Photoacoustic Imaging Quantifies Drug Release from Nanocarriers via Redox Chemistry of Dye-Labeled Cargo
Ananthakrishnan Soundaram Jeevarathinam
Department of NanoEngineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093 USA
These authors contributed equally to this work.
Search for more papers by this authorJeanne E. Lemaster
Department of NanoEngineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093 USA
These authors contributed equally to this work.
Search for more papers by this authorFang Chen
Department of NanoEngineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093 USA
Department of Radiology, University of California San Diego, 9500 Gilman Dr., La Jolla, CA, 92093 USA
Current address: Stanford University, USA
Search for more papers by this authorEric Zhao
Department of NanoEngineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093 USA
Search for more papers by this authorCorresponding Author
Assoc. Prof. Jesse V. Jokerst
Department of NanoEngineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093 USA
Materials Science and Engineering Program, University of California San Diego, 9500 Gilman Dr., La Jolla, CA, 92093 USA
Department of Radiology, University of California San Diego, 9500 Gilman Dr., La Jolla, CA, 92093 USA
Search for more papers by this authorAnanthakrishnan Soundaram Jeevarathinam
Department of NanoEngineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093 USA
These authors contributed equally to this work.
Search for more papers by this authorJeanne E. Lemaster
Department of NanoEngineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093 USA
These authors contributed equally to this work.
Search for more papers by this authorFang Chen
Department of NanoEngineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093 USA
Department of Radiology, University of California San Diego, 9500 Gilman Dr., La Jolla, CA, 92093 USA
Current address: Stanford University, USA
Search for more papers by this authorEric Zhao
Department of NanoEngineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093 USA
Search for more papers by this authorCorresponding Author
Assoc. Prof. Jesse V. Jokerst
Department of NanoEngineering, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093 USA
Materials Science and Engineering Program, University of California San Diego, 9500 Gilman Dr., La Jolla, CA, 92093 USA
Department of Radiology, University of California San Diego, 9500 Gilman Dr., La Jolla, CA, 92093 USA
Search for more papers by this authorGraphical Abstract
A covalently linked paclitaxel–methylene blue conjugate (PTX-MB) is used for real-time monitoring of drug release from nanocarriers via photoacoustic imaging. The PTX-MB remained in acoustically silent form when encapsulated in poly(lactic-co-glycolic acid) (PLGA) nanoparticles. After release, PTX-MB instantly oxidized to the photoacoustically active form to report quantity and biodistribution.
Abstract
We report a new approach to monitor drug release from nanocarriers via a paclitaxel–methylene blue conjugate (PTX-MB) with redox activity. This construct is in a photoacoustically silent reduced state inside poly(lactic-co-glycolic acid) (PLGA) nanoparticles (PTX-MB@PLGA NPs). During release, PTX-MB is spontaneously oxidized to produce a concentration-dependent photoacoustic signal. An in vitro drug-release study showed an initial burst release (25 %) between 0–24 h and a sustained release between 24–120 h with a cumulative release of 40.6 % and a 670-fold increase in photoacoustic signal. An in vivo murine drug release showed a photoacoustic signal enhancement of up to 649 % after 10 hours. PTX-MB@PLGA NPs showed an IC50 of 78 μg mL−1 and 44.7±4.8 % decrease of tumor burden in an orthotopic model of colon cancer via luciferase-positive CT26 cells.
Conflict of interest
The authors declare no conflict of interest.
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References
- 1D. Bobo, K. J. Robinson, J. Islam, K. J. Thurecht, S. R. Corrie, Pharm. Res. 2016, 33, 2373–2387.
- 2S. C. White, P. Lorigan, G. P. Margison, J. M. Margison, F. Martin, N. Thatcher, H. Anderson, M. Ranson, Br. J. Cancer 2006, 95, 822–828.
- 3W. R. Sanhai, J. H. Sakamoto, R. Canady, M. Ferrari, Nat. Nanotechnol. 2008, 3, 242.
- 4W. Chen, A. Palazzo, W. E. Hennink, R. J. Kok, Mol. Pharm. 2017, 14, 459–467.
- 5
- 5aW. Chen, C.-A. Cheng, J. I. Zink, ACS Nano 2019, 13, 1292–1308;
- 5bA. E. Dunn, D. J. Dunn, A. Macmillan, R. Whan, T. Stait-Gardner, W. S. Price, M. Lim, C. Boyer, Polym. Chem. 2014, 5, 3311–3315.
- 6
- 6aF. Man, T. Lammers, R. T. M. de Rosales, Mol. Imaging Biol. 2018, 20, 683–695;
- 6bD. Luo, S. Goel, H.-J. Liu, K. A. Carter, D. Jiang, J. Geng, C. J. Kutyreff, J. W. Engle, W.-C. Huang, S. Shao, C. Fang, W. Cai, J. F. Lovell, ACS Nano 2017, 11, 12482–12491.
- 7
- 7aS. S. Liow, Q. Dou, D. Kai, Z. Li, S. Sugiarto, C. Y. Y. Yu, R. T. K. Kwok, X. Chen, Y.-L. Wu, S. T. Ong, A. Kizhakeyil, N. K. Verma, B. Z. Tang, X. J. Loh, Small 2017, 13, 1603404;
- 7bJ. Liu, J. Bu, W. Bu, S. Zhang, L. Pan, W. Fan, F. Chen, L. Zhou, W. Peng, K. Zhao, J. Du, J. Shi, Angew. Chem. Int. Ed. 2014, 53, 4551–4555; Angew. Chem. 2014, 126, 4639–4643.
