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Recent advances in nanomaterials for sonodynamic therapy

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Abstract

Sonodynamic therapy (SDT), as a novel non-invasive strategy for eliminating tumor, has the advantages of deeper tissue penetration, fewer side effects, and better patient compliance, compared with photodynamic therapy (PDT). In SDT, ultrasound was used to activate sonosensitizer to produce cytotoxic reactive oxygen species (ROS), induce the collapse of vacuoles in solution, and bring about irreversible damage to cancer cells. In recent years, much effort has been devoted to developing highly efficient sonosensitizers which can efficiently generate ROS. However, the traditional organic sonosensitizers, such as porphyrins, hypericin, and curcumins, suffer from complex synthesis, poor water solubility, and low tumor targeting efficacy which limit the benefits of SDT. In contrast, inorganic sonosensitizers show good in vivo stability, controllable physicochemical properties, ease of achieving multifunctionality, and high tumor targeting, which greatly expanded their application in SDT. In this review, we systematically summarize the nanomaterials which act as the carrier of molecular sonosensitizers, and directly produce ROS under ultrasound. Moreover, the prospects of inorganic nanomaterials for SDT application are also discussed.

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References

  1. Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R. L.; Torre, L. A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: Cancer J. Clin. 2018, 68, 394–424.

    Google Scholar 

  2. Chen, W. Q.; Zheng, R. S.; Baade, P. D.; Zhang, S. W.; Zeng, H. M.; Bray, F.; Jemal, A.; Yu, X. Q.; He, J. Cancer statistics in China, 2015. CA: Cancer J. Clin. 2016, 66, 115–132.

    Google Scholar 

  3. Siegel, R. L.; Miller, K. D.; Jemal, A. Cancer statistics, 2017. CA: Cancer J. Clin. 2017, 67, 7–30.

    Google Scholar 

  4. Wyld, L.; Audisio, R. A.; Poston, G. J. The evolution of cancer surgery and future perspectives. Nat. Rev. Clin. Oncol. 2015, 12, 115–124.

    Google Scholar 

  5. Moran, M. S. Radiation therapy in the locoregional treatment of triple-negative breast cancer. Lancet Oncol. 2015, 16, e113–e122.

    Google Scholar 

  6. Ray, A.; Das, D. S.; Song, Y.; Hideshima, T.; Tai, Y. T.; Chauhan, D.; Anderson, K. C. Combination of a novel HDAC6 inhibitor ACY-241 and anti-PD-L1 antibody enhances anti-tumor immunity and cytotoxicity in multiple myeloma. Leukemia 2018, 32, 843–846.

    CAS  Google Scholar 

  7. Deng, G. L.; Zeng, S.; Shen, H. Chemotherapy and target therapy for hepatocellular carcinoma: New advances and challenges. World J. Hepatol. 2015, 7, 787–798.

    Google Scholar 

  8. Nguyen, V. D.; Min, H. K.; Kim, C. S.; Han, J.; Park, J. O.; Choi, E. Folate receptor-targeted liposomal nanocomplex for effective synergistic photothermal-chemotherapy of breast cancer in vivo. Colloids Surf. B 2019, 173, 539–548.

    CAS  Google Scholar 

  9. Wang, J.; Xu, D. J.; Deng, T.; Li, Y. Y.; Xue, L.; Yan, T.; Huang, D. C.; Deng, D. W. Self-decomposable mesoporous doxorubicin@silica nanocomposites for nuclear targeted chemo-photodynamic combination therapy. ACS Appl. Mater. Interfaces 2018, 1, 1976–1984.

    CAS  Google Scholar 

  10. Shen, S.; Guo, X. M.; Wu, L.; Wang, M.; Wang, X. S.; Kong, F. F.; Shen, H. J.; Xie, M.; Ge, Y. R.; Jin, Y. Dual-core@shell-structured Fe3O4-NaYF4@TiO2 nanocomposites as a magnetic targeting drug carrier for bioimaging and combined chemo-sonodynamic therapy. J. Mater. Chem. B 2014, 2, 5775–5784.

    CAS  Google Scholar 

  11. Ge, J. C.; Lan, M. H; Zhou, B. J.; Liu, W. M.; Guo, L.; Wang, H.; Jia, Q. Y.; Niu, G. L.; Huang, X.; Zhou, H. Y. et al. A graphene quantum dot photodynamic therapy agent with high singlet oxygen generation. Nat. Commun. 2014, 5, 4596.

    CAS  Google Scholar 

  12. Fan, W. P.; Yung, B.; Huang, P.; Chen, X. Y. Nanotechnology for multimodal synergistic cancer therapy. Chem. Rev. 2017, 117, 13566–13638.

    CAS  Google Scholar 

  13. Lan, M. H.; Zhao, S. J.; Xie, Y. S.; Zhao, J. F.; Guo, L.; Niu, G. L.; Li, Y.; Sun, H. Y.; Zhang, H. Y.; Liu, W. M. et al. Water-soluble polythiophene for two-photon excitation fluorescence imaging and photodynamic therapy of cancer. ACS Appl. Mater. Interfaces 2017, 9, 14590–14595.

    CAS  Google Scholar 

  14. Monro, S.; Colón, K. L.; Yin, H.; Roque III, J.; Konda, P.; Gujar, S.; Thummel, R. P.; Lilge, L.; Cameron, C. G.; McFarland, S. A. Transition metal complexes and photodynamic therapy from a tumor-centered approach: Challenges, opportunities, and highlights from the development of TLD1433. Chem. Rev. 2019, 119, 797–828.

