Skip to main content
Log in

Sonodynamic therapy (SDT): a novel strategy for cancer nanotheranostics

  • Review
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Sonodynamic therapy (SDT) is a promising non-invasive therapeutic modality. Compared to photo-inspired therapy, SDT provides many opportunities and benefits, including deeper tissue penetration, high precision, less side effects, and good patient compliance. Thanks to the facile engineerable nature of nanotechnology, nanoparticles-based sonosensitizers exhibit predominant advantages, such as increased SDT efficacy, binding avidity, and targeting specificity. This review aims to summarize the possible mechanisms of SDT, which can be expected to provide the theoretical basis for SDT development in the future. We also extensively discuss nanoparticle-assisted sonosensitizers to enhance the outcome of SDT. Additionally, we focus on the potential strategy of combinational SDT with other therapeutic modalities and discuss the limitations and challenges of SDT toward clinical applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alekseev, S., Korytko, D., Iazykov, M., Khainakov, S., and Lysenko, V. (2015). Electrochemical synthesis of carbon fluorooxide nanoparticles from 3C-SiC substrates. J Phys Chem C 119, 20503–20514.

    Article  CAS  Google Scholar 

  • Ando, H., Feril Jr., L.B., Kondo, T., Tabuchi, Y., Ogawa, R., Zhao, Q.L., Cui, Z.G., Umemura, S., Yoshikawa, H., and Misaki, T. (2006). An echo-contrast agent, Levovist, lowers the ultrasound intensity required to induce apoptosis of human leukemia cells. Cancer Lett 242, 37–45.

    Article  CAS  PubMed  Google Scholar 

  • Ashush, H., Rozenszajn, L.A., Blass, M., Barda-Saad, M., Azimov, D., Radnay, J., Zipori, D., and Rosenschein, U. (2000). Apoptosis induction of human myeloid leukemic cells by ultrasound exposure. Cancer Res 60, 1014–1020.

    CAS  PubMed  Google Scholar 

  • Bai, W.K., Shen, E., and Hu, B. (2012). Induction of the apoptosis of cancer cell by sonodynamic therapy: a review. Chin J Cancer Res 24, 368–373.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bertrand, N., Wu, J., Xu, X., Kamaly, N., and Farokhzad, O.C. (2014). Cancer nanotechnology: the impact of passive and active targeting in the era of modern cancer biology. Adv Drug Deliver Rev 66, 2–25.

    Article  CAS  Google Scholar 

  • Canaparo, R., Varchi, G., Ballestri, M., Foglietta, F., Sotgiu, G., Guerrini, A., Francovich, A., Civera, P., Frairia, R., and Serpe, L. (2013). Polymeric nanoparticles enhance the sonodynamic activity of meso-tetrakis (4-sulfonatophenyl) porphyrin in an in vitro neuroblastoma model. Int J Nanomed 8, 4247–4263.

    Google Scholar 

  • Chen, H., Zhou, X., Gao, Y., Zheng, B., Tang, F., and Huang, J. (2014). Recent progress in development of new sonosensitizers for sonodynamic cancer therapy. Drug Discov Today 19, 502–509.

    Article  CAS  PubMed  Google Scholar 

  • Chen, M.J., Xu, A., He, W., Ma, W., and Shen, S. (2017). Ultrasound triggered drug delivery for mitochondria targeted sonodynamic therapy. J Drug Deliver Sci Tech 39, 501–507.

    Article  CAS  Google Scholar 

  • Chen, W.S., Brayman, A.A., Matula, T.J., Crum, L.A., and Miller, M.W. (2003). The pulse length-dependence of inertial cavitation dose and hemolysis. Ultrasound Med Biol 29, 739–748.

    Article  PubMed  Google Scholar 

  • Chen, Y.W., Liu, T.Y., Chang, P.H., Hsu, P.H., Liu, H.L., Lin, H.C., and Chen, S.Y. (2016). A theranostic nrGO@MSN-ION nanocarrier developed to enhance the combination effect of sonodynamic therapy and ultrasound hyperthermia for treating tumor. Nanoscale 8, 12648–12657.

    Article  CAS  PubMed  Google Scholar 

  • Cheng, L., Wang, C., Feng, L., Yang, K., and Liu, Z. (2014). Functional nanomaterials for phototherapies of cancer. Chem Rev 114, 10869–10939.

