Nanomaterials Enhanced Sonodynamic Therapy for Multiple Tumor Treatment
Corresponding Author: Aibing Chen
Nano-Micro Letters,
Vol. 17 (2025), Article Number: 157
Abstract
Sonodynamic therapy (SDT) as an emerging modality for malignant tumors mainly involves in sonosensitizers and low-intensity ultrasound (US), which can safely penetrate the tissue without significant attenuation. SDT not only has the advantages including high precision, non-invasiveness, and minimal side effects, but also overcomes the limitation of low penetration of light to deep tumors. The cytotoxic reactive oxygen species can be produced by the utilization of sonosensitizers combined with US and kill tumor cells. However, the underlying mechanism of SDT has not been elucidated, and its unsatisfactory efficiency retards its further clinical application. Herein, we shed light on the main mechanisms of SDT and the types of sonosensitizers, including organic sonosensitizers and inorganic sonosensitizers. Due to the development of nanotechnology, many novel nanoplatforms are utilized in this arisen field to solve the barriers of sonosensitizers and enable continuous innovation. This review also highlights the potential advantages of nanosonosensitizers and focus on the enhanced efficiency of SDT based on nanosonosensitizers with monotherapy or synergistic therapy for deep tumors that are difficult to reach by traditional treatment, especially orthotopic cancers.
Highlights:
1 The main mechanisms and clinical potential of sonodynamic therapy are emphasized.
2 The nanomaterials provide new prospects and development directions for enhancing the treatment of cancer.
3 Recent developments of sonodynamic therapy for deep tumors that are difficult to reach by traditional treatment, especially orthotopic cancers.
Keywords
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- F. Bray, M. Laversanne, E. Weiderpass, I. Soerjomataram, The ever-increasing importance of cancer as a leading cause of premature death worldwide. Cancer 127, 3029–3030 (2021). https://doi.org/10.1002/cncr.33587
- X. Zhang, L. Cheng, Y. Lu, J. Tang, Q. Lv et al., A MXene-based bionic cascaded-enzyme nanoreactor for tumor phototherapy/enzyme dynamic therapy and hypoxia-activated chemotherapy. Nano-Micro Lett. 14, 22 (2021). https://doi.org/10.1007/s40820-021-00761-w
- H. Sung, J. Ferlay, R.L. Siegel, M. Laversanne, I. Soerjomataram, A. Jemal, F. Bray, Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer J. Clin. 71, 209–249 (2021). https://doi.org/10.3322/caac.21660
- V.-N. Nguyen, T.N.T. Dao, M. Cho, H. Jeong, M.-T. Nguyen-Le et al., Recent advances in extracellular vesicle-based organic nanotherapeutic drugs for precision cancer therapy. Coord. Chem. Rev. 479, 215006 (2023). https://doi.org/10.1016/j.ccr.2022.215006
- C. Holohan, S. Van Schaeybroeck, D.B. Longley, P.G. Johnston, Cancer drug resistance: an evolving paradigm. Nat. Rev. Cancer 13, 714–726 (2013). https://doi.org/10.1038/nrc3599
- L. Cai, P. Zhu, F. Huan, J. Wang, L. Zhou et al., Toxicity-attenuated mesoporous silica Schiff-base bonded anticancer drug complexes for chemotherapy of drug resistant cancer. Colloids Surf. B Biointerfaces 205, 111839 (2021). https://doi.org/10.1016/j.colsurfb.2021.111839
- Y.-Y. Zhao, H. Kim, V.-N. Nguyen, S. Jang, W.J. Jang et al., Recent advances and prospects in organic molecule-based phototheranostic agents for enhanced cancer phototherapy. Coord. Chem. Rev. 501, 215560 (2024). https://doi.org/10.1016/j.ccr.2023.215560
- Y. Gao, Y. Liu, X. Li, H. Wang, Y. Yang et al., A stable open-shell conjugated diradical polymer with ultra-high photothermal conversion efficiency for NIR-II photo-immunotherapy of metastatic tumor. Nano-Micro Lett. 16, 21 (2023). https://doi.org/10.1007/s40820-023-01219-x
- Z. Xie, T. Fan, J. An, W. Choi, Y. Duo et al., Emerging combination strategies with phototherapy in cancer nanomedicine. Chem. Soc. Rev. 49, 8065–8087 (2020). https://doi.org/10.1039/d0cs00215a
- M. Yang, Z. Özdemir, H. Kim, S. Nah, E. Andris et al., Acid-responsive nanoporphyrin evolution for near-infrared fluorescence-guided photo-ablation of biofilm. Adv. Healthc. Mater. 11, e2200529 (2022). https://doi.org/10.1002/adhm.202200529
- L. Jin, S. Zhou, T. Zhang, F. Cui, H. Yu et al., A multi-functional cascade nanoreactor for remodeling tumor microenvironment to realize mitochondria dysfunction via ROS/Zn2+ ions overload. Small 2408639 (2024). https://doi.org/10.1002/smll.202408639
- M. Yang, X. Li, G. Kim, R. Wang, S.-J. Hong et al., A J-aggregated nanoporphyrin overcoming phototoxic side effects in superior phototherapy with two-pronged effects. Chem. Sci. 13, 12738–12746 (2022). https://doi.org/10.1039/d2sc04873f
- Z. Xie, Y. Duo, T. Fan, Y. Zhu, S. Feng et al., Light-induced tumor theranostics based on chemical-exfoliated borophene. Light Sci. Appl. 11, 324 (2022). https://doi.org/10.1038/s41377-022-00980-9
- M. Yang, X. Li, J. Yoon, Activatable supramolecular photosensitizers: advanced design strategies. Mater. Chem. Front. 5, 1683–1693 (2021). https://doi.org/10.1039/D0QM00827C
- R. Chang, Q. Zou, L. Zhao, Y. Liu, R. Xing et al., Amino-acid-encoded supramolecular photothermal nanomedicine for enhanced cancer therapy. Adv. Mater. 34, 2200139 (2022). https://doi.org/10.1002/adma.202200139
- J. Zou, J. Zhu, Z. Yang, L. Li, W. Fan et al., A phototheranostic strategy to continuously deliver singlet oxygen in the dark and hypoxic tumor microenvironment. Angew. Chem. Int. Ed. 59, 8833–8838 (2020). https://doi.org/10.1002/anie.201914384
- M. Li, Y. Shao, J.H. Kim, Z. Pu, X. Zhao et al., Unimolecular photodynamic O2-economizer to overcome hypoxia resistance in phototherapeutics. J. Am. Chem. Soc. 142, 5380–5388 (2020). https://doi.org/10.1021/jacs.0c00734
- M. Tavakkoli Yaraki, B. Liu, Y.N. Tan, Emerging strategies in enhancing singlet oxygen generation of nano-photosensitizers toward advanced phototherapy. Nano-Micro Lett. 14, 123 (2022). https://doi.org/10.1007/s40820-022-00856-y
- R. Li, T. Yang, X. Peng, Q. Feng, Y. Hou et al., Enhancing the photosensitivity of hypocrellin a by perylene diimide metallacage-based host-guest complexation for photodynamic therapy. Nano-Micro Lett. 16, 226 (2024). https://doi.org/10.1007/s40820-024-01438-w
- S. Li, R. Chang, L. Zhao, R. Xing, J.C.M. van Hest et al., Two-photon nanoprobes based on bioorganic nanoarchitectonics with a photo-oxidation enhanced emission mechanism. Nat. Commun. 14, 5227 (2023). https://doi.org/10.1038/s41467-023-40897-4
- P. Agostinis, K. Berg, K.A. Cengel, T.H. Foster, A.W. Girotti et al., Photodynamic therapy of cancer: an update. CA A Cancer J. Clin. 61, 250–281 (2011). https://doi.org/10.3322/caac.20114
- H. Yang, R. Liu, Y. Xu, L. Qian, Z. Dai, Photosensitizer nanops boost photodynamic therapy for pancreatic cancer treatment. Nano-Micro Lett. 13, 35 (2021). https://doi.org/10.1007/s40820-020-00561-8
- R. Chang, L. Zhao, R. Xing, J. Li, X. Yan, Functional chromopeptide nanoarchitectonics: molecular design, self-assembly and biological applications. Chem. Soc. Rev. 52, 2688–2712 (2023). https://doi.org/10.1039/d2cs00675h
- X. Pang, D. Li, J. Zhu, J. Cheng, G. Liu, Beyond antibiotics: photo/sonodynamic approaches for bacterial theranostics. Nano-Micro Lett. 12, 144 (2020). https://doi.org/10.1007/s40820-020-00485-3
- J. Ouyang, A. Xie, J. Zhou, R. Liu, L. Wang et al., Minimally invasive nanomedicine: nanotechnology in photo-/ ultrasound-/ radiation-/ magnetism-mediated therapy and imaging. Chem. Soc. Rev. 51, 4996–5041 (2022). https://doi.org/10.1039/d1cs01148k
- C. Firschke, J.R. Lindner, N.C. Goodman, D.M. Skyba, K. Wei et al., Myocardial contrast echocardiography in acute myocardial infarction using aortic root injections of microbubbles in conjunction with harmonic imaging: potential application in the cardiac catheterization laboratory. J. Am. Coll. Cardiol. 29, 207–216 (1997). https://doi.org/10.1016/S0735-1097(96)00426-3
- G. Salomon, J. Köllerman, I. Thederan, F.K.H. Chun, L. Budäus et al., Evaluation of prostate cancer detection with ultrasound real-time elastography: a comparison with step section pathological analysis after radical prostatectomy. Eur. Urol. 54, 1354–1362 (2008). https://doi.org/10.1016/j.eururo.2008.02.035
- S.-I. Umemura, N. Yumita, R. Nishigaki, K. Umemura, Sonochemical activation of hematoporphyrin: a potential modality for cancer treatment. In: Proceedings., IEEE Ultrasonics Symposium. October 3-6, 1989, Montreal, QC, Canada. IEEE, (1989)., 955–960
- S. Umemura, K. Kawabata, N. Yumita, R. Nishigaki, K. Umemura, Sonodynamic approach to tumor treatment. In: IEEE 1992 Ultrasonics Symposium Proceedings. October 20-23, 1992, Tucson, AZ, USA. IEEE, (2002)., 1231–1240.