    CAS  Google Scholar 

  15. Fan, W. P.; Huang, P.; Chen, X. Y. Overcoming the Achilles’ heel of photodynamic therapy. Chem. Soc. Rev. 2016, 45, 6488–6519.

    CAS  Google Scholar 

  16. Lan, M. H.; Zhao, S. J.; Liu, W. M.; Lee, C. S.; Zhang, W. J.; Wang, P. F. Photosensitizers for photodynamic therapy. Adv. Healthc. Mater. 2019, 8, 1900132.

    Google Scholar 

  17. MacDonald, I. J.; Dougherty, T. J. Basic principles of photodynamic therapy. J. Porphyr. Phthalocyanines 2001, 5, 105–129.

    CAS  Google Scholar 

  18. Lucky, S. S.; Soo, K. C.; Zhang, Y. Nanoparticles in photodynamic therapy. Chem. Rev. 2015, 115, 1990–2042.

    CAS  Google Scholar 

  19. Wilson, B. C. Photodynamic therapy for cancer: Principles. Can. J. Gastroenterol. 2002, 16, 743109.

    Google Scholar 

  20. Wang, P. Y.; Wang, X. D.; Luo, Q.; Li, Y.; Lin, X. X.; Fan, L. L.; Zhang, Y.; Liu, J. F.; Liu, X. L. Fabrication of red blood cell-based multimodal theranostic probes for second near-infrared window fluorescence imaging-guided tumor surgery and photodynamic therapy. Theranostics 2019, 9, 369–380.

    CAS  Google Scholar 

  21. Wang, C.; Tao, H. Q.; Cheng, L.; Liu, Z. Near-infrared light induced in vivo photodynamic therapy of cancer based on upconversion nanoparticles. Biomaterials 2011, 32, 6145–6154.

    CAS  Google Scholar 

  22. Zhang, J. Y.; Chen, S.; Wang, P.; Jiang, D. J.; Ban, D. X.; Zhong, N. Z.; Jiang, G. C.; Li, H.; Hu, Z.; Xiao, J. R. et al. NaYbF4 nanoparticles as near infrared light excited inorganic photosensitizers for deep penetration in photodynamic therapy. Nanoscale 2017, 9, 2706–2710.

    CAS  Google Scholar 

  23. Yumita, N.; Nishigaki, R.; Umemura, K.; Umemura, S. Hematoporphyrin as a sensitizer of cell-damaging effect of ultrasound. Jpn. J. Cancer Res. 1989, 80, 219–222.

    CAS  Google Scholar 

  24. Yumita, N.; Nishigaki, R.; Umemura, K.; Umemura, S. Synergistic effect of ultrasound and hematoporphyrin on sarcoma 180. Jpn. J. Cancer Res. 1990, 81, 304–308.

    CAS  Google Scholar 

  25. Umemura, S.; Yumita, N.; Nishigaki, R.; Umemura, K. Mechanism of cell damage by ultrasound in combination with hematoporphyrin. Jpn. J. Cancer Res. 1990, 81, 962–966.

    CAS  Google Scholar 

  26. Umemura, S.; Yumita, N.; Nishigaki, R. Enhancement of ultrasonically induced cell damage by a gallium-porphyrin complex, ATX-70. Jpn. J. Cancer Res. 1993, 84, 582–588.

    CAS  Google Scholar 

  27. Yue, W. W.; Chen, L.; Yu, L. D.; Zhou, B. G.; Yin, H. H.; Ren, W. W.; Liu, C.; Guo, L. H.; Zhang, Y. F.; Sun, L. P. et al. Checkpoint blockade and nanosonosensitizer-augmented noninvasive sonodynamic therapy combination reduces tumour growth and metastases in mice. Nat. Commun. 2019, 10, 2025.

    Google Scholar 

  28. Wang, L.; Hu, Y. J.; Hao, Y. W.; Li, L.; Zheng, C. X.; Zhao, H. J.; Niu, M. Y.; Yin, Y. Y.; Zhang, Z. Z; Zhang, Y. Tumor-targeting core-shell structured nanoparticles for drug procedural controlled release and cancer sonodynamic combined therapy. J. Control. Release 2018, 286, 74–84.

    CAS  Google Scholar 

  29. 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. Long-circulating Au-TiO2 nanocomposite as a sonosensitizer for ROS-mediated eradication of cancer. Nano Lett. 2016, 16, 6257–6264.

    CAS  Google Scholar 

  30. Liu, Y.; Wan, G. Y.; Guo, H.; Liu, Y. Y.; Zhou, P.; Wang, H. M.; Wang, D.; Zhang, S. P.; Wang Y. S.; Zhang, N. A multifunctional nanoparticle system combines sonodynamic therapy and chemotherapy to treat hepatocellular carcinoma. Nano Res. 2017, 10, 834–855.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  32. Huang, P.; Qian, X. Q.; Chen, Y.; Yu, L. D.; Lin, H.; Wane, L. Y.; Zhu, Y. F.; Shi, J. L. Metalloporphyrin-encapsulated biodegradable nanosystems for highly efficient magnetic resonance imaging-guided sonodynamic cancer therapy. J. Am. Chem. Soc. 2017, 139, 1275–1284.

