"Targeting" nanoparticles: The constraints of physical laws and physical barriers

Journal of Controlled Release

Volumn 164, Issue 2, 2012, Pages 115-124

  Florence, Alexander T ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Aggregation; Diffusion; Jamming; Nanoparticles; Targeting; Tumors

Indexed keywords

CHANGING ENVIRONMENT; COMPLEX MEDIA; CONFINED SPACE; IN-VITRO; IN-VIVO; INTRAVENOUS ADMINISTRATION; MATERIAL SCIENCE; NANOCARRIERS; PHYSICAL BARRIERS; PHYSICAL LAWS; PHYSICAL PHENOMENA; PHYSICOCHEMICAL PARAMETERS; PHYSICOCHEMICAL PROPERTY; SIZE DEPENDENT; SURFACE SCIENCE; TARGETING;

AGGLOMERATION; DIFFUSION; FLOCCULATION; JAMMING; NANOPARTICLES; RANDOM PROCESSES; TUMORS;

PARTICLE SIZE;

NANOCARRIER; NANOPARTICLE;

ARTICLE; COLLOID; DIFFUSION; DISPERSION; DRUG RELEASE; DRUG TARGETING; FLOCCULATION; PARTICLE SIZE; PHYSICOCHEMICAL MODEL; PRIORITY JOURNAL; STOCHASTIC MODEL; TUMOR LOCALIZATION;

ANIMALS; COLLOIDS; DRUG DELIVERY SYSTEMS; HUMANS; NANOPARTICLES; NEOPLASMS; PARTICLE SIZE;

EID: 84869488700     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2012.03.022     Document Type: Article

References (132)