- R. Canaparo, F. Foglietta, N. Barbero, L. Serpe, The promising interplay between sonodynamic therapy and nanomedicine. Adv. Drug Deliv. Rev. 189, 114495 (2022). https://doi.org/10.1016/j.addr.2022.114495
- Z. Gong, Z. Dai, Design and challenges of sonodynamic therapy system for cancer theranostics: from equipment to sensitizers. Adv. Sci. 8, 2002178 (2021). https://doi.org/10.1002/advs.202002178
- X. Lin, J. Song, X. Chen, H. Yang, Ultrasound-activated sensitizers and applications. Angew. Chem. Int. Ed. 59, 14212–14233 (2020). https://doi.org/10.1002/anie.201906823
- S. Sun, M. Wu, Sonodynamic therapy: another “light” in tumor treatment by exogenous stimulus. Smart Mater. Med. 2, 145–149 (2021). https://doi.org/10.1016/j.smaim.2021.05.001
- Y. Zhu, G. Arkin, T. He, F. Guo, L. Zhang et al., Ultrasound imaging guided targeted sonodynamic therapy enhanced by magnetophoretically controlled magnetic microbubbles. Int. J. Pharm. 655, 124015 (2024). https://doi.org/10.1016/j.ijpharm.2024.124015
- C. McEwan, H. Nesbitt, D. Nicholas, O.N. Kavanagh, K. McKenna et al., Comparing the efficacy of photodynamic and sonodynamic therapy in non-melanoma and melanoma skin cancer. Bioorg. Med. Chem. 24, 3023–3028 (2016). https://doi.org/10.1016/j.bmc.2016.05.015
- Z. Jiang, W. Xiao, Q. Fu, Stimuli responsive nanosonosensitizers for sonodynamic therapy. J. Control. Release 361, 547–567 (2023). https://doi.org/10.1016/j.jconrel.2023.08.003
- S. Liang, X. Deng, P.-A. Ma, Z. Cheng, J. Lin, Recent advances in nanomaterial-assisted combinational sonodynamic cancer therapy. Adv. Mater. 32, 2003214 (2020). https://doi.org/10.1002/adma.202003214
- S. Liang, J. Yao, D. Liu, L. Rao, X. Chen et al., Harnessing nanomaterials for cancer sonodynamic immunotherapy. Adv. Mater. 35, 2211130 (2023). https://doi.org/10.1002/adma.202211130
- D.F. Quail, J.A. Joyce, Microenvironmental regulation of tumor progression and metastasis. Nat. Med. 19, 1423–1437 (2013). https://doi.org/10.1038/nm.3394
- L. Li, Z. Yu, J. Liu, M. Yang, G. Shi et al., Swarming responsive photonic nanorobots for motile-targeting microenvironmental mapping and mapping-guided photothermal treatment. Nano-Micro Lett. 15, 141 (2023). https://doi.org/10.1007/s40820-023-01095-5
- Y. Zhang, X. Zhang, H. Yang, L. Yu, Y. Xu et al., Advanced biotechnology-assisted precise sonodynamic therapy. Chem. Soc. Rev. 50, 11227–11248 (2021). https://doi.org/10.1039/d1cs00403d
- M. Xu, L. Zhou, L. Zheng, Q. Zhou, K. Liu et al., Sonodynamic therapy-derived multimodal synergistic cancer therapy. Cancer Lett. 497, 229–242 (2021). https://doi.org/10.1016/j.canlet.2020.10.037
- S. Li, W. Zhang, R. Xing, C. Yuan, H. Xue et al., Supramolecular nanofibrils formed by coassembly of clinically approved drugs for tumor photothermal immunotherapy. Adv. Mater. 33, e2100595 (2021). https://doi.org/10.1002/adma.202100595
- R. Xing, Q. Zou, C. Yuan, L. Zhao, R. Chang et al., Self-assembling endogenous biliverdin as a versatile near-infrared photothermal nanoagent for cancer theranostics. Adv. Mater. 31, e1900822 (2019). https://doi.org/10.1002/adma.201900822
- H. Wang, Q. Liu, K. Zhang, P. Wang, Q. Xue et al., Comparison between sonodynamic and photodynamic effect on MDA-MB-231 cells. J. Photochem. Photobiol. B. 127, 182–191 (2013). https://doi.org/10.1016/j.jphotobiol.2013.08.015
- W. Qin, Q. Yang, C. Zhu, R. Jiao, X. Lin et al., A distinctive insight into inorganic sonosensitizers: design principles and application domains. Small 20, 2311228 (2024). https://doi.org/10.1002/smll.202311228
- X. Wang, X. Zhong, F. Gong, Y. Chao, L. Cheng, Newly developed strategies for improving sonodynamic therapy. Mater. Horiz. 7, 2028–2046 (2020). https://doi.org/10.1039/d0mh00613k
- R. Wang, Q. Liu, A. Gao, N. Tang, Q. Zhang et al., Recent developments of sonodynamic therapy in antibacterial application. Nanoscale 14, 12999–13017 (2022). https://doi.org/10.1039/d2nr01847k
- P. Tharkar, R. Varanasi, W.S.F. Wong, C.T. Jin, W. Chrzanowski, Nano-enhanced drug delivery and therapeutic ultrasound for cancer treatment and beyond. Front. Bioeng. Biotechnol. 7, 324 (2019). https://doi.org/10.3389/fbioe.2019.00324
- X. Qian, Y. Zheng, Y. Chen, Micro/nanop-augmented sonodynamic therapy (SDT): breaking the depth shallow of photoactivation. Adv. Mater. 28, 8097–8129 (2016). https://doi.org/10.1002/adma.201602012
- Y. He, D. Xing, S. Tan, Y. Tang, K.-I. Ueda, In vivo sonoluminescence imaging with the assistance of FCLA. Phys. Med. Biol. 47, 1535–1541 (2002). https://doi.org/10.1088/0031-9155/47/9/308
- Y. Yin, X. Jiang, L. Sun, H. Li, C. Su et al., Continuous inertial cavitation evokes massive ROS for reinforcing sonodynamic therapy and immunogenic cell death against breast carcinoma. Nano Today 36, 101009 (2021). https://doi.org/10.1016/j.nantod.2020.101009
- L. Fan, A. Idris Muhammad, B. Bilyaminu Ismail, D. Liu, Sonodynamic antimicrobial chemotherapy: an emerging alternative strategy for microbial inactivation. Ultrason Sonochem 75, 105591 (2021). https://doi.org/10.1016/j.ultsonch.2021.105591
- C. McEwan, S. Kamila, J. Owen, H. Nesbitt, B. Callan et al., Combined sonodynamic and antimetabolite therapy for the improved treatment of pancreatic cancer using oxygen loaded microbubbles as a delivery vehicle. Biomaterials 80, 20–32 (2016). https://doi.org/10.1016/j.biomaterials.2015.11.033
- I. Rosenthal, J.Z. Sostaric, P. Riesz, Sonodynamic therapy: a review of the synergistic effects of drugs and ultrasound. Ultrason. Sonochem. 11, 349–363 (2004). https://doi.org/10.1016/j.ultsonch.2004.03.004
- Y. Tang, L. Ge, L. Jiang, X. Jiang, Pore-enhanced reactive oxygen species generation by using covalent organic frameworks for improving sonodynamic therapy of cancer. Nano Today 55, 102166 (2024). https://doi.org/10.1016/j.nantod.2024.102166
- G.Y. Wan, Y. Liu, B.W. Chen, Y.Y. Liu, Y.S. Wang et al., Recent advances of sonodynamic therapy in cancer treatment. Cancer Biol. Med. 13, 325–338 (2016). https://doi.org/10.20892/j.issn.2095-3941.2016.0068
- S. Liao, M. Cai, R. Zhu, T. Fu, Y. Du et al., Antitumor effect of photodynamic therapy/sonodynamic therapy/sono-photodynamic therapy of chlorin e6 and other applications. Mol. Pharm. 20, 875–885 (2023). https://doi.org/10.1021/acs.molpharmaceut.2c00824
- X. Xing, S. Zhao, T. Xu, L. Huang, Y. Zhang et al., Advances and perspectives in organic sonosensitizers for sonodynamic therapy. Coord. Chem. Rev. 445, 214087 (2021). https://doi.org/10.1016/j.ccr.2021.214087
- H. Chen, X. Zhou, Y. Gao, B. Zheng, F. Tang et al., Recent progress in development of new sonosensitizers for sonodynamic cancer therapy. Drug Discov. Today 19, 502–509 (2014). https://doi.org/10.1016/j.drudis.2014.01.010
- S. Son, J.H. Kim, X. Wang, C. Zhang, S.A. Yoon et al., Multifunctional sonosensitizers in sonodynamic cancer therapy. Chem. Soc. Rev. 49, 3244–3261 (2020). https://doi.org/10.1039/c9cs00648f
- M. Zhang, D. Yang, C. Dong, H. Huang, G. Feng et al., Two-dimensional MXene-originated in situ nanosonosensitizer generation for augmented and synergistic sonodynamic tumor nanotherapy. ACS Nano 16, 9938–9952 (2022). https://doi.org/10.1021/acsnano.2c04630
- B. Geng, J. Hu, Y. Li, S. Feng, D. Pan et al., Near-infrared phosphorescent carbon dots for sonodynamic precision tumor therapy. Nat. Commun. 13, 5735 (2022). https://doi.org/10.1038/s41467-022-33474-8
- L.A. Osminkina, A.A. Kudryavtsev, S.V. Zinovyev, A.P. Sviridov, Y.V. Kargina et al., Silicon nanops as amplifiers of the ultrasonic effect in sonodynamic therapy. Bull. Exp. Biol. Med. 161, 296–299 (2016). https://doi.org/10.1007/s10517-016-3399-x
- J. Zhu, A. Ouyang, Z. Shen, Z. Pan, S. Banerjee et al., Sonodynamic cancer therapy by novel iridium-gold nanoassemblies. Chin. Chem. Lett. 33, 1907–1912 (2022). https://doi.org/10.1016/j.cclet.2021.11.017
- L. Raspagliesi, A. D’Ammando, M. Gionso, N.D. Sheybani, M.B. Lopes et al., Intracranial sonodynamic therapy with 5-aminolevulinic acid and sodium fluorescein: safety study in a porcine model. Front. Oncol. 11, 679989 (2021). https://doi.org/10.3389/fonc.2021.679989
- X. Zhang, C. Li, Y. Zhang, X. Guan, L. Mei et al., Construction of long-wavelength emissive organic nanosonosensitizer targeting mitochondria for precise and efficient in vivo sonotherapy. Adv. Funct. Mater. 32, 2207259 (2022). https://doi.org/10.1002/adfm.202207259
- H.B. Cheng, H. Dai, X. Tan, H. Li, H. Liang et al., A facile, protein-derived supramolecular theranostic strategy for multimodal-imaging-guided photodynamic and photothermal immunotherapy in vivo. Adv. Mater. 34, e2109111 (2022). https://doi.org/10.1002/adma.202109111
- H.-B. Cheng, X. Cao, S. Zhang, K. Zhang, Y. Cheng et al., BODIPY as a multifunctional theranostic reagent in biomedicine: self-assembly, properties, and applications. Adv. Mater. 35, 2207546 (2023). https://doi.org/10.1002/adma.202207546
- X. Li, X. Sun, H. Chen, X. Chen, Y. Li et al., Exploring BODIPY derivatives as sonosensitizers for anticancer sonodynamic therapy. Eur. J. Med. Chem. 264, 116035 (2024). https://doi.org/10.1016/j.ejmech.2023.116035
- K. Liu, Z. Jiang, F. Zhao, W. Wang, F. Jäkle et al., Triarylboron-doped acenethiophenes as organic sonosensitizers for highly efficient sonodynamic therapy with low phototoxicity. Adv. Mater. 34, e2206594 (2022). https://doi.org/10.1002/adma.202206594
- P.-H. Zhao, Y.-L. Wu, X.-Y. Li, L.-L. Feng, L. Zhang et al., Aggregation-enhanced sonodynamic activity of phthalocyanine–artesunate conjugates. Angew. Chem. Int. Ed. 61, e202113506 (2022). https://doi.org/10.1002/anie.202113506