    Article  CAS  PubMed  Google Scholar 

  • Dai, C., Zhang, S., Liu, Z., Wu, R., and Chen, Y. (2017). Two-dimensional graphene augments nanosonosensitized sonocatalytic tumor eradication. ACS Nano 11, 9467–9480.

    Article  CAS  PubMed  Google Scholar 

  • Deepagan, V.G., You, D.G., Um, W., Ko, H., Kwon, S., Choi, K.Y., Yi, G. R., Lee, J.Y., Lee, D.S., Kim, K., et al. (2016). Long-circulating Au- TiO2 nanocomposite as a sonosensitizer for ROS-mediated eradication of cancer. Nano Lett 16, 6257–6264.

    Article  CAS  PubMed  Google Scholar 

  • Ding, Y., Song, Z., Liu, Q., Wei, S., Zhou, L., Zhou, J., and Shen, J. (2017). An enhanced chemotherapeutic effect facilitated by sonication of MSN. Dalton Trans 46, 11875–11883.

    Article  CAS  PubMed  Google Scholar 

  • Duvshani-Eshet, M., Benny, O., Morgenstern, A., and Machluf, M. (2007). Therapeutic ultrasound facilitates antiangiogenic gene delivery and inhibits prostate tumor growth. Mol Cancer Therapeut 6, 2371–2382.

    Article  CAS  Google Scholar 

  • Escoffre, J.M., Zeghimi, A., Novell, A., and Bouakaz, A. (2013). In-vivo gene delivery by sonoporation: recent progress and prospects. Curr Gene Ther 13, 2–14.

    Article  CAS  PubMed  Google Scholar 

  • Fan, C.H., Ting, C.Y., Lin, H.J., Wang, C.H., Liu, H.L., Yen, T.C., and Yeh, C.K. (2013). SPIO-conjugated, doxorubicin-loaded microbubbles for concurrent MRI and focused-ultrasound enhanced brain-tumor drug delivery. Biomaterials 34, 3706–3715.

    Article  CAS  PubMed  Google Scholar 

  • Feril, L.B.Jr., Kondo, T., Ogawa, R., and Zhao, Q.L. (2003a). Dose-dependent inhibition of ultrasound-induced cell killing and free radical production by carbon dioxide. Ultrasons Sonochem 10, 81–84.

    Article  CAS  Google Scholar 

  • Feril, L.B.Jr., Kondo, T., Zhao, Q.L., Ogawa, R., Tachibana, K., Kudo, N., Fujimoto, S., and Nakamura, S. (2003b). Enhancement of ultrasoundinduced apoptosis and cell lysis by echo-contrast agents. Ultrasound Med Biol 29, 331–337.

    Article  PubMed  Google Scholar 

  • Feril, L.B., Tsuda, Y., Kondo, T., Zhao, Q.L., Ogawa, R., Cui, Z.G., Tsukada, K., and Riesz, P. (2004b). Ultrasound-induced killing of monocytic U937 cells enhanced by 2,2′-azobis(2-amidinopropane) dihydrochloride. Cancer Sci 95, 181–185.

    Article  CAS  PubMed  Google Scholar 

  • Feril, L.B.Jr., Kondo, T., Takaya, K., and Riesz, P. (2004a). Enhanced ultrasound-induced apoptosis and cell lysis by a hypotonic medium. Int J Radiat Biol 80, 165–175.

    Article  CAS  PubMed  Google Scholar 

  • Gordon, M.S., Mendelson, D.S., and Kato, G. (2010). Tumor angiogenesis and novel antiangiogenic strategies. Int J Cancer 126, 1777–1787.

    Article  CAS  PubMed  Google Scholar 

  • Grüll, H., and Langereis, S. (2012). Hyperthermia-triggered drug delivery from temperature-sensitive liposomes using MRI-guided high intensity focused ultrasound. J Control Release 161, 317–327.

    Article  PubMed  CAS  Google Scholar 

  • Harada, A., Ono, M., Yuba, E., and Kono, K. (2013). Titanium dioxide nanoparticle-entrapped polyion complex micelles generate singlet oxygen in the cells by ultrasound irradiation for sonodynamic therapy. Biomater Sci 1, 65–73.

