Testing nanoparticles for angiogenesis-related disease: Charting the fastest route to the clinic

Journal of Biomedical Nanotechnology

Volumn 10, Issue 9, 2014, Pages 1641-1676

  Sarsons, Christopher D ^a   Tekrony, Amy ^a   Yaehne, Kristin ^a   Childs, Sarah ^b   Rinker, Kristina D ^a   Cramb, David ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Chicken embryo chorioallantoic membrane; Drug delivery; Flow chamber; Microfluidics; Microvasculature; Nanocarriers; Protein corona; Tumor microenvironment and models; Zebrafish embryos

Indexed keywords

DRUG DELIVERY; DRUG INTERACTIONS; ENZYME INHIBITION; MAMMALS; MICROFLUIDICS; NANOPARTICLES; TUMORS;

CHORIO-ALLANTOIC MEMBRANES; FLOW CHAMBERS; MICRO-VASCULATURE; NANO-CARRIERS; PROTEIN CORONAS; TUMOR MICROENVIRONMENT; ZEBRAFISH EMBRYOS;

DIAGNOSIS;

NANOCARRIER; NANOPARTICLE;

ANGIOGENESIS; BLOOD CELL; CHICK EMBRYO; CHORIOALLANTOIS; CONTROLLED DRUG RELEASE; CULTURE MEDIUM; DRUG DELIVERY SYSTEM; DRUG RELEASE; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; ENVIRONMENT; EXTRACELLULAR MATRIX; FLUID FLOW; GENETIC CONSERVATION; HIGH THROUGHPUT SCREENING; HUMAN; IMMUNE SYSTEM; INFLAMMATION; MICROFLUIDICS; MUSCLE CELL; NANOTOXICOLOGY; NONHUMAN; PERICYTE; REVIEW; TISSUE DISTRIBUTION; TUMOR MICROENVIRONMENT; ZEBRA FISH; ANIMAL; BIOASSAY; CHEMISTRY; FLOW KINETICS; NEOVASCULARIZATION, PATHOLOGIC; TRANSLATIONAL RESEARCH; VASCULARIZATION;

ANIMALS; BIOLOGICAL ASSAY; CHORIOALLANTOIC MEMBRANE; HUMANS; NANOPARTICLES; NEOVASCULARIZATION, PATHOLOGIC; RHEOLOGY; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84904879060     PISSN: 15507033     EISSN: 15507041     Source Type: Journal    
DOI: 10.1166/jbn.2014.1931     Document Type: Review

References (372)

1. E. Blanco, A. Hsiao, A. Mann, M. Landry, F. Meric-Bernstam, and M. Ferrari, Nanomedicine in cancer therapy: Innovative trends and prospects. Cancer Sci. 102, 1247 (2011).
2. C. Buzea, Pacheco, II, and K. Robbie, Nanomaterials and nanoparticles: Sources and toxicity. Biointerphases 2, MR17 (2007).
3. Z. Chen, Small-molecule delivery by nanoparticles for anticancer therapy. Trends Mol. Med. 16, 594 (2010).
4. Y. W. Cho, Y. S. Kim, I. S. Yjm, R. W. Park, S. J. Oh, D. H. Moon, S. Y. Kim, and I. C. Kwon, Tumoral accumulation of long-circulating, Copyright: American self-assembled nanoparticles and its visualization by gamma scintigraphy. Macomol Res. 16, 15 (2008).
5. Y. Matsumura and H. Maeda, A new concept for macromolecular therapeutics in cancer chemotherapy: Mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res. 46, 6387 (1986).
6. K. Jain, Advances in the field of nanooncology. BMC Med. 8, 83 (2010).
7. R. K. Jain and T. Stylianopoulos, Delivering nanomedicine to solid tumors. Nat. Rev. Clin. Oncol. 7, 653 (2010).
8. B. Y. S. Kim, J. T. Rutka, and W. C. W. Chan, Current concepts: Nanomedicine. N. Engl. J. Med. 363, 2434 (2010).
9. S. Krasnici, A. Werner, M. E. Eichhorn, M. Schmitt-Sody, S. A. Pahernik, B. Sauer, B. Schulze, M. Teifel, U. Michaelis, K. Naujoks, and M. Dellian, Effect of the surface charge of liposomes on their uptake by angiogenic tumor vessels. Int. J. Cancer. 105, 561 (2003).
10. B. A. Barut and L. I. Zon, Realizing the potential of zebrafish as a model for human disease. Physiol. Genomics. 2, 49 (2000).
11. K. Howe, M. D. Clark, C. F. Torroja, J. Torrance, C. Berthelot, M. Muffato, J. E. Collins, S. Humphray, K. McLaren, L. Matthews, S. McLaren, I. Sealy, M. Caccamo, C. Churcher, C. Scott, J. C. Barrett, R. Koch, G.-J. Rauch, S. White, W. Chow, B. Kilian, L. T. Quintais, J. A. Guerra-Assuncao, Y. Zhou, Y. Gu, J. Yen, J.-H. Vogel, T. Eyre, S. Redmond, R. Banerjee, J. Chi, B. Fu, E. Langley, S. F. Maguire, G. K. Laird, D. Lloyd, E. Kenyon, S. Donaldson, H. Sehra, J. Almeida-King, J. Loveland, S. Trevanion, M. Jones, M. Quail, D. Willey, A. Hunt, J. Burton, S. Sims, K. McLay, B. Plumb, J. Davis, C. Clee, K. Oliver, R. Clark, C. Riddle, D. Eliott, G. Threadgold, G. Harden, D. Ware, B. Mortimer, G. Kerry, P. Heath, B. Phillimore, A. Tracey, N. Corby, M. Dunn, C. Johnson, J. Wood, S. Clark, S. Pelan, G. Griffiths, M. Smith, R. Glithero, P. Howden, N. Barker, C. Stevens, J. Harley, K. Holt, G. Panagiotidis, J. Lovell, H. Beasley, C. Henderson, D. Gordon, K. Auger, D. Wright, J. Collins, C. Raisen, L. Dyer, K. Leung, L. Robertson, K. Ambridge, D. Leongamornlert, S. McGuire, R. Gilderthorp, C. Griffiths, D. Manthravadi, S. Nichol, G. Barker, S. Whitehead, M. Kay, J. Brown, C. Murnane, E. Gray, M. Humphries, N. Sycamore, D. Barker, D. Saunders, J. Wallis, A. Babbage, S. Hammond, M. Mashreghi-Mohammadi, L. Barr, S. Martin, P. Wray, A. Ellington, N. Matthews, M. Ellwood, R. Woodmansey, G. Clark, J. Cooper, A. Tromans, D. Grafham, C. Skuce, R. Pandian, R. Andrews, E. Harrison, A. Kimberley, J. Garnett, N. Fosker, R. Hall, P. Garner, D. Kelly, C. Bird, S. Palmer, I. Gehring, A. Berger, C. M. Dooley, Z. Ersan-Ueruen, C. Eser, H. Geiger, M. Geisler, L. Karotki, A. Kirn, J. Konantz, M. Konantz, M. Oberlaender, S. Rudolph-Geiger, M. Teucke, K. Osoegawa, B. Zhu, A. Rapp, S. Widaa, C. Langford, F. Yang, N. P. Carter, J. Harrow, Z. Ning, J. Herrero, S. M. J. Searle, A. Enright, R. Geisler, R. H. A. Plasterk, C. Lee, M. Westerfield, P. J. de Jong, L. I. Zon, J. H. Postlethwait, C. Nuesslein-Volhard, T. J. P. Hubbard, H. R. Crollius, J. Rogers, and D. L. Stemple, The zebrafish reference genome sequence and its relationship to the human genome. Nature 496, 498 (2013).
12. J. Sprague, L. Bayraktaroglu, Y. Bradford, T. Conlin, N. Dunn, D. Fashena, K. Frazer, M. Haendel, D. G. Howe, J. Knight, P. Mani, S. A. T. Moxon, C. Pich, S. Ramachandran, K. Schaper, E. Segerdell, X. Shao, A. Singer, P. Song, B. Sprunger, C. E. Van Slyke, and M. Westerfield, The zebrafish information network: The zebrafish model organism database provides expanded support for genotypes and phenotypes. Nucleic Acids Res. 36, D768 (2008).
13. M. Mimeault and S. K. Batra, Emergence of zebrafish models in oncology for validating novel anticancer drug targets and nanomaterials. Drug Discov. Today. 18, 128 (2013).
14. C. Nusslein-Volhard and R. Dahm, Zebrafish, OUP, Oxford, UK (2002).
15. H. W. Detrich, M. Westerfield, L. I. Zon, and A. S. F. C. Biology, The Zebrafish: Biology, Academic Press, Waltham, Massachusetts, USA (1999).
16. G. Kari, U. Rodeck, and A. P. Dicker, Zebrafish: An emerging model system for human disease and drug discovery. Clin. Pharmacol. Ther. 82, 70 (2007).
17. S. Ali, D. L. Champagne, H. P. Spaink, and M. K. Richardson, Zebrafish embryos and larvae: A new generation of disease models and drug screens. Birth Defects Res. Part C-Embryo Today-Rev. 93, 115 (2011).
18. R. Dahm and R. Geisler, Learning from small fry: The zebrafish as a genetic model organism for aquaculture fish species. Mar. Biotechnol. 8, 329 (2006).
19. G. Streisinger, C. Walker, N. Dower, D. Knauber, and F. Singer, Production of clones of homozygous diploid zebra fish (brachydanio-rerio). Nature 291, 293 (1981).
20. C. Walker and G. Streisinger, Induction of mutations by gamma-rays in pre-gonial germ-cells of zebrafish embryos. Genetics 103, 125 (1983).
21. D. J. Grunwald and G. Streisinger, Induction of mutations in the zebrafish with ultraviolet-light. Genet. Res. 59, 93 (1992).
22. Danio rerio (ID 50) - Genome - NCBI [Internet]. National Centre for Biotechnology Information, U.S. National Library of Medicine, Bethesda, MD. Available from: http://www.ncbi.nlm.nih.gov/genome?term=danio%20rerio.
23. K. Kawakami, H. Takeda, N. Kawakami, M. Kobayashi, N. Matsuda, and M. Mishina, A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev. Cell. 7, 133 (2004).
24. H. E. Sabaawy, M. Azuma, L. J. Embree, H.-J. Tsai, M. F. Starost, and D. D. Hickstein, TEL-AML1 transgenic zebrafish model of precursor B cell acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. USA 103, 15166 (2006).
25. D. A. Kane, Cell cycles and development in the embryonic zebrafish. Method Cell Biol. 59, 11 (1999).
26. C. B. Kimmel, W. W. Ballard, S. R. Kimmel, B. Ullmann, and T. F. Schilling, Stages of embryonic-development of the zebrafish. Dev. Dyn. 203, 253 (1995).
27. K. J. Lee, P. D. Nallathamby, L. M. Browning, C. J. Osgood, and X.-H. N. Xu, In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos. Acs Nano 1, 133 (2007).
28. E. Ellertsdottir, A. Lenard, Y. Blum, A. Krudewig, L. Herwig, M. Affolter, and H.-G. Belting, Vascular morphogenesis in the zebrafish embryo. Dev. Biol. 341, 56 (2010).
29. K. R. Kidd and B. M. Weinstein, Fishing for novel angiogenic therapies. Br. J. Pharmacol. 140, 585 (2003).
30. N. D. Lawson and B. M. Weinstein, Arteries and veins: Making a difference with zebrafish. Nat. Rev. Genet. 3, 674 (2002).
31. N. D. Lawson and B. M. Weinstein, In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307 (2002).
32. C. Parng, W. L. Seng, C. Semino, and P. McGrath, Zebrafish: A preclinical model for drug screening. Assay Drug Dev. Technol. 1, 41 (2002).
33. S. Childs, J. N. Chen, D. M. Garrity, and M. C. Fishman, Patterning of angiogenesis in the zebrafish embryo. Development 129, 973 (2002).
34. J. Folkman, Opinion - Angiogenesis: An organizing principle for drug discovery? Nat. Rev. Drug Discov. 6, 273 (2007).
35. L. I. Zon and R. T. Peterson, In vivo drug discovery in the zebrafish. Nat. Rev. Drug Discov. 4, 35 (2005).
36. L. M. Cross, M. A. Cook, S. Lin, J. N. Chen, and A. L. Rubinstein, Rapid analysis of angiogenesis drugs in a live fluorescent zebrafish assay. Arterioscl Throm Vas. 23, 911 (2003).