1. S.M. Moghimi, A.C. Hunter, and T.L. Andresen Factors controlling nanoparticle pharmacokinetics: an integrated analysis and perspective Annu. Rev. Pharmacol. Toxicol. 52 2010 481 503
2. H. Holbeck, and Y. Yeo Intratumoral drug delivery with nanoparticulate carriers Pharm. Res. 28 2011 1819 1830
3. D. Peer, J.M. Karp, S. Hong, O.C. Farakhzad, R. Margalit, and R. Langer Nanocarriers as an emerging platform for cancer therapy Nat. Nanotechnol. 2 2007 751 760
4. J. Kreuter Nanoparticles - a historical perspective Int. J. Pharm. 331 2007 1 10
5. M. Caldorera-Moore, N. Giumard, L. Shi, and K. Roy Designer nanoparticles: incorporating size, shape and triggered release into nanoscale drug carriers Expert Opin. Drug Deliv. 7 2012 479 495
6. L. Illum, I.M. Hunneyball, and S.S. Davis The effect of hydrophilic coatings on the uptake of colloidal particles by the liver and by peritoneal macrophages Int. J. Pharm. 29 1986 53 65
7. A.M. Hillery, and A.T. Florence Effect of adsorbed poloxamer 188-407 surfactants on the intestinal uptake of 60 nm polystyrene particles after oral administration Int. J. Pharm. 132 1996 123 133
8. K.F. Pirollo, and E.H. Chane Does a targeting ligand influence nanoparticle tumor localisation or uptake? Trends Biotechnol. 26 2008 552 558
9. D.B. Kirpotin, D.C. Drummond, Y. Sheo, M.R. Shalaby, K. Hong, U.B. Nielsen, J.D. Marks, C.C. Benz, and J.W. Park Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localisation but does increase internalisation in animal models Cancer Res. 66 2006 6732 6740
10. R.K. Jain, and T. Stylianopoulos Delivering nanomedicine to solid tumors Nat. Rev. Clin. Oncol. 7 2010 653 664
11. P. Decuzzi, R. Pasquini, W. Arap, and M. Ferrari Intravascular delivery of particulate systems: does geometry really matter? Pharm. Res. 26 2009 235 243
12. V.P. Torchilin Targeted pharmaceutical nanocarriers for cancer therapy and imaging AAPS J. 9 2 2007 article 15
13. I. Hamad, and S. Moghimi Critical issues in site-specific targeting of solid tumors: the carrier, the tumor barriers and the bioavailable drug Expert Opin. Drug Deliv. 5 2008 205 219
14. Y.H. Bae, and K. Park Targeted drug delivery to tumors: myths, reality and possibility J. Control. Release 153 2011 198 205
15. W.R. Sanhai, J.H. Sakamoto, R. Canady, and M. Ferrari Seven challenges for nanomedicine Nat. Nanotechnol. 3 2008 242 244
16. M. Ferrari Cancer nanotechnology: opportunities and challenges Nat. Rev. Cancer 5 2005 161 171
17. T. Lammers, F. Kiessling, W.E. Hennick, and G. Storm Drug targeting to tumors: principles, pitfalls and (pre-) clinical progress J. Control. Release 161 2012 175 187
18. K. Kosterelos, A. Bianco, and M. Prato Promises, facts and challenges for carbon nanotubes in imaging and therapeutics Nat. Nanotechnol. 4 2009 627 633
19. D. Vinck Les Nanotechnologies Idées Reçues 2009 Editions Le Cavalier Blue 75
20. see: 100 years ago Nature 481 2012 272
21. Anon Further developments in the investigation of cancer JAMA 63 1914 33 34
22. Z. Lui, W. Cai, L. He, N. Nakayama, K. Chen, X. Sun, X. Chen, and H. Dai In vivo distribution and highly efficient tumour targeting of carbon nanotubes in mice Nat. Nanotechnol. 2 2007 47 52
23. Y. Lu, and H. Wang Nanotechnology tackles tumours Nat. Nanotechnol. 2 2007 20 21
24. A. de la Zerda, and S.S. Gambhir Drug delivery: keeping tabs on nanocarriers Nat. Nanotechnol. 2 2007 745 746
25. N.M. Moore, N.Z. Kuhn, S.E. Hanlon, J.S.H. Lee, and L.A. Nagahara De-convoluting cancer's complexity: using a 'physical science lens' to provide a different clearer perspective of cancer Phys. Biol. 8 2011 1 4 10.1088/1478-3975/8/1/010302
26. A. Trabesinger Complexity Nat. Phys. 8 2012 13
27. A.T. Florence Reductionism and complexity in nanoparticle-vectored drug targeting J. Control. Release 161 2012 399 402
28. A.-L. Barabási The network takeover Nat. Phys. 8 2012 14 16
29. P. Ruenraroengsak, J.M. Cook, and A.T. Florence Nanosystem drug targeting; facing up to complex realities J. Control. Release 141 2010 265 276