    Article  CAS  PubMed  Google Scholar 

  • Harada, Y., Ogawa, K., Irie, Y., Endo, H., Feril Jr., L.B., Uemura, T., and Tachibana, K. (2011). Ultrasound activation of TiO2 in melanoma tumors. J Control Release 149, 190–195.

    Article  CAS  PubMed  Google Scholar 

  • Harrison, G.H., Balcer-Kubiczek, E.K., and Gutierrez, P.L. (1996). In vitro mechanisms of chemopotentiation by tone-burst ultrasound. Ultrasound Med Biol 22, 355–362.

    Article  CAS  PubMed  Google Scholar 

  • Huang, P., Qian, X., Chen, Y., Yu, L., Lin, H., Wang, L., Zhu, Y., and Shi, J. (2017). Metalloporphyrin-encapsulated biodegradable nanosystems for highly efficient magnetic resonance imaging-guided sonodynamic cancer therapy. J Am Chem Soc 139, 1275–1284.

    Article  CAS  PubMed  Google Scholar 

  • Huang, Z., Moseley, H., and Bown, S. (2010). Rationale of combined PDT and SDT modalities for treating cancer patients in terminal stage: the proper use of photosensitizer. Integr Cancer Ther 9, 317–319.

    Article  PubMed  Google Scholar 

  • Hutcheson, J.D., Schlicher, R.K., Hicks, H.K., and Prausnitz, M.R. (2010). Saving cells from ultrasound-induced apoptosis: quantification of cell death and uptake following sonication and effects of targeted calcium chelation. Ultrasound Med Biol 36, 1008–1021.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang, J.H., Brayman, A.A., Reidy, M.A., Matula, T.J., Kimmey, M.B., and Crum, L.A. (2005). Vascular effects induced by combined 1-MHz ultrasound and microbubble contrast agent treatments in vivo. Ultrasound Med Biol 31, 553–564.

    Article  PubMed  Google Scholar 

  • Inui, T., Makita, K., Miura, H., Matsuda, A., Kuchiike, D., Kubo, K., Mette, M., Uto, Y., Nishikata, T., and Hori, H. (2014). Case report: a breast cancer patient treated with GcMAF, sonodynamic therapy and hormone therapy. Anticancer Res 34, 4589–4593.

    PubMed  Google Scholar 

  • Jia, G., Wang, H., Yan, L., Wang, X., Pei, R., Yan, T., Zhao, Y., and Guo, X. (2005). Cytotoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube, and fullerene. Environ Sci Technol 39, 1378–13–83.

    Google Scholar 

  • Jin, Z., Miyoshi, N., Ishiguro, K., Umemura, S., Kawabata, K., Yumita, N., Sakata, I., Takaoka, K., Udagawa, T., Nakajima, S., et al. (2000). Combination effect of photodynamic and sonodynamic therapy on experimental skin squamous cell carcinoma in C3H/HeN mice. J Dermatol 27, 294–306.

    Article  CAS  PubMed  Google Scholar 

  • Juffermans, L.J.M., Dijkmans, P.A., Musters, R.J.P., Visser, C.A., and Kamp, O. (2006). Transient permeabilization of cell membranes by ultrasound- exposed microbubbles is related to formation of hydrogen peroxide. Am J Physiol Heart Circ Physiol 291, H1595–H1601.

    Article  CAS  PubMed  Google Scholar 

  • Konan, Y.N., Gurny, R., and Allémann, E. (2002). State of the art in the delivery of photosensitizers for photodynamic therapy. J Photochem Photobiol B 66, 89–106.

    Article  CAS  PubMed  Google Scholar 

  • Konofagou, E.E. (2012). Optimization of the ultrasound-induced bloodbrain barrier opening. Theranostics 2, 1223–1237.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotopoulis, S., Dimcevski, G., Helge Gilja, O., Hoem, D., and Postema, M. (2013). Treatment of human pancreatic cancer using combined ultrasound, microbubbles, and gemcitabine: a clinical case study. Med Phys 40, 072902.

    Article  PubMed  CAS  Google Scholar 

  • Kumon, R.E., Aehle, M., Sabens, D., Parikh, P., Han, Y.W., Kourennyi, D., and Deng, C.X. (2009). Spatiotemporal effects of sonoporation measured by real-time calcium imaging. Ultrasound Med Biol 35, 494–506.

