journal article·2016-09Open access

Magnetic nanoparticle-promoted droplet vaporization for in vivo stimuli-responsive cancer theranostics

Yang Zhou, Ronghui Wang, Zhaogang Teng, Zhigang Wang, Bing Hu, Michael Kolios, Hangrong Chen, Nan Zhang, Yanjie Wang, Pan Li, Xing Wu, Guangming Lu, Yu Chen, Yuanyi Zheng

NPG Asia Materials· Volume 8· Issue 9

Abstract

The development of efficient strategies for in vivo stimuli-responsive cancer treatment and personalized biomedicine is a great challenge. To overcome the critical issues and limitations of traditional protocols using acoustic droplet vaporization and optical droplet vaporization in stimuli-responsive tumor treatment, we herein report a new strategy, magnetic droplet vaporization (MDV), based on nanobiotechnology, for efficient magnetic field-responsive cancer theranostics. Perfluorohexane (PFH)-encapsulated superparamagnetic hollow iron oxide nanoparticles with a high magnetic-thermal energy transfer capability quickly respond to an external alternating current (a.c.) magnetic field to produce thermal energy and raise the temperature of the surrounding tumor tissue. The encapsulated PFH, with a desirable boiling point of ~56 °C, can be vaporized to enhance the performance of ultrasound imaging of tumors, as systematically demonstrated both in vitro and in vivo. The magnetic–thermal energy transfer further ablated and removed tumors in mice tumor xenograft models. This unique MDV principle with high versatility and performance is expected to broaden the biomedical applications of nanotechnology and promote clinical translations of intelligent diagnostic and therapeutic modalities, especially for battling cancer. Hollow iron nanoparticles can enhance both the imaging and complete removal of tumours in live mice using magnetically simulated heat. Ultrasound molecular imaging is one of the safest ways to track cancerous cell growth, but its success depends on producing gas-filled microbubbles that attach to the targeted tissue. As an alternative to optical or acoustic microbubble generators, Yu Chen from the Shanghai Institute of Ceramics, Yuanyi Zheng from Shanghai Sixth People's Hospital and colleagues have used superparamagnetic iron oxide probes with an encapsulated, low-boiling-point gas inside their nanoshells. After injecting the probes into breast cancer cells, the team applied a non-intrusive alternating-current magnetic field. This stimulus generated thermal energy that raised tissue temperature slightly, releasing numerous microbubbles through vapourization. The ultrasound-guided probes could then heat tumours sufficiently to stop regrowth using longer field exposure times. A novel magnetic droplet vaporization strategy was developed for efficient magnetic field-responsive cancer theranostics. Perfluorohexane (PFH)-encapsulated superparamagnetic hollow iron oxide nanoparticles with high magnetic-thermal energy transfer capability quickly respond to external alternating current (a.c.) magnetic field to produce thermal energy and raise the surrounding temperature of tumor tissue. The encapsulated PFH with desirable boiling point of about 56 °C can be vaporized to enhance the ultrasound imaging performance for responsive imaging. Such a magnetic–thermal energy transfer can further completely ablate and remove the tumor against a mice tumor xenograft model.
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Research context

OpenAlex topics: Nanoparticle-Based Drug Delivery · Nanoplatforms for cancer theranostics · Radiation Therapy and Dosimetry

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (45)