37. R. Harfouche, S. Basu, S. Soni, D. M. Hentschel, R. A. Mashelkar, and S. Sengupta, Nanoparticle-mediated targeting of phosphatidylinositol-3-kinase signaling inhibits angiogenesis. Angiogenesis 12, 325 (2009).
38. F. Li, S. Zhang, Z. Wang, and H. Li, Genes of the adaptive immune system are expressed early in zebrafish larval development following lipopolysaccharide stimulation. Chin. J. Oceanol. Limnol. 29, 326 (2011).
39. S. H. Lam, H. L. Chua, Z. Gong, T. J. Lam, and Y. M. Sin, Development and maturation of the immune system in zebrafish, Danio rerio: A gene expression profiling, in situ hybridization and immunological study. Dev. Comp. Immunol. 28, 9 (2004).
40. S. Nicoli and M. Presta, The zebrafish/tumor xenograft angiogenesis assay. Nat. Protoc. 2, 2918 (2007).
41. J. S. Zhang, S. Bai, C. Tanase, H. Nagase, and M. P. Sarras, The expression of tissue inhibitor of metalloproteinase 2 (TIMP-2) is required for normal development of zebrafish embryos. Dev. Genes Evol. 213, 382 (2003).
42. W. X. Zhang, Nanoscale iron particles for environmental remediation: An overview. J. Nanopart. Res. 5, 323 (2003).
43. J. H. Postlethwait, I. G. Woods, P. Ngo-Hazelett, Y. L. Yan, P. D. Kelly, F. Chu, H. Huang, A. Hill-Force, and W. S. Talbot, Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res. 10, 1890 (2000).
44. S. H. Lam, Y. L. Wu, V. B. Vega, L. D. Miller, J. Spitsbergen, Y. Tong, H. Q. Zhan, K. R. Govindarajan, S. Lee, S. Mathavan, K. R. K. Murthy, D. R. Buhler, E. T. Liu, and Z. Y. Gong, Conservation of gene expression signatures between zebrafish and human liver tumors and tumor progression. Nat. Biotechnol. 24, 73 (2006).
45. J. F. Amatruda, J. L. Shepard, H. M. Stern, and L. I. Zon, Zebrafish as a cancer model system. Cancer Cell 1, 229 (2002).
46. U. Langheinrich, Zebrafish: A new model on the pharmaceutical catwalk. Bioessays 25, 904 (2003).
47. E. A. Murphy, D. J. Shields, K. Stoletov, E. Dneprovskaia, M. McElroy, J. I. Greenberg, J. Lindquist, L. M. Acevedo, S. Anand, B. K. Majeti, I. Tsigelny, A. Saldanha, B. Walsh, R. M. Hoffman, M. Bouvet, R. L. Klemke, P. K. Vogt, L. Arnold, W. Wrasidlo, and D. A. Cheresh, Disruption of angiogenesis and tumor growth with an orally active drug that stabilizes the inactive state of PDGFR beta/B-RAF. Proc. Natl. Acad. Sci. USA 107, 4299 (2010).
48. E. Pluskota, J. J. Dowling, N. Gordon, J. A. Golden, D. Szpak, X. Z. West, C. Nestor, Y.-Q. Ma, K. Bialkowska, T. Byzova, and E. F. Plow, The integrin coactivator Kindlin-2 plays a critical role in angiogenesis in mice and zebrafish. Blood 117, 4978 (2011).
49. D. J. Y. Hsieh and C. F. Liao, Zebrafish M-2 muscarinic acetylcholine receptor: Cloning, pharmacological characterization, expression patterns and roles in embryonic bradycardia. Br. J. Pharmacol. 137, 782 (2002).
50. T. P. Barros, W. K. Alderton, H. M. Reynolds, A. G. Roach, and S. Berghmans, Zebrafish: An emerging technology for in vivo pharmacological assessment to identify potential safety liabilities in early drug discovery. Br. J. Pharmacol. 154, 1400 (2008).
51. V. E. Fako and D. Y. Furgeson, Zebrafish as a correlative and predictive model for assessing biomaterial nanotoxicity. Adv. Drug Del. Rev. 61, 478 (2009).
52. S. Harper, C. Usenko, J. E. Hutchison, B. L. S. Maddux, and R. L. Tanguay, In vivo biodistribution and toxicity depends on nanomaterial composition, size, surface functionalisation and route of exposure. J. Exp. Nanosci. 3, 195 (2008).
53. J. P. Bohnsack, S. Assemi, J. D. Miller, and D. Y. Furgeson, The primacy of physicochemical characterization of nanomaterials for reliable toxicity assessment: A review of the zebrafish nanotoxicology model. Method Mol. Cell Biol. 926, 261 (2012).
54. Y. Wang, J. L. Seebald, D. P. Szeto, and J. Irudayaraj, Biocompatibility and biodistribution of surface-enhanced raman scattering nanoprobes in zebrafish embryos: In vivo and multiplex imaging. Acs Nano 4, 4039 (2010).
55. B. M. Weinstein, D. L. Stemple, W. Driever, and M. C. Fishman, Gridlock, a localized heritable vascular patterning defect in the zebrafish. Nat. Med. 1, 1143 (1995).
56. P. V. Asharani, L. Yi, Z. Gong, and S. Valiyaveettil, Comparison of the toxicity of silver, gold and platinum nanoparticles in developing zebrafish embryos. Nanotoxicology 5, 43 (2011).
57. P. V. Asharani, Y. L. Wu, Z. Gong, and S. Valiyaveettil, Toxicity of silver nanoparticles in zebrafish models. Nanotechnology 19, 255102 (2008).
58. L. M. Browning, K. J. Lee, T. Huang, P. D. Nallathamby, J. E. Lowman, and X.-H. N. Xu, Random walk of single gold nanoparticles in zebrafish embryos leading to stochastic toxic effects on embryonic developments. Nanoscale 1, 138 (2009).
59. P. D. Nallathamby, K. J. Lee, and X.-H. N. Xu, Design of stable and uniform single nanoparticle photonics for in vivo dynamics Imaging of nanoenvironments of zebrafish embryonic fluids. Acs Nano 2, 1371 (2008).
60. T. C. K. Heiden, E. Dengler, W. J. Kao, W. Heideman, and R. E. Peterson, Developmental toxicity of low generation PAMAM dendrimers in zebrafish. Toxicol. Appl. Pharmacol. 225, 70 (2007).
61. J. P. Cheng, E. Flahaut, and S. H. Cheng, Effect of carbon nanotubes on developing zebrafish (Danio rerio) embryos. Environ. Toxicol. Chem. 26, 708 (2007).
62. J. Cheng, Y.-J. Gu, Y. Wang, S. H. Cheng, and W.-T. Wong, Nanotherapeutics in angiogenesis: Synthesis and in vivo assessment of drug efficacy and biocompatibility in zebrafish embryos. Int. J. Nanomed. 6, 2007 (2011).
63. C. Gong, S. Deng, Q. Wu, M. Xiang, X. Wei, L. Li, X. Gao, B. Wang, L. Sun, Y. Chen, Y. Li, L. Liu, Z. Qian, and Y. Wei, Improving antiangiogenesis and anti-tumor activity of curcumin by biodegradable polymeric micelles. Biomaterials 34, 1413 (2013).
64. K. Men, W. Liu, L. Li, X. Duan, P. Wang, M. Gou, X. Wei, X. Gao, B. Wang, Y. Du, M. Huang, L. Chen, Z. Qian, and Y. Wei, Delivering instilled hydrophobic drug to the bladder by a cationic nanoparticle and thermo-sensitive hydrogel composite system. Nanoscale 4, 6425 (2012).
65. K. Peng, I. Tomatsu, and A. Kros, Cyclodextrin/dextran based drug carriers for a controlled release of hydrophobic drugs in zebrafish embryos. Abstr. Pap. Am. Chem. S 6, 3778 (2010).
66. F. Sharif, F. Porta, A. H. Meijer, A. Kros, and M. K. Richardson, Mesoporous silica nanoparticles as a compound delivery system in zebrafish embryos. Int. J. Nanomed. 7, 1875 (2012).
67. H. Yan, C. Teh, S. Sreejith, L. Zhu, A. Kwok, W. Fang, X. Ma, N. Kim Truc, V. Korzh, and Y. Zhao, Functional mesoporous silica nanoparticles for photothermal-controlled drug delivery in vivo. Angew Chem. Int. Edit. 51, 8373 (2012).
68. J. Cheng, C. M. Chan, L. M. Veca, W. L. Poon, P. K. Chan, L. Qu, Y.-P. Sun, and S. H. Cheng, Acute and long-term effects after single loading of functionalized multi-walled carbon nanotubes into zebrafish (Danio rerio). Toxicol. Appl. Pharmacol. 235, 216 (2009).
69. H. Feitsma and E. Cuppen, Zebrafish as a cancer model. Mol. Cancer Res. 6, 685 (2008).
70. D. M. Langenau, M. D. Keefe, N. Y. Storer, J. R. Guyon, J. L. Kutok, X. Le, W. Goessling, D. S. Neuberg, L. M. Kunkel, and L. I. Zon, Effects of RAS on the genesis of embryonal rhabdomyosarcoma. Genes Dev. 21, 1382 (2007).
71. M. Gou, K. Men, H. Shi, M. Xiang, J. Zhang, J. Song, J. Long, Y. Wan, F. Luo, X. Zhao, and Z. Qian, Curcumin-loaded biodegradable polymeric micelles for colon cancer therapy in vitro and in vivo. Nanoscale 3, 1558 (2011).
72. S. W. Park, J. M. Davison, J. Rhee, R. H. Hruban, A. Maitra, and S. D. Leach, Oncogenic KRAS induces progenitor cell expansion and malignant transformation in zebrafish exocrine pancreas. Gastroenterology 134, 2080 (2008).
73. D. S. Wagner, N. A. Delk, E. Y. Lukianova-Hleb, J. H. Hafner, M. C. Farach-Carson, and D. O. Lapotko, The in vivo performance of plasmonic nanobubbles as cell theranostic agents in zebrafish hosting prostate cancer xenografts. Biomaterials 31, 7567 (2010).
74. X.-J. Yang, G.-L. Chen, S.-C. Yu, C. Xu, Y.-H. Xin, T.-T. Li, Y. Shi, A. Gu, J.-J. Duan, C. Qian, Y.-H. Cui, X. Zhang, and X.-W. Bian, TGF-beta 1 enhances tumor-induced angiogenesis via JNK pathway and macrophage infiltration in an improved zebrafish embryo/xenograft glioma model. International Immunopharmacology 15, 191 (2013).
75. S. Rieger, R. P. Kulkarni, D. Darcy, S. E. Fraser, and R. W. Koster, Quantum dots are powerful multipurpose vital labeling agents in zebrafish embryos. Dev. Dyn. 234, 670 (2005).
76. K. Yaehne, A. Tekrony, A. Clancy, Y. Gregoriou, J. Walker, K. Dean, T. Nguyen, A. Doiron, K. Rinker, X. Jiang, S. Childs, and D. Cramb, Nanoparticle accumulation in angiogenic tissues: Towards predictable pharmacokinetics. Small 9, 3118 (2013).
77. S. Y. Lee, M. Ferrari, and P. Decuzzi, Shaping nano-/micro-particles for enhanced vascular interaction in laminar flows. Nanotechnology 20, 495101 (2009).
78. S. M. Nelson, T. Mahmoud, M. Beaux, II, P. Shapiro, D. N. McIlroy, and D. L. Stenkamp, Toxic and teratogenic silica nanowires in developing vertebrate embryos. Nanomed-Nanotechnol. 6, 93 (2010).
79. D. R. Love, F. B. Pichler, A. Dodd, B. R. Copp, and D. R. Greenwood, Technology for high-throughput screens: The present and future using zebrafish. Curr. Opin. Biotechnol. 15, 564 (2004).
80. N. Anh Tuan, A. Emelyanov, C. H. V. Koh, J. M. Spitsbergen, S. Parinov, and Z. Gong, An inducible kras(V12) transgenic zebrafish model for liver tumorigenesis and chemical drug screening. Disease Models and Mechanisms 5, 63 (2012).