    CAS  Google Scholar 

  33. Pan, X. T.; Wang, H. Y.; Wang, S. H.; Sun, X.; Wang, L. J.; Wang, W. W.; Shen, H. Y.; Liu, H. Y. Sonodynamic therapy (SDT): A novel strategy for cancer nanotheranostics. Sci China Life Sci. 2018, 61, 415–426.

    Google Scholar 

  34. Bogdan, J.; Plawińska-Czarnak, J.; Zarzyńska, J. Nanoparticles of titanium and zinc oxides as novel agents in tumor treatment: A review. Nanoscale Res. Lett. 2017, 12, 225.

    Google Scholar 

  35. Cavalli, R.; Marano, F.; Argenziano, M.; Varese, A.; Frairia, R.; Catalano, M. G. Combining drug-loaded nanobubbles and extracorporeal shock waves for difficult-to-treat cancers. Curr. Drug Deliv. 2018, 15, 752–754.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  37. Liu, R. G.; Zhang, Q. Y.; Lang, Y. H.; Peng, Z. Z.; Li, L. B. Sonodynamic therapy, a treatment developing from photodynamic therapy. Photodiagn. Photodyn. Ther. 2017, 19, 159–166.

    Google Scholar 

  38. Rosenthal, I.; Sostaric, J. Z.; Riesz, P. Sonodynamic therapy—A review of the synergistic effects of drugs and ultrasound. Ultrason. Sonochem. 2004, 11, 349–363.

    CAS  Google Scholar 

  39. Pecha, R.; Gompf, B. Microimplosions: Cavitation collapse and shock wave emission on a nanosecond time scale. Phys. Rev. Lett. 2000, 84, 1328–1330.

    CAS  Google Scholar 

  40. Pan, X. T.; Bai, L. X.; Wang, H.; Wu, Q. Y.; Wang, H. Y.; Liu, S.; Xu, B. L.; Shi, X. H.; Liu, H. Y. Metal-organic-framework-derived carbon nanostructure augmented sonodynamic cancer therapy. Adv. Mater. 2018, 30, 1800180.

    Google Scholar 

  41. Xu, J.; Xia, X. S.; Leung, A. W.; Xiang, J. Y.; Jiang, Y.; Yu, H. P.; Bai, D. Q.; Li, X. H.; Xu, C. S. Sonodynamic action of pyropheophorbide—A methyl ester induces mitochondrial damage in liver cancer cells. Ultrasonics 2011, 51, 480–484.

    CAS  Google Scholar 

  42. Pang, X.; Xu, C. S.; Jiang, Y.; Xiao, Q. C.; Leung, A. W. Natural products in the discovery of novel sonosensitizers. Pharmacol. Ther. 2016, 162, 144–151.

    CAS  Google Scholar 

  43. Jin, H.; Zhong, X.; Wang, Z. Y.; Huang, X.; Ye, H. Y.; Ma, S. Y.; Chen, Y.; Cai, J. Y. Sonodynamic effects of hematoporphyrin monomethyl ether on CNE-2 cells detected by atomic force microscopy. J. Cell. Biochem. 2011, 112, 169–178.

    CAS  Google Scholar 

  44. Qian, J. L.; Gao, Q. P. Sonodynamic therapy mediated by emodin induces the oxidation of microtubules to facilitate the sonodynamic effect. Ultrasound Med. Biol. 2018, 44, 853–860.

    Google Scholar 

  45. Didenko, Y. T.; Suslick, K. S. The energy efficiency of formation of photons, radicals and ions during single-bubble cavitation. Nature 2002, 418, 394–397.

    CAS  Google Scholar 

  46. Wu, J. R.; Nyborg, W. L. Ultrasound, cavitation bubbles and their interaction with cells. Adv. Drug Deliv. Rev. 2008, 60, 1103–1116.

    CAS  Google Scholar 

  47. Hirschberg, H.; Madsen, S. J. Synergistic efficacy of ultrasound, sonosensitizers and chemotherapy: A review. Ther. Deliv. 2017, 8, 331–342.

    CAS  Google Scholar 

  48. Yumita, N.; Iwase, Y.; Nishi, K.; Komatsu, H.; Takeda, K.; Onodera, K.; Fukai, T.; Ikeda, T.; Umemura, S.; Okudaira, K. et al. Involvement of reactive oxygen species in sonodynamically induced apoptosis using a novel porphyrin derivative. Theranostics 2012, 2, 880–888.

    CAS  Google Scholar 

  49. Chen, B.; Zheng, R. N.; Liu, D.; Li, B. F.; Lin, J. R.; Zhang, W. M. The tumor affinity of chlorin e6 and its sonodynamic effects on non-small cell lung cancer. Ultrason. Sonochem. 2013, 20, 667–673.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  51. Zhang, H. J.; Liu, X.; Liu, Y. B.; Wu, Y.; Li, H. X.; Zhao, C. B.; Li, H. Z.; Meng, Q. G.; Li, W. Effect of hematoporphyrin monomethyl ether-sonodynamic therapy (HMME-SDT) on hypertrophic scarring. PLoS One 2014, 9, e86003.

    Google Scholar 

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

    CAS  Google Scholar 

  53. Zhao, X.; Liu, Q. H.; Tang, W.; Wang, X. B.; Wang, P.; Gong, L. Y.; Wang, Y. Damage effects of protoporphyrin IX—Sonodynamic therapy on the cytoskeletal F-actin of Ehrlich ascites carcinoma cells. Ultrason. Sonochem. 2009, 16, 50–56.