Show source-provided references
1. Wagner, V., Dullaart, A., Bock, A. K. & Zweck, A. The emerging nanomedicine landscape. Nat. Biotechnol. 24, 1211–1217 (2006).10.1038/nbt1006-1211 ↗
2. Piao, Y., Kim, J., Na, H. B., Kim, D., Baek, J.S., Ko, M.K., Lee, J. H., Shokouhimehr, M. & Hyeon, T. Wrap-bake-peel process for nanostructural transformation from beta-FeOOH nanorods to biocompatible iron oxide nanocapsules. Nat. Mater. 7, 242–247 (2008).10.1038/nmat2118 ↗
3. Medarova, Z., Pham, W., Farrar, C., Petkova, V. & Moore, A. In vivo imaging of siRNA delivery and silencing in tumors. Nat. Med. 13, 372–377 (2007).10.1038/nm1486 ↗
4. Peer, D., Karp, J. M., Hong, S., Farokhzad, O. C., Margalit, R. & Langer, R. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2, 751–760 (2007).10.1038/nnano.2007.387 ↗
5. Allen, T. M. & Cullis, P. R. Drug delivery systems: entering the mainstream. Science 303, 1818–1822 (2004).10.1126/science.1095833 ↗
6. Chen, Y., Chen, H. & Shi, J. In vivo bio-safety evaluations and diagnostic/therapeutic applications of chemically designed mesoporous silica nanoparticles. Adv. Mater. 25, 3144–3176 (2013).10.1002/adma.201205292 ↗
7. Ferrari, M. Cancer nanotechnology: opportunities and challenges. Nat. Rev. Cancer 5, 161–171 (2005).10.1038/nrc1566 ↗
8. Chen, Y., Chen, H. & Shi, J. Inorganic nanoparticle-based drug codelivery nanosystems to overcome the multidrug resistance of cancer cells. Mol. Pharm. 11, 2495–2510 (2013).10.1021/mp400596v ↗
9. Lee, N., Choi, S. H., Hyeon, T. & Nano-Sized, CT Contrast agents. Adv. Mater. 25, 2641–2660 (2013).10.1002/adma.201300081 ↗
10. Lee, J. E., Lee, N., Kim, T., Kim, J. & Hyeon, T. Multifunctional mesoporous silica nanocomposite nanoparticles for theranostic applications. Acc. Chem. Res. 44, 893–902 (2011).10.1021/ar2000259 ↗
11. Na, H. B., Song, I. C. & Hyeon, T. Inorganic nanoparticles for MRI contrast agents. Adv. Mater. 21, 2133–2148 (2009).10.1002/adma.200802366 ↗
12. Lee, N. & Hyeon, T. Designed synthesis of uniformly sized iron oxide nanoparticles for efficient magnetic resonance imaging contrast agents. Chem. Soc. Rev. 41, 2575–2589 (2012).10.1039/C1CS15248C ↗
13. Kang, E., Min, H. S., Lee, J., Han, M.H., Ahn, H. J., Yoon, I. C., Choi, K., Kim, K., Park, K. & Kwon, I. C. Nanobubbles from gas-generating polymeric nanoparticles: ultrasound imaging of living subjects. Angew. Chem. Int. Ed. 49, 524–528 (2010).10.1002/anie.200903841 ↗
14. Schutt, E. G., Klein, D. H., Mattrey, R. M. & Riess, J. G. Injectable microbubbles as contrast agents for diagnostic ultrasound imaging: the key role of perfluorochemicals. Angew. Chem. Int. Ed. 42, 3218–3235 (2003).10.1002/anie.200200550 ↗
15. Chen, Y., Chen, H. & Shi, J. Nanobiotechnology promotes noninvasive high-intensity focused ultrasound cancer surgery. Adv. Healtc. Mater. 4, 158–165 (2015).10.1002/adhm.201400127 ↗
16. Zhou, Y., Wang, Z., Chen, Y., Shen, H ., Luo, Z., Li, A., Wang, Q., Ran, H., Li, P., Song, W., Yang, Z., Chen, H., Wang, Z., Lu, G. & Zheng, Y. Microbubbles from gas-generating perfluorohexane nanoemulsions for targeted temperature-sensitive ultrasonography and synergistic HIFU ablation of tumors. Adv. Mater. 25, 4123–4130 (2013).10.1002/adma.201301655 ↗
17. Wang, X., Chen, H., Zheng, Y., Ma, M., Chen, Y., Zhang, K., Zeng, D. & Shi, J. Au-nanoparticle coated mesoporous silica nanocapsule-based multifunctional platform for ultrasound mediated imaging, cytoclasis and tumor ablation. Biomaterials 34, 2057–2068 (2013).10.1016/j.biomaterials.2012.11.044 ↗
