Generic placeholder image

Current Medicinal Chemistry


ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Advances and Prospects of Ultrasound Targeted Drug Delivery Systems Using Biomaterial-modified Micro/Nanobubbles for Tumor Therapy

Author(s): Chen Lin, Ye-Zi Chen, Bo Wu, Meng-Ting Yang, Chao-Qi Liu* and Yun Zhao*

Volume 29, Issue 30, 2022

Published on: 20 May, 2022

Page: [5062 - 5075] Pages: 14

DOI: 10.2174/0929867329666220331110315

Price: $65


The incidence of malignant tumors is rising rapidly and tends to be in the younger, which has been one of the most important factors endangering the safety of human life. Ultrasound micro/nanobubbles, as a noninvasive and highly specific antitumor strategy, can reach and destroy tumor tissue through their effects of cavitation and acoustic perforation under the guidance of ultrasound. Meanwhile, micro/nanobubbles are now used as a novel drug carrier, releasing drugs at a target region, especially on the prospects of biomaterial-modified micro/nanobubbles as a dual modality for drug delivery and therapeutic monitoring. Successful evaluation of the sonoporation mechanism(s), ultrasound parameters, drug type, and dose will need to be addressed before translating this technology for clinical use. Therefore, this paper collects the literature on the experimental and clinical studies of ultrasound biomaterial-modified micro/nanobubbles therapy in vitro and in vivo in recent years.

Keywords: Ultrasound, micro/nanobubble, targeting, drug delivery system, molecule delivery, tumor therapy, biomaterial.

Wu, C.; Li, M.; Meng, H.; Liu, Y.; Niu, W.; Zhou, Y.; Zhao, R.; Duan, Y.; Zeng, Z.; Li, X.; Li, G.; Xiong, W.; Zhou, M. Analysis of status and countermeasures of cancer incidence and mortality in China. Sci. China Life Sci., 2019, 62(5), 640-647.
[] [PMID: 30900169]
Feng, G.; Hao, L.; Xu, C.; Ran, H.; Zheng, Y.; Li, P.; Cao, Y.; Wang, Q.; Xia, J.; Wang, Z. High-intensity focused ultrasound-triggered nanoscale bubble-generating liposomes for efficient and safe tumor ablation under photoacoustic imaging monitoring. Int. J. Nanomedicine, 2017, 12, 4647-4659.
[] [PMID: 28721041]
Wrobel, P.; Ahmed, S. Current status of immunotherapy in metastatic colorectal cancer. Int. J. Colorectal Dis., 2019, 34(1), 13-25.
[] [PMID: 30465238]
Ji, T.T.; Chen, Q.N.; Tao, S.D.; Yu, L. Reaserch advance on bruton tyrosine kinase inhibitors in the treatment of B- cell tumors-review. Zhongguo Shi Yan Xue Ye Xue Za Zhi, 2020, 28(1), 333-338.
[PMID: 32027299]
de Leon, A.; Perera, R.; Nittayacharn, P.; Cooley, M.; Jung, O.; Exner, A.A. Ultrasound contrast agents and delivery systems in cancer detection and therapy. Adv. Cancer Res., 2018, 139, 57-84.
[] [PMID: 29941107]
Luo, M.H.; Yeh, C.K.; Situ, B.; Yu, J.S.; Li, B.C.; Chen, Z.Y. Microbubbles: A novel strategy for chemotherapy. Curr. Pharm. Des., 2017, 23(23), 3383-3390.
[] [PMID: 28088911]
Tzu-Yin, W.; Wilson, K.E.; Machtaler, S.; Willmann, J.K. Ultrasound and microbubble guided drug delivery: Mechanistic understanding and clinical implications. Curr. Pharm. Biotechnol., 2013, 14(8), 743-752.
[PMID: 24372231]
Khokhlova, T.D.; Haider, Y.; Hwang, J.H. Therapeutic potential of ultrasound microbubbles in gastrointestinal oncology: Recent advances and future prospects. Therap. Adv. Gastroenterol., 2015, 8(6), 384-394.
