Vol 4, No 3 (2019)
Review article
Published online: 2019-09-20
Microbubble based sonoporation — from the basics into clinical implications
Medical Research Journal 2019;4(3):178-183.
Abstract
Sonoporation is a rapidly developing novel technique serving for drug delivery and non-viral gene therapy. It is based on the interaction between microbubbles located in the surrounding of a cell and its membrane. The interaction is obtained by excitation of microbubbles with ultrasounds. This leads to reversible cell membrane poration. Depending on the intensity of ultrasounds, structure of microbubbles used in an experiment and different environmental factors, microbubbles can interact in two manners. First, in lower ultrasound intensities, stable cavitation – regular microbubbles oscillations due to changes in the environment pressure. Microbubbles have to be very close to a cell membrane, therefore, they are usually targeted to an antigen located on the cell membrane by antibodies. Consequently, microbubbles push and pull on the cell membrane and create microstreaming around it causing its disruption. Second, inertial cavitation, where in contrary to the previous one, oscillations cause rapid collapse of microbubbles, which creates shock waves and microjets for the same purpose. No matter in which manner prorated, cells tend to reseal their disrupted cell membrane. Ca2+ ions play a crucial role in the process as well as endo exocytosis. Sonoporation has proved to be an effective modality against different diseases, including variety of cancer types in of both laboratory and clinical studies.
Keywords: sonoporationmicrobubblenanobubblesinertial cavitationgene therapy
References
- Diagnostic ultrasound Imaging : Inside out. Ultraschall in der Medizin - European Journal of Ultrasound. 2005; 25(06): 407–407.
- Thampy A, Huang Z, Slade A, et al. A Smart Ultrasonic Cutting System for Surgery. IFMBE Proceedings. 2009: 907–910.
- Coussios >, Farny CH, Haar GT, et al. Role of acoustic cavitation in the delivery and monitoring of cancer treatment by high-intensity focused ultrasound (HIFU). International Journal of Hyperthermia. 2009; 23(2): 105–120.
- Sackmann M, Delius M, Sauerbruch T, et al. Shock-Wave Lithotripsy of Gallbladder Stones. New England Journal of Medicine. 1988; 318(7): 393–397.
- Datta S, Coussios CC, Ammi AY, et al. Ultrasound-enhanced thrombolysis using Definity as a cavitation nucleation agent. Ultrasound Med Biol. 2008; 34(9): 1421–1433.
- Vaezy S, Martin R, Schmiedl U, et al. Liver hemostasis using high-intensity focused ultrasound. Ultrasound in Medicine & Biology. 1997; 23(9): 1413–1420.
- Hynynen K, McDannold N, Sheikov NA, et al. Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications. Neuroimage. 2005; 24(1): 12–20.
- Tachibana K, Feril LB, Ikeda-Dantsuji Y. Sonodynamic therapy. Ultrasonics. 2008; 48(4): 253–259.
- Ohl CD, Arora M, Ikink R, et al. Sonoporation from jetting cavitation bubbles. Biophys J. 2006; 91(11): 4285–4295.
- Cavalli R, Soster M, Argenziano M. Nanobubbles: a promising efficient tool for therapeutic delivery. Ther Deliv. 2016; 7(2): 117–138.
- Fan Z, Kumon RE, Park J, et al. Intracellular delivery and calcium transients generated in sonoporation facilitated by microbubbles. J Control Release. 2010; 142(1): 31–39.
- Park J, Fan Z, Deng CX. Effects of shear stress cultivation on cell membrane disruption and intracellular calcium concentration in sonoporation of endothelial cells. J Biomech. 2011; 44(1): 164–169.
- Zhou Y, Cui J, Deng C. Dynamics of Sonoporation Correlated with Acoustic Cavitation Activities. Biophysical Journal. 2008; 94(7): L51–L53.
- Ohgaki K, Khanh N, Joden Y, et al. Physicochemical approach to nanobubble solutions. Chemical Engineering Science. 2010; 65(3): 1296–1300.
- Perera RH, Hernandez C, Zhou H, et al. Ultrasound imaging beyond the vasculature with new generation contrast agents. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2015; 7(4): 593–608.
- Yin T, Wang P, Zheng R, et al. Nanobubbles for enhanced ultrasound imaging of tumors. Int J Nanomedicine. 2012; 7: 895–904.
- Xu JS, Huang J, Qin R, et al. Synthesizing and binding dual-mode poly (lactic-co-glycolic acid) (PLGA) nanobubbles for cancer targeting and imaging. Biomaterials. 2010; 31(7): 1716–1722.
- Byl NN. The use of ultrasound as an enhancer for transcutaneous drug delivery: phonophoresis. Phys Ther. 1995; 75(6): 539–553.
- Stride E. Physical principles of microbubbles for ultrasound imaging and therapy. Front Neurol Neurosci. 2015; 36: 11–22.
- Wu J, Ross JP, Chiu JF. Reparable sonoporation generated by microstreaming. J Acoust Soc Am. 2002; 111(3): 1460–1464.
- Collis J, Manasseh R, Liovic P, et al. Cavitation microstreaming and stress fields created by microbubbles. Ultrasonics. 2010; 50(2): 273–279.
- Qiu Y, Zhang C, Tu J, et al. Microbubble-induced sonoporation involved in ultrasound-mediated DNA transfection in vitro at low acoustic pressures. J Biomech. 2012; 45(8): 1339–1345.
- Fan Z, Kumon RE, Deng CX. Mechanisms of microbubble-facilitated sonoporation for drug and gene delivery. Ther Deliv. 2014; 5(4): 467–486.
