State-of-the-art in design rules for drug delivery platforms: Lessons learned from FDA-approved nanomedicines

Journal of Controlled Release

Volumn 187, Issue , 2014, Pages 133-144

  Dawidczyk, Charlene M ^a,b   Kim, Chloe ^a,b   Park, Jea Ho ^a,b   Russell, Luisa M ^a,b   Lee, Kwan Hyi ^c   Pomper, Martin G ^a,b,d   Searson, Peter C ^a,b  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c Korea Institute of Science and Technology   (South Korea)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Active targeting; Circulation; Enhanced permeability and retention (EPR) effect; Liposomes; Nanoparticles; Tumor targeting

Indexed keywords

BOILER CIRCULATION; CONTROLLED DRUG DELIVERY; DRUG INTERACTIONS; LIPOSOMES; MONOCLONAL ANTIBODIES; NANOPARTICLES; TUMORS;

ACTIVE TARGETING; ANTIBODY-DRUG CONJUGATES; DESIGN CONSTRAINTS; DESIGN STRATEGIES; ENHANCED PERMEABILITY AND RETENTION EFFECTS; SYSTEMIC DELIVERIES; TARGETED DELIVERY; TUMOR TARGETING;

TARGETED DRUG DELIVERY;

ALBUMIN; BRENTUXIMAB VEDOTIN; DAUNORUBICIN; DOXORUBICIN; LIPOSOME; MACROGOL; NANOCARRIER; PACLITAXEL; TRASTUZUMAB EMTANSINE; VINCRISTINE SULFATE; ANTIBODY CONJUGATE; ANTINEOPLASTIC AGENT; NANOPARTICLE;

AREA UNDER THE CURVE; ARTICLE; BLOOD VESSEL PERMEABILITY; CANCER CHEMOTHERAPY; CIRCULATION; DISTRIBUTION VOLUME; DRUG ACCUMULATION; DRUG BLOOD LEVEL; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG ELIMINATION; DRUG EXTRAVASATION; DRUG FORMULATION; DRUG HALF LIFE; DRUG RELEASE; DRUG SOLUBILITY; DRUG TRANSPORT; ENDOCYTOSIS; ENDOSOME; ENHANCED PERMEABILITY AND RETENTION EFFECT; INTERNALIZATION; MOLECULARLY TARGETED THERAPY; MONONUCLEAR PHAGOCYTE; NONHUMAN; PRIORITY JOURNAL; SURFACE TENSION; TISSUE PRESSURE; TRANSCYTOSIS; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; ANIMAL; DRUG APPROVAL; DRUG DESIGN; FOOD AND DRUG ADMINISTRATION; HUMAN; METABOLISM; NANOMEDICINE; NEOPLASMS; UNITED STATES;

ANIMALS; ANTINEOPLASTIC AGENTS; DRUG APPROVAL; DRUG DELIVERY SYSTEMS; DRUG DESIGN; HUMANS; IMMUNOCONJUGATES; NANOMEDICINE; NANOPARTICLES; NEOPLASMS; UNITED STATES; UNITED STATES FOOD AND DRUG ADMINISTRATION;

EID: 84902136468     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.05.036     Document Type: Review

References (112)

1. D. Schrama, R.A. Reisfeld, and J.C. Becker Antibody targeted drugs as cancer therapeutics Nat. Rev. Drug Discov. 5 2006 147 159
2. G.P. Adams, and L.M. Weiner Monoclonal antibody therapy of cancer Nat. Biotechnol. 23 2005 1147 1157 (Pubitemid 41486396)
3. A.M. Scott, J.P. Allison, and J.D. Wolchok Monoclonal antibodies in cancer therapy Cancer Immun. 12 2012 14
4. L. Galluzzi, E. Vacchelli, W.H. Fridman, J. Galon, C. Sautes-Fridman, E. Tartour, J. Zucman-Rossi, L. Zitvogel, and G. Kroemer Trial watch: monoclonal antibodies in cancer therapy Oncoimmunology 1 2012 28 37
5. M.A. Firer, and G. Gellerman Targeted drug delivery for cancer therapy: the other side of antibodies J. Hematol. Oncol. 5 2012 70
6. T.R. Daniels, E. Bernabeu, J.A. Rodriguez, S. Patel, M. Kozman, D.A. Chiappetta, E. Holler, J.Y. Ljubimova, G. Helguera, and M.L. Penichet The transferrin receptor and the targeted delivery of therapeutic agents against cancer Biochim. Biophys. Acta 1820 2012 291 317
