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      Sonoporation: Underlying Mechanisms and Applications in Cellular Regulation

      1 , , 1 , , 2

      BIO Integration

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      Microbubble, multidisciplinary, reprogramming, sonoporation, ultrasound

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          Abstract

          Ultrasound combined with microbubble-mediated sonoporation has been applied to enhance drug or gene intracellular delivery. Sonoporation leads to the formation of openings in the cell membrane, triggered by ultrasound-mediated oscillations and destruction of microbubbles. Multiple mechanisms are involved in the occurrence of sonoporation, including ultrasonic parameters, microbubbles size, and the distance of microbubbles to cells. Recent advances are beginning to extend applications through the assistance of contrast agents, which allow ultrasound to connect directly to cellular functions such as gene expression, cellular apoptosis, differentiation, and even epigenetic reprogramming. In this review, we summarize the current state of the art concerning microbubble–cell interactions and sonoporation effects leading to cellular functions.

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          Most cited references 90

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          Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors.

          Differentiated cells can be reprogrammed to an embryonic-like state by transfer of nuclear contents into oocytes or by fusion with embryonic stem (ES) cells. Little is known about factors that induce this reprogramming. Here, we demonstrate induction of pluripotent stem cells from mouse embryonic or adult fibroblasts by introducing four factors, Oct3/4, Sox2, c-Myc, and Klf4, under ES cell culture conditions. Unexpectedly, Nanog was dispensable. These cells, which we designated iPS (induced pluripotent stem) cells, exhibit the morphology and growth properties of ES cells and express ES cell marker genes. Subcutaneous transplantation of iPS cells into nude mice resulted in tumors containing a variety of tissues from all three germ layers. Following injection into blastocysts, iPS cells contributed to mouse embryonic development. These data demonstrate that pluripotent stem cells can be directly generated from fibroblast cultures by the addition of only a few defined factors.
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            Clinical trial of blood-brain barrier disruption by pulsed ultrasound.

            The blood-brain barrier (BBB) limits the delivery of systemically administered drugs to the brain. Methods to circumvent the BBB have been developed, but none are used in standard clinical practice. The lack of adoption of existing methods is due to procedural invasiveness, serious adverse effects, and the complications associated with performing such techniques coincident with repeated drug administration, which is customary in chemotherapeutic protocols. Pulsed ultrasound, a method for disrupting the BBB, was shown to effectively increase drug concentrations and to slow tumor growth in preclinical studies. We now report the interim results of an ultrasound dose-escalating phase 1/2a clinical trial using an implantable ultrasound device system, SonoCloud, before treatment with carboplatin in patients with recurrent glioblastoma (GBM). The BBB of each patient was disrupted monthly using pulsed ultrasound in combination with systemically injected microbubbles. Contrast-enhanced magnetic resonance imaging (MRI) indicated that the BBB was disrupted at acoustic pressure levels up to 1.1 megapascals without detectable adverse effects on radiologic (MRI) or clinical examination. Our preliminary findings indicate that repeated opening of the BBB using our pulsed ultrasound system, in combination with systemic microbubble injection, is safe and well tolerated in patients with recurrent GBM and has the potential to optimize chemotherapy delivery in the brain.
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              Understanding ultrasound induced sonoporation: definitions and underlying mechanisms.

              In the past two decades, research has underlined the potential of ultrasound and microbubbles to enhance drug delivery. However, there is less consensus on the biophysical and biological mechanisms leading to this enhanced delivery. Sonoporation, i.e. the formation of temporary pores in the cell membrane, as well as enhanced endocytosis is reported. Because of the variety of ultrasound settings used and corresponding microbubble behavior, a clear overview is missing. Therefore, in this review, the mechanisms contributing to sonoporation are categorized according to three ultrasound settings: i) low intensity ultrasound leading to stable cavitation of microbubbles, ii) high intensity ultrasound leading to inertial cavitation with microbubble collapse, and iii) ultrasound application in the absence of microbubbles. Using low intensity ultrasound, the endocytotic uptake of several drugs could be stimulated, while short but intense ultrasound pulses can be applied to induce pore formation and the direct cytoplasmic uptake of drugs. Ultrasound intensities may be adapted to create pore sizes correlating with drug size. Small molecules are able to diffuse passively through small pores created by low intensity ultrasound treatment. However, delivery of larger drugs such as nanoparticles and gene complexes, will require higher ultrasound intensities in order to allow direct cytoplasmic entry. Copyright © 2013 Elsevier B.V. All rights reserved.
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                Author and article information

                Journal
                BIOI
                BIO Integration
                BIOI
                Compuscript (Ireland )
                2712-0082
                2712-0074
                01 April 2021
                06 February 2021
                : 2
                : 1
                : 29-36
                Affiliations
                1First Affiliated Hospital of University of South China, Hengyang, China
                2Department of Pediatrics, St Christopher’s Hospital for Children, Tower Health and Drexel University, Philadelphia, PA (S.G.)
                Author notes
                *Correspondence: Zhiyi Chen, E-mail: zhiyi_chen@ 123456usc.edu.cn ; Shuping Ge, E-mail: Shuping.Ge@ 123456towerhealth.org
                Article
                bioi20200028
                10.15212/bioi-2020-0028
                Copyright © 2020 The Authors

                This is an open access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/). See https://bio-integration.org/copyright-and-permissions/

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