18. Shpak, O., Verweij, M., Vos, H. J., de Jong, N., Lohse, D. & Versluis, M. Acoustic droplet vaporization is initiated by superharmonic focusing. Proc. Natl Acad. Sci. USA 111, 1697–1702 (2014).10.1073/pnas.1312171111 ↗
19. Kagan, D., Benchimol, M.J., Claussen, J.C., Chuluun-Erdene, E., Esener, S. & Wang, J. Acoustic droplet vaporization and propulsion of perfluorocarbon-loaded microbullets for targeted tissue penetration and deformation. Angew. Chem. Int. Ed. 51, 7519–7522 (2012).10.1002/anie.201201902 ↗
20. Kang, S.-T. & Yeh, C.-K. Intracellular acoustic droplet vaporization in a single peritoneal macrophage for drug delivery applications. Langmuir 27, 13183–13188 (2011).10.1021/la203212p ↗
21. Strohm, E., Rui, M., Gorelikov, I., Matsuura, N. & Kolios, M. Vaporization of perfluorocarbon droplets using optical irradiation. Biomed. Opt. Express 2, 1432–1442 (2011).10.1364/BOE.2.001432 ↗
22. Jian, J., Liu, C., Gong, Y., Su, L., Zhang, B., Wang, Z., Wang, D., Zhou, Y., Xu, F., Li, P., Zheng, Y., Song, L. & Zhou, X. India ink incorporated multifunctional phase-transition nanodroplets for photoacoustic/ultrasound dual-modality imaging and photoacoustic effect based tumor therapy. Theranostics 4, 1026–1038 (2014).10.7150/thno.9754 ↗
23. Sun, Y., Wang, Y., Niu, C., Strohm, E. M., Zheng, Y., Ran, H., Huang, R., Zhou, D., Gong, Y., Wang, Z., Wang, D. & Michael, C. K. Laser-activatible PLGA microparticles for image-guided cancer therapy in vivo. Adv. Funct. Mater. 24, 7674–7680 (2014).10.1002/adfm.201402631 ↗
24. Lee, J. H., Jang, J. T., Choi, J. S, Moo, S. H., Noh, S. H., Kim, J. W., Kim, J. G., Kim, I.S., Park, K.I. & Cheon, J. Exchange-coupled magnetic nanoparticles for efficient heat induction. Nat. Nanotechnol. 6, 418–422 (2011).10.1038/nnano.2011.95 ↗
25. Chen, Y., Jiang, L., Wang, R., Lu, M., Zhang, Q., Zhou, Y., Wang, Z., Lu, G., Liang, P., Ran, H., Chen, H. & Zheng, Y. Injectable smart phase-transformation implants for highly efficient in vivo magnetic-hyperthermia regression of tumors. Adv. Mater. 26, 7468–7473 (2104).10.1002/adma.201402509 ↗
26. Chen, Y., Chen, H., Sun, Y., Zheng, Y., Zeng, D, Li, F., Zhang, S., Wang, X., Zhang, K., Ma, M., He, Q., Zhang, L. & Shi, J. Multifunctional mesoporous composite nanocapsules for highly efficient MRI-guided high-intensity focused ultrasound cancer surgery. Angew. Chem. Int. Ed. 50, 12505–12509 (2011).10.1002/anie.201106180 ↗
27. Sun, Y., Zheng, Y., Ran, H., Zhou, Y., Shen, H., Chen, Y., Chen, H., Krupka, T. M., Li, A., Li, P., Wang, Z. & Wang, Z. Superparamagnetic PLGA-iron oxide microcapsules for dual-modality US/MR imaging and high intensity focused US breast cancer ablation. Biomaterials 33, 5854–5864 (2012).10.1016/j.biomaterials.2012.04.062 ↗
28. Gao, Z., Kennedy, A. M., Christensen, D. A. & Rapoport, N. Y. Drug-loaded nano/microbubbles for combining ultrasonography and targeted chemotherapy. Ultrasonics 48, 260–270 (2008).10.1016/j.ultras.2007.11.002 ↗
29. Rapoport, N. Y., Efros, A. L., Christensen, D. A., Kennedy, A. M. & Nam, K. H. Microbubble generation in phase-shift nanoemulsions used as anticancer drug carriers. Bubble Sci. Eng. Technol. 1, 31–39 (2009).10.1179/175889709X446516 ↗
30. Oeffinger, B. E. & Wheatley, M. A. Development and characterization of a nano-scale contrast agent. Ultrasonics 42, 343–347 (2004).10.1016/j.ultras.2003.11.011 ↗
31. Luo, B, Xu, S., Ma, W., Wang, W., Wang, S., Guo, J., Yang, W., Hu, J. & Wang, C. Fabrication of magnetite hollow porous nanocrystal shells as a drug carrier for paclitaxel. J. Mater. Chem. 20, 7107–7113 (2010).10.1039/c0jm00726a ↗