7. N. Parker, M.J. Turk, E. Westrick, J.D. Lewis, P.S. Low, and C.P. Leamon Folate receptor expression in carcinomas and normal tissues determined by a quantitative radioligand binding assay Anal. Biochem. 338 2005 284 293 (Pubitemid 40312593)
8. S.M. Paul, D.S. Mytelka, C.T. Dunwiddie, C.C. Persinger, B.H. Munos, S.R. Lindborg, and A.L. Schacht How to improve R&D productivity: the pharmaceutical industry's grand challenge Nat. Rev. Drug Discov. 9 2010 203 214
9. R.V. Chari, M.L. Miller, and W.C. Widdison Antibody-drug conjugates: an emerging concept in cancer therapy Angew. Chem. Int. Ed. Engl. 53 2014 3796 3827
10. A. Mullard Maturing antibody-drug conjugate pipeline hits 30 Nat. Rev. Drug Discov. 12 2013 329 332
11. B. Nolting Linker technologies for antibody-drug conjugates Methods Mol. Biol. 1045 2013 71 100
12. E.L. Sievers, and P.D. Senter Antibody-drug conjugates in cancer therapy Annu. Rev. Med. 64 2013 15 29
13. I. Sassoon, and V. Blanc Antibody-drug conjugate (ADC) clinical pipeline: a review Methods Mol. Biol. 1045 2013 1 27
14. A.M. Bradley, M. Devine, and D. DeRemer Brentuximab vedotin: an anti-CD30 antibody-drug conjugate Am. J. Health Syst. Pharm. 70 2013 589 597
15. D. Lu, H.A. Burris, B. Wang, E.C. Dees, J. Cortes, A. Joshi, M. Gupta, J.H. Yi, Y.W. Chu, T. Shih, L. Fang, and S. Girish Drug interaction potential of trastuzumab emtansine (T-DM1) combined with pertuzumab in patients with HER2-positive metastatic breast cancer Curr. Drug Metab. 13 2012 911 922
16. S. Verma, D. Miles, L. Gianni, I.E. Krop, M. Welslau, J. Baselga, M. Pegram, D.Y. Oh, V. Dieras, E. Guardino, L. Fang, M.W. Lu, S. Olsen, K. Blackwell, and E.S. Group Trastuzumab emtansine for HER2-positive advanced breast cancer N. Engl. J. Med. 367 2012 1783 1791
17. P.M. LoRusso, D. Weiss, E. Guardino, S. Girish, and M.X. Sliwkowski Trastuzumab emtansine: a unique antibody-drug conjugate in development for human epidermal growth factor receptor 2-positive cancer Clin. Cancer Res. 17 2011 6437 6447
18. S. Girish, M. Gupta, B. Wang, D. Lu, I.E. Krop, C.L. Vogel, H.A. Burris, P.M. LoRusso, J.H. Yi, O. Saad, B. Tong, Y.W. Chu, S. Holden, and A. Joshi Clinical pharmacology of trastuzumab emtansine (T-DM1): an antibody-drug conjugate in development for the treatment of HER2-positive cancer Cancer Chemother. Pharmacol. 69 2012 1229 1240
19. P.A. Trail Antibody-drug conjugates as cancer therapeutics Antibodies 2 2013 113 129
20. B.Q. Shen, K. Xu, L. Liu, H. Raab, S. Bhakta, M. Kenrick, K.L. Parsons-Reponte, J. Tien, S.F. Yu, E. Mai, D. Li, J. Tibbitts, J. Baudys, O.M. Saad, S.J. Scales, P.J. McDonald, P.E. Hass, C. Eigenbrot, T. Nguyen, W.A. Solis, R.N. Fuji, K.M. Flagella, D. Patel, S.D. Spencer, L.A. Khawli, A. Ebens, W.L. Wong, R. Vandlen, S. Kaur, M.X. Sliwkowski, R.H. Scheller, P. Polakis, and J.R. Junutula Conjugation site modulates the in vivo stability and therapeutic activity of antibody-drug conjugates Nat. Biotechnol. 30 2012 184 189