    Article  CAS  PubMed  Google Scholar 

  • Lagneaux, L., de Meulenaer, E.C., Delforge, A., Dejeneffe, M., Massy, M., Moerman, C., Hannecart, B., Canivet, Y., Lepeltier, M.F., and Bron, D. (2002). Ultrasonic low-energy treatment. Exp Hematol 30, 1293–1301.

    Article  PubMed  Google Scholar 

  • Li, S.Q., Zhu, R.R., Zhu, H., Xue, M., Sun, X.Y., Yao, S.D., and Wang, S.L. (2008). Nanotoxicity of TiO2 nanoparticles to erythrocyte in vitro. Food Chem Toxicol 46, 3626–3631.

    Article  CAS  PubMed  Google Scholar 

  • Liu, R., Zhang, Q., Lang, Y., Peng, Z., and Li, L. (2017). Sonodynamic therapy, a treatment developing from photodynamic therapy. Photodiagnosis Photodynamic Ther 19, 159–166.

    Article  Google Scholar 

  • Madanshetty, S.I., and Apfel, R.E. (1991). Acoustic microcavitation: enhancement and applications. J Acoust Soc Am 90, 1508–1514.

    Article  CAS  PubMed  Google Scholar 

  • Mano, S.S., Kanehira, K., Sonezaki, S., and Taniguchi, A. (2012). Effect of polyethylene glycol modification of TiO2 nanoparticles on cytotoxicity and gene expressions in human cell lines. Int J Mol Sci 13, 3703–3717.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDannold, N., Arvanitis, C.D., Vykhodtseva, N., and Livingstone, M.S. (2012). Temporary disruption of the blood-brain barrier by use of ultrasound and microbubbles: safety and efficacy evaluation in rhesus macaques. Cancer Res 72, 3652–3663.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meidani, A.R.N., and Hasan, M. (2004). Mathematical and physical modelling of bubble growth due to ultrasound. Appl Math Model 28, 333–351.

    Article  Google Scholar 

  • Miller, M.W., Luque, A.E., Battaglia, L.F., Mazza, S., and Everbach, E.C. (2003a). Biological and environmental factors affecting ultrasound-induced hemolysis in vitro: 1. HIV macrocytosis (cell size). Ultrasound Med Biol 29, 77–91.

    Article  PubMed  Google Scholar 

  • Miller, M.W., Battaglia, L.F., and Mazza, S. (2003b). Biological and environmental factors affecting ultrasound-induced hemolysis in vitro: medium tonicity. Ultrasound Med Biol 29, 713–724.

    Article  PubMed  Google Scholar 

  • Miller, M.W., Everbach, E.C., Miller, W.M., and Battaglia, L.F. (2003c). Biological and environmental factors affecting ultrasound-induced hemolysis in vitro: 2. medium dissolved gas (pO2) content. Ultrasound Med Biol 29, 93–102.

    Article  PubMed  Google Scholar 

  • Miyoshi, N., Mišík, V., Fukuda, M., Riesz, P., and Misik, V. (1995). Effect of gallium-porphyrin analogue ATX-70 on nitroxide formation from a cyclic secondary amine by ultrasound: on the mechanism of sonodynamic activation. Radiat Res 143, 194–202.

    Article  CAS  PubMed  Google Scholar 

  • Miyoshi, N., Kundu, S.K., Tuziuti, T., Yasui, K., Shimada, I., and Ito, Y. (2016). Combination of sonodynamic and photodynamic therapy against cancer would be effective through using a regulated size of nanoparticles. Nanosci Nanoeng 4, 1–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizrahi, N., Zhou, E.H., Lenormand, G., Krishnan, R., Weihs, D., Butler, J. P., Weitz, D.A., Fredberg, J.J., and Kimmel, E. (2012). Low intensity ultrasound perturbs cytoskeleton dynamics. Soft Matter 8, 2438–2443.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mo, S., Coussios, C.C., Seymour, L., and Carlisle, R. (2012). Ultrasoundenhanced drug delivery for cancer. Expert Opin Drug Deliver 9, 1525–1538.