[] [PMID: 26557894]
Pellow, C.; O’Reilly, M.A.; Hynynen, K.; Zheng, G.; Goertz, D.E. Simultaneous intravital optical and acoustic monitoring of ultrasound-triggered nanobubble generation and extravasation. Nano Lett., 2020, 20(6), 4512-4519.
[] [PMID: 32374617]
Mauri, G.; Nicosia, L.; Xu, Z.; Di Pietro, S.; Monfardini, L.; Bonomo, G.; Varano, G.M.; Prada, F.; Della Vigna, P.; Orsi, F. Focused ultrasound: Tumour ablation and its potential to enhance immunological therapy to cancer. Br. J. Radiol., 2018, 91(1083), 20170641.
[] [PMID: 29168922]
Tharkar, P.; Varanasi, R.; Wong, W.S.F.; Jin, C.T.; Chrzanowski, W. Nano-Enhanced drug delivery and therapeutic ultrasound for cancer treatment and beyond. Front. Bioeng. Biotechnol., 2019, 7, 324.
[] [PMID: 31824930]
Duan, L.; Yang, L.; Jin, J.; Yang, F.; Liu, D.; Hu, K.; Wang, Q.; Yue, Y.; Gu, N. Micro/nano-bubble-assisted ultrasound to enhance the EPR effect and potential theranostic applications. Theranostics, 2020, 10(2), 462-483.
[] [PMID: 31903132]
Kopechek, J.A.; Carson, A.R.; McTiernan, C.F.; Chen, X.; Hasjim, B.; Lavery, L.; Sen, M.; Grandis, J.R.; Villanueva, F.S. Ultrasound targeted microbubble destruction-mediated delivery of a transcription factor decoy inhibits STAT3 signaling and tumor growth. Theranostics, 2015, 5(12), 1378-1387.
[] [PMID: 26681983]
Fan, C.H.; Cheng, Y.H.; Ting, C.Y.; Ho, Y.J.; Hsu, P.H.; Liu, H.L.; Yeh, C.K. Ultrasound/Magnetic targeting with SPIO-DOX-Microbubble complex for image-guided drug delivery in brain tumors. Theranostics, 2016, 6(10), 1542-1556.
[] [PMID: 27446489]
Ibsen, S.; Schutt, C.E.; Esener, S. Microbubble-mediated ultrasound therapy: A review of its potential in cancer treatment. Drug Des. Devel. Ther., 2013, 7, 375-388.
[] [PMID: 23667309]
Ambika Rajendran, M. Ultrasound-guided microbubble in the treatment of cancer: A mini narrative review. Cureus, 2018, 10(9), e3256.
[] [PMID: 30416906]
Ilovitsh, T.; Ilovitsh, A.; Foiret, J.; Caskey, C.F.; Kusunose, J.; Fite, B.Z.; Zhang, H.; Mahakian, L.M.; Tam, S.; Butts-Pauly, K.; Qin, S.; Ferrara, K.W. Enhanced microbubble contrast agent oscillation following 250 kHz insonation. Sci. Rep., 2018, 8(1), 16347.
[] [PMID: 30397280]
Song, K.H.; Harvey, B.K.; Borden, M.A. State-of-the-art of microbubble-assisted blood-brain barrier disruption. Theranostics, 2018, 8(16), 4393-4408.
[] [PMID: 30214628]
Thurman, J.; Gueler, F. Recent advances in renal imaging. F1000Res, 2018, 7, F1000.
Errico, C.; Pierre, J.; Pezet, S.; Desailly, Y.; Lenkei, Z.; Couture, O.; Tanter, M. Ultrafast ultrasound localization microscopy for deep super-resolution vascular imaging. Nature, 2015, 527(7579), 499-502.
[] [PMID: 26607546]
Hossen, S.; Hossain, M.K.; Basher, M.K.; Mia, M.N.H.; Rahman, M.T.; Uddin, M.J. Smart nanocarrier-based drug delivery systems for cancer therapy and toxicity studies: A review. J. Adv. Res., 2018, 15, 1-18.