21. A. Younes, N.L. Bartlett, J.P. Leonard, D.A. Kennedy, C.M. Lynch, E.L. Sievers, and A. Forero-Torres Brentuximab vedotin (SGN-35) for relapsed CD30-positive lymphomas N. Engl. J. Med. 363 2010 1812 1821
22. A. Gabizon, H. Shmeeda, and Y. Barenholz Pharmacokinetics of pegylated liposomal Doxorubicin: review of animal and human studies Clin. Pharmacokinet. 42 2003 419 436 (Pubitemid 36649037)
23. R. Erttmann, N. Erb, A. Steinhoff, and G. Landbeck Pharmacokinetics of doxorubicin in man: dose and schedule dependence J. Cancer Res. Clin. Oncol. 114 1988 509 513
24. J.M. Jacquet, F. Bressolle, M. Galtier, M. Bourrier, D. Donadio, J. Jourdan, and J.F. Rossi Doxorubicin and doxorubicinol: intra- and inter-individual variations of pharmacokinetic parameters Cancer Chemother. Pharmacol. 27 1990 219 225
25. S.C. Piscitelli, K.A. Rodvold, D.A. Rushing, and D.A. Tewksbury Pharmacokinetics and pharmacodynamics of doxorubicin in patients with small cell lung cancer Clin. Pharmacol. Ther. 53 1993 555 561 (Pubitemid 23161203)
26. P.S. Gill, J. Wernz, D.T. Scadden, P. Cohen, G.M. Mukwaya, J.H. von Roenn, M. Jacobs, S. Kempin, I. Silverberg, G. Gonzales, M.U. Rarick, A.M. Myers, F. Shepherd, C. Sawka, M.C. Pike, and M.E. Ross Randomized phase III trial of liposomal daunorubicin versus doxorubicin, bleomycin, and vincristine in AIDS-related Kaposi's sarcoma J. Clin. Oncol. 14 1996 2353 2364 (Pubitemid 26264888)
27. J.A. Silverman, and S.R. Deitcher Marqibo(R) (vincristine sulfate liposome injection) improves the pharmacokinetics and pharmacodynamics of vincristine Cancer Chemother. Pharmacol. 71 2013 555 564
28. A. Sparreboom, C.D. Scripture, V. Trieu, P.J. Williams, T. De, A. Yang, B. Beals, W.D. Figg, M. Hawkins, and N. Desai Comparative preclinical and clinical pharmacokinetics of a cremophor-free, nanoparticle albumin-bound paclitaxel (ABI-007) and paclitaxel formulated in Cremophor (Taxol) Clin. Cancer Res. 11 2005 4136 4143 (Pubitemid 40791578)
29. M. Ando, K. Yonemori, N. Katsumata, C. Shimizu, T. Hirata, H. Yamamoto, K. Hashimoto, M. Yunokawa, K. Tamura, and Y. Fujiwara Phase I and pharmacokinetic study of nab-paclitaxel, nanoparticle albumin-bound paclitaxel, administered weekly to Japanese patients with solid tumors and metastatic breast cancer Cancer Chemother. Pharmacol. 69 2012 457 465
30. T.E. Stinchcombe, M.A. Socinski, C.M. Walko, B.H. O'Neil, F.A. Collichio, A. Ivanova, H. Mu, M.J. Hawkins, R.M. Goldberg, C. Lindley, and E. Claire Dees Phase I and pharmacokinetic trial of carboplatin and albumin-bound paclitaxel, ABI-007 (Abraxane) on three treatment schedules in patients with solid tumors Cancer Chemother. Pharmacol. 60 2007 759 766 (Pubitemid 47247287)
31. G. Leriche, L. Chisholm, and A. Wagner Cleavable linkers in chemical biology Bioorg. Med. Chem. 20 2012 571 582
32. B.J. Mills, and C.A. Lang Differential distribution of free and bound glutathione and cyst(e)ine in human blood Biochem. Pharmacol. 52 1996 401 406 (Pubitemid 26233582)
33. C.D. Austin, X.H. Wen, L. Gazzard, C. Nelson, R.H. Scheller, and S.J. Scales Oxidizing potential of endosomes and lysosomes limits intracellular cleavage of disulfide-based antibody-drug conjugates Proc. Natl. Acad. Sci. U. S. A. 102 2005 17987 17992 (Pubitemid 41798489)