- 8C. L. Bayer, G. P. Luke, S. Y. Emelianov, Acoust. Today 2012, 8, 15–23.
- 9Y. Zhang, M. Jeon, L. J. Rich, H. Hong, J. Geng, Y. Zhang, S. Shi, T. E. Barnhart, P. Alexandridis, J. D. Huizinga, M. Seshadri, W. Cai, C. Kim, J. F. Lovell, Nat. Nanotechnol. 2014, 9, 631.
- 10
- 10aY. Zhang, J. Yu, R. A. Kahkoska, Z. Gu, Sensors 2017, 17, 17061400;
- 10bX. Jun, K. Chulhong, F. L. Jonathan, Curr. Drug Targets 2015, 16, 571–581.
- 11
- 11aX. Li, M. Bottini, L. Zhang, S. Zhang, J. Chen, T. Zhang, L. Liu, N. Rosato, X. Ma, X. Shi, Y. Wu, W. Guo, X.-J. Liang, ACS Nano 2019, 13, 176–186;
- 11bN. Bhutiani, A. Samykutty, K. M. McMasters, N. K. Egilmez, L. R. McNally, Photoacoustics 2019, 13, 46–52.
- 12T. Limpanuparb, P. Roongruangsree, C. Areekul, R. Soc. Open Sci. 2017, 4, 170708.
- 13N. Murakami, H. Maruno, RSC Adv. 2016, 6, 65518–65523.
- 14R. Wang, L. Zhou, W. Wang, X. Li, F. Zhang, Nat. Commun. 2017, 8, 14702.
- 15
- 15aM. H. Cohen, J. Gootenberg, P. Keegan, R. Pazdur, Oncologist 2007, 12, 713–718;
- 15bT. M. Baran, B. R. Giesselman, R. Hu, M. A. Biel, T. H. Foster, Lasers Surg. Med. 2010, 42, 728–735.
- 16
- 16aY. Gao, Y. Kuang, Z.-F. Guo, Z. Guo, I. J. Krauss, B. Xu, J. Am. Chem. Soc. 2009, 131, 13576–13577;
- 16bH. M. Deutsch, J. A. Glinski, M. Hernandez, R. D. Haugwitz, V. L. Narayanan, M. Suffness, L. H. Zalkow, J. Med. Chem. 1989, 32, 788–792.
- 17D. G. I. Kingston, D. R. Hawkins, L. Ovington, J. Nat. Prod. 1982, 45, 466–470.
- 18A. Felgentraeger, T. Maisch, D. Dobler, A. Spaeth, BioMed Res. Int. 2013, 482167, 482112 pp.
- 19P.-C. Chiang, S. Gould, M. Nannini, A. Qin, Y. Deng, A. Arrazate, K. R. Kam, Y. Ran, H. Wong, Nanoscale Res. Lett. 2014, 9, 156–156.
- 20J. Wang, A. S. Jeevarathinam, K. Humphries, A. Jhunjhunwala, F. Chen, A. Hariri, B. R. Miller, J. V. Jokerst, Bioconjugate Chem. 2018, 29, 3768–3775.
- 21
- 21aC. Dollendorf, M. Hetzer, H. Ritter, Beilstein J. Org. Chem. 2013, 9, 1652–1662;
- 21bT. Snehalatha, K. C. Rajanna, P. K. Saiprakash, J. Chem. Educ. 1997, 74, 228.
- 22Y. Galagan, W.-F. Su, J. Photochem. Photobiol. A 2008, 195, 378–383.
- 23
- 23aS. S. Dhapare, A. K. Dash, Ther. Delivery 2015, 6, 27–39;
- 23bB. Michen, C. Geers, D. Vanhecke, C. Endes, B. Rothen-Rutishauser, S. Balog, A. Petri-Fink, Sci. Rep. 2015, 5, 9793.
- 24K. Buchholz, R. H. Schirmer, J. K. Eubel, M. B. Akoachere, T. Dandekar, K. Becker, S. Gromer, Antimicrob. Agents Chemother. 2008, 52, 183–191.
- 25A. Hariri, E. Zhao, A. S. Jeevarathinam, J. Lemaster, J. Zhang, J. V. Jokerst, Sci. Rep. 2019, 9, 11378.
- 26L. Vicari, T. Musumeci, I. Giannone, L. Adamo, C. Conticello, R. De Maria, R. Pignatello, G. Puglisi, M. Gulisano, BMC Cancer 2008, 8, 212.
- 27G. Li, J. Liu, Y. Pang, R. Wang, L. Mao, D. Yan, X. Zhu, J. Sun, Biomacromolecules 2011, 12, 2016–2026.
- 28C. Fonseca, S. Simoes, R. Gaspar, J. Controlled Release 2002, 83, 273–286.
- 29A. Cabanes, K. E. Briggs, P. C. Gokhale, J. Treat, A. Rahman, Int. J. Oncol. 1998, 12, 1035–1075.
- 30
- 30aT.-S. Hsieh, J.-Y. Wu, C.-C. Chang, Dyes Pigm. 2015, 112, 34–41;
- 30bT.-S. Hsieh, J.-Y. Wu, C.-C. Chang, Chem. Eur. J. 2014, 20, 9709–9715.
- 31J. E. Lemaster, F. Chen, T. Kim, A. Hariri, J. V. Jokerst, ACS Appl. Nano Mater. 2018, 1, 1321–1331.
