Microvessels-on-a-chip to assess targeted ultrasound-assisted drug delivery

ACS Applied Materials and Interfaces

Volumn 8, Issue 46, 2016, Pages 31541-31549

  Park, Yoonjee C ^a,e   Zhang, Chentian ^a   Kim, Sudong ^b   Mohamedi, Graciela ^a   Beigie, Carl ^a   Nagy, Jon O ^c   Holt, R Glynn ^a   Cleveland, Robin O ^d   Jeon, Noo Li ^b   Wong, Joyce Y ^a  

^a Boston University   (United States)

^b Seoul National University   (South Korea)

^c NanoValent Pharmaceuticals Inc   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e 705 Engineering Research Center   (United States)

Author keywords

antiangiogenesis; focused ultrasound; microvasculature on a chip; targeted drug delivery; ultrasound assisted drug delivery

Indexed keywords

DIAGNOSIS; DRUG DOSAGE; LIPOSOMES; MICROFLUIDICS; MOLECULAR BIOLOGY; ULTRASONICS;

ANTIANGIOGENESIS; CELLULAR DAMAGE; FOCUSED ULTRASOUND; INTEGRIN RECEPTORS; MICRO-VASCULATURE; PULSED ULTRASOUNDS; TARGETED DRUG DELIVERY; TARGETING LIGANDS;

BLOOD VESSELS;

DOXORUBICIN; LIPOSOME;

DRUG DELIVERY SYSTEM; MICROBUBBLE; MICROVASCULATURE; ULTRASOUND;

DOXORUBICIN; DRUG DELIVERY SYSTEMS; LIPOSOMES; MICROBUBBLES; MICROVESSELS; ULTRASONICS;

EID: 84999115137     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.6b09071     Document Type: Article

References (36)