34. B.A. Chabner, and T.G. Roberts Timeline - chemotherapy and the war on cancer Nat. Rev. Cancer 5 2005 65 72
35. V.T. DeVita, and E. Chu A history of cancer chemotherapy Cancer Res. 68 2008 8643 8653
36. R. Kim, K. Tanabe, Y. Uchida, M. Emi, H. Inoue, and T. Toge Current status of the molecular mechanisms of anticancer drug-induced apoptosis - the contribution of molecular-level analysis to cancer chemotherapy Cancer Chemother. Pharmacol. 50 2002 343 352 (Pubitemid 35440522)
37. K.E. Gascoigne, and S.S. Taylor How do anti-mitotic drugs kill cancer cells? J. Cell Sci. 122 2009 2579 2585
38. M.J. Hannon Metal-based anticancer drugs: from a past anchored in platinum post-genomic future and biology Pure Appl. Chem. 79 2007 2243 2261
39. S. Nussbaumer, P. Bonnabry, J.L. Veuthey, and S. Fleury-Souverain Analysis of anticancer drugs: a review Talanta 85 2011 2265 2289
40. V.P. Torchilin Recent advances with liposomes as pharmaceutical carriers Nat. Rev. Drug Discov. 4 2005 145 160 (Pubitemid 40282557)
41. P.G. Rose Pegylated liposomal doxorubicin: optimizing the dosing schedule in ovarian cancer Oncologist 10 2005 205 214 (Pubitemid 40463158)
42. J.F. Galloway, A. Winter, K.H. Lee, J.H. Park, C.M. Dvoracek, P. Devreotes, and P.C. Searson Quantitative characterization of the lipid encapsulation of quantum dots for biomedical applications Nanomedicine 8 2012 1190 1199
43. M.L. Immordino, F. Dosio, and L. Cattel Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential Int. J. Nanomedicine 1 2006 297 315
44. D. Vllasaliu, R. Fowler, and S. Stolnik PEGylated nanomedicines: recent progress and remaining concerns Expert Opin. Drug Deliv. 11 2014 139 154
45. Y. Barenholz Doxil(R) - the first FDA-approved nano-drug: lessons learned J. Control. Release 160 2012 117 134
46. A. Gabizon, R. Catane, B. Uziely, B. Kaufman, T. Safra, R. Cohen, F. Martin, A. Huang, and Y. Barenholz Prolonged circulation time and enhanced accumulation in malignant exudates of doxorubicin encapsulated in polyethylene-glycol coated liposomes Cancer Res. 54 1994 987 992 (Pubitemid 24085451)
47. D.D. Lasic, P.M. Frederik, M.C. Stuart, Y. Barenholz, and T.J. McIntosh Gelation of liposome interior. A novel method for drug encapsulation FEBS Lett. 312 1992 255 258
48. G. Haran, R. Cohen, L.K. Bar, and Y. Barenholz Transmembrane ammonium sulfate gradients in liposomes produce efficient and stable entrapment of amphipathic weak bases Biochim. Biophys. Acta 1151 1993 201 215 (Pubitemid 23283973)
49. K. Mross, B. Niemann, U. Massing, J. Drevs, C. Unger, R. Bhamra, and C.E. Swenson Pharmacokinetics of liposomal doxorubicin (TLC-D99; Myocet) in patients with solid tumors: an open-label, single-dose study Cancer Chemother. Pharmacol. 54 2004 514 524 (Pubitemid 40022247)
50. D.L. Gustafson, J.C. Rastatter, T. Colombo, and M.E. Long Doxorubicin pharmacokinetics: macromolecule binding, metabolism, and excretion in the context of a physiologic model J. Pharm. Sci. 91 2002 1488 1501 (Pubitemid 34633964)
