Aqueous Two‐Phase System Patterning of Microbubbles: Localized Induction of Apoptosis in Sonoporated Cells
dc.contributor.author | Frampton, John P. | en_US |
dc.contributor.author | Fan, Zhenzhen | en_US |
dc.contributor.author | Simon, Arlyne | en_US |
dc.contributor.author | Chen, Di | en_US |
dc.contributor.author | Deng, Cheri X. | en_US |
dc.contributor.author | Takayama, Shuichi | en_US |
dc.date.accessioned | 2013-08-02T20:51:19Z | |
dc.date.available | 2014-09-02T14:12:53Z | en_US |
dc.date.issued | 2013-07-19 | en_US |
dc.identifier.citation | Frampton, John P.; Fan, Zhenzhen; Simon, Arlyne; Chen, Di; Deng, Cheri X.; Takayama, Shuichi (2013). "Aqueous Two‐Phase System Patterning of Microbubbles: Localized Induction of Apoptosis in Sonoporated Cells." Advanced Functional Materials 23(27): 3420-3431. <http://hdl.handle.net/2027.42/99004> | en_US |
dc.identifier.issn | 1616-301X | en_US |
dc.identifier.issn | 1616-3028 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/99004 | |
dc.description.abstract | Ultrasound‐driven microbubbles produce mechanical forces that can disrupt cell membranes (sonoporation). However, it is difficult to control microbubble location with respect to cells. This lack of control leads to low sonoporation efficiencies and variable outcomes. In this study, aqueous two‐phase system (ATPS) droplets are used to localize microbubbles in select micro‐regions at the surface of living cells. This is achieved by stably partitioning microbubbles in dextran (DEX) droplets, deposited on living adherent cells in medium containing polyethylene glycol (PEG). The interfacial energy at the PEG‐DEX interface overcomes microbubble buoyancy and prevents microbubbles from floating away from the cells. Spreading of the small DEX droplets retains microbubbles at the cell surface in defined lateral positions without the need for antibody or cell‐binding ligand conjugation. The patterned microbubbles are activated on a cell monolayer exposed to a broadly applied ultrasound field (center frequency 1.25 MHz, active element diameter 0.6 cm, pulse duration 8 μs or 30 s). This system enables efficient testing of different ultrasound conditions for their effects on sonoporation‐mediated membrane disruption and cell viability. Regions of cells without patterned microbubbles show no injury or membrane disruption. In microbubble patterned regions, 8 μs ultrasound pulses (0.2‐0.6 MPa) produce cell death that is primarily apoptotic. Ultrasound‐induced apoptosis increases with higher extracellular calcium concentrations, with cells displaying all of the hallmarks of apoptosis including annexinV labeling, loss of mitochondrial membrane potential, caspase activation and changes in nuclear morphology. A new method is described for patterning microbubbles on cell monolayers to target ultrasound treatment to cells. This novel platform provides a controlled system for high throughput testing of the effects of ultrasound‐mediated cell membrane disruption on cell physiology. Using this patterning method, it is possible to induce apoptosis in select populations of cells. | en_US |
dc.publisher | WILEY‐VCH Verlag | en_US |
dc.subject.other | Sonoporation | en_US |
dc.subject.other | Aqueous Two‐Phase System | en_US |
dc.subject.other | Microbubble | en_US |
dc.subject.other | Ultrasound | en_US |
dc.subject.other | Apoptosis | en_US |
dc.title | Aqueous Two‐Phase System Patterning of Microbubbles: Localized Induction of Apoptosis in Sonoporated Cells | en_US |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | en_US |