    Google Scholar 

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

    CAS  Google Scholar 

  55. Paris, J. L.; Mannaris, C.; Victoria Cabañas, M.; Carlisle, R.; Manzano, M.; Vallet-Regi, M.; Coussios, C. C. Ultrasound-mediated cavitation-enhanced extravasation of mesoporous silica nanoparticles for controlled-release drug delivery. Chem. Eng. J. 2018, 340, 2–8.

    CAS  Google Scholar 

  56. Wang, Y. F.; Liu, J.; Ma, X. W.; Liang X. J. Nanomaterial-assisted sensitization of oncotherapy. Nano Res. 2018, 11, 2932–2950.

    Google Scholar 

  57. Lin, X. H.; Qiu, Y.; Song, L.; Chen, S.; Chen, X. F.; Huang, G. M.; Song, J. B.; Chen, X. Y.; Yang, H. H. Ultrasound activation of liposomes for enhanced ultrasound imaging and synergistic gas and sonodynamic cancer therapy. Nanoscale Horiz. 2019, 4, 747–756.

    CAS  Google Scholar 

  58. Di, J.; Yu, J. C.; Wang, Q.; Yao, S. S.; Suo, D. J.; Ye, Y. Q.; Pless, M.; Zhu, Y.; Jing, Y.; Gu, Z. Ultrasound-triggered noninvasive regulation of blood glucose levels using microgels integrated with insulin nanocapsules. Nano Res. 2017, 10, 1393–1402.

    CAS  Google Scholar 

  59. Han, H. J.; Ekweremadu, C.; Patel, N. Advanced drug delivery system with nanomaterials for personalised medicine to treat breast cancer. J. Drug Deliv. Sci. Technol. 2019, 52, 1051–1060.

    CAS  Google Scholar 

  60. Xing, R. J.; Bhirde, A. A.; Wang, S. J.; Sun, X. L.; Liu, G.; Hou, Y. L.; Chen, X. Y. Hollow iron oxide nanoparticles as multidrug resistant drug delivery and imaging vehicles. Nano Res. 2013, 6, 1–9.

    CAS  Google Scholar 

  61. Wang, L.; Niu, M. Y.; Zheng, C X.; Zhao, H. J.; Niu, X. X.; Li, L.; Hu, Y. J.; Zhang, Y. J.; Shi, J. J.; Zhang, Z. Z. A core-shell nano-platform for synergistic enhanced sonodynamic therapy of hypoxic tumor via cascaded strategy. Adv. Healthc. Mater. 2018, 7, 1800819.

    Google Scholar 

  62. Du, J. Z.; Lane, L. A.; Nie, S. M. Stimuli-responsive nanoparticles for targeting the tumor microenvironment. J. Control. Release 2015, 219, 205–214.

    CAS  Google Scholar 

  63. Bordat, A.; Boissenot, T.; Nicolas, J.; Tsapis, N. Thermoresponsive polymer nanocarriers for biomedical applications. Adv. Drug Deliv. Rev. 2019, 138, 167–192.

    CAS  Google Scholar 

  64. Castillo, R. R.; Colilla, M.; Vallet-Regí, M. Advances in mesoporous silica-based nanocarriers for co-delivery and combination therapy against cancer. Expert Opin. Drug Deliv. 2017, 14, 229–243.

    CAS  Google Scholar 

  65. Xiao, M.; Wang, Z. L.; Lyu, M. Q.; Luo, B.; Wang, S. C.; Liu, G.; Cheng, H. M.; Wang, L. Z. Hollow nanostructures for photocatalysis: Advantages and challenges. Adv. Mater. 2019, 31, 1801369.

    Google Scholar 

  66. Yu, L.; Yu, X. Y.; Lou, X. W. The design and synthesis of hollow micro-/nanostructures: Present and future trends. Adv. Mater. 2018, 30, 1800939.

    Google Scholar 

  67. Qi, J.; Lai, X. Y.; Wang, J. Y.; Tang, H. J.; Ren, H.; Yang, Y.; Jin, Q.; Zhang, L. J.; Yu, R. B.; Ma, G. H. et al. Multi-shelled hollow micro-/nanostructures. Chem. Soc. Rev. 2015, 44, 6749–6773.

    CAS  Google Scholar 

  68. Sonvico, F.; Clementino, A.; Buttini, F.; Colombo, G.; Pescina, S.; Guterres, S. S.; Pohlmann, A. R.; Nicoli, S. Surface-modified nanocarriers for nose-to-brain delivery: From bioadhesion to targeting. Pharmaceutics 2018, 10, 34.

    Google Scholar 

  69. Peng, L.; Liu, S. Y.; Feng, A. C.; Yuan, J. Y. Polymeric nanocarriers based on cyclodextrins for drug delivery: Host-guest interaction as stimuli responsive linker. Mol. Pharmaceutics 2017, 14, 2475–2486.

    CAS  Google Scholar 

  70. Feng, Q. H.; Zhang, W. X.; Yang, X. M.; Li, Y. Z.; Hao, Y. W.; Zhang, H. L.; Hou, L.; Zhang, Z. Z. pH/ultrasound dual-responsive gas generator for ultrasound imaging-guided therapeutic inertial cavitation and sonodynamic therapy. Adv. Healthc. Mater. 2018, 7, 1700957.

