miura Y., Takenaka T., Toh K., Wu S., Nishihara H., Kano M.R., Ino Y., Nomoto T., Matsumoto Y., Koyama H., Cabral H., Nishiyama N., Kataoka K. Cyclic RGD-linked polymeric micelles for targeted delivery of platinum anticancer drugs to glioblastoma through the blood-brain tumor barrier. ACS Nano 2013, 7:8583-8592.
92. Carmeliet P., Jain R.K. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases. Nat. Rev. Drug Discov. 2011, 10:417-427.
93. Fukumura D., Yuan F., Monsky W.L., Chen Y., Jain R.K. Effect of host microenvironment on the microcirculation of human colon adenocarcinoma. Am. J. Pathol. 1997, 151:679-688.
94. Jain R.K. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005, 307:58-62.
95. Orcutt K.D., Rhoden J.J., Ruiz-Yi B., Frangioni J.V., Wittrup K.D. Effect of small-molecule-binding affinity on tumor uptake in vivo: a systematic study using a pretargeted bispecific antibody. Mol. Cancer Ther. 2012, 11:1365-1372.
96. Valencia C.A., Rhodenizer D., Bhide S., Chin E., Littlejohn M.R., Keong L.M., Rutkowski A., Bonnemann C., Hegde M. Assessment of target enrichment platforms using massively parallel sequencing for the mutation detection for congenital muscular dystrophy. J. Mol. Diagn. 2012, 14:233-246.
97. Munn L.L. Aberrant vascular architecture in tumors and its importance in drug-based therapies. Drug Discov. Today 2003, 8:396-403.
98. Harrington K.J., Mohammadtaghi S., Uster P.S., Glass D., Peters A.M., Vile R.G., Stewart J.S. Effective targeting of solid tumors in patients with locally advanced cancers by radiolabeled pegylated liposomes. Clin. Cancer Res. 2001, 7:243-254.
99. Koukourakis M.I., Koukouraki S., Giatromanolaki A., Archimandritis S.C., Skarlatos J., Beroukas K., Bizakis J.G., Retalis G., Karkavitsas N., Helidonis E.S. Liposomal doxorubicin and conventionally fractionated radiotherapy in the treatment of locally advanced non-small-cell lung cancer and head and neck cancer. J. Clin. Oncol. 1999, 17:3512-3521.
100. Chauhan V.P., Stylianopoulos T., Martin J.D., Popovic Z., Chen O., Kamoun W.S., Bawendi M.G., Fukumura D., Jain R.K. Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner. Nat. Nanotechnol. 2012, 7:383-388.
101. Seynhaeve A.L., Hoving S., Schipper D., Vermeulen C.E., de Wiel-Ambagtsheer G., van Tiel S.T., Eggermont A.M., Ten Hagen T.L. Tumor necrosis factor alpha mediates homogeneous distribution of liposomes in murine melanoma that contributes to a better tumor response. Cancer Res. 2007, 67:9455-9462.
102. Lammers T., Peschke P., Kuhnlein R., Subr V., Ulbrich K., Debus J., Huber P., Hennink W., Storm G. Effect of radiotherapy and hyperthermia on the tumor accumulation of HPMA copolymer-based drug delivery systems. J. Control. Release 2007, 117:333-341.
103. Reinhold H., Endrich B. Tumour microcirculation as a target for hyperthermia. Int. J. Hyperth. 1986, 2:111-137.
104. Jain R.K., Ward-Hartley K. Tumor blood flow-characterization, modifications, and role in hyperthermia. IEEE Trans. Ultrason. 1984, 31:504-526.
105. Song C., Park H., Lee C., Griffin R. Implications of increased tumor blood flow and oxygenation caused by mild temperature hyperthermia in tumor treatment. Int. J. Hyperth. 2005, 21:761-767.
106. Park J.S., Qiao L., Su Z.Z., Hinman D., Willoughby K., McKinstry R., Yacoub A., Duigou G.J., Young C.S., Grant S., Hagan M.P., Ellis E., Fisher P.B., Dent P. Ionizing radiation modulates vascular endothelial growth factor (VEGF) expression through multiple mitogen activated protein kinase dependent pathways. Oncogene 2001, 20:3266-3280.