81. S. Arora, J. M. Rajwade, and K. M. Paknikar, Nanotoxicology and in vitro studies: The need of the hour. Toxicol. Appl. Pharmacol. 258, 151 (2012).
82. S. George, T. Xia, R. Rallo, Y. Zhao, Z. Ji, S. Lin, X. Wang, H. Zhang, B. France, D. Schoenfeld, R. Damoiseaux, R. Liu, S. Lin, K. A. Bradley, Y. Cohen, and A. E. Nal, Use of a high-throughput screening approach coupled with in vivo zebrafish embryo screening to develop hazard ranking for engineered nanomaterials. Acs Nano 5, 1805 (2011).
83. K.-T. Kim and R. L. Tanguay, Integrating zebrafish toxicology and nanoscience for safer product development. Green Chemistry 15, 872 (2013).
84. J. Akagi, F. Zhu, C. J. Hall, K. Khoshmanesh, K. Kalantar-Zadeh, A. Mitchell, K. E. Crosier, P. S. Crosier, and D. Wlodkowic, Dynamic analysis of angiogenesis in transgenic zebrafish embryos using a 3D multilayer chip-based technology, Microfluidics, Biomems, and Medical Microsystems Xi, edited by H. Becker and B. L. Gray (2013), Vol. 8615, p. 86151B.
85. S. Lin, Y. Zhao, A. E. Nel, and S. Lin, Zebrafish: An in vivo model for nano EHS studies. Small 9, 1608 (2013).
86. H. P. Spaink, C. Cui, M. I. Wiweger, H. J. Jansen, W. J. Veneman, R. Marin-Juez, J. de Sonneville, A. Ordas, V. Torraca, W. van der Ent, W. P. Leenders, A. H. Meijer, B. E. Snaar-Jagalska, and R. P. Dirks, Robotic injection of zebrafish embryos for high-throughput screening in disease models. Methods 62, 246 (2013).
87. W. H. Wang, X. Y. Liu, and Y. Sun, High-throughput automated injection of individual biological cells. Ieee Transactions on Automation Science and Engineering 6, 209 (2009).
88. A. Vogt, A. Cholewinski, X. Shen, S. G. Nelson, J. S. Lazo, M. Tsang, and N. A. Hukriede, Automated image-based phenotypic analysis in zebrafish embryos. Dev. Dyn. 238, 656 (2009).
89. H. M. Chen, C. S. Wang, M. J. Li, E. Sanchez, J. Li, A. Berenson, E. Wirtschafter, J. Wang, J. Shen, Z. W. Li, B. Bonavida, and J. R. Berenson, A novel angiogenesis model for screening antiangiogenic compounds: The chorioallantoic membrane/feather bud assay. Int. J. Oncol. 37, 71 (2010).
90. Y. J. Li, C. L. Duan, J. X. Liu, and Y. G. Xu, Pro-angiogenic actions of Salvianolic acids on in vitro cultured endothelial progenitor cells and chick embryo chorioallantoic membrane model. J. Ethnopharmacol. 131, 562 (2010).
91. E. I. Yurlova, K. A. Rubina, V. Y. Sysoeva, G. V. Sharonov, E. V. Semina, E. V. Parfenova, and V. A. Tkachuk, T-cadherin suppresses the cell proliferation of mouse melanoma B16F10 and tumor angiogenesis in the model of the chorioallantoic membrane. Russ. J. Dev. Biol. 41, 217 (2010).
92. A. M. Cimpean, D. Ribatti, and M. Raica, The chick embryo chorioallantoic membrane as a model to study tumor metastasis. Angiogenesis 11, 311 (2008).
93. M. Richardson, L. Y. Liu, L. Dunphy, D. Wong, Y. M. Sun, K. Viswanathan, G. Singh, and A. Lucas, Viral serpin, Serp-1, inhibits endogenous angiogenesis in the chicken chorioallantoic membrane model. Cardiovascular Pathology 16, 191 (2007).
94. A. C. Tufan, and N. L. Satiroglu-Tufan, The chick embryo chorioallantoic membrane as a model system for the study of tumor angiogenesis, invasion and development of anti-angiogenic agents. Current Cancer Drug Targets 5, 249 (2005).
95. C. D. Willey, T. M. Burleson, L. Zhai, and J. C. Anderson, The development of a chorioallantoic membrane-tumor xenograft model for tumor vascular targeting with radiation. International Journal of Radiation Oncology Biology Physics 78, S624 (2010).
96. Q. Tan, R. Steiner, M. Hilbe, S. Hillinger, W. Weder, and S. Lu, Tissue engineered tumor cultured on chick embryo chorioallantoic membrane (CAM): A new model of spontaneous metastasis. Journal of Thoracic Oncology 4, S639 (2009).
97. E. I. Deryugina, and J. P. Quigley, Chick embryo chorioallantoic membrane model systems to study and visualize human tumor cell metastasis. Histochem. Cell Biol. 130, 1119 (2008).
98. M. G. Gabrielli and D. Accili, The chick chorioallantoic membrane: A model of molecular, structural, and functional adaptation to transepithelial ion transport and barrier function during embryonic development. J. Biomed. Biotechnol. 2010, 940741 (2010).
99. D. Slodownik, I. Grinberg, R. M. Spira, Y. Skornik, and R. S. Goldstein, The human skin/chick chorioallantoic membrane model accurately predicts the potency of cosmetic allergens. Exp. Dermatol. 18, 409 (2009).
100. B. Martinez-Madrid, J. Donnez, A. S. Van Eyck, A. Veiga-Lopez, M. M. Dolmans, and A. Van Langendonckt, Chick embryo chorioallantoic membrane (CAM) model: A useful tool to study short-term transplantation of cryopreserved human ovarian tissue. Fertil. Steril. 91, 285 (2009).
101. A. Nap, P. G. Groothuis, C. Punyadeera, L. K. Hitpass, R. Kamps, B. Delvoux, and G. A. J. Dunselman, Contraceptives prevent the development of endometriosis in the chicken chorioallantoic membrane model. Hum. Reprod. 22, O117 (2007).
102. A. W. Nap, P. G. Groothuis, C. Punyadeera, L. Klein-Hitpass, R. Kamps, B. Delvoux, and G. A. J. Dunselman, Oral contraceptives prevent the development of endometriosis in the chicken chorioallantoic membrane model. Contraception 78, 257 (2008).
103. E. Larger, M. Marre, P. Corvol, and J. M. Gasc, Hyperglycemia-induced defects in angiogenesis in the chicken chorioallantoic membrane model. Diabetes 53, 752 (2004).
104. W. W. L. Chin, P. W. S. Heng, P. L. Lim, W. K. O. Lau, and M. Olivo, Membrane transport enhancement of chlorin e6-polyvinylpyrrolidone and its photodynamic efficacy on the chick chorioallantoic model. J. Biophotonics 1, 395 (2008).
105. A. L. Romanoff, The Avian Embryo, The Macmillan Company, New York, NY (1960).
106. H. Gupta, S. Jain, R. Mathur, P. Mishra, A. K. Mishra, and T. Velpandian, Sustained ocular drug delivery from a temperature and pH triggered novel in situ gel system. Drug Deliv. 14, 507 (2007).
107. C. L. L. Saw, P. W. S. Heng, W. W. L. Chin, K. C. Soo, and M. Olivo, Enhanced photodynamic activity of hypericin by penetration enhancer N -methyl pyrrolidone formulations in the chick chorioallantoic membrane model. Cancer Letters 238, 104 (2006).
108. K. S. Samkoe and D. T. Cramb, Application of an ex ovo chicken chorioallantoic membrane model for two-photon excitation photodynamic therapy of age-related macular degeneration. Journal of Biomedical Optics 8, 410 (2003).
109. K. S. Samkoe, A. A. Clancy, A. Karotki, B. C. Wilson, and D. T. Cramb, Complete blood vessel occlusion in the chick chorioallantoic membrane using two-photon excitation photodynamic therapy: Implications for treatment of wet age-related macular degeneration. Journal of Biomedical Optics 12, 034025 (2007).
110. C. L. L. Saw, P. W. S. Heng, and C. V. Liew, Chick chorioallantoic membrane as an in situ biological membrane for pharmaceutical formulation development: A review. Drug Dev. Ind. Pharm. 34, 1168 (2008).
111. C. Staton, M. Reed, and N. Brown, A critical analysis of current in vitro and in vivo angiogenesis assays. Int. J. Exp. Pathol. 90, 195 (2009).
112. J. R. Coleman and A. R. Terepka, Fine-structural changes associated with onset of calcium, sodium and water transport by chick chorioallantoic membrane. J. Membr. Biol. 7, 111 (1972).
113. S. Miller, K. Bresee, C. Michaelson, and D. Tyrell, Domains of differential cell proliferation and formation of amnion folds in chick embryo ectoderm. The Anatomical Record 238, 225 (1994).
114. V. Maksimov, I. Korostyshevskaya, and S. Kurganov, Functional morphology of chorioallantoic vascular network in chicken. Bull. Exp. Biol. Med. 142, 367 (2006).
115. P. Schlatter, M. F. Konig, L. M. Karlsson, and P. H. Burri, Quantitative study of intussusceptive capillary growth in the chorioallantoic membrane (CAM) of the chicken embryo. Microvasc. Res. 54, 65 (1997).
116. A. R. Terepka, M. E. Stewart, and N. Merkel, Transport functions of chick chorio-allantoic membrane .2. Active calcium transport, in vitro. Exp. Cell Res. 58, 107 (1969).
117. V. Rizzo, D. Kim, W. N. Duran, and D. O. Defouw, Ontogeny of Microvascular permeability to macromolecules in the chick chorioallantoic membrane during normal angiogenesis. Microvasc. Res. 49, 49 (1995).
118. M. Richardson and G. Singh, Observations on the use of the avian chorioallantoic membrane (CAM) model in investigations into angiogenesis. Curr. Drug Targets: Cardiovasc. Hematol. Disord. 3, 155 (2003).
119. D. S. Dohle, S. D. Pasa, S. Gustmann, M. Laub, J. H. Wissler, H. P. Jennissen, and N. Dunker, Chick ex ovo culture and ex ovo CAM assay: How it really works. J. Vis. Exp. (33), e1620, doi:10.3791/1620 (2009).
120. D. Ribatti, Chick embryo chorioallantoic membrane as a useful tool to study angiogenesis. Int. Rev. Cell. Mol. Bio. 270, 181 (2008).
121. J. Murphy, Transplantability of tissues to the embryo of foreign species: Its bearing on questions of tissue specificity and tumor immunity. J Exp Med. 17, 482 (1913).
122. K. Norrby, In vivo models of angiogenesis. J. Cell. Mol. Med. 10, 588 (2006).
123. C. L. Saw, P. Heng, and C. Liew, Chick chorioallantoic membrane as an in situ biological membrane for pharmaceutical formulation development: A review. Drug Dev. Ind. Pharm. 34, 1168 (2008).
124. X. Liu, X. Wang, A. Horii, X. Wang, L. Qiao, S. Zhang, and F.-Z. Cui, In vivo studies on angiogenic activity of two designer self-assembling peptide scaffold hydrogels in the chicken embryo chorioallantoic membrane. Nanoscale 4, 2720 (2012).
125. Z. Popoviæ, W. Liu, V. Chauhan, J. Lee, C. Wong, A. Greytak, N. Insin, D. Nocera, D. Fukumura, R. Jain, and M. Bawendi, A nanoparticle size series for in vivo fluorescence imaging. Angewandte Chemie (International ed. in English) 49, 8649 (2010).
126. G. Aleem, A. N. Ojas, Y. Jianming, A. I. Michael, E. T. Jessica, and C. B.-D. Lora, N 2-Trimethylacetyl substituted and unsubstituted-N 4-phenylsubstituted-6-(2-pyridin-2-ylethyl)-7H-pyrrolo[2,3-d]pyrimidine-2, 4-diamines: Design, cellular receptor tyrosine kinase inhibitory activities and in vivo evaluation as antiangiogenic, antimetastatic and antitumor agents. Biorg. Med. Chem. 21, 1312 (2013).
127. M. Grodzik, E. Sawosz, M. Wierzbicki, P. Orlowski, A. Hotowy, T. Niemiec, M. Szmidt, K. Mitura, and A. Chwalibog, Nanoparticles of carbon allotropes inhibit glioblastoma multiforme angiogenesis in ovo. Int. J. Nanomed. 6, 3041 (2011).