dc.subject.hlbsecondlevel | Materials Science and Engineering | en_US |
dc.subject.hlbsecondlevel | Engineering (General) | en_US |
dc.subject.hlbtoplevel | Engineering | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.contributor.affiliationum | Department of Biomedical Engineering, University of Michigan, Ann Arbor, USA | en_US |
dc.contributor.affiliationum | Department of Macromolecular Science and Engineering, University of Michigan, Ann Arbor, USA | en_US |
dc.contributor.affiliationum | Department of Biomedical Engineering, University of Michigan, Ann Arbor, USA. | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/99004/1/3420_ftp.pdf | |
dc.identifier.doi | 10.1002/adfm.201203321 | en_US |
dc.identifier.source | Advanced Functional Materials | en_US |
dc.identifier.citedreference | A. van Wamel, K. Kooiman, M. Harteveld, M. Emmer, F. J. ten Cate, M. Versluis, N. de Jong, J. Controlled Release 2006, 112, 149. | en_US |
dc.identifier.citedreference | M. S. Al‐Dosari, X. Gao, AAPS J. 2009, 11, 671. | en_US |
dc.identifier.citedreference | S. Mehier‐Humbert, R. H. Guy, Adv. Drug Delivery Rev. 2005, 57, 733. | en_US |
dc.identifier.citedreference | J. Villemejane, L. M. Mir, Brit. J. Pharmacol. 2009, 157, 207. | en_US |
dc.identifier.citedreference | D. J. Wells, Gene Ther. 2004, 11, 1363. | en_US |
dc.identifier.citedreference | J. L. Lee, C. W. Lo, S. M. Ka, A. Chen, W. S. Chen, J. Controlled Release 2012, 160, 64. | en_US |
dc.identifier.citedreference | R. Suzuki, Y. Oda, N. Utoguchi, K. Maruyama, J. Controlled Release 2011, 149, 36. | en_US |
dc.identifier.citedreference | D. J. Wells, Cell Biology Toxicology 2010, 26, 21. | en_US |
dc.identifier.citedreference | L. H. Treat, N. McDannold, N. Vykhodtseva, Y. Zhang, K. Tam, K. Hynynen, Int. J. Cancer 2007, 121, 901. | en_US |
dc.identifier.citedreference | W. Zhong, W. H. Sit, J. M. Wan, A. C. Yu, Ultrasound Med. Biol. 2011, 37, 2149. | en_US |
dc.identifier.citedreference | A. Lawrie, A. F. Brisken, S. E. Francis, D. C. Cumberland, D. C. Crossman, C. M. Newman, Gene Ther. 2000, 7, 2023. | en_US |
dc.identifier.citedreference | S. Zhang, J. Cheng, Y. X. Qin, PLoS One 2012, 7, 38343. | en_US |
dc.identifier.citedreference | R. Karshafian, P. D. Bevan, R. Williams, S. Samac, P. N. Burns, Ultrasound Med. Biol. 2009, 35, 847. | en_US |
dc.identifier.citedreference | L. C. Phillips, A. L. Klibanov, B. R. Wamhoff, J. A. Hossack, Ultrasound Med. Biol. 2010, 36, 1470. | en_US |
dc.identifier.citedreference | B. D. Meijering, L. J. Juffermans, A. van Wamel, R. H. Henning, I. S. Zuhorn, M. Emmer, A. M. Versteilen, W. J. Paulus, W. H. van Gilst, K. Kooiman, N. de Jong, R. J. Musters, L. E. Deelman, O. Kamp, Circ. Res. 2009, 104, 679. | en_US |
dc.identifier.citedreference | J. L. Tlaxca, C. R. Anderson, A. L. Klibanov, B. Lowrey, J. A. Hossack, J. S. Alexander, M. B. Lawrence, J. J. Rychak, Ultrasound Med. Biol. 2010, 36, 1907. | en_US |
dc.identifier.citedreference | H. Honda, T. Kondo, Q. L. Zhao, L. B. Feril Jr., H. Kitagawa, Ultrasound Med. Biol. 2004, 30, 683. | en_US |
dc.identifier.citedreference | M. A. Hassan, P. Campbell, T. Kondo, Drug Discovery Today 2010, 15, 892. | en_US |
dc.identifier.citedreference | L. B. Feril Jr., T. Kondo, Q. L. Zhao, R. Ogawa, K. Tachibana, N. Kudo, S. Fujimoto, S. Nakamura, Ultrasound Med. Biol. 2003, 29, 331. | en_US |
dc.identifier.citedreference | D. Huh, H. Fujioka, Y. C. Tung, N. Futai, R. Paine, 3rd, J. B. Grotberg, S. Takayama, Proc. Natl. Acad. Sci. USA 2007, 104, 18886. | en_US |