    Article  CAS  Google Scholar 

  • Naghibi, S., Madaah Hosseini, H.R., and Faghihi Sani, M.A. (2013). Colloidal stability of dextran and dextran/poly ethylene glycol coated TiO2 nanoparticles by hydrothermal assisted sol-gel method. Ceramics Int 39, 8377–8384.

    Article  CAS  Google Scholar 

  • Naghibi, S., Madaah Hosseini, H.R., Faghihi Sani, M.A., Shokrgozar, M. A., and Mehrjoo, M. (2014). Mortality response of folate receptoractivated, PEG-functionalized TiO2 nanoparticles for doxorubicin loading with and without ultraviolet irradiation. Ceramics Int 40, 5481–5488.

    Article  CAS  Google Scholar 

  • Nie, F., Xu, H.X., Lu, M.D., Wang, Y., and Tang, Q. (2008). Anti-angiogenic gene therapy for hepatocellular carcinoma mediated by microbubble-enhanced ultrasound exposure: an in vivo experimental study. J Drug Target 16, 389–395.

    Article  CAS  PubMed  Google Scholar 

  • Nishimori, H., Kondoh, M., Isoda, K., Tsunoda, S.I., Tsutsumi, Y., and Yagi, K. (2009). Silica nanoparticles as hepatotoxicants. Eur J Pharm BioPharm 72, 496–501.

    Article  CAS  PubMed  Google Scholar 

  • Osaki, T., Yokoe, I., Uto, Y., Ishizuka, M., Tanaka, T., Yamanaka, N., Kurahashi, T., Azuma, K., Murahata, Y., Tsuka, T., et al. (2016). Bleomycin enhances the efficacy of sonodynamic therapy using aluminum phthalocyanine disulfonate. Ultrasons Sonochem 28, 161–168.

    Article  CAS  Google Scholar 

  • Osminkina, L.A., Nikolaev, A.L., Sviridov, A.P., Andronova, N.V., Tamarov, K.P., Gongalsky, M.B., Kudryavtsev, A.A., Treshalina, H.M., and Timoshenko, V.Y. (2015). Porous silicon nanoparticles as efficient sensitizers for sonodynamic therapy of cancer. Microporous Mesoporous Mater 210, 169–175.

    Article  CAS  Google Scholar 

  • Ozawa, K., Emori, M., Yamamoto, S., Yukawa, R., Yamamoto, S., Hobara, R., Fujikawa, K., Sakama, H., and Matsuda, I. (2014). Electron-hole recombination time at TiO2 single-crystal surfaces: influence of surface band bending. J Phys Chem Lett 5, 1953–1957.

    Article  CAS  PubMed  Google Scholar 

  • Pecha, R., and Gompf, B. (2000). Microimplosions: cavitation collapse and shock wave emission on a nanosecond time scale. Phys Rev Lett 84, 1328–1330.

    Article  CAS  PubMed  Google Scholar 

  • Qian, X., Zheng, Y., and Chen, Y. (2016). Micro/nanoparticle-augmented sonodynamic therapy (SDT): breaking the depth shallow of photoactivation. Adv Mater 28, 8097–8129.

    Article  CAS  PubMed  Google Scholar 

  • Riesz, P., and Christman, C. (1986). Sonochemical free radical formation in aqueous solutions. In: Federation Proceedings, P., Riesz, and C., Christman. (Maryland, The Federation), pp. 2485–2492.

    Google Scholar 

  • Rosenthal, I., Sostaric, J.Z., and Riesz, P. (2004). Sonodynamic therapy-a review of the synergistic effects of drugs and ultrasound. Ultrason Sonochem 11, 349–363.

    CAS  PubMed  Google Scholar 

  • Saad, A.H., and Hahn, G.M. (1992). Ultrasound-enhanced effects of adriamycin against murine tumors. Ultrasound Med Biol 18, 715–723.

    Article  CAS  PubMed  Google Scholar 

  • Sazgarnia, A., Shanei, A., Eshghi, H., Hassanzadeh-Khayyat, M., Esmaily, H., and Shanei, M.M. (2013). Detection of sonoluminescence signals in a gel phantom in the presence of Protoporphyrin IX conjugated to gold nanoparticles. Ultrasonics 53, 29–35.