107. Chung Y.L., Jian J.J., Cheng S.H., Tsai S.Y., Chuang V.P., Soong T., Lin Y.M., Horng C.F. Sublethal irradiation induces vascular endothelial growth factor and promotes growth of hepatoma cells: implications for radiotherapy of hepatocellular carcinoma. Clin. Cancer Res. 2006, 12:2706-2715.
108. Lee Y.J., Galoforo S.S., Berns C.M., Erdos G., Gupta A.K., Ways D.K., Corry P.M. Effect of ionizing radiation on AP-1 binding activity and basic fibroblast growth factor gene expression in drug-sensitive human breast carcinoma MCF-7 and multidrug-resistant MCF-7/ADR cells. J. Biol. Chem. 1995, 270:28790-28796.
109. Ianiski F.R., Alves C.B., Souza A.C., Pinton S., Roman S.S., Rhoden C.R., Alves M.P., Luchese C. Protective effect of meloxicam-loaded nanocapsules against amyloid-beta peptide-induced damage in mice. Behav. Brain Res. 2012, 230:100-107.
110. Hatch N.W., Srodulski S.J., Chan H.W., Zhang X., Tannock L.R., King V.L. Endogenous androgen deficiency enhances diet-induced hypercholesterolemia and atherosclerosis in low-density lipoprotein receptor-deficient mice. Gend. Med. 2012, 9:319-328.
111. Tang T., Thompson J.C., Wilson P.G., Nelson C., Williams K.J., Tannock L.R. Decreased body fat, elevated plasma transforming growth factor-beta levels, and impaired BMP4-like signaling in biglycan-deficient mice. Connect. Tissue Res. 2013, 54:5-13.
112. Seruga B., Pond G.R., Hertz P.C., Amir E., Ocana A., Tannock I.F. Comparison of absolute benefits of anticancer therapies determined by snapshot and area methods. Ann. Oncol. 2012, 23:2977-2982.
113. Heldin C.H., Rubin K., Pietras K., Ostman A. High interstitial fluid pressure - an obstacle in cancer therapy. Nat. Rev. Cancer 2004, 4:806-813.
114. Lunt S.J., Fyles A., Hill R.P., Milosevic M. Interstitial fluid pressure in tumors: therapeutic barrier and biomarker of angiogenesis. Future Oncol. 2008, 4:793-802.
115. Chauhan V.P., Stylianopoulos T., Boucher Y., Jain R.K. Delivery of molecular and nanoscale medicine to tumors: transport barriers and strategies. Annu. Rev. Chem. Biomol. Eng. 2011, 2:281-298.
116. Fung A.S., Jonkman J., Tannock I.F. Quantitative immunohistochemistry for evaluating the distribution of Ki67 and other biomarkers in tumor sections and use of the method to study repopulation in xenografts after treatment with paclitaxel. Neoplasia 2012, 14:324-+.
117. Rhoden J.J., Wittrup K.D. Dose dependence of intratumoral perivascular distribution of monoclonal antibodies. J. Pharm. Sci. 2012, 101:860-867.
118. White S.C., Lorigan P., Margison G.P., Margison J.M., Martin F., Thatcher N., Anderson H., Ranson M. Phase II study of SPI-77 (sterically stabilised liposomal cisplatin) in advanced non-small-cell lung cancer. Br. J. Cancer 2006, 95:822-828.
119. Batrakova E.V., Kabanov A.V. Pluronic block copolymers: evolution of drug delivery concept from inert nanocarriers to biological response modifiers. J. Control. Release 2008, 130:98-106.
120. Alakhov V.Y., Moskaleva E.Y., Batrakova E.V., Kabanov A.V. Hypersensitization of multidrug resistant human ovarian carcinoma cells by pluronic P85 block copolymer. Bioconjug. Chem. 1996, 7:209-216.
