{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2024,1,18]],"date-time":"2024-01-18T13:02:59Z","timestamp":1705582979825},"reference-count":69,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,4,19]],"date-time":"2023-04-19T00:00:00Z","timestamp":1681862400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Genet."],"abstract":"Background:<\/jats:bold> Focused ultrasound (FUS) has become an important non-invasive therapy for prostate tumor ablation via<\/jats:italic> thermal effects in the clinic. The cavitation effect induced by FUS is applied for histotripsy, support drug delivery, and the induction of blood vessel destruction for cancer therapy. Numerous studies report that cavitation-induced sonoporation could provoke multiple anti-proliferative effects on cancer cells. Therefore, cavitation alone or in combination with thermal treatment is of great interest but research in this field is inadequate.<\/jats:p>Methods:<\/jats:bold> Human prostate cancer cells (LNCap and PC-3) were exposed to 40\u00a0s cavitation using a FUS system, followed by water bath hyperthermia (HT). The clonogenic assay, WST-1 assay, and Transwell\u00ae<\/jats:sup> invasion assay, respectively, were used to assess cancer cell clonogenic survival, metabolic activity, and invasion potential. Fluorescence microscopy using propidium iodide (PI) as a probe of cell membrane integrity was used to identify sonoporation. The H2A.X assay and Nicoletti test were conducted in the mechanism investigation to detect DNA double-strand breaks (DSBs) and cell cycle arrest. Immunofluorescence microscopy and flow cytometry were performed to determine the distribution and expression of 5\u03b1-reductase (SRD5A).<\/jats:p>Results:<\/jats:bold> Short FUS shots with cavitation (<\/jats:bold>FUS-Cav) in combination with HT resulted in, respectively, a 2.2, 2.3, and 2.8-fold decrease (LNCap) and a 2.0, 1.5, and 1.6-fold decrease (PC-3) in the clonogenic survival, cell invasiveness and metabolic activity of prostate cancer cells when compared to HT alone. FUS-Cav immediately induced sonoporation in 61.7% of LNCap cells, and the combination treatment led to a 1.4 (LNCap) and 1.6-fold (PC-3) increase in the number of DSBs compared to HT alone. Meanwhile, the combination therapy resulted in 26.68% of LNCap and 31.70% of PC-3 with cell cycle arrest in the Sub-G1 phase and 35.37% of PC-3 with cell cycle arrest in the G2\/M phase. Additionally, the treatment of FUS-Cav combined with HT block the androgen receptor (AR) signal pathway by reducing the relative Type I 5\u03b1-reductase (SRD5A1) level to 38.28 \u00b1 3.76% in LNCap cells, and decreasing the relative Type III 5\u03b1-reductase 3 (SRD5A3) level to 22.87 \u00b1 4.88% in PC-3 cells, in contrast, the relative SRD5A level in untreated groups was set to 100%.<\/jats:p>Conclusion:<\/jats:bold> FUS-induced cavitation increases the effects of HT by interrupting cancer cell membranes, inducing the DSBs and cell cycle arrest, and blocking the AR signal pathway of the prostate cancer cells, with the potential to be a promising adjuvant therapy in prostate cancer treatment.<\/jats:p>","DOI":"10.3389\/fgene.2023.1122758","type":"journal-article","created":{"date-parts":[[2023,4,19]],"date-time":"2023-04-19T04:40:33Z","timestamp":1681879233000},"update-policy":"http:\/\/dx.doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":1,"title":["Ultrasound-induced cavitation renders prostate cancer cells susceptible to hyperthermia: Analysis of potential cellular and molecular mechanisms"],"prefix":"10.3389","volume":"14","author":[{"given":"Shaonan","family":"Hu","sequence":"first","affiliation":[]},{"given":"Xinrui","family":"Zhang","sequence":"additional","affiliation":[]},{"given":"Andreas","family":"Melzer","sequence":"additional","affiliation":[]},{"given":"Lisa","family":"Landgraf","sequence":"additional","affiliation":[]}],"member":"1965","published-online":{"date-parts":[[2023,4,19]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"356","DOI":"10.1093\/cvr\/cvm111","article-title":"Visfatin induces human endothelial VEGF and MMP-2\/9 production via MAPK and PI3K\/akt signalling pathways: Novel insights into visfatin-induced angiogenesis","volume":"78","author":"Adya","year":"2008","journal-title":"Cardiovasc. Res."