51. R. Bellott, A. Auvrignon, T. Leblanc, Y. Perel, V. Gandemer, Y. Bertrand, F. Mechinaud, P. Bellenger, J. Vernois, G. Leverger, A. Baruchel, and J. Robert Pharmacokinetics of liposomal daunorubicin [DaunoXome] during a phase I-II study in children with relapsed acute lymphoblastic leukaemia Cancer Chemother. Pharmacol. 47 2001 15 21 (Pubitemid 32664507)
52. R. Solomon, and A.A. Gabizon Clinical pharmacology of liposomal anthracyclines: focus on pegylated liposomal doxorubicin Clin. Lymphoma Myeloma 8 2008 21 32 (Pubitemid 351449716)
53. A.H. Sarris, F. Hagemeister, J. Romaguera, M.A. Rodriguez, P. McLaughlin, A.M. Tsimberidou, L.J. Medeiros, B. Samuels, O. Pate, M. Oholendt, H. Kantarjian, C. Burge, and F. Cabanillas Liposomal vincristine in relapsed non-Hodgkin's lymphomas: early results of an ongoing phase II trial Ann. Oncol. 11 2000 69 72 (Pubitemid 30084582)
54. K.M. Skubitz Phase II trial of pegylated-liposomal doxorubicin (Doxil (TM)) in sarcoma Cancer Investig. 21 2003 167 176 (Pubitemid 36532162)
55. T. Safra, F. Muggia, S. Jeffers, D.D. Tsao-Wei, S. Groshen, O. Lyass, R. Henderson, G. Berry, and A. Gabizon Pegylated liposomal doxorubicin (doxil): reduced clinical cardiotoxicity in patients reaching or exceeding cumulative doses of 500 mg/m(2) Ann. Oncol. 11 2000 1029 1033
56. M.E. O'Brien, N. Wigler, M. Inbar, R. Rosso, E. Grischke, A. Santoro, R. Catane, D.G. Kieback, P. Tomczak, S.P. Ackland, F. Orlandi, L. Mellars, L. Alland, and C. Tendler Reduced cardiotoxicity and comparable efficacy in a phase III trial of pegylated liposomal doxorubicin HCl (CAELYX/Doxil) versus conventional doxorubicin for first-line treatment of metastatic breast cancer Ann. Oncol. 15 2004 440 449 (Pubitemid 38444547)
57. M. Cianfrocca, S. Lee, J. Von Roenn, A. Tulpule, B.J. Dezube, D.M. Aboulafia, R.F. Ambinder, J.Y. Lee, S.E. Krown, and J.A. Sparano Randomized trial of paclitaxel versus pegylated liposomal doxorubicin for advanced human immunodeficiency virus-associated Kaposi sarcoma: evidence of symptom palliation from chemotherapy Cancer 116 2010 3969 3977
58. A.N. Gordon, J.T. Fleagle, D. Guthrie, D.E. Parkin, M.E. Gore, and A.J. Lacave Recurrent epithelial ovarian carcinoma: a randomized phase III study of pegylated liposomal doxorubicin versus topotecan J. Clin. Oncol. 19 2001 3312 3322 (Pubitemid 32642183)
59. E. Paszko, and M.O. Senge Immunoliposomes Curr. Med. Chem. 19 2012 5239 5277
60. A. Tojo, and S. Kinugasa Mechanisms of glomerular albumin filtration and tubular reabsorption Int. J. Nephrol. 2012 2012 481520
61. T. Peters All About Albumin: Biochemistry, Genetics, and Medical Applications 1996 Academic Press San Diego
62. E. Miele, G.P. Spinelli, E. Miele, F. Tomao, and S. Tomao Albumin-bound formulation of paclitaxel (Abraxane ABI-007) in the treatment of breast cancer Int. J. Nanomedicine 4 2009 99 105
63. D.A. Yardley nab-Paclitaxel mechanisms of action and delivery J. Control. Release 170 2013 365 372
64. W.C. Aird Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms Circ. Res. 100 2007 158 173 (Pubitemid 46208717)