    Article  CAS  PubMed  Google Scholar 

  • Shanei, A., Sazgarnia, A., Meibodi, N.T., Eshghi, H., Hassanzadeh-Khayyat, M., Esmaily, H., and Kakhki, N.A. (2012). Sonodynamic therapy using protoporphyrin IX conjugated to gold nanoparticles: an in vivo study on a colon tumor model. Iran J Basic Med Sci 15, 759–767.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi, J., Chen, Z., Wang, B., Wang, L., Lu, T., and Zhang, Z. (2015). Reactive oxygen species-manipulated drug release from a smart envelope- type mesoporous titanium nanovehicle for tumor sonodynamicchemotherapy. ACS Appl Mater Interfaces 7, 28554–28565.

    Article  CAS  PubMed  Google Scholar 

  • Shi, W.T., Forsberg, F., Vaidyanathan, P., Tornes, A., Østensen, J., and Goldberg, B.B. (2006). The influence of acoustic transmit parameters on the destruction of contrast microbubbles in vitro. Phys Med Biol 51, 4031–4045.

    Article  PubMed  Google Scholar 

  • Shibaguchi, H., Tsuru, H., Kuroki, M., and Kuroki, M. (2011). Sonodynamic cancer therapy: a non-invasive and repeatable approach using low-intensity ultrasound with a sonosensitizer. Anticancer Res 31, 24-25–2429.

    Google Scholar 

  • Shimizu, N., Ogino, C., Dadjour, M.F., and Murata, T. (2007). Sonocatalytic degradation of methylene blue with TiO2 pellets in water. Ultrasons Sonochem 14, 184–190.

    Article  CAS  Google Scholar 

  • Siegel, R.L., Miller, K.D., and Jemal, A. (2017). Cancer statistics, 2017. CA Cancer J Clin 67, 7–30.

    Article  PubMed  Google Scholar 

  • Sirsi, S.R., and Borden, M.A. (2014). State-of-the-art materials for ultrasound- triggered drug delivery. Adv Drug Deliver Rev 72, 3–14.

    Article  CAS  Google Scholar 

  • Sun, T., Zhang, Y.S., Pang, B., Hyun, D.C., Yang, M., and Xia, Y. (2014). Engineered nanoparticles for drug delivery in cancer therapy. Angew Chem Int Ed 53, 12320–12364.

    CAS  Google Scholar 

  • Sundaram, J., Mellein, B.R., and Mitragotri, S. (2003). An experimental and theoretical analysis of ultrasound-induced permeabilization of cell membranes. Biophys J 84, 3087–3101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suslick, K.S., (1988). Ultrasound: Its Chemical, Physical, and Biological Effects. (New York: VCH Publishers).

    Google Scholar 

  • Sviridov, A.P., Andreev, V.G., Ivanova, E.M., Osminkina, L.A., Tamarov, K.P., and Timoshenko, V.Y. (2013). Porous silicon nanoparticles as sensitizers for ultrasonic hyperthermia. Appl Phys Lett 103, 193110.

    Article  CAS  Google Scholar 

  • Sviridov, A.P., Osminkina, L.A., Kharin, A.Y., Gongansky, M.B., Kargina, J.V., Kudryavtsev, A.A., Bezsudnova, Y.I., Perova, T.S., Geloen, A., Lysenko, V., et al. (2017). Cytotoxicity control of silicon nanoparticles by biopolymer coating and ultrasound irradiation for cancer theranostic applications. Nanotechnology 28, 105102.

    Article  CAS  PubMed  Google Scholar 

  • Tabuchi, Y., Takasaki, I., Zhao, Q.L., Wada, S., Hori, T., Feril Jr., L.B., Tachibana, K., Nomura, T., and Kondo, T. (2008). Genetic networks responsive to low-intensity pulsed ultrasound in human lymphoma U- 937 cells. Cancer Lett 270, 286–294.

    Article  CAS  PubMed  Google Scholar 

  • Tachibana, K., Feril Jr., L.B., and Ikeda-Dantsuji, Y. (2008). Sonodynamic therapy. Ultrasonics 48, 253–259.

    Article  CAS  PubMed  Google Scholar 

  • Tang, W., Liu, Q., Zhang, J., Cao, B., Zhao, P., and Qin, X. (2010). In vitro activation of mitochondria-caspase signaling pathway in sonodynamic therapy-induced apoptosis in sarcoma 180 cells. Ultrasonics 50, 567–576.