},{"key":"B2","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1590\/S1677-5538.IBJU.2021.0091","article-title":"Available evidence on HIFU for focal treatment of prostate cancer: A systematic review","volume":"48","author":"Bakavicius","year":"2022","journal-title":"Int. braz J. Urol."},{"key":"B3","doi-asserted-by":"crossref","article-title":"Cavitation detection using a fibre\u2010optic hydrophone: A pilot study","author":"Bull","year":"2011","DOI":"10.1063\/1.3607887"},{"key":"B4","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1111\/j.1872-034X.2008.00449.x","article-title":"Involvement of PI3K\/PTEN\/AKT\/mTOR pathway in invasion and metastasis in hepatocellular carcinoma: Association with MMP\u20109","volume":"39","author":"Chen","year":"2009","journal-title":"Hepatology Res."},{"key":"B5","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1046\/j.1523-1747.1998.00080.x","article-title":"Evidence of heterogeneity and quantitative differences of the type 1 5alpha-reductase expression in cultured human skin cells-evidence of its presence in melanocytes","volume":"110","author":"Chen","year":"1998","journal-title":"J. investigative dermatology"},{"key":"B6","doi-asserted-by":"publisher","first-page":"1075","DOI":"10.1016\/j.ultrasmedbio.2013.01.008","article-title":"Sonoporation as a cellular stress: Induction of morphological repression and developmental delays","volume":"39","author":"Chen","year":"2013","journal-title":"Ultrasound Med. Biol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1007\/s11010-009-0217-z","article-title":"Antimetastatic potential of fisetin involves inactivation of the PI3K\/Akt and JNK signaling pathways with downregulation of MMP-2\/9 expressions in prostate cancer PC-3 cells","volume":"333","author":"Chien","year":"2010","journal-title":"Mol. Cell. Biochem."},{"key":"B8","doi-asserted-by":"publisher","first-page":"609","DOI":"10.3109\/02656736.2015.1040471","article-title":"Hyperthermia-related clinical trials on cancer treatment within the ClinicalTrials. gov registry","volume":"31","author":"Cihoric","year":"2015","journal-title":"Int. J. Hyperth."},{"key":"B9","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1016\/j.canlet.2017.09.037","article-title":"Localized microbubble cavitation-based antivascular therapy for improving HCC treatment response to radiotherapy","volume":"411","author":"Daecher","year":"2017","journal-title":"Cancer Lett."},{"key":"B10","doi-asserted-by":"publisher","first-page":"586","DOI":"10.1158\/1535-7163.MCT-14-0102","article-title":"Inhibition of the GTPase Rac1 mediates the anti-migratory effects of metformin in prostate cancer cells","volume":"14","author":"Dirat","year":"2015","journal-title":"Mol. Cancer Ther."},{"key":"B11","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1109\/TBME.2009.2028133","article-title":"The correlation between bubble-enhanced HIFU heating and cavitation power","volume":"57","author":"Farny","year":"2009","journal-title":"IEEE Trans. Biomed. Eng."},{"key":"B12","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1269\/jrr.45.479","article-title":"Biological effects of low intensity ultrasound: The mechanism involved, and its implications on therapy and on biosafety of ultrasound","volume":"45","author":"Feril","year":"2004","journal-title":"J. Radiat. Res."},{"key":"B13","doi-asserted-by":"publisher","first-page":"2315","DOI":"10.1038\/nprot.2006.339","article-title":"Clonogenic assay of cells in vitro","volume":"1","author":"Franken","year":"2006","journal-title":"Nat. Protoc."