65. M. Lundqvist, J. Stigler, T. Cedervall, T. Berggard, M.B. Flanagan, I. Lynch, G. Elia, and K. Dawson The evolution of the protein corona around nanoparticles: a test study ACS Nano 5 2011 7503 7509
66. M. Lundqvist, J. Stigler, G. Elia, I. Lynch, T. Cedervall, and K.A. Dawson Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts Proc. Natl. Acad. Sci. U. S. A. 105 2008 14265 14270
67. S. Tenzer, D. Docter, S. Rosfa, A. Wlodarski, J. Kuharev, A. Rekik, S.K. Knauer, C. Bantz, T. Nawroth, C. Bier, J. Sirirattanapan, W. Mann, L. Treuel, R. Zellner, M. Maskos, H. Schild, and R.H. Stauber Nanoparticle size is a critical physicochemical determinant of the human blood plasma corona: a comprehensive quantitative proteomic analysis ACS Nano 5 2011 7155 7167
68. D.A. Hume The mononuclear phagocyte system Curr. Opin. Immunol. 18 2006 49 53 (Pubitemid 43049647)
69. T. Groth, Z.M. Liu, M. Niepel, D. Peschel, K. Kirchhof, G. Altankov, and N. Faucheux Chemical and physical modifications of biomaterial surfaces to control adhesion of cells Adv. Role Nanotechnol. Eng. Princ. 2010 253 284
70. R. Medzhitov, and C.A. Janeway Jr. Decoding the patterns of self and nonself by the innate immune system Science 296 2002 298 300 (Pubitemid 34303673)
71. P.A. Oldenborg, A. Zheleznyak, Y.F. Fang, C.F. Lagenaur, H.D. Gresham, and F.P. Lindberg Role of CD47 as a marker of self on red blood cells Science 288 2000 2051- +
72. P.L. Rodriguez, T. Harada, D.A. Christian, D.A. Pantano, R.K. Tsai, and D.E. Discher Minimal "self" peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles Science 339 2013 971 975
73. J. Fang, H. Nakamura, and H. Maeda 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. 63 2011 136 151
74. H. Maeda Macromolecular therapeutics in cancer treatment: the EPR effect and beyond J. Control. Release 164 2012 138 144
75. R.K. Jain, and T. Stylianopoulos Delivering nanomedicine to solid tumors Nat. Rev. Clin. Oncol. 7 2010 653 664
76. N. Bertrand, J. Wu, X. Xu, N. Kamaly, and O.C. Farokhzad Cancer nanotechnology: the impact of passive and active targeting in the era of modern cancer biology Adv. Drug Deliv. Rev. 66C 2014 2 25
77. V. Torchilin Tumor delivery of macromolecular drugs based on the EPR effect Adv. Drug Deliv. Rev. 63 2011 131 135
78. F. Yuan, M. Dellian, D. Fukumura, M. Leunig, D.A. Berk, V.P. Torchilin, and R.K. Jain Vascular-permeability in a human tumor xenograft - molecular-size dependence and cutoff size Cancer Res. 55 1995 3752 3756
79. F. Yuan, H.A. Salehi, Y. Boucher, U.S. Vasthare, R.F. Tuma, and R.K. Jain Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows Cancer Res. 54 1994 4564 4568 (Pubitemid 24276471)
80. Y. Matsumura A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent SMANCS Cancer Res. 46 1986 6387 6392 (Pubitemid 17221789)
81. H. Maeda Tumor-selective delivery of macromolecular drugs via the EPR effect: background and future prospects Bioconjugate Chem 21 2010 797 802
82. R.K. Jain Transport of molecules across tumor vasculature Cancer Metastasis Rev. 6 1987 559 593