121. Rapoport N., Marin A., Luo Y., Prestwich G.D., Muniruzzaman M. Intracellular uptake and trafficking of pluronic micelles in drug-sensitive and MDR cells: effect on the intracellular drug localization. J. Pharm. Sci. 2002, 91:157-170.
122. Yoo H.S., Park T.G. Biodegradable polymeric micelles composed of doxorubicin conjugated PLGA-PEG block copolymer. J. Control. Release 2001, 70:63-70.
123. Du W.J., Xu Z.Q., Nystrom A.M., Zhang K., Leonard J.R., Wooley K.L. F-19- and fluorescently labeled micelles as nanoscopic assemblies for chemotherapeutic delivery. Bioconjug. Chem. 2008, 19:2492-2498.
124. Talelli M., Rijcken C.J.F., Hennink W.E., Lammers T. Polymeric micelles for cancer therapy: 3 C's to enhance efficacy. Curr. Opin. Solid State Mater. Sci. 2012, 16:302-309.
125. Hoang B., Reilly R.M., Allen C. Block copolymer micelles target Auger electron radiotherapy to the nucleus of HER2-positive breast cancer cells. Biomacromolecules 2012, 13:455-465.
126. Barenholz Y. Doxil (R) - the first FDA-approved nano-drug: Lessons learned. J. Control. Release 2012, 160:117-134.
127. Grislain L., Couvreur P., Lenaerts V., Roland M., Deprezdecampeneere D., Speiser P. Pharmacokinetics and distribution of a biodegradable drug-carrier. Int. J. Pharm. 1983, 15:335-345.
128. Ekdawi S.N., Mikhail A.S., Stapelton S., Zheng J., Eetezadi S., Jaffray D.A., Allen C. Long circulation and tumor accumulation. Cancer Targeted Drug Delivery 2013, 543-571. Springer, New York. Y.H. Bae, J.M. Randall, K. Park (Eds.).
129. Prabhakar U., Maeda H., Jain R.K., Sevick-Muraca E.M., Zamboni W., Farokhzad O.C., Barry S.T., Gabizon A., Grodzinski P., Blakey D.C. Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology. Cancer Res. 2013, 73:2412-2417.
130. Nishiyama N., Okazaki S., Cabral H., Miyamoto M., Kato Y., Sugiyama Y., Nishio K., Matsumura Y., Kataoka K. Novel cisplatin-incorporated polymeric micelles can eradicate solid tumors in mice. Cancer Res. 2003, 63:8977-8983.
131. Uchino H., Matsumura Y., Negishi T., Koizumi F., Hayashi T., Honda T., Nishiyama N., Kataoka K., Naito S., Kakizoe T. Cisplatin-incorporating polymeric micelles (NC-6004) can reduce nephrotoxicity and neurotoxicity of cisplatin in rats. Br. J. Cancer 2005, 93:678-687.
132. Plummer R., Wilson R.H., Calvert H., Boddy A.V., Griffin M., Sludden J., Tilby M.J., Eatock M., Pearson D.G., Ottley C.J., Matsumura Y., Kataoka K., Nishiya T. A Phase I clinical study of cisplatin-incorporated polymeric micelles (NC-6004) in patients with solid tumours. Br. J. Cancer 2011, 104:593-598.
133. Emoto S., Yamaguchi H., Kishikawa J., Yamashita H., Ishigami H., Kitayama J. Antitumor effect and pharmacokinetics of intraperitoneal NK105, a nanomicellar paclitaxel formulation for peritoneal dissemination. Cancer Sci. 2012, 103:1304-1310.
134. Kato K., Chin K., Yoshikawa T., Yamaguchi K., Tsuji Y., Esaki T., Sakai K., Kimura M., Hamaguchi T., Shimada Y., Matsumura Y., Ikeda R. Phase II study of NK105, a paclitaxel-incorporating micellar nanoparticle, for previously treated advanced or recurrent gastric cancer. Invest. New Drugs 2012, 30:1621-1627.