30. E.C. Cho, Q. Zhang, and Y. Xia The effect of sedimentation and diffusion on cellular uptake of gold nanoparticles Nat. Nanotechnol. 6 2011 385 391
31. A.T. Florence Pharmaceutical nanotechnology: more than size. Ten topics for research Int. J. Pharm. 339 2007 1 2
32. J.K. Vasir, M.K. reddy, and V.D. Labhasetwar Nanosystems in drug targeting: opportunities and challenges Curr. Nanosci. 1 2005 47 64
33. A.T. Florence, and P. Ruenraroengsak Cytoplasmic diffusion of dendrimers and dendriplexes V. Weissig, G.M. D'Souza, Organelle Specific Pharmaceutical Nanotechnology 2010 Wiley New York
34. L. Tao, and C. Nicholson Maximum geometric hindrance to diffusion in brain extracellular space surrounding uniformly spaced convex cells J. Theor. Biol. 229 2004 59 68
35. T.S. Chow Size-dependent adhesion of nanoparticles on rough substrates J. Phys. Condens. Matter 15 2003 1.83 1.87
36. S. Zhang, J. Li, G. Lykotrafitis, G. Bao, and S. Suresh Size-dependent endocytosis of nanoparticles Adv. Mater. 21 2009 419 424
37. H. Maeda, J. Wu, T. Sawa, Y. Matsumura, and K. Hori Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review J. Control. Release 65 2000 271 284
38. S.S. Rogers, N. Flores-Rodriquez, V.J. Allan, P.G. Woodman, and T.A. Waigh The first passage probability of intracellular particle trafficking Phys. Chem. Chem. Phys. 12 2001 3753 3761
39. I.F. Tannock, C.M. Lee, J.K. Tunggal, D.S.M. Cowan, and M.J. Egorin Limited penetration of anticancer drugs through tumor tissue: a potential cause of resistance of solid tumors to chemotherapy Clin. Cancer Res. 8 2002 878 884
40. R. Grantab, S. Sivananthan, and I.F. Tannock The penetration of anticancer drugs through tumor tissue as a function of cellular adhesion and packing density of cells Cancer Res. 66 2006 1033 1039
41. Y. Han, A.M. Alsayed, M. Nobili, J. Zhang, T.C. Lubensky, and A.G. Yodh Brownian motion of an ellipsoid Science 314 2006 626 630
42. J.B. Hubbard, and J.F. Douglas Hydrodynamic friction of arbitrarily shaped Brownian particles Phys. Rev. E 47 1993 R2983 R2986
43. L. Mirny Cell commuters avoid delays Nat. Phys. 4 2008 93 94
44. A.T. Florence, and P. Ruenraroengsak Cytoplasmic diffusion of dendrimers and dendriplexes V. Weissig, G.G.M. D'Souza, Organelle-Specific Pharmaceutical Nanotechnology 2006 Wiley New York
45. G.L. Lukacs, P. Haggie, O. Seksek, D. Lehardeurt, N. Freedman, and A.S. Verkmann Size-dependent DNA mobility on cytoplasm and nucleus J. Biol. Chem. 275 2000 1625 1629
46. S. Frey, R.P. Richter, and D. Görlich FG-rich repeats of nuclear pore proteins form a three dimensional meshwork with hydrogel-like properties Science 314 2006 815 817
47. B. Burke Nuclear pore complex models gel Science 314 2006 766 767
48. see also M. Elbaum Polymers in the pore Science 314 2006 766 767
49. R.M. Reilly, J. Sandhu, T.M. Alvarez-Diez, S. Gallinger, J. Kirsh, and H. Stern Problems of delivery of monoclonal antibodies Clin. Pharmacokinet. 28 1995 126 142
50. Anon Tumour cell diversity Lancet I 1983 222
51. R. McFadden, and C.S. Kwok Mathematical model of simultaneous diffusion and binding of antitumor antibodies in multicellular tumor spheroids Cancer Res. 48 1988 4032 4037
52. H. Fricke A mathematical treatment of the electrical conductivity and capacity of disperse systems Phys. Rev. 24 1923 575
53. J.S. Mackie, and P. Meares The diffusion of electrolytes in a cation-exchange resin membrane Proc. R. Soc. Lond. A 232 1955 498 509
54. L. Masaro, and X.X. Zhu Physical models of diffusion for polymer solutions, gels and solids Prog. Polym. Sci. 25 1999 731 775
55. J.H. Wang Theory of the self-diffusion of water in protein solutions. A new method for studying the hydration and shape of protein molecules J. Am. Chem. Soc. 76 1954 4755 4763
56. H. Fricke A mathematical treatment of the electrical conductivity and capacity of disperse systems, II: the capacity of a suspension of a conducting spheroid surrounded by a non-conducting membrane for a current of low-frequency Phys. Rev. 24 1924 575 587