83. H. Maeda, G.Y. Bharate, and J. Daruwalla Polymeric drugs for efficient tumor-targeted drug delivery based on EPR-effect Eur. J. Pharm. Biopharm. 71 2009 409 419
84. Z. Symon, A. Peyser, D. Tzemach, O. Lyass, E. Sucher, E. Shezen, and A. Gabizon Selective delivery of doxorubicin to patients with breast carcinoma metastases by stealth liposomes Cancer 86 1999 72 78 (Pubitemid 29293379)
85. A. Pyka, M. Babuska, and M. Zachariasz A comparison of theoretical methods of calculation of partition coefficients for selected drugs Acta Pol. Pharm. 63 2006 159 167 (Pubitemid 351359750)
86. S.K. Hobbs, W.L. Monsky, F. Yuan, W.G. Roberts, L. Griffith, V.P. Torchilin, and R.K. Jain Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment Proc. Natl. Acad. Sci. U. S. A. 95 1998 4607 4612 (Pubitemid 28207960)
87. R.K. Jain Determinants of tumor blood-flow - a review Cancer Res. 48 1988 2641 2658
88. D. Peer, J.M. Karp, S. Hong, O.C. Farokhzad, R. Margalit, and R. Langer Nanocarriers as an emerging platform for cancer therapy Nat. Nanotechnol. 2 2007 751 760 (Pubitemid 350223348)
89. R.K. Jain Delivery of molecular and cellular medicine to solid tumors Adv. Drug Deliv. Rev. 26 1997 71 90 (Pubitemid 27289526)
90. G.J. Doherty, and H.T. McMahon Mechanisms of endocytosis Annu. Rev. Biochem. 78 2009 857 902
91. C.M. Paulos, J.A. Reddy, C.P. Leamon, M.J. Turk, and P.S. Low Ligand binding and kinetics of folate receptor recycling in vivo: impact on receptor-mediated drug delivery Mol. Pharmacol. 66 2004 1406 1414 (Pubitemid 39564767)
92. A. Nel, T. Xia, L. Madler, and N. Li Toxic potential of materials at the nanolevel Science 311 2006 622 627 (Pubitemid 43191298)
93. K.K. Frese, and D.A. Tuveson Maximizing mouse cancer models Nat. Rev. Cancer 7 2007 645 658 (Pubitemid 47327410)
94. M. Liu, and D. Hicklin Human tumor xenograft efficacy models B.A. Teicher, Tumor Models in Cancer Research 2011 Springer 99 124
95. S.D. Steichen, M. Caldorera-Moore, and N.A. Peppas A review of current nanoparticle and targeting moieties for the delivery of cancer therapeutics Eur. J. Pharm. Sci. 48 2012 416 427
96. G. Zhang, Z. Yang, W. Lu, R. Zhang, Q. Huang, M. Tian, L. Li, D. Liang, and C. Li Influence of anchoring ligands and particle size on the colloidal stability and in vivo biodistribution of polyethylene glycol-coated gold nanoparticles in tumor-xenografted mice Biomaterials 30 2009 1928 1936
97. G. von Maltzahn, J.H. Park, A. Agrawal, N.K. Bandaru, S.K. Das, M.J. Sailor, and S.N. Bhatia Computationally guided photothermal tumor therapy using long-circulating gold nanorod antennas Cancer Res. 69 2009 3892 3900
98. R. Rossin, D.P.J. Pan, K. Qi, J.L. Turner, X.K. Sun, K.L. Wooley, and M.J. Welch Cu-64-labeled folate-conjugated shell cross-linked nanoparticles for tumor imaging and radiotherapy: synthesis, radiolabeling, and biologic evaluation J. Nucl. Med. 46 2005 1210 1218 (Pubitemid 43741084)
99. M.O. Oyewumi, R.A. Yokel, M. Jay, T. Coakley, and R.J. Mumper Comparison of cell uptake, biodistribution and tumor retention of folate-coated and PEG-coated gadolinium nanoparticles in tumor-bearing mice J. Control. Release 95 2004 613 626 (Pubitemid 38340510)