135. Lankelma J., Dekker H., Luque R.F., Luykx S., Hoekman K., van der Valk P., van Diest P.J., Pinedo H.M. Doxorubicin gradients in human breast cancer. Clin. Cancer Res. 1999, 5:1703-1707.
136. Primeau A.J., Rendon A., Hedley D., Lilge L., Tannock I.F. The distribution of the anticancer drug doxorubicin in relation to blood vessels in solid tumors. Clin. Cancer Res. 2005, 11:8782-8788.
137. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
138. Martin A., Clynes M. Comparison of 5 microplate colorimetric assays for in vitro cytotoxicity testing and cell proliferation assays. Cytotechnology 1993, 11:49-58.
139. Shoemaker R.H. The NCI60 human tumour cell line anticancer drug screen. Nat. Rev. Cancer 2006, 6:813-823.
140. Lorenzi P.L., Reinhold W.C., Varma S., Hutchinson A.A., Pommier Y., Chanock S.J., Weinstein J.N. DNA fingerprinting of the NCI-60 cell line panel. Mol. Cancer Ther. 2009, 8:713-724.
141. Johnson J.I., Decker S., Zaharevitz D., Rubinstein L.V., Venditti J., Schepartz S., Kalyandrug S., Christian M., Arbuck S., Hollingshead M., Sausville E.A. Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. Br. J. Cancer 2001, 84:1424-1431.
142. Phillips R.M., Bibby M.C., Double J.A. A critical appraisal of the predictive value of in vitro chemosensitivity assays. J. Natl. Cancer Inst. 1990, 82:1457-1468.
143. Mikhail A.S., Eetezadi S., Allen C. Multicellular tumor spheroids for evaluation of cytotoxicity and tumor growth inhibitory effects of nanomedicines in vitro: a comparison of docetaxel-loaded block copolymer micelles and taxotere (R). PLoS One 2013, 8.
144. Olive P.L., Durand R.E. Drug and radiation resistance in spheroids: cell contact and kinetics. Cancer Metastasis Rev. 1994, 13:121-138.
145. Hirschhaeuser F., Menne H., Dittfeld C., West J., Mueller-Klieser W., Kunz-Schughart L.A. Multicellular tumor spheroids: an underestimated tool is catching up again. J. Biotechnol. 2010, 148:3-15.
146. Kim T.H., Mount C.W., Gombotz W.R., Pun S.H. The delivery of doxorubicin to 3-D multicellular spheroids and tumors in a murine xenograft model using tumor-penetrating triblock polymeric micelles. Biomaterials 2010, 31:7386-7397.
147. Tsukioka Y., Matsumura Y., Hamaguchi T., Koike H., Moriyasu F., Kakizoe T. Pharmaceutical and biomedical differences between micellar doxorubicin (NK911) and liposomal doxorubicin (Doxil). Jpn. J. Cancer Res. 2002, 93:1145-1153.
148. Ruggeri B.A., Camp F., Miknyoczki S. Animal models of disease: pre-clinical animal models of cancer and their applications and utility in drug discovery. Biochem. Pharmacol. 2014, 87:150-161.
149. Das Thakur M., Pryer N.K., Singh M. Mouse tumour models to guide drug development and identify resistance mechanisms. J. Pathol. 2014, 232:103-111.
150. Singh M., Ferrara N. Modeling and predicting clinical efficacy for drugs targeting the tumor milieu. Nat. Biotechnol. 2012, 30:648-657.
151. Vassileva V., Moriyama E.H., De Souza R., Grant J., Allen C.J., Wilson B.C., Piquette-Miller M. Efficacy assessment of sustained intraperitoneal paclitaxel therapy in a murine model of ovarian cancer using bioluminescent imaging. Br. J. Cancer 2008, 99:2037-2043.
152. Malaney P., Nicosia S.V., Dave V. One mouse, one patient paradigm: new avatars of personalized cancer therapy. Cancer Lett. 2014, 344:1-12.
153. Sharpless N.E., DePinho R.A. Model organisms - the mighty mouse: genetically engineered mouse models in cancer drug development. Nat. Rev. Drug Discov. 2006, 5:741-754.
