Ultrasound-Responsive Aqueous Two-Phase Microcapsules for On-Demand Drug Release.

Publisher: Wiley-VCH Country of Publication: Germany NLM ID: 0370543 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1521-3773 (Electronic) Linking ISSN: 14337851 NLM ISO Abbreviation: Angew Chem Int Ed Engl Subsets: MEDLINE

Publication: <2004-> : Weinheim : Wiley-VCH
Original Publication: Weinheim/Bergstr. : New York, : Verlag Chemie ; Academic Press, c1962-

Hydrogels* ; Microfluidics*; Capsules/chemistry ; Drug Delivery Systems ; Drug Liberation ; Ultrasonography ; Water

Traditional implanted drug delivery systems cannot easily change their release profile in real time to respond to physiological changes. Here we present a microfluidic aqueous two-phase system to generate microcapsules that can release drugs on demand as triggered by focused ultrasound (FUS). The biphasic microcapsules are made of hydrogels with an outer phase of mixed molecular weight (MW) poly(ethylene glycol) diacrylate that mitigates premature payload release and an inner phase of high MW dextran with payload that breaks down in response to FUS. Compound release from microcapsules could be triggered as desired; 0.4 μg of payload was released across 16 on-demand steps over days. We detected broadband acoustic signals amidst low heating, suggesting inertial cavitation as a key mechanism for payload release. Overall, FUS-responsive microcapsules are a biocompatible and wirelessly triggerable structure for on-demand drug delivery over days to weeks.
(© 2022 Wiley-VCH GmbH.)