[] [PMID: 30581608]
Jurney, P.; Agarwal, R.; Singh, V.; Choi, D.; Roy, K.; Sreenivasan, S.V.; Shi, L. Unique size and shape-dependent uptake behaviors of non-spherical nanoparticles by endothelial cells due to a shearing flow. J. Control. Release, 2017, 245, 170-176.
[] [PMID: 27916535]
Wolfram, J.; Zhu, M.; Yang, Y.; Shen, J.; Gentile, E.; Paolino, D.; Fresta, M.; Nie, G.; Chen, C.; Shen, H.; Ferrari, M.; Zhao, Y. Safety of nanoparticles in medicine. Curr. Drug Targets, 2015, 16(14), 1671-1681.
[] [PMID: 26601723]
Kumar, A.; Zhang, X.; Liang, X.J. Gold nanoparticles: Emerging paradigm for targeted drug delivery system. Biotechnol. Adv., 2013, 31(5), 593-606.
[] [PMID: 23111203]
Singh, P.; Pandit, S.; Mokkapati, V.R.S.S.; Garg, A.; Ravikumar, V.; Mijakovic, I. Gold nanoparticles in diagnostics and therapeutics for human cancer. Int. J. Mol. Sci., 2018, 19(7), 1979.
[] [PMID: 29986450]
Petkar, K.C.; Chavhan, S.S.; Agatonovik-Kustrin, S.; Sawant, K.K. Nanostructured materials in drug and gene delivery: A review of the state of the art. Crit. Rev. Ther. Drug Carrier Syst., 2011, 28(2), 101-164.
[] [PMID: 21663574]
Mieszawska, A.J.; Mulder, W.J.; Fayad, Z.A.; Cormode, D.P. Multifunctional gold nanoparticles for diagnosis and therapy of disease. Mol. Pharm., 2013, 10(3), 831-847.
[] [PMID: 23360440]
Cruje, C.; Chithrani, B.D. Integration of peptides for enhanced uptake of pegylayed gold nanoparticles. J. Nanosci. Nanotechnol., 2015, 15(3), 2125-2131.
[] [PMID: 26413630]
Aminabad, N.S.; Farshbaf, M.; Akbarzadeh, A. Recent advances of gold nanoparticles in biomedical applications: State of the art. Cell Biochem. Biophys., 2019, 77(2), 123-137.
[] [PMID: 30570696]
Tietze, R.; Zaloga, J.; Unterweger, H.; Lyer, S.; Friedrich, R.P.; Janko, C.; Pöttler, M.; Dürr, S.; Alexiou, C. Magnetic nanoparticle-based drug delivery for cancer therapy. Biochem. Biophys. Res. Commun., 2015, 468(3), 463-470.
[] [PMID: 26271592]
Khan, D.R.; Rezler, E.M.; Lauer-Fields, J.; Fields, G.B. Effects of drug hydrophobicity on liposomal stability. Chem. Biol. Drug Des., 2008, 71(1), 3-7.
[] [PMID: 18086150]
Zununi Vahed, S.; Salehi, R.; Davaran, S.; Sharifi, S. Liposome-based drug co-delivery systems in cancer cells. Mater. Sci. Eng. C, 2017, 71, 1327-1341.
[] [PMID: 27987688]
Ma, Y.; Han, J.; Jiang, J.; Zheng, Z.; Tan, Y.; Liu, C.; Zhao, Y. Ultrasound targeting of microbubble-bound anti PD-L1 mAb to enhance anti-tumor effect of cisplatin in cervical cancer xenografts treatment. Life Sci., 2020, 262, 118565.
[] [PMID: 33038371]
Xu, R.X. Multifunctional microbubbles and nanobubbles for photoacoustic imaging. Contrast Media Mol. Imaging, 2011, 6(5), 401-411.