- C. Deng, J. Zhang, F. Hu, S. Han, M. Zheng et al., A GSH-responsive prodrug with simultaneous triple-activation capacity for photodynamic/sonodynamic combination therapy with inhibited skin phototoxicity. Small 20, e2400667 (2024). https://doi.org/10.1002/smll.202400667
- L. Sun, P. Wang, J. Zhang, Y. Sun, S. Sun et al., Design and application of inorganic nanops for sonodynamic cancer therapy. Biomater. Sci. 9, 1945–1960 (2021). https://doi.org/10.1039/d0bm01875a
- Y. Zeng, Q. Ouyang, Y. Yu, L. Tan, X. Liu et al., Defective homojunction porphyrin-based metal-organic frameworks for highly efficient sonodynamic therapy. Small Methods 7, e2201248 (2023). https://doi.org/10.1002/smtd.202201248
- X. Wang, X. Zhong, L. Cheng, Titanium-based nanomaterials for cancer theranostics. Coord. Chem. Rev. 430, 213662 (2021). https://doi.org/10.1016/j.ccr.2020.213662
- F. Gong, L. Cheng, N. Yang, Y. Gong, Y. Ni et al., Preparation of TiH1.924 nanodots by liquid-phase exfoliation for enhanced sonodynamic cancer therapy. Nat. Commun. 11, 3712 (2020). https://doi.org/10.1038/s41467-020-17485-x
- S. Yang, X. Wang, P. He, A. Xu, G. Wang et al., Graphene quantum dots with pyrrole N and pyridine N: superior reactive oxygen species generation efficiency for metal-free sonodynamic tumor therapy. Small 17, e2004867 (2021). https://doi.org/10.1002/smll.202004867
- S. Kwon, H. Ko, D.G. You, K. Kataoka, J.H. Park, Nanomedicines for reactive oxygen species mediated approach: an emerging paradigm for cancer treatment. Acc. Chem. Res. 52, 1771–1782 (2019). https://doi.org/10.1021/acs.accounts.9b00136
- Q. Jiang, B. Qiao, X. Lin, J. Cao, N. Zhang et al., A hydrogen peroxide economizer for on-demand oxygen production-assisted robust sonodynamic immunotherapy. Theranostics 12, 59–75 (2022). https://doi.org/10.7150/thno.64862
- L. Song, X. Hou, K.F. Wong, Y. Yang, Z. Qiu et al., Gas-filled protein nanostructures as cavitation nuclei for molecule-specific sonodynamic therapy. Acta Biomater. 136, 533–545 (2021). https://doi.org/10.1016/j.actbio.2021.09.010
- M.A. Subhan, S.S.K. Yalamarty, N. Filipczak, F. Parveen, V.P. Torchilin, Recent advances in tumor targeting via EPR effect for cancer treatment. J. Pers. Med. 11, 571 (2021). https://doi.org/10.3390/jpm11060571
- F. Bosca, F. Foglietta, A. Gimenez, R. Canaparo, G. Durando et al., Exploiting lipid and polymer nanocarriers to improve the anticancer sonodynamic activity of chlorophyll. Pharmaceutics 12, 605 (2020). https://doi.org/10.3390/pharmaceutics12070605
- X. Li, C.-Y. Kim, S. Lee, D. Lee, H.-M. Chung et al., Nanostructured phthalocyanine assemblies with protein-driven switchable photoactivities for biophotonic imaging and therapy. J. Am. Chem. Soc. 139, 10880–10886 (2017). https://doi.org/10.1021/jacs.7b05916
- M. Yang, C. Zhang, R. Wang, X. Wu, H. Li et al., Cancer immunotherapy elicited by immunogenic cell death based on smart nanomaterials. Small Meth. 7, 2201381 (2023). https://doi.org/10.1002/smtd.202201381
- H. Chen, L. Liu, A. Ma, T. Yin, Z. Chen et al., Noninvasively immunogenic sonodynamic therapy with manganese protoporphyrin liposomes against triple-negative breast cancer. Biomaterials 269, 120639 (2021). https://doi.org/10.1016/j.biomaterials.2020.120639
- W. Lei, C. Yang, Y. Wu, G. Ru, X. He et al., Nanocarriers surface engineered with cell membranes for cancer targeted chemotherapy. J. Nanobiotechnol. 20, 45 (2022). https://doi.org/10.1186/s12951-022-01251-w
- H. Yan, D. Shao, Y.-H. Lao, M. Li, H. Hu et al., Engineering cell membrane-based nanotherapeutics to target inflammation. Adv. Sci. 6, 1900605 (2019). https://doi.org/10.1002/advs.201900605
- P. Dash, A.M. Piras, M. Dash, Cell membrane coated nanocarriers - an efficient biomimetic platform for targeted therapy. J. Control. Release 327, 546–570 (2020). https://doi.org/10.1016/j.jconrel.2020.09.012
- Y. Zhang, J. Zhao, L. Zhang, Y. Zhao, Y. Zhang et al., A cascade nanoreactor for enhancing sonodynamic therapy on colorectal cancer via synergistic ROS augment and autophagy blockage. Nano Today 49, 101798 (2023). https://doi.org/10.1016/j.nantod.2023.101798
- X. Wang, M. Wu, H. Li, J. Jiang, S. Zhou et al., Enhancing penetration ability of semiconducting polymer nanops for sonodynamic therapy of large solid tumor. Adv. Sci. 9, e2104125 (2022). https://doi.org/10.1002/advs.202104125
- H. Li, J. Wang, H. Kim, X. Peng, J. Yoon, Activatable near-infrared versatile fluorescent and chemiluminescent dyes based on the dicyanomethylene-4H-pyran scaffold: from design to imaging and theranostics. Angew. Chem. Int. Ed. 63, e202311764 (2024). https://doi.org/10.1002/anie.202311764
- C. Deng, M. Zheng, S. Han, Y. Wang, J. Xin et al., GSH-activated porphyrin sonosensitizer prodrug for fluorescence imaging-guided cancer sonodynamic therapy. Adv. Funct. Mater. 33, 2300348 (2023). https://doi.org/10.1002/adfm.202300348
- J. Li, J. Wang, L. Xu, H. Chi, X. Liang et al., A class of activatable NIR-II photoacoustic dyes for high-contrast bioimaging. Angew. Chem. Int. Ed. 63, e202312632 (2024). https://doi.org/10.1002/anie.202312632
- S. Sun, D. Wang, R. Yin, P. Zhang, R. Jiang et al., A two-In-one nanoprodrug for photoacoustic imaging-guided enhanced sonodynamic therapy. Small 18, 2202558 (2022). https://doi.org/10.1002/smll.202202558
- F. Gong, L. Cheng, N. Yang, O. Betzer, L. Feng et al., Ultrasmall oxygen-deficient bimetallic oxide MnWOX nanops for depletion of endogenous GSH and enhanced sonodynamic cancer therapy. Adv. Mater. 31, e1900730 (2019). https://doi.org/10.1002/adma.201900730
- S. Li, W. Zhang, H. Xue, R. Xing, X. Yan, Tumor microenvironment-oriented adaptive nanodrugs based on peptide self-assembly. Chem. Sci. 11, 8644–8656 (2020). https://doi.org/10.1039/d0sc02937h
- X. Ren, D. Chen, Y. Wang, H. Li, Y. Zhang et al., Nanozymes-recent development and biomedical applications. J. Nanobiotechnology 20, 92 (2022). https://doi.org/10.1186/s12951-022-01295-y
- Y. Wang, D. Fei Gong, Z. Han, H. Lei, Y. Zhou et al., Oxygen-deficient molybdenum oxide nanosensitizers for ultrasound-enhanced cancer metalloimmunotherapy. Angew. Chem. Int. Ed. 62, e202215467 (2023). https://doi.org/10.1002/anie.202215467
- T. Nie, W. Zou, Z. Meng, L. Wang, T. Ying et al., Bioactive iridium nanoclusters with glutathione depletion ability for enhanced sonodynamic-triggered ferroptosis-like cancer cell death. Adv. Mater. 34, e2206286 (2022). https://doi.org/10.1002/adma.202206286
- Y. Duan, Y. Yu, P. Peilai Liu, Y. Gao, D. Xinyue Dai et al., Reticular chemistry-enabled sonodynamic activity of covalent organic frameworks for nanodynamic cancer therapy. Angew. Chem. Int. Ed. 62, e202302146 (2023). https://doi.org/10.1002/anie.202302146
- S. Zhang, S. Xia, L. Chen, Y. Chen, J. Zhou, Covalent organic framework nanobowls as activatable nanosensitizers for tumor-specific and ferroptosis-augmented sonodynamic therapy. Adv. Sci. 10, e2206009 (2023). https://doi.org/10.1002/advs.202206009
- P. Vaupel, F. Kallinowski, P. Okunieff, Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res. 49, 6449–6465 (1989). https://doi.org/10.1097/00002820-198912000-00001
- S. Mura, J. Nicolas, P. Couvreur, Stimuli-responsive nanocarriers for drug delivery. Nat. Mater. 12, 991–1003 (2013). https://doi.org/10.1038/nmat3776
- K. Yang, L. Yue, G. Yu, L. Rao, R. Tian et al., A hypoxia responsive nanoassembly for tumor specific oxygenation and enhanced sonodynamic therapy. Biomaterials 275, 120822 (2021). https://doi.org/10.1016/j.biomaterials.2021.120822
- X. Li, D. Lee, J.-D. Huang, J. Yoon, Phthalocyanine-assembled nanodots as photosensitizers for highly efficient Type I photoreactions in photodynamic therapy. Angew. Chem. Int. Ed. 57, 9885–9890 (2018). https://doi.org/10.1002/anie.201806551
- Z. Liu, Z. Yan, Y. Di, S. Yang, Y. Ning et al., Current advances in metal–organic frameworks for cancer nanodynamic therapies. Coord. Chem. Rev. 497, 215434 (2023). https://doi.org/10.1016/j.ccr.2023.215434
- L. Zhong, T. Yang, P. Li, L. Shi, J. Lai et al., Metal-organic framework-based nanotherapeutics with tumor hypoxia-relieving ability for synergistic sonodynamic/chemo-therapy. Front. Mater. 9, 841503 (2022). https://doi.org/10.3389/fmats.2022.841503
- H. Xiao, X. Li, B. Li, Y. Zhong, J. Qin et al., Sono-promoted drug penetration and extracellular matrix modulation potentiate sonodynamic therapy of pancreatic ductal adenocarcinoma. Acta Biomater. 161, 265–274 (2023). https://doi.org/10.1016/j.actbio.2023.02.038
- G. Li, X. Zhong, X. Wang, F. Gong, H. Lei et al., Titanium carbide nanosheets with defect structure for photothermal-enhanced sonodynamic therapy. Bioact. Mater. 8, 409–419 (2021). https://doi.org/10.1016/j.bioactmat.2021.06.021
- S. Liu, B. Wang, Y. Yu, Y. Liu, Z. Zhuang et al., Cationization-enhanced type I and type II ROS generation for photodynamic treatment of drug-resistant bacteria. ACS Nano 16, 9130–9141 (2022). https://doi.org/10.1021/acsnano.2c01206
- D. Chen, Q. Xu, W. Wang, J. Shao, W. Huang et al., Type I photosensitizers revitalizing photodynamic oncotherapy. Small 17, e2006742 (2021). https://doi.org/10.1002/smll.202006742
- J. Cao, Y. Sun, C. Zhang, X. Wang, Y. Zeng et al., Tablet-like TiO2/C nanocomposites for repeated type I sonodynamic therapy of pancreatic cancer. Acta Biomater. 129, 269–279 (2021). https://doi.org/10.1016/j.actbio.2021.05.029
- Z. Zhang, B. Li, L. Xie, W. Sang, H. Tian et al., Metal-phenolic network-enabled lactic acid consumption reverses immunosuppressive tumor microenvironment for sonodynamic therapy. ACS Nano 15, 16934–16945 (2021). https://doi.org/10.1021/acsnano.1c08026
- D.W. Felsher, Cancer revoked: oncogenes as therapeutic targets. Nat. Rev. Cancer 3, 375–380 (2003). https://doi.org/10.1038/nrc1070