.
S. A. Stewart, J. Domínguez-Robles, R. F. Donnelly, E. Larrañeta, Polymer 2018, 10, 1379;.
S. Talebian, J. Foroughi, S. J. Wade, K. L. Vine, A. Dolatshahi-Pirouz, M. Mehrali, J. Conde, G. G. Wallace, Adv. Mater. 2018, 30, 1706665.
 .
Y. Zhang, J. Yu, H. N. Bomba, Y. Zhu, Z. Gu, Chem. Rev. 2016, 116, 12536-12563;.
W. Zhang, L. Qu, H. Pei, Z. Qin, J. Didier, Z. Wu, F. Bobe, D. E. Ingber, D. A. Weitz, Small 2019, 15, 1903087;.
S. Guo, G. Kang, D. Phan, M. Hsu, Y. Por, C. Chen, Sci. Rep. 2018, 8, 1-10;.
T. Watanabe, I. Motohiro, T. Ono, Langmuir 2019, 35, 2358-2367;.
Q. Liu, M. Zhao, S. Mytnyk, B. Klemm, K. Zhang, Y. Wang, D. Yan, E. Mendes, J. H. van Esch, Angew. Chem. Int. Ed. 2019, 58, 547-551;.
Angew. Chem. 2019, 131, 557-561;.
A. G. Skirtach, B. G. De Geest, A. Mamedov, A. A. Antipov, N. A. Kotov, G. B. Sukhorukov, J. Mater. Chem. 2007, 17, 1050-1054;.
A. M. Pavlov, V. Saez, A. Cobley, J. Graves, G. B. Sukhorukov, T. J. Mason, Soft Matter 2011, 7, 4341-4347;.
J. Chen, S. Ratnayaka, A. Alford, V. Kozlovskaya, F. Liu, B. Xue, K. Hoyt, E. Kharlampieva, ACS Nano 2017, 11, 3135-3146;.
S. Tsirkin, R. Goldbart, T. Traitel, J. Kost, ACS Appl. Mater. Interfaces 2021, 13, 25748-25758;.
M. C. Cochran, J. Eisenbrey, R. O. Ouma, M. Soulen, M. A. Wheatley, Int. J. Pharm. 2011, 414, 161-170;.
N. Huebsch, C. J. Kearney, X. Zhao, J. Kim, C. A. Cezar, Z. Suo, D. J. Mooney, Proc. Natl. Acad. Sci. USA 2014, 111, 9762-9767.
 .
Y. Wang, M. S. Shim, N. S. Levinson, H. W. Sung, Y. Xia, Adv. Funct. Mater. 2014, 24, 4206-4220;.
C. S. Linsley, B. M. Wu, Ther. Delivery 2017, 8, 89-107;.
A. M. Goodman, O. Neumann, K. Nørregaard, L. Henderson, M.-R. Choi, S. E. Clare, N. J. Halas, Proc. Natl. Acad. Sci. USA 2017, 114, 12419-12424.
 .
C. H. Lu, I. Willner, Angew. Chem. Int. Ed. 2015, 54, 12212-12235;.
Angew. Chem. 2015, 127, 12380-12405;.
B. P. Timko, T. Dvir, D. S. Kohane, Adv. Mater. 2010, 22, 4925-4943;.
A. G. Skirtach, A. Muñoz Javier, O. Kreft, K. Köhler, A. Piera Alberola, H. Möhwald, W. J. Parak, G. B. Sukhorukov, Angew. Chem. Int. Ed. 2006, 45, 4612-4617;.
Angew. Chem. 2006, 118, 4728-4733;.
Y. Wang, D. S. Kohane, Nat. Rev. Mater. 2017, 2, 17020.
T. Boissenot, A. Bordat, E. Fattal, N. Tsapis, J. Controlled Release 2016, 241, 144-163.
 .
A. G. Skirtach, P. Karageorgiev, M. F. Bédard, G. B. Sukhorukov, H. Möhwald, J. Am. Chem. Soc. 2008, 130, 11572-11573;.
M. Dang, A. J. Koh, T. Danciu, L. K. McCauley, P. X. Ma, Adv. Healthcare Mater. 2017, 6, 1600901.
K. Scholten, E. Meng, Int. J. Pharm. 2018, 544, 319-334.
 .
R. Vadlapatla, E. Y. Wong, S. G. Gayakwad, J. Drug Delivery Sci. Technol. 2017, 41, 359-366;.
T. Albuquerque, A. R. Neves, T. Quintela, D. Costa, J. Mol. Med. 2021, 1-23;.
A. Potruch, S. T. Khoury, Y. Ilan, Seizure 2020, 0, 0;.
D. W. Kim, E. Zavala, J. K. Kim, Curr. Opin. Syst. Biol. 2020, 0, 0.
R. D. Field, P. N. Anandakumaran, S. K. Sia, Appl. Phys. Rev. 2019, 6, 041305.
 .
J. N. Belling, L. K. Heidenreich, Z. Tian, A. M. Mendoza, T.-T. Chiou, Y. Gong, N. Y. Chen, T. D. Young, N. Wattanatorn, J. H. Park, L. Scarabelli, N. Chiang, J. Takahashi, S. G. Young, A. Z. Stieg, S. De Oliveira, T. J. Huang, P. S. Weiss, S. J. Jonas, Proc. Natl. Acad. Sci. USA 2020, 117, 10976;.
J. Rich, Z. Tian, T. J. Huang, Adv. Mater. Technol. Adv. Mater. Technologies 2022, 7, 2100885.
W. Wang, S. Li, L. Mair, S. Ahmed, T. J. Huang, T. E. Mallouk, Angew. Chem. Int. Ed. 2014, 53, 3201-3204;.
Angew. Chem. 2014, 126, 3265-3268.
P. Zhang, H. Bachman, A. Ozcelik, T. J. Huang, Annu. Rev. Anal. Chem. 2020, 13, 17-43.
A. Y. Rwei, B. Wang, T. Ji, D. S. Kohane, J. Controlled Release 2018, 286, 55-63.
