Landscape of Cellular Bioeffects Triggered by Ultrasound-Induced Sonoporation

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2022 Oct 14

PMID 36232532

Authors

Dawid Przystupski

Marek Ussowicz

Affiliations

Soon will be listed here.

Abstract

Sonoporation is the process of transient pore formation in the cell membrane triggered by ultrasound (US). Numerous studies have provided us with firm evidence that sonoporation may assist cancer treatment through effective drug and gene delivery. However, there is a massive gap in the body of literature on the issue of understanding the complexity of biophysical and biochemical sonoporation-induced cellular effects. This study provides a detailed explanation of the US-triggered bioeffects, in particular, cell compartments and the internal environment of the cell, as well as the further consequences on cell reproduction and growth. Moreover, a detailed biophysical insight into US-provoked pore formation is presented. This study is expected to review the knowledge of cellular effects initiated by US-induced sonoporation and summarize the attempts at clinical implementation.

Citing Articles

Harnessing Ultrasonic Technologies to Treat Skin Infections.

Hulme J Molecules. 2025; 30(3).

PMID: 39942617 PMC: 11819699. DOI: 10.3390/molecules30030512.

Influence of cell shape on sonoporation efficiency in microbubble-facilitated delivery using micropatterned cell arrays.

Baig M, Du Y, Zan Z, Fan Z Sci Rep. 2024; 14(1):30845.

PMID: 39730459 PMC: 11680583. DOI: 10.1038/s41598-024-81410-1.

Ultrasound-stimulated Microbubbles for Treatment of Pancreatic Cancer Cells with Radiation and Nanoparticles: Study.

Nakayama M, Noda A, Akasaka H, Tominaga T, McCorkell G, Geso M J Med Phys. 2024; 49(3):326-334.

PMID: 39526155 PMC: 11548062. DOI: 10.4103/jmp.jmp_30_24.

Development and mechanism exploration of a quantitative model for Escherichia coli transformation efficiency based on ultrasonic power.

Leng F, Wang Y, Zhu N, Guo X, Luo W, Wang Y Ultrason Sonochem. 2024; 111:107132.

PMID: 39481288 PMC: 11554641. DOI: 10.1016/j.ultsonch.2024.107132.

Focused ultrasound-induced cell apoptosis for the treatment of tumours.

Wang N, Luo L, Xu X, Zhou H, Li F PeerJ. 2024; 12:e17886.

PMID: 39184389 PMC: 11344538. DOI: 10.7717/peerj.17886.

References

Paskeviciute M, Petrikaite V . Overcoming transporter-mediated multidrug resistance in cancer: failures and achievements of the last decades. Drug Deliv Transl Res. 2018; 9(1):379-393. DOI: 10.1007/s13346-018-0584-7. View

Duan L, Yang L, Jin J, Yang F, Liu D, Hu K . Micro/nano-bubble-assisted ultrasound to enhance the EPR effect and potential theranostic applications. Theranostics. 2020; 10(2):462-483. PMC: 6929974. DOI: 10.7150/thno.37593. View

Khayamian M, Baniassadi M, Abdolahad M . Monitoring the effect of sonoporation on the cells using electrochemical approach. Ultrason Sonochem. 2017; 41:619-625. DOI: 10.1016/j.ultsonch.2017.10.030. View

Furusawa Y, Iizumi T, Fujiwara Y, Hassan M, Tabuchi Y, Nomura T . Ultrasound activates ataxia telangiectasia mutated- and rad3-related (ATR)-checkpoint kinase 1 (Chk1) pathway in human leukemia Jurkat cells. Ultrason Sonochem. 2012; 19(6):1246-51. DOI: 10.1016/j.ultsonch.2012.04.003. View

Boissenot T, Bordat A, Fattal E, Tsapis N . Ultrasound-triggered drug delivery for cancer treatment using drug delivery systems: From theoretical considerations to practical applications. J Control Release. 2016; 241:144-163. DOI: 10.1016/j.jconrel.2016.09.026. View