- F. Cairnduff, M.R. Stringer, E.J. Hudson, D.V. Ash, S.B. Brown, Superficial photodynamic therapy with topical 5-aminolaevulinic acid for superficial primary and secondary skin cancer. Br. J. Cancer 69, 605–608 (1994). https://doi.org/10.1038/bjc.1994.112
- M. Zhan, F. Wang, Y. Liu, J. Zhou, W. Zhao et al., Dual-cascade activatable nanopotentiators reshaping adenosine metabolism for sono-chemodynamic-immunotherapy of deep tumors. Adv. Sci. 10, e2207200 (2023). https://doi.org/10.1002/advs.202207200
- T. Chen, W. Zeng, C. Tie, M. Yu, H. Hao et al., Engineered gold/black phosphorus nanoplatforms with remodeling tumor microenvironment for sonoactivated catalytic tumor theranostics. Bioact. Mater. 10, 515–525 (2021). https://doi.org/10.1016/j.bioactmat.2021.09.016
- T. Yamaguchi, S. Kitahara, K. Kusuda, J. Okamoto, Y. Horise et al., Current landscape of sonodynamic therapy for treating cancer. Cancers 13, 6184 (2021). https://doi.org/10.3390/cancers13246184
- M. Lafond, T. Lambin, R.A. Drainville, A. Dupré, M. Pioche et al., Pancreatic ductal adenocarcinoma: current and emerging therapeutic uses of focused ultrasound. Cancers 14, 2577 (2022). https://doi.org/10.3390/cancers14112577
- R.J. Browning, S. Able, J.-L. Ruan, L. Bau, P.D. Allen et al., Combining sonodynamic therapy with chemoradiation for the treatment of pancreatic cancer. J. Control. Release 337, 371–377 (2021). https://doi.org/10.1016/j.jconrel.2021.07.020
- S. Zeng, M. Pöttler, B. Lan, R. Grützmann, C. Pilarsky et al., Chemoresistance in pancreatic cancer. Int. J. Mol. Sci. 20, 4504 (2019). https://doi.org/10.3390/ijms20184504
- M.H. Sherman, G.L. Beatty, Tumor microenvironment in pancreatic cancer pathogenesis and therapeutic resistance. Annu. Rev. Pathol. Mech. Dis. 18, 123–148 (2023). https://doi.org/10.1146/annurev-pathmechdis-031621-024600
- T. Zhang, Y. Sun, J. Cao, J. Luo, J. Wang et al., Intrinsic nucleus-targeted ultra-small metal-organic framework for the type I sonodynamic treatment of orthotopic pancreatic carcinoma. J. Nanobiotechnol. 19, 315 (2021). https://doi.org/10.1186/s12951-021-01060-7
- Y. He, T. Wang, Y. Song, C. Fang, Y. Wang et al., Targeting vascular destruction by sonosensitizer-free sonocatalytic nanomissiles instigates Thrombus aggregation and nutrition deprivation to starve pancreatic cancer. Adv. Funct. Mater. 34, 2315394 (2024). https://doi.org/10.1002/adfm.202315394
- Z. Tang, Y. Liu, M. He, W. Bu, Chemodynamic therapy: tumour microenvironment-mediated Fenton and Fenton-like reactions. Angew. Chem. Int. Ed. 58, 946–956 (2019). https://doi.org/10.1002/anie.201805664
- Y. Pu, H. Yin, C. Dong, H. Xiang, W. Wu et al., Sono-controllable and ROS-sensitive CRISPR-Cas9 genome editing for augmented/synergistic ultrasound tumor nanotherapy. Adv. Mater. 33, e2104641 (2021). https://doi.org/10.1002/adma.202104641
- X. Zhong, X. Wang, L. Cheng, Y.-A. Tang, G. Zhan et al., GSH-depleted PtCu3 nanocages for chemodynamic- enhanced sonodynamic cancer therapy. Adv. Funct. Mater. 30, 1907954 (2020). https://doi.org/10.1002/adfm.201907954
- C. Fang, Z. Deng, G. Cao, Q. Chu, Y. Wu et al., Co–ferrocene MOF/glucose oxidase as cascade nanozyme for effective tumor therapy. Adv. Funct. Mater. 30, 1910085 (2020). https://doi.org/10.1002/adfm.201910085
- S. Liang, X. Xiao, L. Bai, B. Liu, M. Yuan et al., Conferring Ti-based MOFs with defects for enhanced sonodynamic cancer therapy. Adv. Mater. 33, e2100333 (2021). https://doi.org/10.1002/adma.202100333
- B. Xu, Z. Huang, Y. Liu, S. Li, H. Liu, MOF-based nanomedicines inspired by structures of natural active components. Nano Today 48, 101690 (2023). https://doi.org/10.1016/j.nantod.2022.101690
- Y. Sun, J. Cao, X. Wang, C. Zhang, J. Luo et al., Hypoxia-adapted sono-chemodynamic treatment of orthotopic pancreatic carcinoma using copper metal–organic frameworks loaded with an ultrasound-induced free radical initiator. ACS Appl. Mater. Interfaces 13, 38114–38126 (2021). https://doi.org/10.1021/acsami.1c11017
- A.D. Waldman, J.M. Fritz, M.J. Lenardo, A guide to cancer immunotherapy: from T cell basic science to clinical practice. Nat. Rev. Immunol. 20, 651–668 (2020). https://doi.org/10.1038/s41577-020-0306-5
- S. Gao, X. Yang, J. Xu, N. Qiu, G. Zhai, Nanotechnology for boosting cancer immunotherapy and remodeling tumor microenvironment: the horizons in cancer treatment. ACS Nano 15, 12567–12603 (2021). https://doi.org/10.1021/acsnano.1c02103
- Y. Xia, S. Fu, Q. Ma, Y. Liu, N. Zhang, Application of nano-delivery systems in lymph nodes for tumor immunotherapy. Nano-Micro Lett. 15, 145 (2023). https://doi.org/10.1007/s40820-023-01125-2
- H. Lei, J.H. Kim, S. Son, L. Chen, Z. Pei et al., Immunosonodynamic therapy designed with activatable sonosensitizer and immune stimulant imiquimod. ACS Nano 16, 10979–10993 (2022). https://doi.org/10.1021/acsnano.2c03395
- T. Wang, W. Peng, M. Du, Z. Chen, Immunogenic sonodynamic therapy for inducing immunogenic cell death and activating antitumor immunity. Front. Oncol. 13, 1167105 (2023). https://doi.org/10.3389/fonc.2023.1167105
- H. Nesbitt, K. Logan, K. Thomas, B. Callan, J. Gao et al., Sonodynamic therapy complements PD-L1 immune checkpoint inhibition in a murine model of pancreatic cancer. Cancer Lett. 517, 88–95 (2021). https://doi.org/10.1016/j.canlet.2021.06.003
- M. Wu, Q. Huang, Y. Xie, X. Wu, H. Ma et al., Improvement of the anticancer efficacy of PD-1/PD-L1 blockade via combination therapy and PD-L1 regulation. J. Hematol. Oncol. 15, 24 (2022). https://doi.org/10.1186/s13045-022-01242-2
- J. Chen, L. Feng, P. Jin, J. Shen, J. Lu et al., Cavitation assisted endoplasmic reticulum targeted sonodynamic droplets to enhanced anti-PD-L1 immunotherapy in pancreatic cancer. J. Nanobiotechnology 20, 283 (2022). https://doi.org/10.1186/s12951-022-01459-w
- J. Li, N. Yu, D. Cui, J. Huang, Y. Luo et al., Activatable semiconducting polymer pro-nanomodulators for deep-tissue sono-immunotherapy of orthotopic pancreatic cancer. Angew. Chem. Int. Ed. 62, e202305200 (2023). https://doi.org/10.1002/anie.202305200
- A.C. Lai, D. Momar Toure, D. Doris Hellerschmied, J. Salami, D. Saul Jaime-Figueroa et al., Modular PROTAC design for the degradation of oncogenic BCR-ABL. Angew. Chem. Int. Ed. 55, 807–810 (2016). https://doi.org/10.1002/anie.201507634
- S.-M. Qi, J. Dong, Z.-Y. Xu, X.-D. Cheng, W.-D. Zhang et al., PROTAC: an effective targeted protein degradation strategy for cancer therapy. Front. Pharmacol. 12, 692574 (2021). https://doi.org/10.3389/fphar.2021.692574
- M. Békés, D.R. Langley, C.M. Crews, PROTAC targeted protein degraders: the past is prologue. Nat. Rev. Drug Discov. 21, 181–200 (2022). https://doi.org/10.1038/s41573-021-00371-6
- S. He, Y. Fang, Y. Zhu, Z. Ma, G. Dong et al., Drugtamer-PROTAC conjugation strategy for targeted PROTAC delivery and synergistic antitumor therapy. Adv. Sci. 11, e2401623 (2024). https://doi.org/10.1002/advs.202401623
- J. Liu, H. Chen, L. Ma, Z. He, D. Wang et al., Light-induced control of protein destruction by opto-PROTAC. Sci. Adv. 6, eaay5154 (2020). https://doi.org/10.1126/sciadv.aay5154
- Z. Chen, L. Chen, Y. Ma, Y. Liu, Q. Zhang et al., Peptide-appended nanosonosensitizers targeting tumor glycolysis for synergistic sonodynamic-immunometabolic therapy of spinal-metastasized tumors. Adv. Mater. 35, e2304246 (2023). https://doi.org/10.1002/adma.202304246
- H. Tang, X. Xu, Y. Chen, H. Xin, T. Wan et al., Reprogramming the tumor microenvironment through second-near-infrared-window photothermal genome editing of PD-L1 mediated by supramolecular gold nanorods for enhanced cancer immunotherapy. Adv. Mater. 33, e2006003 (2021). https://doi.org/10.1002/adma.202006003
- Y. Liu, H. Wang, M. Ding, W. Yao, K. Wang et al., Ultrasound-activated PROTAC prodrugs overcome immunosuppression to actuate efficient deep-tissue sono-immunotherapy in orthotopic pancreatic tumor mouse models. Nano Lett. 24, 8741–8751 (2024). https://doi.org/10.1021/acs.nanolett.4c02287
- M. Li, Y. Liu, Y. Zhang, N. Yu, J. Li, Sono-activatable semiconducting polymer nanoreshapers multiply remodel tumor microenvironment for potent immunotherapy of orthotopic pancreatic cancer. Adv. Sci. 10, e2305150 (2023). https://doi.org/10.1002/advs.202305150
- L. Chen, W. Xue, J. Cao, S. Zhang, Y. Zeng et al., TiSe2-mediated sonodynamic and checkpoint blockade combined immunotherapy in hypoxic pancreatic cancer. J. Nanobiotechnol. 20, 453 (2022). https://doi.org/10.1186/s12951-022-01659-4
- X. Li, J.S. Oh, Y. Lee, E.C. Lee, M. Yang et al., Albumin-binding photosensitizer capable of targeting glioma via the SPARC pathway. Biomater. Res. 27, 23 (2023). https://doi.org/10.1186/s40824-023-00360-3
- H.-J. Liu, H.-M. Hu, G.-Z. Li, Y. Zhang, F. Wu et al., Ferroptosis-related gene signature predicts glioma cell death and glioma patient progression. Front. Cell Dev. Biol. 8, 538 (2020). https://doi.org/10.3389/fcell.2020.00538
- Y. Pan, C. Xu, H. Deng, Q. You, C. Zhao et al., Localized NIR-II laser mediated chemodynamic therapy of glioblastoma. Nano Today 43, 101435 (2022). https://doi.org/10.1016/j.nantod.2022.101435
- J.N. Sarkaria, L.S. Hu, I.F. Parney, D.H. Pafundi, D.H. Brinkmann et al., Is the blood–brain barrier really disrupted in all glioblastomas? A critical assessment of existing clinical data. Neuro Oncol. 20, 184–191 (2018). https://doi.org/10.1093/neuonc/nox175
- S. Watkins, S. Robel, I.F. Kimbrough, S.M. Robert, G. Ellis-Davies et al., Disruption of astrocyte–vascular coupling and the blood–brain barrier by invading glioma cells. Nat. Commun. 5, 4196 (2014). https://doi.org/10.1038/ncomms5196
- X. Wang, Y. Jia, P. Wang, Q. Liu, H. Zheng, Current status and future perspectives of sonodynamic therapy in glioma treatment. Ultrason. Sonochem. 37, 592–599 (2017). https://doi.org/10.1016/j.ultsonch.2017.02.020