[] [PMID: 22025340]
Tan, Y.; Yang, S.; Ma, Y.; Li, J.; Xie, Q.; Liu, C.; Zhao, Y. Nanobubbles containing sPD-1 and Ce6 mediate combination immunotherapy and suppress hepatocellular carcinoma in mice. Int. J. Nanomedicine, 2021, 16, 3241-3254.
[] [PMID: 34007176]
Liu, Y.; Jiang, J.; Liu, C.; Zhao, W.; Ma, Y.; Zheng, Z.; Zhou, Q.; Zhao, Y. Synergistic anti-tumor effect of anti-PD-L1 antibody cationic microbubbles for delivery of the miR-34a gene combined with ultrasound on cervical carcinoma. Am. J. Transl. Res., 2021, 13(3), 988-1005.
[PMID: 33841635]
Khayamian, M.A.; Shalileh, S.; Vanaei, S.; Salemizadeh Parizi, M.; Ansaryan, S.; Saghafi, M.; Abbasvandi, F.; Ebadi, A.; Soltan Khamsi, P.; Abdolahad, M. Electrochemical generation of microbubbles by carbon nanotube interdigital electrodes to increase the permeability and material uptakes of cancer cells. Drug Deliv., 2019, 26(1), 928-934.
[] [PMID: 31526074]
Song, R.; Peng, C.; Xu, X.; Wang, J.; Yu, M.; Hou, Y.; Zou, R.; Yao, S. Controllable formation of monodisperse polymer microbubbles as ultrasound contrast agents. ACS Appl. Mater. Interfaces, 2018, 10(17), 14312-14320.
[] [PMID: 29637761]
Chen, M.; Liang, X.; Gao, C.; Zhao, R.; Zhang, N.; Wang, S.; Chen, W.; Zhao, B.; Wang, J.; Dai, Z. Ultrasound triggered conversion of porphyrin/camptothecin-fluoroxyuridine triad microbubbles into nanoparticles overcomes multidrug resistance in colorectal cancer. ACS Nano, 2018, 12(7), 7312-7326.
[] [PMID: 29901986]
Song, K.H.; Trudeau, T.; Kar, A.; Borden, M.A.; Gutierrez-Hartmann, A. Ultrasound-mediated delivery of siESE complexed with microbubbles attenuates HER2+/- cell line proliferation and tumor growth in rodent models of breast cancer. Nanotheranostics, 2019, 3(2), 212-222.
[] [PMID: 31183315]
Upadhyay, A.; Yagnik, B.; Desai, P.; Dalvi, S.V. Microbubble-Mediated enhanced delivery of curcumin to cervical cancer cells. ACS Omega, 2018, 3(10), 12824-12831.
[] [PMID: 30411020]
Ren, S.T.; Shen, S.; He, X.Y.; Liao, Y.R.; Sun, P.F.; Wang, B.; Zhao, W.B.; Han, S.P.; Wang, Y.L.; Tian, T. The effect of docetaxel-loaded micro-bubbles combined with low-frequency ultrasound in H22 hepatocellular carcinoma-bearing mice. Ultrasound Med. Biol., 2016, 42(2), 549-560.
[] [PMID: 26651601]
Chen, H.K.; Zhang, S.M.; Chang, J.L.; Chen, H.C.; Lin, Y.C.; Shih, C.P.; Sytwu, H.K.; Fang, M.C.; Lin, Y.Y.; Kuo, C.Y.; Liao, A.H.; Chu, Y.H.; Wang, C.H. Insonation of systemically delivered cisplatin-loaded microbubbles significantly attenuates nephrotoxicity of chemotherapy in experimental models of head and neck cancer. Cancers (Basel), 2018, 10(9), 311.
[] [PMID: 30189620]
Iijima, M.; Gombodorj, N.; Tachibana, Y.; Tachibana, K.; Yokobori, T.; Honma, K.; Nakano, T.; Asao, T.; Kuwahara, R.; Aoyama, K.; Yasuda, H.; Kelly, M.; Kuwano, H.; Yamanouchi, D. Development of single nanometer-sized ultrafine oxygen bubbles to overcome the hypoxia-induced resistance to radiation therapy via the suppression of hypoxia-inducible factor-1α. Int. J. Oncol., 2018, 52(3), 679-686.