57. A. Pluen, Y. Boucher, and S. Ramanujan Role of tumor-host interactions in interstitial diffusion of macromolecules: cranial vs. subcutaneous tumors Proc. Natl. Acad. Sci. U. S. A. 98 2001 4628 4633
58. C. Nicholson, and E. Syková Extracellular space structure revealed by diffusion analysis Trends Neurosci. 21 1998 207 215
59. H. Berry, and H. Chaté Anomalous sub-diffusion due to obstacles: a critical survey 2011 ArXiv. 1103.2206 v1 q-bio.QM
60. D.A. Weitz, and P.A. Janmey The soft framework of the cellular machine Proc. Natl. Acad. Sci. U. S. A. 105 2008 1105 1106
61. E.B. Brown, Y. Boucher, S. Nasser, and R.K. Jain Measurement of macromolecular diffusion coefficients in human tumors Microvasc. Res. 67 2004 231 236
62. R.K. Jain Transport of molecules, particles and cells in solid tumors Annu. Rev. Biomed. Eng. 1 1999 241 263
63. S.T. Reddy, D.A. Berk, R.K. Jain, and M.A. Swartz A sensitive in vivo model for quantifying interstitial convective transport of injected macromolecules and nanoparticles J. Appl. Physiol. 101 2006 1162 1169
64. K. Ushida, and A. Masuda General importance of anomalous diffusion in biological inhomogeneous systems H. Masuhara, S. Kawat, F. Tokunaga, Handai Nanophotonics 3 2007 Elsevier Amsterdam 175 et seq. '
65. H. Al-Obaidi, B. Nasseri, and A.T. Florence Dynamics of microparticles in lipid vesicles: movement in confined spaces J. Drug Target. 18 2010 821 830
66. G. Guigas, and M. Weiss Sampling the cell with anomalous diffusion - the discovery of slowness Biophys. J. 94 2008 90 94
67. C. Loverdo, O. Benichou, M. Moreau, and P. Voituriez Enhanced kinetics in biological cells Nat. Phys. 4 2008 134 137
68. M.H.G. Duits, Y. Li, S.A. Vanapalli, and F. Mugele Mapping of spatio-temporal heterogeneous particle dynamics in living cells Phys. Rev. E 79 2009 051910
69. N. Willmott, Y. Chen, and A.T. Florence Haemoglobin, transferrin and albumin/polyaspartic acid microspheres as carriers for the cytotoxic drug adriamycin: in vitro release rate J. Control. Release 8 1988 103 109
70. N. Willmott, Y. Chen, J. Goldberg, C. McCardle, and A.T. Florence Biodegradation rate of embolized protein microspheres in lung, liver and kidney of rats J. Pharm. Pharmacol. 41 1989 433 438
71. J.M. Cook, and A.T. Florence Penetration of etoposide into multicellular tumour spheroids: uptake and efflux J. Pharm. Pharmacol. 43 1991 26
72. J. Panyam, and V. Labhasetwar Dynamics of endocytosis and exocytosis of poly (D, L-lactide-co-glycolide) nanoparticles in vascular smooth muscle cells Pharm. Res. 20 2001 212 220
73. K.A. Johnson, G.B. Westermann-Clark, and D.O. Shah Diffusion of micelle-solubilised pyrene through microporous membranes J. Colloid Interface Sci. 130 1989 480 488
74. P. Stilbs A comparative study of micellar solubilization for combinations of surfactants and solubilizates using the Fourier transform pulsed gradient spin-echo NMR multicomponent self diffusion technique J. Colloid Interface Sci. 94 1983 463 469
75. D. Attwood, and A.T. Florence Surfactant Systems: Their Chemistry, Biology and Pharmacy 1983 Chapman and Hall London
76. H. Gao, W. Shi, and L.B. Freund Mechanics of receptor-mediated endocytosis Proc. Natl. Acad. Sci. U. S. A. 102 2005 9469 9479
77. P. Decuzzi, and M. Ferrari The role of specific and non-specific interactions in receptor mediated endocytosis Biomaterials 28 2007 2915 2923
78. S. Tenzer, D. Docter, S. Rosfa, A. Wlodarski, J. Kuharev, A. Rekik, S.K. Knauer, C. Bantz, T. Nawroth, C. Bier, J. Sirirahanapan, W. Mann, L. Treuel, R. Zellner, M. Maskos, H. Schield, and R.H. Staube Nanoparticle size is a critical physicochemical determinant of the human blood plasma corona: a comprehensive quantitative proteomic analysis ACS Nano 5 2011 7155 7167
79. N. Hussain, B. Singh, T. Sakthivel, and A.T. Florence Formulation and stability of surface tethered DNA-gold-dendron nanoparticles Int. J. Pharm. 254 2003 27 31
80. B. Singh, and A.T. Florence Hydrophobic dendrimer-derived nanoparticles Int. J. Pharm. 298 2005 348 353
