Volume 14 Issue 5
May  2024
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Yan Zhang, Ying Yang, Yudi Feng, Xueyan Gao, Liping Pei, Xiaopan Li, Bingxin Gao, Lin Liu, Chengzeng Wang, Shuochen Gao. Sonodynamic therapy for the treatment of atherosclerosis[J]. Journal of Pharmaceutical Analysis, 2024, 14(5): 100909. doi: 10.1016/j.jpha.2023.11.016
Citation: Yan Zhang, Ying Yang, Yudi Feng, Xueyan Gao, Liping Pei, Xiaopan Li, Bingxin Gao, Lin Liu, Chengzeng Wang, Shuochen Gao. Sonodynamic therapy for the treatment of atherosclerosis[J]. Journal of Pharmaceutical Analysis, 2024, 14(5): 100909. doi: 10.1016/j.jpha.2023.11.016

Sonodynamic therapy for the treatment of atherosclerosis

doi: 10.1016/j.jpha.2023.11.016
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We are grateful for financial support from the Natural Science Foundation of Henan, China (Grant No.: 202300410446) and the National Natural Science Foundation of China (Grant No.: 82071950).

  • Received Date: Aug. 11, 2023
  • Accepted Date: Nov. 27, 2023
  • Rev Recd Date: Nov. 18, 2023
  • Publish Date: May 30, 2024
  • Atherosclerosis (AS) is a chronic inflammatory disease of large and medium-sized arteries that leads to ischemic heart disease, stroke, and peripheral vascular disease. Despite the current treatments, mortality and disability still remain high. Sonodynamic therapy (SDT), a non-invasive and localized methodology, has been developed as a promising new treatment for inhibiting atherosclerotic progression and stabilizing plaques. Promising progress has been made through cell and animal assays, as well as clinical trials. For example, the effect of SDT on apoptosis and autophagy of cells in AS, especially macrophages, and the concept of non-lethal SDT has also been proposed. In this review, we summarize the ultrasonic parameters and known sonosensitizers utilized in SDT for AS; we elaborate on SDT's therapeutic effects and mechanisms in terms of macrophages, T lymphocytes, neovascularization, smooth muscle cells, lipid, extracellular matrix and efferocytosis within plaques; additionally, we discuss the safety of SDT. A comprehensive summary of the confirmed effects of SDT on AS is conducted to establish a framework for future researchers.
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  • [1]
    D. Wolf, K. Ley, Immunity and Inflammation in Atherosclerosis, Circ. Res. 124 (2019) 315-327.
    [2]
    M.E. Kruk, A.D. Gage, N.T. Joseph, et al., Mortality due to low-quality health systems in the universal health coverage era: a systematic analysis of amenable deaths in 137 countries, Lancet 392 (2018) 2203-2212.
    [3]
    M. Tomaszewski, K.M. Stepien, J. Tomaszewska, et al., Statin-induced myopathies, Pharmacol. Rep. 63 (2011) 859-866.
    [4]
    A.F. AbuRahma, E.D. Avgerinos, R.W. Chang, et al., Society for Vascular Surgery clinical practice guidelines for management of extracranial cerebrovascular disease, J. Vasc. Surg. 75 (2022) 4S-22S.
    [5]
    Y. Yang, Y. Liu, X. Chen, et al., 5-Aminolevulinic Acid-Mediated Sonodynamic Therapy Alleviates Atherosclerosis via Enhancing Efferocytosis and Facilitating a Shift in the Th1/Th2 Balance Toward Th2 Polarization, Cell Physiol Biochem 47 (2018) 83-96.
    [6]
    C. Geng, Y. Zhang, T.H. Hidru, et al., Sonodynamic therapy: A potential treatment for atherosclerosis, Life Sci. 207 (2018) 304-313.
    [7]
    R. Liu, Q. Zhang, Y. Lang, et al., Sonodynamic therapy, a treatment developing from photodynamic therapy, Photodiagn. Photodyn. Ther. 19 (2017) 159-166.