 .
O. Ordeig, S. Y. Chin, S. Kim, P. V. Chitnis, S. K. Sia, Sci. Rep. 2016, 6, 22803;.
G. ter Haar, C. Coussios, Int. J. Hyperthermia 2007, 23, 89-104.
 .
A. A. Atchley, A. Prosperetti, J. Acoust. Soc. Am. 1989, 86, 1065-1084;.
B. M. Borkent, M. Arora, C.-D. Ohl, J. Acoust. Soc. Am. 2007, 121, 1406-1412;.
B. M. Borkent, S. Gekle, A. Prosperetti, D. Lohse, Phys. Fluids 2009, 21, 102003.
 .
I. Lentacker, B. Geers, J. Demeester, S. C. De Smedt, N. N. Sanders, Mol. Ther. 2010, 18, 101-108;.
F. Dong, J. Zhang, K. Wang, Z. Liu, J. Guo, J. Zhang, Nanoscale 2019, 11, 1123-1130;.
E. Stride, C. Coussios, Nat. Rev. Phys. 2019, 1, 495-509.
L. Zhang, L. H. Cai, P. S. Lienemann, T. Rossow, I. Polenz, Q. Vallmajo-Martin, M. Ehrbar, H. Na, D. J. Mooney, D. A. Weitz, Angew. Chem. Int. Ed. 2016, 55, 13470-13474;.
Angew. Chem. 2016, 128, 13668-13672.
 .
B. Y. Zaslavsky, Aqueous two-phase partitioning: physical chemistry and bioanalytical applications, CRC, Boca Raton, 1994;.
R. Hatti-Kaul, Springer, Berlin, 2001;.
A. G. Teixeira, R. Agarwal, K. R. Ko, J. Grant-Burt, B. M. Leung, J. P. Frampton, Adv. Healthcare Mater. 2018, 7, 1701036.
J. J. Kwan, R. Myers, C. M. Coviello, S. M. Graham, A. R. Shah, E. Stride, R. C. Carlisle, C. C. Coussios, Small 2015, 11, 5305-5314.
Q. Liu, M. Zhao, S. Mytnyk, B. Klemm, K. Zhang, Y. Wang, D. Yan, E. Mendes, J. H. van Esch, Angew. Chem. Int. Ed. 2019, 58, 547-551;.
Angew. Chem. 2019, 131, 557-561.
S. Bashir, M. Bashir, J. M. Rees, W. B. J. Zimmerman, BioChip J. 2014, 8, 122-128.
Q. Jin, P. X. Ma, W. V. Giannobile, Adv. Skin Wound Care 2010, 1, 375-381.
I. Leibacher, S. Schatzer, J. Dual, Lab Chip 2014, 14, 463-470.
S. A. Sapareto, W. C. Dewey, Int. J. Radiat. Oncol. Biol. Phys. 1984, 10, 787-800.
 .
M. L. Fabiilli, K. J. Haworth, N. H. Fakhri, O. D. Kripfgans, P. L. Carson, J. B. Fowlkes, IEEE Trans. Sonics Ultrason. 2009, 56, 1006-1017;.
M. Lafond, J.-L. Mestas, F. Prieur, K. Chettab, S. Geraci, P. Clézardin, C. Lafon, Ultrasound Med. Biol. 2016, 42, 220-231;.
C. Coussios, C. Farny, G. Ter Haar, R. Roy, Int. J. Hyperthermia 2007, 23, 105-120.
A. J. Croockewit, P. P. Koopmans, B. E. de Pauw, Clin. Pharmacol. Ther. 1996, 59, 1-6.
G. L. Re, D. A. Santeufemia, F. L. Re, R. Bortolus, P. Doretto, W. Marus, L. Buttazzi, O. Lenardon, A. Falda, R. Piazza, S. Sulfaro, Cytokine 2020, 128, 154984.
 .
S. Chan, L. Rowbottom, R. McDonald, G. A. Bjarnason, M. Tsao, C. Danjoux, E. Barnes, M. Popovic, H. Lam, C. DeAngelis, E. Chow, Clin. Oncol. 2017, 29, 231-238;.
R. C. Hermida, D. E. Ayala, J. R. Fernández, A. Mojón, M. H. Smolensky, Eur. J. Clin. Invest. 2018, 48, e12909.
 .
A. Y. Rwei, J. L. Paris, B. Wang, W. Wang, C. D. Axon, M. Vallet-Regí, R. Langer, D. S. Kohane, Nat. Biomed. Eng. 2017, 1, 644-653;.
S. H. Lee, Y. B. Lee, B. H. Kim, C. Lee, Y. M. Cho, S.-N. Kim, C. G. Park, Y.-C. Cho, Y. B. Choy, Nat. Commun. 2017, 8, 15032.
Y. Song, A. Sauret, H. Cheung Shum, Biomicrofluidics 2013, 7, 061301.
R. M. Ramanan, P. Chellamuthu, L. Tang, K. T. Nguyen, Biotechnol. Prog. 2006, 22, 118-125.
G. Sun, C.-C. Chu, Carbohydr. Polym. 2006, 65, 273-287.
 .
K. Chojnacka-Górka, K. Wolski, S. Zapotoczny, ACS Appl. Mater. Interfaces 2021, 13, 1562-1572;.
S. Ye, C. Wang, X. Liu, Z. Tong, B. Ren, F. Zeng, J. Controlled Release 2006, 112, 79-87.

TL1TR001875 Center for Clinical and Translational Science, Columbia University

Keywords: Drug Delivery; Focused Ultrasound; Microcapsules; Microfluidics; Polymers

0 (Capsules)
0 (Hydrogels)
059QF0KO0R (Water)

Date Created: 20220302 Date Completed: 20220503 Latest Revision: 20220601

20250114

10.1002/anie.202116515

35233907