},{"key":"B14","doi-asserted-by":"publisher","first-page":"2061","DOI":"10.1016\/j.ultsonch.2014.02.028","article-title":"Effects of therapeutic ultrasound on the nucleus and genomic DNA","volume":"21","author":"Furusawa","year":"2014","journal-title":"Ultrason. sonochemistry"},{"key":"B15","doi-asserted-by":"publisher","first-page":"1033","DOI":"10.1002\/pros.21318","article-title":"5\u03b1\u2010reductase type 3 expression in human benign and malignant tissues: A comparative analysis during prostate cancer progression","volume":"71","author":"Godoy","year":"2011","journal-title":"Prostate"},{"key":"B16","doi-asserted-by":"publisher","first-page":"316","DOI":"10.1016\/j.jconrel.2013.05.038","article-title":"Ultrasound-mediated targeted drug delivery with a novel cyclodextrin-based drug carrier by mechanical and thermal mechanisms","volume":"170","author":"Gourevich","year":"2013","journal-title":"J. Control. release"},{"key":"B17","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2013\/672873","article-title":"Hyperthermia versus oncothermia: Cellular effects in complementary cancer therapy","volume":"2013","author":"Hegyi","year":"2013","journal-title":"Evidence-Based Complementary Altern. Med."},{"key":"B18","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/s1040-8428(01)00179-2","article-title":"The cellular and molecular basis of hyperthermia","volume":"43","author":"Hildebrandt","year":"2002","journal-title":"Crit. Rev. oncology\/hematology"},{"key":"B19","doi-asserted-by":"publisher","first-page":"2595","DOI":"10.3390\/cells9122595","article-title":"Focused ultrasound-induced cavitation sensitizes cancer cells to radiation therapy and hyperthermia","volume":"9","author":"Hu","year":"2020","journal-title":"Cells"},{"key":"B20","doi-asserted-by":"crossref","article-title":"Hyperthermia, radiation and chemotherapy: The role of heat in multidisciplinary cancer care","volume-title":"Seminars in oncology","author":"Hurwitz","year":"2014","DOI":"10.1053\/j.seminoncol.2014.09.014"},{"key":"B21","doi-asserted-by":"publisher","first-page":"1085","DOI":"10.1016\/j.ultrasmedbio.2017.01.023","article-title":"Mechanical and biological effects of ultrasound: A review of present knowledge","volume":"43","author":"Izadifar","year":"2017","journal-title":"Ultrasound Med. Biol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1007\/s40846-018-0391-0","article-title":"Ultrasound cavitation\/microbubble detection and medical applications","volume":"39","author":"Izadifar","year":"2019","journal-title":"J. Med. Biol. Eng."},{"key":"B23","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1080\/09553000010024687","article-title":"Hyperthermic radiosensitization: Mode of action and clinical relevance","volume":"77","author":"Kampinga","year":"2001","journal-title":"Int. J. Radiat. Biol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"691","DOI":"10.1016\/j.ultras.2010.01.009","article-title":"Microbubble mediated sonoporation of cells in suspension: Clonogenic viability and influence of molecular size on uptake","volume":"50","author":"Karshafian","year":"2010","journal-title":"Ultrasonics"},{"key":"B25","doi-asserted-by":"publisher","first-page":"847","DOI":"10.3109\/0284186X.2014.962665","article-title":"VMAT technique enables concomitant radiotherapy of prostate cancer and pelvic bone metastases","volume":"54","author":"Kiljunen","year":"2015","journal-title":"Acta Oncol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"284","DOI":"10.2307\/3576590","article-title":"Damage in DNA irradiated with 1.2 MHz ultrasound and its effect on template activity of DNA for RNA synthesis","volume":"104","author":"Kondo","year":"1985","journal-title":"Radiat. Res."},{"key":"B27","doi-asserted-by":"publisher","first-page":"1983","DOI":"10.1016\/j.ultrasmedbio.2013.03.025","article-title":"Ultrasound-mediated microbubble enhancement of radiation therapy studied using three-dimensional high-frequency power Doppler ultrasound","volume":"39","author":"Kwok","year":"2013","journal-title":"Ultrasound Med. Biol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"1931","DOI":"10.1016\/j.ultrasmedbio.2006.06.020","article-title":"Quantitative relations of acoustic inertial cavitation with sonoporation and cell viability","volume":"32","author":"Lai","year":"2006","journal-title":"Ultrasound Med. Biol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"3169","DOI":"10.3892\/mmr.2014.2630","article-title":"Sox2 is involved in paclitaxel resistance of the prostate cancer cell line PC-3 via the PI3K\/Akt pathway","volume":"10","author":"Li","year":"2014","journal-title":"Mol. Med. Rep."