    [8]
    S. Wang, Z. Gao, Y. Yang, et al., Sonodynamic Therapy With Concentric Ultrasound Imaging Array for Precision Theranostics for Atherosclerotic Plaque, IEEE Trans. Ultrason. Ferroelectr. Freq. Control 69 (2022) 3270-3283.
    [9]
    S. Guo, X. Sun, J. Cheng, et al., Apoptosis of THP-1 macrophages induced by protoporphyrin IX-mediated sonodynamic therapy, Int. J. Nanomed. 8 (2013) 2239-2246.
    [10]
    Q. Li, J. Kang, X. Xiong, et al., Protoporphyrin IX-mediated sonodynamic therapy promotes autophagy in vascular smooth muscle cells, Oncol. Lett. 14 (2017) 2097-2102.
    [11]
    Z. Cao, T. Zhang, X. Sun, et al., Membrane-permeabilized sonodynamic therapy enhances drug delivery into macrophages, PLoS One 14 (2019) e217511.
    [12]
    Z. Li, X. Sun, S. Guo, et al., Rapid stabilisation of atherosclerotic plaque with 5-aminolevulinic acid-mediated sonodynamic therapy, Thromb. Haemost. 114 (2015) 793-803.
    [13]
    X. Sun, S. Guo, J. Yao, et al., Rapid inhibition of atherosclerotic plaque progression by sonodynamic therapy, Cardiovasc. Res. 115 (2019) 190-203.
    [14]
    C. Peng, Y. Li, H. Liang, et al., Detection and photodynamic therapy of inflamed atherosclerotic plaques in the carotid artery of rabbits, J. Photochem. Photobiol. B. 102 (2011) 26-31.
    [15]
    Y. Yang, J. Wang, S. Guo, et al., Non-lethal sonodynamic therapy facilitates the M1-to-M2 transition in advanced atherosclerotic plaques via activating the ROS-AMPK-mTORC1-autophagy pathway, Redox Biol. 32 (2020) 101501.
    [16]
    Y. Wang, W. Wang, H. Xu, et al., Non-Lethal Sonodynamic Therapy Inhibits Atherosclerotic Plaque Progression in ApoE-/-Mice and Attenuates ox-LDL-mediated Macrophage Impairment by Inducing Heme Oxygenase-1, Cell Physiol Biochem 41 (2017) 2432-2446.
    [17]
    X. Sun, S. Guo, W. Wang, et al., Potential involvement of the 18 kDa translocator protein and reactive oxygen species in apoptosis of THP-1 macrophages induced by sonodynamic therapy, PLoS One 13 (2018) e196541.
    [18]
    H. Wang, Y. Yang, X. Sun, et al., Sonodynamic therapy-induced foam cells apoptosis activates the phagocytic PPARgamma-LXRalpha-ABCA1/ABCG1 pathway and promotes cholesterol efflux in advanced plaque, Theranostics 8 (2018) 4969-4984.
    [19]
    Y. Jiang, J. Fan, Y. Li, et al., Rapid reduction in plaque inflammation by sonodynamic therapy inpatients with symptomatic femoropopliteal peripheral artery disease:A randomized controlled trial, Int. J. Cardiol. 325 (2021) 132-139.
    [20]
    B. Li, J. Gong, S. Sheng, et al., Sonodynamic therapy reduces iron retention of hemorrhagic plaque, Bioeng. Transl. Med. 6 (2021) e10193.
    [21]
    J. Yao, W. Gao, Y. Wang, et al., Sonodynamic Therapy Suppresses Neovascularization in Atherosclerotic Plaques via Macrophage Apoptosis-Induced Endothelial Cell Apoptosis, JACC-Basic Transl. Sci. 5 (2019) 53-65.
    [22]
    J.Y. Kou, Y. Li, Z.Y. Zhong, et al., Berberine-sonodynamic therapy induces autophagy and lipid unloading in macrophage, Cell Death Dis. 8 (2017) e2558.