- Kooiman K, Foppen-Harteveld M, van der Steen AFW, et al. Sonoporation of endothelial cells by vibrating targeted microbubbles. J Control Release. 2011; 154(1): 35–41.
- Liang HD, Tang J, Halliwell M. Sonoporation, drug delivery, and gene therapy. Proc Inst Mech Eng H. 2010; 224(2): 343–361.
- Miller M, Miller D, Brayman A. A review of in vitro bioeffects of inertial ultrasonic cavitation from a mechanistic perspective. Ultrasound in Medicine & Biology. 1996; 22(9): 1131–1154.
- Miller D, Thomas R. Ultrasound contrast agents nucleate inertial cavitation in vitro. Ultrasound in Medicine & Biology. 1995; 21(8): 1059–1065.
- Beerlage H, Leenders Gv, Oosterhof G, et al. High-intensity focused ultrasound (HIFU) followed after one to two weeks by radical retropubic prostatectomy: Results of a prospective study. The Prostate. 1999; 39(1): 41–46, doi: 10.1002/(sici)1097-0045(19990401)39:1<41::aid-pros7>3.0.co;2-5.
- Rosenthal I, Sostaric JZ, Riesz P. Sonodynamic therapy--a review of the synergistic effects of drugs and ultrasound. Ultrason Sonochem. 2004; 11(6): 349–363.
- Yu H, Xu L. Cell experimental studies on sonoporation: state of the art and remaining problems. J Control Release. 2014; 174: 151–160.
- Lentacker I, De Cock I, Deckers R, et al. Understanding ultrasound induced sonoporation: definitions and underlying mechanisms. Adv Drug Deliv Rev. 2014; 72: 49–64.
- Fan Z, Liu H, Mayer M, et al. Spatiotemporally controlled single cell sonoporation. Proc Natl Acad Sci U S A. 2012; 109(41): 16486–16491.
- Zhao YZ, Luo YK, Lu CT, et al. Phospholipids-based microbubbles sonoporation pore size and reseal of cell membrane cultured in vitro. J Drug Target. 2008; 16(1): 18–25.
- Zhou Y, Shi J, Cui J, et al. Effects of extracellular calcium on cell membrane resealing in sonoporation. J Control Release. 2008; 126(1): 34–43.
- Mayer CR, Geis NA, Katus HA, et al. Ultrasound targeted microbubble destruction for drug and gene delivery. Expert Opin Drug Deliv. 2008; 5(10): 1121–1138.
- Sirsi SR, Borden MA. Advances in ultrasound mediated gene therapy using microbubble contrast agents. Theranostics. 2012; 2(12): 1208–1222.
- Dimcevski G, Kotopoulis S, Bjånes T, et al. A human clinical trial using ultrasound and microbubbles to enhance gemcitabine treatment of inoperable pancreatic cancer. J Control Release. 2016; 243: 172–181.
- Rinaldi L, Franci G, Folliero V, et al. Sonoporation by microbubbles as gene therapy approach for liver cancer. Ultraschall in der Medizin - European Journal of Ultrasound. 2016; 37(S 01).
- Hirabayashi F, Iwanaga K, Okinaga T, et al. Epidermal growth factor receptor-targeted sonoporation with microbubbles enhances therapeutic efficacy in a squamous cell carcinoma model. PLoS One. 2017; 12(9): e0185293.
- Sarkar S, Quinn BA, Shen XN, et al. Therapy of prostate cancer using a novel cancer terminator virus and a small molecule BH-3 mimetic. Oncotarget. 2015; 6(13): 10712–10727.
- Rizzitelli S, Giustetto P, Faletto D, et al. The release of Doxorubicin from liposomes monitored by MRI and triggered by a combination of US stimuli led to a complete tumor regression in a breast cancer mouse model. J Control Release. 2016; 230: 57–63.
- Awad NS, Paul V, Al-Sayah MH, et al. Ultrasonically controlled albumin-conjugated liposomes for breast cancer therapy. Artif Cells Nanomed Biotechnol. 2019; 47(1): 705–714.
- Prasad C, Banerjee R. Ultrasound-Triggered Spatiotemporal Delivery of Topotecan and Curcumin as Combination Therapy for Cancer. J Pharmacol Exp Ther. 2019; 370(3): 876–893.
- Cai W, Lv W, Feng Y, et al. The therapeutic effect in gliomas of nanobubbles carrying siRNA combined with ultrasound-targeted destruction. Int J Nanomedicine. 2018; 13: 6791–6807.
- Ebben HP, Nederhoed JH, Lely RJ, et al. MUST collaborators. Microbubbles and UltraSound-accelerated Thrombolysis (MUST) for peripheral arterial occlusions: protocol for a phase II single-arm trial. BMJ Open. 2017; 7(8): e014365.
- Zhu Q, Dong G, Wang Z, et al. Intra-clot Microbubble-Enhanced Ultrasound Accelerates Catheter-Directed Thrombolysis for Deep Vein Thrombosis: A Clinical Study. Ultrasound Med Biol. 2019; 45(9): 2427–2433.
- D'Arrigo JS. Nanotherapy for Alzheimer's disease and vascular dementia: Targeting senile endothelium. Adv Colloid Interface Sci. 2018; 251: 44–54.
- Fan CH, Ting CY, Lin CY, et al. Noninvasive, Targeted, and Non-Viral Ultrasound-Mediated GDNF-Plasmid Delivery for Treatment of Parkinson's Disease. Sci Rep. 2016; 6: 19579.