},{"key":"B30","doi-asserted-by":"publisher","first-page":"e28840","DOI":"10.1371\/journal.pone.0028840","article-title":"Androgen regulation of 5\u03b1-reductase isoenzymes in prostate cancer: Implications for prostate cancer prevention","volume":"6","author":"Li","year":"2011","journal-title":"PloS one"},{"key":"B31","doi-asserted-by":"publisher","first-page":"833","DOI":"10.1016\/j.ultsonch.2013.10.017","article-title":"Stabilizing in vitro ultrasound-mediated gene transfection by regulating cavitation","volume":"21","author":"Lo","year":"2014","journal-title":"Ultrason. sonochemistry"},{"key":"B32","doi-asserted-by":"publisher","first-page":"20","DOI":"10.4103\/1477-3163.83937","article-title":"Androgen receptor signaling in prostate cancer development and progression","volume":"10","author":"Lonergan","year":"2011","journal-title":"J. Carcinog."},{"key":"B33","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1016\/j.ultrasmedbio.2012.09.004","article-title":"Probability of cavitation for single ultrasound pulses applied to tissues and tissue-mimicking materials","volume":"39","author":"Maxwell","year":"2013","journal-title":"Ultrasound Med. Biol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"780","DOI":"10.2741\/1063","article-title":"Androgens and androgen receptor in prostate and ovarian malignancies","volume":"8","author":"Meehan","year":"2003","journal-title":"Front. Bioscience-Landmark"},{"key":"B35","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1016\/j.ultrasmedbio.2008.06.007","article-title":"Induction of apoptosis in sonoporation and ultrasonic gene transfer","volume":"35","author":"Miller","year":"2009","journal-title":"Ultrasound Med. Biol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"3611","DOI":"10.1121\/1.3117437","article-title":"A Fabry\u2013P\u00e9rot fiber-optic ultrasonic hydrophone for the simultaneous measurement of temperature and acoustic pressure","volume":"125","author":"Morris","year":"2009","journal-title":"J. Acoust. Soc. Am."},{"key":"B37","doi-asserted-by":"publisher","first-page":"374","DOI":"10.1269\/jrr.10102","article-title":"Carbon ion irradiation suppresses metastatic potential of human non-small cell lung cancer A549 cells through the phosphatidylinositol-3-kinase\/Akt signaling pathway","volume":"52","author":"Ogata","year":"2011","journal-title":"J. Radiat. Res."},{"key":"B38","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1158\/0008-5472.113.65.1","article-title":"Particle irradiation suppresses metastatic potential of cancer cells","volume":"65","author":"Ogata","year":"2005","journal-title":"Cancer Res."},{"key":"B39","doi-asserted-by":"publisher","first-page":"132","DOI":"10.3389\/fonc.2017.00132","article-title":"Integrating hyperthermia into modern radiation oncology: What evidence is necessary?","volume":"7","author":"Peeken","year":"2017","journal-title":"Front. Oncol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/S0076-6879(08)01606-6","article-title":"DNA damage response and apoptosis","volume":"446","author":"Plesca","year":"2008","journal-title":"Methods Enzym."},{"key":"B41","volume-title":"Interventional magnetic resonance imaging","author":"Rieke","year":"2011"},{"key":"B42","doi-asserted-by":"publisher","first-page":"204","DOI":"10.1016\/j.canlet.2013.04.016","article-title":"Targeted manipulation of apoptotic pathways by using High Intensity Focused Ultrasound in cancer treatment","volume":"338","author":"Saliev","year":"2013","journal-title":"Cancer Lett."