    [23]
    X. Li, L. Gao, L. Zheng, et al., The efficacy and mechanism of apoptosis induction by hypericin-mediated sonodynamic therapy in THP-1 macrophages, Int. J. Nanomed. 10 (2015) 821-838.
    [24]
    X. Li, X. Zhang, L. Zheng, et al., Hypericin-mediated sonodynamic therapy induces autophagy and decreases lipids in THP-1 macrophage by promoting ROS-dependent nuclear translocation of TFEB, Cell Death Dis. 7 (2016) e2527.
    [25]
    Y. Jiang, J. Kou, X. Han, et al., ROS-Dependent Activation of Autophagy through the PI3K/Akt/mTOR Pathway Is Induced by Hydroxysafflor Yellow A-Sonodynamic Therapy in THP-1 Macrophages, Oxidative Med. Cell. Longev. 2017 (2017) 8519169.
    [26]
    Z. Qi, F. Yan, W. Shi, et al., AKT-related autophagy contributes to the neuroprotective efficacy of hydroxysafflor yellow A against ischemic stroke in rats, Transl. Stroke Res. 5 (2014) 501-509.
    [27]
    F. Wang, Q. Gao, S. Guo, et al., The sonodynamic effect of curcumin on THP-1 cell-derived macrophages, Biomed Res. Int. 2013 (2013) 737264.
    [28]
    L. Zheng, X. Sun, X. Zhu, et al., Apoptosis of THP-1 derived macrophages induced by sonodynamic therapy using a new sonosensitizer hydroxyl acetylated curcumin, PLoS One 9 (2014) e93133.
    [29]
    L. Jiang, J. Wang, J. Jiang, et al., Sonodynamic therapy in atherosclerosis by curcumin nanosuspensions: Preparation design, efficacy evaluation, and mechanisms analysis, Eur. J. Pharm. Biopharm. 146 (2020) 101-110.
    [30]
    H. Kim, J. Han, J.H. Park, Cyclodextrin polymer improves atherosclerosis therapy and reduces ototoxicity, J. Control. Release 319 (2020) 77-86.
    [31]
    K.O. Goncalvez, D.P. Vieira, L.C. Courrol, Study of THP-1 Macrophage Viability after Sonodynamic Therapy Using Methyl Ester of 5-Aminolevulinic Acid Gold Nanoparticles, Ultrasound Med. Biol. 44 (2018) 2009-2017.
    [32]
    J. Yao, Z. Yang, L. Huang, et al., Low-Intensity Focused Ultrasound-Responsive Ferrite-Encapsulated Nanoparticles for Atherosclerotic Plaque Neovascularization Theranostics, Adv. Sci. 8 (2021) e2100850.
    [33]
    Z. Cao, G. Yuan, L. Zeng, et al., Macrophage-Targeted Sonodynamic/Photothermal Synergistic Therapy for Preventing Atherosclerotic Plaque Progression Using CuS/TiO(2) Heterostructured Nanosheets, ACS Nano 16 (2022) 10608-10622.
    [34]
    A.P. McHale, J.F. Callan, N. Nomikou, et al., Sonodynamic Therapy: Concept, Mechanism and Application to Cancer Treatment, Adv. Exp. Med. Biol. 880 (2016) 429-450.
    [35]
    J. Yao, X. Zhao, F. Tan, et al., Early modulation of macrophage ROS-PPARgamma-NF-kappaB signalling by sonodynamic therapy attenuates neointimal hyperplasia in rabbits, Sci. Rep. 10 (2020) 11638.
    [36]
    D. Costley, E.C. Mc, C. Fowley, et al., Treating cancer with sonodynamic therapy: a review, Int. J. Hyperthermia. 31 (2015) 107-117.
    [37]
    Y. Cao, J. Yao, W. Gao, et al., Sonodynamic Therapy Promotes Efferocytosis via CD47 Down-Regulation in Advanced Atherosclerotic Plaque, Int. Heart J. 63 (2022) 131-140.