81. G.R. Wiese, and T.W. Healy Effect of particle size on colloid stability Trans. Faraday Soc. 66 1970 490 499
82. X.-R. Xia, N.A. Monteiro-Riviere, and J.E. Riviere An index for characterization of nanomaterials in biological systems Nat. Nanotechnol. 5 2010 671 675
83. Y.S. Sun, J.P. Landry, Y.Y. Fei, X.D. Zhu, J.T. Luo, X.B. Wang, and K.S. Lam Effect of fluorescently labeling protein probes on kinetics of protein-ligand reactions Langmuir 24 2008 13399 13405
84. A.T. Florence Nanoparticle flow: implications for drug delivery V.P. Torchilin, Nanoparticulates as Drug Carriers 2006 Imperial College Press London
85. E. Chambers, and S. Mitragotri Prolonged circulation of larger polymeric nanoparticles by non-covalent adsorption on erythrocytes J. Control. Release 100 2004 111 119
86. J.L. McWhirter, H. Noguchi, and G. Gomper Deformation and clustering of red blood cells in microcapillary flow Soft Matter 7 2011 10967 10977
87. B. Nasseri, and A.T. Florence Some properties of extruded non-ionic surfactant vesicles Int. J. Pharm. 254 2003 11 16
88. Z. Adamczyk Particle transfer and deposition from flowing colloid suspensions Colloids Surf. 35 1989 283 308
89. K. Papadopoulos, and C.-H. Kuo The van der Waals interaction between a colloid and its host pore Colloids Surf. 46 1990 115 125
90. H. Brenner, and L.J. Gaydos The constrained Brownian movement of spherical particles in cylindrical pores of comparable radius J. Colloid Interface Sci. 58 1997 312 356
91. D.M. Malone, and J.L. Anderson Hindered diffusion of particles through small pores Chem. Eng. Sci. 33 1978 1429 1438
92. V.R.S. Patil, C.J. Campbell, Y.H. Yun, S.M. Slack, and D.J. Goetz Particle diameter influences adhesion under flow Biophys. J. 80 2001 1733 1743
93. Y. Ding, and D. Wen Particle migration in a flow of nanoparticle suspensions Powder Technol. 149 2005 84 92
94. T.T. Goodman, J. Chen, K. Matveev, and S.H. Pun Spatio-temporal modeling of nanoparticle delivery to multicellular tumor spheroids Biotechnol. Bioeng. 101 2008 388 396
95. J.M. Cook, A.T. Florence, J. Russel, and T. Wheldon Etoposide (VP-16) uptake by tumour spheroids and activity in the presence of Brij 30, formulation additives and sodium salicylate Eur. J. Cancer Res. 23 1989 311 318
96. D. Wirtz, K. Konstantopoulos, and P.C. Searson The physics of cancer: the role of physical interactions and mechanical forces in metastases Nat. Rev. Cancer 11 2011 512 522
97. S.C. James, and C.V. Chrysikopoulos Dense colloid transport in a bifurcating fracture J. Colloid Interface Sci. 270 2004 250 254
98. D.E. Goertz, J.L. Yu, R.S. Kerbel, P.N. Burns, and F.S. Foster High frequency 3-D color-flow imaging of the microcirculation Ultrasound Med. Biol. 29 2003 39 51
99. T. Hara, S. Iriyama, K. Makino, H. Terada, and M. Ohya Mathematical description of drug movement into tumor with EPR effect and estimation of its configuration for DDS Colloids Surf. B 75 2010 42 46
100. V. Trappe, L. Cipelletti, P.N. Segre, and D.A. Weitz Jamming phase diagram for attractive particles Nature 411 2001 772 775
101. K. Stratford, R. Adhikari, I. Pagonabarraga, J.-C. Despiat, and M.E. Cates Colloidal jamming at interfaces: a route to fluid-discontinuous gels Science 309 2005 2198 2201
102. N. Roussel, Th.L.H. Nguyen, and P. Cousset General probabilistic approach to the filtration process Phys. Rev. Lett. 98 2007 114502
103. B. Herzhaft, É. Guazzailli, M.B. Mackaplow, and E.S.G. Shaqfeh Experimental investigation of the sedimentaion of dilute fiber suspension Phys. Rev. Lett. 77 1996 290 293
104. D.N.T. Chen, K. Chen, L.A. Hough, M.F. Islam, and A.G. Yodh Rheology of carbon nanotube networks during gelation Macromolecules 43 2010 2048 2053
105. E.K. Hobbie, and D.J. Fry Rheology of concentrated carbon nanotube suspensions J. Chem. Phys. 126 2007 124907
106. S.J. Chapman, R.J. Shipley, and R. Jawad Multiscale modeling of fluid transport in tumors Bull. Math. Biol. 70 2008 2334 2357
107. A. Zilman, J. Pearson, and G. Bel Effects of jamming on transport times in nanochannels Phys. Rev. Lett. 103 2009 128103