},{"key":"B43","doi-asserted-by":"publisher","first-page":"1957","DOI":"10.1016\/j.juro.2012.07.006","article-title":"Histotripsy focal ablation of implanted prostate tumor in an ACE-1 canine cancer model","volume":"188","author":"Schade","year":"2012","journal-title":"J. urology"},{"key":"B44","doi-asserted-by":"publisher","first-page":"184","DOI":"10.1016\/j.urology.2017.12.033","article-title":"Histotripsy treatment of benign prostatic enlargement using the vortx rx system: Initial human safety and efficacy outcomes","volume":"114","author":"Schuster","year":"2018","journal-title":"Urology"},{"key":"B45","doi-asserted-by":"crossref","article-title":"Magnetic resonance-guided high-intensity focused ultrasound (MR-HIFU): Technical background and overview of current clinical applications (part 1)","volume-title":"R\u00f6Fo-Fortschritte auf dem Gebiet der R\u00f6ntgenstrahlen und der bildgebenden Verfahren","author":"Siedek","year":"2019","DOI":"10.1055\/a-0817-5645"},{"key":"B46","first-page":"626","article-title":"Improvement of tumor oxygenation status by mild temperature hyperthermia alone or in combination with carbogen","volume":"24","author":"Song","year":"1997","journal-title":"Seminars Oncol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"864","DOI":"10.4103\/1008-682X.129132","article-title":"Physiological normal levels of androgen inhibit proliferation of prostate cancer cells in vitro","volume":"16","author":"Song","year":"2014","journal-title":"Asian J. Androl."},{"key":"B48","doi-asserted-by":"publisher","first-page":"903","DOI":"10.1172\/JCI116665","article-title":"Tissue distribution and ontogeny of steroid 5 alpha-reductase isozyme expression","volume":"92","author":"Thigpen","year":"1993","journal-title":"J. Clin. investigation"},{"key":"B49","doi-asserted-by":"publisher","first-page":"2022","DOI":"10.34133\/2022\/9807347","article-title":"Ultrasound-mediated drug delivery: Sonoporation mechanisms, biophysics, and critical factors","volume":"2022","author":"Tu","year":"2022","journal-title":"BME Front."},{"key":"B50","doi-asserted-by":"publisher","first-page":"3059","DOI":"10.1121\/1.3646905","article-title":"The mechanism of interaction between focused ultrasound and microbubbles in blood-brain barrier opening in mice","volume":"130","author":"Tung","year":"2011","journal-title":"J. Acoust. Soc. Am."},{"key":"B51","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1111\/j.1349-7006.2007.00656.x","article-title":"Novel 5\u03b1\u2010steroid reductase (SRD5A3, type\u20103) is overexpressed in hormone\u2010refractory prostate cancer","volume":"99","author":"Uemura","year":"2008","journal-title":"Cancer Sci."},{"key":"B52","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/j.jconrel.2006.02.007","article-title":"Vibrating microbubbles poking individual cells: Drug transfer into cells via sonoporation","volume":"112","author":"Van Wamel","year":"2006","journal-title":"J. Control. release"},{"key":"B53","doi-asserted-by":"publisher","first-page":"495","DOI":"10.3892\/ol.2013.1389","article-title":"Sonoporation by low-frequency and low-power ultrasound enhances chemotherapeutic efficacy in prostate cancer cells in vitro","volume":"6","author":"Wang","year":"2013","journal-title":"Oncol. Lett."},{"key":"B54","doi-asserted-by":"publisher","first-page":"2150006","DOI":"10.1142\/s1793984421500069","article-title":"Ultrasound-induced microbubble cavitation combined with paclitaxel-loaded nanoparticles for the elimination of PC-3 cells in vitro","volume":"12","author":"Wang","year":"2022","journal-title":"Nano LIFE"},{"key":"B55","doi-asserted-by":"publisher","first-page":"1372","DOI":"10.3892\/ol.2014.2310","article-title":"Combined treatment of PC-3 cells with ultrasound and microbubbles suppresses invasion and migration","volume":"8","author":"Wei","year":"2014","journal-title":"Oncol. Lett."},{"key":"B56","doi-asserted-by":"publisher","first-page":"937","DOI":"10.1098\/rsta.2003.1356","article-title":"Foundations of chaotic mixing","volume":"362","author":"Wiggins","year":"2004","journal-title":"Philosophical Trans. R. Soc. Lond. Ser. A Math. Phys. Eng. Sci."},{"key":"B57","doi-asserted-by":"publisher","first-page":"1470","DOI":"10.1002\/pros.22694","article-title":"Prostate cancer cells differ in testosterone accumulation, dihydrotestosterone conversion, and androgen receptor signaling response to steroid 5\u03b1\u2010reductase inhibitors","volume":"73","author":"Wu","year":"2013","journal-title":"Prostate"},{"key":"B58","doi-asserted-by":"publisher","first-page":"101177","DOI":"10.1016\/j.tranon.2021.101177","article-title":"Ultrasound-mediated microbubbles cavitation enhanced chemotherapy of advanced prostate cancer by increasing the permeability of blood-prostate barrier","volume":"14","author":"Xia","year":"2021","journal-title":"Transl. Oncol."