    Article  CAS  PubMed  Google Scholar 

  • Tinkov, S., Coester, C., Serba, S., Geis, N.A., Katus, H.A., Winter, G., and Bekeredjian, R. (2010). New doxorubicin-loaded phospholipid microbubbles for targeted tumor therapy: in-vivo characterization. J Control Release 148, 368–372.

    Article  CAS  PubMed  Google Scholar 

  • Trepat, X., Deng, L., An, S.S., Navajas, D., Tschumperlin, D.J., Gerthoffer, W.T., Butler, J.P., and Fredberg, J.J. (2007). Universal physical responses to stretch in the living cell. Nature 447, 592–595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umemura, S., Kawabata, K., Yumita, N., Nishigaki, R., and Umemura, K. (1992). Sonodynamic approach to tumor treatment. In: Proceedings of Ultrasonics Symposium, S., Umemura, K., Kawabata, and N., Yumita, eds. (Arizona, USA), pp. 1231–1240.

    Google Scholar 

  • Umemura, S.I., Yumita, N., Nishigaki, R., and Umemura, K. (1990). Mechanism of cell damage by ultrasound in combination with hematoporphyrin. Cancer Sci 81, 962–966.

    CAS  Google Scholar 

  • Umemura, S.I., Yumita, N., and Nishigaki, R. (1993). Enhancement of ultrasonically induced cell damage by a gallium-porphyrin complex, ATX-70. Cancer Sci 84, 582–588.

    CAS  Google Scholar 

  • Vargas, A., Pegaz, B., Debefve, E., Konan-Kouakou, Y., Lange, N., Ballini, J.P., van den Bergh, H., Gurny, R., and Delie, F. (2004). Improved photodynamic activity of porphyrin loaded into nanoparticles: an in vivo evaluation using chick embryos. Int J Pharm 286, 131–145.

    Article  CAS  PubMed  Google Scholar 

  • Wang, H., Yang, Y., Chen, H., Dan, J., Cheng, J., Guo, S., Sun, X., Wang, W., Ai, Y., Li, S., et al. (2014). The predominant pathway of apoptosis in THP-1 macrophage-derived foam cells induced by 5-aminolevulinic acid-mediated sonodynamic therapy is the mitochondria-caspase pathway despite the participation of endoplasmic reticulum stress. Cell P-hysiol Biochem 33, 1789–1801.

    Article  CAS  Google Scholar 

  • Wang, X.B., Liu, Q.H., Wang, P., Zhang, K., Tang, W., and Wang, B.L. (2008). Enhancement of apoptosis by sonodynamic therapy with protoporphyrin IX in isolate sarcoma 180 cells. Cancer Biother Radiopharmaceut 23, 238–246.

    Article  CAS  Google Scholar 

  • Wang, X., Zhang, W., Xu, Z., Luo, Y., Mitchell, D., and Moss, R.W. (2009). Sonodynamic and photodynamic therapy in advanced breast carcinoma: a report of 3 cases. Integr Cancer Ther 8, 283–287.

    Article  PubMed  Google Scholar 

  • Wang, X., Wang, W., Yu, L., Tang, Y., Cao, J., and Chen, Y. (2017). Sitespecific sonocatalytic tumor suppression by chemically engineered single- crystalline mesoporous titanium dioxide sonosensitizers. J Mater Chem B 5, 4579–4586.

    Article  CAS  PubMed  Google Scholar 

  • Wood, A.K.W., Bunte, R.M., Price, H.E., Deitz, M.S., Tsai, J.H., Lee, W.M. F., and Sehgal, C.M. (2008). The disruption of murine tumor neovasculature by low-intensity ultrasound-comparison between 1- and 3-MHz sonication frequencies. Academic Rad 15, 1133–1141.

    Article  Google Scholar 

  • Worthington, A., Thompson, J., Rauth, A., and Hunt, J. (1997). Mechanism of ultrasound enhanced porphyrin cytotoxicity. Part I: a search for free radical effects. Ultrasound Med Biol 23, 1095–1105.

    Article  CAS  PubMed  Google Scholar 

  • Wu, J., and Nyborg, W.L. (2008). Ultrasound, cavitation bubbles and their interaction with cells. Adv Drug Deliver Rev 60, 1103–1116.