154. Hamzah J., Altin J.G., Herringson T., Parish C.R., Hammerling G.J., O'Donoghue H., Ganss R. Targeted liposomal delivery of TLR9 ligands activates spontaneous antitumor immunity in an autochthonous cancer model. J. Immunol. 2009, 183:1091-1098.
155. Cabral H., Murakami M., Hojo H., Terada Y., Kano M.R., Chung U., Nishiyama N., Kataoka K. Targeted therapy of spontaneous murine pancreatic tumors by polymeric micelles prolongs survival and prevents peritoneal metastasis. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:11397-11402.
156. Fridlyand J., Simon R.M., Walrath J.C., Roach N., Buller R., Schenkein D.P., Flaherty K.T., Allen J.D., Sigal E.V., Scher H.I. Considerations for the successful co-development of targeted cancer therapies and companion diagnostics. Nat. Rev. Drug Discov. 2013, 12:743-755.
157. US Food & Drug Administration Guidance for industry: enrichment strategies for clinical trials to support approval of human drugs and biological products (draft duidance) in. http://www.fda.gov/downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/UCM332181.pdf.
158. Lanza G.M., Moonen C., Baker J.R., Chang E., Cheng Z., Grodzinski P., Ferrara K., Hynynen K., Kelloff G., Lee Y.E., Patri A.K., Sept D., Schnitzer J.E., Wood B.J., Zhang M., Zheng G., Farahani K. Assessing the barriers to image-guided drug delivery. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2014, 6:1-14.
159. Kim K., Kim J.H., Park H., Kim Y.S., Park K., Nam H., Lee S., Park J.H., Park R.W., Kim I.S., Choi K., Kim S.Y., Park K., Kwon I.C. Tumor-homing multifunctional nanoparticles for cancer theragnosis: simultaneous diagnosis, drug delivery, and therapeutic monitoring. J. Control. Release 2010, 146:219-227.
160. Mura S., Couvreur P. Nanotheranostics for personalized medicine. Adv. Drug Deliv. Rev. 2012, 64:1394-1416.
161. Merrimack Pharmaceuticals Merrimack announces encouraging clinical data from expanded phase 1 study of MM-302 for the treatment of advanced HER2-positive breast cancer in. http://investors.merrimackpharma.com/releasedetail.cfm?ReleaseID=813850.
162. Lammers T., Rizzo L.Y., Storm G., Kiessling F. Personalized nanomedicine. Clin. Cancer Res. 2012, 18:4889-4894.
163. Cabral H., Kataoka K. Multifunctional nanoassemblies of block copolymers for future cancer therapy. Sci. Technol. Adv. Mater. 2010, 11.
164. Nasongkla N., Bey E., Ren J.M., Ai H., Khemtong C., Guthi J.S., Chin S.F., Sherry A.D., Boothman D.A., Gao J.M. Multifunctional polymeric micelles as cancer-targeted, MRI-ultrasensitive drug delivery systems. Nano Lett. 2006, 6:2427-2430.
165. Khemtong C., Kessinger C.W., Ren J.M., Bey E.A., Yang S.G., Guthi J.S., Boothman D.A., Sherry A.D., Gao J.M. In vivo off-resonance saturation magnetic resonance imaging of alpha(v)beta(3)-targeted superparamagnetic nanoparticles. Cancer Res. 2009, 69:1651-1658.
166. Kim D., Gao Z.G., Lee E.S., Bae Y.H. In vivo evaluation of doxorubicin-loaded polymeric micelles targeting folate receptors and early endosomal pH in drug-resistant ovarian cancer. Mol. Pharm. 2009, 6:1353-1362.
167. Tsai H.C., Chang W.H., Lo C.L., Tsai C.H., Chang C.H., Ou T.W., Yen T.C., Hsiue G.H. Graft and diblock copolymer multifunctional micelles for cancer chemotherapy and imaging. Biomaterials 2010, 31:2293-2301.