    Google Scholar 

  71. Teng, Z. G.; Li, W.; Tang, Y. X.; Elzatahry, A.; Lu, G. M.; Zhao, D. Y. Mesoporous organosilica hollow nanoparticles: Synthesis and applications. Adv. Mater. 2019, 31, 1707612.

    Google Scholar 

  72. Zhang, J. F.; Zhang, J.; Li, W. Y.; Chen, R.; Zhang, Z. Y.; Zhang, W. J.; Tang, Y. B.; Chen, X. Y.; Liu, G.; Lee, C. S. Degradable hollow mesoporous silicon/carbon nanoparticles for photoacoustic imaging-guided highly effective chemo-thermal tumor therapy in vitro and in vivo. Theranostics 2017, 7, 3007–3020.

    CAS  Google Scholar 

  73. Salonen, J.; Lehto, V. P. Fabrication and chemical surface modification of mesoporous silicon for biomedical applications. Chem. Eng. J. 2008, 137, 162–172.

    CAS  Google Scholar 

  74. Wu, M. Y.; Meng, Q. S.; Chen, Y.; Zhang, L. X.; Li, M. L.; Cai, X. J.; Li, Y. P.; Yu, P. C.; Zhang, L. L.; Shi, J. L. Large pore-sized hollow mesoporous organosilica for redox-responsive gene delivery and synergistic cancer chemotherapy. Adv. Mater. 2016, 28, 1963–1969.

    CAS  Google Scholar 

  75. Lu, L. L.; Xiong, W. Y.; Ma, J. B.; Gao, T. F.; Peng, S. Y.; Xiao, W. Design of dual-responsive nanocarries with high drug loading capacity based on hollow mesoporous organosilica nanoparticles. Mater. Chem. Phys. 2019, 233, 230–235.

    CAS  Google Scholar 

  76. Yang, S.; Fan, J.; Lin, S. T.; Wang, Y. R.; Liu, C. Novel pH-responsive biodegradable organosilica nanoparticles as drug delivery system for cancer therapy. Colloids Surf. A 2020, 585, 124133.

    Google Scholar 

  77. Yu, L. D.; Chen, Y.; Lin, H.; Du, W. X.; Chen, H. R.; Shi, J. L. Ultrasmall mesoporous organosilica nanoparticles: Morphology modulations and redox-responsive biodegradability for tumor-specific drug delivery. Biomaterials 2018, 161, 292–305.

    CAS  Google Scholar 

  78. An, J.; Hu, Y. G.; Li, C.; Hou, X. L.; Cheng, K.; Zhang, B.; Zhang, R. Y.; Li, D. Y.; Liu, S. J.; Liu, B. et al. A pH/ultrasound dual-response biomimetic nanoplatform for nitric oxide gas-sonodynamic combined therapy and repeated ultrasound for relieving hypoxia. Biomaterials 2020, 230, 119636.

    CAS  Google Scholar 

  79. Liu, X. L.; Pan, Y. C.; Yang, J. J.; Gao, Y. F.; Huang, T.; Luan, X. W.; Wang, Y. Z.; Song, Y. J. Gold nanoparticles doped metal-organic frameworks as near-infrared light-enhanced cascade nanozyme against hypoxic tumors. Nano Res. 2020, 13, 653–660.

    CAS  Google Scholar 

  80. Pan, X. T.; Wang, W. W.; Huang, Z. J.; Liu, S.; Guo, J.; Zhang, F. R.; Yuan, H. J.; Li, X.; Liu, F. Y.; Liu, H. Y. MOF-derived double-layer hollow nanoparticles with oxygen generation ability for multimodal imaging-guided sonodynamic therapy. Angew. Chem., Int. Ed., in press, DOI: https://doi.org/10.1002/anie.202004894.

  81. Zhu, P.; Chen, Y.; Shi, J. L. Nanoenzyme-augmented cancer sonodynamic therapy by catalytic tumor oxygenation. ACS Nano 2018, 12, 3780–3795.

    CAS  Google Scholar 

  82. Zhang, Y. J.; Wang, H. L.; Jia, X. D.; Du, S. Z.; Yin, Y. Y.; Zhang, X. J. Cascade catalytic nanoplatform for enhanced starvation and sonodynamic therapy. J. Drug Target. 2020, 28, 195–203.

    CAS  Google Scholar 

  83. Khan, M. S.; Hwang, J.; Lee, K.; Choi, Y.; Kim, K.; Koo, H. J.; Hong, J. W.; Choi, J. Oxygen-carrying micro/nanobubbles: Composition, synthesis techniques and potential prospects in photo-triggered theranostics. Molecules 2018, 23, 2210.

    Google Scholar 

  84. Song, R. Y.; Hu, D. H.; Chung, H. Y.; Sheng, Z. H.; Yao, S. H. Lipid-polymer bilaminar oxygen nanobubbles for enhanced photodynamic therapy of cancer. ACS Appl. Mater. Interfaces 2018, 10, 36805–36813.

    CAS  Google Scholar 

  85. Wang, J. P.; Liu, L.; You, Q.; Song, Y. L.; Sun, Q.; Wang, Y. D.; Cheng, Y.; Tan, F. P.; Li, N. All-in-one theranostic nanoplatform based on hollow MoSX for photothermally-maneuvered oxygen self-enriched photodynamic therapy. Theranostics 2018, 8, 955–971.

    CAS  Google Scholar 

  86. Song, G. S.; Liang, C.; Yi, X.; Zhao, Q.; Cheng, L.; Yang, K.; Liu, Z. Perfluorocarbon-loaded hollow Bi2Se3 nanoparticles for timely supply of oxygen under near-infrared light to enhance the radiotherapy of cancer. Adv. Mater. 2016, 28, 2716–2723.