128. E. Deryugina and J. Quigley, Chapter 2. Chick embryo chorioallantoic membrane models to quantify angiogenesis induced by inflammatory and tumor cells or purified effector molecules. Methods Enzymol. 444, 21 (2008).
129. L. Kirchner, S. Schmidt, and B. Gruber, Quantitation of angiogenesis in the chick chorioallantoic membrane model using fractal analysis. Microvasc. Res. 51, 2 (1996).
130. E. Ruoslahti, S. Bhatia, and M. Sailor, Targeting of drugs and nanoparticles to tumors. J. Cell Biol. 188, 759 (2010).
131. S. Sourabh, L. A. Amber, M. W. Amy, L. L. Karin, D. L. John, and F. S. Nicole, Increased Tumor Homing and Tissue Penetration of the Filamentous Plant Viral Nanoparticle Potato virus X. Mol. Pharm. 10, 33 (2013).
132. D. E. Mihaiescu, A. S. Buteica, J. Neamtu, D. Istrati, and I. Mindrila, Fe3O4/Salicylic acid nanoparticles behavior on chick CAM vasculature. J. Nanopart. Res. 15, 1857 (2013).
133. A. Vargas, B. Pegaz, E. Debefve, Y. Konan-Kouakou, N. Lange, J.-P. Ballini, H. van den Bergh, R. Gurny, and F. Delie, Improved photodynamic activity of porphyrin loaded into nanoparticles: An in vivo evaluation using chick embryos. Int. J. Pharm. 286, 131 (2004).
134. M. Zeisser-Labouebe, F. Delie, R. Gurny, and N. Lange, Screening of nanoparticulate delivery systems for the photodetection of cancer in a simple and cost-effective model. Nanomedicine 4, 135 (2009).
135. A. A. Clancy, Y. Gregoriou, K. Yaehne, and D. T. Cramb, Measuring properties of nanoparticles in embryonic blood vessels: Towards a physicochemical basis for nanotoxicity. Chem. Phys. Lett. 488, 99 (2010).
136. J. Smith, G. Fisher, A. Waggoner, and P. Campbell, The use of quantum dots for analysis of chick CAM vasculature. Microvasc. Res. 73, 75 (2007).
137. J. Lewis, G. Destito, A. Zijlstra, M. Gonzalez, J. Quigley, M. Manchester, and H. Stuhlmann, Viral nanoparticles as tools for intravital vascular imaging. Nat. Med. 12, 354 (2006).
138. 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. Controlled Release 95, 613 (2004).
139. M. R. Dreher, W. G. Liu, C. R. Michelich, M. W. Dewhirst, F. Yuan, and A. Chilkoti, Tumor vascular permeability, accumulation, and penetration of macromolecular drug carriers. J. Natl. Cancer Inst. 98, 335 (2006).
140. Z. Popoviæ, W. Liu, V. P. Chauhan, J. Lee, C. Wong, A. B. Greytak, N. Insin, D. G. Nocera, D. Fukumura, R. K. Jain, and M. G. Bawendi, A nanoparticle size series for in vivo fluorescence imaging. Angew. Chem. 122, 8831 (2010).
141. G. Alexandrakis, E. Brown, R. Tong, T. McKee, R. Campbell, Y. Boucher, and R. Jain, Two-photon fluorescence correlation microscopy reveals the two-phase nature of transport in tumors. Nat. Med. 10, 203 (2004).
142. 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, 3752 (1995).
143. C. Wong, T. Stylianopoulos, J. Cui, J. Martin, V. P. Chauhan, W. Jiang, Z. Popovic, R. K. Jain, M. G. Bawendi, and D. Fukumura, Multistage nanoparticle delivery system for deep penetration into tumor tissue. Proc. Natl. Acad. Sci. USA 108, 2426 (2011).
144. C. A. Dehelean, S. Feflea, D. Gheorgheosu, S. Ganta, A. M. Cimpean, D. Muntean, and M. M. Amiji, Anti-angiogenic and anti-cancer evaluation of betulin nanoemulsion in chicken chorioallantoic membrane and skin carcinoma in Balb/c mice. J. Biomed. Nanotechnol. 9, 577 (2013).
145. A. Vargas, M. Zeisser-Labouèbe, N. Lange, R. Gurny, and F. Delie, The chick embryo and its chorioallantoic membrane (CAM) for the in vivo evaluation of drug delivery systems. Adv. Drug Del. Rev. 59, 1162 (2007).
146. M. Rose and E. Orlans, Immunoglobulins in the egg, embryo and young chick. Dev. Comp. Immunol. 5, 15 (1981).
147. J. B. West, R. R. Watson, and Z. Fu, Major differences in the pulmonary circulation between birds and mammals. Resp. Physiol. Neurobi. 157, 382 (2007).
148. P. M. Valencia, O. C. Farokhzad, R. Karnik, and R. Langer, Microfluidic technologies for accelerating the clinical translation of nanoparticles. Nat. Nanotechnol. 7, 623 (2012).
149. A. Albanese, P. S. Tang, and W. C. Chan, The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu. Rev. Biomed. Eng. 14, 1 (2012).
150. A. E. Nel, L. Madler, D. Velegol, T. Xia, E. M. Hoek, P. Somasundaran, F. Klaessig, V. Castranova, and M. Thompson, Understanding biophysicochemical interactions at the nano-bio interface. Nat. Mater. 8, 543 (2009).
151. P. Rivera Gil, G. Oberdorster, A. Elder, V. Puntes, and W. J. Parak, Correlating physico-chemical with toxicological properties of nanoparticles: The present and the future. Acs Nano 4, 5527 (2010).
152. X. Mulet, D. F. Kennedy, C. E. Conn, A. Hawley, and C. J. Drummond, High throughput preparation and characterisation of amphiphilic nanostructured nanoparticulate drug delivery vehicles. Int. J. Pharm. 395, 290 (2010).
153. K. T. Nguyen, K. P. Shukla, M. Moctezuma, A. R. Braden, J. Zhou, Z. Hu, and L. Tang, Studies of the cellular uptake of hydrogel nanospheres and microspheres by phagocytes, vascular endothelial cells, and smooth muscle cells. Journal of biomedical Materials Research. Part A. 88, 1022 (2009).
154. L. K. Petersen, C. K. Sackett, and B. Narasimhan, High-throughput analysis of protein stability in polyanhydride nanoparticles. Acta Biomater. 6, 3873 (2010).
155. L. Balogh, S. S. Nigavekar, B. M. Nair, W. Lesniak, C. Zhang, L. Y. Sung, M. S. Kariapper, A. El-Jawahri, M. Llanes, B. Bolton, F. Mamou, W. Tan, A. Hutson, L. Minc, and M. K. Khan, Significant effect of size on the in vivo
156. I. Brigger, C. Dubernet, and P. Couvreur, Nanoparticles in cancer therapy and diagnosis. Adv. Drug Deliv. Rev. 54, 631 (2002).
157. K. R. Chaudhari, M. Ukawala, A. S. Manjappa, A. Kumar, P. K. Mundada, A. K. Mishra, R. Mathur, J. Monkkonen, and R. S. Murthy, Opsonization, biodistribution, cellular uptake and apoptosis study of PEGylated PBCA nanoparticle as potential drug delivery carrier. Pharm. Res. 29, 53 (2012).
158. M. J. Ernsting, W. L. Tang, N. W. MacCallum, and S. D. Li, Preclinical pharmacokinetic, biodistribution, and anti-cancer efficacy studies of a docetaxel-carboxymethylcellulose nanoparticle in mouse models. Biomaterials. 33, 1445 (2012).
159. S. Ganesh, A. K. Iyer, F. Gattacceca, D. V. Morrissey, and M. M. Amiji, In vivo biodistribution of siRNA and cisplatin administered using CD44-targeted hyaluronic acid nanoparticles. J. Control Release 172, 699 (2013).
160. S. A. Kulkarni and S. S. Feng, Effects of particle size and surface modification on cellular uptake and biodistribution of polymeric nanoparticles for drug delivery. Pharm. Res. 30, 2512 (2013).
161. J. W. Nichols and Y. H. Bae, Odyssey of a cancer nanoparticle: From injection site to site of action. Nano Today 7, 606 (2012).
162. Y. H. Bae and K. Park, Targeted drug delivery to tumors: Myths, reality and possibility. J Control Release 153, 198 (2011).
163. W. Jiang, B. Y. Kim, J. T. Rutka, and W. C. Chan, Nanoparticle-mediated cellular response is size-dependent. Nat Nanotechnol. 3, 145 (2008).
164. V. P. Chauhan, T. Stylianopoulos, J. D. Martin, Z. Popovic, O. Chen, W. S. Kamoun, M. G. Bawendi, D. Fukumura, and R. K. Jain, Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner. Nat. Nanotechnol. 7, 383 (2012).
165. S. P. Samuel, N. Jain, F. O'Dowd, T. Paul, D. Kashanin, V. A. Gerard, Y. K. Gun'ko, A. Prina-Mello, and Y. Volkov, Multifactorial determinants that govern nanoparticle uptake by human endothelial cells under flow. Int. J. Nanomedicine 7, 2943 (2012).
166. J. Davda and V. Labhasetwar, Characterization of nanoparticle uptake by endothelial cells. Int. J. Pharm. 233, 51 (2002).
167. 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, 212 (2003).
168. L. Zhang, H. Nishihara, and M. R. Kano, Pericyte-coverage of human tumor vasculature and nanoparticle permeability. Biol. Pharm. Bull. 35, 761 (2012).
169. P. Charoenphol, P. J. Onyskiw, M. Carrasco-Teja, and O. Eniola-Adefeso, Particle-cell dynamics in human blood flow: Implications for vascular-targeted drug delivery. J. Biomech. 45, 2822 (2012).
170. J. Tan, A. Thomas, and Y. Liu, Influence of red blood cells on nanoparticle targeted delivery in microcirculation. Soft Matter. 8, 1934 (2011).
171. A. Gojova, B. Guo, R. S. Kota, J. C. Rutledge, I. M. Kennedy, and A. I. Barakat, Induction of inflammation in vascular endothelial cells by metal oxide nanoparticles: Effect of particle composition. Environmental Health Perspectives 115, 403 (2007).
172. M. S. Lord, B. Tsoi, C. Gunawan, W. Y. Teoh, R. Amal, and J. M. Whitelock, Anti-angiogenic activity of heparin functionalised cerium oxide nanoparticles. Biomaterials 34, 8808 (2013).
173. S. M. Hartig, R. R. Greene, G. Carlesso, J. N. Higginbotham, W. N. Khan, A. Prokop, and J. M. Davidson, Kinetic analysis of nanoparticulate polyelectrolyte complex interactions with endothelial cells. Biomaterials 28, 3843 (2007).
174. A. Lin, A. Sabnis, S. Kona, S. Nattama, H. Patel, J.-F. Dong, and K. T. Nguyen, Shear-regulated uptake of nanoparticles by endothelial cells and development of endothelial-targeting nanoparticles. Journal of Biomedical Materials Research Part A 93A, 833 (2010).
175. S. T. Stern, P. P. Adiseshaiah, and R. M. Crist, Autophagy and lysosomal dysfunction as emerging mechanisms of nanomaterial toxicity. Particle and Fibre Toxicology 9, 20 (2012).
176. F. Y. Yang, M. X. Yu, Q. Zhou, W. L. Chen, P. Gao, and Z. Huang, Effects of iron oxide nanoparticle labeling on human endothelial cells. Cell Transplant. 21, 1805 (2012).
177. A. A. Shvedova, V. E. Kagan, and B. Fadeel, Close encounters of the small kind: Adverse effects of man-made materials interfacing with the nano-cosmos of biological systems. Annu. Rev. Pharmacol. Toxicol., Annual Reviews, Palo Alto 50, 63 (2010).
178. S. Das, S. Singh, J. M. Dowding, S. Oommen, A. Kumar, T. X. T. Sayle, S. Saraf, C. R. Patra, N. E. Vlahakis, D. C. Sayle, W. T. Self, and S. Seal, The induction of angiogenesis by cerium oxide nanoparticles through the modulation of oxygen in intracellular environments. Biomaterials 33, 7746 (2012).
179. G. Y. Ge, H. F. Wu, F. Xiong, Y. Zhang, Z. R. Guo, Z. P. Bian, J. D. Xu, C. R. Gu, N. Gu, X. J. Chen, and D. Yang, The cytotoxicity evaluation of magnetic iron oxide nanoparticles on human aortic endothelial cells. Nanoscale Res. Lett. 8, 10 (2013).