- T. Jia, J. Du, J. Yang, Y. Li, T.Y. Ohulchanskyy et al., Metalloporphyrin MOFs-based nanoagent enabling tumor microenvironment responsive sonodynamic therapy of intracranial glioma signaled by NIR-IIb luminescence imaging. Adv. Funct. Mater. 34, 2307816 (2024). https://doi.org/10.1002/adfm.202307816
- Y. Zhu, X. Niu, C. Ding, Y. Lin, W. Fang et al., Carrier-free self-assembly nano-sonosensitizers for sonodynamic-amplified cuproptosis-ferroptosis in glioblastoma therapy. Adv. Sci. 11, e2402516 (2024). https://doi.org/10.1002/advs.202402516
- F. Qu, P. Wang, K. Zhang, Y. Shi, Y. Li et al., Manipulation of Mitophagy by “All-in-One” nanosensitizer augments sonodynamic glioma therapy. Autophagy 16, 1413–1435 (2020). https://doi.org/10.1080/15548627.2019.1687210
- Y. Sun, H. Wang, P. Wang, K. Zhang, X. Geng et al., Tumor targeting DVDMS-nanoliposomes for an enhanced sonodynamic therapy of gliomas. Biomater. Sci. 7, 985–994 (2019). https://doi.org/10.1039/c8bm01187g
- V.G. Abramson, B.D. Lehmann, T.J. Ballinger, J.A. Pietenpol, Subtyping of triple-negative breast cancer: implications for therapy. Cancer 121, 8–16 (2015). https://doi.org/10.1002/cncr.28914
- W. Pei, Y. Li, Y. Wu, Y. Wu, L. Cai et al., A tumoricidal lipoprotein complex electrostatically stabilized on mesoporous silica as nanotherapeutics and nanoadjuvant for potentiating immunotherapy of triple negative breast cancer. Adv. Funct. Mater. 33, 2308117 (2023). https://doi.org/10.1002/adfm.202308117
- T. Inui, K. Makita, H. Miura, A. Matsuda, D. Kuchiike et al., Case report: a breast cancer patient treated with GcMAF, sonodynamic therapy and hormone therapy. Anticancer Res 34, 4589–4593 (2014). https://doi.org/10.1016/j.urolonc.2014.05.010
- Y. Li, W. Chen, Y. Kang, X. Zhen, Z. Zhou et al., Nanosensitizer-mediated augmentation of sonodynamic therapy efficacy and antitumor immunity. Nat. Commun. 14, 6973 (2023). https://doi.org/10.1038/s41467-023-42509-7
- Y. Zheng, Z. Li, Y. Yang, H. Shi, H. Chen et al., A nanosensitizer self-assembled from oleanolic acid and chlorin e6 for synergistic chemo/sono-photodynamic cancer therapy. Phytomedicine 93, 153788 (2021). https://doi.org/10.1016/j.phymed.2021.153788
- X. Lin, T. He, R. Tang, Q. Li, N. Wu et al., Biomimetic nanoprobe-augmented triple therapy with photothermal, sonodynamic and checkpoint blockade inhibits tumor growth and metastasis. J. Nanobiotechnology 20, 80 (2022). https://doi.org/10.1186/s12951-022-01287-y
- G. Yuan, B. Yang, P. Chen, L. Bai, G. Qiao et al., Regulating manganese-site electronic structure via reconstituting nitrogen coordination for efficient non-oxygen-dependent sonocatalytic therapy against orthotopic breast cancer. ACS Nano 18, 27630–27641 (2024). https://doi.org/10.1021/acsnano.4c09052
References
F. Bray, M. Laversanne, E. Weiderpass, I. Soerjomataram, The ever-increasing importance of cancer as a leading cause of premature death worldwide. Cancer 127, 3029–3030 (2021). https://doi.org/10.1002/cncr.33587
X. Zhang, L. Cheng, Y. Lu, J. Tang, Q. Lv et al., A MXene-based bionic cascaded-enzyme nanoreactor for tumor phototherapy/enzyme dynamic therapy and hypoxia-activated chemotherapy. Nano-Micro Lett. 14, 22 (2021). https://doi.org/10.1007/s40820-021-00761-w
H. Sung, J. Ferlay, R.L. Siegel, M. Laversanne, I. Soerjomataram, A. Jemal, F. Bray, Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer J. Clin. 71, 209–249 (2021). https://doi.org/10.3322/caac.21660
V.-N. Nguyen, T.N.T. Dao, M. Cho, H. Jeong, M.-T. Nguyen-Le et al., Recent advances in extracellular vesicle-based organic nanotherapeutic drugs for precision cancer therapy. Coord. Chem. Rev. 479, 215006 (2023). https://doi.org/10.1016/j.ccr.2022.215006
C. Holohan, S. Van Schaeybroeck, D.B. Longley, P.G. Johnston, Cancer drug resistance: an evolving paradigm. Nat. Rev. Cancer 13, 714–726 (2013). https://doi.org/10.1038/nrc3599
L. Cai, P. Zhu, F. Huan, J. Wang, L. Zhou et al., Toxicity-attenuated mesoporous silica Schiff-base bonded anticancer drug complexes for chemotherapy of drug resistant cancer. Colloids Surf. B Biointerfaces 205, 111839 (2021). https://doi.org/10.1016/j.colsurfb.2021.111839
Y.-Y. Zhao, H. Kim, V.-N. Nguyen, S. Jang, W.J. Jang et al., Recent advances and prospects in organic molecule-based phototheranostic agents for enhanced cancer phototherapy. Coord. Chem. Rev. 501, 215560 (2024). https://doi.org/10.1016/j.ccr.2023.215560
Y. Gao, Y. Liu, X. Li, H. Wang, Y. Yang et al., A stable open-shell conjugated diradical polymer with ultra-high photothermal conversion efficiency for NIR-II photo-immunotherapy of metastatic tumor. Nano-Micro Lett. 16, 21 (2023). https://doi.org/10.1007/s40820-023-01219-x
Z. Xie, T. Fan, J. An, W. Choi, Y. Duo et al., Emerging combination strategies with phototherapy in cancer nanomedicine. Chem. Soc. Rev. 49, 8065–8087 (2020). https://doi.org/10.1039/d0cs00215a
M. Yang, Z. Özdemir, H. Kim, S. Nah, E. Andris et al., Acid-responsive nanoporphyrin evolution for near-infrared fluorescence-guided photo-ablation of biofilm. Adv. Healthc. Mater. 11, e2200529 (2022). https://doi.org/10.1002/adhm.202200529
L. Jin, S. Zhou, T. Zhang, F. Cui, H. Yu et al., A multi-functional cascade nanoreactor for remodeling tumor microenvironment to realize mitochondria dysfunction via ROS/Zn2+ ions overload. Small 2408639 (2024). https://doi.org/10.1002/smll.202408639
M. Yang, X. Li, G. Kim, R. Wang, S.-J. Hong et al., A J-aggregated nanoporphyrin overcoming phototoxic side effects in superior phototherapy with two-pronged effects. Chem. Sci. 13, 12738–12746 (2022). https://doi.org/10.1039/d2sc04873f
Z. Xie, Y. Duo, T. Fan, Y. Zhu, S. Feng et al., Light-induced tumor theranostics based on chemical-exfoliated borophene. Light Sci. Appl. 11, 324 (2022). https://doi.org/10.1038/s41377-022-00980-9
M. Yang, X. Li, J. Yoon, Activatable supramolecular photosensitizers: advanced design strategies. Mater. Chem. Front. 5, 1683–1693 (2021). https://doi.org/10.1039/D0QM00827C
R. Chang, Q. Zou, L. Zhao, Y. Liu, R. Xing et al., Amino-acid-encoded supramolecular photothermal nanomedicine for enhanced cancer therapy. Adv. Mater. 34, 2200139 (2022). https://doi.org/10.1002/adma.202200139
J. Zou, J. Zhu, Z. Yang, L. Li, W. Fan et al., A phototheranostic strategy to continuously deliver singlet oxygen in the dark and hypoxic tumor microenvironment. Angew. Chem. Int. Ed. 59, 8833–8838 (2020). https://doi.org/10.1002/anie.201914384
M. Li, Y. Shao, J.H. Kim, Z. Pu, X. Zhao et al., Unimolecular photodynamic O2-economizer to overcome hypoxia resistance in phototherapeutics. J. Am. Chem. Soc. 142, 5380–5388 (2020). https://doi.org/10.1021/jacs.0c00734
M. Tavakkoli Yaraki, B. Liu, Y.N. Tan, Emerging strategies in enhancing singlet oxygen generation of nano-photosensitizers toward advanced phototherapy. Nano-Micro Lett. 14, 123 (2022). https://doi.org/10.1007/s40820-022-00856-y
R. Li, T. Yang, X. Peng, Q. Feng, Y. Hou et al., Enhancing the photosensitivity of hypocrellin a by perylene diimide metallacage-based host-guest complexation for photodynamic therapy. Nano-Micro Lett. 16, 226 (2024). https://doi.org/10.1007/s40820-024-01438-w
S. Li, R. Chang, L. Zhao, R. Xing, J.C.M. van Hest et al., Two-photon nanoprobes based on bioorganic nanoarchitectonics with a photo-oxidation enhanced emission mechanism. Nat. Commun. 14, 5227 (2023). https://doi.org/10.1038/s41467-023-40897-4
P. Agostinis, K. Berg, K.A. Cengel, T.H. Foster, A.W. Girotti et al., Photodynamic therapy of cancer: an update. CA A Cancer J. Clin. 61, 250–281 (2011). https://doi.org/10.3322/caac.20114
H. Yang, R. Liu, Y. Xu, L. Qian, Z. Dai, Photosensitizer nanops boost photodynamic therapy for pancreatic cancer treatment. Nano-Micro Lett. 13, 35 (2021). https://doi.org/10.1007/s40820-020-00561-8
R. Chang, L. Zhao, R. Xing, J. Li, X. Yan, Functional chromopeptide nanoarchitectonics: molecular design, self-assembly and biological applications. Chem. Soc. Rev. 52, 2688–2712 (2023). https://doi.org/10.1039/d2cs00675h
X. Pang, D. Li, J. Zhu, J. Cheng, G. Liu, Beyond antibiotics: photo/sonodynamic approaches for bacterial theranostics. Nano-Micro Lett. 12, 144 (2020). https://doi.org/10.1007/s40820-020-00485-3
J. Ouyang, A. Xie, J. Zhou, R. Liu, L. Wang et al., Minimally invasive nanomedicine: nanotechnology in photo-/ ultrasound-/ radiation-/ magnetism-mediated therapy and imaging. Chem. Soc. Rev. 51, 4996–5041 (2022). https://doi.org/10.1039/d1cs01148k
C. Firschke, J.R. Lindner, N.C. Goodman, D.M. Skyba, K. Wei et al., Myocardial contrast echocardiography in acute myocardial infarction using aortic root injections of microbubbles in conjunction with harmonic imaging: potential application in the cardiac catheterization laboratory. J. Am. Coll. Cardiol. 29, 207–216 (1997). https://doi.org/10.1016/S0735-1097(96)00426-3
G. Salomon, J. Köllerman, I. Thederan, F.K.H. Chun, L. Budäus et al., Evaluation of prostate cancer detection with ultrasound real-time elastography: a comparison with step section pathological analysis after radical prostatectomy. Eur. Urol. 54, 1354–1362 (2008). https://doi.org/10.1016/j.eururo.2008.02.035
S.-I. Umemura, N. Yumita, R. Nishigaki, K. Umemura, Sonochemical activation of hematoporphyrin: a potential modality for cancer treatment. In: Proceedings., IEEE Ultrasonics Symposium. October 3-6, 1989, Montreal, QC, Canada. IEEE, (1989)., 955–960
S. Umemura, K. Kawabata, N. Yumita, R. Nishigaki, K. Umemura, Sonodynamic approach to tumor treatment. In: IEEE 1992 Ultrasonics Symposium Proceedings. October 20-23, 1992, Tucson, AZ, USA. IEEE, (2002)., 1231–1240.