dc.identifier.citedreference | N. J. Douville, P. Zamankhan, Y. C. Tung, R. Li, B. L. Vaughan, C. F. Tai, J. White, P. J. Christensen, J. B. Grotberg, S. Takayama, Lab Chip 2011, 11, 609. | en_US |
dc.identifier.citedreference | G. Wickman, L. Julian, M. F. Olson, Cell Death Differ. 2012, 19, 735. | en_US |
dc.identifier.citedreference | G. J. Czarnota, R. Karshafian, P. N. Burns, S. Wong, A. Al Mahrouki, J. W. Lee, A. Caissie, W. Tran, C. Kim, M. Furukawa, E. Wong, A. Giles, Proc. Natl. Acad. Sci. USA 2012, 109, 2033. | en_US |
dc.identifier.citedreference | Z. Xu, Z. Fan, T. L. Hall, F. Winterroth, J. B. Fowlkes, C. A. Cain, Ultrasound Med. Biol. 2009, 35, 245. | en_US |
dc.identifier.citedreference | Z. Xu, T. L. Hall, J. B. Fowlkes, C. A. Cain, J. Acoust. Soc. Am. 2007, 122, 229. | en_US |
dc.identifier.citedreference | J. E. Kennedy, Nat. Rev. Cancer 2005, 5, 321. | en_US |
dc.identifier.citedreference | M. J. van den Hoff, A. F. Moorman, W. H. Lamers, Nucleic Acids Res. 1992, 20, 2902. | en_US |
dc.identifier.citedreference | Z. Fan, R. E. Kumon, J. Park, C. X. Deng, J. Controlled Release 2010, 142, 31. | en_US |
dc.identifier.citedreference | A. L. Hook, H. Thissen, N. H. Voelcker, Trends Biotechnol. 2006, 24, 471. | en_US |
dc.identifier.citedreference | S. Takayama, E. Ostuni, P. LeDuc, K. Naruse, D. E. Ingber, G. M. Whitesides, Nature 2001, 411, 1016. | en_US |
dc.identifier.citedreference | S. Takayama, E. Ostuni, P. LeDuc, K. Naruse, D. E. Ingber, G. M. Whitesides, Chem. Biol. 2003, 10, 123. | en_US |
dc.identifier.citedreference | T. Jain, J. Muthuswamy, Biosens. Bioelectron. 2007, 22, 863. | en_US |
dc.identifier.citedreference | J. K. Valley, S. Neale, H. Y. Hsu, A. T. Ohta, A. Jamshidi, M. C. Wu, Lab Chip 2009, 9, 1714. | en_US |
dc.identifier.citedreference | H. Tavana, A. Jovic, B. Mosadegh, Q. Y. Lee, X. Liu, K. E. Luker, G. D. Luker, S. J. Weiss, S. Takayama, Nat. Mater. 2009, 8, 736. | en_US |
dc.identifier.citedreference | H. Tavana, B. Mosadegh, S. Takayama, Adv. Mater. 2010, 22, 2628. | en_US |
dc.identifier.citedreference | P. A. K. Albertsson, Partition of cell particles and macromolecules: separation and purification of biomolecules, cell organelles, membranes, and cells in aqueous polymer two‐phase systems and their use in biochemical analysis and biotechnology, Wiley, New York 1986. | en_US |
dc.identifier.citedreference | Y. Fang, J. P. Frampton, S. Raghavan, R. Sabahi‐Kaviani, G. Luker, C. X. Deng, S. Takayama, Tissue Eng., C 2012, 18, 647. | en_US |
dc.identifier.citedreference | T. Yaguchi, M. Dwidar, C. K. Byun, B. Leung, S. Lee, Y. K. Cho, R. J. Mitchell, S. Takayama, Biomacromolecules 2012, 13, 2655. | en_US |
dc.identifier.citedreference | P. Marmottant, S. Hilgenfeldt, Nature 2003, 423, 153. | en_US |
dc.identifier.citedreference | M. Postema, A. van Wamel, C. T. Lancee, N. de Jong, Ultrasound Med. Biol. 2004, 30, 827. | en_US |
dc.identifier.citedreference | P. Prentice, A. Cuschieri, K. Dholakia, M. Prausnitz, P. Campbell, Nat. Phys. 2005, 1, 107. | en_US |
dc.identifier.citedreference | C. D. Ohl, M. Arora, R. Ikink, N. de Jong, M. Versluis, M. Delius, D. Lohse, Biophysical J. 2006, 91, 4285. | en_US |
dc.identifier.citedreference | D. L. Miller, S. V. Pislaru, J. E. Greenleaf, Somatic Cell Mol. Genet. 2002, 27, 115. | en_US |
dc.identifier.citedreference | N. Kudo, K. Okada, K. Yamamoto, Biophys. J. 2009, 96, 4866. | en_US |
dc.identifier.citedreference | K. W. Ferrara, M. A. Borden, H. Zhang, Acc. Chem. Res. 2009, 42, 881. | en_US |