180. T. Xia, M. Kovochich, M. Liong, J. I. Zink, and A. E. Nel, Cationic polystyrene nanosphere toxicity depends on cell-specific endocytic and mitochondrial injury pathways. Acs Nano 2, 85 (2008).
181. J. M. Worle-Knirsch, K. Pulskamp, and H. F. Krug, Oops they did it again! Carbon nanotubes hoax scientists in viability assays. Nano Lett. 6, 1261 (2006).
182. S. M. Griffiths, N. Singh, G. J. S. Jenkins, P. M. Williams, A. W. Orbaek, A. R. Barron, C. J. Wright, and S. H. Doak, Dextran coated ultrafine superparamagnetic iron oxide nanoparticles: Compatibility with common fluorometric and colorimetric dyes. Anal. Chem. 83, 3778 (2011).
183. A. L. Holder, R. Goth-Goldstein, D. Lucas, and C. P. Koshland, Particle-induced artifacts in the mtt and ldh viability assays. Chem. Res. Toxicol. 25, 1885 (2012).
184. A. Kroll, M. H. Pillukat, D. Hahn, and J. Schnekenburger, Interference of engineered nanoparticles with in vitro toxicity assays. Arch. Toxicol. 86, 1123 (2012).
185. J. H. Li, X. R. Liu, Y. Zhang, F. F. Tian, G. Y. Zhao, Q. L. Y. Yu, F. L. Jiang, and Y. Liu, Toxicity of nano zinc oxide to mitochondria. Toxicol. Res. 1, 137 (2012).
186. C. H. Lin, L. W. Chang, Y. H. Wei, S. B. Wu, C. S. Yang, W. H. Chang, Y. C. Chen, and P. P. Lin, Electronic microscopy evidence for mitochondria as targets for Cd/Se/Te-based quantum dot 705 toxicity in vivo. Kaohsiung J. Med. Sci. 28, S53 (2012).
187. M. T. Zhu, B. Wang, Y. Wang, L. Yuan, H. J. Wang, M. Wang, H. Ouyang, Z. F. Chai, W. Y. Feng, and Y. L. Zhao, Endothelial dysfunction and inflammation induced by iron oxide nanoparticle exposure: Risk factors for early atherosclerosis. Toxicol. Lett. 203, 162 (2011).
188. M. T. Zhu, W. Yun, W. Y. Feng, W. Bing, W. Meng, O. Y. Hong, and Z. F. Chai, Oxidative stress and apoptosis induced by iron oxide nanoparticles in cultured human umbilical endothelial cells. J. Nanosci. Nanotechnol. 10, 8584 (2010).
189. P. L. Apopa, Y. Qian, R. Shao, N. L. Guo, D. Schwegler-Berry, M. Pacurari, D. Porter, X. L. Shi, V. Vallyathan, V. Castranova, and D. C. Flynn, Iron oxide nanoparticles induce human microvascular endothelial cell permeability through reactive oxygen species production and microtubule remodeling. Particle and Fibre Toxicology 6, 1 (2009).
190. J. Sun, S. C. Wang, D. Zhao, F. H. Hun, L. Weng, and H. Liu, Cytotoxicity, permeability, and inflammation of metal oxide nanoparticles in human cardiac microvascular endothelial cells cytotoxicity, permeability, and inflammation of metal oxide nanoparticles. Cell Biology and Toxicology 27, 333 (2011).
191. S. Nadanaciva and Y. Will, Investigating mitochondrial dysfunction to increase drug safety in the pharmaceutical industry. Curr. Drug Targets. 12, 774 (2011).
192. K. B. Wallace, Mitochondrial off targets of drug therapy. Trends Pharmacol. Sci. 29, 361 (2008).
193. S. Marrache and S. Dhar, Engineering of blended nanoparticle platform for delivery of mitochondria-acting therapeutics. Proceedings of the National Academy of Sciences of the United States of America 109, 16288 (2012).
194. D. B. Cochran, P. P. Wattamwar, R. Wydra, J. Z. Hilt, K. W. Anderson, R. E. Eitel, and T. D. Dziubla, Suppressing iron oxide nanoparticle toxicity by vascular targeted antioxidant polymer nanoparticles. Biomaterials 34, 9615 (2013).
195. R. Wiewrodt, A. P. Thomas, L. Cipelletti, M. Christofidou-Solomidou, D. A. Weitz, S. I. Feinstein, D. Schaffer, S. M. Albelda, M. Koval, and V. R. Muzykantov, Size-dependent intracellular immunotargeting of therapeutic cargoes into endothelial cells. Blood 99, 912 (2002).
196. E. Oesterling, N. Chopra, V. Gavalas, X. Arzuaga, E. J. Lim, R. Sultana, D. A. Butterfield, L. Bachas, and B. Hennig, Alumina nanoparticles induce expression of endothelial cell adhesion molecules. Toxicol. Lett. 178, 160 (2008).
197. N. Zhang, C. Chittasupho, C. Duangrat, T. J. Siahaan, and C. Berkland, PLGA nanoparticle-peptide conjugate effectively targets intercellular cell-adhesion molecule-1. Bioconjugate Chem. 19, 145 (2008).
198. J. Kusunose, M. K. J. Gagnon, J. W. Seo, and K. W. Ferrara, Quantitation of nanoparticle accumulation in flow using optimized microfluidic chambers. Journal of Drug Targeting 22, 48 (2014).
199. Q. Y. Hu, X. L. Gao, T. Kang, X. Y. Feng, D. Jiang, Y. F. Tu, Q. X. Song, L. Yao, X. G. Jiang, H. Z. Chen, and J. Chen, CGKRK-modified nanoparticles for dual-targeting drug delivery to tumor cells and angiogenic blood vessels. Biomaterials 34, 9496 (2013).
200. N. Ucciferri, E. M. Collnot, B. K. Gaiser, A. Tirella, V. Stone, C. Domenici, C. M. Lehr, and A. Ahluwalia, In vitro toxicological screening of nanoparticles on primary human endothelial cells and the role of flow in modulating cell response. Nanotoxicology 8, 697 (2014).
201. A. L. Doiron, B. Clark, and K. D. Rinker, Endothelial nanoparticle binding kinetics are matrix and size dependent. Biotechnol Bioeng. 108, 2988 (2011).
202. M. I. Hermanns, J. Kasper, P. Dubruel, C. Pohl, C. Uboldi, V. Vermeersch, S. Fuchs, R. E. Unger, and C. J. Kirkpatrick, An impaired alveolar-capillary barrier in vitro: Effect of proinflammatory cytokines and consequences on nanocarrier interaction. Journal of the Royal Society Interface 7, S41 (2010).
203. C. J. Edgell, C. C. McDonald, and J. B. Graham, Permanent cellline expressing human factor-VIII-related antigen established by hybridization. Proceedings of the National Academy of Sciences of the United States of America-Biological Sciences 80, 3734 (1983).
204. J. Bauer, M. Margolis, C. Schreiner, C. J. Edgell, J. Azizkhan, E. Lazarowski, and R. L. Juliano, Invitro model of angiogenesis using a human endothelium-derived permanent cell-linecontributions of induced gene-expression, G-proteins, and integrins. J. Cell. Physiol. 153, 437 (1992).
205. L. R. Farcal, C. Uboldi, D. Mehn, G. Giudetti, P. Nativo, J. Ponti, D. Gilliland, F. Rossi, and A. Bal-Price, Mechanisms of toxicity induced by SiO2 nanoparticles of in vitro human alveolar barrier: Effects on cytokine production, oxidative stress induction, surfactant proteins A mRNA expression and nanoparticles uptake. Nanotoxicology 7, 1095 (2013).
206. R. E. Unger, V. Krump-Konvalinkova, K. Peters, and C. J. Kirkpatrick, In vitro expression of the endothelial phenotype: Comparative study of primary isolated cells and cell lines, including the novel cell line HPMEC-ST1.6R. Microvascular Research 64, 384 (2002).
207. J. Xiao, X. Duan, Q. Yin, Z. Miao, H. Yu, C. Chen, Z. Zhang, J. Wang, and Y. Li, The inhibition of metastasis and growth of breast cancer by blocking the NF-kappa B signaling pathway using bioreducible PEI-based/p65 shRNA complex nanoparticles. Biomaterials 34, 5381 (2013).
208. E. W. Ades, F. J. Candal, R. A. Swerlick, V. G. George, S. Summers, D. C. Bosse, and T. J. Lawley, HMEC-1-establishment of an immortalized human microvascular endothelial-cell line. Journal of Investigative Dermatology. 99, 683 (1992).
209. A. M. Muller, M. I. Hermanns, C. Skrzynski, M. Nesslinger, K. M. Muller, and C. J. Kirkpatrick, Expression of the endothelial markers PECAM-1, vWf, and CD34 in vivo and in vitro. Exp. Mol. Pathol. 72, 221 (2002).
210. R. E. Unger, V. Krump-Konvalinkova, K. Peters, and C. J. Kirkpatrick, In vitro expression of the endothelial phenotype: Comparative study of primary isolated cells and cell lines, including the novel cell line HPMEC-ST1.6R. Microvasc. Res. 64, 384 (2002).
211. D. Bouis, G. A. Hospers, C. Meijer, G. Molema, and N. H. Mulder, Endothelium in vitro: A review of human vascular endothelial cell lines for blood vessel-related research. Angiogenesis 4, 91 (2001).
212. D. N. Ho, N. Kohler, A. Sigdel, R. Kalluri, J. R. Morgan, C. J. Xu, and S. H. Sun, Penetration of endothelial cell coated multicellular tumor spheroids by iron oxide nanoparticles. Theranostics 2, 66 (2012).
213. E. Garcia-Garcia, S. Gil, K. Andrieux, D. Desmaele, V. Nicolas, F. Taran, D. Georgin, J. P. Andreux, F. Roux, and P. Couvreur, A relevant in vitro rat model for the evaluation of blood-brain barrier translocation of nanoparticles. Cell. Mol. Life Sci. 62, 1400 (2005).
214. T. Y. Cheang, S. M. Wang, Z. J. Hu, Z. H. Xing, G. Q. Chang, C. Yao, Y. Liu, H. Zhang, and A. W. Xu, Calcium carbonate/CaIP6 nanocomposite particles as gene delivery vehicles for human vascular smooth muscle cells. J. Mater. Chem. 20, 8050 (2010).
215. C. M. Shanahan and P. L. Weissberg, Smooth muscle cell heterogeneity-patterns of gene expression in vascular smooth muscle cells in vitro and in vivo. Arterioscl Throm Vas. 18, 333 (1998).
216. Z. Gu, B. E. Rolfe, Z. P. Xu, A. C. Thomas, J. H. Campbell, and G. Q. Lu, Enhanced effects of low molecular weight heparin intercalated with layered double hydroxide nanoparticles on rat vascular smooth muscle cells. Biomaterials 31, 5455 (2010).
217. P. Carmeliet and R. K. Jain, Angiogenesis in cancer and other diseases. Nature 407, 249 (2000).
218. S. Kerkar, M. Williams, J. M. Blocksom, R. F. Wilson, J. G. Tyburski, and C. P. Steffes, TNF-alpha and IL-1beta increase pericyte/endothelial cell co-culture permeability. J. Surg. Res. 132, 40 (2006).
219. B. M. Rothen-Rutishauser, S. Schurch, B. Haenni, N. Kapp, and P. Gehr, Interaction of fine particles and nanoparticles with red blood cells visualized with advanced microscopic techniques. Environ. Sci. Technol. 40, 4353 (2006).
220. S. Krajewski, R. Prucek, A. Panacek, M. Avci-Adali, A. Nolte, A. Straub, R. Zboril, H. P. Wendel, and L. Kvitek, Hemocompatibility evaluation of different silver nanoparticle concentrations employing a modified Chandler-loop in vitro assay on human blood. Acta Biomater. 9, 7460 (2013).
221. E. Chambers and S. Mitragotri, Long circulating nanoparticles via adhesion on red blood cells: Mechanism and extended circulation. Exp. Biol. Med. (Maywood) 232, 958 (2007).
222. A. C. Anselmo, V. Gupta, B. J. Zern, D. Pan, M. Zakrewsky, V. Muzykantov, and S. Mitragotri, Delivering nanoparticles to lungs while avoiding liver and spleen through adsorption on red blood cells. ACS Nano 7, 11129 (2013).