R. Canaparo, F. Foglietta, N. Barbero, L. Serpe, The promising interplay between sonodynamic therapy and nanomedicine. Adv. Drug Deliv. Rev. 189, 114495 (2022). https://doi.org/10.1016/j.addr.2022.114495
Z. Gong, Z. Dai, Design and challenges of sonodynamic therapy system for cancer theranostics: from equipment to sensitizers. Adv. Sci. 8, 2002178 (2021). https://doi.org/10.1002/advs.202002178
X. Lin, J. Song, X. Chen, H. Yang, Ultrasound-activated sensitizers and applications. Angew. Chem. Int. Ed. 59, 14212–14233 (2020). https://doi.org/10.1002/anie.201906823
S. Sun, M. Wu, Sonodynamic therapy: another “light” in tumor treatment by exogenous stimulus. Smart Mater. Med. 2, 145–149 (2021). https://doi.org/10.1016/j.smaim.2021.05.001
Y. Zhu, G. Arkin, T. He, F. Guo, L. Zhang et al., Ultrasound imaging guided targeted sonodynamic therapy enhanced by magnetophoretically controlled magnetic microbubbles. Int. J. Pharm. 655, 124015 (2024). https://doi.org/10.1016/j.ijpharm.2024.124015
C. McEwan, H. Nesbitt, D. Nicholas, O.N. Kavanagh, K. McKenna et al., Comparing the efficacy of photodynamic and sonodynamic therapy in non-melanoma and melanoma skin cancer. Bioorg. Med. Chem. 24, 3023–3028 (2016). https://doi.org/10.1016/j.bmc.2016.05.015
Z. Jiang, W. Xiao, Q. Fu, Stimuli responsive nanosonosensitizers for sonodynamic therapy. J. Control. Release 361, 547–567 (2023). https://doi.org/10.1016/j.jconrel.2023.08.003
S. Liang, X. Deng, P.-A. Ma, Z. Cheng, J. Lin, Recent advances in nanomaterial-assisted combinational sonodynamic cancer therapy. Adv. Mater. 32, 2003214 (2020). https://doi.org/10.1002/adma.202003214
S. Liang, J. Yao, D. Liu, L. Rao, X. Chen et al., Harnessing nanomaterials for cancer sonodynamic immunotherapy. Adv. Mater. 35, 2211130 (2023). https://doi.org/10.1002/adma.202211130
D.F. Quail, J.A. Joyce, Microenvironmental regulation of tumor progression and metastasis. Nat. Med. 19, 1423–1437 (2013). https://doi.org/10.1038/nm.3394
L. Li, Z. Yu, J. Liu, M. Yang, G. Shi et al., Swarming responsive photonic nanorobots for motile-targeting microenvironmental mapping and mapping-guided photothermal treatment. Nano-Micro Lett. 15, 141 (2023). https://doi.org/10.1007/s40820-023-01095-5
Y. Zhang, X. Zhang, H. Yang, L. Yu, Y. Xu et al., Advanced biotechnology-assisted precise sonodynamic therapy. Chem. Soc. Rev. 50, 11227–11248 (2021). https://doi.org/10.1039/d1cs00403d
M. Xu, L. Zhou, L. Zheng, Q. Zhou, K. Liu et al., Sonodynamic therapy-derived multimodal synergistic cancer therapy. Cancer Lett. 497, 229–242 (2021). https://doi.org/10.1016/j.canlet.2020.10.037
S. Li, W. Zhang, R. Xing, C. Yuan, H. Xue et al., Supramolecular nanofibrils formed by coassembly of clinically approved drugs for tumor photothermal immunotherapy. Adv. Mater. 33, e2100595 (2021). https://doi.org/10.1002/adma.202100595
R. Xing, Q. Zou, C. Yuan, L. Zhao, R. Chang et al., Self-assembling endogenous biliverdin as a versatile near-infrared photothermal nanoagent for cancer theranostics. Adv. Mater. 31, e1900822 (2019). https://doi.org/10.1002/adma.201900822
H. Wang, Q. Liu, K. Zhang, P. Wang, Q. Xue et al., Comparison between sonodynamic and photodynamic effect on MDA-MB-231 cells. J. Photochem. Photobiol. B. 127, 182–191 (2013). https://doi.org/10.1016/j.jphotobiol.2013.08.015
W. Qin, Q. Yang, C. Zhu, R. Jiao, X. Lin et al., A distinctive insight into inorganic sonosensitizers: design principles and application domains. Small 20, 2311228 (2024). https://doi.org/10.1002/smll.202311228
X. Wang, X. Zhong, F. Gong, Y. Chao, L. Cheng, Newly developed strategies for improving sonodynamic therapy. Mater. Horiz. 7, 2028–2046 (2020). https://doi.org/10.1039/d0mh00613k
R. Wang, Q. Liu, A. Gao, N. Tang, Q. Zhang et al., Recent developments of sonodynamic therapy in antibacterial application. Nanoscale 14, 12999–13017 (2022). https://doi.org/10.1039/d2nr01847k
P. Tharkar, R. Varanasi, W.S.F. Wong, C.T. Jin, W. Chrzanowski, Nano-enhanced drug delivery and therapeutic ultrasound for cancer treatment and beyond. Front. Bioeng. Biotechnol. 7, 324 (2019). https://doi.org/10.3389/fbioe.2019.00324
X. Qian, Y. Zheng, Y. Chen, Micro/nanop-augmented sonodynamic therapy (SDT): breaking the depth shallow of photoactivation. Adv. Mater. 28, 8097–8129 (2016). https://doi.org/10.1002/adma.201602012
Y. He, D. Xing, S. Tan, Y. Tang, K.-I. Ueda, In vivo sonoluminescence imaging with the assistance of FCLA. Phys. Med. Biol. 47, 1535–1541 (2002). https://doi.org/10.1088/0031-9155/47/9/308
Y. Yin, X. Jiang, L. Sun, H. Li, C. Su et al., Continuous inertial cavitation evokes massive ROS for reinforcing sonodynamic therapy and immunogenic cell death against breast carcinoma. Nano Today 36, 101009 (2021). https://doi.org/10.1016/j.nantod.2020.101009
L. Fan, A. Idris Muhammad, B. Bilyaminu Ismail, D. Liu, Sonodynamic antimicrobial chemotherapy: an emerging alternative strategy for microbial inactivation. Ultrason Sonochem 75, 105591 (2021). https://doi.org/10.1016/j.ultsonch.2021.105591
C. McEwan, S. Kamila, J. Owen, H. Nesbitt, B. Callan et al., Combined sonodynamic and antimetabolite therapy for the improved treatment of pancreatic cancer using oxygen loaded microbubbles as a delivery vehicle. Biomaterials 80, 20–32 (2016). https://doi.org/10.1016/j.biomaterials.2015.11.033
I. Rosenthal, J.Z. Sostaric, P. Riesz, Sonodynamic therapy: a review of the synergistic effects of drugs and ultrasound. Ultrason. Sonochem. 11, 349–363 (2004). https://doi.org/10.1016/j.ultsonch.2004.03.004
Y. Tang, L. Ge, L. Jiang, X. Jiang, Pore-enhanced reactive oxygen species generation by using covalent organic frameworks for improving sonodynamic therapy of cancer. Nano Today 55, 102166 (2024). https://doi.org/10.1016/j.nantod.2024.102166
G.Y. Wan, Y. Liu, B.W. Chen, Y.Y. Liu, Y.S. Wang et al., Recent advances of sonodynamic therapy in cancer treatment. Cancer Biol. Med. 13, 325–338 (2016). https://doi.org/10.20892/j.issn.2095-3941.2016.0068
S. Liao, M. Cai, R. Zhu, T. Fu, Y. Du et al., Antitumor effect of photodynamic therapy/sonodynamic therapy/sono-photodynamic therapy of chlorin e6 and other applications. Mol. Pharm. 20, 875–885 (2023). https://doi.org/10.1021/acs.molpharmaceut.2c00824
X. Xing, S. Zhao, T. Xu, L. Huang, Y. Zhang et al., Advances and perspectives in organic sonosensitizers for sonodynamic therapy. Coord. Chem. Rev. 445, 214087 (2021). https://doi.org/10.1016/j.ccr.2021.214087
H. Chen, X. Zhou, Y. Gao, B. Zheng, F. Tang et al., Recent progress in development of new sonosensitizers for sonodynamic cancer therapy. Drug Discov. Today 19, 502–509 (2014). https://doi.org/10.1016/j.drudis.2014.01.010
S. Son, J.H. Kim, X. Wang, C. Zhang, S.A. Yoon et al., Multifunctional sonosensitizers in sonodynamic cancer therapy. Chem. Soc. Rev. 49, 3244–3261 (2020). https://doi.org/10.1039/c9cs00648f
M. Zhang, D. Yang, C. Dong, H. Huang, G. Feng et al., Two-dimensional MXene-originated in situ nanosonosensitizer generation for augmented and synergistic sonodynamic tumor nanotherapy. ACS Nano 16, 9938–9952 (2022). https://doi.org/10.1021/acsnano.2c04630
B. Geng, J. Hu, Y. Li, S. Feng, D. Pan et al., Near-infrared phosphorescent carbon dots for sonodynamic precision tumor therapy. Nat. Commun. 13, 5735 (2022). https://doi.org/10.1038/s41467-022-33474-8
L.A. Osminkina, A.A. Kudryavtsev, S.V. Zinovyev, A.P. Sviridov, Y.V. Kargina et al., Silicon nanops as amplifiers of the ultrasonic effect in sonodynamic therapy. Bull. Exp. Biol. Med. 161, 296–299 (2016). https://doi.org/10.1007/s10517-016-3399-x
J. Zhu, A. Ouyang, Z. Shen, Z. Pan, S. Banerjee et al., Sonodynamic cancer therapy by novel iridium-gold nanoassemblies. Chin. Chem. Lett. 33, 1907–1912 (2022). https://doi.org/10.1016/j.cclet.2021.11.017
L. Raspagliesi, A. D’Ammando, M. Gionso, N.D. Sheybani, M.B. Lopes et al., Intracranial sonodynamic therapy with 5-aminolevulinic acid and sodium fluorescein: safety study in a porcine model. Front. Oncol. 11, 679989 (2021). https://doi.org/10.3389/fonc.2021.679989
X. Zhang, C. Li, Y. Zhang, X. Guan, L. Mei et al., Construction of long-wavelength emissive organic nanosonosensitizer targeting mitochondria for precise and efficient in vivo sonotherapy. Adv. Funct. Mater. 32, 2207259 (2022). https://doi.org/10.1002/adfm.202207259
H.B. Cheng, H. Dai, X. Tan, H. Li, H. Liang et al., A facile, protein-derived supramolecular theranostic strategy for multimodal-imaging-guided photodynamic and photothermal immunotherapy in vivo. Adv. Mater. 34, e2109111 (2022). https://doi.org/10.1002/adma.202109111
H.-B. Cheng, X. Cao, S. Zhang, K. Zhang, Y. Cheng et al., BODIPY as a multifunctional theranostic reagent in biomedicine: self-assembly, properties, and applications. Adv. Mater. 35, 2207546 (2023). https://doi.org/10.1002/adma.202207546
X. Li, X. Sun, H. Chen, X. Chen, Y. Li et al., Exploring BODIPY derivatives as sonosensitizers for anticancer sonodynamic therapy. Eur. J. Med. Chem. 264, 116035 (2024). https://doi.org/10.1016/j.ejmech.2023.116035
K. Liu, Z. Jiang, F. Zhao, W. Wang, F. Jäkle et al., Triarylboron-doped acenethiophenes as organic sonosensitizers for highly efficient sonodynamic therapy with low phototoxicity. Adv. Mater. 34, e2206594 (2022). https://doi.org/10.1002/adma.202206594
P.-H. Zhao, Y.-L. Wu, X.-Y. Li, L.-L. Feng, L. Zhang et al., Aggregation-enhanced sonodynamic activity of phthalocyanine–artesunate conjugates. Angew. Chem. Int. Ed. 61, e202113506 (2022). https://doi.org/10.1002/anie.202113506
C. Deng, J. Zhang, F. Hu, S. Han, M. Zheng et al., A GSH-responsive prodrug with simultaneous triple-activation capacity for photodynamic/sonodynamic combination therapy with inhibited skin phototoxicity. Small 20, e2400667 (2024). https://doi.org/10.1002/smll.202400667
L. Sun, P. Wang, J. Zhang, Y. Sun, S. Sun et al., Design and application of inorganic nanops for sonodynamic cancer therapy. Biomater. Sci. 9, 1945–1960 (2021). https://doi.org/10.1039/d0bm01875a
Y. Zeng, Q. Ouyang, Y. Yu, L. Tan, X. Liu et al., Defective homojunction porphyrin-based metal-organic frameworks for highly efficient sonodynamic therapy. Small Methods 7, e2201248 (2023). https://doi.org/10.1002/smtd.202201248
X. Wang, X. Zhong, L. Cheng, Titanium-based nanomaterials for cancer theranostics. Coord. Chem. Rev. 430, 213662 (2021). https://doi.org/10.1016/j.ccr.2020.213662
F. Gong, L. Cheng, N. Yang, Y. Gong, Y. Ni et al., Preparation of TiH1.924 nanodots by liquid-phase exfoliation for enhanced sonodynamic cancer therapy. Nat. Commun. 11, 3712 (2020). https://doi.org/10.1038/s41467-020-17485-x