    CAS  Google Scholar 

  87. Zhang, H. J.; Chen, J. J.; Zhu, X.; Ren, Y. P.; Cao, F.; Zhu, L.; Hou, L.; Zhang, H. L.; Zhang, Z. Z. Ultrasound induced phase-transition and invisible nanobomb for imaging-guided tumor sonodynamic therapy. J. Mater. Chem. B 2018, 6, 6108–6121.

    CAS  Google Scholar 

  88. Yu, M.; Xu, X. L.; Cai, Y. J.; Zou, L. Y.; Shuai, X. T. Perfluorohexane-cored nanodroplets for stimulations-responsive ultrasonography and O2-potentiated photodynamic therapy. Biomaterials 2018, 175, 61–71.

    CAS  Google Scholar 

  89. Xu, L. F.; Qiu, X. F.; Zhang, Y. T.; Cao, K.; Zhao, X. Z.; Wu, J. H.; Hu, Y. Q.; Guo, H. Q. Liposome encapsulated perfluorohexane enhances radiotherapy in mice without additional oxygen supply. J. Transl. Med. 2016, 14, 268.

    Google Scholar 

  90. Wang, Y.; Liu, Y.; Wu, H. X.; Zhang, J. P.; Tian, Q. W.; Yang, S. P. Functionalized holmium-doped hollow silica nanospheres for combined sonodynamic and hypoxia-activated therapy. Adv. Funct. Mater. 2019, 29, 1805764.

    Google Scholar 

  91. Guan, G. Q.; Wang, X.; Huang, X. J.; Zhang, W. L.; Cui, Z.; Zhang, Y. F.; Lu, X. W.; Zou, R. J.; Hu, J. Q. Porous cobalt sulfide hollow nanospheres with tunable optical property for magnetic resonance imaging-guided photothermal therapy. Nanoscale 2018, 10, 14190–14200.

    CAS  Google Scholar 

  92. Janetanakit, W.; Wang, L. P.; Santacruz-Gomez, K.; Landon, P. B.; Sud, P. L.; Patel, N.; Jang, G.; Jain, M.; Yepremyan, A.; Kazmi, S. A. et al. Gold-embedded hollow silica nanogolf balls for imaging and photothermal therapy. ACS Appl. Mater. Interfaces 2017, 9, 27533–27543.

    CAS  Google Scholar 

  93. Zhou, H.; Yang, H.; Tang, L.; Wang, Y.; Li, Y.; Liu, N.; Zeng, X. D.; Yan, Y.; Wu, J. Z.; Chen, S. Z. et al. Mn-loaded apolactoferrin dots for in vivo MRI and NIR-II cancer imaging. J. Mater. Chem. C 2019, 7, 9448–9454.

    CAS  Google Scholar 

  94. Sun, Y. H.; Chen, H. D.; Liu, G. F.; Ma, L. N.; Wang, Z. X. The controllable growth of ultrathin MnO2 on polydopamine nanospheres as a single nanoplatform for the MRI-guided synergistic therapy of tumors. J. Mater. Chem. B 2019, 7, 7152–7161.

    CAS  Google Scholar 

  95. Tian, X. T.; Cao, P. P.; Zhang, H.; Li, Y. H.; Yin, X. B. GSH-activated MRI-guided enhanced photodynamic- and chemo-combination therapy with a MnO2-coated porphyrin metal organic framework. Chem. Commun. 2019, 55, 6241–6244.

    CAS  Google Scholar 

  96. Fragai, M.; Ravera, E.; Tedoldi, F.; Luchinat, C.; Parigi, G. Relaxivity of Gd-based MRI contrast agents in crosslinked hyaluronic acid as a model for tissues. ChemPhysChem 2019, 20, 2204–2209.

    CAS  Google Scholar 

  97. Liang, S.; Deng, X. R.; Chang, Y.; Sun, C. Q.; Shao, S.; Xie, Z. X.; Xiao, X.; Ma, P. A.; Zhang, H. Y.; Cheng, Z. Y. et al. Intelligent hollow Pt-CuS Janus architecture for synergistic catalysis-enhanced sonodynamic and photothermal cancer therapy. Nano Lett. 2019, 19, 4134–4145.

    CAS  Google Scholar 

  98. Chen, F. H.; Zhang, L. M.; Chen, Q. T.; Zhang, Y.; Zhang, Z. J. Synthesis of a novel magnetic drug delivery system composed of doxorubicin-conjugated Fe3O4 nanoparticle cores and a PEG-functionalized porous silica shell. Chem. Commun. 2010, 46, 8633–8635.

    CAS  Google Scholar 

  99. Tuziuti, T.; Yasui, K.; Sivakumar, M.; Iida, Y.; Miyoshi, N. Correlation between acoustic cavitation noise and yield enhancement of sonochemical reaction by particle addition. J. Phys. Chem. A 2005, 109, 4869–4872.

    CAS  Google Scholar 

  100. Farny, C. H.; Wu, T. M.; Holt, R. G.; Murray, T. W.; Roy, R. A. Nucleating cavitation from laser-illuminated nano-particles. Acoust. Res. Lett. Online 2005, 6, 138–143.