223. M. Nahrendorf, H. W. Zhang, S. Hembrador, P. Panizzi, D. E. Sosnovik, E. Aikawa, P. Libby, F. K. Swirski, and R. Weissleder, Nanoparticle PET-CT imaging of macrophages in inflammatory atherosclerosis. Circulation 117, 379 (2008).
224. A. Agrawal and M. Manchester, Differential uptake of chemically modified cowpea mosaic virus nanoparticles in macrophage subpopulations present in inflammatory and tumor microenvironments. Biomacromolecules 13, 3320 (2012).
225. S. K. Baek, A. R. Makkouk, T. Krasieva, C. H. Sun, S. J. Madsen, and H. Hirschberg, Photothermal treatment of glioma; an in vitro study of macrophage-mediated delivery of gold nanoshells. Journal of Neuro-Oncology 104, 439 (2011).
226. N. Jonjic, T. Valkovic, K. Lucin, Z. Iternicka, M. Krstulja, E. Mustac, R. Dobi-Babic, F. Sasso, and M. Melato, Comparison of microvessel density with tumor associated macrophages in invasive breast carcinoma. Anticancer Res. 18, 3767 (1998).
227. S. Park, S. Kang, X. Chen, E. J. Kim, J. Kim, N. Kim, J. Kim, and M. M. Jin, Tumor suppression via paclitaxel-loaded drug carriers that target inflammation marker upregulated in tumor vasculature and macrophages. Biomaterials 34, 598 (2013).
228. F. Alexis, E. Pridgen, L. K. Molnar, and O. C. Farokhzad, Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol Pharm. 5, 505 (2008).
229. M. Bartneck, H. A. Keul, S. Singh, K. Czaja, J. Bornemann, M. Bockstaller, M. Moeller, G. Zwadlo-Klarwasser, and J. Groll, Rapid uptake of gold nanorods by primary human blood phagocytes and immunomodulatory effects of surface chemistry. ACS Nano 4, 3073 (2010).
230. A. Franca, P. Aggarwal, E. V. Barsov, S. V. Kozlov, M. A. Dobrovolskaia, and A. Gonzalez-Fernandez, Macrophage scavenger receptor A mediates the uptake of gold colloids by macrophages in vitro. Nanomedicine (Lond) 6, 1175 (2011).
231. Y. Sheng, Y. Yuan, C. Liu, X. Tao, X. Shan, and F. Xu, In vitro macrophage uptake and in vivo biodistribution of PLA-PEG nanoparticles loaded with hemoglobin as blood substitutes: Effect of PEG content. J. Mater. Sci. Mater. Med. 20, 1881 (2009).
232. S. Tsuchiya, Y. Kobayashi, Y. Goto, H. Okumura, S. Nakae, T. Konno, and K. Tada, Induction of maturation in cultured human monocytic leukemia cells by a phorbol diester. Cancer Res. 42, 1530 (1982).
233. O. Lunov, T. Syrovets, C. Loos, J. Beil, M. Delacher, K. Tron, G. U. Nienhaus, A. Musyanovych, V. Mailänder, K. Landfester, and T. Simmet, Differential uptake of functionalized polystyrene nanoparticles by human macrophages and a monocytic cell line. ACS Nano 5, 1657 (2011).
234. L. G. Griffith and M. A. Swartz, Capturing complex 3D tissue physiology in vitro. Nat. Rev. Mol. Cell Biol. 7, 211 (2006).
235. P. Friedl and E. B. Bröcker, The biology of cell locomotion within three-dimensional extracellular matrix. CMLS, Cell. Mol. Life Sci. 57, 41 (2000).
236. S.-H. Kim, J. Turnbull, and S. Guimond, Extracellular matrix and cell signalling: The dynamic cooperation of integrin, proteoglycan and growth factor receptor. J. Endocrinol. 209, 139 (2011).
237. C. J. Flaim, S. Chien, and S. N. Bhatia, An extracellular matrix microarray for probing cellular differentiation. Nat. Methods. 2, 119 (2005).
238. B. Geiger, A. Bershadsky, R. Pankov, and K. M. Yamada, Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2, 793 (2001).
239. D. E. Discher, P. Janmey, and Y.-l. Wang, Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139 (2005).
240. P. C. Georges and P. A. Janmey, Cell type-specific response to growth on soft materials. J. Appl. Physiol. 98, 1547 (2005).
241. M. P. Lutolf and J. A. Hubbell, Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat. Biotechnol. 23, 47 (2005).
242. A. L. Doiron, B. Clark, and K. D. Rinker, Endothelial Nanoparticle Binding Kinetics are Matrix and Size Dependent. Biotechnol. Bioeng. 108, 2988 (2011).
243. L. E. Dike, C. S. Chen, M. Mrksich, J. Tien, G. M. Whitesides, and D. E. Ingber, Geometric control of switching between growth, apoptosis, and differentiation during angiogenesis using micropatterned substrates. In Vitro Cellular and Developmental Biology-Animal 35, 441 (1999).
244. R. Kalluri and M. Zeisberg, Fibroblasts in cancer. Nat Rev Cancer. 6, 392 (2006).
245. R. K. Jain and T. Stylianopoulos, Delivering nanomedicine to solid tumors. Nature Reviews. Clinical Oncology 7, 653 (2010).
246. P. A. Netti, D. A. Berk, M. A. Swartz, A. J. Grodzinsky, and R. K. Jain, Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Research 60, 2497 (2000).
247. A. Pluen, Y. Boucher, S. Ramanujan, T. D. McKee, T. Gohongi, E. di Tomaso, E. B. Brown, Y. Izumi, R. B. Campbell, D. A. Berk, and R. K. Jain, Role of tumor-host interactions in interstitial diffusion of macromolecules: Cranial vs. subcutaneous tumors. Proceedings of the National Academy of Sciences 98, 4628 (2001).
248. C. Wong, T. Stylianopoulos, J. Cui, J. Martin, V. P. Chauhan, W. Jiang, Z. Popovic, R. K. Jain, M. G. Bawendi, and D. Fukumura, Multistage nanoparticle delivery system for deep penetration into tumor tissue. Proc. Natl. Acad Sci. USA 108, 2426 (2011).
249. S. J. Kuhn, S. K. Finch, D. E. Hallahan, and T. D. Giorgio, Proteolytic surface functionalization enhances in vitro magnetic nanoparticle mobility through extracellular matrix. Nano Lett. 6, 306 (2006).
250. B. Kim, G. Han, B. J. Toley, C. K. Kim, V. M. Rotello, and N. S. Forbes, Tuning payload delivery in tumour cylindroids using gold nanoparticles. Nat Nanotechnol. 5, 465 (2010).
251. T. Stylianopoulos, B. Diop-Frimpong, L. L. Munn, and R. K. Jain, Diffusion anisotropy in collagen gels and tumors: The effect of fiber network orientation. Biophys. J. 99, 3119 (2010).
252. T. Stylianopoulos, M. Z. Poh, N. Insin, M. G. Bawendi, D. Fukumura, L. L. Munn, and R. K. Jain, Diffusion of particles in the extracellular matrix: The effect of repulsive electrostatic interactions. Biophys. J. 99, 1342 (2010).
253. Z. Ji, X. Jin, S. George, T. Xia, H. Meng, X. Wang, E. Suarez, H. Zhang, E. M. V. Hoek, H. Godwin, A. E. Nel, and J. I. Zink, Dispersion and stability optimization of TiO2 nanoparticles in cell culture media. Environ. Sci. Technol. 44, 7309 (2010).
254. G. Maiorano, S. Sabella, B. Sorce, V. Brunetti, M. A. Malvindi, R. Cingolani, and P. P. Pompa, Effects of cell culture media on the dynamic formation of protein-nanoparticle complexes and influence on the cellular response. ACS Nano 4, 7481 (2010).
255. J. M. Brown and W. R. Wilson, Exploiting tumour hypoxia in cancer treatment. Nat. Rev. Cancer 4, 437 (2004).
256. S. Jain, J. Coulter, K. Butterworth, A. Hounsell, S. McMahon, W. Hyland, M. Muir, G. Dickson, K. Prise, F. Currell, D. Hirst, and J. O'Sullivan, Gold nanoparticle cellular uptake, toxicity and radiosensitisation in hypoxic conditions. Radiother. Oncol. (2014).
257. J. S. Lewis, D. W. McCarthy, T. J. McCarthy, Y. Fujibayashi, and M. J. Welch, Evaluation of 64Cu-ATSM in vitro and in vivo in a hypoxic tumor model. Journal of Nuclear Medicine: Official Publication, Society of Nuclear Medicine 40, 177 (1999).
258. Y.-H. Hsu, M. L. Moya, P. Abiri, C. C. W. Hughes, S. C. George, and A. P. Lee, Full range physiological mass transport control in 3D tissue cultures. Lab on a Chip. 13, 81 (2013).
259. M. L. Moya, Y. H. Hsu, A. P. Lee, C. C. W. Hughes, and S. C. George, In vitro perfused human capillary networks. Tissue Eng Part C-Me. 19, 730 (2013).
260. G. A. Truskey, Endothelial cell vascular smooth muscle cell coculture assay for high throughput screening assays for discovery of anti-angiogenesis agents and other therapeutic molecules. International Journal of High Throughput Screening 2010, 171 (2010).
261. M. S. Pepper, N. Ferrara, L. Orci, and R. Montesano, Potent synergism between vascular endothelial growth factor and basic fibroblast growth factor in the induction of angiogenesis in vitro. Biochem. Biophys. Res. Commun. 189, 824 (1992).
262. F. Silvagno, A. Follenzi, M. Arese, M. Prat, E. Giraudo, G. Gaudino, G. Camussi, P. M. Comoglio, and F. Bussolino, In-vivo activation of met tyrosine kinase by heterodimeric hepatocyte growth-factor molecule promotes angiogenesis. Arterioscler. Thromb. Vasc. Biol. 15, 1857 (1995).
263. R. Salcedo, M. L. Ponce, H. A. Young, K. Wasserman, J. M. Ward, H. K. Kleinman, J. J. Oppenheim, and W. J. Murphy, Human endothelial cells express CCR2 and respond to MCP-1: Direct role of MCP-1 in angiogenesis and tumor progression. Blood 96, 34 (2000).
264. M. Kono, Y. D. Mi, Y. J. Liu, T. Sasaki, M. L. Allende, Y. P. Wu, T. Yamashita, and R. L. Proia, The sphingosine-1-phosphate receptors S1P1, S1P2, and S1P3 function coordinately during embryonic angiogenesis. Journal of Biological Chemistry 279, 29367 (2004).
265. K. J. Bayless and G. E. Davis, Sphingosine-1-phosphate markedly induces matrix metalloproteinase and integrin-dependent human endothelial cell invasion and lumen formation in three-dimensional collagen and fibrin matrices. Biochemical and Biophysical Research Communications. 312, 903 (2003).
266. R. Montesano and L. Orci, Tumor-promoting phorbol esters induce angiogenesis in vitro. Cell 42, 469 (1985).
267. M. Klagsbrun, Angiogenic factors: Regulators of blood supplyside biology. FGF, endothelial cell growth factors and angiogenesis: A keystone symposium, Keystone, CO, USA, April 1-7, 1991. New Biol. 3, 745 (1991).
268. A. L. Aulanier, A. L. Doiron, R. D. Shepherd, K. D. Rinker, R. Frayne, and L. B. Andersen, A human cell model for dynamic testing of MR contrast agents. Biotechniques 50, 120 (2011).
269. D. Fukumura, H. A. Salehi, B. Witwer, R. F. Tuma, R. J. Melder, and R. K. Jain, Tumor necrosis factor α-induced leukocyte adhesion in normal and tumor vessels: Effect of tumor type, transplantation site, and host strain. Cancer Research 55, 4824 (1995).
270. R. Goel, N. Shah, R. Visaria, G. F. Paciotti, and J. C. Bischof, Biodistribution of TNF-alpha-coated gold nanoparticles in an in vivo model system. Nanomedicine (Lond) 4, 401 (2009).
271. M. M. Shenoi, I. Iltis, J. Choi, N. A. Koonce, G. J. Metzger, R. J. Griffin, and J. C. Bischof, Nanoparticle delivered vascular disrupting agents (VDAs): Use of TNF-alpha conjugated gold nanoparticles for multimodal cancer therapy. Molecular Pharmaceutics 10, 1683 (2013).