32. Wang, X., Chen, H., Chen, Y., Ma, M., Zhang, K., Li, F., Zheng, Y., Zeng, D., Wang, Q. & Shi, J Perfluorohexane-encapsulated mesoporous silica nanocapsules as enhancement agents for highly efficient high intensity focused ultrasound (HIFU). Adv. Mater. 24, 785–791 (2012).10.1002/adma.201104033 ↗
33. Wang, Y., Shim, M. S., Levinson, N. S., Sung, H.-W. & Xia, Y. Stimuli-responsive materials for controlled release of theranostic agents. Adv. Funct. Mater. 24, 4206–4220 (2014).10.1002/adfm.201400279 ↗
34. Chen, Y., Ye, D., Wu, M., Chen, H., Zhang, L., Shi, J. & Wang, L. Break-up of two-dimensional MnO2 nanosheets promotes ultrasensitive pH-triggered theranostics of cancer. Adv. Mater. 26, 7019–7026 (2014).10.1002/adma.201402572 ↗
35. Chen, Y., Meng, Q., Wu, M., Wang, S., Xu, P., Chen, H., Li, Y., Zhang, L., Wang, L. & Shi, J Hollow mesoporous organosilica nanoparticles: a generic intelligent framework-hybridization approach for biomedicine. J. Am. Chem. Soc. 136, 16326–16334 (2014).10.1021/ja508721y ↗
36. Patel, K., Angelos, S., Dichtel, W. R., Coskun, A., Yang, Y. W., Zink, J. I. & Stoddart, J. F. Enzyme-responsive snap-top covered silica nanocontainers. J. Am. Chem. Soc. 130, 2382–2383 (2008).10.1021/ja0772086 ↗
37. Liu, T., Wang, C., Gu, X., Gong, H., Cheng, L., Shi, X., Feng, L., Sun, B . & Liu, Z Drug delivery with PEGylated MoS2 nano-sheets for combined photothermal and chemotherapy of cancer. Adv. Mater. 26, 3433–3440 (2014).10.1002/adma.201305256 ↗
38. Ma., M., Xu, H., Chen, H., Jia, X., Zhang, K., Wang, Q., Zheng, S., Wu, R., Yao, M., Cai, X., Li, F. & Shi, J. A drug–perfluorocarbon nanoemulsion with an ultrathin silica coating for the synergistic effect of chemotherapy and ablation by high-intensity focused ultrasound. Adv. Mater. 26, 7378–7385 (2014).10.1002/adma.201402969 ↗
39. Yu, J., Ju, Y., Zhao, L., Chu, X., Yang, W., Tian, Y., Sheng, F., Lin, J., Liu, F., Dong, Y. & Hou, Y. Multistimuli-regulated photochemothermal cancer therapy remotely controlled via Fe5C2 nanoparticles. ACS Nano 10, 159–169 (2015).10.1021/acsnano.5b04706 ↗
40. Shin, J., Anisur, R. M., Ko, M. K., Im, G. H., Lee, J. H. & Lee, I. S. Hollow manganese phosphate nanoparticles as smart multifunctional probes for cancer cell targeted magnetic resonance imaging and drug delivery. Nano Res. 5, 679–694 (2012).10.1007/s12274-012-0252-z ↗
41. Yang, C., Wu, J. & Hou, Y. Fe3O4 nanostructures: synthesis, growth mechanism, properties and applications. Chem. Commun. 47, 5130–5141 (2011).10.1039/c0cc05862a ↗
42. Yu, J., Chu, X. & Hou, Y. Stimuli-responsive cancer therapy based on nanoparticles. Chem. Commun. 50, 11614–11630 (2014).10.1039/C4CC03984J ↗
43. Yu, J,. Yang, C., Li, J., Ding, Y., Zhang, L., Yousaf, M. Z., Lin, J., Pang, R., Wei, L., Xu, L., Sheng, F., Li, C., Li, G., Zhao, L. & Hou, Y. Multifunctional Fe5C2 nanoparticles: a targeted theranostic platform for magnetic resonance imaging and photoacoustic tomography‐guided photothermal therapy. Adv. Mater. 26, 4114–4120 (2014).10.1002/adma.201305811 ↗
44. Fabiilli, M. L., Lee, J. A., Kripfgans, O. D., Carson, P. L. & Fowlkes, J. B. Delivery of water-soluble drugs using acoustically triggered perfluorocarbon double emulsions. Pharm. Res. 27, 2753–2765 (2010).10.1007/s11095-010-0277-5 ↗
45. Zhang, M., Fabiilli, M., Carson, P., Padilla, F., Swanson, S., Kripfgans, O. & Fowlkes, B. Acoustic droplet vaporization for enhancement of thermal ablation by high intensity focused ultrasound. Acad. Radiol. 18, 1123–1132 (2011).10.1016/j.acra.2011.04.012 ↗