    Google Scholar 

  101. Beik, J.; Khateri, M.; Khosravi, Z.; Kamrava, S. K.; Kooranifar, S.; Ghaznavi, H.; Shakeri-Zadeh, A. Gold nanoparticles in combinatorial cancer therapy strategies. Coord. Chem. Rev. 2019, 387, 299–324.

    CAS  Google Scholar 

  102. Sztandera, K.; Gorzkiewicz, M.; Klajnert-Maculewicz, B. Gold nanoparticles in cancer treatment. Mol. Pharmaceutics 2019, 16, 1–23.

    CAS  Google Scholar 

  103. Elahi, N.; Kamali, M.; Baghersad, M. H. Recent biomedical applications of gold nanoparticles: A review. Talanta 2018, 184, 537–556.

    CAS  Google Scholar 

  104. Kang, Z.; Yan, X. Q.; Zhao, L. Q.; Liao, Q. L.; Zhao, K.; Du, H. W.; Zhang, X. H.; Zhang, X. J.; Zhang, Y. Gold nanoparticle/ZnO nanorod hybrids for enhanced reactive oxygen species generation and photodynamic therapy. Nano Res. 2015, 8, 2004–2014.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  107. Cao, Y.; Wu, T. T.; Dai, W. H.; Dong, H. F.; Zhang, X. J. TiO2 nanosheets with the Au nanocrystal-decorated edge for mitochondria-targeting enhanced sonodynamic therapy. Chem. Mater. 2019, 31, 9105–9114.

    CAS  Google Scholar 

  108. Wei, B.; Dong, F.; Yang, W.; Luo, C. H.; Dong, Q. J.; Zhou, Z. Q.; Yang, Z.; Sheng, L. Q. Synthesis of carbon-dots@SiO2@TiO2 nanoplatform for photothermal imaging induced multimodal synergistic antitumor. J. Adv. Res. 2020, 23, 13–23.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  110. Ninomiya, K.; Noda, K.; Ogino, C.; Kuroda, S.; Shimizu, N. Enhanced OH radical generation by dual-frequency ultrasound with TiO2 nanoparticles: Its application to targeted sonodynamic therapy. Ultrason. Sonochem. 2014, 21, 289–294.

    CAS  Google Scholar 

  111. You, D. G.; Deepagan, V. G.; Um, W.; Jeon, S.; Son, S.; Chang, H.; Yoon, H. I.; Cho, Y. W.; Swierczewska, M.; Lee, S. et al. ROS-generating TiO2 nanoparticles for non-invasive sonodynamic therapy of cancer. Sci. Rep. 2016, 6, 23200.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  113. Ogino, C.; Shibata, N.; Sasai, R.; Takaki, K.; Miyachi, Y.; Kuroda, S.; Ninomiya, K.; Shimizu, N. Construction of protein-modified TiO2 nanoparticles for use with ultrasound irradiation in a novel cell injuring method. Bioorg. Med. Chem. Lett. 2010, 20, 5320–5325.

    CAS  Google Scholar 

  114. Ninomiya, K.; Fukuda, A.; Ogino, C.; Shimizu, N. Targeted sonocatalytic cancer cell injury using avidin-conjugated titanium dioxide nanoparticles. Ultrason. Sonochem. 2014, 21, 1624–1628.

    CAS  Google Scholar 

  115. McMaster, W. A.; Wang, X. J.; Caruso, R. A. Collagen-templated bioactive titanium dioxide porous networks for drug delivery. ACS Appl. Mater. Interfaces 2012, 4, 4717–4725.

    CAS  Google Scholar 

  116. Liu, D.; Bi, Y. G. Controllable fabrication of hollow TiO2 spheres as sustained release drug carrier. Adv. Powder Technol. 2019, 30, 2169–2177.

    CAS  Google Scholar 

  117. Shi, J. J.; Chen, Z. Y.; Wang, B. H.; Wang, L.; Lu, T. T.; Zhang, Z. Z. Reactive oxygen species-manipulated drug release from a smart envelope-type mesoporous titanium nanovehicle for tumor sonodynamic-chemotherapy. ACS Appl. Mater. Interfaces 2015, 7, 28554–28565.

    CAS  Google Scholar 

  118. Malekmohammadi, S.; Hadadzadeh, H.; Rezakhani, S.; Amirghofran, Z. Design and synthesis of gatekeeper coated dendritic silica/titania mesoporous nanoparticles with sustained and controlled drug release properties for targeted synergetic chemo-sonodynamic therapy. ACS Biomater. Sci. Eng. 2019, 5, 4405–4415.

    CAS  Google Scholar 

  119. Feng, Q. H.; Yang, X. M.; Hao, Y. T.; Wang, N.; Feng, X. B.; Hou, L.; Zhang, Z. Z. Cancer cell membrane-biomimetic nanoplatform for enhanced sonodynamic therapy on breast cancer via autophagy regulation strategy. ACS Appl. Mater. Interfaces 2019, 11, 32729–32738.

    CAS  Google Scholar 

  120. Gao, F. L.; He, G. L.; Yin, H.; Chen, J.; Liu, Y. B.; Lan, C.; Zhang, S. R.; Yang, B. C. Titania-coated 2D gold nanoplates as nanoagents for synergistic photothermal/sonodynamic therapy in the second near-infrared window. Nanoscale 2019, 11, 2374–2384.