1. Taniyama, Y.; Tachibana, K.; Hiraoka, K.; Namba, T.; Yamasaki, K.; Hashiya, N.; Aoki, M.; Ogihara, T.; Yasufumi, K.; Morishita, R. Local Delivery of Plasmid DNA into Rat Carotid Artery Uing Ultrasound Circulation 2002, 105 (10) 1233-1239
2. Hynynen, K.; McDannold, N.; Vykhodtseva, N.; Jolesz, F. A. Noninvasive MR Imaging-guided Focal Opening of the Blood-Brain Barrier in Rabbits 1 Radiology 2001, 220 (3) 640-646 10.1148/radiol.2202001804
3. Escoffre, J. M.; Novell, A.; Serriere, S.; Lecomte, T.; Bouakaz, A. Irinotecan Delivery by Microbubble-Assisted Ultrasound: In Vitro Validation and a Pilot Preclinical Study Mol. Pharmaceutics 2013, 10 (7) 2667-2675 10.1021/mp400081b
4. Qin, J.; Wang, T. Y.; Willmann, J. K. Sonoporation: Applications for Cancer Therapy. In Therapeutic Ultrasound; Escoffre, J. M.; Bouakaz, A., Eds.; Springer International: Cham, Switzerland, 2016; Vol. 880, pp 263-291.
5. Kinoshita, M.; McDannold, N.; Jolesz, F. A.; Hynynen, K. Noninvasive Localized Delivery of Herceptin to the Mouse Brain by MRI-guided Focused Ultrasound-Induced Blood-Brain Barrier Disruption Proc. Natl. Acad. Sci. U. S. A. 2006, 103 (31) 11719-11723 10.1073/pnas.0604318103
6. Capelo-Martínez, J.-L. Ultrasound in Chemistry: Analytical Applications; John Wiley & Sons: New York, 2008.
7. Shi, W.; Forsberg, F.; Raichlen, J.; Needleman, L.; Goldberg, B. Pressure Dependence of Subharmonic Signals From Contrast Microbubbles Ultrasound in medicine & biology 1999, 25 (2) 275-283 10.1016/S0301-5629(98)00163-X
8. Hauser, J.; Ellisman, M.; Steinau, H.-U.; Stefan, E.; Dudda, M.; Hauser, M. Ultrasound Enhanced Endocytotic Activity of Human Fibroblasts Ultrasound in medicine & biology 2009, 35 (12) 2084-2092 10.1016/j.ultrasmedbio.2009.06.1090
9. Meijering, B. D.; Juffermans, L. J.; van Wamel, A.; Henning, R. H.; Zuhorn, I. S.; Emmer, M.; Versteilen, A. M.; Paulus, W. J.; van Gilst, W. H.; Kooiman, K. et al. Ultrasound and Microbubble-Targeted Delivery of Macromolecules is Regulated by Induction of Endocytosis and Pore Formation Circ. Res. 2009, 104 (5) 679-687 10.1161/CIRCRESAHA.108.183806
10. Zeghimi, A.; Escoffre, J. M.; Bouakaz, A. Role of Endocytosis in Sonoporation-Mediated Membrane Permeabilization and Uptake of Small Molecules: a Electron Microscopy Study Phys. Biol. 2015, 12 (6) 066007 10.1088/1478-3975/12/6/066007
11. Derieppe, M.; Rojek, K.; Escoffre, J.-M.; de Senneville, B. D.; Moonen, C.; Bos, C. Recruitment of Endocytosis in Sonopermeabilization-Mediated Drug Delivery: a Real-Time Study Phys. Biol. 2015, 12 (4) 046010 10.1088/1478-3975/12/4/046010
12. Qin, S.; Caskey, C. F.; Ferrara, K. W. Ultrasound Contrast Microbubbles in Imaging and Therapy: Physical Principles and Engineering Phys. Med. Biol. 2009, 54 (6) R27 10.1088/0031-9155/54/6/R01
13. Tung, Y.-S.; Vlachos, F.; Choi, J. J.; Deffieux, T.; Selert, K.; Konofagou, E. E. In vivo Transcranial Cavitation Threshold Detection During Ultrasound-Induced Blood-Brain Barrier Opening in Mice Phys. Med. Biol. 2010, 55 (20) 6141 10.1088/0031-9155/55/20/007
14. Pastorino, F.; Brignole, C.; Marimpietri, D.; Cilli, M.; Gambini, C.; Ribatti, D.; Longhi, R.; Allen, T. M.; Corti, A.; Ponzoni, M. Vascular Damage and Anti-Angiogenic Effects of Tumor Vessel-Targeted Liposomal Chemotherapy Cancer Res. 2003, 63 (21) 7400-7409
15. Chang, D.-K.; Chiu, C.-Y.; Kuo, S.-Y.; Lin, W.-C.; Lo, A.; Wang, Y.-P.; Li, P.-C.; Wu, H.-C. Antiangiogenic Targeting Liposomes Increase Therapeutic Efficacy for Solid Tumors J. Biol. Chem. 2009, 284 (19) 12905-12916 10.1074/jbc.M900280200
16. Kim, S.; Lee, H.; Chung, M.; Jeon, N. L. Engineering of Functional, Perfusable 3D Microvascular Networks On a Chip Lab Chip 2013, 13 (8) 1489-1500 10.1039/c3lc41320a
17. Less, J. R.; Posner, M. C.; Skalak, T. C.; Wolmark, N.; Jain, R. K. Geometric Resistance and Microvascular Network Architecture of Human Colorectal Carcinoma Microcirculation 1997, 4 (1) 25-33 10.3109/10739689709148315
18. Leunig, M.; Yuan, F.; Menger, M. D.; Boucher, Y.; Goetz, A. E.; Messmer, K.; Jain, R. K. Angiogenesis, Microvascular Architecture, Microhemodynamics, and Interstitial Fluid Pressure During Early Growth of Human Adenocarcinoma LS174T in SCID mice Cancer Res. 1992, 52 (23) 6553-6560