[] [PMID: 29393397]
Deng, L.; Cai, X.; Sheng, D.; Yang, Y.; Strohm, E.M.; Wang, Z.; Ran, H.; Wang, D.; Zheng, Y.; Li, P.; Shang, T.; Ling, Y.; Wang, F.; Sun, Y. A laser-activated biocompatible theranostic nanoagent for targeted multimodal imaging and photothermal therapy. Theranostics, 2017, 7(18), 4410-4423.
[] [PMID: 29158836]
Wei, Z.; Lin, X.; Wu, M.; Zhao, B.; Lin, R.; Zhang, D.; Zhang, Y.; Liu, G.; Liu, X.; Liu, J. Core-shell NaGdF4@CaCO3 nanoparticles for enhanced magnetic resonance/ultrasonic dual-modal imaging via tumor acidic micro-enviroment triggering. Sci. Rep., 2017, 7(1), 5370.
[] [PMID: 28710468]
Kooiman, K.; Roovers, S.; Langeveld, S.A.G.; Kleven, R.T.; Dewitte, H.; O’Reilly, M.A.; Escoffre, J.M.; Bouakaz, A.; Verweij, M.D.; Hynynen, K.; Lentacker, I.; Stride, E.; Holland, C.K. Ultrasound-Responsive cavitation nuclei for therapy and drug delivery. Ultrasound Med. Biol., 2020, 46(6), 1296-1325.
[] [PMID: 32165014]
Zhang, J.; Liu, S.; Zhu, Y.; Zhang, L.; Li, W.; Wang, F.; Huang, S. Preparation and characterization of luteinising-hormone releasing hormone nanoliposomal microbubbles specifically targeting ovarian cancer cells in vitro. Mol. Med. Rep., 2014, 10(1), 567-571.
[] [PMID: 24805264]
Zhang, J.; Song, L.; Zhang, H.; Zhou, S.; Jiao, Y.; Zhang, X.; Zhao, Y.; Wang, Y. New polylactic acid multifunctional ultrasound contrast agent based on graphene oxide as the carrier of targeted factor and drug delivery. ACS Omega, 2019, 4(3), 4691-4696.
[] [PMID: 31459655]
Wu, H.; Abenojar, E.C.; Perera, R.; De Leon, A.C.; An, T.; Exner, A.A. Time-intensity-curve analysis and tumor extravasation of nanobubble ultrasound contrast agents. Ultrasound Med. Biol., 2019, 45(9), 2502-2514.
[] [PMID: 31248638]
Song, L.; Wang, G.; Hou, X.; Kala, S.; Qiu, Z.; Wong, K.F.; Cao, F.; Sun, L. Biogenic nanobubbles for effective oxygen delivery and enhanced photodynamic therapy of cancer. Acta Biomater., 2020, 108, 313-325.
[] [PMID: 32268236]
Endo-Takahashi, Y.; Negishi, Y. Microbubbles and nanobubbles with ultrasound for systemic gene delivery. Pharmaceutics, 2020, 12(10), 964.
[] [PMID: 33066531]
Hamanishi, J.; Mandai, M.; Matsumura, N.; Abiko, K.; Baba, T.; Konishi, I. PD-1/PD-L1 blockade in cancer treatment: Perspectives and issues. Int. J. Clin. Oncol., 2016, 21(3), 462-473.
[] [PMID: 26899259]
Rowshanravan, B.; Halliday, N.; Sansom, D.M. CTLA-4: A moving target in immunotherapy. Blood, 2018, 131(1), 58-67.
[] [PMID: 29118008]
Buchbinder, E.I.; Desai, A. CTLA-4 and PD-1 pathways: Similarities, differences, and implications of their inhibition. Am. J. Clin. Oncol., 2016, 39(1), 98-106.