    [38]
    J. Pedro-Botet, E. Climent, D. Benaiges, Atherosclerosis and inflammation. New therapeutic approaches, Med. Clin. (Barc). 155 (2020) 256-262.
    [39]
    G. Kroemer, The proto-oncogene Bcl-2 and its role in regulating apoptosis, Nat. Med. 3 (1997) 614-620.
    [40]
    L. Zheng, Y. Li, X. Li, et al., Combination of Hydroxyl Acetylated Curcumin and Ultrasound Induces Macrophage Autophagy with Anti-Apoptotic and Anti-Lipid Aggregation Effects, Cell Physiol Biochem 39 (2016) 1746-1760.
    [41]
    X. Sun, H. Xu, J. Shen, et al., Real-time detection of intracellular reactive oxygen species and mitochondrial membrane potential in THP-1 macrophages during ultrasonic irradiation for optimal sonodynamic therapy, Ultrason. Sonochem. 22 (2015) 7-14.
    [42]
    V. Jeney, G. Balla, J. Balla, Red blood cell, hemoglobin and heme in the progression of atherosclerosis, Front. Physiol. 5 (2014) 379.
    [43]
    A. Loboda, M. Damulewicz, E. Pyza, et al., Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: an evolutionarily conserved mechanism, Cell. Mol. Life Sci. 73 (2016) 3221-3247.
    [44]
    J.L. Stoger, M.J. Gijbels, S. van der Velden, et al., Distribution of macrophage polarization markers in human atherosclerosis, Atherosclerosis 225 (2012) 461-468.
    [45]
    L. Edgar, N. Akbar, A.T. Braithwaite, et al., Hyperglycemia Induces Trained Immunity in Macrophages and Their Precursors and Promotes Atherosclerosis, Circulation 144 (2021) 961-982.
    [46]
    G. Chinetti-Gbaguidi, Baron M, M.A. Bouhlel, et al., Human atherosclerotic plaque alternative macrophages display low cholesterol handling but high phagocytosis because of distinct activities of the PPARgamma and LXRalpha pathways, Circ. Res. 108 (2011) 985-995.
    [47]
    S.K. Matta, D. Kumar, AKT mediated glycolytic shift regulates autophagy in classically activated macrophages, Int. J. Biochem. Cell Biol. 66 (2015) 121-133.
    [48]
    P. Libby, J.E. Buring, L. Badimon, et al., Atherosclerosis, Nat. Rev. Dis. Primers 5 (2019) 56.
    [49]
    R. Saigusa, H. Winkels, K. Ley, T cell subsets and functions in atherosclerosis, Nat. Rev. Cardiol. 17 (2020) 387-401.
    [50]
    Z. Su, H. Lu, H. Jiang, et al., IFN-gamma-producing Th17 cells bias by HMGB1-T-bet/RUNX3 axis might contribute to progression of coronary artery atherosclerosis, Atherosclerosis 243 (2015) 421-428.
    [51]
    Y.L. Chen, Y. Jian, M.J. Liu, et al., [Role of the Th17/Treg functional imbalance on the development of atherosclerosis in apo E knockout mice], Zhonghua. Xin. Xue. Guan. Bing. Za. Zhi. 41 (2013) 416-421.
    [52]
    G.J. Koelwyn, E.M. Corr, E. Erbay, et al., Regulation of macrophage immunometabolism in atherosclerosis, Nat. Immunol. 19 (2018) 526-537.
    [53]
    Y. Xie, H. Chen, P. Qu, et al., Novel insight on the role of Macrophages in atherosclerosis: Focus on polarization, apoptosis and efferocytosis, Int. Immunopharmacol. 113 (2022) 109260.
    [54]
    A. Aarup, T.X. Pedersen, N. Junker, et al., Hypoxia-Inducible Factor-1alpha Expression in Macrophages Promotes Development of Atherosclerosis, Arterioscler. Thromb. Vasc. Biol. 36 (2016) 1782-1790.