Beekers I, Vegter M, Lattwein K, Mastik F, Beurskens R, van der Steen A . Opening of endothelial cell-cell contacts due to sonoporation. J Control Release. 2020; 322:426-438. DOI: 10.1016/j.jconrel.2020.03.038. View

Awada A, Piccart M . Strategies offering protection from the toxic effects of anticancer treatments with a focus on chemoprotective agents. Curr Opin Oncol. 2000; 12(4):289-96. DOI: 10.1097/00001622-200007000-00003. View

Deng C, Sieling F, Pan H, Cui J . Ultrasound-induced cell membrane porosity. Ultrasound Med Biol. 2004; 30(4):519-26. DOI: 10.1016/j.ultrasmedbio.2004.01.005. View

Chen X, Leow R, Hu Y, Wan J, Yu A . Single-site sonoporation disrupts actin cytoskeleton organization. J R Soc Interface. 2014; 11(95):20140071. PMC: 4006247. DOI: 10.1098/rsif.2014.0071. View

10.

Bonner W, Redon C, Dickey J, Nakamura A, Sedelnikova O, Solier S . GammaH2AX and cancer. Nat Rev Cancer. 2008; 8(12):957-67. PMC: 3094856. DOI: 10.1038/nrc2523. View

11.

Basta G, Venneri L, Lazzerini G, Pasanisi E, Pianelli M, Vesentini N . In vitro modulation of intracellular oxidative stress of endothelial cells by diagnostic cardiac ultrasound. Cardiovasc Res. 2003; 58(1):156-61. DOI: 10.1016/s0008-6363(02)00665-x. View

12.

Lai C, Wu C, Chen C, Li P . Quantitative relations of acoustic inertial cavitation with sonoporation and cell viability. Ultrasound Med Biol. 2006; 32(12):1931-41. DOI: 10.1016/j.ultrasmedbio.2006.06.020. View

13.

Juffermans L, Kamp O, Dijkmans P, Visser C, Musters R . Low-intensity ultrasound-exposed microbubbles provoke local hyperpolarization of the cell membrane via activation of BK(Ca) channels. Ultrasound Med Biol. 2007; 34(3):502-8. DOI: 10.1016/j.ultrasmedbio.2007.09.010. View

14.

Yu H, Xu L . Cell experimental studies on sonoporation: state of the art and remaining problems. J Control Release. 2013; 174:151-60. DOI: 10.1016/j.jconrel.2013.11.010. View

15.

Nozaki T, Ogawa R, Feril Jr L, Kagiya G, Fuse H, Kondo T . Enhancement of ultrasound-mediated gene transfection by membrane modification. J Gene Med. 2003; 5(12):1046-55. DOI: 10.1002/jgm.445. View

16.

Beguin E, Shrivastava S, Dezhkunov N, McHale A, Callan J, Eleanor Stride . Direct Evidence of Multibubble Sonoluminescence Using Therapeutic Ultrasound and Microbubbles. ACS Appl Mater Interfaces. 2019; 11(22):19913-19919. PMC: 7006998. DOI: 10.1021/acsami.9b07084. View

17.

Day C, Kenworthy A . Tracking microdomain dynamics in cell membranes. Biochim Biophys Acta. 2008; 1788(1):245-53. PMC: 2792115. DOI: 10.1016/j.bbamem.2008.10.024. View

18.

Deng Z, Yan F, Jin Q, Li F, Wu J, Liu X . Reversal of multidrug resistance phenotype in human breast cancer cells using doxorubicin-liposome-microbubble complexes assisted by ultrasound. J Control Release. 2013; 174:109-16. DOI: 10.1016/j.jconrel.2013.11.018. View

19.

Lim K, Lee C, Earnest A, Seet R, Halliwell B . Does radiotherapy increase oxidative stress? A study with nasopharyngeal cancer patients revealing anomalies in isoprostanes measurements. Free Radic Res. 2010; 44(9):1064-71. DOI: 10.3109/10715762.2010.499906. View

20.

Le Gac S, Zwaan E, van den Berg A, Ohl C . Sonoporation of suspension cells with a single cavitation bubble in a microfluidic confinement. Lab Chip. 2007; 7(12):1666-72. DOI: 10.1039/b712897p. View