[] [PMID: 26558876]
Simons, M.; Gordon, E.; Claesson-Welsh, L. Mechanisms and regulation of endothelial VEGF receptor signalling. Nat. Rev. Mol. Cell Biol., 2016, 17(10), 611-625.
[] [PMID: 27461391]
Eschbach, R.S.; Clevert, D.A.; Hirner-Eppeneder, H.; Ingrisch, M.; Moser, M.; Schuster, J.; Tadros, D.; Schneider, M.; Kazmierczak, P.M.; Reiser, M.; Cyran, C.C. Contrast-Enhanced ultrasound with VEGFR2-Targeted microbubbles for monitoring regorafenib therapy effects in experimental colorectal adenocarcinomas in rats with DCE-MRI and immunohistochemical validation. PLoS One, 2017, 12(1), e0169323.
[] [PMID: 28060884]
Ingram, N.; McVeigh, L.E.; Abou-Saleh, R.H.; Maynard, J.; Peyman, S.A.; McLaughlan, J.R.; Fairclough, M.; Marston, G.; Valleley, E.M.A.; Jimenez-Macias, J.L.; Charalambous, A.; Townley, W.; Haddrick, M.; Wierzbicki, A.; Wright, A.; Volpato, M.; Simpson, P.B.; Treanor, D.E.; Thomson, N.H.; Loadman, P.M.; Bushby, R.J.; Johnson, B.R.G.; Jones, P.F.; Evans, J.A.; Freear, S.; Markham, A.F.; Evans, S.D.; Coletta, P.L. Ultrasound-triggered therapeutic microbubbles enhance the efficacy of cytotoxic drugs by increasing circulation and tumor drug accumulation and limiting bioavailability and toxicity in normal tissues. Theranostics, 2020, 10(24), 10973-10992.
[] [PMID: 33042265]
Dimitrov, D.S. Therapeutic proteins. Methods Mol. Biol., 2012, 899, 1-26.
[] [PMID: 22735943]
Sloand, J.N.; Nguyen, T.T.; Zinck, S.A.; Cook, E.C.; Zimudzi, T.J.; Showalter, S.A.; Glick, A.B.; Simon, J.C.; Medina, S.H. Ultrasound-Guided cytosolic protein delivery via transient fluorous masks. ACS Nano, 2020, 14(4), 4061-4073.
[] [PMID: 32134630]
Wu, H.; Chisholm, C.F.; Puryear, M.; Movafaghi, S.; Smith, S.D.; Pokhilchuk, Y.; Lengsfeld, C.S.; Randolph, T.W. Container surfaces control initiation of cavitation and resulting particle formation in protein formulations after application of mechanical shock. J. Pharm. Sci., 2020, 109(3), 1270-1280.
[] [PMID: 31758950]
Xiong, X.; Zhao, F.; Shi, M.; Yang, H.; Liu, Y. Polymeric microbubbles for ultrasonic molecular imaging and targeted therapeutics. J. Biomater. Sci. Polym. Ed., 2011, 22(4-6), 417-428.
[] [PMID: 21144258]
Owen, J.; Kamila, S.; Shrivastava, S.; Carugo, D.; Bernardino de la Serna, J.; Mannaris, C.; Pereno, V.; Browning, R.; Beguin, E.; McHale, A.P.; Callan, J.F.; Stride, E. The role of PEG-40-stearate in the production, morphology, and stability of microbubbles. Langmuir, 2019, 35(31), 10014-10024.
[] [PMID: 30485112]
Ergen, C.; Heymann, F.; Al Rawashdeh, W.; Gremse, F.; Bartneck, M.; Panzer, U.; Pola, R.; Pechar, M.; Storm, G.; Mohr, N.; Barz, M.; Zentel, R.; Kiessling, F.; Trautwein, C.; Lammers, T.; Tacke, F. Targeting distinct myeloid cell populations in vivo using polymers, liposomes and microbubbles. Biomaterials, 2017, 114, 106-120.