100. X. Yang, H. Hong, J.J. Grailer, I.J. Rowland, A. Javadi, S.A. Hurley, Y. Xiao, Y. Yang, Y. Zhang, R.J. Nickles, W. Cai, D.A. Steeber, and S. Gong cRGD-functionalized, DOX-conjugated, and (6)(4)Cu-labeled superparamagnetic iron oxide nanoparticles for targeted anticancer drug delivery and PET/MR imaging Biomaterials 32 2011 4151 4160
101. M. Benezra, O. Penate-Medina, P.B. Zanzonico, D. Schaer, H. Ow, A. Burns, E. DeStanchina, V. Longo, E. Herz, S. Iyer, J. Wolchok, S.M. Larson, U. Wiesner, and M.S. Bradbury Multimodal silica nanoparticles are effective cancer-targeted probes in a model of human melanoma J. Clin. Investig. 121 2011 2768 2780
102. 89Zr-labeled cetuximab in mice Contrast Media Mol. Imaging. 8 2013 402 408
103. N. Chattopadhyay, H. Fonge, Z. Cai, D. Scollard, E. Lechtman, S.J. Done, J.-P. Pignol, and R.M. Reilly Role of antibody-mediated tumor targeting and route of administration in nanoparticle tumor accumulation in vivo Mol. Pharm. 9 2012 2168 2179
104. A. Natarajan, C. Gruettner, R. Ivkov, G.L. DeNardo, G. Mirick, A. Yuan, A. Foreman, and S.J. DeNardo NanoFerrite particle based radioimmunonanoparticles: binding affinity and in vivo pharmacokinetics Bioconjug. Chem. 19 2008 1211 1218 (Pubitemid 351874943)
105. B. Cornelissen, S. Able, V. Kersemans, P.A. Waghorn, S. Myhra, K. Jurkshat, A. Crossley, and K.A. Vallis Nanographene oxide-based radioimmunoconstructs for in vivo targeting and SPECT imaging of HER2-positive tumors Biomaterials 34 2013 1146 1154
106. M.P. Melancon, W. Lu, Z. Yang, R. Zhang, Z. Cheng, A.M. Elliot, J. Stafford, T. Olson, J.Z. Zhang, and C. Li In vitro and in vivo targeting of hollow gold nanoshells directed at epidermal growth factor receptor for photothermal ablation therapy Mol. Cancer Ther. 7 2008 1730 1739
107. H. Hong, Y. Zhang, J.W. Engle, T.R. Nayak, C.P. Theuer, R.J. Nickles, T.E. Barnhart, and W. Cai In vivo targeting and positron emission tomography imaging of tumor vasculature with Ga-66-labeled nano-graphene Biomaterials 33 2012 4147 4156
108. B.J. Hicke, A.W. Stephens, T. Gould, Y.F. Chang, C.K. Lynott, J. Heil, S. Borkowski, C.S. Hilger, G. Cook, S. Warren, and P.G. Schmidt Tumor targeting by an aptamer J. Nucl. Med. 47 2006 668 678 (Pubitemid 46768469)
109. E.-K. Lim, B. Kim, Y. Choi, Y. Ro, E.-J. Cho, J. Lee, S.-H. Ryu, J.-S. Suh, S. Haam, and Y.-M. Huh Aptamer-conjugated magnetic nanoparticles enable efficient targeted detection of integrin avb3 via magnetic resonance imaging J. Biomed. Mater. A 102 2013 45 49
110. M. Kumar, M. Yigit, G.P. Dai, A. Moore, and Z. Medarova Image-guided breast tumor therapy using a small interfering RNA nanodrug Cancer Res. 70 2010 7553 7561
111. N. Chanda, V. Kattumuri, R. Shukla, A. Zambre, K. Katti, A. Upendran, R.R. Kulkarni, P. Kan, G.M. Fent, S.W. Casteel, C.J. Smith, E. Boote, J.D. Robertson, C. Cutler, J.R. Lever, K.V. Katti, and R. Kannan Bombesin functionalized gold nanoparticles show in vitro and in vivo cancer receptor specificity Proc. Natl. Acad. Sci. U. S. A. 107 2010 8760 8765
112. C.H.J. 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