S. Yang, X. Wang, P. He, A. Xu, G. Wang et al., Graphene quantum dots with pyrrole N and pyridine N: superior reactive oxygen species generation efficiency for metal-free sonodynamic tumor therapy. Small 17, e2004867 (2021). https://doi.org/10.1002/smll.202004867
S. Kwon, H. Ko, D.G. You, K. Kataoka, J.H. Park, Nanomedicines for reactive oxygen species mediated approach: an emerging paradigm for cancer treatment. Acc. Chem. Res. 52, 1771–1782 (2019). https://doi.org/10.1021/acs.accounts.9b00136
Q. Jiang, B. Qiao, X. Lin, J. Cao, N. Zhang et al., A hydrogen peroxide economizer for on-demand oxygen production-assisted robust sonodynamic immunotherapy. Theranostics 12, 59–75 (2022). https://doi.org/10.7150/thno.64862
L. Song, X. Hou, K.F. Wong, Y. Yang, Z. Qiu et al., Gas-filled protein nanostructures as cavitation nuclei for molecule-specific sonodynamic therapy. Acta Biomater. 136, 533–545 (2021). https://doi.org/10.1016/j.actbio.2021.09.010
M.A. Subhan, S.S.K. Yalamarty, N. Filipczak, F. Parveen, V.P. Torchilin, Recent advances in tumor targeting via EPR effect for cancer treatment. J. Pers. Med. 11, 571 (2021). https://doi.org/10.3390/jpm11060571
F. Bosca, F. Foglietta, A. Gimenez, R. Canaparo, G. Durando et al., Exploiting lipid and polymer nanocarriers to improve the anticancer sonodynamic activity of chlorophyll. Pharmaceutics 12, 605 (2020). https://doi.org/10.3390/pharmaceutics12070605
X. Li, C.-Y. Kim, S. Lee, D. Lee, H.-M. Chung et al., Nanostructured phthalocyanine assemblies with protein-driven switchable photoactivities for biophotonic imaging and therapy. J. Am. Chem. Soc. 139, 10880–10886 (2017). https://doi.org/10.1021/jacs.7b05916
M. Yang, C. Zhang, R. Wang, X. Wu, H. Li et al., Cancer immunotherapy elicited by immunogenic cell death based on smart nanomaterials. Small Meth. 7, 2201381 (2023). https://doi.org/10.1002/smtd.202201381
H. Chen, L. Liu, A. Ma, T. Yin, Z. Chen et al., Noninvasively immunogenic sonodynamic therapy with manganese protoporphyrin liposomes against triple-negative breast cancer. Biomaterials 269, 120639 (2021). https://doi.org/10.1016/j.biomaterials.2020.120639
W. Lei, C. Yang, Y. Wu, G. Ru, X. He et al., Nanocarriers surface engineered with cell membranes for cancer targeted chemotherapy. J. Nanobiotechnol. 20, 45 (2022). https://doi.org/10.1186/s12951-022-01251-w
H. Yan, D. Shao, Y.-H. Lao, M. Li, H. Hu et al., Engineering cell membrane-based nanotherapeutics to target inflammation. Adv. Sci. 6, 1900605 (2019). https://doi.org/10.1002/advs.201900605
P. Dash, A.M. Piras, M. Dash, Cell membrane coated nanocarriers - an efficient biomimetic platform for targeted therapy. J. Control. Release 327, 546–570 (2020). https://doi.org/10.1016/j.jconrel.2020.09.012
Y. Zhang, J. Zhao, L. Zhang, Y. Zhao, Y. Zhang et al., A cascade nanoreactor for enhancing sonodynamic therapy on colorectal cancer via synergistic ROS augment and autophagy blockage. Nano Today 49, 101798 (2023). https://doi.org/10.1016/j.nantod.2023.101798
X. Wang, M. Wu, H. Li, J. Jiang, S. Zhou et al., Enhancing penetration ability of semiconducting polymer nanops for sonodynamic therapy of large solid tumor. Adv. Sci. 9, e2104125 (2022). https://doi.org/10.1002/advs.202104125
H. Li, J. Wang, H. Kim, X. Peng, J. Yoon, Activatable near-infrared versatile fluorescent and chemiluminescent dyes based on the dicyanomethylene-4H-pyran scaffold: from design to imaging and theranostics. Angew. Chem. Int. Ed. 63, e202311764 (2024). https://doi.org/10.1002/anie.202311764
C. Deng, M. Zheng, S. Han, Y. Wang, J. Xin et al., GSH-activated porphyrin sonosensitizer prodrug for fluorescence imaging-guided cancer sonodynamic therapy. Adv. Funct. Mater. 33, 2300348 (2023). https://doi.org/10.1002/adfm.202300348
J. Li, J. Wang, L. Xu, H. Chi, X. Liang et al., A class of activatable NIR-II photoacoustic dyes for high-contrast bioimaging. Angew. Chem. Int. Ed. 63, e202312632 (2024). https://doi.org/10.1002/anie.202312632
S. Sun, D. Wang, R. Yin, P. Zhang, R. Jiang et al., A two-In-one nanoprodrug for photoacoustic imaging-guided enhanced sonodynamic therapy. Small 18, 2202558 (2022). https://doi.org/10.1002/smll.202202558
F. Gong, L. Cheng, N. Yang, O. Betzer, L. Feng et al., Ultrasmall oxygen-deficient bimetallic oxide MnWOX nanops for depletion of endogenous GSH and enhanced sonodynamic cancer therapy. Adv. Mater. 31, e1900730 (2019). https://doi.org/10.1002/adma.201900730
S. Li, W. Zhang, H. Xue, R. Xing, X. Yan, Tumor microenvironment-oriented adaptive nanodrugs based on peptide self-assembly. Chem. Sci. 11, 8644–8656 (2020). https://doi.org/10.1039/d0sc02937h
X. Ren, D. Chen, Y. Wang, H. Li, Y. Zhang et al., Nanozymes-recent development and biomedical applications. J. Nanobiotechnology 20, 92 (2022). https://doi.org/10.1186/s12951-022-01295-y
Y. Wang, D. Fei Gong, Z. Han, H. Lei, Y. Zhou et al., Oxygen-deficient molybdenum oxide nanosensitizers for ultrasound-enhanced cancer metalloimmunotherapy. Angew. Chem. Int. Ed. 62, e202215467 (2023). https://doi.org/10.1002/anie.202215467
T. Nie, W. Zou, Z. Meng, L. Wang, T. Ying et al., Bioactive iridium nanoclusters with glutathione depletion ability for enhanced sonodynamic-triggered ferroptosis-like cancer cell death. Adv. Mater. 34, e2206286 (2022). https://doi.org/10.1002/adma.202206286
Y. Duan, Y. Yu, P. Peilai Liu, Y. Gao, D. Xinyue Dai et al., Reticular chemistry-enabled sonodynamic activity of covalent organic frameworks for nanodynamic cancer therapy. Angew. Chem. Int. Ed. 62, e202302146 (2023). https://doi.org/10.1002/anie.202302146
S. Zhang, S. Xia, L. Chen, Y. Chen, J. Zhou, Covalent organic framework nanobowls as activatable nanosensitizers for tumor-specific and ferroptosis-augmented sonodynamic therapy. Adv. Sci. 10, e2206009 (2023). https://doi.org/10.1002/advs.202206009
P. Vaupel, F. Kallinowski, P. Okunieff, Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res. 49, 6449–6465 (1989). https://doi.org/10.1097/00002820-198912000-00001
S. Mura, J. Nicolas, P. Couvreur, Stimuli-responsive nanocarriers for drug delivery. Nat. Mater. 12, 991–1003 (2013). https://doi.org/10.1038/nmat3776
K. Yang, L. Yue, G. Yu, L. Rao, R. Tian et al., A hypoxia responsive nanoassembly for tumor specific oxygenation and enhanced sonodynamic therapy. Biomaterials 275, 120822 (2021). https://doi.org/10.1016/j.biomaterials.2021.120822
X. Li, D. Lee, J.-D. Huang, J. Yoon, Phthalocyanine-assembled nanodots as photosensitizers for highly efficient Type I photoreactions in photodynamic therapy. Angew. Chem. Int. Ed. 57, 9885–9890 (2018). https://doi.org/10.1002/anie.201806551
Z. Liu, Z. Yan, Y. Di, S. Yang, Y. Ning et al., Current advances in metal–organic frameworks for cancer nanodynamic therapies. Coord. Chem. Rev. 497, 215434 (2023). https://doi.org/10.1016/j.ccr.2023.215434
L. Zhong, T. Yang, P. Li, L. Shi, J. Lai et al., Metal-organic framework-based nanotherapeutics with tumor hypoxia-relieving ability for synergistic sonodynamic/chemo-therapy. Front. Mater. 9, 841503 (2022). https://doi.org/10.3389/fmats.2022.841503
H. Xiao, X. Li, B. Li, Y. Zhong, J. Qin et al., Sono-promoted drug penetration and extracellular matrix modulation potentiate sonodynamic therapy of pancreatic ductal adenocarcinoma. Acta Biomater. 161, 265–274 (2023). https://doi.org/10.1016/j.actbio.2023.02.038
G. Li, X. Zhong, X. Wang, F. Gong, H. Lei et al., Titanium carbide nanosheets with defect structure for photothermal-enhanced sonodynamic therapy. Bioact. Mater. 8, 409–419 (2021). https://doi.org/10.1016/j.bioactmat.2021.06.021
S. Liu, B. Wang, Y. Yu, Y. Liu, Z. Zhuang et al., Cationization-enhanced type I and type II ROS generation for photodynamic treatment of drug-resistant bacteria. ACS Nano 16, 9130–9141 (2022). https://doi.org/10.1021/acsnano.2c01206
D. Chen, Q. Xu, W. Wang, J. Shao, W. Huang et al., Type I photosensitizers revitalizing photodynamic oncotherapy. Small 17, e2006742 (2021). https://doi.org/10.1002/smll.202006742
J. Cao, Y. Sun, C. Zhang, X. Wang, Y. Zeng et al., Tablet-like TiO2/C nanocomposites for repeated type I sonodynamic therapy of pancreatic cancer. Acta Biomater. 129, 269–279 (2021). https://doi.org/10.1016/j.actbio.2021.05.029
Z. Zhang, B. Li, L. Xie, W. Sang, H. Tian et al., Metal-phenolic network-enabled lactic acid consumption reverses immunosuppressive tumor microenvironment for sonodynamic therapy. ACS Nano 15, 16934–16945 (2021). https://doi.org/10.1021/acsnano.1c08026
D.W. Felsher, Cancer revoked: oncogenes as therapeutic targets. Nat. Rev. Cancer 3, 375–380 (2003). https://doi.org/10.1038/nrc1070
F. Cairnduff, M.R. Stringer, E.J. Hudson, D.V. Ash, S.B. Brown, Superficial photodynamic therapy with topical 5-aminolaevulinic acid for superficial primary and secondary skin cancer. Br. J. Cancer 69, 605–608 (1994). https://doi.org/10.1038/bjc.1994.112
M. Zhan, F. Wang, Y. Liu, J. Zhou, W. Zhao et al., Dual-cascade activatable nanopotentiators reshaping adenosine metabolism for sono-chemodynamic-immunotherapy of deep tumors. Adv. Sci. 10, e2207200 (2023). https://doi.org/10.1002/advs.202207200
T. Chen, W. Zeng, C. Tie, M. Yu, H. Hao et al., Engineered gold/black phosphorus nanoplatforms with remodeling tumor microenvironment for sonoactivated catalytic tumor theranostics. Bioact. Mater. 10, 515–525 (2021). https://doi.org/10.1016/j.bioactmat.2021.09.016
T. Yamaguchi, S. Kitahara, K. Kusuda, J. Okamoto, Y. Horise et al., Current landscape of sonodynamic therapy for treating cancer. Cancers 13, 6184 (2021). https://doi.org/10.3390/cancers13246184
M. Lafond, T. Lambin, R.A. Drainville, A. Dupré, M. Pioche et al., Pancreatic ductal adenocarcinoma: current and emerging therapeutic uses of focused ultrasound. Cancers 14, 2577 (2022). https://doi.org/10.3390/cancers14112577
R.J. Browning, S. Able, J.-L. Ruan, L. Bau, P.D. Allen et al., Combining sonodynamic therapy with chemoradiation for the treatment of pancreatic cancer. J. Control. Release 337, 371–377 (2021). https://doi.org/10.1016/j.jconrel.2021.07.020
S. Zeng, M. Pöttler, B. Lan, R. Grützmann, C. Pilarsky et al., Chemoresistance in pancreatic cancer. Int. J. Mol. Sci. 20, 4504 (2019). https://doi.org/10.3390/ijms20184504
M.H. Sherman, G.L. Beatty, Tumor microenvironment in pancreatic cancer pathogenesis and therapeutic resistance. Annu. Rev. Pathol. Mech. Dis. 18, 123–148 (2023). https://doi.org/10.1146/annurev-pathmechdis-031621-024600