[] [PMID: 27855336]
Li, L.; Fu, J.; Wang, X.; Chen, Q.; Zhang, W.; Cao, Y.; Ran, H. Biomimetic “Nanoplatelets” as a targeted drug delivery platform for breast cancer theranostics. ACS Appl. Mater. Interfaces, 2021, 13(3), 3605-3621.
[] [PMID: 33449625]
Cerroni, B.; Cicconi, R.; Oddo, L.; Scimeca, M.; Bonfiglio, R.; Bernardini, R.; Palmieri, G.; Domenici, F.; Bonanno, E.; Mattei, M.; Paradossi, G. In vivo biological fate of poly(vinylalcohol) microbubbles in mice. Heliyon, 2018, 4(9), e00770.
[] [PMID: 30238062]
Basuony, S.A.H.A.E.; Hamed, R.S. Anti-Micro RNA-221 a promising genetic therapy of oral squamous cell carcinoma (SCC-25). Braz. Dent. J., 2020, 31(6), 634-639.
[] [PMID: 33237235]
Goldshtein, M.; Shamir, S.; Vinogradov, E.; Monsonego, A.; Cohen, S. Co-assembled Ca2+ alginate-sulfate nanoparticles for intracellular plasmid DNA delivery. Mol. Ther. Nucleic Acids, 2019, 16, 378-390.
[] [PMID: 31003172]
Ruvinov, E.; Kryukov, O.; Forti, E.; Korin, E.; Goldstein, M.; Cohen, S. Calcium-siRNA nanocomplexes: What reversibility is all about. J. Control. Release, 2015, 203, 150-160.
[] [PMID: 25702963]
Wu, M.; Song, Z.; Zhang, S.; Dan, Q.; Tang, C.; Peng, C.; Liang, Y.; Zhang, L.; Wang, H.; Li, Y. Local tumor ischemia-reperfusion mediated by ultrasound-targeted microbubble destruction enhances the anti-tumor efficacy of doxorubicin chemotherapy. Cancer Manag. Res., 2019, 11, 9387-9395.
[] [PMID: 31807068]
Zhou, S.; Zheng, S.; Shan, Y.; Li, L.; Zhang, X.; Wang, C. Rituximab-conjugated and doxorubicin-loaded microbubbles combined with ultrasound irradiation inhibits proliferation and induces apoptosis in Raji cell lines. Oncol. Rep., 2016, 35(2), 801-808.
[] [PMID: 26718487]
a) Li, T.; Hu, Z.; Wang, C.; Yang, J.; Zeng, C.; Fan, R.; Guo, J. PD-L1-targeted microbubbles loaded with docetaxel produce a synergistic effect for the treatment of lung cancer under ultrasound irradiation. Biomater. Sci., 2020, 8(5), 1418-1430. (b) Yu, J.; Zhao, Y.; Liu, C.; Hu, B.; Zhao, M.; Ma, Y.; Jiang, J. Synergistic anti-tumor effect of paclitaxel and miR-34a combined with ultrasound microbubbles on cervical cancer in vivo and in vitro. Clin. Translat. Oncol., 2020, 22(1), 60-69.
[] [PMID: 31093891]
McEwan, C.; Fowley, C.; Nomikou, N.; McCaughan, B.; McHale, A.P.; Callan, J.F. Polymeric microbubbles as delivery vehicles for sensitizers in sonodynamic therapy. Langmuir, 2014, 30(49), 14926-14930.
[] [PMID: 25409533]
Gao, X.; Nan, Y.; Yuan, Y.; Gong, X.; Sun, Y.; Zhou, H.; Zong, Y.; Zhang, L.; Yu, M. Gas-filled ultrasound microbubbles enhance the immunoactivity of the HSP70- MAGEA1 fusion protein against MAGEA1-expressing tumours. Mol. Med. Rep., 2018, 18(1), 315-321.
[] [PMID: 29749485]
Zhang, B.; Chen, M.; Zhang, Y.; Chen, W.; Zhang, L.; Chen, L. An ultrasonic nanobubble-mediated PNP/fludarabine suicide gene system: A new approach for the treatment of hepatocellular carcinoma. PLoS One, 2018, 13(5), e0196686.