dc.identifier.citedreference | A. L. Klibanov, Med. Biol. Eng. Comput. 2009, 47, 875. | en_US |
dc.identifier.citedreference | J. R. Lindner, Nat. Rev. Drug Discovery 2004, 3, 527. | en_US |
dc.identifier.citedreference | X. Wang, C. E. Hagemeyer, J. D. Hohmann, E. Leitner, P. C. Armstrong, F. Jia, M. Olschewski, A. Needles, K. Peter, I. Ahrens, Circulation 2012, 125, 3117. | en_US |
dc.identifier.citedreference | K. Kooiman, M. Foppen‐Harteveld, A. F. van der Steen, N. de Jong, J. Controlled Release 2011, 154, 35. | en_US |
dc.identifier.citedreference | G. Korpanty, S. Chen, R. V. Shohet, J. Ding, B. Yang, P. A. Frenkel, P. A. Grayburn, Gene Ther. 2005, 12, 1305. | en_US |
dc.identifier.citedreference | J. M. Warram, A. G. Sorace, R. Saini, A. V. Borovjagin, K. Hoyt, K. R. Zinn, Cancer Gene Ther. 2012, 19, 545. | en_US |
dc.identifier.citedreference | Z. Fan, H. Liu, M. Mayer, C. X. Deng, Proc. Natl. Acad. Sci. USA 2012, 109, 16486. | en_US |
dc.identifier.citedreference | P. A. Dayton, K. E. Morgan, A. L. Klibanov, G. Brandenburger, K. R. Nightingale, K. W. Ferrara, IEEE Trans. Ultrason. Ferroelectr. Freq. Control 1997, 44, 1264. | en_US |
dc.identifier.citedreference | V. Bjerknes, Fields of force; supplementary lectures, applications to meteorology; a course of lectures in mathematical physics delivered December 1 to 23, 1905, The Columbia University Press, New York 1906. | en_US |
dc.identifier.citedreference | J. C. Yarrow, Z. E. Perlman, N. J. Westwood, T. J. Mitchison, BMC Biotechnol. 2004, 4, 21. | en_US |
dc.identifier.citedreference | C. C. Liang, A. Y. Park, J. L. Guan, Nat. Protoc. 2007, 2, 329. | en_US |
dc.identifier.citedreference | C. R. Keese, J. Wegener, S. R. Walker, I. Giaever, Proc. Natl. Acad. Sci. USA 2004, 101, 1554. | en_US |
dc.identifier.citedreference | F. Q. Nie, M. Yamada, J. Kobayashi, M. Yamato, A. Kikuchi, T. Okano, Biomaterials 2007, 28, 4017. | en_US |
dc.identifier.citedreference | S. L. Fink, B. T. Cookson, Infect. Immun. 2005, 73, 1907. | en_US |
dc.identifier.citedreference | U. Ziegler, P. Groscurth, News Physiol. Sci. 2004, 19, 124. | en_US |
dc.identifier.citedreference | Y. Zhou, J. Shi, J. Cui, C. X. Deng, J. Controlled Release 2008, 126, 34. | en_US |
dc.identifier.citedreference | C. X. Deng, F. Sieling, H. Pan, J. Cui, Ultrasound Med. Biol. 2004, 30, 519. | en_US |
dc.identifier.citedreference | P. L. McNeil, M. Terasaki, Nat. Cell Biol. 2001, 3, E124. | en_US |
dc.identifier.citedreference | S. Orrenius, B. Zhivotovsky, P. Nicotera, Nat. Rev. Mol. Cell Biol. 2003, 4, 552. | en_US |
dc.identifier.citedreference | D. Falconnet, G. Csucs, H. M. Grandin, M. Textor, Biomaterials 2006, 27, 3044. | en_US |
dc.identifier.citedreference | J. Y. Lim, H. J. Donahue, Tissue Eng. 2007, 13, 1879. | en_US |
dc.identifier.citedreference | B. R. Ringeisen, C. M. Othon, J. A. Barron, D. Young, B. J. Spargo, Biotechnol. J. 2006, 1, 930. | en_US |
dc.identifier.citedreference | D. Wright, B. Rajalingam, S. Selvarasah, M. R. Dokmeci, A. Khademhosseini, Lab Chip 2007, 7, 1272. | en_US |
dc.identifier.citedreference | H. Tavana, B. Mosadegh, P. Zamankhan, J. B. Grotberg, S. Takayama, Biotechnol. Bioeng. 2011, 108, 2509. | en_US |
dc.identifier.citedreference | H. Tavana, S. Takayama, Biomicrofluidics 2011, 5, 13404. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
Remediation of Harmful Language
The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.
Accessibility
If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.