    Article  CAS  Google Scholar 

  • Xu, H., Zhang, X., Han, R., Yang, P., Ma, H., Song, Y., Lu, Z., Yin, W., Wu, X.X., and Wang, H. (2016). Nanoparticles in sonodynamic therapy: state of the art review. RSC Adv 6, 50697–50705.

    Article  CAS  Google Scholar 

  • Xu, Z.Y., Wang, K., Li, X.Q., Chen, S., Deng, J.M., Cheng, Y., and Wang, Z.G. (2013). The ABCG2 transporter is a key molecular determinant of the efficacy of sonodynamic therapy with Photofrin in glioma stem-like cells. Ultrasonics 53, 232–238.

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi, S., Kobayashi, H., Narita, T., Kanehira, K., Sonezaki, S., Kudo, N., Kubota, Y., Terasaka, S., and Houkin, K. (2011). Sonodynamic therapy using water-dispersed TiO2-polyethylene glycol compound on glioma cells: comparison of cytotoxic mechanism with photodynamic therapy. Ultrasons Sonochem 18, 1197–1204.

    Article  CAS  Google Scholar 

  • Yamamoto, S., Yuba, E., Harada, A., and Kono, K. (2015). Effective condensation of multivalent anions into polyion complex micelles prepared from TiO2 nanoparticles and polyallylamine bearing poly(ethylene glycol) grafts. Langmuir 31, 8583–8588.

    Article  CAS  PubMed  Google Scholar 

  • Yu, T., Wang, Z., and Jiang, S. (2001). Potentiation of cytotoxicity of adriamycin on human ovarian carcinoma cell line 3AO by low-level ultrasound. Ultrasonics 39, 307–309.

    Article  CAS  PubMed  Google Scholar 

  • Yu, T., Wang, Z., and Mason, T.J. (2004). A review of research into the uses of low level ultrasound in cancer therapy. Ultrasons Sonochem 11, 95–103.

    Article  CAS  Google Scholar 

  • Yumita, N., Nishigaki, R., Umemura, K., and Umemura, S.I. (1989). Hematoporphyrin as a sensitizer of cell-damaging effect of ultrasound. Cancer Sci 80, 219–222.

    CAS  Google Scholar 

  • Yumita, N., Nishigaki, R., Umemura, K., and Umemura, S.I. (1990). Synergistic effect of ultrasound and hematoporphyrin on sarcoma 180. Cancer Sci 81, 304–308.

    CAS  Google Scholar 

  • Yumita, N., Iwase, Y., Nishi, K., Ikeda, T., Umemura, S.I., Sakata, I., and Momose, Y. (2010a). Sonodynamically induced cell damage and membrane lipid peroxidation by novel porphyrin derivative, DCPH-P-Na (I). Anticancer Res 30, 2241–2246.

    CAS  PubMed  Google Scholar 

  • Yumita, N., Okudaira, K., Momose, Y., and Umemura, S.I. (2010b). Sonodynamically induced apoptosis and active oxygen generation by gallium- porphyrin complex, ATX-70. Cancer Chemother Pharmacol 66, 1071–1078.

    Article  CAS  PubMed  Google Scholar 

  • Zeghimi, A., Escoffre, J.M., and Bouakaz, A. (2015). Role of endocytosis in sonoporation-mediated membrane permeabilization and uptake of small molecules: an electron microscopy study. Phys Biol 12, 066007.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, J., Liang, Y.C., Lin, X., Zhu, X., Yan, L., Li, S., Yang, X., Zhu, G., Rogach, A.L., Yu, P.K.N., et al. (2015). Self-monitoring and self-delivery of photosensitizer-doped nanoparticles for highly effective combination cancer therapy in vitro and in vivo. ACS Nano 9, 9741–9756.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (51572271, 51772018), National Basic Research Program of China (2016YFA0201500) and Fundamental Research Funds for the Central Universities (buctrc201610, JD1609, PYBZ1705).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Huiyu Liu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pan, X., Wang, H., Wang, S. et al. Sonodynamic therapy (SDT): a novel strategy for cancer nanotheranostics. Sci. China Life Sci. 61, 415–426 (2018). https://doi.org/10.1007/s11427-017-9262-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-017-9262-x

Keywords

Navigation