[] [PMID: 29718963]
Zhang, Y.; Zhang, M.; Fan, X.; Mao, D.; Lv, S.; Chen, P. Effect of STAT3 decoy oligodeoxynucleotides mediated by ultrasound-targeted microbubbles combined with ultrasound on the growth of squamous cell carcinoma of the esophagus. Oncol. Lett., 2019, 17(2), 2151-2158.
[PMID: 30675281]
Devulapally, R.; Lee, T.; Barghava-Shah, A.; Sekar, T.V.; Foygel, K.; Bachawal, S.V.; Willmann, J.K.; Paulmurugan, R. Ultrasound-guided delivery of thymidine kinase-nitroreductase dual therapeutic genes by PEGylated-PLGA/PIE nanoparticles for enhanced triple negative breast cancer therapy. Nanomedicine (Lond.), 2018, 13(9), 1051-1066.
[] [PMID: 29790803]
Ilovitsh, T.; Feng, Y.; Foiret, J.; Kheirolomoom, A.; Zhang, H.; Ingham, E.S.; Ilovitsh, A.; Tumbale, S.K.; Fite, B.Z.; Wu, B.; Raie, M.N.; Zhang, N.; Kare, A.J.; Chavez, M.; Qi, L.S.; Pelled, G.; Gazit, D.; Vermesh, O.; Steinberg, I.; Gambhir, S.S.; Ferrara, K.W. Low-frequency ultrasound-mediated cytokine transfection enhances T cell recruitment at local and distant tumor sites. Proc. Natl. Acad. Sci. USA, 2020, 117(23), 12674-12685.
[] [PMID: 32430322]
Cao, Y.; Chen, Y.; Yu, T.; Guo, Y.; Liu, F.; Yao, Y.; Li, P.; Wang, D.; Wang, Z.; Chen, Y.; Ran, H. Drug release from phase-changeable nanodroplets triggered by low-intensity focused ultrasound. Theranostics, 2018, 8(5), 1327-1339.
[] [PMID: 29507623]
Marshalek, J.P.; Sheeran, P.S.; Ingram, P.; Dayton, P.A.; Witte, R.S.; Matsunaga, T.O. Intracellular delivery and ultrasonic activation of folate receptor-targeted phase-change contrast agents in breast cancer cells in vitro . J. Control. Release, 2016, 243, 69-77.
[] [PMID: 27686582]
Luo, W.; Wen, G.; Yang, L.; Tang, J.; Wang, J.; Wang, J.; Zhang, S.; Zhang, L.; Ma, F.; Xiao, L.; Wang, Y.; Li, Y. Dual-targeted and pH-sensitive doxorubicin prodrug-microbubble complex with ultrasound for tumor treatment. Theranostics, 2017, 7(2), 452-465.
[] [PMID: 28255342]
Eisenbrey, J.R.; Shraim, R.; Liu, J.B.; Li, J.; Stanczak, M.; Oeffinger, B.; Leeper, D.B.; Keith, S.W.; Jablonowski, L.J.; Forsberg, F.; O’Kane, P.; Wheatley, M.A. Sensitization of hypoxic tumors to radiation therapy using ultrasound-sensitive oxygen microbubbles. Int. J. Radiat. Oncol. Biol. Phys., 2018, 101(1), 88-96.
[] [PMID: 29477294]
Ferrara, K.; Pollard, R.; Borden, M. Ultrasound microbubble contrast agents: Fundamentals and application to gene and drug delivery. Annu. Rev. Biomed. Eng., 2007, 9(1), 415-447.
[] [PMID: 17651012]
Hu, Y.Z.; Zhu, J.A.; Jiang, Y.G.; Hu, B. Ultrasound microbubble contrast agents: Application to therapy for peripheral vascular disease. Adv. Ther., 2009, 26(4), 425-434.
[] [PMID: 19381521]

Rights & Permissions Print Export Cite as
© 2023 Bentham Science Publishers | Privacy Policy