    [55]
    X. Yang, H. Yao, Y. Chen, et al., Inhibition of Glutathione Production Induces Macrophage CD36 Expression and Enhances Cellular-oxidized Low Density Lipoprotein (oxLDL) Uptake, J. Biol. Chem. 290 (2015) 21788-21799.
    [56]
    J.E. McLaren, D.R. Michael, T.G. Ashlin, et al., Cytokines, macrophage lipid metabolism and foam cells: implications for cardiovascular disease therapy, Prog. Lipid Res. 50 (2011) 331-347.
    [57]
    R. Kleemann, S. Zadelaar, T. Kooistra, Cytokines and atherosclerosis: a comprehensive review of studies in mice, Cardiovasc. Res. 79 (2008) 360-376.
    [58]
    A.M. Moerman, S. Korteland, K. Dilba, et al., The Correlation Between Wall Shear Stress and Plaque Composition in Advanced Human Carotid Atherosclerosis, Front. Bioeng. Biotechnol. 9 (2021) 828577.
    [59]
    T. Ziegler, C. Kupatt, Sonodynamic Therapy of Atherosclerotic Plaques: Breaking the Cycle, JACC-Basic Transl. Sci. 5 (2020) 66-68.
    [60]
    J.B. Michel, J.L. Martin-Ventura, A. Nicoletti, et al., Pathology of human plaque vulnerability: mechanisms and consequences of intraplaque haemorrhages, Atherosclerosis 234 (2014) 311-319.
    [61]
    D.B. Kell, Iron behaving badly: inappropriate iron chelation as a major contributor to the aetiology of vascular and other progressive inflammatory and degenerative diseases, BMC Med. Genomics 2 (2009) 2.
    [62]
    J. Torrado, L. Buckley, A. Duran, et al., Restenosis, Stent Thrombosis, and Bleeding Complications: Navigating Between Scylla and Charybdis, J. Am. Coll. Cardiol. 71 (2018) 1676-1695.
    [63]
    S.S. Rensen, P.A. Doevendans, G.J. van Eys, Regulation and characteristics of vascular smooth muscle cell phenotypic diversity, Neth. Heart J. 15 (2007) 100-108.
    [64]
    H. Zhu, Y. Zhang, Life and Death Partners in Post-PCI Restenosis: Apoptosis, Autophagy, and The Cross-talk Between Them, Curr. Drug Targets 19 (2018) 1003-1008.
    [65]
    M. Wanjare, F. Kuo, S. Gerecht, Derivation and maturation of synthetic and contractile vascular smooth muscle cells from human pluripotent stem cells, Cardiovasc. Res. 97 (2013) 321-330.
    [66]
    K. Arakawa, K. Hagisawa, H. Kusano, et al., Sonodynamic therapy decreased neointimal hyperplasia after stenting in the rabbit iliac artery, Circulation 105 (2002) 149-151.
    [67]
    J Dan, X Sun, W Li, et al., 5-Aminolevulinic Acid-Mediated Sonodynamic Therapy Promotes Phenotypic Switching from Dedifferentiated to Differentiated Phenotype via Reactive Oxygen Species and p38 Mitogen-Activated Protein Kinase in Vascular Smooth Muscle Cells, Ultrasound Med Biol, 41, 2015, 1681–1689.
    [68]
    A. Page-McCaw, A.J. Ewald, Z. Werb, Matrix metalloproteinases and the regulation of tissue remodelling, Nat. Rev. Mol. Cell Biol. 8 (2007) 221-233.
    [69]
    Y. Tian, S. Sheng, W. Gao, et al., Sonodynamic therapy suppresses matrix collagen degradation in vulnerable atherosclerotic plaque by modulating caspase 3-PEDF/HIF-1alpha - MMP-2/MMP-9 signaling in macrophages, PLoS One 17 (2022) e279191.
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