108. G.H. Goldsztein Volume of suspension that flows through a small orifice before it closes SIAM J. Appl. Math. 66 2005 228 238
109. F. Yuen, M. Dellian, D. Fukumura, M. Leunig, D.A. Berk, V.P. Torchilin, and R.K. Jain Vascular permeability in a human tumour xenograft: molecular size dependence and cut-off size Cancer Res. 55 1995 3752 3756
110. H. Cabral, Y. Matsumoto, K. Mizuno, Q. Chen, M. Murakami, M. Kumara, Y. Terada, M.R. Kano, K. Miyazono, N. 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
111. P.A. Netti, L.T. Baxter, Y. Boucher, and R.K. Jain Time dependent behaviour of interstitial fluid pressure in solid tumors: implications for drug delivery Cancer Res. 55 1995 5451 5458
112. P. Dechadilok, and W.M. Deen Hindrance factors for diffusion and convection in pores Ind. Eng. Chem. Res. 45 2006 6953 6959
113. K.B. Neaves, A.J. Sawyer, C.P. Foley, W.M. Saltzman, and W.L. Olbricht Dilation and degradation of the brain extracellular matrix enhances penetration of infused nanoparticles Brain Res. 1180 2007 121 132
114. D.W. Bartlett, H. Su, I.J. Hildebrandt, W.A. Weber, and M.E. Davis Impact of tumor-specific targeting on the biodistribution of siRNA nanoparticles as measured by multimodality in vivo imaging Proc. Natl. Acad. Sci. U. S. A. 104 2007 15549 15554
115. D.B. Kirpotin, D.C. Drummond, Y. Shao, N.F. Shalaby, K. Hong, V.B. Nielsen, J.D. Marks, C.C. Benz, and J.W. Park Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models Cancer Res. 66 2006 6732 6740
116. K.F. Pirollo, and E.H. Chan Does a targeting ligand influence nanoparticle tumor localization or uptake? Trends Biotechnol. 26 2008 552 558
117. Y. Yoshizawa, Y. Kono, K. Ogawara, T. Kimura, and K. Higaki PEG liposomalization improved its in vivo and anti-tumor efficacy Int. J. Pharm. 412 2011 132 141
118. M. Wang, and M. Thanou Targeting nanoparticles to cancer Pharmacol. Res. 62 2010 90 99
119. D.Y. Afrifin, L.Y. Lee, and C.-H. Wang Mathematical modeling and simulation of drug release from microspheres: implications in drug delivery Adv. Drug Deliv. Rev. 58 2006 1274 1325
120. J. Siepmann, and F. Siepmann Mathematical modeling of drug delivery Int. J. Pharm. 364 2008 328 342
121. C. Washington Drug release from microdisperse systems: a critical review Int. J. Pharm. 58 1990 1 12
122. J. Siepmann, F. Siepmann, and A.T. Florence Local controlled drug delivery to the brain. Mathematical modeling of the underlying mass transport mechanisms Int. J. Pharm. 314 2006 101 119
123. J.E. Visvader Cells of origin in cancer Nature 469 2011 314 322
124. H.A. Bayele, T. Sakthivel, M. O'Donell, K.J. Pasi, A.F. Wilderspin, C.A. lee, I. Toth, and A.T. Florence Versatile peptide dendrimers for nucleic acid delivery J. Pharm. Sci. 94 2005 446 457
125. J.A. Kim, C. Åberg, A. Salvati, and K.A. Dawson Role of cell cycle on the cellular uptake and dilution of nanoparticles in a cell population Nat. Nanotechnol. 7 2012 62 68
126. F. Wickson Narratives of nature and nanotechnology Nat. Nanotechnol. 3 2008 313 315
127. M. Ferrari Beyond drug delivery Nat. Nanotechnol. 3 2008 131 132
128. K.T. Al-Jamal, W.T. Al-Jamal, K. Kostarelos, J.A. Turton, and A.T. Florence Anti-angiogenic poly-L-lysine dendrimer binds heparin and neutralizes its activity Results Pharma Sci. 2 2012 9 15
129. M. Ferrari Experimental therapies: vectoring siRNA therapeutics into the clinic Nat. Rev. Clin. Oncol. 7 2010 485 486
130. A. Schroeder, D.A. Heller, M.M. Winslow, J.E. Dahlmann, G.W. Pratt, R.A. Langer, T. Jacks, and D.C. Anderson Treating metastatic cancer with nanotechnology Nat. Rev. Cancer 12 2012 39 50
131. E.K. Chow, X.-Q. Xhang, M. Cheng, R. Lam, C. Robinson, H. Huang, D. Schaffer, E. Osawa, A. Goga, and B. Ho Nanodiamond therapeutic delivery agents mediate enhanced chemoresistant tumor treatment Sci. Trans. Med. 3 2011 73ra21
132. X. Li, J. Shao, Y. Qin, C. Shao, T. Zheng, and L. Ye TAT-conjugated nanodiamond for the enhanced delivery of doxorubicin J. Mater. Chem. 21 2011 7966 7973