Vascular bursts enhance permeability of tumour blood vessels and improve nanoparticle delivery

Nature Nanotechnology

Volumn 11, Issue 6, 2016, Pages 533-538

  Matsumoto, Yu ^a   Nichols, Joseph W ^b   Toh, Kazuko ^a   Nomoto, Takahiro ^c   Cabral, Horacio ^d   Miura, Yutaka ^a   Christie, R James ^a,i   Yamada, Naoki ^a   Ogura, Tadayoshi ^e   Kano, Mitsunobu R ^f   Matsumura, Yasuhiro ^g   Nishiyama, Nobuhiro ^c   Yamasoba, Tatsuya ^a   Bae, You Han ^h   Kataoka, Kazunori ^a,d  

^a UNIVERSITY OF TOKYO   (Japan)

^b University of Utah   (United States)

^c TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e Nikon Instech Company Limited   (Japan)

^f OKAYAMA UNIVERSITY   (Japan)

^g NATIONAL CANCER CENTER HOSPITAL EAST   (Japan)

^h UNIVERSITY OF UTAH   (United States)

ⁱ MEDIMMUNE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; DRUG DELIVERY; NANOPARTICLES; STOCHASTIC SYSTEMS; TUMORS;

CONFOCAL LASER SCANNING MICROSCOPY; DYNAMIC PHENOMENA; ENHANCED PERMEABILITY; INTERSTITIAL SPACE; UNDERLYING DISTRIBUTION; VASCULAR WALL;

BLOOD VESSELS;

DOXORUBICIN; NANOPARTICLE; ANTINEOPLASTIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL PERMEABILITY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; EXTRAVASATION; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; INTRAVITAL MICROSCOPY; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; TUMOR VASCULARIZATION; VASCULAR TUMOR; ANIMAL; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; CAPILLARY PERMEABILITY; CHEMISTRY; COMPUTER SIMULATION; CONFOCAL MICROSCOPY; DRUG EFFECT; NANOMEDICINE; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PARTICLE SIZE; PROCEDURES; VASCULARIZATION;

ANIMALS; ANTINEOPLASTIC AGENTS; CAPILLARY PERMEABILITY; COMPUTER SIMULATION; FEMALE; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; MODELS, CARDIOVASCULAR; NANOMEDICINE; NANOPARTICLES; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PARTICLE SIZE;

EID: 84958087723     PISSN: 17483387     EISSN: 17483395     Source Type: Journal    
DOI: 10.1038/nnano.2015.342     Document Type: Article

References (27)

1. Hashizume, H. et al. Openings between defective endothelial cells explain tumor vessel leakiness. Am. J. Pathol. 156, 1363-1380 (2000).
2. Matsumura, Y. & Maeda, H. A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs. Cancer Res. 46, 6387-6392 (1986).
3. Li, Y. et al. Direct labeling and visualization of blood vessels with lipophilic carbocyanine dye DiI. Nature Protoc. 3, 1703-1708 (2008).
4. Matsumoto, Y. et al. Direct and instantaneous observation of intravenously injected substances using intravital confocal micro-videography. Biomed. Opt. Express 1, 1209-1216 (2010).
5. Nomoto, T. et al. In situ quantitative monitoring of polyplexes and polyplex micelles in the blood circulation using intravital real-time confocal laser scanning microscopy. J. Control. Release 151, 104-109 (2011).
6. Cabral, H. et al. Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size. Nature Nanotech. 6, 815-823 (2011).
7. Jain, R. K. & Stylianopoulos, T. Delivering nanomedicine to solid tumors. Nat. Rev. Clin. Oncol. 7, 653-664 (2010).
8. Lee, H., Fonge, H., Hoang, B., Reilly, R. M. & Allen, C. The effects of particle size and molecular targeting on the intratumoral and subcellular distribution of polymeric nanoparticles. Mol. Pharm. 7, 1195-1208 (2010).
9. Matsumoto, K. et al. Study of normal and pathological blood vessel morphogenesis in Flt1-tdsRed BAC Tg mice. Genesis 50, 561-571 (2012).
10. Dvorak, H. F., Nagy, J. A., Dvorak, J. T. & Dvorak, A. M. Identification and characterization of the blood vessels of solid tumors that are leaky to circulating macromolecules. Am. J. Pathol. 133, 95-109 (1988).
11. Ruggeri, B. A., Camp, F. & Miknyoczki, S. Animal models of disease: pre-clinical animal models of cancer and their applications and utility in drug discovery. Biochem. Pharmacol. 87, 150-161 (2014).
12. Tsuzuki, Y. et al. Pancreas microenvironment promotes VEGF expression and tumor growth: novel window models for pancreatic tumor angiogenesis and microcirculation. Lab. Invest. 81, 1439-1451 (2001).
13. Stirland, D. L., Nichols, J. W., Miura, S. & Bae, Y. H. Mind the gap: A survey of how cancer drug carriers are susceptible to the gap between research and practice. J. Control. Release 172, 1045-1064 (2013).
14. Holback, H. & Yeo, Y. Intratumoral drug delivery with nanoparticulate carriers. Pharm Res 28, 1819-1830 (2011).
15. Kumar, A. & Graham, M. D. Mechanism of margination in confined flows of blood and other multicomponent suspensions. Phys. Rev. Lett. 109, 108102 (2012).
16. Lee, S. Y., Ferrari, M. & Decuzzi, P. Design of bio-mimetic particles with enhanced vascular interaction. J. Biomech. 42, 1885-1890 (2009).
17. Lee, S. Y., Ferrari, M. & Decuzzi, P. Shaping nano-/micro-particles for enhanced vascular interaction in laminar flows. Nanotechnology 20, 495101 (2009).
18. Mitragotri, S. & Lahann, J. Physical approaches to biomaterial design. Nature Mater. 8, 15-23 (2009).
19. Wong, C. et al. Multistage nanoparticle delivery system for deep penetration into tumor tissue. Proc. Natl Acad. Sci. USA 108, 2426-2431 (2011).
20. Baron, V. T., Welsh, J., Abedinpour, P. & Borgstrom, P. Intravital microscopy in the mouse dorsal chamber model for the study of solid tumors. Am. J. Cancer Res. 1, 674-686 (2011).
21. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671-675 (2012).
22. Weller, H. G. & Tabor, G. A tensorial approach to computational continuum mechanics using object-oriented techniques. Comput. Phys. 12, 620-631 (1998).
23. Issa, R. I. Solution of the implicitly discretised fluid flow equations by operatorsplitting. J. Comput. Phys. 62, 40-65 (1985).
24. Hobbs, S. K. et al. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc. Natl Acad. Sci. USA 95, 4607-4612 (1998).
25. Boucher, Y. & Jain, R. K. Microvascular pressure is the principal driving force for interstitial hypertension in solid tumors: implications for vascular collapse. Cancer Res. 52, 5110-5114 (1992).
26. Levick, J. R. & Michel, C. C. Microvascular fluid exchange and the revised Starling principle. Cardiovasc. Res. 87, 198-210 (2010).
27. Stohrer, M., Boucher, Y., Stangassinger, M. & Jain, R. K. Oncotic pressure in solid tumors is elevated. Cancer Res. 60, 4251-4255 (2000).