272. 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 Research 54, 4564 (1994).
273. R. K. Jain, Delivery of molecular and cellular medicine to solid tumors. Adv. Drug Del. Rev. 64, 353 (2012).
274. R. D. Shepherd, S. M. Kos, and K. D. Rinker, Flow-dependent Smad2 phosphorylation and TGIF nuclear localization in human aortic endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 301, H98 (2011).
275. V. Z. McKinney, K. D. Rinker, and G. A. Truskey, Normal and shear stresses influence the spatial distribution of intracellular adhesion molecule-1 expression in human umbilical vein endothelial cells exposed to sudden expansion flow. J. Biomech. 39, 806 (2006).
276. C. L. Ives, S. G. Eskin, and L. V. McIntire, Mechanical effects on endothelial cell morphology: In vitro assessment. In Vitro Cell Dev. Biol. 22, 500 (1986).
277. M. Gouverneur, J. A. E. Spaan, H. Pannekoek, R. D. Fontijn, and H. Vink, Fluid shear stress stimulates incorporation of hyaluronan into endothelial cell glycocalyx. American Journal of Physiology-Heart and Circulatory Physiology 290, H458 (2006).
278. A. Koo, C. F. Dewey, and G. Garcia-Cardena, Hemodynamic shear stress characteristic of atherosclerosis-resistant regions promotes glycocalyx formation in cultured endothelial cells. American Journal of Physiology-Cell Physiology 304, C137 (2013).
279. A. R. Pries and T. W. Secomb, Microvascular blood viscosity in vivo and the endothelial surface layer. American Journal of Physiology-Heart and Circulatory Physiology 289, H2657 (2005).
280. A. R. Pries, T. W. Secomb, H. Jacobs, M. Sperandio, K. Osterloh, and P. Gaehtgens, Microvascular blood flow resistance: Role of endothelial surface layer. American Journal of Physiology-Heart and Circulatory Physiology 273, H2272 (1997).
281. J. W. Song and L. L. Munn, Fluid forces control endothelial sprouting. Proc. Natl. Acad. Sci. USA 108, 15342 (2011).
282. K. D. Rinker, V. Prabhakar, and G. A. Truskey, Effect of contact time and force on monocyte adhesion to vascular endothelium. Biophys. J. 80, 1722 (2001).
283. A. Lin, A. Sabnis, S. Kona, S. Nattama, H. Patel, J. F. Dong, and K. T. Nguyen, Shear-regulated uptake of nanoparticles by endothelial cells and development of endothelial-targeting nanoparticles. J. Biomed. Mater. Res. A 93, 833 (2010).
284. T. Secomb, B. Styp-Rekowska, and A. Pries, Two-dimensional simulation of red blood cell deformation and lateral migration in microvessels. Ann. Biomed. Eng. 35, 755 (2007).
285. E. M. Sevick and R. K. Jain, Viscous resistance to blood flow in solid tumors: Effect of hematocrit on intratumor blood viscosity. Cancer Res. 49, 3513 (1989).
286. A. J. Thompson, E. M. Mastria, and O. Eniola-Adefeso, The margination propensity of ellipsoidal micro/nanoparticles to the endothelium in human blood flow. Biomaterials 34, 5863 (2013).
287. Y. Boucher and R. K. Jain, Microvascular pressure is the principal driving force for interstitial hypertension in solid tumors: Implications for vascular collapse. Cancer Res. 52, 5110 (1992).
288. R. K. Jain, Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science 307, 58 (2005).
289. D. B. Peckys and N. de Jonge, Visualizing gold nanoparticle uptake in live cells with liquid scanning transmission electron microscopy. Nano Lett. 11, 1733 (2011).
290. A. S. Chung, J. Lee, and N. Ferrara, Targeting the tumour vasculature: Insights from physiological angiogenesis. Nat. Rev. Cancer 10, 505 (2010).
291. D. Salani, G. Taraboletti, L. Rosano, V. Di Castro, P. Borsotti, R. Giavazzi, and A. Bagnato, Endothelin-1 induces an angiogenic phenotype in cultured endothelial cells and stimulates neovascularization in vivo. American Journal of Pathology 157, 1703 (2000).
292. A. Ueda, M. Koga, M. Ikeda, S. Kudo, and K. Tanishita, Effect of shear stress on microvessel network formation of endothelial cells with in vitro three-dimensional model. American Journal of Physiology-Heart and Circulatory Physiology 287, H994 (2004).
293. C. J. Kirkpatrick, S. Fuchs, and R. E. Unger, Co-culture systems for vascularization - Learning from nature. Adv. Drug Del. Rev. 63, 291 (2011).
294. W. M. Elbjeirami and J. L. West, Angiogenesis-like activity of endothelial cells co-cultured with VEGF-producing smooth muscle cells. Tissue Engineering 12, 381 (2006).
295. D. Hogemann, V. Ntziachristos, L. Josephson, and R. Weissleder, High throughput magnetic resonance imaging for evaluating targeted nanoparticle probes. Bioconjug. Chem. 13, 116 (2002).
296. R. Weissleder, K. Kelly, E. Y. Sun, T. Shtatland, and L. Josephson, Cell-specific targeting of nanoparticles by multivalent attachment of small molecules. Nat. Biotechnol. 23, 1418 (2005).
297. Y. C. Lin, L. W. Tsai, E. Perevedentseva, H. H. Chang, C. H. Lin, D. S. Sun, A. E. Lugovtsov, A. Priezzhev, J. Mona, and C. L. Cheng, The influence of nanodiamond on the oxygenation states and micro rheological properties of human red blood cells in vitro. Journal of biomedical optics. 17, 101512 (2012).
298. S. Zhao, L. Yuan, J. Wang, X. Zhang, Z. He, and Q. Zhang, A novel and facile approach to imaging nanoparticles transport across transwell filter grown cell monolayer in real-time and 〈i〉 in Situ 〈/i〉 under confocal laser scanning microscopy. Biol. Pharm. Bull. 35, 335 (2012).
299. P. D. Richardson, S. F. Mohammad, and R. G. Mason, Flow chamber studies of platelet-adhesion at controlled, spatially varied shear rates. Artificial Organs. 1, 128 (1977).
300. J. Frangos, S. Eskin, L. McIntire, and C. Ives, Flow effects on prostacyclin production by cultured human endothelial cells. Science 227, 1477 (1985).
301. J. Ruel, J. Lemay, G. Dumas, C. Doillon, and J. Charara, Development of a parallel plate flow chamber for studying cell behavior under pulsatile flow. ASAIO journal (American Society for Artificial Internal Organs: 1992) 41, 876 (1995).
302. B. J. Chung, A. M. Robertson, and D. G. Peters, The numerical design of a parallel plate flow chamber for investigation of endothelial cell response to shear stress. Comput. Struct. 81, 535 (2003).
303. J. A. McCann, S. D. Peterson, M. W. Plesniak, T. J. Webster, and K. M. Haberstroh, Non-uniform flow behavior in a parallel plate flow chamber alters endothelial cell responses. Ann. Biomed. Eng. 33, 328 (2005).
304. S. Kona, J. F. Dong, Y. L. Liu, J. F. Tan, and K. T. Nguyen, Biodegradable nanoparticles mimicking platelet binding as a targeted and controlled drug delivery system. International Journal of Pharmaceutics 423, 516 (2012).
305. J. B. Haun, G. P. Robbins, and D. A. Hammer, Engineering therapeutic nanocarriers with optimal adhesion for targeting. J. Adhes. 86, 131 (2010).
306. J. B. Haun, L. R. Pepper, E. T. Boder, and D. A. Hammer, Using engineered single-chain antibodies to correlate molecular binding properties and nanoparticle adhesion dynamics. Langmuir 27, 13701 (2011).
307. J. E. Blackwell, N. M. Dagia, J. B. Dickerson, E. L. Berg, and D. J. Goetz, Ligand coated nanosphere adhesion to E- and P-selectin under static and flow conditions. Annals of Biomedical Engineering. 29, 523 (2001).
308. L. E. M. Paulis, I. Jacobs, N. M. van den Akker, T. Geelen, D. G. Molin, L. W. E. Starmans, K. Nicolay, and G. J. Strijkers, Targeting of ICAM-1 on vascular endothelium under static and shear stress conditions using a liposomal Gd-based MRI contrast agent. J. Nanobiotechnol. 10, 12 (2012).
309. L. Hosta-Rigau and B. Stadler, Shear stress and its effect on the interaction of myoblast cells with nanosized drug delivery vehicles. Molecular Pharmaceutics 10, 2707 (2013).
310. B. Prabhakarpandian, M. C. Shen, K. Pant, and M. F. Kiani, Microfluidic devices for modeling cell-cell and particle-cell interactions in the microvasculature. Microvasc Res. 82, 210 (2011).
311. K. H. K. Wong, J. M. Chan, R. D. Kamm, and J. Tien, Microfluidic models of vascular functions. Annual Review of Biomedical Engineering 14, 205 (2012).
312. N. T. Nguyen, S. A. Shaegh, N. Kashaninejad, and D. T. Phan, Design, fabrication and characterization of drug delivery systems based on lab-on-a-chip technology. Adv. Drug Deliv. Rev. 65, 1403 (2013).
313. P. Neuzi, S. Giselbrecht, K. Lange, T. J. Huang, and A. Manz, Revisiting lab-on-a-chip technology for drug discovery. Nature Reviews. Drug Discovery 11, 620 (2012).
314. A. D. van der Meer, A. A. Poot, J. Feijen, and I. Vermes, Analyzing shear stress-induced alignment of actin filaments in endothelial cells with a microfluidic assay. Biomicrofluidics 4, 11103 (2010).
315. K. M. Chrobak, D. R. Potter, and J. Tien, Formation of perfused, functional microvascular tubes in vitro. Microvasc Res. 71, 185 (2006).
316. W. B. Saunders, B. L. Bohnsack, J. B. Faske, N. J. Anthis, K. J. Bayless, K. K. Hirschi, and G. E. Davis, Coregulation of vascular tube stabilization by endothelial cell TIMP-2 and pericyte TIMP-3. The Journal of Cell Biology 175, 179 (2006).
317. A. D. van der Meer, V. V. Orlova, P. ten Dijke, A. van den Berg, and C. L. Mummery, Three-dimensional co-cultures of human endothelial cells and embryonic stem cell-derived pericytes inside a microfluidic device. Lab Chip. 13, 3562 (2013).
318. Y. Zheng, J. Chen, M. Craven, N. W. Choi, S. Totorica, A. Diaz-Santana, P. Kermani, B. Hempstead, C. Fischbach-Teschl, J. A. Lopez, and A. D. Stroock, In vitro microvessels for the study of angiogenesis and thrombosis. Proc. Natl. Acad. Sci. USA 109, 9342 (2012).
319. S. Kim, H. Lee, M. Chung, and N. L. Jeon, Engineering of functional, perfusable 3D microvascular networks on a chip. Lab on a Chip 13, 1489 (2013).
320. K. H. K. Wong, J. G. Truslow, A. H. Khankhel, K. L. S. Chan, and J. Tien, Artificial lymphatic drainage systems for vascularized microfluidic scaffolds. Journal of Biomedical Materials Research Part A 101A, 2181 (2013).
321. J. H. Sung and M. L. Shuler, A micro cell culture analog (microCCA) with 3-D hydrogel culture of multiple cell lines to assess metabolism-dependent cytotoxicity of anti-cancer drugs. Lab Chip 9, 1385 (2009).
322. E. C. Costa, V. M. Gaspar, J. G. Marques, P. Coutinho, and I. J. Correia, Evaluation of nanoparticle uptake in co-culture cancer models. PLoS One 8, e70072 (2013).
323. C. F. Buchanan, E. E. Voigt, C. S. Szot, J. W. Freeman, P. P. Vlachos, and M. N. Rylander, Three-dimensional microfluidic collagen hydrogels for investigating flow-mediated tumor-endothelial signaling and vascular organization. Tissue Engineering Part C-Methods 20, 64 (2014).
324. H. Dolznig, C. Rupp, C. Puri, C. Haslinger, N. Schweifer, E. Wieser, D. Kerjaschki, and P. Garin-Chesa, Modeling colon adenocarcinomas in vitro: A 3d co-culture system induces cancer-relevant pathways upon tumor cell and stromal fibroblast interaction. The American Journal of Pathology 179, 487 (2011).