19. Farny, C. H.; Holt, R. G.; Roy, R. The Correlation Between Bubble-Enhanced HIFU Heating and Cavitation Power IEEE Trans. Biomed. Eng. 2010, 57 (1) 175-184 10.1109/TBME.2009.2028133
20. Hashizume, H.; Baluk, P.; Morikawa, S.; McLean, J. W.; Thurston, G.; Roberge, S.; Jain, R. K.; McDonald, D. M. Openings Between Defective Endothelial Cells Explain Tumor Vessel Leakiness Am. J. Pathol. 2000, 156 (4) 1363-1380 10.1016/S0002-9440(10)65006-7
21. Yang, F.-Y.; Fu, W.-M.; Yang, R.-S.; Liou, H.-C.; Kang, K.-H.; Lin, W.-L. Quantitative Evaluation of Focused Ultrasound With a Contrast Agent on Blood-Brain Barrier Disruption Ultrasound in medicine & biology 2007, 33 (9) 1421-1427 10.1016/j.ultrasmedbio.2007.04.006
22. Guzmán, H. R.; McNamara, A. J.; Nguyen, D. X.; Prausnitz, M. R. Bioeffects Caused by Changes in Acoustic Cavitation Bubble Density and Cell Concentration: a Unified Explanation Based on Cell-to-Bubble Ratio and Blast Radius Ultrasound in medicine & biology 2003, 29 (8) 1211-1222 10.1016/S0301-5629(03)00899-8
23. Danhier, F.; Breton, A. L.; Préat, V. r. RGD-based Strategies to Target Alpha (v) Beta (3) Integrin in Cancer Therapy and Diagnosi Mol. Pharmaceutics 2012, 9 (11) 2961-2973 10.1021/mp3002733
24. Brooks, P. C.; Clark, R.; Cheresh, D. A. Requirement of Vascular Integrin Alpha v Beta 3 for Angiogenesis Science 1994, 264 (5158) 569-571 10.1126/science.7512751
25. Wickham, T. J.; Mathias, P.; Cheresh, D. A.; Nemerow, G. R. Integrins αvβ3 and αvβ5 Promote Adenovirus Internalization But Not Virus Attachment Cell 1993, 73 (2) 309-319 10.1016/0092-8674(93)90231-E
26. Federman, N.; Chan, J.; Nagy, J. O.; Landaw, E. M.; McCabe, K.; Wu, A. M.; Triche, T.; Kang, H.; Liu, B.; Marks, J. D.; Denny, C. T. Enhanced Growth Inhibition of Osteosarcoma by Cytotoxic Polymerized Liposomal Nanoparticles Targeting the Alcam Cell Surface Receptor Sarcoma 2012, 2012, 1 10.1155/2012/126906
27. Garde, S. V.; Forté, A. J.; Ge, M.; Lepekhin, E. A.; Panchal, C. J.; Rabbani, S. A.; Wu, J. J. Binding and Internalization of NGR-Peptide-Targeted Liposomal Doxorubicin (TVT-DOX) in CD13-Expressing Cells and Its Antitumor Effects Anti-Cancer Drugs 2007, 18 (10) 1189-1200 10.1097/CAD.0b013e3282a213ce
28. Goren, D.; Horowitz, A. T.; Tzemach, D.; Tarshish, M.; Zalipsky, S.; Gabizon, A. Nuclear Delivery of Doxorubicin Via Folate-Targeted Liposomes With Bypass of Multidrug-Resistance Efflux Pump Clin. Cancer Res. 2000, 6 (5) 1949-1957
29. Sirsi, S. R.; Borden, M. A. Advances in Ultrasound Mediated Gene Therapy Using Microbubble Contrast Agents Theranostics 2012, 2 (12) 1208 10.7150/thno.4306
30. Alonso, A.; Reinz, E.; Jenne, J. W.; Fatar, M.; Schmidt-Glenewinkel, H.; Hennerici, M. G.; Meairs, S. Reorganization of Gap Junctions After Focused Ultrasound Blood-Brain Barrier Opening in the Rat Brain J. Cereb. Blood Flow Metab. 2010, 30 (7) 1394-1402 10.1038/jcbfm.2010.41
31. Zhou, Y.; Yang, K.; Cui, J.; Ye, J.; Deng, C. Controlled Permeation of Cell Membrane by Single Bubble Acoustic Cavitation J. Controlled Release 2012, 157 (1) 103-111 10.1016/j.jconrel.2011.09.068
32. Jin, L.-F.; Li, F.; Wang, H.-P.; Wei, F.; Qin, P.; Du, L.-F. Ultrasound Targeted Microbubble DestructionStimulates Cellular Endocytosis in Facilitation of Adeno-Associated Virus Delivery Int. J. Mol. Sci. 2013, 14 (5) 9737-9750 10.3390/ijms14059737
33. Shay-Salit, A.; Shushy, M.; Wolfovitz, E.; Yahav, H.; Breviario, F.; Dejana, E.; Resnick, N. VEGF Receptor 2 and the Adherens Junction As a Mechanical Transducer in Vascular Endothelial Cells Proc. Natl. Acad. Sci. U. S. A. 2002, 99 (14) 9462-9467 10.1073/pnas.142224299
34. Wu, J. Theoretical Study On Shear Stress Generated By Microstreaming Surrounding Contrast Agents Attached To Living Cells Ultrasound in medicine & biology 2002, 28 (1) 125-129 10.1016/S0301-5629(01)00497-5
35. Changenet-Barret, P.; Gustavsson, T.; Markovitsi, D.; Manet, I.; Monti, S. Unravelling Molecular Mechanisms in the Fluorescence Spectra of Doxorubicin in Aqueous Solution by Femtosecond Fluorescence Spectroscopy Phys. Chem. Chem. Phys. 2013, 15 (8) 2937-2944 10.1039/c2cp44056c
36. Chazotte, B. Labeling Nuclear DNA With Hoechst 33342 Cold Spring Harbor Protocols 2011, 2011 (1) pdb.prot5557 10.1101/pdb.prot5557