},{"key":"B59","doi-asserted-by":"publisher","first-page":"1573","DOI":"10.3892\/or.2011.1240","article-title":"Effect of hyperthermia on invasion ability and TGF-\u03b21 expression of breast carcinoma MCF-7 cells","volume":"25","author":"Xie","year":"2011","journal-title":"Oncol. Rep."},{"key":"B60","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1080\/02656736.2021.1905189","article-title":"Histotripsy: The first noninvasive, non-ionizing, non-thermal ablation technique based on ultrasound","volume":"38","author":"Xu","year":"2021","journal-title":"Int. J. Hyperth."},{"key":"B61","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1021\/acs.molpharmaceut.5b00421","article-title":"Low intensity ultrasound mediated liposomal doxorubicin delivery using polymer microbubbles","volume":"13","author":"Yu","year":"2016","journal-title":"Mol. Pharm."},{"key":"B62","doi-asserted-by":"publisher","first-page":"674","DOI":"10.1007\/s12032-013-0674-9","article-title":"Androgen receptor in human prostate cancer-associated fibroblasts promotes prostate cancer epithelial cell growth and invasion","volume":"30","author":"Yu","year":"2013","journal-title":"Med. Oncol."},{"key":"B63","doi-asserted-by":"publisher","first-page":"1181","DOI":"10.2967\/jnumed.120.256230","article-title":"Image-guided high-intensity focused ultrasound, A novel application for interventional nuclear medicine?","volume":"62","author":"Zhang","year":"2021","journal-title":"J. Nucl. Med."},{"key":"B64","doi-asserted-by":"publisher","first-page":"2149","DOI":"10.1016\/j.ultrasmedbio.2011.09.012","article-title":"Sonoporation induces apoptosis and cell cycle arrest in human promyelocytic leukemia cells","volume":"37","author":"Zhong","year":"2011","journal-title":"Ultrasound Med. Biol."},{"key":"B65","doi-asserted-by":"publisher","first-page":"2629","DOI":"10.3892\/or.2017.5961","article-title":"Suppression of STIM1 inhibits the migration and invasion of human prostate cancer cells and is associated with PI3K\/Akt signaling inactivation","volume":"38","author":"Zhou","year":"2017","journal-title":"Oncol. Rep."},{"key":"B66","doi-asserted-by":"publisher","first-page":"1756","DOI":"10.1016\/j.ultrasmedbio.2009.05.012","article-title":"The size of sonoporation pores on the cell membrane","volume":"35","author":"Zhou","year":"2009","journal-title":"Ultrasound Med. Biol."},{"key":"B67","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1016\/j.jconrel.2011.09.068","article-title":"Controlled permeation of cell membrane by single bubble acoustic cavitation","volume":"157","author":"Zhou","year":"2012","journal-title":"J. Control. release"},{"key":"B68","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1093\/abbs\/gmy165","article-title":"miR-188-5p regulates proliferation and invasion via PI3K\/Akt\/MMP-2\/9 signaling in keloids","volume":"51","author":"Zhu","year":"2019","journal-title":"Acta Biochimica Biophysica Sinica"},{"key":"B69","doi-asserted-by":"publisher","first-page":"1537","DOI":"10.1089\/hum.2011.076","article-title":"Sonoporation delivery of interleukin-27 gene therapy efficiently reduces prostate tumor cell growth in vivo","volume":"22","author":"Zolochevska","year":"2011","journal-title":"Hum. gene Ther."}],"container-title":["Frontiers in Genetics"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fgene.2023.1122758\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,4,19]],"date-time":"2023-04-19T04:40:44Z","timestamp":1681879244000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fgene.2023.1122758\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,19]]},"references-count":69,"alternative-id":["10.3389\/fgene.2023.1122758"],"URL":"http:\/\/dx.doi.org\/10.3389\/fgene.2023.1122758","relation":{},"ISSN":["1664-8021"],"issn-type":[{"value":"1664-8021","type":"electronic"}],"subject":["Genetics (clinical)","Genetics","Molecular Medicine"],"published":{"date-parts":[[2023,4,19]]}}}