325. M. T. Santini, G. Rainaldi, and P. L. Indovina, Apoptosis, cell adhesion and the extracellular matrix in the three-dimensional growth of multicellular tumor spheroids. Critical reviews in oncology/hematology 36, 75 (2000).
326. B. J. Toley, J. Park, B.-J. Kim, R. Venkatasubramanian, M. M. Maharbiz, and N. S. Forbes, Micrometer-scale oxygen delivery rearranges cells and prevents necrosis in tumor tissue in vitro. Biotechnology Progress 28, 515 (2012).
327. 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, 7386 (2010).
328. H. L. Ma, Q. Jiang, S. Han, Y. Wu, J. Cui Tomshine, D. Wang, Y. Gan, G. Zou, and X. J. Liang, Multicellular tumor spheroids as an in vivo-like tumor model for three-dimensional imaging of chemotherapeutic and nano material cellular penetration. Mol Imaging 11, 487 (2012).
329. T. T. Goodman, J. Chen, K. Matveev, and S. H. Pun, Spatiotemporal modeling of nanoparticle delivery to multicellular tumor spheroids. Biotechnol. Bioeng. 101, 388 (2008).
330. B. J. Kim and N. S. Forbes, Flux analysis shows that hypoxia-inducible- factor-1-alpha minimally affects intracellular metabolism in tumor spheroids. Biotechnol Bioeng. 96, 1167 (2007).
331. A. Albanese, A. K. Lam, E. A. Sykes, J. V. Rocheleau, and W. C. Chan, Tumour-on-a-chip provides an optical window into nanoparticle tissue transport. Nat Commun. 4, 2718 (2013).
332. I. K. Zervantonakis, S. K. Hughes-Alford, J. L. Charest, J. S. Condeelis, F. B. Gertler, and R. D. Kamm, Three-dimensional microfluidic model for tumor cell intravasation and endothelial barrier function. Proceedings of the National Academy of Sciences 109, 13515 (2012).
333. R. Damoiseaux, S. George, M. Li, S. Pokhrel, Z. Ji, B. France, T. Xia, E. Suarez, R. Rallo, L. Madler, Y. Cohen, E. M. Hoek, and A. Nel, No time to lose-high throughput screening to assess nanomaterial safety. Nanoscale. 3, 1345 (2011).
334. C. Lawlor, M. P. O'Sullivan, N. Sivadas, S. O'Leary, P. J. Gallagher, J. Keane, and S.-A. Cryan, The application of high-content analysis in the study of targeted particulate delivery systems for intracellular drug delivery to alveolar macrophages. Molecular Pharmaceutics. 8, 1100 (2011).
335. P. Libby, Inflammation in atherosclerosis. Nature 420, 868 (2002).
336. J. J. Li, D. W. Zhu, J. W. Yin, Y. X. Liu, F. L. Yao, and K. D. Yao, Formation of nano-hydroxyapatite crystal in situ in chitosan-pectin polyelectrolyte complex network. Mat. Sci. Eng. C-Mater. 30, 795 (2010).
337. M. Magzoub, S. Jin, and A. S. Verkman, Enhanced macromolecule diffusion deep in tumors after enzymatic digestion of extracellular matrix collagen and its associated proteoglycan decorin. FASEB J. 22, 276 (2008).
338. T. E. Mallouk and P. Yang, Chemistry at the nano-bio interface. J. Am. Chem. Soc. 131, 7937 (2009).
339. Y. Ma, M. Sadoqi, and J. Shao, Biodistribution of indocyanine green-loaded nanoparticles with surface modifications of PEG and folic acid. Int. J. Pharm. 436, 25 (2012).
340. L. Mi, X. Zhang, W. Yang, L. Wang, Q. Huang, C. Fan, and J. Hu, Artificial nano-bio-complexes: Effects of nanomaterials on biomolecular reactions and applications in biosensing and detection. J. Nanosci. Nanotechnol. 9, 2247 (2009).
341. L. Milane, Z. F. Duan, and M. Amiji, Pharmacokinetics and biodistribution of lonidamine/paclitaxel loaded, EGFR-targeted nanoparticles in an orthotopic animal model of multi-drug resistant breast cancer. Nanomedicine 7, 435 (2011).
342. A. I. Minchinton and I. F. Tannock, Drug penetration in solid tumours. Nat. Rev. Cancer 6, 583 (2006).
343. A. D. Miller, Lipid-based nanoparticles in cancer diagnosis and therapy. Journal of Drug Delivery 2013, 165981 (2013).
344. C. P. Ng and S. H. Pun, A perfusable 3D cell-matrix tissue culture chamber for in situ evaluation of nanoparticle vehicle penetration and transport. Biotechnol. Bioeng. 99, 1490 (2008).
345. S. Nakagawa, M. A. Deli, S. Nakao, M. Honda, K. Hayashi, R. Nakaoke, Y. Kataoka, and M. Niwa, Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells. Cell. Mol. Neurobiol. 27, 687 (2007).
346. W. L. Mondy, D. Cameron, J. P. Timmermans, N. De Clerck, A. Sasov, C. Casteleyn, and L. A. Piegl, Micro-CT of corrosion casts for use in the computer-aided design of microvasculature. Tissue Eng. Part C-Me 15, 729 (2009).
347. K. Murugesan, V. Bokare, J. R. Jeon, E. J. Kim, J. H. Kim, and Y. S. Chang, Effect of Fe-Pd bimetallic nanoparticles on Sphingomonas sp. PH-07 and a nano-bio hybrid process for triclosan degradation. Bioresour. Technol. 102, 6019 (2011).
348. A. Eberhard, S. Kahlert, V. Goede, B. Hemmerlein, K. H. Plate, and H. G. Augustin, Heterogeneity of angiogenesis and blood vessel maturation in human tumors: Implications for antiangiogenic tumor therapies. Cancer Res. 60, 1388 (2000).
349. N. Mondal, K. K. Halder, M. M. Kamila, M. C. Debnath, T. K. Pal, S. K. Ghosal, B. R. Sarkar, and S. Ganguly, Preparation, characterization, and biodistribution of letrozole loaded PLGA nanoparticles in Ehrlich Ascites tumor bearing mice. Int. J. Pharm. 397, 194 (2010).
350. A. Z. Wang, K. Yuet, L. Zhang, F. X. Gu, M. Huynh-Le, A. F. Radovic-Moreno, P. W. Kantoff, N. H. Bander, R. Langer, and O. C. Farokhzad, ChemoRad nanoparticles: A novel multifunctional nanoparticle platform for targeted delivery of concurrent chemoradiation. Nanomedicine (Lond) 5, 361 (2010).
351. C. L. Tseng, S. Y. Wu, W. H. Wang, C. L. Peng, F. H. Lin, C. C. Lin, T. H. Young, and M. J. Shieh, Targeting efficiency and biodistribution of biotinylated-EGF-conjugated gelatin nanoparticles administered via aerosol delivery in nude mice with lung cancer. Biomaterials 29, 3014 (2008).
352. W. Jiang, B. Y. S. Kim, J. T. Rutka, and W. C. W. Chan, Nanoparticle-mediated cellular response is size-dependent. Nat. Nanotechnol. 3, 145 (2008).
353. T. Yu, A. Malugin, and H. Ghandehari, Impact of silica nanoparticle design on cellular toxicity and hemolytic activity. ACS Nano 5, 5717 (2011).
354. N. N. Ma, C. Ma, C. Y. Li, T. Wang, Y. J. Tang, H. Y. Wang, X. B. Mou, Z. Chen, and N. Y. He, Influence of nanoparticle shape, size, and surface functionalization on cellular uptake. J. Nanosci. Nanotechno. 13, 6485 (2013).
355. A. Verma and F. Stellacci, Effect of surface properties on nanoparticle-cell interactions. Small 6, 12 (2010).
356. J. L. Swift and D. T. Cramb, Nanoparticles as fluorescence labels: Is size all that matters? Biophys. J. 95, 865 (2008).
357. M. T. Wang, Y. Jin, Y. X. Yang, C. Y. Zhao, H. Y. Yang, X. F. Xu, X. Qin, Z. D. Wang, Z. R. Zhang, Y. L. Jian, and Y. Huang, In vivo biodistribution, anti-inflammatory, and hepatoprotective effects of liver targeting dexamethasone acetate loaded nanostructured lipid carrier system. International Journal of Nanomedicine 5, 487 (2010).
358. T. Wang, M. Zou, H. Jiang, Z. Ji, P. Gao, and G. Cheng, Synthesis of a novel kind of carbon nanoparticle with large mesopores and macropores and its application as an oral vaccine adjuvant. Eur. J. Pharm. Sci. 44, 653 (2011).
359. Z. Wang, S. Liu, J. Ma, G. Qu, X. Wang, S. Yu, J. He, J. Liu, T. Xia, and G. B. Jiang, Silver nanoparticles induced RNA polymerase-silver binding and RNA transcription inhibition in erythroid progenitor cells. ACS Nano 7, 4171 (2013).
360. L. C. Cheng, X. Jiang, J. Wang, C. Chen, and R. S. Liu, Nano-bio effects: Interaction of nanomaterials with cells. Nanoscale 5, 3547 (2013).
361. X. Zhang, J. Yin, C. Kang, J. Li, Y. Zhu, W. Li, Q. Huang, and Z. Zhu, Biodistribution and toxicity of nanodiamonds in mice after intratracheal instillation. Toxicol. Lett. 198, 237 (2010).
362. H. Zheng, L. Xing, Y. Cao, and S. Che, Coordination bonding based pH-responsive drug delivery systems. Coordination Chemistry Reviews 257, 1933 (2013).
363. Z. Liu, X. Gao, T. Kang, M. Jiang, D. Miao, G. Gu, Q. Hu, Q. Song, L. Yao, Y. Tu, H. Chen, X. Jiang, and J. Chen, B6 peptide-modified PEG-PLA nanoparticles for enhanced brain delivery of neuroprotective peptide. Bioconjug. Chem. 24, 997 (2013).
364. W. Liu, J. Rose, S. Plantevin, M. Auffan, J.-Y. Bottero, and C. Vidaud, Protein corona formation for nanomaterials and proteins of a similar size: Hard or soft corona? Nanoscale 5, 1658 (2013).
365. K. Hamad-Schifferli, How can we exploit the protein corona? Nanomedicine 8, 1 (2013).
366. E. Casals, T. Pfaller, A. Duschl, G. J. Oostingh, and V. Puntes, Time evolution of the nanoparticle protein corona. Acs Nano 4, 3623 (2010).
367. L. C. Thomassen, V. Rabolli, K. Masschaele, G. Alberto, M. Tomatis, M. Ghiazza, F. Turci, E. Breynaert, G. Martra, C. E. Kirschhock, J. A. Martens, D. Lison, and B. Fubini, Model system to study the influence of aggregation on the hemolytic potential of silica nanoparticles. Chem. Res. Toxicol. 24, 1869 (2011).
368. H. A. Lee, T. L. Leavens, S. E. Mason, N. A. Monteiro-Riviere, and J. E. Riviere, Comparison of Quantum Dot Biodistribution with a Blood-Flow-Limited Physiologically Based Pharmacokinetic Model. Nano Lett. 9, 794 (2009).
369. Y. Qu, W. Li, Y. L. Zhou, X. F. Liu, L. L. Zhang, L. M. Wang, Y. F. Li, A. Iida, Z. Y. Tang, Y. L. Zhao, Z. F. Chai, and C. Y. Chen, Full assessment of fate and physiological behavior of quantum dots utilizing caenorhabditis elegans as a model organism. Nano Lett. 11, 3174 (2011).
370. T. G. van Kooten, J. M. Schakenraad, H. C. Van der Mei, and H. J. Busscher, Development and use of a parallel-plate flow chamber for studying cellular adhesion to solid surfaces. J. Biomed. Mater. Res. 26, 725 (1992).
371. A. V. Gore, K. Monzo, Y. R. Cha, W. Pan, and B. M. Weinstein, Vascular development in the zebrafish. Cold Spring Harbor Perspectives in Medicine 2, a006684 (2012).
372. P. del Pino, B. Pelaz, Q. Zhang, P. Maffre, G. U. Nienhaus, and W. J. Parak, Protein corona formation around nanoparticles - from the past to the future. Mater. Horizons In press (2014).