    CAS  Google Scholar 

  121. Han, X. X.; Huang, J.; Jing, X. X.; Yang, D. Y.; Lin, H.; Wang, Z. G.; Li, P.; Chen, Y. Oxygen-deficient black titania for synergistic/enhanced sonodynamic and photoinduced cancer therapy at near infrared-II biowindow. ACS Nano 2018, 12, 4545–4555.

    CAS  Google Scholar 

  122. Wang, X. W.; Zhong, X. Y.; Bai, L. X.; Xu, J.; Gong, F.; Dong, Z. L.; Yang, Z. J.; Zeng, Z. J.; Liu, Z.; Cheng, L. Ultrafine titanium monoxide (TiO1+x) nanorods for enhanced sonodynamic therapy. J. Am. Chem. Soc. 2020, 142, 6527–6537.

    CAS  Google Scholar 

  123. Sviridov, A.; Tamarov, K.; Fesenko, I.; Xu, W. J.; Andreev, V.; Timoshenko, V.; Lehto, V. P. Cavitation induced by Janus-like mesoporous silicon nanoparticles enhances ultrasound hyperthermia. Front. Chem. 2019, 7, 393.

    Google Scholar 

  124. Osminkina, L. A.; Kudryavtsev, A. A.; Zinovyev, S. V.; Sviridov, A. P.; Kargina, Y. V.; Tamarov, K. P.; Nikiforov, V. N.; Ivanov, A. V.; Vasilyev, A. N.; Timoshenko, V. Y. Silicon nanoparticles as amplifiers of the ultrasonic effect in sonodynamic therapy. Bull. Exp. Biol. Med. 2016, 161, 296–299.

    CAS  Google Scholar 

  125. Osminkina, L. A.; Sivakov, V. A.; Mysov, G. A.; Georgobiani, V. A.; Natashina, U. A.; Talkenberg, F.; Solovyev, V. V.; Kudryavtsev, A. A.; Timoshenko, V. Y. Nanoparticles prepared from porous silicon nanowires for bio-imaging and sonodynamic therapy. Nanoscale Res. Lett. 2014, 9, 463.

    Google Scholar 

  126. Osminkina, L. A.; Nikolaev, A. L.; Sviridov, A. P.; Andronova, N. V.; Tamarov, K. P.; Gongalsky, M. B.; Kudryavtsev, A. A.; Treshalina, H. M.; Timoshenko, V. Y. Porous silicon nanoparticles as efficient sensitizers for sonodynamic therapy of cancer. Micropor. Mesopor. Mater. 2015, 210, 169–175.

    CAS  Google Scholar 

  127. Sviridov, A. P.; Osminkina, L. A.; Nikolaev, A. L.; Kudryavtsev, A. A.; Vasiliev, A. N.; Timoshenko, V. Y. Lowering of the cavitation threshold in aqueous suspensions of porous silicon nanoparticles for sonodynamic therapy applications. Appl. Phys. Lett. 2015, 107, 123107.

    Google Scholar 

  128. Gorgizadeh, M.; Azarpira, N.; Lotfi, M.; Daneshvar, F.; Salehi, F.; Sattarahmady, N. Sonodynamic cancer therapy by a nickel ferrite/carbon nanocomposite on melanoma tumor: In vitro and in vivo studies. Photodiagn. Photodyn. Ther. 2019, 27, 27–33.

    CAS  Google Scholar 

  129. Gong, F.; Cheng, L.; Yang, N. L.; Betzer, O.; Feng, L. Z.; Zhou, Q.; Li, Y. G.; Chen, R. H.; Popovtzer, R.; Liu, Z. Ultrasmall oxygen-deficient bimetallic oxide MnWOx nanoparticles for depletion of endogenous GSH and enhanced sonodynamic cancer therapy. Adv. Mater. 2019, 31, 1900730.

    Google Scholar 

  130. Li, C.; Yang, X. Q.; An, J.; Cheng, K.; Hou, X. L.; Zhang, X. S.; Hu, Y. G.; Liu, B.; Zhao, Y. D. Red blood cell membrane-enveloped O2 self-supplementing biomimetic nanoparticles for tumor imaging-guided enhanced sonodynamic therapy. Theranostics 2020, 10, 867–887.

    CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 61805287), National Science Foundation of Hunan Province, China (No. 2019JJ50824), and the Fundamental Research Funds for Central Universities of the Central South University (Nos. 202045002, 2019zzts432 and 2020CX021).

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Authors and Affiliations

  1. Hunan Provincial Key Laboratory of Micro & Nano Materials Interface Science, College of Chemistry and Chemical Engineering, Central South University, Changsha, 410083, China

    Ting Xu, Shaojing Zhao & Minhuan Lan

  2. Department of Gastrointestinal surgery, The Third Xiang Ya Hospital of Central South University, Changsha, 410013, China

    Changwei Lin

  3. Key Laboratory of Photochemical Conversion and Optoelectronic Materials and City U-CAS Joint Laboratory of Functional Materials and Devices, Technical Institute of Physics and Chemistry (TIPC), Chinese Academy of Sciences, Beijing, 100190, China

    Xiuli Zheng

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  1. Ting Xu
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  2. Shaojing Zhao
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  3. Changwei Lin
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  4. Xiuli Zheng
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  5. Minhuan Lan
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Correspondence to Changwei Lin, Xiuli Zheng or Minhuan Lan.

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Xu, T., Zhao, S., Lin, C. et al. Recent advances in nanomaterials for sonodynamic therapy. Nano Res. 13, 2898–2908 (2020). https://doi.org/10.1007/s12274-020-2992-5

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