T. Zhang, Y. Sun, J. Cao, J. Luo, J. Wang et al., Intrinsic nucleus-targeted ultra-small metal-organic framework for the type I sonodynamic treatment of orthotopic pancreatic carcinoma. J. Nanobiotechnol. 19, 315 (2021). https://doi.org/10.1186/s12951-021-01060-7
Y. He, T. Wang, Y. Song, C. Fang, Y. Wang et al., Targeting vascular destruction by sonosensitizer-free sonocatalytic nanomissiles instigates Thrombus aggregation and nutrition deprivation to starve pancreatic cancer. Adv. Funct. Mater. 34, 2315394 (2024). https://doi.org/10.1002/adfm.202315394
Z. Tang, Y. Liu, M. He, W. Bu, Chemodynamic therapy: tumour microenvironment-mediated Fenton and Fenton-like reactions. Angew. Chem. Int. Ed. 58, 946–956 (2019). https://doi.org/10.1002/anie.201805664
Y. Pu, H. Yin, C. Dong, H. Xiang, W. Wu et al., Sono-controllable and ROS-sensitive CRISPR-Cas9 genome editing for augmented/synergistic ultrasound tumor nanotherapy. Adv. Mater. 33, e2104641 (2021). https://doi.org/10.1002/adma.202104641
X. Zhong, X. Wang, L. Cheng, Y.-A. Tang, G. Zhan et al., GSH-depleted PtCu3 nanocages for chemodynamic- enhanced sonodynamic cancer therapy. Adv. Funct. Mater. 30, 1907954 (2020). https://doi.org/10.1002/adfm.201907954
C. Fang, Z. Deng, G. Cao, Q. Chu, Y. Wu et al., Co–ferrocene MOF/glucose oxidase as cascade nanozyme for effective tumor therapy. Adv. Funct. Mater. 30, 1910085 (2020). https://doi.org/10.1002/adfm.201910085
S. Liang, X. Xiao, L. Bai, B. Liu, M. Yuan et al., Conferring Ti-based MOFs with defects for enhanced sonodynamic cancer therapy. Adv. Mater. 33, e2100333 (2021). https://doi.org/10.1002/adma.202100333
B. Xu, Z. Huang, Y. Liu, S. Li, H. Liu, MOF-based nanomedicines inspired by structures of natural active components. Nano Today 48, 101690 (2023). https://doi.org/10.1016/j.nantod.2022.101690
Y. Sun, J. Cao, X. Wang, C. Zhang, J. Luo et al., Hypoxia-adapted sono-chemodynamic treatment of orthotopic pancreatic carcinoma using copper metal–organic frameworks loaded with an ultrasound-induced free radical initiator. ACS Appl. Mater. Interfaces 13, 38114–38126 (2021). https://doi.org/10.1021/acsami.1c11017
A.D. Waldman, J.M. Fritz, M.J. Lenardo, A guide to cancer immunotherapy: from T cell basic science to clinical practice. Nat. Rev. Immunol. 20, 651–668 (2020). https://doi.org/10.1038/s41577-020-0306-5
S. Gao, X. Yang, J. Xu, N. Qiu, G. Zhai, Nanotechnology for boosting cancer immunotherapy and remodeling tumor microenvironment: the horizons in cancer treatment. ACS Nano 15, 12567–12603 (2021). https://doi.org/10.1021/acsnano.1c02103
Y. Xia, S. Fu, Q. Ma, Y. Liu, N. Zhang, Application of nano-delivery systems in lymph nodes for tumor immunotherapy. Nano-Micro Lett. 15, 145 (2023). https://doi.org/10.1007/s40820-023-01125-2
H. Lei, J.H. Kim, S. Son, L. Chen, Z. Pei et al., Immunosonodynamic therapy designed with activatable sonosensitizer and immune stimulant imiquimod. ACS Nano 16, 10979–10993 (2022). https://doi.org/10.1021/acsnano.2c03395
T. Wang, W. Peng, M. Du, Z. Chen, Immunogenic sonodynamic therapy for inducing immunogenic cell death and activating antitumor immunity. Front. Oncol. 13, 1167105 (2023). https://doi.org/10.3389/fonc.2023.1167105
H. Nesbitt, K. Logan, K. Thomas, B. Callan, J. Gao et al., Sonodynamic therapy complements PD-L1 immune checkpoint inhibition in a murine model of pancreatic cancer. Cancer Lett. 517, 88–95 (2021). https://doi.org/10.1016/j.canlet.2021.06.003
M. Wu, Q. Huang, Y. Xie, X. Wu, H. Ma et al., Improvement of the anticancer efficacy of PD-1/PD-L1 blockade via combination therapy and PD-L1 regulation. J. Hematol. Oncol. 15, 24 (2022). https://doi.org/10.1186/s13045-022-01242-2
J. Chen, L. Feng, P. Jin, J. Shen, J. Lu et al., Cavitation assisted endoplasmic reticulum targeted sonodynamic droplets to enhanced anti-PD-L1 immunotherapy in pancreatic cancer. J. Nanobiotechnology 20, 283 (2022). https://doi.org/10.1186/s12951-022-01459-w
J. Li, N. Yu, D. Cui, J. Huang, Y. Luo et al., Activatable semiconducting polymer pro-nanomodulators for deep-tissue sono-immunotherapy of orthotopic pancreatic cancer. Angew. Chem. Int. Ed. 62, e202305200 (2023). https://doi.org/10.1002/anie.202305200
A.C. Lai, D. Momar Toure, D. Doris Hellerschmied, J. Salami, D. Saul Jaime-Figueroa et al., Modular PROTAC design for the degradation of oncogenic BCR-ABL. Angew. Chem. Int. Ed. 55, 807–810 (2016). https://doi.org/10.1002/anie.201507634
S.-M. Qi, J. Dong, Z.-Y. Xu, X.-D. Cheng, W.-D. Zhang et al., PROTAC: an effective targeted protein degradation strategy for cancer therapy. Front. Pharmacol. 12, 692574 (2021). https://doi.org/10.3389/fphar.2021.692574
M. Békés, D.R. Langley, C.M. Crews, PROTAC targeted protein degraders: the past is prologue. Nat. Rev. Drug Discov. 21, 181–200 (2022). https://doi.org/10.1038/s41573-021-00371-6
S. He, Y. Fang, Y. Zhu, Z. Ma, G. Dong et al., Drugtamer-PROTAC conjugation strategy for targeted PROTAC delivery and synergistic antitumor therapy. Adv. Sci. 11, e2401623 (2024). https://doi.org/10.1002/advs.202401623
J. Liu, H. Chen, L. Ma, Z. He, D. Wang et al., Light-induced control of protein destruction by opto-PROTAC. Sci. Adv. 6, eaay5154 (2020). https://doi.org/10.1126/sciadv.aay5154
Z. Chen, L. Chen, Y. Ma, Y. Liu, Q. Zhang et al., Peptide-appended nanosonosensitizers targeting tumor glycolysis for synergistic sonodynamic-immunometabolic therapy of spinal-metastasized tumors. Adv. Mater. 35, e2304246 (2023). https://doi.org/10.1002/adma.202304246
H. Tang, X. Xu, Y. Chen, H. Xin, T. Wan et al., Reprogramming the tumor microenvironment through second-near-infrared-window photothermal genome editing of PD-L1 mediated by supramolecular gold nanorods for enhanced cancer immunotherapy. Adv. Mater. 33, e2006003 (2021). https://doi.org/10.1002/adma.202006003
Y. Liu, H. Wang, M. Ding, W. Yao, K. Wang et al., Ultrasound-activated PROTAC prodrugs overcome immunosuppression to actuate efficient deep-tissue sono-immunotherapy in orthotopic pancreatic tumor mouse models. Nano Lett. 24, 8741–8751 (2024). https://doi.org/10.1021/acs.nanolett.4c02287
M. Li, Y. Liu, Y. Zhang, N. Yu, J. Li, Sono-activatable semiconducting polymer nanoreshapers multiply remodel tumor microenvironment for potent immunotherapy of orthotopic pancreatic cancer. Adv. Sci. 10, e2305150 (2023). https://doi.org/10.1002/advs.202305150
L. Chen, W. Xue, J. Cao, S. Zhang, Y. Zeng et al., TiSe2-mediated sonodynamic and checkpoint blockade combined immunotherapy in hypoxic pancreatic cancer. J. Nanobiotechnol. 20, 453 (2022). https://doi.org/10.1186/s12951-022-01659-4
X. Li, J.S. Oh, Y. Lee, E.C. Lee, M. Yang et al., Albumin-binding photosensitizer capable of targeting glioma via the SPARC pathway. Biomater. Res. 27, 23 (2023). https://doi.org/10.1186/s40824-023-00360-3
H.-J. Liu, H.-M. Hu, G.-Z. Li, Y. Zhang, F. Wu et al., Ferroptosis-related gene signature predicts glioma cell death and glioma patient progression. Front. Cell Dev. Biol. 8, 538 (2020). https://doi.org/10.3389/fcell.2020.00538
Y. Pan, C. Xu, H. Deng, Q. You, C. Zhao et al., Localized NIR-II laser mediated chemodynamic therapy of glioblastoma. Nano Today 43, 101435 (2022). https://doi.org/10.1016/j.nantod.2022.101435
J.N. Sarkaria, L.S. Hu, I.F. Parney, D.H. Pafundi, D.H. Brinkmann et al., Is the blood–brain barrier really disrupted in all glioblastomas? A critical assessment of existing clinical data. Neuro Oncol. 20, 184–191 (2018). https://doi.org/10.1093/neuonc/nox175
S. Watkins, S. Robel, I.F. Kimbrough, S.M. Robert, G. Ellis-Davies et al., Disruption of astrocyte–vascular coupling and the blood–brain barrier by invading glioma cells. Nat. Commun. 5, 4196 (2014). https://doi.org/10.1038/ncomms5196
X. Wang, Y. Jia, P. Wang, Q. Liu, H. Zheng, Current status and future perspectives of sonodynamic therapy in glioma treatment. Ultrason. Sonochem. 37, 592–599 (2017). https://doi.org/10.1016/j.ultsonch.2017.02.020
T. Jia, J. Du, J. Yang, Y. Li, T.Y. Ohulchanskyy et al., Metalloporphyrin MOFs-based nanoagent enabling tumor microenvironment responsive sonodynamic therapy of intracranial glioma signaled by NIR-IIb luminescence imaging. Adv. Funct. Mater. 34, 2307816 (2024). https://doi.org/10.1002/adfm.202307816
Y. Zhu, X. Niu, C. Ding, Y. Lin, W. Fang et al., Carrier-free self-assembly nano-sonosensitizers for sonodynamic-amplified cuproptosis-ferroptosis in glioblastoma therapy. Adv. Sci. 11, e2402516 (2024). https://doi.org/10.1002/advs.202402516
F. Qu, P. Wang, K. Zhang, Y. Shi, Y. Li et al., Manipulation of Mitophagy by “All-in-One” nanosensitizer augments sonodynamic glioma therapy. Autophagy 16, 1413–1435 (2020). https://doi.org/10.1080/15548627.2019.1687210
Y. Sun, H. Wang, P. Wang, K. Zhang, X. Geng et al., Tumor targeting DVDMS-nanoliposomes for an enhanced sonodynamic therapy of gliomas. Biomater. Sci. 7, 985–994 (2019). https://doi.org/10.1039/c8bm01187g
V.G. Abramson, B.D. Lehmann, T.J. Ballinger, J.A. Pietenpol, Subtyping of triple-negative breast cancer: implications for therapy. Cancer 121, 8–16 (2015). https://doi.org/10.1002/cncr.28914
W. Pei, Y. Li, Y. Wu, Y. Wu, L. Cai et al., A tumoricidal lipoprotein complex electrostatically stabilized on mesoporous silica as nanotherapeutics and nanoadjuvant for potentiating immunotherapy of triple negative breast cancer. Adv. Funct. Mater. 33, 2308117 (2023). https://doi.org/10.1002/adfm.202308117
T. Inui, K. Makita, H. Miura, A. Matsuda, D. Kuchiike et al., Case report: a breast cancer patient treated with GcMAF, sonodynamic therapy and hormone therapy. Anticancer Res 34, 4589–4593 (2014). https://doi.org/10.1016/j.urolonc.2014.05.010
Y. Li, W. Chen, Y. Kang, X. Zhen, Z. Zhou et al., Nanosensitizer-mediated augmentation of sonodynamic therapy efficacy and antitumor immunity. Nat. Commun. 14, 6973 (2023). https://doi.org/10.1038/s41467-023-42509-7
Y. Zheng, Z. Li, Y. Yang, H. Shi, H. Chen et al., A nanosensitizer self-assembled from oleanolic acid and chlorin e6 for synergistic chemo/sono-photodynamic cancer therapy. Phytomedicine 93, 153788 (2021). https://doi.org/10.1016/j.phymed.2021.153788
X. Lin, T. He, R. Tang, Q. Li, N. Wu et al., Biomimetic nanoprobe-augmented triple therapy with photothermal, sonodynamic and checkpoint blockade inhibits tumor growth and metastasis. J. Nanobiotechnology 20, 80 (2022). https://doi.org/10.1186/s12951-022-01287-y
G. Yuan, B. Yang, P. Chen, L. Bai, G. Qiao et al., Regulating manganese-site electronic structure via reconstituting nitrogen coordination for efficient non-oxygen-dependent sonocatalytic therapy against orthotopic breast cancer. ACS Nano 18, 27630–27641 (2024). https://doi.org/10.1021/acsnano.4c09052